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Short title 1
Regulation of furaneol biosynthesis in strawberry 2
3
4
Corresponding author details 5
Kunsong Chen 6
College of Agriculture amp Biotechnology Zhejiang University Zijingang Campus 7
Hangzhou 310058 PR China 8
Zhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology 9
Zhejiang University Zijingang Campus Hangzhou 310058 PR China 10
The State Agriculture Ministry Laboratory of Horticultural Plant Growth 11
Development and Quality Improvement Zhejiang University Zijingang Campus 12
Hangzhou 310058 PR China 13
Email akunzjueducn 14
15
Harry J Klee 16
College of Agriculture amp Biotechnology Zhejiang University Zijingang Campus 17
Hangzhou 310058 PR China 18
Horticultural Sciences Plant Innovation Center Genetics Institute University of 19
Florida Gainesville FL 32611 20
Email hjkleeufledu 21
22
Guihua Jiang 23
Institute of Horticulture Zhejiang Academy of Agricultural Sciences Hangzhou 24
310021 Zhejiang China 25
Email jgh2004267sinacom 26
27
Plant Physiology Preview Published on July 9 2018 as DOI101104pp1800598
Copyright 2018 by the American Society of Plant Biologists
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2
Article title 28
29
An ETHYLENE RESPONSE FACTOR-MYB Transcription Complex Regulates 30
Furaneol Biosynthesis by Activating QUINONE OXIDOREDUCTASE Expression 31
in Strawberry 32
33
34
Yuanyuan Zhang1 Xueren Yin123 Yuwei Xiao1 Zuying Zhang1 Shaojia Li1 35
Xiaofen Liu1 Bo Zhang123 Xiaofang Yang4 Donald Grierson15 Guihua Jiang4 36
Harry J Klee16 Kunsong Chen123 37
1 College of Agriculture amp Biotechnology Zhejiang University Zijingang Campus 38
Hangzhou 310058 PR China 39
2 Zhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology 40
Zhejiang University Zijingang Campus Hangzhou 310058 PR China 41
3 The State Agriculture Ministry Laboratory of Horticultural Plant Growth 42
Development and Quality Improvement Zhejiang University Zijingang Campus 43
Hangzhou 310058 PR China 44
4 Institute of Horticulture Zhejiang Academy of Agricultural Sciences Hangzhou 45
310021 Zhejiang China 46
5 Division of Plant and Crop Sciences School of Biosciences University of 47
Nottingham Sutton Bonington Campus Loughborough LE12 5RD UK 48
6 Horticultural Sciences Plant Innovation Center Genetics Institute University of 49
Florida Gainesville FL 32611 50
These authors contributed equally to this manuscript 51
52
One-sentence summary 53
Fragaria times ananassa quinone oxidoreductase which catalyses the final step in 54
furaneol biosynthesis in strawberry is transcriptionally upregulated by a complex 55
consisting of an ethylene response factor and MYB during ripening 56
57
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3
Footnotes 58
List of author contributions 59
KC HK and GJ conceived the original screening and research plans XrY and 60
YZ designed the experiments YZ YX and ZZ performed the experiments XrY 61
SL XL and XfY provided technical assistance to YZ XrY BZ and KC 62
supervised the experiments YZ and XrY analysed the data YZ and XrY wrote 63
the article with contributions from all the authors DG discussed results and 64
interpretation and supervised the writing and editing of the manuscript 65
66
Funding information 67
This research was supported by the National Key Research and Development 68
Program (2016YFD0400101) the Project of the Science and Technology Department 69
of Zhejiang Province (2016C04001) and the 111 Project (B17039) 70
71
Corresponding author email 72
The authors responsible for distribution of materials integral to the findings presented 73
in this article in accordance with the policy described in the Instructions for Authors 74
(wwwplantphysiolorg) are Kunsong Chen (akunzjueducn) Harry J Klee 75
(hjkleeufledu) and Guihua Jiang (jgh2004267sinacom) 76
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
4
Abstract 77
4-Hydroxy-25-dimethyl-3(2H)-furanone (HDMF) is a major contributor to the aroma 78
of strawberry (Fragaria times ananassa) fruit and the last step in its biosynthesis is 79
catalysed by Fragaria times ananassa quinone oxidoreductase (FaQR) Here an ethylene 80
response factor (FaERF9) was characterized as a positive regulator of the FaQR 81
promoter Linear regression analysis indicated that FaERF9 transcript levels were 82
significantly correlated with both FaQR transcripts and furanone content in different 83
strawberry cultivars Transient overexpression of FaERF9 in strawberry fruit 84
significantly increased FaQR expression and furaneol production Yeast one-hybrid 85
assays however indicated that FaERF9 by itself did not bind to the FaQR promoter 86
An MYB transcription factor (FaMYB98) identified in yeast one-hybrid screening of 87
the strawberry cDNA library was capable of both binding to the promoter and 88
activating the transcription of FaQR by ~56-fold Yeast two-hybrid assay and 89
bimolecular fluorescence complementation confirmed a direct protein-protein 90
interaction between FaERF9 and FaMYB98 and in combination they activated the 91
FaQR promoter 14-fold in transactivation assays These results indicate that an 92
ERF-MYB complex containing FaERF9 and FaMYB98 activates the FaQR 93
promoter and upregulates HDMF biosynthesis in strawberry 94
95
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5
Introduction 96
Strawberry (Fragaria times ananassa) is an economically important globally popular 97
and attractive fruit with nutritional benefits for human health An important feature of 98
its appeal is a unique fragrance with more than 360 different volatile compounds 99
detected in ripe fruit (Meacutenager 2004 Jetti et al 2007) These volatiles include 100
alcohols organic acids aldehydes terpenes lactones esters aromatic hydrocarbons 101
furans and others (Zabetakis and Holden 1997) Sensory evaluation indicates that 102
terpenes confer on strawberry a ldquofresh orangerdquo smell aldehydes generate a ldquoherbal 103
flavourrdquo γ -decalactone is ldquopeach-likerdquo esters are ldquofruityrdquo and 104
4-hydroxy-25-dimethyl-3(2)H-furanone (HDMF) and 105
25-dimethyl-4-methoxy-3(2)H-furanone (DMMF) generate a ldquocaramel-likerdquo aroma 106
(Pyysalo et al 1979 Larsen and Poll 1992) HDMF and DMMF belong to an 107
uncommon group of chemicals with a 25-dimethyl-3(2H)-furanone structure and 108
such compounds possess special odour properties (Schwab and Roscher 1997) They 109
are found at trace levels in various fruits including raspberry some grape cultivars 110
and tomato They are particularly abundant in strawberry and pineapple (Schwab 111
2013 Wuumlst 2017) HDMF is one of the most important volatiles distinguishing 112
strawberry from other fruits (Larsen and Poll 1992 Schwab and Roscher 1997) and 113
is significantly correlated with perceived strawberry fruit intensity (Schwieterman et 114
al 2014) Thus strawberry is an important model for investigating the regulation of 115
furaneol biosynthesis and knowledge of the factors controlling its synthesis is highly 116
desirable for targeting flavor improvement 117
118
HDMF and its methyl ether DMMF have been extensively investigated in research 119
on flavour analyses chemical synthesis and natural product formation in both 120
microbes and plants (Zabetakis et al 1999 Schwab 2013) The first plant studies on 121
the biosynthesis of HDMF used strawberry fruit to investigate potential precursors of 122
furaneol biosynthesis (Pisarnitskii et al 1992) and D-fructose-16-diphosphate was 123
identified as the natural precursor of HDMF and DMMF (Roscher et al 1998 124
Schwab 1998) The immediate precursor of HDMF in strawberry was shown to be 125
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6
4-hydroxy-5-methyl-2-methylene-3(2H)-furanone (HMMF) and Fragaria times 126
ananassa quinone oxidoreductase (FaQR later renamed as FaEO) was identified as 127
the enzyme responsible for reduction of the α β-unsaturated bond of HMMF to form 128
the aroma-active compound HDMF (Raab et al 2006 Klein et al 2007) An 129
O-methyltransferase FaOMT subsequently generates DMMF by methylation of 130
HDMF (Wein et al 2002) HDMF can also be metabolized to 131
25-dimethyl-4-hydroxy-2H-furan-3-one glucoside (HDMF-glucoside) by a 132
UDP-dependent glycosyltransferase (UGT71K3) and further malonylated into 133
25-dimethyl-4-hydroxy-2H-furan-3-one 6rsquo-O-malonyl-β-D-glucopyranoside (HDMF 134
malonyl-glucoside) in strawberry fruit (Roscher et al 1996 Song et al 2016) The 135
biosynthetic pathway of HDMF in other plants is similar to that in strawberry Genes 136
with homology to FaQR have been identified in tomato (SlEO) and mango (MIEO) 137
(Klein et al 2007 Kulkarni et al 2013) 138
139
As an NADH-dependent enone oxidoreductase protein FaQR exhibits o-quinone 140
oxidoreductase activity (Raab et al 2006) FaQR mRNA accumulates in fruit 141
parenchyma tissues but is absent in vascular tissues and FaQR is mainly expressed in 142
the late stages of fruit growth and ripening paralleling furaneol production in the fruit 143
(Raab et al 2006) FaQR is responsive to environmental stimuli associated with 144
furaneol production and in the dark lsquoSweet Charliersquo strawberry fruits have higher 145
levels of FaQR expression and HDMF production at 25degC than at 15degC (Fu et al 146
2017) in contrast the concentration of furanones and the abundance of FaQR protein 147
under low-temperature storage is significantly lower than those under 148
room-temperature storage (Li et al 2015) Thus the regulation of FaQR is important 149
for manipulating furaneol content Although it is assumed that transcription factors 150
control expressions of genes involved in volatile production in plants no such factors 151
regulating FaQR or other furanone biosynthetic genes have been identified 152
153
Different members of the largely plant-specific AP2ERF gene family (Weirauch and 154
Hughes 2011) have diverse functions in plant growth development and stress 155
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7
responses (Agarwal et al 2010 Zhu et al 2010 Licausi et al 2013) In recent years 156
several AP2ERF genes have been reported to regulate aspects of fruit quality (Xie et 157
al 2016) including fruit aroma For example CitAP210 is associated with the 158
synthesis of (+)-valencene in Newhall orange acting via regulation of CsTPS1 (Shen 159
et al 2016) CitERF71 was shown to physically bind to the CsTPS16 promoter and 160
contribute to the synthesis of E-geraniol in citrus fruit (Li et al 2017) These 161
observations raised the possibility that FaQR might also be a target for a member of 162
the AP2ERF family and that ERFs might also control furaneol biosynthesis 163
164
In this study screening of the Fragaria times ananassa AP2ERF gene family led to 165
identification of FaERF9 as an activator of FaQR however it did not bind directly 166
to the promoter A parallel search for proteins that directly bind the FaQR promoter 167
using yeast one-hybrid screening identified a second factor FaMYB98 which was 168
capable of physically interacting with the FaQR promoter FaMYB98 physically 169
interacts with FaERF9 and transient expression assays demonstrated a synergistic 170
effect on FaQR expression and furanone synthesis 171
172
Results 173
Changes in the content of both furanones and the activity of their biosynthetic 174
genes in strawberry fruit 175
lsquoYuexinrsquo fruits at four developmental and ripening stages (G green T turning IR 176
intermediate red R full red) were harvested (Figure 1) and determination of HDMF 177
levels indicated a major increase from about 065 μg per gram fruit at the IR stage to 178
346 μg at the R stage in the apical section implying that furaneol accumulation was 179
closely related to colour change and ripening (Figure 1) Furaneol levels were higher 180
in the apical section than in the basal section HDMF could not be detected at the IR 181
stage in the basal section but the amount increased at the R stage to 142 μg per gram 182
fruit Differences were also found for DMMF with the relative content in the apical 183
section 018 μg per gram at the R stage compared to 008 μg per gram in the basal 184
section at the same stage 185
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8
186
Measurement of mRNA levels by RT-qPCR indicated that the transcript levels of both 187
FaQR (GenBank AY1588361) and FaOMT (GenBank AF2204912) increased 188
throughout ripening (Figure 1) Comparison of the expression of these genes showed 189
that the transcript levels of FaQR and FaOMT significantly increased as early as in T 190
stage in basal fruit sections and for each gene over half of the peak transcript 191
abundance occurred as early as in IR stage in the apical section while for the basal 192
section it was in the R stage indicating a gradient of gene expression and volatile 193
production from apex to base of the fruit during ripening 194
195
Genome-wide identification of AP2ERF gene family in strawberry 196
Coding sequences of 120 non-redundant FaAP2ERF genes were isolated and 197
identified from lsquoYuexinrsquo strawberry and a systematic nomenclature for the AP2ERF 198
family genes was used to distinguish the members based on the structural features 199
defined previously (Supplemental Table S1) (Shigyo and Ito 2004 Nakano et al 200
2006 Licausi et al 2013) CD-search analysis showed that this superfamily is 201
consisted of 95 ERFs 18 AP2 and 6 RAV family members and 1 soloist member 202
(Supplemental Table S2) Phylogenetic analysis of the Fragaria times ananassa and 203
Arabidopsis AP2ERF members is shown in Supplemental Figure S1 with the 120 204
AP2ERF genes divided into three major groups (ERF AP2 RAV) and a soloist and 205
the ERF family being further divided into 10 groups (groups I to X in Supplemental 206
Table S1) 207
208
We performed a dual-luciferase assay to determine the ability of 116 FaAP2ERF 209
members to activate transcription from the promoter of FaQR The results indicated 210
about 12 members (mainly belonging to the ERF and RAV families) showed a 211
significant activation effect on the FaQR promoter while the remaining members 212
showed very limited effects (Figure 2) The relative activity of only the following 12 213
FaAP2ERF transcripts reached the threshold value set at 2 FaERF8FaERF9 214
(group II) FaERF27FaERF29FaERF31FaERF32 (group IV) 215
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9
FaERF37FaERF38 (group V) FaERF62FaERF64 (group VIII) FaERF68 216
(group IX) and FaRAV4 (Figure 2) Of these FaERF9 exhibited the highest 217
activation effect on the FaQR promoter (466-fold) (Figure 2) The strawberry 218
FaERF9 cDNA is 699 bp long and ExPASy Compute pIMw tool analysis indicated 219
that this gene encodes a 232-amino acid protein with a calculated molecular mass of 220
254 KD and a pI of 56 221
222
FaERF9 expression pattern and subcellular localization 223
To further explore the connections between AP2ERFs and furaneol biosynthesis we 224
obtained the transcript profiles of the AP2ERF genes in strawberry fruit samples at 225
different fruit developmental and ripening stages by reverse transcription quantitative 226
PCR (RT-qPCR) excluding genes with very low abundance in the fruit samples The 227
results presented as a heatmap (Supplemental Figure S2) demonstrate that these 228
genes displayed various expression patterns in both the apical and basal sections and 229
by analysing the expression patterns of the members indicated as activators in the 230
dual-luciferase assay we found that only a few genes including FaERF8 FaERF9 231
FaERF27 FaERF32 and FaERF37 were up-regulated during ripening stages and 232
their expression correlated with furaneol accumulation in the fruit (Figure 1) 233
Furthermore the expression patterns of the up-regulated genes in the apical and basal 234
sections showed that one ERF gene FaERF9 not only showed an up-regulation 235
pattern in both sections but its expression in the apical section occurred ahead of that 236
in the basal section (Figure 3) consistent with the actual changes in furaneol content 237
(Figure 1) and the expression pattern of FaQR (Figure 1) The subcellular localization 238
of FaERF9 was predicted to be in the nucleus using the WoLF PSORT program In 239
experimental tests 35S-FaERF9-GFP (green fluorescence protein) showed strong 240
fluorescence in the nucleus and the green signal merged with the red fluorescence 241
signal of mCherry-nucleus-marker in tobacco plants (Figure 3) 242
243
Transient overexpression of FaERF9 in strawberry 244
The expression of FaERF9 in agro-infiltrated fruits was analysed by performing 245
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10
RT-qPCR on the seventh day after infiltration by which time they had reached the IR 246
or R stage and the result showed that the transcript levels were significantly higher 247
(52-fold) than in control fruits (Figure 4) The expression of FaQR was examined in 248
the same fruits and the transcript abundance also increased 22-fold The relative 249
content of HDMF in the FaERF9-overexpressing fruits was 008 μg per gram fruit 250
and undetectable in the control fruits (Figure 4) The relative content of DMMF in the 251
overexpressing fruits was also significantly increased to 038 μg per gram fruit 252
compared to 004 μg per gram fruit in the control (Figure 4) These observations 253
provide direct evidence for a regulatory role for FaERF9 in promoting FaQR 254
biosynthesis and activity in ripening strawberry fruit Taken together these results 255
indicate that by activating the transcription of FaQR FaERF9 functions as a positive 256
regulator in furaneol biosynthesis 257
258
Correlation of FaERF9 expression and FaQR transcript profiles 259
GC-MS quantification showed that furanones are distributed in variable levels among 260
different strawberry cultivars (Supplemental Figure S3) The transcript profiles of 261
FaQR and FaERF9 in fruits of different cultivars were measured and linear 262
regression analysis was performed In the cultivars the changes in FaQR transcripts 263
correlated positively with those in FaERF9 transcripts (r = 079 plt001) (Figure 5) 264
In addition FaERF9 transcript levels also correlated with furanone content across 265
cultivars (Figure 5) 266
267
FaERF9 is an indirect regulator of the FaQR promoter and acts via 268
protein-protein interaction with FaMYB98 269
Although the results of the dual-luciferase assay expression analysis transient 270
overexpression and correlation analysis were all consistent with the suggestion that 271
FaERF9 regulates transcript abundance by acting on the FaQR promoter a yeast 272
one-hybrid assay indicated that FaERF9 cannot bind directly to the FaQR promoter 273
(Figure 6) This led us to speculate that activation may occur via a transcription 274
complex involving an additional as-yet unknown regulator which can bind directly to 275
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11
the FaQR promoter 276
277
In parallel with the investigation of the FaAP2ERF genes a cDNA library screening 278
was performed with a yeast one-hybrid assay using the promoter of FaQR as the bait 279
This screen identified several transcription factors that could physically bind to the 280
FaQR promoter but only one MYB could activate transcription from the FaQR 281
promoter (approximately 56-fold) relative to the control (Figure 6) in the 282
dual-luciferase assay This MYB showed 44 amino acid identity with MYB98 283
(GenBank ABA420611) a transcriptional regulator in the synergid cells in 284
Arabidopsis (Kasahara et al 2005) and it was designated as FaMYB98 The 285
specificity of FaMYB98 binding to the FaQR promoter was confirmed by EMSA 286
assay (Figure 7) and increasing the concentration of the cold probe reduced binding 287
In addition mutating the putative binding sites (Goacutemez-Maldonado et al 2004 288
Punwani et al 2007) as shown in Figure 7 eliminated FaMYB98 protein binding 289
When the combined effect of FaERF9 and FaMYB98 was analysed (Figure 8) a 290
synergistic 14-fold activation of the FaQR promoter was observed compared with the 291
activation by either FaERF9 or FaMYB98 which alone promoted transactivation 292
39-fold and 45-fold respectively In addition overexpression of both genes 293
(FaERF9-FaMYB98-SK) in strawberry fruits resulted in higher expression of 294
FaERF9 transcripts and higher furanone content than overexpression of FaERF9 295
(Supplemental Figure S4 Supplemental Table S3) Subcellular localization analysis 296
revealed that FaMYB98 was also localized in the nucleus (Supplemental Figure S5) 297
298
To investigate the potential interactions between FaERF9 and FaMYB98 the 299
DUALhunter system was used (Figure 9) Cells expressing the FaMYB98 and 300
FaERF9 protein pair using either FaMYB98 or FaERF9 as the bait grew on DDO 301
QDO and QDO supplemented with 1 mM 3-AT selective medium indicating 302
interaction between the two proteins This putative protein-protein interaction was 303
confirmed by BiFC assay and the combinations of FaMYB98-YFPNFaERF9-YFPC 304
and FaERF9-YFPNFaMYB98-YFPC exhibited strong coincident signals in the 305
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12
nucleus while negative controls produced no detectable fluorescence signal (Figure 306
10) In addition coexpression of FaERF9-YFPNFaERF9-YFPC as well as 307
FaMYB98-YFPNFaMYB98-YFPC also generated signals in the nucleus indicating 308
that FaERF9 and FaMYB98 both could form homodimers or possibly multimers in 309
the nucleus (Figure 10) 310
311
Discussion 312
The AP2ERF superfamily in strawberry 313
The AP2ERF superfamily of plant transcription factors is defined by the AP2ERF 314
domain and comprises the ERF AP2 and RAV families as well as one soloist member 315
(Riechmann et al 2000 Weirauch and Hughes 2011) The completion of multiple 316
plant genome sequences has enabled a genome-scale analysis of the AP2ERF family 317
which in recent years has been systematically studied in diverse fruit species such as 318
tomato grape peach and kiwi fruit (Zhuang et al 2009 Sharma et al 2010 Licausi 319
et al 2010 Yin et al 2010 Pirrello et al 2012 Zhang et al 2012 Zhang et al 320
2016) A few AP2ERF genes have been isolated and characterized in strawberry and 321
CBF orthologs (Owens et al 2002 Koehler et al 2012 Zhang et al 2014) have 322
been identified from different strawberry cultivars in several independent studies 323
Although they have distinct names eg Fragaria times ananassa CBF1 (FaCBF1) 324
FaCBF4 (GenBank HQ9105151) and CBF1 (GenBank EU1172142) according to 325
the phylogenetic tree generated in this study the orthologs of 326
CBF1CBF4CBF2CBF3 in Arabidopsis are similar to each other and to FaERF20 327
(Supplemental Figure S1) (Owens et al 2002 Koehler et al 2012 Zhang et al 328
2014) FaERF20 has 85 sequence similarity with FaCBF1 identified by Owens et 329
al (2002) 93 similarity with FaCBF4 amplified by Koehler et al (2012) and 75 330
similarity with CBF1 cloned by Zhang et al (2014) The AP2ERF genes 331
characterized in other studies (Jia et al 2011 GAO et al 2015 Chai and Shen 2016 332
Mu et al 2016) are also noted in Supplemental Table S1 333
334
Based on the computational analysis we have identified a total of 120 AP2ERF 335
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13
genes in octoploid strawberry (Supplemental Table S1) The number of predicted 336
AP2ERF genes (120) is comparable to those observed in other fruits including 337
tomato (112) Chinese plum (116) citrus (126) and peach (131) but lower than those 338
reported for grape (149) (Xie et al 2016) As shown in Supplemental Table S2 79 339
(95 genes) of the AP2ERF genes belong to the ERF family in strawberry constituting 340
the largest sub-family The members of this sub-family can be classified into 10 341
groups (group I to X) according to their sequence similarities to the Arabidopsis ERF 342
genes (Nakano et al 2006) The AP2 family encompasses the same number of genes 343
in Arabidopsis citrus and strawberry (eighteen) (Nakano et al 2006 Xie et al 2014) 344
and there are six RAV genes in strawberry which are highly conserved in dicots such 345
as Vitis vinifera Arabidopsis thaliana and Populus trichocarpa (Licausi et al 2010) 346
347
Role of FaERF9 in regulating the biosynthesis of HDMF a positive regulator 348
acting in an indirect manner 349
The large-scale screening of the AP2ERF superfamily in strawberry led to 350
identification of 11 ERFs and 1 RAV that trans-activated the FaQR promoter more 351
than two-fold with the highest activation caused by FaERF9 which trans-activated 352
the FaQR promoter (Figure 2) as well as up-regulating FaQR expression and furanone 353
production in transient overexpression assays (Figure 4) which has been extensively 354
used to explore the fruit-associated gene functions in strawberry (Han et al 2015 355
Medina-Puche et al 2015 Vallarino et al 2015 Carvalho et al 2016 Song et al 356
2016 Wang et al 2018) FaERF9 transcripts accumulate in the fruit apical section 357
before the basal section (Figure 3) a finding consistent with the actual changes in 358
furaneol content (Figure 1) and the expression of FaQR (Figure 1) The association 359
between FaERF9 transcripts and accumulation of furanones were also established 360
with different strawberry cultivars The correlation between FaERF9 and FaQR 361
expression as well as furanone content among cultivars supports a positive role of 362
FaERF9 in regulating furanone content (Figure 5) These results indicate that 363
FaERF9 transcript abundance may be a good indicator of the abundance of these 364
important flavour volatiles in fruits of different cultivars This should be considered as 365
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
14
a method for high-throughput variety screening to replace direct measurement of 366
volatiles 367
368
FaERF9 is a member of the ERF group II family and is most closely related to the 369
Arabidopsis genes At1g44830 (ATERF014) At1g21910 (DREB26) and At1g77640 370
(Supplemental Figure S1) At1g44830 was observed to be strongly up-regulated in a 371
comprehensive microarray analysis of the root transcriptome following NaCl 372
exposure (Jiang and Deyholos 2006) At1g21910 (DREB26) was functionally 373
characterized as a trans-activator localized in the nucleus exhibiting tissue-specific 374
expression and participating in plant developmental processes as well as biotic andor 375
abiotic stress signalling (Krishnaswamy et al 2011) However none of these genes 376
have been reported as furanone regulators In strawberry another five genes 377
(FaERF6 FaERF7 FaERF8 FaERF10 and FaERF11) also belong to the same 378
group with FaERF8 also showing somewhat weaker activation activity towards the 379
FaQR promoter than FaERF9 The fact that FaERF9 could not bind directly to the 380
promoter of FaQR (Figure 6) indicates that it might function as an indirect regulator 381
of FaQR and furaneol biosynthesis 382
383
A FaERF9 and FaMYB98 complex is involved in regulating FaQR and furaneol 384
biosynthesis 385
The finding that FaERF9 could interact with FaMYB98 protein (Figures 9 and 386
Figure 10) and that FaMYB98 could physically bind to the FaQR promoter (Figure 6 387
and Figure 7) provides evidence for a regulatory mechanism whereby FaERF9 388
regulates FaQR and furaneol production as part of a complex with an MYB 389
transcription factor Since co-overexpression of FaERF9 and FaMYB98 resulted in 390
much higher activation activity towards FaQR we speculate that FaERF9 may 391
recruit FaMYB98 homologs in tobacco to activate the FaQR promoter (Figure 8) 392
FaOMT is another key gene for furanone biosynthesis and a potential target for 393
transcriptional activation However FaERF9 did not significantly activate the 394
FaOMT promoter in a dual-luciferase assay and the transcript level of FaOMT in the 395
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
15
FaERF9-overexpressing fruits showed no significant difference from that in the 396
control (Supplemental Figure S6 Supplemental Figure S7) The FaOMT promoter 397
was significantly induced by FaMYB98 but no synergistic effect of FaERF9 and 398
FaMYB98 on the promoter was observed (Supplemental Figure S6) In previous 399
studies of the regulation of plant volatile compounds MYBs have been characterized 400
as being involved mainly in the regulation of the benzenoidphenylpropanoid pathway 401
that produces floral volatiles in petunia and eugenol in ripe strawberry fruit (Verdonk 402
et al 2005 Dal Cin et al 2011 Colquhoun et al 2011 Spitzer-Rimon et al 2012 403
Medina-Puche et al 2015) but their role in formation of volatiles from other 404
pathways has not been reported Our study demonstrates a role for MYB in the 405
synthesis of furaneol a carbohydrate-derived volatile compound and reveals the 406
synergistic interactions between an MYB and ERF in a transcription complex (Figure 407
8 Figure 9 and Figure 10) 408
409
Recent research has provided evidence for interactions between AP2ERF and MYB 410
transcription factors in regulating other aspects of fruit quality including texture 411
(EjAP2-1 and EjMYB Zeng et al 2015) and colour (PyERF3 and PyMYB114 Yao 412
et al 2017) A group VIII ERF has also recently been shown to interact with an MYB 413
to regulate floral scent production in petunia (Liu et al 2017) In strawberry fruit 414
DOF in combination with an MYB has been reported to be involved in the regulation 415
of eugenol production and the identification of this second transcription factor (DOF) 416
suggests that it is a good target in breeding for improved flavour (Molina-Hidalgo et 417
al 2017 Tieman 2017) Considering its important contribution to flavour in 418
strawberry and many other highly valued fruit crop species (pineapple tomato mango 419
etc) very little is known about regulation of furaneol synthesis Here we established 420
the role of FaERF9 in the regulation of HDMF synthesis by direct protein-protein 421
interactions with FaMYB98 to synergistically trans-activate FaQR The functional 422
identification of this complex enhances our knowledge of the regulation of volatile 423
compound synthesis and identifies a new AP2ERF-MYB complex Further 424
examination of the other ERFs that stimulated transcription from the FaQR promoter 425
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16
(Figure 2) may provide additional information about the complexity of this regulation 426
Overall this study provides important clues for understanding the transcriptional 427
regulation of HDMF synthesis and identifies specific transcription factors that are 428
likely to be good targets for molecular breeding for improved flavour 429
430
Conclusions 431
Screening of the AP2ERF superfamily in strawberry (Fragaria times ananassa) 432
identified candidate members capable of activating the FaQR promoter An ERF 433
transcription factor was identified as a positive regulator of HDMF synthesis in 434
strawberry fruit and the mechanism of activation was shown to involve an ERF-MYB 435
transcription complex that regulates transcription of FaQR leading to the biosynthesis 436
of HDMF the characteristic volatile compound which has a major influence on 437
strawberry aroma 438
439
Materials and Methods 440
441
Plant Materials and Growth conditions 442
The strawberry (Fragaria times ananassa cv lsquoYuexinrsquo an octoploid cultivar) fruit used in 443
this study were bred by Zhejiang Academy of Agricultural Sciences (Haining 444
Zhejiang) Fruits at various developmental and ripening stages including G (green) T 445
(turning) IR (intermediate red) and R (full red) were harvested (Figure 1) and 446
transported to the laboratory within 2 h Thirty-six fruits of uniform size and free of 447
visible defects were selected at each stage with twelve fruits in each biological 448
replicate After removing the calyces fruits were then divided into the basal and 449
apical sections which were sampled separately (Figure 1) They were rapidly cut into 450
pieces frozen immediately in liquid nitrogen and stored at -80deg C until use Red ripe 451
fruits of different strawberry cultivars (Fragaria times ananassa octoploid cultivars) 452
including lsquoYuelirsquo lsquoBenihoppersquo lsquoMengxiangrsquo lsquoAmaoursquo lsquo10-1-4rsquo lsquoAkihimersquo lsquoSweet 453
Charliersquo lsquo07-1-4rsquo lsquoDarselectrsquo lsquoYuexinrsquo and lsquoXuemeirsquo were also provided by Zhejiang 454
Academy of Agricultural Sciences For each cultivar the fruits of three biological 455
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17
replicates were sampled frozen in liquid nitrogen and stored at -80deg C for further use 456
457
Tobacco plants (Nicotiana benthamiana) used for dual-luciferase assays and 458
subcellular localization analysis in this study were grown in a growth chamber with a 459
lightdark cycle of 16 h8 h at 24degC 460
461
Detection of DMMF and HDMF 462
Automated HS-SPME-GC-MS was performed to detect both furanones in lsquoYuexinrsquo 463
strawberry fruit (Zorrilla-Fontanesi et al 2012) Samples were ground into a powder 464
under liquid nitrogen for analysis 465
466
For the detection of DMMF (Figure 1) 05 g (fresh weight) of each sample was 467
weighed in the vial to which was added 1 mL of EDTA solution (100 mM pH 75) 1 468
mL of CaCl2 solution (mv = 20) and 20 microL of 2-octanol as the internal standard 469
(007 μgμL) The mixture was homogenized and the vial closed and placed on the 470
sample tray for analysis by CombiPAL autosampler (CTC Analytic CA USA) The 471
fruit volatiles were sampled by headspace solid-phase microextraction with a 65-μm 472
polydimethylsiloxane-divinylbenzene fibre (PDMS-DVB) Initially vials were 473
pre-incubated at 50degC for 10 min under continuous agitation (500 rpm) then volatiles 474
were extracted for 30 min at the same temperature and agitation speed After that the 475
fibre was desorbed in the GC injection port for 5 min in splitless mode The 7890A 476
GC chromatograph was equipped with a DB-5ms column (60 m times 250 μm times 1 μm 477
JampW Scientific Folsom CA USA) with helium as the carrier gas at a constant flow 478
of 12 mLmin The GC was programmed at an initial temperature of 35degC for 2 min 479
with a ramp of 5degC min up to 250degC and held for 5 min The injection port interface 480
and MS source temperatures were 250degC 260degC and 230degC respectively The 481
ionization potential was set at 70 eV recorded by a 5975B mass spectrometer (Agilent 482
Technologies JampW Scientific Folsom CA USA) and the scanning speed was 7 483
scanss The same method was used to analyse HDMF and DMMF in fruits from 484
different cultivars (Supplemental Figure S3) except for the sample preparation 485
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
18
procedure (Araguumlez et al 2013) briefly 05 g (fresh weight) of powdered fruit was 486
incubated at 30degC in a water bath for 5 min then 2 mL of NaCl (mv = 20) and 20 487
microL of 2-octanol as the internal standard (007 μgμL) were added and homogenized 488
489
For the detection of HDMF (Figure 1) and both furanones (Figure 4 and Supplemental 490
Table S3) a liquid-injection system equipped with CTC Pal ALS was used One gram 491
(fresh weight) of powdered fruit and 2 mL of NaCl (mv = 20) were homogenized in 492
a 10-mL tube and 300 μL of CH2Cl2 and 20 microL of 2-octanol (0766 μgμL) as the 493
internal standard were added to extract the volatiles the mixture was then 494
homogenized again The tubes were stored at room temperature for 20 min and 495
centrifuged at 12000 rpm for 5 min The subnatant was pipetted into a clean 15-mL 496
tube in which 20 mg of anhydrous sodium sulphate was added the tube was left 497
without shaking for half an hour Then 150 μL of the solution was transferred into a 498
GC vial and placed on the sample tray as described above Each sample (1 μL) was 499
injected using the autosampler and the analysis was accomplished by a 7890A 500
GC-MS system (Agilent Technologies JampW Scientific Folsom CA USA) equipped 501
with a DB-WAX column (30 m times 025 mm times 025 μm JampW) Helium (12 mLmin) 502
was used as a carrier gas The injection port (splitless injection mode) interface and 503
MS source temperatures were as described above The oven temperature was set at 504
60degC for 4 min then increased to 180degC at a rate of 4degCmin and maintained for 30 505
min DMMF was identified by comparison of electron ionization mass spectra and 506
retention time data with the data from the NISTEPANIH mass spectral library 507
(NIST-08 and Flavor) HDMF (Figure 1) was identified and qualified by comparison 508
with injected standard (Sigma) The quantitative analysis of both furanones (Figure 4 509
Supplemental Table S3 and Supplemental Figure S3) was determined using the peak 510
area of the internal standard as a reference based on total ion chromatogram (TIC) 511
512
RNA isolation and Reverse Transcription Quantitative PCR (RT-qPCR) 513
Total RNA from strawberry samples was isolated in this study using the CTAB 514
method (Chang et al 1993) Genomic DNA contamination was eliminated by 515
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
19
TURBO Dnase (Ambion) 1 μg of RNA was used to obtain cDNA using an IScriptTM 516
cDNA Synthesis Kit (Bio-Rad) The synthesized cDNA was diluted with water (120) 517
and 2 μL of diluted cDNA was used as the template for RT-qPCR Reactions were 518
performed in a total volume of 20 μL consisting of 10 μL of SYBR PCR supermix 519
(Bio-Rad) 1 μL of each primer (10 μM) 6 μL of DEPC-H2O and 2 μL of diluted 520
cDNA on CFX96 instrument (Bio-Rad) (Yin et al 2012) The oligonucleotide 521
primers for RT-qPCR analysis of genes including the AP2ERF FaQR and FaOMT 522
were designed according to the coding sequences of genes and the specificity was 523
verified before use (Min et al 2012) NCBIPrimer-BLAST was applied to design the 524
primers Relative expression levels were normalized to that of an internal controlmdashthe 525
interspacer 26S-18S strawberry RNA housekeeping gene FaRIB413 526
(Zorrilla-Fontanesi et al 2012) To investigate the differential expression of genes 527
during fruit development and ripening stages relative expression of each gene at the 528
R stage in the basal fruit section was set as 1 using the 2minus∆∆119862119879 method For transient 529
overexpression assay relative expression of control fruits with an empty vector (SK) 530
was set as 1 The primers used in RT-qPCR are listed in Supplemental Table S4 531
532
Gene isolation and analysis 533
Multiple database searches were performed to identify members of the strawberry 534
(Fragaria times ananassa) AP2ERF superfamily in the published strawberry databases 535
and annotations of Fragaria times ananassa and Fragaria times vesca by using the 536
AP2ERF DNA binding domain as a query sequence and 120 genes were identified 537
with AP2ERF domain(s) Based on the BLAST result primers (listed in 538
Supplemental Table S5) were used to amplify the coding full-length cDNAs of 539
AP2ERF genes The deduced amino acid sequences of AP2ERF proteins in 540
Arabidopsis thaliana used for construction of a phylogenetic tree were obtained from 541
the Arabidopsis Information Resource (TAIR) Alignment of the proteins was 542
performed using the neighbour-joining method in ClustalX (v181) and the 543
phylogenetic tree was constructed using FigTree (v131) 544
545
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
20
FaMYB98 was obtained by yeast one-hybrid screening sequencing and the full-length 546
sequences were predicted by BLAST Primers were designed (listed in Supplemental 547
Table S5) to amplify the full-length coding sequence 548
549
The promoter of FaQR was cloned by Genome Walking as previously described (Yin 550
et al 2010) and conserved cis-element motifs in the promoter were manually 551
searched 552
553
Conserved domains within the FaAP2ERF proteins and FaMYB98 were analysed by 554
CD-search (httpswwwncbinlmnihgovStructurecddwrpsbcgi) and cellular 555
locations of proteins including FaERF9 and FaMYB98 were predicted with the 556
WoLF PSORT program (httpswwwgenscriptcomwolf-psorthtml) 557
558
Dual-Luciferase Assays 559
In accordance with a previous protocol (Yin et al 2010) the full-length cDNAs of 560
FaAP2ERF or FaMYB98 transcription factors were cloned into pGreen II 0029 561
62-SK vector and the promoter of FaQR was cloned into pGreen II 0800-LUC vector 562
A luciferase gene from Renillia (REN) driven by a 35S promoter in the LUC vector 563
acted as a positive control The above constructs were transiently expressed in 564
Nicotiana benthamiana leaves by Agrobacterium-mediated infiltration (strain 565
GV3101) and the activity of the TFs on the promoter was measured on the third day 566
after infiltration indicated by the ratio of enzyme activities of firefly luciferase (LUC) 567
and renilla luciferase (REN) using a Modulus Luminometer (Promega Madison WI 568
USA) To determine the activity of a specific transcription factor towards the 569
promoter we mixed the Agrobacterium culture with 1 mL of TF and 100 μL of 570
promoter and the LUCREN value of the empty vector SK on the promoter was set as 571
1 as a calibrator To test the combined effect of two transcription factors on the 572
promoter to the Agrobacterium culture mixture we added 05 mL of each TF and 100 573
μL of promoter the effect of the mixtures that contained each transcription factor (05 574
mL) and empty vector SK (05 mL) was also tested on the promoter as a control 575
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
21
576
Subcellular localization analysis 577
35S-FaERF9-GFP and 35S-FaMYB98-GFP were transiently expressed in tobacco (N 578
benthamiana) leaves by Agrobacterium infiltration (EHA105) using the same method 579
as described in the dual-luciferase assay above The transiently infected leaves were 580
imaged on the third day after infiltration using a Nikon A1-SHS confocal laser 581
scanning microscope The excitation wavelength for GFP fluorescence was 488 nm 582
and fluorescence was detected at 490ndash520 nm The primers used for GFP construction 583
are listed in Supplemental Table S6 584
585
Transient overexpression in strawberry fruit 586
Transient overexpression of FaERF9 and an overexpression binary vector (pGreen II 587
0029 62-SK-FaERF9-FaMYB98) were performed in strawberry fruit using the 588
FaERF9-SK construct described above for the dual-luciferase assays and the binary 589
vector constructed according to Liu et al 2013 The transfection of fruit was carried 590
out at the G stage (Hoffmann et al 2006) The FaERF9-SK construct and binary 591
vector were individually electroporated into Agrobacterium tumefaciens GV3101 and 592
the Agrobacterium culture suspended in infiltration buffer was infiltrated into the 593
whole fruit using a syringe As a control treatment fruits were infiltrated with 594
Agrobacterium carrying an empty vector SK under the same transfection conditions 595
Fruits were left attached to the plants and harvested on the seventh day after 596
infiltration Fruits of three biological replicates were sampled for further analysis 597
598
Yeast one-hybrid assay 599
In order to identify proteins that bind to the FaQR promoter the Matchmaker Gold 600
Yeast One-hybrid Library Screening System (Clontech USA) was used The sequence 601
of the FaQR promoter was cloned into the pAbAi vector and the construct was 602
integrated into the genome of the Y1HGold yeast strain A mixture of total RNA from 603
strawberry fruit at four stages (G T IR R) was used to construct the prey cDNA 604
library (TaKaRa) The background AbAr expression of Y1HGold FaQR-pAbAi strain 605
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
22
was tested according to the system user manual and then screening for protein-DNA 606
interactions was carried out Furthermore the full length of each transcription factor 607
was separately cloned into pGADT7 AD vector to confirm the screening results The 608
relationship between FaERF9 and FaQR promoter was also examined individually 609
Primers used in this assay are listed in Supplemental Table S6 610
611
Expression and purification of FaMYB98 recombinant protein 612
A 405-bp region spanning the DNA-binding domain of FaMYB98 was amplified 613
from FaMYB98 cDNA and cloned into a pET6timesHN vector (Clontech Palo CA USA) 614
to generate the recombinant N-terminal His-tagged protein the primers used are listed 615
in Supplemental Table S6 The resulting construct was sequenced and introduced into 616
Escherichia coli strain Rosetta 2(DE3)pLysS (Novagen) Ten millilitres of the 617
overnight culture was combined with 500 mL of an LB liquid medium (100 μgmL 618
ampicillin and 34 μgmL chloramphenicol) as described (Li et al 2017) Isopropyl 619
β-D-1-thiogalactopyranoside (IPTG) was added to a final concentration of 1 mM and 620
the bacterial culture was incubated at 18degC at 150 rpm for 18 h Then the cells were 621
harvested using a centrifuge and resuspended in 1times PBS buffer (Sangon Biotech) 622
after which they were disrupted by sonication and the supernatant was purified using 623
a HisTALONTM Gravity Column (Clontech) according to the user manual The PD-10 624
Desalting column (GE Healthcare) was then used for buffer change and sample 625
clean-up of proteins according to the gravity protocol SDS-PAGE was performed and 626
the protein was visualized using Coomassie brilliant blue 627
628
Electrophoretic mobility shift assay (EMSA) 629
A Lightshift Chemiluminescent EMSA kit (Thermo) was used to perform EMSA 630
experiments according to the manufacturerrsquos instructions Single-strand 631
oligonucleotides were synthesized and biotinylated by GeneBio Biotech (Hangzhou 632
China) The details of the EMSA assay are provided in Ge et al (2017) The probes 633
used for EMSAs are listed in Supplemental Table S6 634
635
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
23
636
Yeast two-hybrid assay 637
The DUALhunter system (Dualsystems Biotech Switzerland) was used to investigate 638
the interaction between FaERF9 and FaMYB98 Full-length coding sequences of 639
FaERF9 and FaMYB98 were respectively cloned into pDHB1 bait vector and 640
pPR3-N prey vector sequences were verified and the bait plasmid was 641
co-transformed with prey plasmid into NMY51 in the combinations below 642
FaMYB98-pDHB1pPR3-N FaMYB98-pDHB1FaERF9-pPR3-N 643
FaMYB98-pDHB1pOst1-NubI FaERF9-pDHB1pPR3-N 644
FaERF9-pDHB1FaMYB98-pPR3-N and FaERF9-pDHB1pOst1-NubI (Li et al 645
2017) Transformed cells were spread onto the following plates DDO (SD 646
medium-Trp-Leu) QDO (SD medium-Trp-Leu-His-Ade) and QDO+3-AT (QDO 647
medium supplemented with 1 mM 3-amino-124-triazole) The control plasmid 648
pOst1-NubI was used to determine whether the bait was functional the pPR3-N prey 649
vector plasmid was used to test whether the bait displayed non-specific background 650
and positive interactions were indicated by the growth of yeast on QDO and 651
QDO+3-AT plates The Primers used in the DUALhunter assay are listed in 652
Supplemental Table S6 653
654
Bimolecular fluorescence complementation (BiFC) assays 655
Full-length FaERF9 and FaMYB98 respectively were cloned into sequences 656
encoding the N- and C- fragments of YFP protein (Lv et al 2014) All constructs 657
were transiently expressed in tobacco (N benthamiana) leaves by Agrobacterium 658
infiltration (EHA105) The YFP fluorescence of transfected leaves was imaged 40 h 659
after infiltration by using a Nikon A1-SHS confocal laser scanning microscope The 660
excitation wavelength for YFP was 488 nm and fluorescence was detected at 520ndash661
540 nm Primers used are listed in Supplemental Table S6 662
663
Statistics 664
A Studentrsquos two-tailed t test ( plt005 plt001 and plt0001) was used to 665
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
24
determine significant differences between two groups in this study Microsoft Excel 666
was used to perform linear regressive analysis significant differences were 667
determined by SPSS Statistics 200 and scatter plots were prepared with Origin80 668
Least significant difference (LSD) at the 5 level was calculated using Microsoft 669
Excel Figures were prepared with Origin80 (Microcal Software Inc Northampton 670
MA USA) The online tool MetaboAnalyst 36 (httpwwwmetaboanalystca) was 671
used to analyse the transcript abundance of the AP2ERF genes 672
673
Accession numbers 674
Sequence data from this article have been deposited in GenBank under the accession 675
numbers MH332903-MH333022 for AP2ERF genes in Fragaria times ananassa and 676
MH333023 for FaMYB98 GenBank numbers for FaQR and FaOMT were 677
AY1588361 (Raab et al 2006) and AF2204912 (Wein et al 2002) 678
679
Supplemental Material 680
Supplemental Figure S1 Phylogenetic analysis of FaAP2ERF and Arabidopsis 681
AP2ERF proteins 682
Supplemental Figure S2 Analysis of FaAP2ERF gene expression patterns in 683
strawberry fruit during development and ripening 684
Supplemental Figure S3 Contents of furanones in fruit of strawberry cultivars 685
Supplemental Figure S4 Relative expression of FaERF9 in FaERF9-FaMYB98- 686
and FaERF9-overexpressing fruits 687
Supplemental Figure S5 Subcellular localization of FaMYB98 688
Supplemental Figure S6 The combined activation effects of FaERF9FaMYB98 on 689
the FaOMT promoter 690
Supplemental Figure S7 Relative expression of FaOMT in 691
FaERF9-overexpressing fruits 692
Supplemental Table S1 AP2ERF superfamily genes in Fragaria times ananassa 693
Supplemental Table S2 Classification of the AP2ERF superfamily members in 694
Fragaria times ananassa 695
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
25
Supplemental Table S3 Furanone content in FaERF9-FaMYB98- and 696
FaERF9-overexpressing fruits 697
Supplemental Table S4 Primers used for reverse transcription quantitative PCR 698
(RT-qPCR) 699
Supplemental Table S5 Primers used to amplify the full-length coding sequences of 700
AP2ERF genes and FaMYB98 in strawberry (Fragaria times ananassa) 701
Supplemental Table S6 Primers used for vector construction 702
703
Acknowledgments 704
This research was supported by the National Key Research and Development 705
Program (2016YFD0400101) the Project of the Science and Technology Department 706
of Zhejiang Province (2016C04001) and the 111 Project (B17039) 707
708
Figure legends 709
Figure 1 Changes in furanone content and furanone biosynthetic genes during 710
strawberry (Fragaria times ananassa Duch cv Yuexin) fruit development and ripening 711
A Fruits were collected at four ripening stages G (green stage) T (turning stage) IR 712
(intermediate red stage) R (full red stage) B Changes in the contents of furaneol 713
(HDMF) and mesifurane (DMMF) HDMF content was calculated using a standard 714
curve of HDMF while DMMF content was calculated with an internal standard as the 715
reference C Expression levels of FaQR and FaOMT The expression levels of each 716
gene were calculated relative to corresponding values in the basal section at the R 717
stage SEs were calculated from three replicates and LSD values represent the least 718
significant differences at p = 005 719
Figure 2 Regulatory effects of FaAP2ERF on the promoter of FaQR LUCREN 720
values of the empty vector on FaQR promoter were used as the calibrator set as 1 721
and SEs were calculated from five replicates statistical significance was determined 722
by Studentrsquos two-tailed t test ( plt0001) 723
Figure 3 Expression and the subcellular localization of FaERF9 A The expression 724
levels were calculated relative to the levels in the basal section at the R stage B 725
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
26
Subcellular localization analysis was performed in tobacco leaves The tobacco used 726
in the assay was stably transformed with a specific nucleus localized red fluorescence 727
protein construct and the red fluorescence indicates the nucleus-localized signal 728
(NLS) Scale bar = 25 microm SEs were calculated from three replicates 729
Figure 4 Transient overexpression of FaERF9 in strawberry fruit A Relative 730
expression of FaQR and FaERF9 in FaERF9-OX fruit 7 days after infiltration The 731
expression was calculated relative to the average value in control (SK) fruits B 732
HDMF and DMMF content in FaERF9-OX fruit The content of both furanones 733
were quantified using the peak area of the internal standard (2-octanol) as the 734
reference SEs were calculated from three replicates Statistical significance was 735
determined by Studentrsquos two-tailed t test ( plt005 plt001 plt0001) 736
Figure 5 Scatter plots of 11 strawberry cultivars A Linear regression analysis 737
between FaERF9 expression and FaQR expression B Linear regression analysis 738
between FaERF9 expression and furanone content The relative expression was 739
normalized to that of the housekeeping gene FaRIB413 and furanone content was 740
calculated with internal standard as the reference Significant differences were 741
determined by SPSS Statistics 200 742
Figure 6 Interactions of FaERF9 and FaMYB98 with the FaQR promoter A Yeast 743
one-hybrid analysis of the interaction of FaERF9 and FaQR promoter B Yeast 744
one-hybrid analysis of the interaction of FaMYB98 and FaQR promoter C 745
Regulatory effect of FaMYB98 on the FaQR promoter Auto-activation was tested on 746
SD-Ura (synthetically defined medium without uracil) in presence of Aureobasidin A 747
(AbA) and physical interaction was determined on SD-Leu (synthetically defined 748
medium without leucine) in presence of AbA LUCREN values of the empty vector 749
on FaQR promoter were used as the calibrator set as 1 and error bars were calculated 750
from five replicates Statistical significance was determined by Studentrsquos two-tailed t 751
test ( plt005 plt001 plt0001) 752
Figure 7 Electrophoretic mobility shift assay of FaMYB98 binding to FaQR 753
promoter A The probe sequence used for EMSA and mutated nucleotides are 754
indicated with lowercase letters B Purified DNA-binding domain of FaMYB98 755
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
27
protein and biotin-labelled DNA probe were mixed and analysed on 6 native 756
polyacrylamide gels and then photographed Presence or absence of specific probes is 757
marked by the symbol + or - 758
Figure 8 The combined activation effects of FaERF9FaMYB98 on the FaQR 759
promoter LUCREN values obtained with the empty vector and FaQR promoter were 760
used as the calibrator set as 1 and error bars were calculated from five replicates 761
Figure 9 Yeast two-hybrid analysis of the protein-protein interactions between 762
FaMYB98 and FaERF9 Positive interactions were determined by the growth of 763
yeast cells on selection plates Bait with pOST acted as positive controls and bait with 764
pPR3 as negative controls DDO synthetically defined medium without tryptophan 765
and leucine QDO synthetically defined medium without tryptophan leucine 766
histidine and adenine QDO+3AT QDO medium supplemented with 1 mM 767
3-aminotriazole 768
Figure 10 BiFC analysis of the protein-protein interactions between FaMYB98 and 769
FaERF9 The pairs of fusion proteins tested were FaMYB98-YFPN+FaERF9-YFPC 770
FaERF9-YFPN+FaMYB98-YFPC FaMYB98-YFPN+FaMYB98-YFPC and 771
FaERF9-YFPN+FaERF9-YFPC The other combinations were negative controls 772
The tobacco used in the assay was stably transformed with a specific 773
nucleus-localized red fluorescence protein construct and the red fluorescence 774
indicated the nucleus-localized signal (NLS) Fluorescence of the yellow fluorescence 775
protein (YFP) visualized the interaction in vivo Scale bar = 25 microm 776
777
Literature Cited 778
779
Agarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression 780
of PgDREB2A transcription factor enhances abiotic stress tolerance and activates 781
downstream stress-responsive genes Mol Biol Rep 37 1125-1135 782
Araguumlez I Osorio S Hoffmann T Rambla JL Medina-Escobar N Granell A 783
Botella MAacute Schwab W Valpuesta V (2013) Eugenol production in achenes and 784
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
28
receptacles of strawberry fruits is catalyzed by synthases exhibiting distinct kinetics 785
Plant Physiol 163 946-958 786
Carvalho RF Carvalho SD OrsquoGrady K Folta KM (2016) Agroinfiltration of 787
strawberry fruit mdash a powerful transient expression system for gene validation Curr 788
Plant Biol 6 19-37 789
Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic 790
(Amsterdam) 210 34-40 791
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating 792
RNA from pine trees Plant Mol Biol Rep 11 113-116 793
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC 794
Clark DG (2011) PhMYB4 fine-tunes the floral volatile signature of 795
Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143 796
Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz 797
EA Taylor MG Smits-Kroon MT Schuurink RC Haring MA Giovannoni J 798
Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic 799
pathway by ectopic expression of a MYB transcription factor in tomato fruit Plant 800
Cell 23 2738-2753 801
Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan 802
XW Yang ZY (2017) Differential responses of four biosynthetic pathways of 803
aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under 804
interaction of light and temperature Food Chem 221 356-364 805
Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of 806
differentially-expressed genes during somatic embryogenesis in Fragaria times 807
ananassa Duch lsquoBenihopprsquo J Hortic Sci Biotechnol 90 671-681 808
Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 809
transcriptionally regulates chilling-induced lignification of loquat fruit via physical 810
interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136 811
Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM 812
(2004) Functional interactions between a glutamine synthetase promoter and MYB 813
proteins Plant J 39 513-526 814
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
29
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) 815
Sucrose nonfermenting1-related protein kinase26 an ortholog of open stomata1 is 816
a negative regulator of strawberry fruit development and ripening Plant Physiol 817
167 915-930 818
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene 819
expression in strawberry fruit (Fragaria times ananassa) by agroinfiltration a rapid 820
assay for gene function analysis Plant J 48 818-826 821
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of 822
selected aroma-active compounds in strawberries by headspace solid-phase 823
microextraction gas chromatography and correlation with sensory descriptive 824
analysis J Food Sci 72 S487-S496 825
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid 826
plays an important role in the regulation of strawberry fruit ripening Plant Physiol 827
157 188-199 828
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of 829
NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes BMC 830
Plant Biol 6 20 831
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN 832
(2005) MYB98 is required for pollen tube guidance and synergid cell differentiation 833
in Arabidopsis Plant Cell 17 2981-2992 834
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional 835
characterization of enone oxidoreductases from strawberry and tomato fruit J 836
Agric Food Chem 55 6705-6711 837
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You 838
J-S Rohloff J Randall SK Alsheikh M (2012) Proteomic study of 839
low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ 840
in cold tolerance Plant Physiol 159 1787-1805 841
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional 842
characterization of four APETALA2-family genes (RAP26 RAP26L DREB19 843
and DREB26) in Arabidopsis Plant Mol Biol 75 107-127 844
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
30
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon 845
J Gupta V (2013) An oxidoreductase from lsquoAlphonsorsquo mango catalyzing 846
biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494 847
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in 848
strawberries Z Lebensm-Unters Forsch 195 120-123 849
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X 850
(2015) Label-free quantitative proteomics to investigate strawberry fruit proteome 851
changes under controlled atmosphere and low temperature storage J Proteomics 852
120 44-57 853
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 854
cooperates with CitWRKY1 to participate in citric acid degradation via 855
up-regulation of CitAco3 J Exp Bot 68 3419-3426 856
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription 857
factor CitERF71 activates the terpene synthase gene CitTPS16 involved in the 858
synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938 859
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and 860
transcriptomic analysis of the AP2ERF superfamily in Vitis vinifera BMC 861
Genomics 11 719 862
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive 863
Factor (AP2ERF) transcription factors mediators of stress responses and 864
developmental programs New Phytol 199 639-649 865
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 866
interacting with EOBI negatively regulates fragrance biosynthesis in petunia 867
flowers New Phytol 215 1490-1502 868
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu 869
CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 in regulating 870
anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) 871
during anthocyanin biosynthesis Plant Cell Tissue Organ Cult 115 285-298 872
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
31
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao 873
CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphate signaling and 874
homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597 875
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC 876
Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL 877
Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor 878
regulates eugenol production in ripe strawberry fruit receptacles Plant Physiol 168 879
598-614 880
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics 881
and volatile constituents of strawberry (cv Cigaline) during maturation J Agric 882
Food Chem 52 1248-1254 883
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS 884
(2012) Ethylene-responsive transcription factors interact with promoters of ADH 885
and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 886
63 6393-6405 887
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM 888
Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-Franco A 889
Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific 890
transcription factor FaDOF2 regulates the production of eugenol in ripe fruit 891
receptacles J Exp Bot 68 4529-4543 892
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) 893
Comparison and verification of the genes involved in ethylene biosynthesis and 894
signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44 895
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the 896
ERF gene family in Arabidopsis and rice Plant Physiol 140 411-432 897
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in 898
sour cherry and strawberry and the heterologous expression of CBF1 in strawberry 899
J Am Soc Hortic Sci 127 489-494 900
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech 901
JC Ohme-Takagi M Regad F Bouzayen M (2012) Functional analysis and 902
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
32
binding affinity of tomato ethylene response factors provide insight on the 903
molecular bases of plant differential responses to ethylene BMC Plant Biol 12 190 904
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) 905
Methylpentoses are possible precursors of furanones in fruits Prikl Biokhim 906
Mikrobiol 28 123-127 907
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery 908
of synergid-expressed genes encoding filiform apparatus localized proteins Plant 909
Cell 19 2557-2568 910
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria 911
vesca L compared to those of cultivated berries Fragariatimes ananassa cv Senga 912
Sengana J Agric Food Chem 27 19-22 913
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W 914
Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of the strawberry 915
flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone 916
oxidoreductase Plant Cell 18 1023-1037 917
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L 918
Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim M Broun P Zhang 919
JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription 920
factors genome-wide comparative analysis among eukaryotes Science 290 921
2105-2110 922
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the 923
formation of 25-dimethyl-4-hydroxy-3(2H)-furanone in detached ripening 924
strawberry fruits J Agric Food Chem 46 1488-1493 925
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 926
25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in 927
strawberry fruits Phytochemistry 43 155-159 928
Schwab W (1998) Application of stable isotope ratio analysis explaining the 929
bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone in plants by a biological 930
maillard reaction J Agric Food Chem 46 2266ndash2269 931
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33
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) 932
Molecules 18 6936-6951 933
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard 934
products Recent Res Dev Phytochem 1 643-673 935
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL 936
Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJ Sims CA 937
Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical 938
compositions a seasonal influence and effects on sensory perception PLoS One 9 939
e88446 940
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) 941
Identification phylogeny and transcript profiling of ERF family genes during 942
development and abiotic stress treatments in tomato Mol Genet Genomics 284 943
455-475 944
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) 945
CitAP210 activation of the terpene synthase CsTPS1 is associated with the 946
synthesis of (+)-valencene in lsquoNewhallrsquo orange J Exp Bot 67 4105-4115 947
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes 948
Dev Genes Evol 214 105-114 949
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K 950
Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the 951
key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151 952
Spitzer-Rimon B Farhi M Albo B Cnarsquoani A Ben Zvi MM Masci T Edelbaum 953
O Yu YX Shklarman E Ovadis M Vainstein A (2012) The R2R3-MYB-like 954
regulatory factor EOBI acting downstream of EOBII regulates scent production 955
by activating ODO1 and structural scent-related genes in petunia Plant Cell 24 956
5089-5105 957
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp 958
Bot 68 4407-4409 959
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla 960
JF Amaya I Giavalisco P Fernie AR Botella MA Valpuesta V (2015) Central 961
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34
role of FaGAMYB in the transition of the strawberry receptacle from development 962
to ripening New Phytol 208 482-496 963
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 964
regulates fragrance biosynthesis in petunia flowers Plant Cell 17 1612-1624 965
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS 966
(2018) The potassium channel FaTPK1 plays a critical role in fruit quality 967
formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748 968
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) 969
Isolation cloning and expression of a multifunctional O-methyltransferase capable 970
of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma 971
compounds in strawberry fruits Plant J 31 755-765 972
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor 973
types their evolutionary origin and species distribution In A handbook of 974
transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular 975
Biochemistry 52 25-73 976
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of 977
odor (Buettner A Ed) Springer Cham 9-10 978
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS 979
(2014) Isolation classification and transcription profiles of the AP2ERF 980
transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271 981
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in 982
regulation of fruit quality Crit Rev Plant Sci 35 120-130 983
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ 984
Zhang SL Wu J (2017) Map-based cloning of the pear gene MYB114 identifies an 985
interaction with other transcription factors to coordinately regulate fruit 986
anthocyanin biosynthesis Plant J 92 437-451 987
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes 988
involved in regulating fruit ripening Plant Physiol 153 1280-1292 989
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35
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) 990
Expression of ethylene response genes during persimmon fruit astringency removal 991
Planta 235 895-906 992
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25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis and 994
biosynthesis-a review Food Chem 65 139-151 995
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci 996
Food Agric 74 421-434 997
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 998
an AP2ERF gene is a novel regulator of fruit lignification induced by chilling 999
injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1000
1325-1334 1001
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation 1002
classification and transcription profiles of the Ethylene Response Factors (ERFs) in 1003
ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215 1004
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML 1005
(2012) Genome-wide analysis of the AP2ERF superfamily in peach (Prunus 1006
persica) Genet Mol Res 11 4788-4809 1007
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and 1008
expression analysis of a CRTDRE-binding factor gene FaCBF1 from Fragaria times 1009
ananassa Acta Hortic 41 240-248 1010
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The 1011
Arabidopsis AP2ERF transcription factor RAP26 participates in ABA salt and 1012
osmotic stress responses Gene 457 1-12 1013
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B 1014
Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) Genome-wide 1015
analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic 1016
(Amsterdam) 123 73-81 1017
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF 1018
Valpuesta V Botella MA Granell A Amaya I (2012) Genetic analysis of 1019
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36
strawberry fruit aroma and identification of O-methyltransferase FaOMT as the 1020
locus controlling natural variation in mesifurane content Plant Physiol 159 1021
851-870 1022
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
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Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid plays an important role in the regulation of strawberry fruitripening Plant Physiol 157 188-199
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of NaCl-stressed Arabidopsis roots reveals novel classes ofresponsive genes BMC Plant Biol 6 20
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN (2005) MYB98 is required for pollen tube guidance andsynergid cell differentiation in Arabidopsis Plant Cell 17 2981-2992
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional characterization of enone oxidoreductases from strawberry andtomato fruit J Agric Food Chem 55 6705-6711
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You J-S Rohloff J Randall SK Alsheikh M (2012) Proteomicstudy of low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ in cold tolerance Plant Physiol 159 1787-1805
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional characterization of four APETALA2-family genes (RAP26 RAP26LDREB19 and DREB26) in Arabidopsis Plant Mol Biol 75 107-127
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon J Gupta V (2013) An oxidoreductase from Alphonsomango catalyzing biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in strawberries Z Lebensm-Unters Forsch 195 120-123Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X (2015) Label-free quantitative proteomics to investigatestrawberry fruit proteome changes under controlled atmosphere and low temperature storage J Proteomics 120 44-57
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 cooperates with CitWRKY1 to participate in citric aciddegradation via up-regulation of CitAco3 J Exp Bot 68 3419-3426
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription factor CitERF71 activates the terpene synthase geneCitTPS16 involved in the synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and transcriptomic analysis of the AP2ERF superfamily inVitis vinifera BMC Genomics 11 719
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive Factor (AP2ERF) transcription factors mediators of stressresponses and developmental programs New Phytol 199 639-649
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 interacting with EOBI negatively regulates fragrancebiosynthesis in petunia flowers New Phytol 215 1490-1502
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 inregulating anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) during anthocyanin biosynthesis Plant CellTissue Organ Cult 115 285-298
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title wwwplantphysiolorgon February 25 2020 - Published by Downloaded from
Copyright copy 2018 American Society of Plant Biologists All rights reserved
Google Scholar Author Only Title Only Author and Title
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphatesignaling and homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor regulates eugenol production in ripe strawberry fruitreceptacles Plant Physiol 168 598-614
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics and volatile constituents of strawberry (cv Cigaline)during maturation J Agric Food Chem 52 1248-1254
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS (2012) Ethylene-responsive transcription factors interact withpromoters of ADH and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 63 6393-6405
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-FrancoA Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific transcription factor FaDOF2 regulates the production ofeugenol in ripe fruit receptacles J Exp Bot 68 4529-4543
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) Comparison and verification of the genes involved in ethylenebiosynthesis and signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice Plant Physiol140 411-432
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in sour cherry and strawberry and the heterologousexpression of CBF1 in strawberry J Am Soc Hortic Sci 127 489-494
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech JC Ohme-Takagi M Regad F Bouzayen M (2012)Functional analysis and binding affinity of tomato ethylene response factors provide insight on the molecular bases of plant differentialresponses to ethylene BMC Plant Biol 12 190
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) Methylpentoses are possible precursors of furanones in fruits PriklBiokhim Mikrobiol 28 123-127
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery of synergid-expressed genes encoding filiformapparatus localized proteins Plant Cell 19 2557-2568
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria vesca L compared to those of cultivated berriesFragariatimes ananassa cv Senga Sengana J Agric Food Chem 27 19-22
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of thestrawberry flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone oxidoreductase Plant Cell 18 1023-1037
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim MBroun P Zhang JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription factors genome-wide comparative analysisamong eukaryotes Science 290 2105-2110
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
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Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the formation of 25-dimethyl-4-hydroxy-3(2H)-furanonein detached ripening strawberry fruits J Agric Food Chem 46 1488-1493
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Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in strawberry fruits Phytochemistry 43 155-159
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Schwab W (1998) Application of stable isotope ratio analysis explaining the bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone inplants by a biological maillard reaction J Agric Food Chem 46 2266ndash2269
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Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) Molecules 18 6936-6951Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard products Recent Res Dev Phytochem 1 643-673Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJSims CA Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical compositions a seasonal influence and effects on sensoryperception PLoS One 9 e88446
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Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) Identification phylogeny and transcript profiling of ERFfamily genes during development and abiotic stress treatments in tomato Mol Genet Genomics 284 455-475
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Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) CitAP210 activation of the terpene synthase CsTPS1 isassociated with the synthesis of (+)-valencene in Newhall orange J Exp Bot 67 4105-4115
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Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes Dev Genes Evol 214 105-114Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151
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Spitzer-Rimon B Farhi M Albo B Cnaani A Ben Zvi MM Masci T Edelbaum O Yu YX Shklarman E Ovadis M Vainstein A (2012) TheR2R3-MYB-like regulatory factor EOBI acting downstream of EOBII regulates scent production by activating ODO1 and structuralscent-related genes in petunia Plant Cell 24 5089-5105
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Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp Bot 68 4407-4409Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla JF Amaya I Giavalisco P Fernie AR Botella MAValpuesta V (2015) Central role of FaGAMYB in the transition of the strawberry receptacle from development to ripening New Phytol208 482-496
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Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 regulates fragrance biosynthesis in petunia flowers PlantCell 17 1612-1624
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Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS (2018) The potassium channel FaTPK1 plays a critical role infruit quality formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748
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Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) Isolation cloning and expression of a multifunctional O- wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma compounds in strawberry fruitsPlant J 31 755-765
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Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor types their evolutionary origin and speciesdistribution In A handbook of transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular Biochemistry 52 25-73
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Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of odor (Buettner A Ed) Springer Cham 9-10Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS (2014) Isolation classification and transcription profiles ofthe AP2ERF transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271
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Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in regulation of fruit quality Crit Rev Plant Sci 35 120-130
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Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ Zhang SL Wu J (2017) Map-based cloning of the pear geneMYB114 identifies an interaction with other transcription factors to coordinately regulate fruit anthocyanin biosynthesis Plant J 92437-451
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes involved in regulating fruit ripening Plant Physiol 1531280-1292
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Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) Expression of ethylene response genes during persimmonfruit astringency removal Planta 235 895-906
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Zabetakis I Gramshaw JW Robinson DS (1999) 25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis andbiosynthesis-a review Food Chem 65 139-151
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Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci Food Agric 74 421-434Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 an AP2ERF gene is a novel regulator of fruit lignificationinduced by chilling injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1325-1334
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Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation classification and transcription profiles of the Ethylene ResponseFactors (ERFs) in ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215
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Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML (2012) Genome-wide analysis of the AP2ERF superfamily inpeach (Prunus persica) Genet Mol Res 11 4788-4809
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Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and expression analysis of a CRTDRE-binding factor gene FaCBF1from Fragaria times ananassa Acta Hortic 41 240-248
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Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The Arabidopsis AP2ERF transcription factor RAP26 participatesin ABA salt and osmotic stress responses Gene 457 1-12
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Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Genome-wide analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic (Amsterdam) 123 73-81Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF Valpuesta V Botella MA Granell A Amaya I (2012) Geneticanalysis of strawberry fruit aroma and identification of O-methyltransferase FaOMT as the locus controlling natural variation inmesifurane content Plant Physiol 159 851-870
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
2
Article title 28
29
An ETHYLENE RESPONSE FACTOR-MYB Transcription Complex Regulates 30
Furaneol Biosynthesis by Activating QUINONE OXIDOREDUCTASE Expression 31
in Strawberry 32
33
34
Yuanyuan Zhang1 Xueren Yin123 Yuwei Xiao1 Zuying Zhang1 Shaojia Li1 35
Xiaofen Liu1 Bo Zhang123 Xiaofang Yang4 Donald Grierson15 Guihua Jiang4 36
Harry J Klee16 Kunsong Chen123 37
1 College of Agriculture amp Biotechnology Zhejiang University Zijingang Campus 38
Hangzhou 310058 PR China 39
2 Zhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology 40
Zhejiang University Zijingang Campus Hangzhou 310058 PR China 41
3 The State Agriculture Ministry Laboratory of Horticultural Plant Growth 42
Development and Quality Improvement Zhejiang University Zijingang Campus 43
Hangzhou 310058 PR China 44
4 Institute of Horticulture Zhejiang Academy of Agricultural Sciences Hangzhou 45
310021 Zhejiang China 46
5 Division of Plant and Crop Sciences School of Biosciences University of 47
Nottingham Sutton Bonington Campus Loughborough LE12 5RD UK 48
6 Horticultural Sciences Plant Innovation Center Genetics Institute University of 49
Florida Gainesville FL 32611 50
These authors contributed equally to this manuscript 51
52
One-sentence summary 53
Fragaria times ananassa quinone oxidoreductase which catalyses the final step in 54
furaneol biosynthesis in strawberry is transcriptionally upregulated by a complex 55
consisting of an ethylene response factor and MYB during ripening 56
57
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
3
Footnotes 58
List of author contributions 59
KC HK and GJ conceived the original screening and research plans XrY and 60
YZ designed the experiments YZ YX and ZZ performed the experiments XrY 61
SL XL and XfY provided technical assistance to YZ XrY BZ and KC 62
supervised the experiments YZ and XrY analysed the data YZ and XrY wrote 63
the article with contributions from all the authors DG discussed results and 64
interpretation and supervised the writing and editing of the manuscript 65
66
Funding information 67
This research was supported by the National Key Research and Development 68
Program (2016YFD0400101) the Project of the Science and Technology Department 69
of Zhejiang Province (2016C04001) and the 111 Project (B17039) 70
71
Corresponding author email 72
The authors responsible for distribution of materials integral to the findings presented 73
in this article in accordance with the policy described in the Instructions for Authors 74
(wwwplantphysiolorg) are Kunsong Chen (akunzjueducn) Harry J Klee 75
(hjkleeufledu) and Guihua Jiang (jgh2004267sinacom) 76
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
4
Abstract 77
4-Hydroxy-25-dimethyl-3(2H)-furanone (HDMF) is a major contributor to the aroma 78
of strawberry (Fragaria times ananassa) fruit and the last step in its biosynthesis is 79
catalysed by Fragaria times ananassa quinone oxidoreductase (FaQR) Here an ethylene 80
response factor (FaERF9) was characterized as a positive regulator of the FaQR 81
promoter Linear regression analysis indicated that FaERF9 transcript levels were 82
significantly correlated with both FaQR transcripts and furanone content in different 83
strawberry cultivars Transient overexpression of FaERF9 in strawberry fruit 84
significantly increased FaQR expression and furaneol production Yeast one-hybrid 85
assays however indicated that FaERF9 by itself did not bind to the FaQR promoter 86
An MYB transcription factor (FaMYB98) identified in yeast one-hybrid screening of 87
the strawberry cDNA library was capable of both binding to the promoter and 88
activating the transcription of FaQR by ~56-fold Yeast two-hybrid assay and 89
bimolecular fluorescence complementation confirmed a direct protein-protein 90
interaction between FaERF9 and FaMYB98 and in combination they activated the 91
FaQR promoter 14-fold in transactivation assays These results indicate that an 92
ERF-MYB complex containing FaERF9 and FaMYB98 activates the FaQR 93
promoter and upregulates HDMF biosynthesis in strawberry 94
95
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5
Introduction 96
Strawberry (Fragaria times ananassa) is an economically important globally popular 97
and attractive fruit with nutritional benefits for human health An important feature of 98
its appeal is a unique fragrance with more than 360 different volatile compounds 99
detected in ripe fruit (Meacutenager 2004 Jetti et al 2007) These volatiles include 100
alcohols organic acids aldehydes terpenes lactones esters aromatic hydrocarbons 101
furans and others (Zabetakis and Holden 1997) Sensory evaluation indicates that 102
terpenes confer on strawberry a ldquofresh orangerdquo smell aldehydes generate a ldquoherbal 103
flavourrdquo γ -decalactone is ldquopeach-likerdquo esters are ldquofruityrdquo and 104
4-hydroxy-25-dimethyl-3(2)H-furanone (HDMF) and 105
25-dimethyl-4-methoxy-3(2)H-furanone (DMMF) generate a ldquocaramel-likerdquo aroma 106
(Pyysalo et al 1979 Larsen and Poll 1992) HDMF and DMMF belong to an 107
uncommon group of chemicals with a 25-dimethyl-3(2H)-furanone structure and 108
such compounds possess special odour properties (Schwab and Roscher 1997) They 109
are found at trace levels in various fruits including raspberry some grape cultivars 110
and tomato They are particularly abundant in strawberry and pineapple (Schwab 111
2013 Wuumlst 2017) HDMF is one of the most important volatiles distinguishing 112
strawberry from other fruits (Larsen and Poll 1992 Schwab and Roscher 1997) and 113
is significantly correlated with perceived strawberry fruit intensity (Schwieterman et 114
al 2014) Thus strawberry is an important model for investigating the regulation of 115
furaneol biosynthesis and knowledge of the factors controlling its synthesis is highly 116
desirable for targeting flavor improvement 117
118
HDMF and its methyl ether DMMF have been extensively investigated in research 119
on flavour analyses chemical synthesis and natural product formation in both 120
microbes and plants (Zabetakis et al 1999 Schwab 2013) The first plant studies on 121
the biosynthesis of HDMF used strawberry fruit to investigate potential precursors of 122
furaneol biosynthesis (Pisarnitskii et al 1992) and D-fructose-16-diphosphate was 123
identified as the natural precursor of HDMF and DMMF (Roscher et al 1998 124
Schwab 1998) The immediate precursor of HDMF in strawberry was shown to be 125
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6
4-hydroxy-5-methyl-2-methylene-3(2H)-furanone (HMMF) and Fragaria times 126
ananassa quinone oxidoreductase (FaQR later renamed as FaEO) was identified as 127
the enzyme responsible for reduction of the α β-unsaturated bond of HMMF to form 128
the aroma-active compound HDMF (Raab et al 2006 Klein et al 2007) An 129
O-methyltransferase FaOMT subsequently generates DMMF by methylation of 130
HDMF (Wein et al 2002) HDMF can also be metabolized to 131
25-dimethyl-4-hydroxy-2H-furan-3-one glucoside (HDMF-glucoside) by a 132
UDP-dependent glycosyltransferase (UGT71K3) and further malonylated into 133
25-dimethyl-4-hydroxy-2H-furan-3-one 6rsquo-O-malonyl-β-D-glucopyranoside (HDMF 134
malonyl-glucoside) in strawberry fruit (Roscher et al 1996 Song et al 2016) The 135
biosynthetic pathway of HDMF in other plants is similar to that in strawberry Genes 136
with homology to FaQR have been identified in tomato (SlEO) and mango (MIEO) 137
(Klein et al 2007 Kulkarni et al 2013) 138
139
As an NADH-dependent enone oxidoreductase protein FaQR exhibits o-quinone 140
oxidoreductase activity (Raab et al 2006) FaQR mRNA accumulates in fruit 141
parenchyma tissues but is absent in vascular tissues and FaQR is mainly expressed in 142
the late stages of fruit growth and ripening paralleling furaneol production in the fruit 143
(Raab et al 2006) FaQR is responsive to environmental stimuli associated with 144
furaneol production and in the dark lsquoSweet Charliersquo strawberry fruits have higher 145
levels of FaQR expression and HDMF production at 25degC than at 15degC (Fu et al 146
2017) in contrast the concentration of furanones and the abundance of FaQR protein 147
under low-temperature storage is significantly lower than those under 148
room-temperature storage (Li et al 2015) Thus the regulation of FaQR is important 149
for manipulating furaneol content Although it is assumed that transcription factors 150
control expressions of genes involved in volatile production in plants no such factors 151
regulating FaQR or other furanone biosynthetic genes have been identified 152
153
Different members of the largely plant-specific AP2ERF gene family (Weirauch and 154
Hughes 2011) have diverse functions in plant growth development and stress 155
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
7
responses (Agarwal et al 2010 Zhu et al 2010 Licausi et al 2013) In recent years 156
several AP2ERF genes have been reported to regulate aspects of fruit quality (Xie et 157
al 2016) including fruit aroma For example CitAP210 is associated with the 158
synthesis of (+)-valencene in Newhall orange acting via regulation of CsTPS1 (Shen 159
et al 2016) CitERF71 was shown to physically bind to the CsTPS16 promoter and 160
contribute to the synthesis of E-geraniol in citrus fruit (Li et al 2017) These 161
observations raised the possibility that FaQR might also be a target for a member of 162
the AP2ERF family and that ERFs might also control furaneol biosynthesis 163
164
In this study screening of the Fragaria times ananassa AP2ERF gene family led to 165
identification of FaERF9 as an activator of FaQR however it did not bind directly 166
to the promoter A parallel search for proteins that directly bind the FaQR promoter 167
using yeast one-hybrid screening identified a second factor FaMYB98 which was 168
capable of physically interacting with the FaQR promoter FaMYB98 physically 169
interacts with FaERF9 and transient expression assays demonstrated a synergistic 170
effect on FaQR expression and furanone synthesis 171
172
Results 173
Changes in the content of both furanones and the activity of their biosynthetic 174
genes in strawberry fruit 175
lsquoYuexinrsquo fruits at four developmental and ripening stages (G green T turning IR 176
intermediate red R full red) were harvested (Figure 1) and determination of HDMF 177
levels indicated a major increase from about 065 μg per gram fruit at the IR stage to 178
346 μg at the R stage in the apical section implying that furaneol accumulation was 179
closely related to colour change and ripening (Figure 1) Furaneol levels were higher 180
in the apical section than in the basal section HDMF could not be detected at the IR 181
stage in the basal section but the amount increased at the R stage to 142 μg per gram 182
fruit Differences were also found for DMMF with the relative content in the apical 183
section 018 μg per gram at the R stage compared to 008 μg per gram in the basal 184
section at the same stage 185
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
8
186
Measurement of mRNA levels by RT-qPCR indicated that the transcript levels of both 187
FaQR (GenBank AY1588361) and FaOMT (GenBank AF2204912) increased 188
throughout ripening (Figure 1) Comparison of the expression of these genes showed 189
that the transcript levels of FaQR and FaOMT significantly increased as early as in T 190
stage in basal fruit sections and for each gene over half of the peak transcript 191
abundance occurred as early as in IR stage in the apical section while for the basal 192
section it was in the R stage indicating a gradient of gene expression and volatile 193
production from apex to base of the fruit during ripening 194
195
Genome-wide identification of AP2ERF gene family in strawberry 196
Coding sequences of 120 non-redundant FaAP2ERF genes were isolated and 197
identified from lsquoYuexinrsquo strawberry and a systematic nomenclature for the AP2ERF 198
family genes was used to distinguish the members based on the structural features 199
defined previously (Supplemental Table S1) (Shigyo and Ito 2004 Nakano et al 200
2006 Licausi et al 2013) CD-search analysis showed that this superfamily is 201
consisted of 95 ERFs 18 AP2 and 6 RAV family members and 1 soloist member 202
(Supplemental Table S2) Phylogenetic analysis of the Fragaria times ananassa and 203
Arabidopsis AP2ERF members is shown in Supplemental Figure S1 with the 120 204
AP2ERF genes divided into three major groups (ERF AP2 RAV) and a soloist and 205
the ERF family being further divided into 10 groups (groups I to X in Supplemental 206
Table S1) 207
208
We performed a dual-luciferase assay to determine the ability of 116 FaAP2ERF 209
members to activate transcription from the promoter of FaQR The results indicated 210
about 12 members (mainly belonging to the ERF and RAV families) showed a 211
significant activation effect on the FaQR promoter while the remaining members 212
showed very limited effects (Figure 2) The relative activity of only the following 12 213
FaAP2ERF transcripts reached the threshold value set at 2 FaERF8FaERF9 214
(group II) FaERF27FaERF29FaERF31FaERF32 (group IV) 215
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
9
FaERF37FaERF38 (group V) FaERF62FaERF64 (group VIII) FaERF68 216
(group IX) and FaRAV4 (Figure 2) Of these FaERF9 exhibited the highest 217
activation effect on the FaQR promoter (466-fold) (Figure 2) The strawberry 218
FaERF9 cDNA is 699 bp long and ExPASy Compute pIMw tool analysis indicated 219
that this gene encodes a 232-amino acid protein with a calculated molecular mass of 220
254 KD and a pI of 56 221
222
FaERF9 expression pattern and subcellular localization 223
To further explore the connections between AP2ERFs and furaneol biosynthesis we 224
obtained the transcript profiles of the AP2ERF genes in strawberry fruit samples at 225
different fruit developmental and ripening stages by reverse transcription quantitative 226
PCR (RT-qPCR) excluding genes with very low abundance in the fruit samples The 227
results presented as a heatmap (Supplemental Figure S2) demonstrate that these 228
genes displayed various expression patterns in both the apical and basal sections and 229
by analysing the expression patterns of the members indicated as activators in the 230
dual-luciferase assay we found that only a few genes including FaERF8 FaERF9 231
FaERF27 FaERF32 and FaERF37 were up-regulated during ripening stages and 232
their expression correlated with furaneol accumulation in the fruit (Figure 1) 233
Furthermore the expression patterns of the up-regulated genes in the apical and basal 234
sections showed that one ERF gene FaERF9 not only showed an up-regulation 235
pattern in both sections but its expression in the apical section occurred ahead of that 236
in the basal section (Figure 3) consistent with the actual changes in furaneol content 237
(Figure 1) and the expression pattern of FaQR (Figure 1) The subcellular localization 238
of FaERF9 was predicted to be in the nucleus using the WoLF PSORT program In 239
experimental tests 35S-FaERF9-GFP (green fluorescence protein) showed strong 240
fluorescence in the nucleus and the green signal merged with the red fluorescence 241
signal of mCherry-nucleus-marker in tobacco plants (Figure 3) 242
243
Transient overexpression of FaERF9 in strawberry 244
The expression of FaERF9 in agro-infiltrated fruits was analysed by performing 245
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
10
RT-qPCR on the seventh day after infiltration by which time they had reached the IR 246
or R stage and the result showed that the transcript levels were significantly higher 247
(52-fold) than in control fruits (Figure 4) The expression of FaQR was examined in 248
the same fruits and the transcript abundance also increased 22-fold The relative 249
content of HDMF in the FaERF9-overexpressing fruits was 008 μg per gram fruit 250
and undetectable in the control fruits (Figure 4) The relative content of DMMF in the 251
overexpressing fruits was also significantly increased to 038 μg per gram fruit 252
compared to 004 μg per gram fruit in the control (Figure 4) These observations 253
provide direct evidence for a regulatory role for FaERF9 in promoting FaQR 254
biosynthesis and activity in ripening strawberry fruit Taken together these results 255
indicate that by activating the transcription of FaQR FaERF9 functions as a positive 256
regulator in furaneol biosynthesis 257
258
Correlation of FaERF9 expression and FaQR transcript profiles 259
GC-MS quantification showed that furanones are distributed in variable levels among 260
different strawberry cultivars (Supplemental Figure S3) The transcript profiles of 261
FaQR and FaERF9 in fruits of different cultivars were measured and linear 262
regression analysis was performed In the cultivars the changes in FaQR transcripts 263
correlated positively with those in FaERF9 transcripts (r = 079 plt001) (Figure 5) 264
In addition FaERF9 transcript levels also correlated with furanone content across 265
cultivars (Figure 5) 266
267
FaERF9 is an indirect regulator of the FaQR promoter and acts via 268
protein-protein interaction with FaMYB98 269
Although the results of the dual-luciferase assay expression analysis transient 270
overexpression and correlation analysis were all consistent with the suggestion that 271
FaERF9 regulates transcript abundance by acting on the FaQR promoter a yeast 272
one-hybrid assay indicated that FaERF9 cannot bind directly to the FaQR promoter 273
(Figure 6) This led us to speculate that activation may occur via a transcription 274
complex involving an additional as-yet unknown regulator which can bind directly to 275
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
11
the FaQR promoter 276
277
In parallel with the investigation of the FaAP2ERF genes a cDNA library screening 278
was performed with a yeast one-hybrid assay using the promoter of FaQR as the bait 279
This screen identified several transcription factors that could physically bind to the 280
FaQR promoter but only one MYB could activate transcription from the FaQR 281
promoter (approximately 56-fold) relative to the control (Figure 6) in the 282
dual-luciferase assay This MYB showed 44 amino acid identity with MYB98 283
(GenBank ABA420611) a transcriptional regulator in the synergid cells in 284
Arabidopsis (Kasahara et al 2005) and it was designated as FaMYB98 The 285
specificity of FaMYB98 binding to the FaQR promoter was confirmed by EMSA 286
assay (Figure 7) and increasing the concentration of the cold probe reduced binding 287
In addition mutating the putative binding sites (Goacutemez-Maldonado et al 2004 288
Punwani et al 2007) as shown in Figure 7 eliminated FaMYB98 protein binding 289
When the combined effect of FaERF9 and FaMYB98 was analysed (Figure 8) a 290
synergistic 14-fold activation of the FaQR promoter was observed compared with the 291
activation by either FaERF9 or FaMYB98 which alone promoted transactivation 292
39-fold and 45-fold respectively In addition overexpression of both genes 293
(FaERF9-FaMYB98-SK) in strawberry fruits resulted in higher expression of 294
FaERF9 transcripts and higher furanone content than overexpression of FaERF9 295
(Supplemental Figure S4 Supplemental Table S3) Subcellular localization analysis 296
revealed that FaMYB98 was also localized in the nucleus (Supplemental Figure S5) 297
298
To investigate the potential interactions between FaERF9 and FaMYB98 the 299
DUALhunter system was used (Figure 9) Cells expressing the FaMYB98 and 300
FaERF9 protein pair using either FaMYB98 or FaERF9 as the bait grew on DDO 301
QDO and QDO supplemented with 1 mM 3-AT selective medium indicating 302
interaction between the two proteins This putative protein-protein interaction was 303
confirmed by BiFC assay and the combinations of FaMYB98-YFPNFaERF9-YFPC 304
and FaERF9-YFPNFaMYB98-YFPC exhibited strong coincident signals in the 305
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
12
nucleus while negative controls produced no detectable fluorescence signal (Figure 306
10) In addition coexpression of FaERF9-YFPNFaERF9-YFPC as well as 307
FaMYB98-YFPNFaMYB98-YFPC also generated signals in the nucleus indicating 308
that FaERF9 and FaMYB98 both could form homodimers or possibly multimers in 309
the nucleus (Figure 10) 310
311
Discussion 312
The AP2ERF superfamily in strawberry 313
The AP2ERF superfamily of plant transcription factors is defined by the AP2ERF 314
domain and comprises the ERF AP2 and RAV families as well as one soloist member 315
(Riechmann et al 2000 Weirauch and Hughes 2011) The completion of multiple 316
plant genome sequences has enabled a genome-scale analysis of the AP2ERF family 317
which in recent years has been systematically studied in diverse fruit species such as 318
tomato grape peach and kiwi fruit (Zhuang et al 2009 Sharma et al 2010 Licausi 319
et al 2010 Yin et al 2010 Pirrello et al 2012 Zhang et al 2012 Zhang et al 320
2016) A few AP2ERF genes have been isolated and characterized in strawberry and 321
CBF orthologs (Owens et al 2002 Koehler et al 2012 Zhang et al 2014) have 322
been identified from different strawberry cultivars in several independent studies 323
Although they have distinct names eg Fragaria times ananassa CBF1 (FaCBF1) 324
FaCBF4 (GenBank HQ9105151) and CBF1 (GenBank EU1172142) according to 325
the phylogenetic tree generated in this study the orthologs of 326
CBF1CBF4CBF2CBF3 in Arabidopsis are similar to each other and to FaERF20 327
(Supplemental Figure S1) (Owens et al 2002 Koehler et al 2012 Zhang et al 328
2014) FaERF20 has 85 sequence similarity with FaCBF1 identified by Owens et 329
al (2002) 93 similarity with FaCBF4 amplified by Koehler et al (2012) and 75 330
similarity with CBF1 cloned by Zhang et al (2014) The AP2ERF genes 331
characterized in other studies (Jia et al 2011 GAO et al 2015 Chai and Shen 2016 332
Mu et al 2016) are also noted in Supplemental Table S1 333
334
Based on the computational analysis we have identified a total of 120 AP2ERF 335
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13
genes in octoploid strawberry (Supplemental Table S1) The number of predicted 336
AP2ERF genes (120) is comparable to those observed in other fruits including 337
tomato (112) Chinese plum (116) citrus (126) and peach (131) but lower than those 338
reported for grape (149) (Xie et al 2016) As shown in Supplemental Table S2 79 339
(95 genes) of the AP2ERF genes belong to the ERF family in strawberry constituting 340
the largest sub-family The members of this sub-family can be classified into 10 341
groups (group I to X) according to their sequence similarities to the Arabidopsis ERF 342
genes (Nakano et al 2006) The AP2 family encompasses the same number of genes 343
in Arabidopsis citrus and strawberry (eighteen) (Nakano et al 2006 Xie et al 2014) 344
and there are six RAV genes in strawberry which are highly conserved in dicots such 345
as Vitis vinifera Arabidopsis thaliana and Populus trichocarpa (Licausi et al 2010) 346
347
Role of FaERF9 in regulating the biosynthesis of HDMF a positive regulator 348
acting in an indirect manner 349
The large-scale screening of the AP2ERF superfamily in strawberry led to 350
identification of 11 ERFs and 1 RAV that trans-activated the FaQR promoter more 351
than two-fold with the highest activation caused by FaERF9 which trans-activated 352
the FaQR promoter (Figure 2) as well as up-regulating FaQR expression and furanone 353
production in transient overexpression assays (Figure 4) which has been extensively 354
used to explore the fruit-associated gene functions in strawberry (Han et al 2015 355
Medina-Puche et al 2015 Vallarino et al 2015 Carvalho et al 2016 Song et al 356
2016 Wang et al 2018) FaERF9 transcripts accumulate in the fruit apical section 357
before the basal section (Figure 3) a finding consistent with the actual changes in 358
furaneol content (Figure 1) and the expression of FaQR (Figure 1) The association 359
between FaERF9 transcripts and accumulation of furanones were also established 360
with different strawberry cultivars The correlation between FaERF9 and FaQR 361
expression as well as furanone content among cultivars supports a positive role of 362
FaERF9 in regulating furanone content (Figure 5) These results indicate that 363
FaERF9 transcript abundance may be a good indicator of the abundance of these 364
important flavour volatiles in fruits of different cultivars This should be considered as 365
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14
a method for high-throughput variety screening to replace direct measurement of 366
volatiles 367
368
FaERF9 is a member of the ERF group II family and is most closely related to the 369
Arabidopsis genes At1g44830 (ATERF014) At1g21910 (DREB26) and At1g77640 370
(Supplemental Figure S1) At1g44830 was observed to be strongly up-regulated in a 371
comprehensive microarray analysis of the root transcriptome following NaCl 372
exposure (Jiang and Deyholos 2006) At1g21910 (DREB26) was functionally 373
characterized as a trans-activator localized in the nucleus exhibiting tissue-specific 374
expression and participating in plant developmental processes as well as biotic andor 375
abiotic stress signalling (Krishnaswamy et al 2011) However none of these genes 376
have been reported as furanone regulators In strawberry another five genes 377
(FaERF6 FaERF7 FaERF8 FaERF10 and FaERF11) also belong to the same 378
group with FaERF8 also showing somewhat weaker activation activity towards the 379
FaQR promoter than FaERF9 The fact that FaERF9 could not bind directly to the 380
promoter of FaQR (Figure 6) indicates that it might function as an indirect regulator 381
of FaQR and furaneol biosynthesis 382
383
A FaERF9 and FaMYB98 complex is involved in regulating FaQR and furaneol 384
biosynthesis 385
The finding that FaERF9 could interact with FaMYB98 protein (Figures 9 and 386
Figure 10) and that FaMYB98 could physically bind to the FaQR promoter (Figure 6 387
and Figure 7) provides evidence for a regulatory mechanism whereby FaERF9 388
regulates FaQR and furaneol production as part of a complex with an MYB 389
transcription factor Since co-overexpression of FaERF9 and FaMYB98 resulted in 390
much higher activation activity towards FaQR we speculate that FaERF9 may 391
recruit FaMYB98 homologs in tobacco to activate the FaQR promoter (Figure 8) 392
FaOMT is another key gene for furanone biosynthesis and a potential target for 393
transcriptional activation However FaERF9 did not significantly activate the 394
FaOMT promoter in a dual-luciferase assay and the transcript level of FaOMT in the 395
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15
FaERF9-overexpressing fruits showed no significant difference from that in the 396
control (Supplemental Figure S6 Supplemental Figure S7) The FaOMT promoter 397
was significantly induced by FaMYB98 but no synergistic effect of FaERF9 and 398
FaMYB98 on the promoter was observed (Supplemental Figure S6) In previous 399
studies of the regulation of plant volatile compounds MYBs have been characterized 400
as being involved mainly in the regulation of the benzenoidphenylpropanoid pathway 401
that produces floral volatiles in petunia and eugenol in ripe strawberry fruit (Verdonk 402
et al 2005 Dal Cin et al 2011 Colquhoun et al 2011 Spitzer-Rimon et al 2012 403
Medina-Puche et al 2015) but their role in formation of volatiles from other 404
pathways has not been reported Our study demonstrates a role for MYB in the 405
synthesis of furaneol a carbohydrate-derived volatile compound and reveals the 406
synergistic interactions between an MYB and ERF in a transcription complex (Figure 407
8 Figure 9 and Figure 10) 408
409
Recent research has provided evidence for interactions between AP2ERF and MYB 410
transcription factors in regulating other aspects of fruit quality including texture 411
(EjAP2-1 and EjMYB Zeng et al 2015) and colour (PyERF3 and PyMYB114 Yao 412
et al 2017) A group VIII ERF has also recently been shown to interact with an MYB 413
to regulate floral scent production in petunia (Liu et al 2017) In strawberry fruit 414
DOF in combination with an MYB has been reported to be involved in the regulation 415
of eugenol production and the identification of this second transcription factor (DOF) 416
suggests that it is a good target in breeding for improved flavour (Molina-Hidalgo et 417
al 2017 Tieman 2017) Considering its important contribution to flavour in 418
strawberry and many other highly valued fruit crop species (pineapple tomato mango 419
etc) very little is known about regulation of furaneol synthesis Here we established 420
the role of FaERF9 in the regulation of HDMF synthesis by direct protein-protein 421
interactions with FaMYB98 to synergistically trans-activate FaQR The functional 422
identification of this complex enhances our knowledge of the regulation of volatile 423
compound synthesis and identifies a new AP2ERF-MYB complex Further 424
examination of the other ERFs that stimulated transcription from the FaQR promoter 425
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16
(Figure 2) may provide additional information about the complexity of this regulation 426
Overall this study provides important clues for understanding the transcriptional 427
regulation of HDMF synthesis and identifies specific transcription factors that are 428
likely to be good targets for molecular breeding for improved flavour 429
430
Conclusions 431
Screening of the AP2ERF superfamily in strawberry (Fragaria times ananassa) 432
identified candidate members capable of activating the FaQR promoter An ERF 433
transcription factor was identified as a positive regulator of HDMF synthesis in 434
strawberry fruit and the mechanism of activation was shown to involve an ERF-MYB 435
transcription complex that regulates transcription of FaQR leading to the biosynthesis 436
of HDMF the characteristic volatile compound which has a major influence on 437
strawberry aroma 438
439
Materials and Methods 440
441
Plant Materials and Growth conditions 442
The strawberry (Fragaria times ananassa cv lsquoYuexinrsquo an octoploid cultivar) fruit used in 443
this study were bred by Zhejiang Academy of Agricultural Sciences (Haining 444
Zhejiang) Fruits at various developmental and ripening stages including G (green) T 445
(turning) IR (intermediate red) and R (full red) were harvested (Figure 1) and 446
transported to the laboratory within 2 h Thirty-six fruits of uniform size and free of 447
visible defects were selected at each stage with twelve fruits in each biological 448
replicate After removing the calyces fruits were then divided into the basal and 449
apical sections which were sampled separately (Figure 1) They were rapidly cut into 450
pieces frozen immediately in liquid nitrogen and stored at -80deg C until use Red ripe 451
fruits of different strawberry cultivars (Fragaria times ananassa octoploid cultivars) 452
including lsquoYuelirsquo lsquoBenihoppersquo lsquoMengxiangrsquo lsquoAmaoursquo lsquo10-1-4rsquo lsquoAkihimersquo lsquoSweet 453
Charliersquo lsquo07-1-4rsquo lsquoDarselectrsquo lsquoYuexinrsquo and lsquoXuemeirsquo were also provided by Zhejiang 454
Academy of Agricultural Sciences For each cultivar the fruits of three biological 455
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17
replicates were sampled frozen in liquid nitrogen and stored at -80deg C for further use 456
457
Tobacco plants (Nicotiana benthamiana) used for dual-luciferase assays and 458
subcellular localization analysis in this study were grown in a growth chamber with a 459
lightdark cycle of 16 h8 h at 24degC 460
461
Detection of DMMF and HDMF 462
Automated HS-SPME-GC-MS was performed to detect both furanones in lsquoYuexinrsquo 463
strawberry fruit (Zorrilla-Fontanesi et al 2012) Samples were ground into a powder 464
under liquid nitrogen for analysis 465
466
For the detection of DMMF (Figure 1) 05 g (fresh weight) of each sample was 467
weighed in the vial to which was added 1 mL of EDTA solution (100 mM pH 75) 1 468
mL of CaCl2 solution (mv = 20) and 20 microL of 2-octanol as the internal standard 469
(007 μgμL) The mixture was homogenized and the vial closed and placed on the 470
sample tray for analysis by CombiPAL autosampler (CTC Analytic CA USA) The 471
fruit volatiles were sampled by headspace solid-phase microextraction with a 65-μm 472
polydimethylsiloxane-divinylbenzene fibre (PDMS-DVB) Initially vials were 473
pre-incubated at 50degC for 10 min under continuous agitation (500 rpm) then volatiles 474
were extracted for 30 min at the same temperature and agitation speed After that the 475
fibre was desorbed in the GC injection port for 5 min in splitless mode The 7890A 476
GC chromatograph was equipped with a DB-5ms column (60 m times 250 μm times 1 μm 477
JampW Scientific Folsom CA USA) with helium as the carrier gas at a constant flow 478
of 12 mLmin The GC was programmed at an initial temperature of 35degC for 2 min 479
with a ramp of 5degC min up to 250degC and held for 5 min The injection port interface 480
and MS source temperatures were 250degC 260degC and 230degC respectively The 481
ionization potential was set at 70 eV recorded by a 5975B mass spectrometer (Agilent 482
Technologies JampW Scientific Folsom CA USA) and the scanning speed was 7 483
scanss The same method was used to analyse HDMF and DMMF in fruits from 484
different cultivars (Supplemental Figure S3) except for the sample preparation 485
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18
procedure (Araguumlez et al 2013) briefly 05 g (fresh weight) of powdered fruit was 486
incubated at 30degC in a water bath for 5 min then 2 mL of NaCl (mv = 20) and 20 487
microL of 2-octanol as the internal standard (007 μgμL) were added and homogenized 488
489
For the detection of HDMF (Figure 1) and both furanones (Figure 4 and Supplemental 490
Table S3) a liquid-injection system equipped with CTC Pal ALS was used One gram 491
(fresh weight) of powdered fruit and 2 mL of NaCl (mv = 20) were homogenized in 492
a 10-mL tube and 300 μL of CH2Cl2 and 20 microL of 2-octanol (0766 μgμL) as the 493
internal standard were added to extract the volatiles the mixture was then 494
homogenized again The tubes were stored at room temperature for 20 min and 495
centrifuged at 12000 rpm for 5 min The subnatant was pipetted into a clean 15-mL 496
tube in which 20 mg of anhydrous sodium sulphate was added the tube was left 497
without shaking for half an hour Then 150 μL of the solution was transferred into a 498
GC vial and placed on the sample tray as described above Each sample (1 μL) was 499
injected using the autosampler and the analysis was accomplished by a 7890A 500
GC-MS system (Agilent Technologies JampW Scientific Folsom CA USA) equipped 501
with a DB-WAX column (30 m times 025 mm times 025 μm JampW) Helium (12 mLmin) 502
was used as a carrier gas The injection port (splitless injection mode) interface and 503
MS source temperatures were as described above The oven temperature was set at 504
60degC for 4 min then increased to 180degC at a rate of 4degCmin and maintained for 30 505
min DMMF was identified by comparison of electron ionization mass spectra and 506
retention time data with the data from the NISTEPANIH mass spectral library 507
(NIST-08 and Flavor) HDMF (Figure 1) was identified and qualified by comparison 508
with injected standard (Sigma) The quantitative analysis of both furanones (Figure 4 509
Supplemental Table S3 and Supplemental Figure S3) was determined using the peak 510
area of the internal standard as a reference based on total ion chromatogram (TIC) 511
512
RNA isolation and Reverse Transcription Quantitative PCR (RT-qPCR) 513
Total RNA from strawberry samples was isolated in this study using the CTAB 514
method (Chang et al 1993) Genomic DNA contamination was eliminated by 515
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
19
TURBO Dnase (Ambion) 1 μg of RNA was used to obtain cDNA using an IScriptTM 516
cDNA Synthesis Kit (Bio-Rad) The synthesized cDNA was diluted with water (120) 517
and 2 μL of diluted cDNA was used as the template for RT-qPCR Reactions were 518
performed in a total volume of 20 μL consisting of 10 μL of SYBR PCR supermix 519
(Bio-Rad) 1 μL of each primer (10 μM) 6 μL of DEPC-H2O and 2 μL of diluted 520
cDNA on CFX96 instrument (Bio-Rad) (Yin et al 2012) The oligonucleotide 521
primers for RT-qPCR analysis of genes including the AP2ERF FaQR and FaOMT 522
were designed according to the coding sequences of genes and the specificity was 523
verified before use (Min et al 2012) NCBIPrimer-BLAST was applied to design the 524
primers Relative expression levels were normalized to that of an internal controlmdashthe 525
interspacer 26S-18S strawberry RNA housekeeping gene FaRIB413 526
(Zorrilla-Fontanesi et al 2012) To investigate the differential expression of genes 527
during fruit development and ripening stages relative expression of each gene at the 528
R stage in the basal fruit section was set as 1 using the 2minus∆∆119862119879 method For transient 529
overexpression assay relative expression of control fruits with an empty vector (SK) 530
was set as 1 The primers used in RT-qPCR are listed in Supplemental Table S4 531
532
Gene isolation and analysis 533
Multiple database searches were performed to identify members of the strawberry 534
(Fragaria times ananassa) AP2ERF superfamily in the published strawberry databases 535
and annotations of Fragaria times ananassa and Fragaria times vesca by using the 536
AP2ERF DNA binding domain as a query sequence and 120 genes were identified 537
with AP2ERF domain(s) Based on the BLAST result primers (listed in 538
Supplemental Table S5) were used to amplify the coding full-length cDNAs of 539
AP2ERF genes The deduced amino acid sequences of AP2ERF proteins in 540
Arabidopsis thaliana used for construction of a phylogenetic tree were obtained from 541
the Arabidopsis Information Resource (TAIR) Alignment of the proteins was 542
performed using the neighbour-joining method in ClustalX (v181) and the 543
phylogenetic tree was constructed using FigTree (v131) 544
545
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
20
FaMYB98 was obtained by yeast one-hybrid screening sequencing and the full-length 546
sequences were predicted by BLAST Primers were designed (listed in Supplemental 547
Table S5) to amplify the full-length coding sequence 548
549
The promoter of FaQR was cloned by Genome Walking as previously described (Yin 550
et al 2010) and conserved cis-element motifs in the promoter were manually 551
searched 552
553
Conserved domains within the FaAP2ERF proteins and FaMYB98 were analysed by 554
CD-search (httpswwwncbinlmnihgovStructurecddwrpsbcgi) and cellular 555
locations of proteins including FaERF9 and FaMYB98 were predicted with the 556
WoLF PSORT program (httpswwwgenscriptcomwolf-psorthtml) 557
558
Dual-Luciferase Assays 559
In accordance with a previous protocol (Yin et al 2010) the full-length cDNAs of 560
FaAP2ERF or FaMYB98 transcription factors were cloned into pGreen II 0029 561
62-SK vector and the promoter of FaQR was cloned into pGreen II 0800-LUC vector 562
A luciferase gene from Renillia (REN) driven by a 35S promoter in the LUC vector 563
acted as a positive control The above constructs were transiently expressed in 564
Nicotiana benthamiana leaves by Agrobacterium-mediated infiltration (strain 565
GV3101) and the activity of the TFs on the promoter was measured on the third day 566
after infiltration indicated by the ratio of enzyme activities of firefly luciferase (LUC) 567
and renilla luciferase (REN) using a Modulus Luminometer (Promega Madison WI 568
USA) To determine the activity of a specific transcription factor towards the 569
promoter we mixed the Agrobacterium culture with 1 mL of TF and 100 μL of 570
promoter and the LUCREN value of the empty vector SK on the promoter was set as 571
1 as a calibrator To test the combined effect of two transcription factors on the 572
promoter to the Agrobacterium culture mixture we added 05 mL of each TF and 100 573
μL of promoter the effect of the mixtures that contained each transcription factor (05 574
mL) and empty vector SK (05 mL) was also tested on the promoter as a control 575
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
21
576
Subcellular localization analysis 577
35S-FaERF9-GFP and 35S-FaMYB98-GFP were transiently expressed in tobacco (N 578
benthamiana) leaves by Agrobacterium infiltration (EHA105) using the same method 579
as described in the dual-luciferase assay above The transiently infected leaves were 580
imaged on the third day after infiltration using a Nikon A1-SHS confocal laser 581
scanning microscope The excitation wavelength for GFP fluorescence was 488 nm 582
and fluorescence was detected at 490ndash520 nm The primers used for GFP construction 583
are listed in Supplemental Table S6 584
585
Transient overexpression in strawberry fruit 586
Transient overexpression of FaERF9 and an overexpression binary vector (pGreen II 587
0029 62-SK-FaERF9-FaMYB98) were performed in strawberry fruit using the 588
FaERF9-SK construct described above for the dual-luciferase assays and the binary 589
vector constructed according to Liu et al 2013 The transfection of fruit was carried 590
out at the G stage (Hoffmann et al 2006) The FaERF9-SK construct and binary 591
vector were individually electroporated into Agrobacterium tumefaciens GV3101 and 592
the Agrobacterium culture suspended in infiltration buffer was infiltrated into the 593
whole fruit using a syringe As a control treatment fruits were infiltrated with 594
Agrobacterium carrying an empty vector SK under the same transfection conditions 595
Fruits were left attached to the plants and harvested on the seventh day after 596
infiltration Fruits of three biological replicates were sampled for further analysis 597
598
Yeast one-hybrid assay 599
In order to identify proteins that bind to the FaQR promoter the Matchmaker Gold 600
Yeast One-hybrid Library Screening System (Clontech USA) was used The sequence 601
of the FaQR promoter was cloned into the pAbAi vector and the construct was 602
integrated into the genome of the Y1HGold yeast strain A mixture of total RNA from 603
strawberry fruit at four stages (G T IR R) was used to construct the prey cDNA 604
library (TaKaRa) The background AbAr expression of Y1HGold FaQR-pAbAi strain 605
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
22
was tested according to the system user manual and then screening for protein-DNA 606
interactions was carried out Furthermore the full length of each transcription factor 607
was separately cloned into pGADT7 AD vector to confirm the screening results The 608
relationship between FaERF9 and FaQR promoter was also examined individually 609
Primers used in this assay are listed in Supplemental Table S6 610
611
Expression and purification of FaMYB98 recombinant protein 612
A 405-bp region spanning the DNA-binding domain of FaMYB98 was amplified 613
from FaMYB98 cDNA and cloned into a pET6timesHN vector (Clontech Palo CA USA) 614
to generate the recombinant N-terminal His-tagged protein the primers used are listed 615
in Supplemental Table S6 The resulting construct was sequenced and introduced into 616
Escherichia coli strain Rosetta 2(DE3)pLysS (Novagen) Ten millilitres of the 617
overnight culture was combined with 500 mL of an LB liquid medium (100 μgmL 618
ampicillin and 34 μgmL chloramphenicol) as described (Li et al 2017) Isopropyl 619
β-D-1-thiogalactopyranoside (IPTG) was added to a final concentration of 1 mM and 620
the bacterial culture was incubated at 18degC at 150 rpm for 18 h Then the cells were 621
harvested using a centrifuge and resuspended in 1times PBS buffer (Sangon Biotech) 622
after which they were disrupted by sonication and the supernatant was purified using 623
a HisTALONTM Gravity Column (Clontech) according to the user manual The PD-10 624
Desalting column (GE Healthcare) was then used for buffer change and sample 625
clean-up of proteins according to the gravity protocol SDS-PAGE was performed and 626
the protein was visualized using Coomassie brilliant blue 627
628
Electrophoretic mobility shift assay (EMSA) 629
A Lightshift Chemiluminescent EMSA kit (Thermo) was used to perform EMSA 630
experiments according to the manufacturerrsquos instructions Single-strand 631
oligonucleotides were synthesized and biotinylated by GeneBio Biotech (Hangzhou 632
China) The details of the EMSA assay are provided in Ge et al (2017) The probes 633
used for EMSAs are listed in Supplemental Table S6 634
635
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
23
636
Yeast two-hybrid assay 637
The DUALhunter system (Dualsystems Biotech Switzerland) was used to investigate 638
the interaction between FaERF9 and FaMYB98 Full-length coding sequences of 639
FaERF9 and FaMYB98 were respectively cloned into pDHB1 bait vector and 640
pPR3-N prey vector sequences were verified and the bait plasmid was 641
co-transformed with prey plasmid into NMY51 in the combinations below 642
FaMYB98-pDHB1pPR3-N FaMYB98-pDHB1FaERF9-pPR3-N 643
FaMYB98-pDHB1pOst1-NubI FaERF9-pDHB1pPR3-N 644
FaERF9-pDHB1FaMYB98-pPR3-N and FaERF9-pDHB1pOst1-NubI (Li et al 645
2017) Transformed cells were spread onto the following plates DDO (SD 646
medium-Trp-Leu) QDO (SD medium-Trp-Leu-His-Ade) and QDO+3-AT (QDO 647
medium supplemented with 1 mM 3-amino-124-triazole) The control plasmid 648
pOst1-NubI was used to determine whether the bait was functional the pPR3-N prey 649
vector plasmid was used to test whether the bait displayed non-specific background 650
and positive interactions were indicated by the growth of yeast on QDO and 651
QDO+3-AT plates The Primers used in the DUALhunter assay are listed in 652
Supplemental Table S6 653
654
Bimolecular fluorescence complementation (BiFC) assays 655
Full-length FaERF9 and FaMYB98 respectively were cloned into sequences 656
encoding the N- and C- fragments of YFP protein (Lv et al 2014) All constructs 657
were transiently expressed in tobacco (N benthamiana) leaves by Agrobacterium 658
infiltration (EHA105) The YFP fluorescence of transfected leaves was imaged 40 h 659
after infiltration by using a Nikon A1-SHS confocal laser scanning microscope The 660
excitation wavelength for YFP was 488 nm and fluorescence was detected at 520ndash661
540 nm Primers used are listed in Supplemental Table S6 662
663
Statistics 664
A Studentrsquos two-tailed t test ( plt005 plt001 and plt0001) was used to 665
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
24
determine significant differences between two groups in this study Microsoft Excel 666
was used to perform linear regressive analysis significant differences were 667
determined by SPSS Statistics 200 and scatter plots were prepared with Origin80 668
Least significant difference (LSD) at the 5 level was calculated using Microsoft 669
Excel Figures were prepared with Origin80 (Microcal Software Inc Northampton 670
MA USA) The online tool MetaboAnalyst 36 (httpwwwmetaboanalystca) was 671
used to analyse the transcript abundance of the AP2ERF genes 672
673
Accession numbers 674
Sequence data from this article have been deposited in GenBank under the accession 675
numbers MH332903-MH333022 for AP2ERF genes in Fragaria times ananassa and 676
MH333023 for FaMYB98 GenBank numbers for FaQR and FaOMT were 677
AY1588361 (Raab et al 2006) and AF2204912 (Wein et al 2002) 678
679
Supplemental Material 680
Supplemental Figure S1 Phylogenetic analysis of FaAP2ERF and Arabidopsis 681
AP2ERF proteins 682
Supplemental Figure S2 Analysis of FaAP2ERF gene expression patterns in 683
strawberry fruit during development and ripening 684
Supplemental Figure S3 Contents of furanones in fruit of strawberry cultivars 685
Supplemental Figure S4 Relative expression of FaERF9 in FaERF9-FaMYB98- 686
and FaERF9-overexpressing fruits 687
Supplemental Figure S5 Subcellular localization of FaMYB98 688
Supplemental Figure S6 The combined activation effects of FaERF9FaMYB98 on 689
the FaOMT promoter 690
Supplemental Figure S7 Relative expression of FaOMT in 691
FaERF9-overexpressing fruits 692
Supplemental Table S1 AP2ERF superfamily genes in Fragaria times ananassa 693
Supplemental Table S2 Classification of the AP2ERF superfamily members in 694
Fragaria times ananassa 695
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
25
Supplemental Table S3 Furanone content in FaERF9-FaMYB98- and 696
FaERF9-overexpressing fruits 697
Supplemental Table S4 Primers used for reverse transcription quantitative PCR 698
(RT-qPCR) 699
Supplemental Table S5 Primers used to amplify the full-length coding sequences of 700
AP2ERF genes and FaMYB98 in strawberry (Fragaria times ananassa) 701
Supplemental Table S6 Primers used for vector construction 702
703
Acknowledgments 704
This research was supported by the National Key Research and Development 705
Program (2016YFD0400101) the Project of the Science and Technology Department 706
of Zhejiang Province (2016C04001) and the 111 Project (B17039) 707
708
Figure legends 709
Figure 1 Changes in furanone content and furanone biosynthetic genes during 710
strawberry (Fragaria times ananassa Duch cv Yuexin) fruit development and ripening 711
A Fruits were collected at four ripening stages G (green stage) T (turning stage) IR 712
(intermediate red stage) R (full red stage) B Changes in the contents of furaneol 713
(HDMF) and mesifurane (DMMF) HDMF content was calculated using a standard 714
curve of HDMF while DMMF content was calculated with an internal standard as the 715
reference C Expression levels of FaQR and FaOMT The expression levels of each 716
gene were calculated relative to corresponding values in the basal section at the R 717
stage SEs were calculated from three replicates and LSD values represent the least 718
significant differences at p = 005 719
Figure 2 Regulatory effects of FaAP2ERF on the promoter of FaQR LUCREN 720
values of the empty vector on FaQR promoter were used as the calibrator set as 1 721
and SEs were calculated from five replicates statistical significance was determined 722
by Studentrsquos two-tailed t test ( plt0001) 723
Figure 3 Expression and the subcellular localization of FaERF9 A The expression 724
levels were calculated relative to the levels in the basal section at the R stage B 725
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
26
Subcellular localization analysis was performed in tobacco leaves The tobacco used 726
in the assay was stably transformed with a specific nucleus localized red fluorescence 727
protein construct and the red fluorescence indicates the nucleus-localized signal 728
(NLS) Scale bar = 25 microm SEs were calculated from three replicates 729
Figure 4 Transient overexpression of FaERF9 in strawberry fruit A Relative 730
expression of FaQR and FaERF9 in FaERF9-OX fruit 7 days after infiltration The 731
expression was calculated relative to the average value in control (SK) fruits B 732
HDMF and DMMF content in FaERF9-OX fruit The content of both furanones 733
were quantified using the peak area of the internal standard (2-octanol) as the 734
reference SEs were calculated from three replicates Statistical significance was 735
determined by Studentrsquos two-tailed t test ( plt005 plt001 plt0001) 736
Figure 5 Scatter plots of 11 strawberry cultivars A Linear regression analysis 737
between FaERF9 expression and FaQR expression B Linear regression analysis 738
between FaERF9 expression and furanone content The relative expression was 739
normalized to that of the housekeeping gene FaRIB413 and furanone content was 740
calculated with internal standard as the reference Significant differences were 741
determined by SPSS Statistics 200 742
Figure 6 Interactions of FaERF9 and FaMYB98 with the FaQR promoter A Yeast 743
one-hybrid analysis of the interaction of FaERF9 and FaQR promoter B Yeast 744
one-hybrid analysis of the interaction of FaMYB98 and FaQR promoter C 745
Regulatory effect of FaMYB98 on the FaQR promoter Auto-activation was tested on 746
SD-Ura (synthetically defined medium without uracil) in presence of Aureobasidin A 747
(AbA) and physical interaction was determined on SD-Leu (synthetically defined 748
medium without leucine) in presence of AbA LUCREN values of the empty vector 749
on FaQR promoter were used as the calibrator set as 1 and error bars were calculated 750
from five replicates Statistical significance was determined by Studentrsquos two-tailed t 751
test ( plt005 plt001 plt0001) 752
Figure 7 Electrophoretic mobility shift assay of FaMYB98 binding to FaQR 753
promoter A The probe sequence used for EMSA and mutated nucleotides are 754
indicated with lowercase letters B Purified DNA-binding domain of FaMYB98 755
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
27
protein and biotin-labelled DNA probe were mixed and analysed on 6 native 756
polyacrylamide gels and then photographed Presence or absence of specific probes is 757
marked by the symbol + or - 758
Figure 8 The combined activation effects of FaERF9FaMYB98 on the FaQR 759
promoter LUCREN values obtained with the empty vector and FaQR promoter were 760
used as the calibrator set as 1 and error bars were calculated from five replicates 761
Figure 9 Yeast two-hybrid analysis of the protein-protein interactions between 762
FaMYB98 and FaERF9 Positive interactions were determined by the growth of 763
yeast cells on selection plates Bait with pOST acted as positive controls and bait with 764
pPR3 as negative controls DDO synthetically defined medium without tryptophan 765
and leucine QDO synthetically defined medium without tryptophan leucine 766
histidine and adenine QDO+3AT QDO medium supplemented with 1 mM 767
3-aminotriazole 768
Figure 10 BiFC analysis of the protein-protein interactions between FaMYB98 and 769
FaERF9 The pairs of fusion proteins tested were FaMYB98-YFPN+FaERF9-YFPC 770
FaERF9-YFPN+FaMYB98-YFPC FaMYB98-YFPN+FaMYB98-YFPC and 771
FaERF9-YFPN+FaERF9-YFPC The other combinations were negative controls 772
The tobacco used in the assay was stably transformed with a specific 773
nucleus-localized red fluorescence protein construct and the red fluorescence 774
indicated the nucleus-localized signal (NLS) Fluorescence of the yellow fluorescence 775
protein (YFP) visualized the interaction in vivo Scale bar = 25 microm 776
777
Literature Cited 778
779
Agarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression 780
of PgDREB2A transcription factor enhances abiotic stress tolerance and activates 781
downstream stress-responsive genes Mol Biol Rep 37 1125-1135 782
Araguumlez I Osorio S Hoffmann T Rambla JL Medina-Escobar N Granell A 783
Botella MAacute Schwab W Valpuesta V (2013) Eugenol production in achenes and 784
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
28
receptacles of strawberry fruits is catalyzed by synthases exhibiting distinct kinetics 785
Plant Physiol 163 946-958 786
Carvalho RF Carvalho SD OrsquoGrady K Folta KM (2016) Agroinfiltration of 787
strawberry fruit mdash a powerful transient expression system for gene validation Curr 788
Plant Biol 6 19-37 789
Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic 790
(Amsterdam) 210 34-40 791
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating 792
RNA from pine trees Plant Mol Biol Rep 11 113-116 793
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC 794
Clark DG (2011) PhMYB4 fine-tunes the floral volatile signature of 795
Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143 796
Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz 797
EA Taylor MG Smits-Kroon MT Schuurink RC Haring MA Giovannoni J 798
Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic 799
pathway by ectopic expression of a MYB transcription factor in tomato fruit Plant 800
Cell 23 2738-2753 801
Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan 802
XW Yang ZY (2017) Differential responses of four biosynthetic pathways of 803
aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under 804
interaction of light and temperature Food Chem 221 356-364 805
Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of 806
differentially-expressed genes during somatic embryogenesis in Fragaria times 807
ananassa Duch lsquoBenihopprsquo J Hortic Sci Biotechnol 90 671-681 808
Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 809
transcriptionally regulates chilling-induced lignification of loquat fruit via physical 810
interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136 811
Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM 812
(2004) Functional interactions between a glutamine synthetase promoter and MYB 813
proteins Plant J 39 513-526 814
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
29
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) 815
Sucrose nonfermenting1-related protein kinase26 an ortholog of open stomata1 is 816
a negative regulator of strawberry fruit development and ripening Plant Physiol 817
167 915-930 818
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene 819
expression in strawberry fruit (Fragaria times ananassa) by agroinfiltration a rapid 820
assay for gene function analysis Plant J 48 818-826 821
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of 822
selected aroma-active compounds in strawberries by headspace solid-phase 823
microextraction gas chromatography and correlation with sensory descriptive 824
analysis J Food Sci 72 S487-S496 825
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid 826
plays an important role in the regulation of strawberry fruit ripening Plant Physiol 827
157 188-199 828
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of 829
NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes BMC 830
Plant Biol 6 20 831
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN 832
(2005) MYB98 is required for pollen tube guidance and synergid cell differentiation 833
in Arabidopsis Plant Cell 17 2981-2992 834
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional 835
characterization of enone oxidoreductases from strawberry and tomato fruit J 836
Agric Food Chem 55 6705-6711 837
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You 838
J-S Rohloff J Randall SK Alsheikh M (2012) Proteomic study of 839
low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ 840
in cold tolerance Plant Physiol 159 1787-1805 841
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional 842
characterization of four APETALA2-family genes (RAP26 RAP26L DREB19 843
and DREB26) in Arabidopsis Plant Mol Biol 75 107-127 844
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30
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon 845
J Gupta V (2013) An oxidoreductase from lsquoAlphonsorsquo mango catalyzing 846
biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494 847
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in 848
strawberries Z Lebensm-Unters Forsch 195 120-123 849
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X 850
(2015) Label-free quantitative proteomics to investigate strawberry fruit proteome 851
changes under controlled atmosphere and low temperature storage J Proteomics 852
120 44-57 853
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 854
cooperates with CitWRKY1 to participate in citric acid degradation via 855
up-regulation of CitAco3 J Exp Bot 68 3419-3426 856
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription 857
factor CitERF71 activates the terpene synthase gene CitTPS16 involved in the 858
synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938 859
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and 860
transcriptomic analysis of the AP2ERF superfamily in Vitis vinifera BMC 861
Genomics 11 719 862
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive 863
Factor (AP2ERF) transcription factors mediators of stress responses and 864
developmental programs New Phytol 199 639-649 865
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 866
interacting with EOBI negatively regulates fragrance biosynthesis in petunia 867
flowers New Phytol 215 1490-1502 868
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu 869
CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 in regulating 870
anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) 871
during anthocyanin biosynthesis Plant Cell Tissue Organ Cult 115 285-298 872
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31
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao 873
CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphate signaling and 874
homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597 875
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC 876
Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL 877
Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor 878
regulates eugenol production in ripe strawberry fruit receptacles Plant Physiol 168 879
598-614 880
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics 881
and volatile constituents of strawberry (cv Cigaline) during maturation J Agric 882
Food Chem 52 1248-1254 883
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS 884
(2012) Ethylene-responsive transcription factors interact with promoters of ADH 885
and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 886
63 6393-6405 887
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM 888
Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-Franco A 889
Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific 890
transcription factor FaDOF2 regulates the production of eugenol in ripe fruit 891
receptacles J Exp Bot 68 4529-4543 892
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) 893
Comparison and verification of the genes involved in ethylene biosynthesis and 894
signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44 895
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the 896
ERF gene family in Arabidopsis and rice Plant Physiol 140 411-432 897
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in 898
sour cherry and strawberry and the heterologous expression of CBF1 in strawberry 899
J Am Soc Hortic Sci 127 489-494 900
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech 901
JC Ohme-Takagi M Regad F Bouzayen M (2012) Functional analysis and 902
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32
binding affinity of tomato ethylene response factors provide insight on the 903
molecular bases of plant differential responses to ethylene BMC Plant Biol 12 190 904
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) 905
Methylpentoses are possible precursors of furanones in fruits Prikl Biokhim 906
Mikrobiol 28 123-127 907
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery 908
of synergid-expressed genes encoding filiform apparatus localized proteins Plant 909
Cell 19 2557-2568 910
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria 911
vesca L compared to those of cultivated berries Fragariatimes ananassa cv Senga 912
Sengana J Agric Food Chem 27 19-22 913
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W 914
Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of the strawberry 915
flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone 916
oxidoreductase Plant Cell 18 1023-1037 917
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L 918
Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim M Broun P Zhang 919
JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription 920
factors genome-wide comparative analysis among eukaryotes Science 290 921
2105-2110 922
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the 923
formation of 25-dimethyl-4-hydroxy-3(2H)-furanone in detached ripening 924
strawberry fruits J Agric Food Chem 46 1488-1493 925
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 926
25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in 927
strawberry fruits Phytochemistry 43 155-159 928
Schwab W (1998) Application of stable isotope ratio analysis explaining the 929
bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone in plants by a biological 930
maillard reaction J Agric Food Chem 46 2266ndash2269 931
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33
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) 932
Molecules 18 6936-6951 933
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard 934
products Recent Res Dev Phytochem 1 643-673 935
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL 936
Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJ Sims CA 937
Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical 938
compositions a seasonal influence and effects on sensory perception PLoS One 9 939
e88446 940
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) 941
Identification phylogeny and transcript profiling of ERF family genes during 942
development and abiotic stress treatments in tomato Mol Genet Genomics 284 943
455-475 944
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) 945
CitAP210 activation of the terpene synthase CsTPS1 is associated with the 946
synthesis of (+)-valencene in lsquoNewhallrsquo orange J Exp Bot 67 4105-4115 947
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes 948
Dev Genes Evol 214 105-114 949
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K 950
Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the 951
key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151 952
Spitzer-Rimon B Farhi M Albo B Cnarsquoani A Ben Zvi MM Masci T Edelbaum 953
O Yu YX Shklarman E Ovadis M Vainstein A (2012) The R2R3-MYB-like 954
regulatory factor EOBI acting downstream of EOBII regulates scent production 955
by activating ODO1 and structural scent-related genes in petunia Plant Cell 24 956
5089-5105 957
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp 958
Bot 68 4407-4409 959
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla 960
JF Amaya I Giavalisco P Fernie AR Botella MA Valpuesta V (2015) Central 961
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34
role of FaGAMYB in the transition of the strawberry receptacle from development 962
to ripening New Phytol 208 482-496 963
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 964
regulates fragrance biosynthesis in petunia flowers Plant Cell 17 1612-1624 965
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS 966
(2018) The potassium channel FaTPK1 plays a critical role in fruit quality 967
formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748 968
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) 969
Isolation cloning and expression of a multifunctional O-methyltransferase capable 970
of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma 971
compounds in strawberry fruits Plant J 31 755-765 972
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor 973
types their evolutionary origin and species distribution In A handbook of 974
transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular 975
Biochemistry 52 25-73 976
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of 977
odor (Buettner A Ed) Springer Cham 9-10 978
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS 979
(2014) Isolation classification and transcription profiles of the AP2ERF 980
transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271 981
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in 982
regulation of fruit quality Crit Rev Plant Sci 35 120-130 983
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ 984
Zhang SL Wu J (2017) Map-based cloning of the pear gene MYB114 identifies an 985
interaction with other transcription factors to coordinately regulate fruit 986
anthocyanin biosynthesis Plant J 92 437-451 987
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes 988
involved in regulating fruit ripening Plant Physiol 153 1280-1292 989
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
35
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) 990
Expression of ethylene response genes during persimmon fruit astringency removal 991
Planta 235 895-906 992
Zabetakis I Gramshaw JW Robinson DS (1999) 993
25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis and 994
biosynthesis-a review Food Chem 65 139-151 995
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci 996
Food Agric 74 421-434 997
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 998
an AP2ERF gene is a novel regulator of fruit lignification induced by chilling 999
injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1000
1325-1334 1001
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation 1002
classification and transcription profiles of the Ethylene Response Factors (ERFs) in 1003
ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215 1004
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML 1005
(2012) Genome-wide analysis of the AP2ERF superfamily in peach (Prunus 1006
persica) Genet Mol Res 11 4788-4809 1007
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and 1008
expression analysis of a CRTDRE-binding factor gene FaCBF1 from Fragaria times 1009
ananassa Acta Hortic 41 240-248 1010
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The 1011
Arabidopsis AP2ERF transcription factor RAP26 participates in ABA salt and 1012
osmotic stress responses Gene 457 1-12 1013
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B 1014
Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) Genome-wide 1015
analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic 1016
(Amsterdam) 123 73-81 1017
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF 1018
Valpuesta V Botella MA Granell A Amaya I (2012) Genetic analysis of 1019
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
36
strawberry fruit aroma and identification of O-methyltransferase FaOMT as the 1020
locus controlling natural variation in mesifurane content Plant Physiol 159 1021
851-870 1022
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Parsed CitationsAgarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression of PgDREB2A transcription factor enhances abioticstress tolerance and activates downstream stress-responsive genes Mol Biol Rep 37 1125-1135
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Araguumlez I Osorio S Hoffmann T Rambla JL Medina-Escobar N Granell A Botella MAacute Schwab W Valpuesta V (2013) Eugenolproduction in achenes and receptacles of strawberry fruits is catalyzed by synthases exhibiting distinct kinetics Plant Physiol 163 946-958
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Carvalho RF Carvalho SD OGrady K Folta KM (2016) Agroinfiltration of strawberry fruit - a powerful transient expression system forgene validation Curr Plant Biol 6 19-37
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic (Amsterdam) 210 34-40Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating RNA from pine trees Plant Mol Biol Rep 11 113-116Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC Clark DG (2011) PhMYB4 fine-tunes the floral volatilesignature of Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz EA Taylor MG Smits-Kroon MT Schuurink RC HaringMA Giovannoni J Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic pathway by ectopic expression of aMYB transcription factor in tomato fruit Plant Cell 23 2738-2753
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan XW Yang ZY (2017) Differential responses of fourbiosynthetic pathways of aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under interaction of light andtemperature Food Chem 221 356-364
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of differentially-expressed genes during somatic embryogenesis inFragaria times ananassa Duch Benihopp J Hortic Sci Biotechnol 90 671-681
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 transcriptionally regulates chilling-induced lignification ofloquat fruit via physical interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM (2004) Functional interactions between a glutaminesynthetase promoter and MYB proteins Plant J 39 513-526
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) Sucrose nonfermenting1-related protein kinase26 anortholog of open stomata1 is a negative regulator of strawberry fruit development and ripening Plant Physiol 167 915-930
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene expression in strawberry fruit (Fragaria times ananassa) byagroinfiltration a rapid assay for gene function analysis Plant J 48 818-826
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of selected aroma-active compounds in strawberries byheadspace solid-phase microextraction gas chromatography and correlation with sensory descriptive analysis J Food Sci 72 S487-S496
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid plays an important role in the regulation of strawberry fruitripening Plant Physiol 157 188-199
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of NaCl-stressed Arabidopsis roots reveals novel classes ofresponsive genes BMC Plant Biol 6 20
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Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS (2014) Isolation classification and transcription profiles ofthe AP2ERF transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271
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Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in regulation of fruit quality Crit Rev Plant Sci 35 120-130
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Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Genome-wide analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic (Amsterdam) 123 73-81Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
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wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
3
Footnotes 58
List of author contributions 59
KC HK and GJ conceived the original screening and research plans XrY and 60
YZ designed the experiments YZ YX and ZZ performed the experiments XrY 61
SL XL and XfY provided technical assistance to YZ XrY BZ and KC 62
supervised the experiments YZ and XrY analysed the data YZ and XrY wrote 63
the article with contributions from all the authors DG discussed results and 64
interpretation and supervised the writing and editing of the manuscript 65
66
Funding information 67
This research was supported by the National Key Research and Development 68
Program (2016YFD0400101) the Project of the Science and Technology Department 69
of Zhejiang Province (2016C04001) and the 111 Project (B17039) 70
71
Corresponding author email 72
The authors responsible for distribution of materials integral to the findings presented 73
in this article in accordance with the policy described in the Instructions for Authors 74
(wwwplantphysiolorg) are Kunsong Chen (akunzjueducn) Harry J Klee 75
(hjkleeufledu) and Guihua Jiang (jgh2004267sinacom) 76
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
4
Abstract 77
4-Hydroxy-25-dimethyl-3(2H)-furanone (HDMF) is a major contributor to the aroma 78
of strawberry (Fragaria times ananassa) fruit and the last step in its biosynthesis is 79
catalysed by Fragaria times ananassa quinone oxidoreductase (FaQR) Here an ethylene 80
response factor (FaERF9) was characterized as a positive regulator of the FaQR 81
promoter Linear regression analysis indicated that FaERF9 transcript levels were 82
significantly correlated with both FaQR transcripts and furanone content in different 83
strawberry cultivars Transient overexpression of FaERF9 in strawberry fruit 84
significantly increased FaQR expression and furaneol production Yeast one-hybrid 85
assays however indicated that FaERF9 by itself did not bind to the FaQR promoter 86
An MYB transcription factor (FaMYB98) identified in yeast one-hybrid screening of 87
the strawberry cDNA library was capable of both binding to the promoter and 88
activating the transcription of FaQR by ~56-fold Yeast two-hybrid assay and 89
bimolecular fluorescence complementation confirmed a direct protein-protein 90
interaction between FaERF9 and FaMYB98 and in combination they activated the 91
FaQR promoter 14-fold in transactivation assays These results indicate that an 92
ERF-MYB complex containing FaERF9 and FaMYB98 activates the FaQR 93
promoter and upregulates HDMF biosynthesis in strawberry 94
95
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5
Introduction 96
Strawberry (Fragaria times ananassa) is an economically important globally popular 97
and attractive fruit with nutritional benefits for human health An important feature of 98
its appeal is a unique fragrance with more than 360 different volatile compounds 99
detected in ripe fruit (Meacutenager 2004 Jetti et al 2007) These volatiles include 100
alcohols organic acids aldehydes terpenes lactones esters aromatic hydrocarbons 101
furans and others (Zabetakis and Holden 1997) Sensory evaluation indicates that 102
terpenes confer on strawberry a ldquofresh orangerdquo smell aldehydes generate a ldquoherbal 103
flavourrdquo γ -decalactone is ldquopeach-likerdquo esters are ldquofruityrdquo and 104
4-hydroxy-25-dimethyl-3(2)H-furanone (HDMF) and 105
25-dimethyl-4-methoxy-3(2)H-furanone (DMMF) generate a ldquocaramel-likerdquo aroma 106
(Pyysalo et al 1979 Larsen and Poll 1992) HDMF and DMMF belong to an 107
uncommon group of chemicals with a 25-dimethyl-3(2H)-furanone structure and 108
such compounds possess special odour properties (Schwab and Roscher 1997) They 109
are found at trace levels in various fruits including raspberry some grape cultivars 110
and tomato They are particularly abundant in strawberry and pineapple (Schwab 111
2013 Wuumlst 2017) HDMF is one of the most important volatiles distinguishing 112
strawberry from other fruits (Larsen and Poll 1992 Schwab and Roscher 1997) and 113
is significantly correlated with perceived strawberry fruit intensity (Schwieterman et 114
al 2014) Thus strawberry is an important model for investigating the regulation of 115
furaneol biosynthesis and knowledge of the factors controlling its synthesis is highly 116
desirable for targeting flavor improvement 117
118
HDMF and its methyl ether DMMF have been extensively investigated in research 119
on flavour analyses chemical synthesis and natural product formation in both 120
microbes and plants (Zabetakis et al 1999 Schwab 2013) The first plant studies on 121
the biosynthesis of HDMF used strawberry fruit to investigate potential precursors of 122
furaneol biosynthesis (Pisarnitskii et al 1992) and D-fructose-16-diphosphate was 123
identified as the natural precursor of HDMF and DMMF (Roscher et al 1998 124
Schwab 1998) The immediate precursor of HDMF in strawberry was shown to be 125
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
6
4-hydroxy-5-methyl-2-methylene-3(2H)-furanone (HMMF) and Fragaria times 126
ananassa quinone oxidoreductase (FaQR later renamed as FaEO) was identified as 127
the enzyme responsible for reduction of the α β-unsaturated bond of HMMF to form 128
the aroma-active compound HDMF (Raab et al 2006 Klein et al 2007) An 129
O-methyltransferase FaOMT subsequently generates DMMF by methylation of 130
HDMF (Wein et al 2002) HDMF can also be metabolized to 131
25-dimethyl-4-hydroxy-2H-furan-3-one glucoside (HDMF-glucoside) by a 132
UDP-dependent glycosyltransferase (UGT71K3) and further malonylated into 133
25-dimethyl-4-hydroxy-2H-furan-3-one 6rsquo-O-malonyl-β-D-glucopyranoside (HDMF 134
malonyl-glucoside) in strawberry fruit (Roscher et al 1996 Song et al 2016) The 135
biosynthetic pathway of HDMF in other plants is similar to that in strawberry Genes 136
with homology to FaQR have been identified in tomato (SlEO) and mango (MIEO) 137
(Klein et al 2007 Kulkarni et al 2013) 138
139
As an NADH-dependent enone oxidoreductase protein FaQR exhibits o-quinone 140
oxidoreductase activity (Raab et al 2006) FaQR mRNA accumulates in fruit 141
parenchyma tissues but is absent in vascular tissues and FaQR is mainly expressed in 142
the late stages of fruit growth and ripening paralleling furaneol production in the fruit 143
(Raab et al 2006) FaQR is responsive to environmental stimuli associated with 144
furaneol production and in the dark lsquoSweet Charliersquo strawberry fruits have higher 145
levels of FaQR expression and HDMF production at 25degC than at 15degC (Fu et al 146
2017) in contrast the concentration of furanones and the abundance of FaQR protein 147
under low-temperature storage is significantly lower than those under 148
room-temperature storage (Li et al 2015) Thus the regulation of FaQR is important 149
for manipulating furaneol content Although it is assumed that transcription factors 150
control expressions of genes involved in volatile production in plants no such factors 151
regulating FaQR or other furanone biosynthetic genes have been identified 152
153
Different members of the largely plant-specific AP2ERF gene family (Weirauch and 154
Hughes 2011) have diverse functions in plant growth development and stress 155
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
7
responses (Agarwal et al 2010 Zhu et al 2010 Licausi et al 2013) In recent years 156
several AP2ERF genes have been reported to regulate aspects of fruit quality (Xie et 157
al 2016) including fruit aroma For example CitAP210 is associated with the 158
synthesis of (+)-valencene in Newhall orange acting via regulation of CsTPS1 (Shen 159
et al 2016) CitERF71 was shown to physically bind to the CsTPS16 promoter and 160
contribute to the synthesis of E-geraniol in citrus fruit (Li et al 2017) These 161
observations raised the possibility that FaQR might also be a target for a member of 162
the AP2ERF family and that ERFs might also control furaneol biosynthesis 163
164
In this study screening of the Fragaria times ananassa AP2ERF gene family led to 165
identification of FaERF9 as an activator of FaQR however it did not bind directly 166
to the promoter A parallel search for proteins that directly bind the FaQR promoter 167
using yeast one-hybrid screening identified a second factor FaMYB98 which was 168
capable of physically interacting with the FaQR promoter FaMYB98 physically 169
interacts with FaERF9 and transient expression assays demonstrated a synergistic 170
effect on FaQR expression and furanone synthesis 171
172
Results 173
Changes in the content of both furanones and the activity of their biosynthetic 174
genes in strawberry fruit 175
lsquoYuexinrsquo fruits at four developmental and ripening stages (G green T turning IR 176
intermediate red R full red) were harvested (Figure 1) and determination of HDMF 177
levels indicated a major increase from about 065 μg per gram fruit at the IR stage to 178
346 μg at the R stage in the apical section implying that furaneol accumulation was 179
closely related to colour change and ripening (Figure 1) Furaneol levels were higher 180
in the apical section than in the basal section HDMF could not be detected at the IR 181
stage in the basal section but the amount increased at the R stage to 142 μg per gram 182
fruit Differences were also found for DMMF with the relative content in the apical 183
section 018 μg per gram at the R stage compared to 008 μg per gram in the basal 184
section at the same stage 185
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
8
186
Measurement of mRNA levels by RT-qPCR indicated that the transcript levels of both 187
FaQR (GenBank AY1588361) and FaOMT (GenBank AF2204912) increased 188
throughout ripening (Figure 1) Comparison of the expression of these genes showed 189
that the transcript levels of FaQR and FaOMT significantly increased as early as in T 190
stage in basal fruit sections and for each gene over half of the peak transcript 191
abundance occurred as early as in IR stage in the apical section while for the basal 192
section it was in the R stage indicating a gradient of gene expression and volatile 193
production from apex to base of the fruit during ripening 194
195
Genome-wide identification of AP2ERF gene family in strawberry 196
Coding sequences of 120 non-redundant FaAP2ERF genes were isolated and 197
identified from lsquoYuexinrsquo strawberry and a systematic nomenclature for the AP2ERF 198
family genes was used to distinguish the members based on the structural features 199
defined previously (Supplemental Table S1) (Shigyo and Ito 2004 Nakano et al 200
2006 Licausi et al 2013) CD-search analysis showed that this superfamily is 201
consisted of 95 ERFs 18 AP2 and 6 RAV family members and 1 soloist member 202
(Supplemental Table S2) Phylogenetic analysis of the Fragaria times ananassa and 203
Arabidopsis AP2ERF members is shown in Supplemental Figure S1 with the 120 204
AP2ERF genes divided into three major groups (ERF AP2 RAV) and a soloist and 205
the ERF family being further divided into 10 groups (groups I to X in Supplemental 206
Table S1) 207
208
We performed a dual-luciferase assay to determine the ability of 116 FaAP2ERF 209
members to activate transcription from the promoter of FaQR The results indicated 210
about 12 members (mainly belonging to the ERF and RAV families) showed a 211
significant activation effect on the FaQR promoter while the remaining members 212
showed very limited effects (Figure 2) The relative activity of only the following 12 213
FaAP2ERF transcripts reached the threshold value set at 2 FaERF8FaERF9 214
(group II) FaERF27FaERF29FaERF31FaERF32 (group IV) 215
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
9
FaERF37FaERF38 (group V) FaERF62FaERF64 (group VIII) FaERF68 216
(group IX) and FaRAV4 (Figure 2) Of these FaERF9 exhibited the highest 217
activation effect on the FaQR promoter (466-fold) (Figure 2) The strawberry 218
FaERF9 cDNA is 699 bp long and ExPASy Compute pIMw tool analysis indicated 219
that this gene encodes a 232-amino acid protein with a calculated molecular mass of 220
254 KD and a pI of 56 221
222
FaERF9 expression pattern and subcellular localization 223
To further explore the connections between AP2ERFs and furaneol biosynthesis we 224
obtained the transcript profiles of the AP2ERF genes in strawberry fruit samples at 225
different fruit developmental and ripening stages by reverse transcription quantitative 226
PCR (RT-qPCR) excluding genes with very low abundance in the fruit samples The 227
results presented as a heatmap (Supplemental Figure S2) demonstrate that these 228
genes displayed various expression patterns in both the apical and basal sections and 229
by analysing the expression patterns of the members indicated as activators in the 230
dual-luciferase assay we found that only a few genes including FaERF8 FaERF9 231
FaERF27 FaERF32 and FaERF37 were up-regulated during ripening stages and 232
their expression correlated with furaneol accumulation in the fruit (Figure 1) 233
Furthermore the expression patterns of the up-regulated genes in the apical and basal 234
sections showed that one ERF gene FaERF9 not only showed an up-regulation 235
pattern in both sections but its expression in the apical section occurred ahead of that 236
in the basal section (Figure 3) consistent with the actual changes in furaneol content 237
(Figure 1) and the expression pattern of FaQR (Figure 1) The subcellular localization 238
of FaERF9 was predicted to be in the nucleus using the WoLF PSORT program In 239
experimental tests 35S-FaERF9-GFP (green fluorescence protein) showed strong 240
fluorescence in the nucleus and the green signal merged with the red fluorescence 241
signal of mCherry-nucleus-marker in tobacco plants (Figure 3) 242
243
Transient overexpression of FaERF9 in strawberry 244
The expression of FaERF9 in agro-infiltrated fruits was analysed by performing 245
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10
RT-qPCR on the seventh day after infiltration by which time they had reached the IR 246
or R stage and the result showed that the transcript levels were significantly higher 247
(52-fold) than in control fruits (Figure 4) The expression of FaQR was examined in 248
the same fruits and the transcript abundance also increased 22-fold The relative 249
content of HDMF in the FaERF9-overexpressing fruits was 008 μg per gram fruit 250
and undetectable in the control fruits (Figure 4) The relative content of DMMF in the 251
overexpressing fruits was also significantly increased to 038 μg per gram fruit 252
compared to 004 μg per gram fruit in the control (Figure 4) These observations 253
provide direct evidence for a regulatory role for FaERF9 in promoting FaQR 254
biosynthesis and activity in ripening strawberry fruit Taken together these results 255
indicate that by activating the transcription of FaQR FaERF9 functions as a positive 256
regulator in furaneol biosynthesis 257
258
Correlation of FaERF9 expression and FaQR transcript profiles 259
GC-MS quantification showed that furanones are distributed in variable levels among 260
different strawberry cultivars (Supplemental Figure S3) The transcript profiles of 261
FaQR and FaERF9 in fruits of different cultivars were measured and linear 262
regression analysis was performed In the cultivars the changes in FaQR transcripts 263
correlated positively with those in FaERF9 transcripts (r = 079 plt001) (Figure 5) 264
In addition FaERF9 transcript levels also correlated with furanone content across 265
cultivars (Figure 5) 266
267
FaERF9 is an indirect regulator of the FaQR promoter and acts via 268
protein-protein interaction with FaMYB98 269
Although the results of the dual-luciferase assay expression analysis transient 270
overexpression and correlation analysis were all consistent with the suggestion that 271
FaERF9 regulates transcript abundance by acting on the FaQR promoter a yeast 272
one-hybrid assay indicated that FaERF9 cannot bind directly to the FaQR promoter 273
(Figure 6) This led us to speculate that activation may occur via a transcription 274
complex involving an additional as-yet unknown regulator which can bind directly to 275
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11
the FaQR promoter 276
277
In parallel with the investigation of the FaAP2ERF genes a cDNA library screening 278
was performed with a yeast one-hybrid assay using the promoter of FaQR as the bait 279
This screen identified several transcription factors that could physically bind to the 280
FaQR promoter but only one MYB could activate transcription from the FaQR 281
promoter (approximately 56-fold) relative to the control (Figure 6) in the 282
dual-luciferase assay This MYB showed 44 amino acid identity with MYB98 283
(GenBank ABA420611) a transcriptional regulator in the synergid cells in 284
Arabidopsis (Kasahara et al 2005) and it was designated as FaMYB98 The 285
specificity of FaMYB98 binding to the FaQR promoter was confirmed by EMSA 286
assay (Figure 7) and increasing the concentration of the cold probe reduced binding 287
In addition mutating the putative binding sites (Goacutemez-Maldonado et al 2004 288
Punwani et al 2007) as shown in Figure 7 eliminated FaMYB98 protein binding 289
When the combined effect of FaERF9 and FaMYB98 was analysed (Figure 8) a 290
synergistic 14-fold activation of the FaQR promoter was observed compared with the 291
activation by either FaERF9 or FaMYB98 which alone promoted transactivation 292
39-fold and 45-fold respectively In addition overexpression of both genes 293
(FaERF9-FaMYB98-SK) in strawberry fruits resulted in higher expression of 294
FaERF9 transcripts and higher furanone content than overexpression of FaERF9 295
(Supplemental Figure S4 Supplemental Table S3) Subcellular localization analysis 296
revealed that FaMYB98 was also localized in the nucleus (Supplemental Figure S5) 297
298
To investigate the potential interactions between FaERF9 and FaMYB98 the 299
DUALhunter system was used (Figure 9) Cells expressing the FaMYB98 and 300
FaERF9 protein pair using either FaMYB98 or FaERF9 as the bait grew on DDO 301
QDO and QDO supplemented with 1 mM 3-AT selective medium indicating 302
interaction between the two proteins This putative protein-protein interaction was 303
confirmed by BiFC assay and the combinations of FaMYB98-YFPNFaERF9-YFPC 304
and FaERF9-YFPNFaMYB98-YFPC exhibited strong coincident signals in the 305
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12
nucleus while negative controls produced no detectable fluorescence signal (Figure 306
10) In addition coexpression of FaERF9-YFPNFaERF9-YFPC as well as 307
FaMYB98-YFPNFaMYB98-YFPC also generated signals in the nucleus indicating 308
that FaERF9 and FaMYB98 both could form homodimers or possibly multimers in 309
the nucleus (Figure 10) 310
311
Discussion 312
The AP2ERF superfamily in strawberry 313
The AP2ERF superfamily of plant transcription factors is defined by the AP2ERF 314
domain and comprises the ERF AP2 and RAV families as well as one soloist member 315
(Riechmann et al 2000 Weirauch and Hughes 2011) The completion of multiple 316
plant genome sequences has enabled a genome-scale analysis of the AP2ERF family 317
which in recent years has been systematically studied in diverse fruit species such as 318
tomato grape peach and kiwi fruit (Zhuang et al 2009 Sharma et al 2010 Licausi 319
et al 2010 Yin et al 2010 Pirrello et al 2012 Zhang et al 2012 Zhang et al 320
2016) A few AP2ERF genes have been isolated and characterized in strawberry and 321
CBF orthologs (Owens et al 2002 Koehler et al 2012 Zhang et al 2014) have 322
been identified from different strawberry cultivars in several independent studies 323
Although they have distinct names eg Fragaria times ananassa CBF1 (FaCBF1) 324
FaCBF4 (GenBank HQ9105151) and CBF1 (GenBank EU1172142) according to 325
the phylogenetic tree generated in this study the orthologs of 326
CBF1CBF4CBF2CBF3 in Arabidopsis are similar to each other and to FaERF20 327
(Supplemental Figure S1) (Owens et al 2002 Koehler et al 2012 Zhang et al 328
2014) FaERF20 has 85 sequence similarity with FaCBF1 identified by Owens et 329
al (2002) 93 similarity with FaCBF4 amplified by Koehler et al (2012) and 75 330
similarity with CBF1 cloned by Zhang et al (2014) The AP2ERF genes 331
characterized in other studies (Jia et al 2011 GAO et al 2015 Chai and Shen 2016 332
Mu et al 2016) are also noted in Supplemental Table S1 333
334
Based on the computational analysis we have identified a total of 120 AP2ERF 335
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13
genes in octoploid strawberry (Supplemental Table S1) The number of predicted 336
AP2ERF genes (120) is comparable to those observed in other fruits including 337
tomato (112) Chinese plum (116) citrus (126) and peach (131) but lower than those 338
reported for grape (149) (Xie et al 2016) As shown in Supplemental Table S2 79 339
(95 genes) of the AP2ERF genes belong to the ERF family in strawberry constituting 340
the largest sub-family The members of this sub-family can be classified into 10 341
groups (group I to X) according to their sequence similarities to the Arabidopsis ERF 342
genes (Nakano et al 2006) The AP2 family encompasses the same number of genes 343
in Arabidopsis citrus and strawberry (eighteen) (Nakano et al 2006 Xie et al 2014) 344
and there are six RAV genes in strawberry which are highly conserved in dicots such 345
as Vitis vinifera Arabidopsis thaliana and Populus trichocarpa (Licausi et al 2010) 346
347
Role of FaERF9 in regulating the biosynthesis of HDMF a positive regulator 348
acting in an indirect manner 349
The large-scale screening of the AP2ERF superfamily in strawberry led to 350
identification of 11 ERFs and 1 RAV that trans-activated the FaQR promoter more 351
than two-fold with the highest activation caused by FaERF9 which trans-activated 352
the FaQR promoter (Figure 2) as well as up-regulating FaQR expression and furanone 353
production in transient overexpression assays (Figure 4) which has been extensively 354
used to explore the fruit-associated gene functions in strawberry (Han et al 2015 355
Medina-Puche et al 2015 Vallarino et al 2015 Carvalho et al 2016 Song et al 356
2016 Wang et al 2018) FaERF9 transcripts accumulate in the fruit apical section 357
before the basal section (Figure 3) a finding consistent with the actual changes in 358
furaneol content (Figure 1) and the expression of FaQR (Figure 1) The association 359
between FaERF9 transcripts and accumulation of furanones were also established 360
with different strawberry cultivars The correlation between FaERF9 and FaQR 361
expression as well as furanone content among cultivars supports a positive role of 362
FaERF9 in regulating furanone content (Figure 5) These results indicate that 363
FaERF9 transcript abundance may be a good indicator of the abundance of these 364
important flavour volatiles in fruits of different cultivars This should be considered as 365
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14
a method for high-throughput variety screening to replace direct measurement of 366
volatiles 367
368
FaERF9 is a member of the ERF group II family and is most closely related to the 369
Arabidopsis genes At1g44830 (ATERF014) At1g21910 (DREB26) and At1g77640 370
(Supplemental Figure S1) At1g44830 was observed to be strongly up-regulated in a 371
comprehensive microarray analysis of the root transcriptome following NaCl 372
exposure (Jiang and Deyholos 2006) At1g21910 (DREB26) was functionally 373
characterized as a trans-activator localized in the nucleus exhibiting tissue-specific 374
expression and participating in plant developmental processes as well as biotic andor 375
abiotic stress signalling (Krishnaswamy et al 2011) However none of these genes 376
have been reported as furanone regulators In strawberry another five genes 377
(FaERF6 FaERF7 FaERF8 FaERF10 and FaERF11) also belong to the same 378
group with FaERF8 also showing somewhat weaker activation activity towards the 379
FaQR promoter than FaERF9 The fact that FaERF9 could not bind directly to the 380
promoter of FaQR (Figure 6) indicates that it might function as an indirect regulator 381
of FaQR and furaneol biosynthesis 382
383
A FaERF9 and FaMYB98 complex is involved in regulating FaQR and furaneol 384
biosynthesis 385
The finding that FaERF9 could interact with FaMYB98 protein (Figures 9 and 386
Figure 10) and that FaMYB98 could physically bind to the FaQR promoter (Figure 6 387
and Figure 7) provides evidence for a regulatory mechanism whereby FaERF9 388
regulates FaQR and furaneol production as part of a complex with an MYB 389
transcription factor Since co-overexpression of FaERF9 and FaMYB98 resulted in 390
much higher activation activity towards FaQR we speculate that FaERF9 may 391
recruit FaMYB98 homologs in tobacco to activate the FaQR promoter (Figure 8) 392
FaOMT is another key gene for furanone biosynthesis and a potential target for 393
transcriptional activation However FaERF9 did not significantly activate the 394
FaOMT promoter in a dual-luciferase assay and the transcript level of FaOMT in the 395
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15
FaERF9-overexpressing fruits showed no significant difference from that in the 396
control (Supplemental Figure S6 Supplemental Figure S7) The FaOMT promoter 397
was significantly induced by FaMYB98 but no synergistic effect of FaERF9 and 398
FaMYB98 on the promoter was observed (Supplemental Figure S6) In previous 399
studies of the regulation of plant volatile compounds MYBs have been characterized 400
as being involved mainly in the regulation of the benzenoidphenylpropanoid pathway 401
that produces floral volatiles in petunia and eugenol in ripe strawberry fruit (Verdonk 402
et al 2005 Dal Cin et al 2011 Colquhoun et al 2011 Spitzer-Rimon et al 2012 403
Medina-Puche et al 2015) but their role in formation of volatiles from other 404
pathways has not been reported Our study demonstrates a role for MYB in the 405
synthesis of furaneol a carbohydrate-derived volatile compound and reveals the 406
synergistic interactions between an MYB and ERF in a transcription complex (Figure 407
8 Figure 9 and Figure 10) 408
409
Recent research has provided evidence for interactions between AP2ERF and MYB 410
transcription factors in regulating other aspects of fruit quality including texture 411
(EjAP2-1 and EjMYB Zeng et al 2015) and colour (PyERF3 and PyMYB114 Yao 412
et al 2017) A group VIII ERF has also recently been shown to interact with an MYB 413
to regulate floral scent production in petunia (Liu et al 2017) In strawberry fruit 414
DOF in combination with an MYB has been reported to be involved in the regulation 415
of eugenol production and the identification of this second transcription factor (DOF) 416
suggests that it is a good target in breeding for improved flavour (Molina-Hidalgo et 417
al 2017 Tieman 2017) Considering its important contribution to flavour in 418
strawberry and many other highly valued fruit crop species (pineapple tomato mango 419
etc) very little is known about regulation of furaneol synthesis Here we established 420
the role of FaERF9 in the regulation of HDMF synthesis by direct protein-protein 421
interactions with FaMYB98 to synergistically trans-activate FaQR The functional 422
identification of this complex enhances our knowledge of the regulation of volatile 423
compound synthesis and identifies a new AP2ERF-MYB complex Further 424
examination of the other ERFs that stimulated transcription from the FaQR promoter 425
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16
(Figure 2) may provide additional information about the complexity of this regulation 426
Overall this study provides important clues for understanding the transcriptional 427
regulation of HDMF synthesis and identifies specific transcription factors that are 428
likely to be good targets for molecular breeding for improved flavour 429
430
Conclusions 431
Screening of the AP2ERF superfamily in strawberry (Fragaria times ananassa) 432
identified candidate members capable of activating the FaQR promoter An ERF 433
transcription factor was identified as a positive regulator of HDMF synthesis in 434
strawberry fruit and the mechanism of activation was shown to involve an ERF-MYB 435
transcription complex that regulates transcription of FaQR leading to the biosynthesis 436
of HDMF the characteristic volatile compound which has a major influence on 437
strawberry aroma 438
439
Materials and Methods 440
441
Plant Materials and Growth conditions 442
The strawberry (Fragaria times ananassa cv lsquoYuexinrsquo an octoploid cultivar) fruit used in 443
this study were bred by Zhejiang Academy of Agricultural Sciences (Haining 444
Zhejiang) Fruits at various developmental and ripening stages including G (green) T 445
(turning) IR (intermediate red) and R (full red) were harvested (Figure 1) and 446
transported to the laboratory within 2 h Thirty-six fruits of uniform size and free of 447
visible defects were selected at each stage with twelve fruits in each biological 448
replicate After removing the calyces fruits were then divided into the basal and 449
apical sections which were sampled separately (Figure 1) They were rapidly cut into 450
pieces frozen immediately in liquid nitrogen and stored at -80deg C until use Red ripe 451
fruits of different strawberry cultivars (Fragaria times ananassa octoploid cultivars) 452
including lsquoYuelirsquo lsquoBenihoppersquo lsquoMengxiangrsquo lsquoAmaoursquo lsquo10-1-4rsquo lsquoAkihimersquo lsquoSweet 453
Charliersquo lsquo07-1-4rsquo lsquoDarselectrsquo lsquoYuexinrsquo and lsquoXuemeirsquo were also provided by Zhejiang 454
Academy of Agricultural Sciences For each cultivar the fruits of three biological 455
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17
replicates were sampled frozen in liquid nitrogen and stored at -80deg C for further use 456
457
Tobacco plants (Nicotiana benthamiana) used for dual-luciferase assays and 458
subcellular localization analysis in this study were grown in a growth chamber with a 459
lightdark cycle of 16 h8 h at 24degC 460
461
Detection of DMMF and HDMF 462
Automated HS-SPME-GC-MS was performed to detect both furanones in lsquoYuexinrsquo 463
strawberry fruit (Zorrilla-Fontanesi et al 2012) Samples were ground into a powder 464
under liquid nitrogen for analysis 465
466
For the detection of DMMF (Figure 1) 05 g (fresh weight) of each sample was 467
weighed in the vial to which was added 1 mL of EDTA solution (100 mM pH 75) 1 468
mL of CaCl2 solution (mv = 20) and 20 microL of 2-octanol as the internal standard 469
(007 μgμL) The mixture was homogenized and the vial closed and placed on the 470
sample tray for analysis by CombiPAL autosampler (CTC Analytic CA USA) The 471
fruit volatiles were sampled by headspace solid-phase microextraction with a 65-μm 472
polydimethylsiloxane-divinylbenzene fibre (PDMS-DVB) Initially vials were 473
pre-incubated at 50degC for 10 min under continuous agitation (500 rpm) then volatiles 474
were extracted for 30 min at the same temperature and agitation speed After that the 475
fibre was desorbed in the GC injection port for 5 min in splitless mode The 7890A 476
GC chromatograph was equipped with a DB-5ms column (60 m times 250 μm times 1 μm 477
JampW Scientific Folsom CA USA) with helium as the carrier gas at a constant flow 478
of 12 mLmin The GC was programmed at an initial temperature of 35degC for 2 min 479
with a ramp of 5degC min up to 250degC and held for 5 min The injection port interface 480
and MS source temperatures were 250degC 260degC and 230degC respectively The 481
ionization potential was set at 70 eV recorded by a 5975B mass spectrometer (Agilent 482
Technologies JampW Scientific Folsom CA USA) and the scanning speed was 7 483
scanss The same method was used to analyse HDMF and DMMF in fruits from 484
different cultivars (Supplemental Figure S3) except for the sample preparation 485
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18
procedure (Araguumlez et al 2013) briefly 05 g (fresh weight) of powdered fruit was 486
incubated at 30degC in a water bath for 5 min then 2 mL of NaCl (mv = 20) and 20 487
microL of 2-octanol as the internal standard (007 μgμL) were added and homogenized 488
489
For the detection of HDMF (Figure 1) and both furanones (Figure 4 and Supplemental 490
Table S3) a liquid-injection system equipped with CTC Pal ALS was used One gram 491
(fresh weight) of powdered fruit and 2 mL of NaCl (mv = 20) were homogenized in 492
a 10-mL tube and 300 μL of CH2Cl2 and 20 microL of 2-octanol (0766 μgμL) as the 493
internal standard were added to extract the volatiles the mixture was then 494
homogenized again The tubes were stored at room temperature for 20 min and 495
centrifuged at 12000 rpm for 5 min The subnatant was pipetted into a clean 15-mL 496
tube in which 20 mg of anhydrous sodium sulphate was added the tube was left 497
without shaking for half an hour Then 150 μL of the solution was transferred into a 498
GC vial and placed on the sample tray as described above Each sample (1 μL) was 499
injected using the autosampler and the analysis was accomplished by a 7890A 500
GC-MS system (Agilent Technologies JampW Scientific Folsom CA USA) equipped 501
with a DB-WAX column (30 m times 025 mm times 025 μm JampW) Helium (12 mLmin) 502
was used as a carrier gas The injection port (splitless injection mode) interface and 503
MS source temperatures were as described above The oven temperature was set at 504
60degC for 4 min then increased to 180degC at a rate of 4degCmin and maintained for 30 505
min DMMF was identified by comparison of electron ionization mass spectra and 506
retention time data with the data from the NISTEPANIH mass spectral library 507
(NIST-08 and Flavor) HDMF (Figure 1) was identified and qualified by comparison 508
with injected standard (Sigma) The quantitative analysis of both furanones (Figure 4 509
Supplemental Table S3 and Supplemental Figure S3) was determined using the peak 510
area of the internal standard as a reference based on total ion chromatogram (TIC) 511
512
RNA isolation and Reverse Transcription Quantitative PCR (RT-qPCR) 513
Total RNA from strawberry samples was isolated in this study using the CTAB 514
method (Chang et al 1993) Genomic DNA contamination was eliminated by 515
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19
TURBO Dnase (Ambion) 1 μg of RNA was used to obtain cDNA using an IScriptTM 516
cDNA Synthesis Kit (Bio-Rad) The synthesized cDNA was diluted with water (120) 517
and 2 μL of diluted cDNA was used as the template for RT-qPCR Reactions were 518
performed in a total volume of 20 μL consisting of 10 μL of SYBR PCR supermix 519
(Bio-Rad) 1 μL of each primer (10 μM) 6 μL of DEPC-H2O and 2 μL of diluted 520
cDNA on CFX96 instrument (Bio-Rad) (Yin et al 2012) The oligonucleotide 521
primers for RT-qPCR analysis of genes including the AP2ERF FaQR and FaOMT 522
were designed according to the coding sequences of genes and the specificity was 523
verified before use (Min et al 2012) NCBIPrimer-BLAST was applied to design the 524
primers Relative expression levels were normalized to that of an internal controlmdashthe 525
interspacer 26S-18S strawberry RNA housekeeping gene FaRIB413 526
(Zorrilla-Fontanesi et al 2012) To investigate the differential expression of genes 527
during fruit development and ripening stages relative expression of each gene at the 528
R stage in the basal fruit section was set as 1 using the 2minus∆∆119862119879 method For transient 529
overexpression assay relative expression of control fruits with an empty vector (SK) 530
was set as 1 The primers used in RT-qPCR are listed in Supplemental Table S4 531
532
Gene isolation and analysis 533
Multiple database searches were performed to identify members of the strawberry 534
(Fragaria times ananassa) AP2ERF superfamily in the published strawberry databases 535
and annotations of Fragaria times ananassa and Fragaria times vesca by using the 536
AP2ERF DNA binding domain as a query sequence and 120 genes were identified 537
with AP2ERF domain(s) Based on the BLAST result primers (listed in 538
Supplemental Table S5) were used to amplify the coding full-length cDNAs of 539
AP2ERF genes The deduced amino acid sequences of AP2ERF proteins in 540
Arabidopsis thaliana used for construction of a phylogenetic tree were obtained from 541
the Arabidopsis Information Resource (TAIR) Alignment of the proteins was 542
performed using the neighbour-joining method in ClustalX (v181) and the 543
phylogenetic tree was constructed using FigTree (v131) 544
545
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20
FaMYB98 was obtained by yeast one-hybrid screening sequencing and the full-length 546
sequences were predicted by BLAST Primers were designed (listed in Supplemental 547
Table S5) to amplify the full-length coding sequence 548
549
The promoter of FaQR was cloned by Genome Walking as previously described (Yin 550
et al 2010) and conserved cis-element motifs in the promoter were manually 551
searched 552
553
Conserved domains within the FaAP2ERF proteins and FaMYB98 were analysed by 554
CD-search (httpswwwncbinlmnihgovStructurecddwrpsbcgi) and cellular 555
locations of proteins including FaERF9 and FaMYB98 were predicted with the 556
WoLF PSORT program (httpswwwgenscriptcomwolf-psorthtml) 557
558
Dual-Luciferase Assays 559
In accordance with a previous protocol (Yin et al 2010) the full-length cDNAs of 560
FaAP2ERF or FaMYB98 transcription factors were cloned into pGreen II 0029 561
62-SK vector and the promoter of FaQR was cloned into pGreen II 0800-LUC vector 562
A luciferase gene from Renillia (REN) driven by a 35S promoter in the LUC vector 563
acted as a positive control The above constructs were transiently expressed in 564
Nicotiana benthamiana leaves by Agrobacterium-mediated infiltration (strain 565
GV3101) and the activity of the TFs on the promoter was measured on the third day 566
after infiltration indicated by the ratio of enzyme activities of firefly luciferase (LUC) 567
and renilla luciferase (REN) using a Modulus Luminometer (Promega Madison WI 568
USA) To determine the activity of a specific transcription factor towards the 569
promoter we mixed the Agrobacterium culture with 1 mL of TF and 100 μL of 570
promoter and the LUCREN value of the empty vector SK on the promoter was set as 571
1 as a calibrator To test the combined effect of two transcription factors on the 572
promoter to the Agrobacterium culture mixture we added 05 mL of each TF and 100 573
μL of promoter the effect of the mixtures that contained each transcription factor (05 574
mL) and empty vector SK (05 mL) was also tested on the promoter as a control 575
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
21
576
Subcellular localization analysis 577
35S-FaERF9-GFP and 35S-FaMYB98-GFP were transiently expressed in tobacco (N 578
benthamiana) leaves by Agrobacterium infiltration (EHA105) using the same method 579
as described in the dual-luciferase assay above The transiently infected leaves were 580
imaged on the third day after infiltration using a Nikon A1-SHS confocal laser 581
scanning microscope The excitation wavelength for GFP fluorescence was 488 nm 582
and fluorescence was detected at 490ndash520 nm The primers used for GFP construction 583
are listed in Supplemental Table S6 584
585
Transient overexpression in strawberry fruit 586
Transient overexpression of FaERF9 and an overexpression binary vector (pGreen II 587
0029 62-SK-FaERF9-FaMYB98) were performed in strawberry fruit using the 588
FaERF9-SK construct described above for the dual-luciferase assays and the binary 589
vector constructed according to Liu et al 2013 The transfection of fruit was carried 590
out at the G stage (Hoffmann et al 2006) The FaERF9-SK construct and binary 591
vector were individually electroporated into Agrobacterium tumefaciens GV3101 and 592
the Agrobacterium culture suspended in infiltration buffer was infiltrated into the 593
whole fruit using a syringe As a control treatment fruits were infiltrated with 594
Agrobacterium carrying an empty vector SK under the same transfection conditions 595
Fruits were left attached to the plants and harvested on the seventh day after 596
infiltration Fruits of three biological replicates were sampled for further analysis 597
598
Yeast one-hybrid assay 599
In order to identify proteins that bind to the FaQR promoter the Matchmaker Gold 600
Yeast One-hybrid Library Screening System (Clontech USA) was used The sequence 601
of the FaQR promoter was cloned into the pAbAi vector and the construct was 602
integrated into the genome of the Y1HGold yeast strain A mixture of total RNA from 603
strawberry fruit at four stages (G T IR R) was used to construct the prey cDNA 604
library (TaKaRa) The background AbAr expression of Y1HGold FaQR-pAbAi strain 605
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
22
was tested according to the system user manual and then screening for protein-DNA 606
interactions was carried out Furthermore the full length of each transcription factor 607
was separately cloned into pGADT7 AD vector to confirm the screening results The 608
relationship between FaERF9 and FaQR promoter was also examined individually 609
Primers used in this assay are listed in Supplemental Table S6 610
611
Expression and purification of FaMYB98 recombinant protein 612
A 405-bp region spanning the DNA-binding domain of FaMYB98 was amplified 613
from FaMYB98 cDNA and cloned into a pET6timesHN vector (Clontech Palo CA USA) 614
to generate the recombinant N-terminal His-tagged protein the primers used are listed 615
in Supplemental Table S6 The resulting construct was sequenced and introduced into 616
Escherichia coli strain Rosetta 2(DE3)pLysS (Novagen) Ten millilitres of the 617
overnight culture was combined with 500 mL of an LB liquid medium (100 μgmL 618
ampicillin and 34 μgmL chloramphenicol) as described (Li et al 2017) Isopropyl 619
β-D-1-thiogalactopyranoside (IPTG) was added to a final concentration of 1 mM and 620
the bacterial culture was incubated at 18degC at 150 rpm for 18 h Then the cells were 621
harvested using a centrifuge and resuspended in 1times PBS buffer (Sangon Biotech) 622
after which they were disrupted by sonication and the supernatant was purified using 623
a HisTALONTM Gravity Column (Clontech) according to the user manual The PD-10 624
Desalting column (GE Healthcare) was then used for buffer change and sample 625
clean-up of proteins according to the gravity protocol SDS-PAGE was performed and 626
the protein was visualized using Coomassie brilliant blue 627
628
Electrophoretic mobility shift assay (EMSA) 629
A Lightshift Chemiluminescent EMSA kit (Thermo) was used to perform EMSA 630
experiments according to the manufacturerrsquos instructions Single-strand 631
oligonucleotides were synthesized and biotinylated by GeneBio Biotech (Hangzhou 632
China) The details of the EMSA assay are provided in Ge et al (2017) The probes 633
used for EMSAs are listed in Supplemental Table S6 634
635
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
23
636
Yeast two-hybrid assay 637
The DUALhunter system (Dualsystems Biotech Switzerland) was used to investigate 638
the interaction between FaERF9 and FaMYB98 Full-length coding sequences of 639
FaERF9 and FaMYB98 were respectively cloned into pDHB1 bait vector and 640
pPR3-N prey vector sequences were verified and the bait plasmid was 641
co-transformed with prey plasmid into NMY51 in the combinations below 642
FaMYB98-pDHB1pPR3-N FaMYB98-pDHB1FaERF9-pPR3-N 643
FaMYB98-pDHB1pOst1-NubI FaERF9-pDHB1pPR3-N 644
FaERF9-pDHB1FaMYB98-pPR3-N and FaERF9-pDHB1pOst1-NubI (Li et al 645
2017) Transformed cells were spread onto the following plates DDO (SD 646
medium-Trp-Leu) QDO (SD medium-Trp-Leu-His-Ade) and QDO+3-AT (QDO 647
medium supplemented with 1 mM 3-amino-124-triazole) The control plasmid 648
pOst1-NubI was used to determine whether the bait was functional the pPR3-N prey 649
vector plasmid was used to test whether the bait displayed non-specific background 650
and positive interactions were indicated by the growth of yeast on QDO and 651
QDO+3-AT plates The Primers used in the DUALhunter assay are listed in 652
Supplemental Table S6 653
654
Bimolecular fluorescence complementation (BiFC) assays 655
Full-length FaERF9 and FaMYB98 respectively were cloned into sequences 656
encoding the N- and C- fragments of YFP protein (Lv et al 2014) All constructs 657
were transiently expressed in tobacco (N benthamiana) leaves by Agrobacterium 658
infiltration (EHA105) The YFP fluorescence of transfected leaves was imaged 40 h 659
after infiltration by using a Nikon A1-SHS confocal laser scanning microscope The 660
excitation wavelength for YFP was 488 nm and fluorescence was detected at 520ndash661
540 nm Primers used are listed in Supplemental Table S6 662
663
Statistics 664
A Studentrsquos two-tailed t test ( plt005 plt001 and plt0001) was used to 665
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
24
determine significant differences between two groups in this study Microsoft Excel 666
was used to perform linear regressive analysis significant differences were 667
determined by SPSS Statistics 200 and scatter plots were prepared with Origin80 668
Least significant difference (LSD) at the 5 level was calculated using Microsoft 669
Excel Figures were prepared with Origin80 (Microcal Software Inc Northampton 670
MA USA) The online tool MetaboAnalyst 36 (httpwwwmetaboanalystca) was 671
used to analyse the transcript abundance of the AP2ERF genes 672
673
Accession numbers 674
Sequence data from this article have been deposited in GenBank under the accession 675
numbers MH332903-MH333022 for AP2ERF genes in Fragaria times ananassa and 676
MH333023 for FaMYB98 GenBank numbers for FaQR and FaOMT were 677
AY1588361 (Raab et al 2006) and AF2204912 (Wein et al 2002) 678
679
Supplemental Material 680
Supplemental Figure S1 Phylogenetic analysis of FaAP2ERF and Arabidopsis 681
AP2ERF proteins 682
Supplemental Figure S2 Analysis of FaAP2ERF gene expression patterns in 683
strawberry fruit during development and ripening 684
Supplemental Figure S3 Contents of furanones in fruit of strawberry cultivars 685
Supplemental Figure S4 Relative expression of FaERF9 in FaERF9-FaMYB98- 686
and FaERF9-overexpressing fruits 687
Supplemental Figure S5 Subcellular localization of FaMYB98 688
Supplemental Figure S6 The combined activation effects of FaERF9FaMYB98 on 689
the FaOMT promoter 690
Supplemental Figure S7 Relative expression of FaOMT in 691
FaERF9-overexpressing fruits 692
Supplemental Table S1 AP2ERF superfamily genes in Fragaria times ananassa 693
Supplemental Table S2 Classification of the AP2ERF superfamily members in 694
Fragaria times ananassa 695
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
25
Supplemental Table S3 Furanone content in FaERF9-FaMYB98- and 696
FaERF9-overexpressing fruits 697
Supplemental Table S4 Primers used for reverse transcription quantitative PCR 698
(RT-qPCR) 699
Supplemental Table S5 Primers used to amplify the full-length coding sequences of 700
AP2ERF genes and FaMYB98 in strawberry (Fragaria times ananassa) 701
Supplemental Table S6 Primers used for vector construction 702
703
Acknowledgments 704
This research was supported by the National Key Research and Development 705
Program (2016YFD0400101) the Project of the Science and Technology Department 706
of Zhejiang Province (2016C04001) and the 111 Project (B17039) 707
708
Figure legends 709
Figure 1 Changes in furanone content and furanone biosynthetic genes during 710
strawberry (Fragaria times ananassa Duch cv Yuexin) fruit development and ripening 711
A Fruits were collected at four ripening stages G (green stage) T (turning stage) IR 712
(intermediate red stage) R (full red stage) B Changes in the contents of furaneol 713
(HDMF) and mesifurane (DMMF) HDMF content was calculated using a standard 714
curve of HDMF while DMMF content was calculated with an internal standard as the 715
reference C Expression levels of FaQR and FaOMT The expression levels of each 716
gene were calculated relative to corresponding values in the basal section at the R 717
stage SEs were calculated from three replicates and LSD values represent the least 718
significant differences at p = 005 719
Figure 2 Regulatory effects of FaAP2ERF on the promoter of FaQR LUCREN 720
values of the empty vector on FaQR promoter were used as the calibrator set as 1 721
and SEs were calculated from five replicates statistical significance was determined 722
by Studentrsquos two-tailed t test ( plt0001) 723
Figure 3 Expression and the subcellular localization of FaERF9 A The expression 724
levels were calculated relative to the levels in the basal section at the R stage B 725
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
26
Subcellular localization analysis was performed in tobacco leaves The tobacco used 726
in the assay was stably transformed with a specific nucleus localized red fluorescence 727
protein construct and the red fluorescence indicates the nucleus-localized signal 728
(NLS) Scale bar = 25 microm SEs were calculated from three replicates 729
Figure 4 Transient overexpression of FaERF9 in strawberry fruit A Relative 730
expression of FaQR and FaERF9 in FaERF9-OX fruit 7 days after infiltration The 731
expression was calculated relative to the average value in control (SK) fruits B 732
HDMF and DMMF content in FaERF9-OX fruit The content of both furanones 733
were quantified using the peak area of the internal standard (2-octanol) as the 734
reference SEs were calculated from three replicates Statistical significance was 735
determined by Studentrsquos two-tailed t test ( plt005 plt001 plt0001) 736
Figure 5 Scatter plots of 11 strawberry cultivars A Linear regression analysis 737
between FaERF9 expression and FaQR expression B Linear regression analysis 738
between FaERF9 expression and furanone content The relative expression was 739
normalized to that of the housekeeping gene FaRIB413 and furanone content was 740
calculated with internal standard as the reference Significant differences were 741
determined by SPSS Statistics 200 742
Figure 6 Interactions of FaERF9 and FaMYB98 with the FaQR promoter A Yeast 743
one-hybrid analysis of the interaction of FaERF9 and FaQR promoter B Yeast 744
one-hybrid analysis of the interaction of FaMYB98 and FaQR promoter C 745
Regulatory effect of FaMYB98 on the FaQR promoter Auto-activation was tested on 746
SD-Ura (synthetically defined medium without uracil) in presence of Aureobasidin A 747
(AbA) and physical interaction was determined on SD-Leu (synthetically defined 748
medium without leucine) in presence of AbA LUCREN values of the empty vector 749
on FaQR promoter were used as the calibrator set as 1 and error bars were calculated 750
from five replicates Statistical significance was determined by Studentrsquos two-tailed t 751
test ( plt005 plt001 plt0001) 752
Figure 7 Electrophoretic mobility shift assay of FaMYB98 binding to FaQR 753
promoter A The probe sequence used for EMSA and mutated nucleotides are 754
indicated with lowercase letters B Purified DNA-binding domain of FaMYB98 755
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
27
protein and biotin-labelled DNA probe were mixed and analysed on 6 native 756
polyacrylamide gels and then photographed Presence or absence of specific probes is 757
marked by the symbol + or - 758
Figure 8 The combined activation effects of FaERF9FaMYB98 on the FaQR 759
promoter LUCREN values obtained with the empty vector and FaQR promoter were 760
used as the calibrator set as 1 and error bars were calculated from five replicates 761
Figure 9 Yeast two-hybrid analysis of the protein-protein interactions between 762
FaMYB98 and FaERF9 Positive interactions were determined by the growth of 763
yeast cells on selection plates Bait with pOST acted as positive controls and bait with 764
pPR3 as negative controls DDO synthetically defined medium without tryptophan 765
and leucine QDO synthetically defined medium without tryptophan leucine 766
histidine and adenine QDO+3AT QDO medium supplemented with 1 mM 767
3-aminotriazole 768
Figure 10 BiFC analysis of the protein-protein interactions between FaMYB98 and 769
FaERF9 The pairs of fusion proteins tested were FaMYB98-YFPN+FaERF9-YFPC 770
FaERF9-YFPN+FaMYB98-YFPC FaMYB98-YFPN+FaMYB98-YFPC and 771
FaERF9-YFPN+FaERF9-YFPC The other combinations were negative controls 772
The tobacco used in the assay was stably transformed with a specific 773
nucleus-localized red fluorescence protein construct and the red fluorescence 774
indicated the nucleus-localized signal (NLS) Fluorescence of the yellow fluorescence 775
protein (YFP) visualized the interaction in vivo Scale bar = 25 microm 776
777
Literature Cited 778
779
Agarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression 780
of PgDREB2A transcription factor enhances abiotic stress tolerance and activates 781
downstream stress-responsive genes Mol Biol Rep 37 1125-1135 782
Araguumlez I Osorio S Hoffmann T Rambla JL Medina-Escobar N Granell A 783
Botella MAacute Schwab W Valpuesta V (2013) Eugenol production in achenes and 784
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28
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Plant Physiol 163 946-958 786
Carvalho RF Carvalho SD OrsquoGrady K Folta KM (2016) Agroinfiltration of 787
strawberry fruit mdash a powerful transient expression system for gene validation Curr 788
Plant Biol 6 19-37 789
Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic 790
(Amsterdam) 210 34-40 791
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating 792
RNA from pine trees Plant Mol Biol Rep 11 113-116 793
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC 794
Clark DG (2011) PhMYB4 fine-tunes the floral volatile signature of 795
Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143 796
Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz 797
EA Taylor MG Smits-Kroon MT Schuurink RC Haring MA Giovannoni J 798
Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic 799
pathway by ectopic expression of a MYB transcription factor in tomato fruit Plant 800
Cell 23 2738-2753 801
Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan 802
XW Yang ZY (2017) Differential responses of four biosynthetic pathways of 803
aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under 804
interaction of light and temperature Food Chem 221 356-364 805
Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of 806
differentially-expressed genes during somatic embryogenesis in Fragaria times 807
ananassa Duch lsquoBenihopprsquo J Hortic Sci Biotechnol 90 671-681 808
Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 809
transcriptionally regulates chilling-induced lignification of loquat fruit via physical 810
interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136 811
Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM 812
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proteins Plant J 39 513-526 814
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29
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) 815
Sucrose nonfermenting1-related protein kinase26 an ortholog of open stomata1 is 816
a negative regulator of strawberry fruit development and ripening Plant Physiol 817
167 915-930 818
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene 819
expression in strawberry fruit (Fragaria times ananassa) by agroinfiltration a rapid 820
assay for gene function analysis Plant J 48 818-826 821
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of 822
selected aroma-active compounds in strawberries by headspace solid-phase 823
microextraction gas chromatography and correlation with sensory descriptive 824
analysis J Food Sci 72 S487-S496 825
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid 826
plays an important role in the regulation of strawberry fruit ripening Plant Physiol 827
157 188-199 828
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of 829
NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes BMC 830
Plant Biol 6 20 831
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN 832
(2005) MYB98 is required for pollen tube guidance and synergid cell differentiation 833
in Arabidopsis Plant Cell 17 2981-2992 834
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional 835
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Agric Food Chem 55 6705-6711 837
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You 838
J-S Rohloff J Randall SK Alsheikh M (2012) Proteomic study of 839
low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ 840
in cold tolerance Plant Physiol 159 1787-1805 841
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional 842
characterization of four APETALA2-family genes (RAP26 RAP26L DREB19 843
and DREB26) in Arabidopsis Plant Mol Biol 75 107-127 844
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30
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon 845
J Gupta V (2013) An oxidoreductase from lsquoAlphonsorsquo mango catalyzing 846
biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494 847
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in 848
strawberries Z Lebensm-Unters Forsch 195 120-123 849
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X 850
(2015) Label-free quantitative proteomics to investigate strawberry fruit proteome 851
changes under controlled atmosphere and low temperature storage J Proteomics 852
120 44-57 853
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 854
cooperates with CitWRKY1 to participate in citric acid degradation via 855
up-regulation of CitAco3 J Exp Bot 68 3419-3426 856
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription 857
factor CitERF71 activates the terpene synthase gene CitTPS16 involved in the 858
synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938 859
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and 860
transcriptomic analysis of the AP2ERF superfamily in Vitis vinifera BMC 861
Genomics 11 719 862
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive 863
Factor (AP2ERF) transcription factors mediators of stress responses and 864
developmental programs New Phytol 199 639-649 865
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 866
interacting with EOBI negatively regulates fragrance biosynthesis in petunia 867
flowers New Phytol 215 1490-1502 868
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu 869
CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 in regulating 870
anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) 871
during anthocyanin biosynthesis Plant Cell Tissue Organ Cult 115 285-298 872
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31
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao 873
CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphate signaling and 874
homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597 875
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC 876
Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL 877
Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor 878
regulates eugenol production in ripe strawberry fruit receptacles Plant Physiol 168 879
598-614 880
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics 881
and volatile constituents of strawberry (cv Cigaline) during maturation J Agric 882
Food Chem 52 1248-1254 883
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS 884
(2012) Ethylene-responsive transcription factors interact with promoters of ADH 885
and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 886
63 6393-6405 887
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM 888
Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-Franco A 889
Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific 890
transcription factor FaDOF2 regulates the production of eugenol in ripe fruit 891
receptacles J Exp Bot 68 4529-4543 892
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) 893
Comparison and verification of the genes involved in ethylene biosynthesis and 894
signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44 895
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the 896
ERF gene family in Arabidopsis and rice Plant Physiol 140 411-432 897
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in 898
sour cherry and strawberry and the heterologous expression of CBF1 in strawberry 899
J Am Soc Hortic Sci 127 489-494 900
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech 901
JC Ohme-Takagi M Regad F Bouzayen M (2012) Functional analysis and 902
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32
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molecular bases of plant differential responses to ethylene BMC Plant Biol 12 190 904
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) 905
Methylpentoses are possible precursors of furanones in fruits Prikl Biokhim 906
Mikrobiol 28 123-127 907
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery 908
of synergid-expressed genes encoding filiform apparatus localized proteins Plant 909
Cell 19 2557-2568 910
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria 911
vesca L compared to those of cultivated berries Fragariatimes ananassa cv Senga 912
Sengana J Agric Food Chem 27 19-22 913
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W 914
Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of the strawberry 915
flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone 916
oxidoreductase Plant Cell 18 1023-1037 917
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L 918
Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim M Broun P Zhang 919
JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription 920
factors genome-wide comparative analysis among eukaryotes Science 290 921
2105-2110 922
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the 923
formation of 25-dimethyl-4-hydroxy-3(2H)-furanone in detached ripening 924
strawberry fruits J Agric Food Chem 46 1488-1493 925
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 926
25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in 927
strawberry fruits Phytochemistry 43 155-159 928
Schwab W (1998) Application of stable isotope ratio analysis explaining the 929
bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone in plants by a biological 930
maillard reaction J Agric Food Chem 46 2266ndash2269 931
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33
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) 932
Molecules 18 6936-6951 933
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products Recent Res Dev Phytochem 1 643-673 935
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL 936
Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJ Sims CA 937
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compositions a seasonal influence and effects on sensory perception PLoS One 9 939
e88446 940
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) 941
Identification phylogeny and transcript profiling of ERF family genes during 942
development and abiotic stress treatments in tomato Mol Genet Genomics 284 943
455-475 944
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) 945
CitAP210 activation of the terpene synthase CsTPS1 is associated with the 946
synthesis of (+)-valencene in lsquoNewhallrsquo orange J Exp Bot 67 4105-4115 947
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes 948
Dev Genes Evol 214 105-114 949
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K 950
Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the 951
key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151 952
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O Yu YX Shklarman E Ovadis M Vainstein A (2012) The R2R3-MYB-like 954
regulatory factor EOBI acting downstream of EOBII regulates scent production 955
by activating ODO1 and structural scent-related genes in petunia Plant Cell 24 956
5089-5105 957
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp 958
Bot 68 4407-4409 959
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla 960
JF Amaya I Giavalisco P Fernie AR Botella MA Valpuesta V (2015) Central 961
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34
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to ripening New Phytol 208 482-496 963
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 964
regulates fragrance biosynthesis in petunia flowers Plant Cell 17 1612-1624 965
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS 966
(2018) The potassium channel FaTPK1 plays a critical role in fruit quality 967
formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748 968
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) 969
Isolation cloning and expression of a multifunctional O-methyltransferase capable 970
of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma 971
compounds in strawberry fruits Plant J 31 755-765 972
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor 973
types their evolutionary origin and species distribution In A handbook of 974
transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular 975
Biochemistry 52 25-73 976
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of 977
odor (Buettner A Ed) Springer Cham 9-10 978
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS 979
(2014) Isolation classification and transcription profiles of the AP2ERF 980
transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271 981
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in 982
regulation of fruit quality Crit Rev Plant Sci 35 120-130 983
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ 984
Zhang SL Wu J (2017) Map-based cloning of the pear gene MYB114 identifies an 985
interaction with other transcription factors to coordinately regulate fruit 986
anthocyanin biosynthesis Plant J 92 437-451 987
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes 988
involved in regulating fruit ripening Plant Physiol 153 1280-1292 989
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
35
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) 990
Expression of ethylene response genes during persimmon fruit astringency removal 991
Planta 235 895-906 992
Zabetakis I Gramshaw JW Robinson DS (1999) 993
25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis and 994
biosynthesis-a review Food Chem 65 139-151 995
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci 996
Food Agric 74 421-434 997
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 998
an AP2ERF gene is a novel regulator of fruit lignification induced by chilling 999
injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1000
1325-1334 1001
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation 1002
classification and transcription profiles of the Ethylene Response Factors (ERFs) in 1003
ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215 1004
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML 1005
(2012) Genome-wide analysis of the AP2ERF superfamily in peach (Prunus 1006
persica) Genet Mol Res 11 4788-4809 1007
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and 1008
expression analysis of a CRTDRE-binding factor gene FaCBF1 from Fragaria times 1009
ananassa Acta Hortic 41 240-248 1010
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The 1011
Arabidopsis AP2ERF transcription factor RAP26 participates in ABA salt and 1012
osmotic stress responses Gene 457 1-12 1013
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B 1014
Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) Genome-wide 1015
analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic 1016
(Amsterdam) 123 73-81 1017
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF 1018
Valpuesta V Botella MA Granell A Amaya I (2012) Genetic analysis of 1019
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
36
strawberry fruit aroma and identification of O-methyltransferase FaOMT as the 1020
locus controlling natural variation in mesifurane content Plant Physiol 159 1021
851-870 1022
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Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphatesignaling and homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597
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Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS (2012) Ethylene-responsive transcription factors interact withpromoters of ADH and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 63 6393-6405
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Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-FrancoA Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific transcription factor FaDOF2 regulates the production ofeugenol in ripe fruit receptacles J Exp Bot 68 4529-4543
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Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) Comparison and verification of the genes involved in ethylenebiosynthesis and signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44
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Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) Identification phylogeny and transcript profiling of ERFfamily genes during development and abiotic stress treatments in tomato Mol Genet Genomics 284 455-475
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Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes Dev Genes Evol 214 105-114Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
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Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp Bot 68 4407-4409Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
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Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The Arabidopsis AP2ERF transcription factor RAP26 participatesin ABA salt and osmotic stress responses Gene 457 1-12
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Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Genome-wide analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic (Amsterdam) 123 73-81Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF Valpuesta V Botella MA Granell A Amaya I (2012) Geneticanalysis of strawberry fruit aroma and identification of O-methyltransferase FaOMT as the locus controlling natural variation inmesifurane content Plant Physiol 159 851-870
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
4
Abstract 77
4-Hydroxy-25-dimethyl-3(2H)-furanone (HDMF) is a major contributor to the aroma 78
of strawberry (Fragaria times ananassa) fruit and the last step in its biosynthesis is 79
catalysed by Fragaria times ananassa quinone oxidoreductase (FaQR) Here an ethylene 80
response factor (FaERF9) was characterized as a positive regulator of the FaQR 81
promoter Linear regression analysis indicated that FaERF9 transcript levels were 82
significantly correlated with both FaQR transcripts and furanone content in different 83
strawberry cultivars Transient overexpression of FaERF9 in strawberry fruit 84
significantly increased FaQR expression and furaneol production Yeast one-hybrid 85
assays however indicated that FaERF9 by itself did not bind to the FaQR promoter 86
An MYB transcription factor (FaMYB98) identified in yeast one-hybrid screening of 87
the strawberry cDNA library was capable of both binding to the promoter and 88
activating the transcription of FaQR by ~56-fold Yeast two-hybrid assay and 89
bimolecular fluorescence complementation confirmed a direct protein-protein 90
interaction between FaERF9 and FaMYB98 and in combination they activated the 91
FaQR promoter 14-fold in transactivation assays These results indicate that an 92
ERF-MYB complex containing FaERF9 and FaMYB98 activates the FaQR 93
promoter and upregulates HDMF biosynthesis in strawberry 94
95
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5
Introduction 96
Strawberry (Fragaria times ananassa) is an economically important globally popular 97
and attractive fruit with nutritional benefits for human health An important feature of 98
its appeal is a unique fragrance with more than 360 different volatile compounds 99
detected in ripe fruit (Meacutenager 2004 Jetti et al 2007) These volatiles include 100
alcohols organic acids aldehydes terpenes lactones esters aromatic hydrocarbons 101
furans and others (Zabetakis and Holden 1997) Sensory evaluation indicates that 102
terpenes confer on strawberry a ldquofresh orangerdquo smell aldehydes generate a ldquoherbal 103
flavourrdquo γ -decalactone is ldquopeach-likerdquo esters are ldquofruityrdquo and 104
4-hydroxy-25-dimethyl-3(2)H-furanone (HDMF) and 105
25-dimethyl-4-methoxy-3(2)H-furanone (DMMF) generate a ldquocaramel-likerdquo aroma 106
(Pyysalo et al 1979 Larsen and Poll 1992) HDMF and DMMF belong to an 107
uncommon group of chemicals with a 25-dimethyl-3(2H)-furanone structure and 108
such compounds possess special odour properties (Schwab and Roscher 1997) They 109
are found at trace levels in various fruits including raspberry some grape cultivars 110
and tomato They are particularly abundant in strawberry and pineapple (Schwab 111
2013 Wuumlst 2017) HDMF is one of the most important volatiles distinguishing 112
strawberry from other fruits (Larsen and Poll 1992 Schwab and Roscher 1997) and 113
is significantly correlated with perceived strawberry fruit intensity (Schwieterman et 114
al 2014) Thus strawberry is an important model for investigating the regulation of 115
furaneol biosynthesis and knowledge of the factors controlling its synthesis is highly 116
desirable for targeting flavor improvement 117
118
HDMF and its methyl ether DMMF have been extensively investigated in research 119
on flavour analyses chemical synthesis and natural product formation in both 120
microbes and plants (Zabetakis et al 1999 Schwab 2013) The first plant studies on 121
the biosynthesis of HDMF used strawberry fruit to investigate potential precursors of 122
furaneol biosynthesis (Pisarnitskii et al 1992) and D-fructose-16-diphosphate was 123
identified as the natural precursor of HDMF and DMMF (Roscher et al 1998 124
Schwab 1998) The immediate precursor of HDMF in strawberry was shown to be 125
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6
4-hydroxy-5-methyl-2-methylene-3(2H)-furanone (HMMF) and Fragaria times 126
ananassa quinone oxidoreductase (FaQR later renamed as FaEO) was identified as 127
the enzyme responsible for reduction of the α β-unsaturated bond of HMMF to form 128
the aroma-active compound HDMF (Raab et al 2006 Klein et al 2007) An 129
O-methyltransferase FaOMT subsequently generates DMMF by methylation of 130
HDMF (Wein et al 2002) HDMF can also be metabolized to 131
25-dimethyl-4-hydroxy-2H-furan-3-one glucoside (HDMF-glucoside) by a 132
UDP-dependent glycosyltransferase (UGT71K3) and further malonylated into 133
25-dimethyl-4-hydroxy-2H-furan-3-one 6rsquo-O-malonyl-β-D-glucopyranoside (HDMF 134
malonyl-glucoside) in strawberry fruit (Roscher et al 1996 Song et al 2016) The 135
biosynthetic pathway of HDMF in other plants is similar to that in strawberry Genes 136
with homology to FaQR have been identified in tomato (SlEO) and mango (MIEO) 137
(Klein et al 2007 Kulkarni et al 2013) 138
139
As an NADH-dependent enone oxidoreductase protein FaQR exhibits o-quinone 140
oxidoreductase activity (Raab et al 2006) FaQR mRNA accumulates in fruit 141
parenchyma tissues but is absent in vascular tissues and FaQR is mainly expressed in 142
the late stages of fruit growth and ripening paralleling furaneol production in the fruit 143
(Raab et al 2006) FaQR is responsive to environmental stimuli associated with 144
furaneol production and in the dark lsquoSweet Charliersquo strawberry fruits have higher 145
levels of FaQR expression and HDMF production at 25degC than at 15degC (Fu et al 146
2017) in contrast the concentration of furanones and the abundance of FaQR protein 147
under low-temperature storage is significantly lower than those under 148
room-temperature storage (Li et al 2015) Thus the regulation of FaQR is important 149
for manipulating furaneol content Although it is assumed that transcription factors 150
control expressions of genes involved in volatile production in plants no such factors 151
regulating FaQR or other furanone biosynthetic genes have been identified 152
153
Different members of the largely plant-specific AP2ERF gene family (Weirauch and 154
Hughes 2011) have diverse functions in plant growth development and stress 155
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
7
responses (Agarwal et al 2010 Zhu et al 2010 Licausi et al 2013) In recent years 156
several AP2ERF genes have been reported to regulate aspects of fruit quality (Xie et 157
al 2016) including fruit aroma For example CitAP210 is associated with the 158
synthesis of (+)-valencene in Newhall orange acting via regulation of CsTPS1 (Shen 159
et al 2016) CitERF71 was shown to physically bind to the CsTPS16 promoter and 160
contribute to the synthesis of E-geraniol in citrus fruit (Li et al 2017) These 161
observations raised the possibility that FaQR might also be a target for a member of 162
the AP2ERF family and that ERFs might also control furaneol biosynthesis 163
164
In this study screening of the Fragaria times ananassa AP2ERF gene family led to 165
identification of FaERF9 as an activator of FaQR however it did not bind directly 166
to the promoter A parallel search for proteins that directly bind the FaQR promoter 167
using yeast one-hybrid screening identified a second factor FaMYB98 which was 168
capable of physically interacting with the FaQR promoter FaMYB98 physically 169
interacts with FaERF9 and transient expression assays demonstrated a synergistic 170
effect on FaQR expression and furanone synthesis 171
172
Results 173
Changes in the content of both furanones and the activity of their biosynthetic 174
genes in strawberry fruit 175
lsquoYuexinrsquo fruits at four developmental and ripening stages (G green T turning IR 176
intermediate red R full red) were harvested (Figure 1) and determination of HDMF 177
levels indicated a major increase from about 065 μg per gram fruit at the IR stage to 178
346 μg at the R stage in the apical section implying that furaneol accumulation was 179
closely related to colour change and ripening (Figure 1) Furaneol levels were higher 180
in the apical section than in the basal section HDMF could not be detected at the IR 181
stage in the basal section but the amount increased at the R stage to 142 μg per gram 182
fruit Differences were also found for DMMF with the relative content in the apical 183
section 018 μg per gram at the R stage compared to 008 μg per gram in the basal 184
section at the same stage 185
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8
186
Measurement of mRNA levels by RT-qPCR indicated that the transcript levels of both 187
FaQR (GenBank AY1588361) and FaOMT (GenBank AF2204912) increased 188
throughout ripening (Figure 1) Comparison of the expression of these genes showed 189
that the transcript levels of FaQR and FaOMT significantly increased as early as in T 190
stage in basal fruit sections and for each gene over half of the peak transcript 191
abundance occurred as early as in IR stage in the apical section while for the basal 192
section it was in the R stage indicating a gradient of gene expression and volatile 193
production from apex to base of the fruit during ripening 194
195
Genome-wide identification of AP2ERF gene family in strawberry 196
Coding sequences of 120 non-redundant FaAP2ERF genes were isolated and 197
identified from lsquoYuexinrsquo strawberry and a systematic nomenclature for the AP2ERF 198
family genes was used to distinguish the members based on the structural features 199
defined previously (Supplemental Table S1) (Shigyo and Ito 2004 Nakano et al 200
2006 Licausi et al 2013) CD-search analysis showed that this superfamily is 201
consisted of 95 ERFs 18 AP2 and 6 RAV family members and 1 soloist member 202
(Supplemental Table S2) Phylogenetic analysis of the Fragaria times ananassa and 203
Arabidopsis AP2ERF members is shown in Supplemental Figure S1 with the 120 204
AP2ERF genes divided into three major groups (ERF AP2 RAV) and a soloist and 205
the ERF family being further divided into 10 groups (groups I to X in Supplemental 206
Table S1) 207
208
We performed a dual-luciferase assay to determine the ability of 116 FaAP2ERF 209
members to activate transcription from the promoter of FaQR The results indicated 210
about 12 members (mainly belonging to the ERF and RAV families) showed a 211
significant activation effect on the FaQR promoter while the remaining members 212
showed very limited effects (Figure 2) The relative activity of only the following 12 213
FaAP2ERF transcripts reached the threshold value set at 2 FaERF8FaERF9 214
(group II) FaERF27FaERF29FaERF31FaERF32 (group IV) 215
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9
FaERF37FaERF38 (group V) FaERF62FaERF64 (group VIII) FaERF68 216
(group IX) and FaRAV4 (Figure 2) Of these FaERF9 exhibited the highest 217
activation effect on the FaQR promoter (466-fold) (Figure 2) The strawberry 218
FaERF9 cDNA is 699 bp long and ExPASy Compute pIMw tool analysis indicated 219
that this gene encodes a 232-amino acid protein with a calculated molecular mass of 220
254 KD and a pI of 56 221
222
FaERF9 expression pattern and subcellular localization 223
To further explore the connections between AP2ERFs and furaneol biosynthesis we 224
obtained the transcript profiles of the AP2ERF genes in strawberry fruit samples at 225
different fruit developmental and ripening stages by reverse transcription quantitative 226
PCR (RT-qPCR) excluding genes with very low abundance in the fruit samples The 227
results presented as a heatmap (Supplemental Figure S2) demonstrate that these 228
genes displayed various expression patterns in both the apical and basal sections and 229
by analysing the expression patterns of the members indicated as activators in the 230
dual-luciferase assay we found that only a few genes including FaERF8 FaERF9 231
FaERF27 FaERF32 and FaERF37 were up-regulated during ripening stages and 232
their expression correlated with furaneol accumulation in the fruit (Figure 1) 233
Furthermore the expression patterns of the up-regulated genes in the apical and basal 234
sections showed that one ERF gene FaERF9 not only showed an up-regulation 235
pattern in both sections but its expression in the apical section occurred ahead of that 236
in the basal section (Figure 3) consistent with the actual changes in furaneol content 237
(Figure 1) and the expression pattern of FaQR (Figure 1) The subcellular localization 238
of FaERF9 was predicted to be in the nucleus using the WoLF PSORT program In 239
experimental tests 35S-FaERF9-GFP (green fluorescence protein) showed strong 240
fluorescence in the nucleus and the green signal merged with the red fluorescence 241
signal of mCherry-nucleus-marker in tobacco plants (Figure 3) 242
243
Transient overexpression of FaERF9 in strawberry 244
The expression of FaERF9 in agro-infiltrated fruits was analysed by performing 245
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10
RT-qPCR on the seventh day after infiltration by which time they had reached the IR 246
or R stage and the result showed that the transcript levels were significantly higher 247
(52-fold) than in control fruits (Figure 4) The expression of FaQR was examined in 248
the same fruits and the transcript abundance also increased 22-fold The relative 249
content of HDMF in the FaERF9-overexpressing fruits was 008 μg per gram fruit 250
and undetectable in the control fruits (Figure 4) The relative content of DMMF in the 251
overexpressing fruits was also significantly increased to 038 μg per gram fruit 252
compared to 004 μg per gram fruit in the control (Figure 4) These observations 253
provide direct evidence for a regulatory role for FaERF9 in promoting FaQR 254
biosynthesis and activity in ripening strawberry fruit Taken together these results 255
indicate that by activating the transcription of FaQR FaERF9 functions as a positive 256
regulator in furaneol biosynthesis 257
258
Correlation of FaERF9 expression and FaQR transcript profiles 259
GC-MS quantification showed that furanones are distributed in variable levels among 260
different strawberry cultivars (Supplemental Figure S3) The transcript profiles of 261
FaQR and FaERF9 in fruits of different cultivars were measured and linear 262
regression analysis was performed In the cultivars the changes in FaQR transcripts 263
correlated positively with those in FaERF9 transcripts (r = 079 plt001) (Figure 5) 264
In addition FaERF9 transcript levels also correlated with furanone content across 265
cultivars (Figure 5) 266
267
FaERF9 is an indirect regulator of the FaQR promoter and acts via 268
protein-protein interaction with FaMYB98 269
Although the results of the dual-luciferase assay expression analysis transient 270
overexpression and correlation analysis were all consistent with the suggestion that 271
FaERF9 regulates transcript abundance by acting on the FaQR promoter a yeast 272
one-hybrid assay indicated that FaERF9 cannot bind directly to the FaQR promoter 273
(Figure 6) This led us to speculate that activation may occur via a transcription 274
complex involving an additional as-yet unknown regulator which can bind directly to 275
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11
the FaQR promoter 276
277
In parallel with the investigation of the FaAP2ERF genes a cDNA library screening 278
was performed with a yeast one-hybrid assay using the promoter of FaQR as the bait 279
This screen identified several transcription factors that could physically bind to the 280
FaQR promoter but only one MYB could activate transcription from the FaQR 281
promoter (approximately 56-fold) relative to the control (Figure 6) in the 282
dual-luciferase assay This MYB showed 44 amino acid identity with MYB98 283
(GenBank ABA420611) a transcriptional regulator in the synergid cells in 284
Arabidopsis (Kasahara et al 2005) and it was designated as FaMYB98 The 285
specificity of FaMYB98 binding to the FaQR promoter was confirmed by EMSA 286
assay (Figure 7) and increasing the concentration of the cold probe reduced binding 287
In addition mutating the putative binding sites (Goacutemez-Maldonado et al 2004 288
Punwani et al 2007) as shown in Figure 7 eliminated FaMYB98 protein binding 289
When the combined effect of FaERF9 and FaMYB98 was analysed (Figure 8) a 290
synergistic 14-fold activation of the FaQR promoter was observed compared with the 291
activation by either FaERF9 or FaMYB98 which alone promoted transactivation 292
39-fold and 45-fold respectively In addition overexpression of both genes 293
(FaERF9-FaMYB98-SK) in strawberry fruits resulted in higher expression of 294
FaERF9 transcripts and higher furanone content than overexpression of FaERF9 295
(Supplemental Figure S4 Supplemental Table S3) Subcellular localization analysis 296
revealed that FaMYB98 was also localized in the nucleus (Supplemental Figure S5) 297
298
To investigate the potential interactions between FaERF9 and FaMYB98 the 299
DUALhunter system was used (Figure 9) Cells expressing the FaMYB98 and 300
FaERF9 protein pair using either FaMYB98 or FaERF9 as the bait grew on DDO 301
QDO and QDO supplemented with 1 mM 3-AT selective medium indicating 302
interaction between the two proteins This putative protein-protein interaction was 303
confirmed by BiFC assay and the combinations of FaMYB98-YFPNFaERF9-YFPC 304
and FaERF9-YFPNFaMYB98-YFPC exhibited strong coincident signals in the 305
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12
nucleus while negative controls produced no detectable fluorescence signal (Figure 306
10) In addition coexpression of FaERF9-YFPNFaERF9-YFPC as well as 307
FaMYB98-YFPNFaMYB98-YFPC also generated signals in the nucleus indicating 308
that FaERF9 and FaMYB98 both could form homodimers or possibly multimers in 309
the nucleus (Figure 10) 310
311
Discussion 312
The AP2ERF superfamily in strawberry 313
The AP2ERF superfamily of plant transcription factors is defined by the AP2ERF 314
domain and comprises the ERF AP2 and RAV families as well as one soloist member 315
(Riechmann et al 2000 Weirauch and Hughes 2011) The completion of multiple 316
plant genome sequences has enabled a genome-scale analysis of the AP2ERF family 317
which in recent years has been systematically studied in diverse fruit species such as 318
tomato grape peach and kiwi fruit (Zhuang et al 2009 Sharma et al 2010 Licausi 319
et al 2010 Yin et al 2010 Pirrello et al 2012 Zhang et al 2012 Zhang et al 320
2016) A few AP2ERF genes have been isolated and characterized in strawberry and 321
CBF orthologs (Owens et al 2002 Koehler et al 2012 Zhang et al 2014) have 322
been identified from different strawberry cultivars in several independent studies 323
Although they have distinct names eg Fragaria times ananassa CBF1 (FaCBF1) 324
FaCBF4 (GenBank HQ9105151) and CBF1 (GenBank EU1172142) according to 325
the phylogenetic tree generated in this study the orthologs of 326
CBF1CBF4CBF2CBF3 in Arabidopsis are similar to each other and to FaERF20 327
(Supplemental Figure S1) (Owens et al 2002 Koehler et al 2012 Zhang et al 328
2014) FaERF20 has 85 sequence similarity with FaCBF1 identified by Owens et 329
al (2002) 93 similarity with FaCBF4 amplified by Koehler et al (2012) and 75 330
similarity with CBF1 cloned by Zhang et al (2014) The AP2ERF genes 331
characterized in other studies (Jia et al 2011 GAO et al 2015 Chai and Shen 2016 332
Mu et al 2016) are also noted in Supplemental Table S1 333
334
Based on the computational analysis we have identified a total of 120 AP2ERF 335
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13
genes in octoploid strawberry (Supplemental Table S1) The number of predicted 336
AP2ERF genes (120) is comparable to those observed in other fruits including 337
tomato (112) Chinese plum (116) citrus (126) and peach (131) but lower than those 338
reported for grape (149) (Xie et al 2016) As shown in Supplemental Table S2 79 339
(95 genes) of the AP2ERF genes belong to the ERF family in strawberry constituting 340
the largest sub-family The members of this sub-family can be classified into 10 341
groups (group I to X) according to their sequence similarities to the Arabidopsis ERF 342
genes (Nakano et al 2006) The AP2 family encompasses the same number of genes 343
in Arabidopsis citrus and strawberry (eighteen) (Nakano et al 2006 Xie et al 2014) 344
and there are six RAV genes in strawberry which are highly conserved in dicots such 345
as Vitis vinifera Arabidopsis thaliana and Populus trichocarpa (Licausi et al 2010) 346
347
Role of FaERF9 in regulating the biosynthesis of HDMF a positive regulator 348
acting in an indirect manner 349
The large-scale screening of the AP2ERF superfamily in strawberry led to 350
identification of 11 ERFs and 1 RAV that trans-activated the FaQR promoter more 351
than two-fold with the highest activation caused by FaERF9 which trans-activated 352
the FaQR promoter (Figure 2) as well as up-regulating FaQR expression and furanone 353
production in transient overexpression assays (Figure 4) which has been extensively 354
used to explore the fruit-associated gene functions in strawberry (Han et al 2015 355
Medina-Puche et al 2015 Vallarino et al 2015 Carvalho et al 2016 Song et al 356
2016 Wang et al 2018) FaERF9 transcripts accumulate in the fruit apical section 357
before the basal section (Figure 3) a finding consistent with the actual changes in 358
furaneol content (Figure 1) and the expression of FaQR (Figure 1) The association 359
between FaERF9 transcripts and accumulation of furanones were also established 360
with different strawberry cultivars The correlation between FaERF9 and FaQR 361
expression as well as furanone content among cultivars supports a positive role of 362
FaERF9 in regulating furanone content (Figure 5) These results indicate that 363
FaERF9 transcript abundance may be a good indicator of the abundance of these 364
important flavour volatiles in fruits of different cultivars This should be considered as 365
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14
a method for high-throughput variety screening to replace direct measurement of 366
volatiles 367
368
FaERF9 is a member of the ERF group II family and is most closely related to the 369
Arabidopsis genes At1g44830 (ATERF014) At1g21910 (DREB26) and At1g77640 370
(Supplemental Figure S1) At1g44830 was observed to be strongly up-regulated in a 371
comprehensive microarray analysis of the root transcriptome following NaCl 372
exposure (Jiang and Deyholos 2006) At1g21910 (DREB26) was functionally 373
characterized as a trans-activator localized in the nucleus exhibiting tissue-specific 374
expression and participating in plant developmental processes as well as biotic andor 375
abiotic stress signalling (Krishnaswamy et al 2011) However none of these genes 376
have been reported as furanone regulators In strawberry another five genes 377
(FaERF6 FaERF7 FaERF8 FaERF10 and FaERF11) also belong to the same 378
group with FaERF8 also showing somewhat weaker activation activity towards the 379
FaQR promoter than FaERF9 The fact that FaERF9 could not bind directly to the 380
promoter of FaQR (Figure 6) indicates that it might function as an indirect regulator 381
of FaQR and furaneol biosynthesis 382
383
A FaERF9 and FaMYB98 complex is involved in regulating FaQR and furaneol 384
biosynthesis 385
The finding that FaERF9 could interact with FaMYB98 protein (Figures 9 and 386
Figure 10) and that FaMYB98 could physically bind to the FaQR promoter (Figure 6 387
and Figure 7) provides evidence for a regulatory mechanism whereby FaERF9 388
regulates FaQR and furaneol production as part of a complex with an MYB 389
transcription factor Since co-overexpression of FaERF9 and FaMYB98 resulted in 390
much higher activation activity towards FaQR we speculate that FaERF9 may 391
recruit FaMYB98 homologs in tobacco to activate the FaQR promoter (Figure 8) 392
FaOMT is another key gene for furanone biosynthesis and a potential target for 393
transcriptional activation However FaERF9 did not significantly activate the 394
FaOMT promoter in a dual-luciferase assay and the transcript level of FaOMT in the 395
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15
FaERF9-overexpressing fruits showed no significant difference from that in the 396
control (Supplemental Figure S6 Supplemental Figure S7) The FaOMT promoter 397
was significantly induced by FaMYB98 but no synergistic effect of FaERF9 and 398
FaMYB98 on the promoter was observed (Supplemental Figure S6) In previous 399
studies of the regulation of plant volatile compounds MYBs have been characterized 400
as being involved mainly in the regulation of the benzenoidphenylpropanoid pathway 401
that produces floral volatiles in petunia and eugenol in ripe strawberry fruit (Verdonk 402
et al 2005 Dal Cin et al 2011 Colquhoun et al 2011 Spitzer-Rimon et al 2012 403
Medina-Puche et al 2015) but their role in formation of volatiles from other 404
pathways has not been reported Our study demonstrates a role for MYB in the 405
synthesis of furaneol a carbohydrate-derived volatile compound and reveals the 406
synergistic interactions between an MYB and ERF in a transcription complex (Figure 407
8 Figure 9 and Figure 10) 408
409
Recent research has provided evidence for interactions between AP2ERF and MYB 410
transcription factors in regulating other aspects of fruit quality including texture 411
(EjAP2-1 and EjMYB Zeng et al 2015) and colour (PyERF3 and PyMYB114 Yao 412
et al 2017) A group VIII ERF has also recently been shown to interact with an MYB 413
to regulate floral scent production in petunia (Liu et al 2017) In strawberry fruit 414
DOF in combination with an MYB has been reported to be involved in the regulation 415
of eugenol production and the identification of this second transcription factor (DOF) 416
suggests that it is a good target in breeding for improved flavour (Molina-Hidalgo et 417
al 2017 Tieman 2017) Considering its important contribution to flavour in 418
strawberry and many other highly valued fruit crop species (pineapple tomato mango 419
etc) very little is known about regulation of furaneol synthesis Here we established 420
the role of FaERF9 in the regulation of HDMF synthesis by direct protein-protein 421
interactions with FaMYB98 to synergistically trans-activate FaQR The functional 422
identification of this complex enhances our knowledge of the regulation of volatile 423
compound synthesis and identifies a new AP2ERF-MYB complex Further 424
examination of the other ERFs that stimulated transcription from the FaQR promoter 425
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16
(Figure 2) may provide additional information about the complexity of this regulation 426
Overall this study provides important clues for understanding the transcriptional 427
regulation of HDMF synthesis and identifies specific transcription factors that are 428
likely to be good targets for molecular breeding for improved flavour 429
430
Conclusions 431
Screening of the AP2ERF superfamily in strawberry (Fragaria times ananassa) 432
identified candidate members capable of activating the FaQR promoter An ERF 433
transcription factor was identified as a positive regulator of HDMF synthesis in 434
strawberry fruit and the mechanism of activation was shown to involve an ERF-MYB 435
transcription complex that regulates transcription of FaQR leading to the biosynthesis 436
of HDMF the characteristic volatile compound which has a major influence on 437
strawberry aroma 438
439
Materials and Methods 440
441
Plant Materials and Growth conditions 442
The strawberry (Fragaria times ananassa cv lsquoYuexinrsquo an octoploid cultivar) fruit used in 443
this study were bred by Zhejiang Academy of Agricultural Sciences (Haining 444
Zhejiang) Fruits at various developmental and ripening stages including G (green) T 445
(turning) IR (intermediate red) and R (full red) were harvested (Figure 1) and 446
transported to the laboratory within 2 h Thirty-six fruits of uniform size and free of 447
visible defects were selected at each stage with twelve fruits in each biological 448
replicate After removing the calyces fruits were then divided into the basal and 449
apical sections which were sampled separately (Figure 1) They were rapidly cut into 450
pieces frozen immediately in liquid nitrogen and stored at -80deg C until use Red ripe 451
fruits of different strawberry cultivars (Fragaria times ananassa octoploid cultivars) 452
including lsquoYuelirsquo lsquoBenihoppersquo lsquoMengxiangrsquo lsquoAmaoursquo lsquo10-1-4rsquo lsquoAkihimersquo lsquoSweet 453
Charliersquo lsquo07-1-4rsquo lsquoDarselectrsquo lsquoYuexinrsquo and lsquoXuemeirsquo were also provided by Zhejiang 454
Academy of Agricultural Sciences For each cultivar the fruits of three biological 455
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17
replicates were sampled frozen in liquid nitrogen and stored at -80deg C for further use 456
457
Tobacco plants (Nicotiana benthamiana) used for dual-luciferase assays and 458
subcellular localization analysis in this study were grown in a growth chamber with a 459
lightdark cycle of 16 h8 h at 24degC 460
461
Detection of DMMF and HDMF 462
Automated HS-SPME-GC-MS was performed to detect both furanones in lsquoYuexinrsquo 463
strawberry fruit (Zorrilla-Fontanesi et al 2012) Samples were ground into a powder 464
under liquid nitrogen for analysis 465
466
For the detection of DMMF (Figure 1) 05 g (fresh weight) of each sample was 467
weighed in the vial to which was added 1 mL of EDTA solution (100 mM pH 75) 1 468
mL of CaCl2 solution (mv = 20) and 20 microL of 2-octanol as the internal standard 469
(007 μgμL) The mixture was homogenized and the vial closed and placed on the 470
sample tray for analysis by CombiPAL autosampler (CTC Analytic CA USA) The 471
fruit volatiles were sampled by headspace solid-phase microextraction with a 65-μm 472
polydimethylsiloxane-divinylbenzene fibre (PDMS-DVB) Initially vials were 473
pre-incubated at 50degC for 10 min under continuous agitation (500 rpm) then volatiles 474
were extracted for 30 min at the same temperature and agitation speed After that the 475
fibre was desorbed in the GC injection port for 5 min in splitless mode The 7890A 476
GC chromatograph was equipped with a DB-5ms column (60 m times 250 μm times 1 μm 477
JampW Scientific Folsom CA USA) with helium as the carrier gas at a constant flow 478
of 12 mLmin The GC was programmed at an initial temperature of 35degC for 2 min 479
with a ramp of 5degC min up to 250degC and held for 5 min The injection port interface 480
and MS source temperatures were 250degC 260degC and 230degC respectively The 481
ionization potential was set at 70 eV recorded by a 5975B mass spectrometer (Agilent 482
Technologies JampW Scientific Folsom CA USA) and the scanning speed was 7 483
scanss The same method was used to analyse HDMF and DMMF in fruits from 484
different cultivars (Supplemental Figure S3) except for the sample preparation 485
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18
procedure (Araguumlez et al 2013) briefly 05 g (fresh weight) of powdered fruit was 486
incubated at 30degC in a water bath for 5 min then 2 mL of NaCl (mv = 20) and 20 487
microL of 2-octanol as the internal standard (007 μgμL) were added and homogenized 488
489
For the detection of HDMF (Figure 1) and both furanones (Figure 4 and Supplemental 490
Table S3) a liquid-injection system equipped with CTC Pal ALS was used One gram 491
(fresh weight) of powdered fruit and 2 mL of NaCl (mv = 20) were homogenized in 492
a 10-mL tube and 300 μL of CH2Cl2 and 20 microL of 2-octanol (0766 μgμL) as the 493
internal standard were added to extract the volatiles the mixture was then 494
homogenized again The tubes were stored at room temperature for 20 min and 495
centrifuged at 12000 rpm for 5 min The subnatant was pipetted into a clean 15-mL 496
tube in which 20 mg of anhydrous sodium sulphate was added the tube was left 497
without shaking for half an hour Then 150 μL of the solution was transferred into a 498
GC vial and placed on the sample tray as described above Each sample (1 μL) was 499
injected using the autosampler and the analysis was accomplished by a 7890A 500
GC-MS system (Agilent Technologies JampW Scientific Folsom CA USA) equipped 501
with a DB-WAX column (30 m times 025 mm times 025 μm JampW) Helium (12 mLmin) 502
was used as a carrier gas The injection port (splitless injection mode) interface and 503
MS source temperatures were as described above The oven temperature was set at 504
60degC for 4 min then increased to 180degC at a rate of 4degCmin and maintained for 30 505
min DMMF was identified by comparison of electron ionization mass spectra and 506
retention time data with the data from the NISTEPANIH mass spectral library 507
(NIST-08 and Flavor) HDMF (Figure 1) was identified and qualified by comparison 508
with injected standard (Sigma) The quantitative analysis of both furanones (Figure 4 509
Supplemental Table S3 and Supplemental Figure S3) was determined using the peak 510
area of the internal standard as a reference based on total ion chromatogram (TIC) 511
512
RNA isolation and Reverse Transcription Quantitative PCR (RT-qPCR) 513
Total RNA from strawberry samples was isolated in this study using the CTAB 514
method (Chang et al 1993) Genomic DNA contamination was eliminated by 515
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
19
TURBO Dnase (Ambion) 1 μg of RNA was used to obtain cDNA using an IScriptTM 516
cDNA Synthesis Kit (Bio-Rad) The synthesized cDNA was diluted with water (120) 517
and 2 μL of diluted cDNA was used as the template for RT-qPCR Reactions were 518
performed in a total volume of 20 μL consisting of 10 μL of SYBR PCR supermix 519
(Bio-Rad) 1 μL of each primer (10 μM) 6 μL of DEPC-H2O and 2 μL of diluted 520
cDNA on CFX96 instrument (Bio-Rad) (Yin et al 2012) The oligonucleotide 521
primers for RT-qPCR analysis of genes including the AP2ERF FaQR and FaOMT 522
were designed according to the coding sequences of genes and the specificity was 523
verified before use (Min et al 2012) NCBIPrimer-BLAST was applied to design the 524
primers Relative expression levels were normalized to that of an internal controlmdashthe 525
interspacer 26S-18S strawberry RNA housekeeping gene FaRIB413 526
(Zorrilla-Fontanesi et al 2012) To investigate the differential expression of genes 527
during fruit development and ripening stages relative expression of each gene at the 528
R stage in the basal fruit section was set as 1 using the 2minus∆∆119862119879 method For transient 529
overexpression assay relative expression of control fruits with an empty vector (SK) 530
was set as 1 The primers used in RT-qPCR are listed in Supplemental Table S4 531
532
Gene isolation and analysis 533
Multiple database searches were performed to identify members of the strawberry 534
(Fragaria times ananassa) AP2ERF superfamily in the published strawberry databases 535
and annotations of Fragaria times ananassa and Fragaria times vesca by using the 536
AP2ERF DNA binding domain as a query sequence and 120 genes were identified 537
with AP2ERF domain(s) Based on the BLAST result primers (listed in 538
Supplemental Table S5) were used to amplify the coding full-length cDNAs of 539
AP2ERF genes The deduced amino acid sequences of AP2ERF proteins in 540
Arabidopsis thaliana used for construction of a phylogenetic tree were obtained from 541
the Arabidopsis Information Resource (TAIR) Alignment of the proteins was 542
performed using the neighbour-joining method in ClustalX (v181) and the 543
phylogenetic tree was constructed using FigTree (v131) 544
545
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
20
FaMYB98 was obtained by yeast one-hybrid screening sequencing and the full-length 546
sequences were predicted by BLAST Primers were designed (listed in Supplemental 547
Table S5) to amplify the full-length coding sequence 548
549
The promoter of FaQR was cloned by Genome Walking as previously described (Yin 550
et al 2010) and conserved cis-element motifs in the promoter were manually 551
searched 552
553
Conserved domains within the FaAP2ERF proteins and FaMYB98 were analysed by 554
CD-search (httpswwwncbinlmnihgovStructurecddwrpsbcgi) and cellular 555
locations of proteins including FaERF9 and FaMYB98 were predicted with the 556
WoLF PSORT program (httpswwwgenscriptcomwolf-psorthtml) 557
558
Dual-Luciferase Assays 559
In accordance with a previous protocol (Yin et al 2010) the full-length cDNAs of 560
FaAP2ERF or FaMYB98 transcription factors were cloned into pGreen II 0029 561
62-SK vector and the promoter of FaQR was cloned into pGreen II 0800-LUC vector 562
A luciferase gene from Renillia (REN) driven by a 35S promoter in the LUC vector 563
acted as a positive control The above constructs were transiently expressed in 564
Nicotiana benthamiana leaves by Agrobacterium-mediated infiltration (strain 565
GV3101) and the activity of the TFs on the promoter was measured on the third day 566
after infiltration indicated by the ratio of enzyme activities of firefly luciferase (LUC) 567
and renilla luciferase (REN) using a Modulus Luminometer (Promega Madison WI 568
USA) To determine the activity of a specific transcription factor towards the 569
promoter we mixed the Agrobacterium culture with 1 mL of TF and 100 μL of 570
promoter and the LUCREN value of the empty vector SK on the promoter was set as 571
1 as a calibrator To test the combined effect of two transcription factors on the 572
promoter to the Agrobacterium culture mixture we added 05 mL of each TF and 100 573
μL of promoter the effect of the mixtures that contained each transcription factor (05 574
mL) and empty vector SK (05 mL) was also tested on the promoter as a control 575
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
21
576
Subcellular localization analysis 577
35S-FaERF9-GFP and 35S-FaMYB98-GFP were transiently expressed in tobacco (N 578
benthamiana) leaves by Agrobacterium infiltration (EHA105) using the same method 579
as described in the dual-luciferase assay above The transiently infected leaves were 580
imaged on the third day after infiltration using a Nikon A1-SHS confocal laser 581
scanning microscope The excitation wavelength for GFP fluorescence was 488 nm 582
and fluorescence was detected at 490ndash520 nm The primers used for GFP construction 583
are listed in Supplemental Table S6 584
585
Transient overexpression in strawberry fruit 586
Transient overexpression of FaERF9 and an overexpression binary vector (pGreen II 587
0029 62-SK-FaERF9-FaMYB98) were performed in strawberry fruit using the 588
FaERF9-SK construct described above for the dual-luciferase assays and the binary 589
vector constructed according to Liu et al 2013 The transfection of fruit was carried 590
out at the G stage (Hoffmann et al 2006) The FaERF9-SK construct and binary 591
vector were individually electroporated into Agrobacterium tumefaciens GV3101 and 592
the Agrobacterium culture suspended in infiltration buffer was infiltrated into the 593
whole fruit using a syringe As a control treatment fruits were infiltrated with 594
Agrobacterium carrying an empty vector SK under the same transfection conditions 595
Fruits were left attached to the plants and harvested on the seventh day after 596
infiltration Fruits of three biological replicates were sampled for further analysis 597
598
Yeast one-hybrid assay 599
In order to identify proteins that bind to the FaQR promoter the Matchmaker Gold 600
Yeast One-hybrid Library Screening System (Clontech USA) was used The sequence 601
of the FaQR promoter was cloned into the pAbAi vector and the construct was 602
integrated into the genome of the Y1HGold yeast strain A mixture of total RNA from 603
strawberry fruit at four stages (G T IR R) was used to construct the prey cDNA 604
library (TaKaRa) The background AbAr expression of Y1HGold FaQR-pAbAi strain 605
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
22
was tested according to the system user manual and then screening for protein-DNA 606
interactions was carried out Furthermore the full length of each transcription factor 607
was separately cloned into pGADT7 AD vector to confirm the screening results The 608
relationship between FaERF9 and FaQR promoter was also examined individually 609
Primers used in this assay are listed in Supplemental Table S6 610
611
Expression and purification of FaMYB98 recombinant protein 612
A 405-bp region spanning the DNA-binding domain of FaMYB98 was amplified 613
from FaMYB98 cDNA and cloned into a pET6timesHN vector (Clontech Palo CA USA) 614
to generate the recombinant N-terminal His-tagged protein the primers used are listed 615
in Supplemental Table S6 The resulting construct was sequenced and introduced into 616
Escherichia coli strain Rosetta 2(DE3)pLysS (Novagen) Ten millilitres of the 617
overnight culture was combined with 500 mL of an LB liquid medium (100 μgmL 618
ampicillin and 34 μgmL chloramphenicol) as described (Li et al 2017) Isopropyl 619
β-D-1-thiogalactopyranoside (IPTG) was added to a final concentration of 1 mM and 620
the bacterial culture was incubated at 18degC at 150 rpm for 18 h Then the cells were 621
harvested using a centrifuge and resuspended in 1times PBS buffer (Sangon Biotech) 622
after which they were disrupted by sonication and the supernatant was purified using 623
a HisTALONTM Gravity Column (Clontech) according to the user manual The PD-10 624
Desalting column (GE Healthcare) was then used for buffer change and sample 625
clean-up of proteins according to the gravity protocol SDS-PAGE was performed and 626
the protein was visualized using Coomassie brilliant blue 627
628
Electrophoretic mobility shift assay (EMSA) 629
A Lightshift Chemiluminescent EMSA kit (Thermo) was used to perform EMSA 630
experiments according to the manufacturerrsquos instructions Single-strand 631
oligonucleotides were synthesized and biotinylated by GeneBio Biotech (Hangzhou 632
China) The details of the EMSA assay are provided in Ge et al (2017) The probes 633
used for EMSAs are listed in Supplemental Table S6 634
635
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
23
636
Yeast two-hybrid assay 637
The DUALhunter system (Dualsystems Biotech Switzerland) was used to investigate 638
the interaction between FaERF9 and FaMYB98 Full-length coding sequences of 639
FaERF9 and FaMYB98 were respectively cloned into pDHB1 bait vector and 640
pPR3-N prey vector sequences were verified and the bait plasmid was 641
co-transformed with prey plasmid into NMY51 in the combinations below 642
FaMYB98-pDHB1pPR3-N FaMYB98-pDHB1FaERF9-pPR3-N 643
FaMYB98-pDHB1pOst1-NubI FaERF9-pDHB1pPR3-N 644
FaERF9-pDHB1FaMYB98-pPR3-N and FaERF9-pDHB1pOst1-NubI (Li et al 645
2017) Transformed cells were spread onto the following plates DDO (SD 646
medium-Trp-Leu) QDO (SD medium-Trp-Leu-His-Ade) and QDO+3-AT (QDO 647
medium supplemented with 1 mM 3-amino-124-triazole) The control plasmid 648
pOst1-NubI was used to determine whether the bait was functional the pPR3-N prey 649
vector plasmid was used to test whether the bait displayed non-specific background 650
and positive interactions were indicated by the growth of yeast on QDO and 651
QDO+3-AT plates The Primers used in the DUALhunter assay are listed in 652
Supplemental Table S6 653
654
Bimolecular fluorescence complementation (BiFC) assays 655
Full-length FaERF9 and FaMYB98 respectively were cloned into sequences 656
encoding the N- and C- fragments of YFP protein (Lv et al 2014) All constructs 657
were transiently expressed in tobacco (N benthamiana) leaves by Agrobacterium 658
infiltration (EHA105) The YFP fluorescence of transfected leaves was imaged 40 h 659
after infiltration by using a Nikon A1-SHS confocal laser scanning microscope The 660
excitation wavelength for YFP was 488 nm and fluorescence was detected at 520ndash661
540 nm Primers used are listed in Supplemental Table S6 662
663
Statistics 664
A Studentrsquos two-tailed t test ( plt005 plt001 and plt0001) was used to 665
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
24
determine significant differences between two groups in this study Microsoft Excel 666
was used to perform linear regressive analysis significant differences were 667
determined by SPSS Statistics 200 and scatter plots were prepared with Origin80 668
Least significant difference (LSD) at the 5 level was calculated using Microsoft 669
Excel Figures were prepared with Origin80 (Microcal Software Inc Northampton 670
MA USA) The online tool MetaboAnalyst 36 (httpwwwmetaboanalystca) was 671
used to analyse the transcript abundance of the AP2ERF genes 672
673
Accession numbers 674
Sequence data from this article have been deposited in GenBank under the accession 675
numbers MH332903-MH333022 for AP2ERF genes in Fragaria times ananassa and 676
MH333023 for FaMYB98 GenBank numbers for FaQR and FaOMT were 677
AY1588361 (Raab et al 2006) and AF2204912 (Wein et al 2002) 678
679
Supplemental Material 680
Supplemental Figure S1 Phylogenetic analysis of FaAP2ERF and Arabidopsis 681
AP2ERF proteins 682
Supplemental Figure S2 Analysis of FaAP2ERF gene expression patterns in 683
strawberry fruit during development and ripening 684
Supplemental Figure S3 Contents of furanones in fruit of strawberry cultivars 685
Supplemental Figure S4 Relative expression of FaERF9 in FaERF9-FaMYB98- 686
and FaERF9-overexpressing fruits 687
Supplemental Figure S5 Subcellular localization of FaMYB98 688
Supplemental Figure S6 The combined activation effects of FaERF9FaMYB98 on 689
the FaOMT promoter 690
Supplemental Figure S7 Relative expression of FaOMT in 691
FaERF9-overexpressing fruits 692
Supplemental Table S1 AP2ERF superfamily genes in Fragaria times ananassa 693
Supplemental Table S2 Classification of the AP2ERF superfamily members in 694
Fragaria times ananassa 695
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
25
Supplemental Table S3 Furanone content in FaERF9-FaMYB98- and 696
FaERF9-overexpressing fruits 697
Supplemental Table S4 Primers used for reverse transcription quantitative PCR 698
(RT-qPCR) 699
Supplemental Table S5 Primers used to amplify the full-length coding sequences of 700
AP2ERF genes and FaMYB98 in strawberry (Fragaria times ananassa) 701
Supplemental Table S6 Primers used for vector construction 702
703
Acknowledgments 704
This research was supported by the National Key Research and Development 705
Program (2016YFD0400101) the Project of the Science and Technology Department 706
of Zhejiang Province (2016C04001) and the 111 Project (B17039) 707
708
Figure legends 709
Figure 1 Changes in furanone content and furanone biosynthetic genes during 710
strawberry (Fragaria times ananassa Duch cv Yuexin) fruit development and ripening 711
A Fruits were collected at four ripening stages G (green stage) T (turning stage) IR 712
(intermediate red stage) R (full red stage) B Changes in the contents of furaneol 713
(HDMF) and mesifurane (DMMF) HDMF content was calculated using a standard 714
curve of HDMF while DMMF content was calculated with an internal standard as the 715
reference C Expression levels of FaQR and FaOMT The expression levels of each 716
gene were calculated relative to corresponding values in the basal section at the R 717
stage SEs were calculated from three replicates and LSD values represent the least 718
significant differences at p = 005 719
Figure 2 Regulatory effects of FaAP2ERF on the promoter of FaQR LUCREN 720
values of the empty vector on FaQR promoter were used as the calibrator set as 1 721
and SEs were calculated from five replicates statistical significance was determined 722
by Studentrsquos two-tailed t test ( plt0001) 723
Figure 3 Expression and the subcellular localization of FaERF9 A The expression 724
levels were calculated relative to the levels in the basal section at the R stage B 725
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
26
Subcellular localization analysis was performed in tobacco leaves The tobacco used 726
in the assay was stably transformed with a specific nucleus localized red fluorescence 727
protein construct and the red fluorescence indicates the nucleus-localized signal 728
(NLS) Scale bar = 25 microm SEs were calculated from three replicates 729
Figure 4 Transient overexpression of FaERF9 in strawberry fruit A Relative 730
expression of FaQR and FaERF9 in FaERF9-OX fruit 7 days after infiltration The 731
expression was calculated relative to the average value in control (SK) fruits B 732
HDMF and DMMF content in FaERF9-OX fruit The content of both furanones 733
were quantified using the peak area of the internal standard (2-octanol) as the 734
reference SEs were calculated from three replicates Statistical significance was 735
determined by Studentrsquos two-tailed t test ( plt005 plt001 plt0001) 736
Figure 5 Scatter plots of 11 strawberry cultivars A Linear regression analysis 737
between FaERF9 expression and FaQR expression B Linear regression analysis 738
between FaERF9 expression and furanone content The relative expression was 739
normalized to that of the housekeeping gene FaRIB413 and furanone content was 740
calculated with internal standard as the reference Significant differences were 741
determined by SPSS Statistics 200 742
Figure 6 Interactions of FaERF9 and FaMYB98 with the FaQR promoter A Yeast 743
one-hybrid analysis of the interaction of FaERF9 and FaQR promoter B Yeast 744
one-hybrid analysis of the interaction of FaMYB98 and FaQR promoter C 745
Regulatory effect of FaMYB98 on the FaQR promoter Auto-activation was tested on 746
SD-Ura (synthetically defined medium without uracil) in presence of Aureobasidin A 747
(AbA) and physical interaction was determined on SD-Leu (synthetically defined 748
medium without leucine) in presence of AbA LUCREN values of the empty vector 749
on FaQR promoter were used as the calibrator set as 1 and error bars were calculated 750
from five replicates Statistical significance was determined by Studentrsquos two-tailed t 751
test ( plt005 plt001 plt0001) 752
Figure 7 Electrophoretic mobility shift assay of FaMYB98 binding to FaQR 753
promoter A The probe sequence used for EMSA and mutated nucleotides are 754
indicated with lowercase letters B Purified DNA-binding domain of FaMYB98 755
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
27
protein and biotin-labelled DNA probe were mixed and analysed on 6 native 756
polyacrylamide gels and then photographed Presence or absence of specific probes is 757
marked by the symbol + or - 758
Figure 8 The combined activation effects of FaERF9FaMYB98 on the FaQR 759
promoter LUCREN values obtained with the empty vector and FaQR promoter were 760
used as the calibrator set as 1 and error bars were calculated from five replicates 761
Figure 9 Yeast two-hybrid analysis of the protein-protein interactions between 762
FaMYB98 and FaERF9 Positive interactions were determined by the growth of 763
yeast cells on selection plates Bait with pOST acted as positive controls and bait with 764
pPR3 as negative controls DDO synthetically defined medium without tryptophan 765
and leucine QDO synthetically defined medium without tryptophan leucine 766
histidine and adenine QDO+3AT QDO medium supplemented with 1 mM 767
3-aminotriazole 768
Figure 10 BiFC analysis of the protein-protein interactions between FaMYB98 and 769
FaERF9 The pairs of fusion proteins tested were FaMYB98-YFPN+FaERF9-YFPC 770
FaERF9-YFPN+FaMYB98-YFPC FaMYB98-YFPN+FaMYB98-YFPC and 771
FaERF9-YFPN+FaERF9-YFPC The other combinations were negative controls 772
The tobacco used in the assay was stably transformed with a specific 773
nucleus-localized red fluorescence protein construct and the red fluorescence 774
indicated the nucleus-localized signal (NLS) Fluorescence of the yellow fluorescence 775
protein (YFP) visualized the interaction in vivo Scale bar = 25 microm 776
777
Literature Cited 778
779
Agarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression 780
of PgDREB2A transcription factor enhances abiotic stress tolerance and activates 781
downstream stress-responsive genes Mol Biol Rep 37 1125-1135 782
Araguumlez I Osorio S Hoffmann T Rambla JL Medina-Escobar N Granell A 783
Botella MAacute Schwab W Valpuesta V (2013) Eugenol production in achenes and 784
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
28
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Plant Physiol 163 946-958 786
Carvalho RF Carvalho SD OrsquoGrady K Folta KM (2016) Agroinfiltration of 787
strawberry fruit mdash a powerful transient expression system for gene validation Curr 788
Plant Biol 6 19-37 789
Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic 790
(Amsterdam) 210 34-40 791
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating 792
RNA from pine trees Plant Mol Biol Rep 11 113-116 793
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC 794
Clark DG (2011) PhMYB4 fine-tunes the floral volatile signature of 795
Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143 796
Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz 797
EA Taylor MG Smits-Kroon MT Schuurink RC Haring MA Giovannoni J 798
Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic 799
pathway by ectopic expression of a MYB transcription factor in tomato fruit Plant 800
Cell 23 2738-2753 801
Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan 802
XW Yang ZY (2017) Differential responses of four biosynthetic pathways of 803
aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under 804
interaction of light and temperature Food Chem 221 356-364 805
Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of 806
differentially-expressed genes during somatic embryogenesis in Fragaria times 807
ananassa Duch lsquoBenihopprsquo J Hortic Sci Biotechnol 90 671-681 808
Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 809
transcriptionally regulates chilling-induced lignification of loquat fruit via physical 810
interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136 811
Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM 812
(2004) Functional interactions between a glutamine synthetase promoter and MYB 813
proteins Plant J 39 513-526 814
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29
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) 815
Sucrose nonfermenting1-related protein kinase26 an ortholog of open stomata1 is 816
a negative regulator of strawberry fruit development and ripening Plant Physiol 817
167 915-930 818
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene 819
expression in strawberry fruit (Fragaria times ananassa) by agroinfiltration a rapid 820
assay for gene function analysis Plant J 48 818-826 821
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of 822
selected aroma-active compounds in strawberries by headspace solid-phase 823
microextraction gas chromatography and correlation with sensory descriptive 824
analysis J Food Sci 72 S487-S496 825
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid 826
plays an important role in the regulation of strawberry fruit ripening Plant Physiol 827
157 188-199 828
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of 829
NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes BMC 830
Plant Biol 6 20 831
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN 832
(2005) MYB98 is required for pollen tube guidance and synergid cell differentiation 833
in Arabidopsis Plant Cell 17 2981-2992 834
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional 835
characterization of enone oxidoreductases from strawberry and tomato fruit J 836
Agric Food Chem 55 6705-6711 837
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You 838
J-S Rohloff J Randall SK Alsheikh M (2012) Proteomic study of 839
low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ 840
in cold tolerance Plant Physiol 159 1787-1805 841
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional 842
characterization of four APETALA2-family genes (RAP26 RAP26L DREB19 843
and DREB26) in Arabidopsis Plant Mol Biol 75 107-127 844
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
30
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon 845
J Gupta V (2013) An oxidoreductase from lsquoAlphonsorsquo mango catalyzing 846
biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494 847
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in 848
strawberries Z Lebensm-Unters Forsch 195 120-123 849
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X 850
(2015) Label-free quantitative proteomics to investigate strawberry fruit proteome 851
changes under controlled atmosphere and low temperature storage J Proteomics 852
120 44-57 853
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 854
cooperates with CitWRKY1 to participate in citric acid degradation via 855
up-regulation of CitAco3 J Exp Bot 68 3419-3426 856
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription 857
factor CitERF71 activates the terpene synthase gene CitTPS16 involved in the 858
synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938 859
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and 860
transcriptomic analysis of the AP2ERF superfamily in Vitis vinifera BMC 861
Genomics 11 719 862
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive 863
Factor (AP2ERF) transcription factors mediators of stress responses and 864
developmental programs New Phytol 199 639-649 865
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 866
interacting with EOBI negatively regulates fragrance biosynthesis in petunia 867
flowers New Phytol 215 1490-1502 868
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu 869
CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 in regulating 870
anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) 871
during anthocyanin biosynthesis Plant Cell Tissue Organ Cult 115 285-298 872
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
31
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao 873
CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphate signaling and 874
homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597 875
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC 876
Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL 877
Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor 878
regulates eugenol production in ripe strawberry fruit receptacles Plant Physiol 168 879
598-614 880
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics 881
and volatile constituents of strawberry (cv Cigaline) during maturation J Agric 882
Food Chem 52 1248-1254 883
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS 884
(2012) Ethylene-responsive transcription factors interact with promoters of ADH 885
and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 886
63 6393-6405 887
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM 888
Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-Franco A 889
Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific 890
transcription factor FaDOF2 regulates the production of eugenol in ripe fruit 891
receptacles J Exp Bot 68 4529-4543 892
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) 893
Comparison and verification of the genes involved in ethylene biosynthesis and 894
signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44 895
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the 896
ERF gene family in Arabidopsis and rice Plant Physiol 140 411-432 897
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in 898
sour cherry and strawberry and the heterologous expression of CBF1 in strawberry 899
J Am Soc Hortic Sci 127 489-494 900
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech 901
JC Ohme-Takagi M Regad F Bouzayen M (2012) Functional analysis and 902
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32
binding affinity of tomato ethylene response factors provide insight on the 903
molecular bases of plant differential responses to ethylene BMC Plant Biol 12 190 904
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) 905
Methylpentoses are possible precursors of furanones in fruits Prikl Biokhim 906
Mikrobiol 28 123-127 907
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery 908
of synergid-expressed genes encoding filiform apparatus localized proteins Plant 909
Cell 19 2557-2568 910
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria 911
vesca L compared to those of cultivated berries Fragariatimes ananassa cv Senga 912
Sengana J Agric Food Chem 27 19-22 913
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W 914
Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of the strawberry 915
flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone 916
oxidoreductase Plant Cell 18 1023-1037 917
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L 918
Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim M Broun P Zhang 919
JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription 920
factors genome-wide comparative analysis among eukaryotes Science 290 921
2105-2110 922
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the 923
formation of 25-dimethyl-4-hydroxy-3(2H)-furanone in detached ripening 924
strawberry fruits J Agric Food Chem 46 1488-1493 925
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 926
25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in 927
strawberry fruits Phytochemistry 43 155-159 928
Schwab W (1998) Application of stable isotope ratio analysis explaining the 929
bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone in plants by a biological 930
maillard reaction J Agric Food Chem 46 2266ndash2269 931
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
33
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) 932
Molecules 18 6936-6951 933
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard 934
products Recent Res Dev Phytochem 1 643-673 935
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL 936
Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJ Sims CA 937
Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical 938
compositions a seasonal influence and effects on sensory perception PLoS One 9 939
e88446 940
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) 941
Identification phylogeny and transcript profiling of ERF family genes during 942
development and abiotic stress treatments in tomato Mol Genet Genomics 284 943
455-475 944
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) 945
CitAP210 activation of the terpene synthase CsTPS1 is associated with the 946
synthesis of (+)-valencene in lsquoNewhallrsquo orange J Exp Bot 67 4105-4115 947
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes 948
Dev Genes Evol 214 105-114 949
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K 950
Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the 951
key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151 952
Spitzer-Rimon B Farhi M Albo B Cnarsquoani A Ben Zvi MM Masci T Edelbaum 953
O Yu YX Shklarman E Ovadis M Vainstein A (2012) The R2R3-MYB-like 954
regulatory factor EOBI acting downstream of EOBII regulates scent production 955
by activating ODO1 and structural scent-related genes in petunia Plant Cell 24 956
5089-5105 957
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp 958
Bot 68 4407-4409 959
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla 960
JF Amaya I Giavalisco P Fernie AR Botella MA Valpuesta V (2015) Central 961
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
34
role of FaGAMYB in the transition of the strawberry receptacle from development 962
to ripening New Phytol 208 482-496 963
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 964
regulates fragrance biosynthesis in petunia flowers Plant Cell 17 1612-1624 965
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS 966
(2018) The potassium channel FaTPK1 plays a critical role in fruit quality 967
formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748 968
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) 969
Isolation cloning and expression of a multifunctional O-methyltransferase capable 970
of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma 971
compounds in strawberry fruits Plant J 31 755-765 972
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor 973
types their evolutionary origin and species distribution In A handbook of 974
transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular 975
Biochemistry 52 25-73 976
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of 977
odor (Buettner A Ed) Springer Cham 9-10 978
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS 979
(2014) Isolation classification and transcription profiles of the AP2ERF 980
transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271 981
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in 982
regulation of fruit quality Crit Rev Plant Sci 35 120-130 983
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ 984
Zhang SL Wu J (2017) Map-based cloning of the pear gene MYB114 identifies an 985
interaction with other transcription factors to coordinately regulate fruit 986
anthocyanin biosynthesis Plant J 92 437-451 987
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes 988
involved in regulating fruit ripening Plant Physiol 153 1280-1292 989
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
35
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) 990
Expression of ethylene response genes during persimmon fruit astringency removal 991
Planta 235 895-906 992
Zabetakis I Gramshaw JW Robinson DS (1999) 993
25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis and 994
biosynthesis-a review Food Chem 65 139-151 995
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci 996
Food Agric 74 421-434 997
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 998
an AP2ERF gene is a novel regulator of fruit lignification induced by chilling 999
injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1000
1325-1334 1001
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation 1002
classification and transcription profiles of the Ethylene Response Factors (ERFs) in 1003
ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215 1004
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML 1005
(2012) Genome-wide analysis of the AP2ERF superfamily in peach (Prunus 1006
persica) Genet Mol Res 11 4788-4809 1007
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and 1008
expression analysis of a CRTDRE-binding factor gene FaCBF1 from Fragaria times 1009
ananassa Acta Hortic 41 240-248 1010
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The 1011
Arabidopsis AP2ERF transcription factor RAP26 participates in ABA salt and 1012
osmotic stress responses Gene 457 1-12 1013
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B 1014
Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) Genome-wide 1015
analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic 1016
(Amsterdam) 123 73-81 1017
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF 1018
Valpuesta V Botella MA Granell A Amaya I (2012) Genetic analysis of 1019
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
36
strawberry fruit aroma and identification of O-methyltransferase FaOMT as the 1020
locus controlling natural variation in mesifurane content Plant Physiol 159 1021
851-870 1022
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Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp Bot 68 4407-4409Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla JF Amaya I Giavalisco P Fernie AR Botella MAValpuesta V (2015) Central role of FaGAMYB in the transition of the strawberry receptacle from development to ripening New Phytol208 482-496
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 regulates fragrance biosynthesis in petunia flowers PlantCell 17 1612-1624
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS (2018) The potassium channel FaTPK1 plays a critical role infruit quality formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) Isolation cloning and expression of a multifunctional O- wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma compounds in strawberry fruitsPlant J 31 755-765
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Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor types their evolutionary origin and speciesdistribution In A handbook of transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular Biochemistry 52 25-73
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Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of odor (Buettner A Ed) Springer Cham 9-10Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS (2014) Isolation classification and transcription profiles ofthe AP2ERF transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in regulation of fruit quality Crit Rev Plant Sci 35 120-130
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ Zhang SL Wu J (2017) Map-based cloning of the pear geneMYB114 identifies an interaction with other transcription factors to coordinately regulate fruit anthocyanin biosynthesis Plant J 92437-451
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes involved in regulating fruit ripening Plant Physiol 1531280-1292
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) Expression of ethylene response genes during persimmonfruit astringency removal Planta 235 895-906
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zabetakis I Gramshaw JW Robinson DS (1999) 25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis andbiosynthesis-a review Food Chem 65 139-151
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci Food Agric 74 421-434Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 an AP2ERF gene is a novel regulator of fruit lignificationinduced by chilling injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1325-1334
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation classification and transcription profiles of the Ethylene ResponseFactors (ERFs) in ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML (2012) Genome-wide analysis of the AP2ERF superfamily inpeach (Prunus persica) Genet Mol Res 11 4788-4809
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and expression analysis of a CRTDRE-binding factor gene FaCBF1from Fragaria times ananassa Acta Hortic 41 240-248
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The Arabidopsis AP2ERF transcription factor RAP26 participatesin ABA salt and osmotic stress responses Gene 457 1-12
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Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Genome-wide analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic (Amsterdam) 123 73-81Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF Valpuesta V Botella MA Granell A Amaya I (2012) Geneticanalysis of strawberry fruit aroma and identification of O-methyltransferase FaOMT as the locus controlling natural variation inmesifurane content Plant Physiol 159 851-870
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
5
Introduction 96
Strawberry (Fragaria times ananassa) is an economically important globally popular 97
and attractive fruit with nutritional benefits for human health An important feature of 98
its appeal is a unique fragrance with more than 360 different volatile compounds 99
detected in ripe fruit (Meacutenager 2004 Jetti et al 2007) These volatiles include 100
alcohols organic acids aldehydes terpenes lactones esters aromatic hydrocarbons 101
furans and others (Zabetakis and Holden 1997) Sensory evaluation indicates that 102
terpenes confer on strawberry a ldquofresh orangerdquo smell aldehydes generate a ldquoherbal 103
flavourrdquo γ -decalactone is ldquopeach-likerdquo esters are ldquofruityrdquo and 104
4-hydroxy-25-dimethyl-3(2)H-furanone (HDMF) and 105
25-dimethyl-4-methoxy-3(2)H-furanone (DMMF) generate a ldquocaramel-likerdquo aroma 106
(Pyysalo et al 1979 Larsen and Poll 1992) HDMF and DMMF belong to an 107
uncommon group of chemicals with a 25-dimethyl-3(2H)-furanone structure and 108
such compounds possess special odour properties (Schwab and Roscher 1997) They 109
are found at trace levels in various fruits including raspberry some grape cultivars 110
and tomato They are particularly abundant in strawberry and pineapple (Schwab 111
2013 Wuumlst 2017) HDMF is one of the most important volatiles distinguishing 112
strawberry from other fruits (Larsen and Poll 1992 Schwab and Roscher 1997) and 113
is significantly correlated with perceived strawberry fruit intensity (Schwieterman et 114
al 2014) Thus strawberry is an important model for investigating the regulation of 115
furaneol biosynthesis and knowledge of the factors controlling its synthesis is highly 116
desirable for targeting flavor improvement 117
118
HDMF and its methyl ether DMMF have been extensively investigated in research 119
on flavour analyses chemical synthesis and natural product formation in both 120
microbes and plants (Zabetakis et al 1999 Schwab 2013) The first plant studies on 121
the biosynthesis of HDMF used strawberry fruit to investigate potential precursors of 122
furaneol biosynthesis (Pisarnitskii et al 1992) and D-fructose-16-diphosphate was 123
identified as the natural precursor of HDMF and DMMF (Roscher et al 1998 124
Schwab 1998) The immediate precursor of HDMF in strawberry was shown to be 125
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6
4-hydroxy-5-methyl-2-methylene-3(2H)-furanone (HMMF) and Fragaria times 126
ananassa quinone oxidoreductase (FaQR later renamed as FaEO) was identified as 127
the enzyme responsible for reduction of the α β-unsaturated bond of HMMF to form 128
the aroma-active compound HDMF (Raab et al 2006 Klein et al 2007) An 129
O-methyltransferase FaOMT subsequently generates DMMF by methylation of 130
HDMF (Wein et al 2002) HDMF can also be metabolized to 131
25-dimethyl-4-hydroxy-2H-furan-3-one glucoside (HDMF-glucoside) by a 132
UDP-dependent glycosyltransferase (UGT71K3) and further malonylated into 133
25-dimethyl-4-hydroxy-2H-furan-3-one 6rsquo-O-malonyl-β-D-glucopyranoside (HDMF 134
malonyl-glucoside) in strawberry fruit (Roscher et al 1996 Song et al 2016) The 135
biosynthetic pathway of HDMF in other plants is similar to that in strawberry Genes 136
with homology to FaQR have been identified in tomato (SlEO) and mango (MIEO) 137
(Klein et al 2007 Kulkarni et al 2013) 138
139
As an NADH-dependent enone oxidoreductase protein FaQR exhibits o-quinone 140
oxidoreductase activity (Raab et al 2006) FaQR mRNA accumulates in fruit 141
parenchyma tissues but is absent in vascular tissues and FaQR is mainly expressed in 142
the late stages of fruit growth and ripening paralleling furaneol production in the fruit 143
(Raab et al 2006) FaQR is responsive to environmental stimuli associated with 144
furaneol production and in the dark lsquoSweet Charliersquo strawberry fruits have higher 145
levels of FaQR expression and HDMF production at 25degC than at 15degC (Fu et al 146
2017) in contrast the concentration of furanones and the abundance of FaQR protein 147
under low-temperature storage is significantly lower than those under 148
room-temperature storage (Li et al 2015) Thus the regulation of FaQR is important 149
for manipulating furaneol content Although it is assumed that transcription factors 150
control expressions of genes involved in volatile production in plants no such factors 151
regulating FaQR or other furanone biosynthetic genes have been identified 152
153
Different members of the largely plant-specific AP2ERF gene family (Weirauch and 154
Hughes 2011) have diverse functions in plant growth development and stress 155
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7
responses (Agarwal et al 2010 Zhu et al 2010 Licausi et al 2013) In recent years 156
several AP2ERF genes have been reported to regulate aspects of fruit quality (Xie et 157
al 2016) including fruit aroma For example CitAP210 is associated with the 158
synthesis of (+)-valencene in Newhall orange acting via regulation of CsTPS1 (Shen 159
et al 2016) CitERF71 was shown to physically bind to the CsTPS16 promoter and 160
contribute to the synthesis of E-geraniol in citrus fruit (Li et al 2017) These 161
observations raised the possibility that FaQR might also be a target for a member of 162
the AP2ERF family and that ERFs might also control furaneol biosynthesis 163
164
In this study screening of the Fragaria times ananassa AP2ERF gene family led to 165
identification of FaERF9 as an activator of FaQR however it did not bind directly 166
to the promoter A parallel search for proteins that directly bind the FaQR promoter 167
using yeast one-hybrid screening identified a second factor FaMYB98 which was 168
capable of physically interacting with the FaQR promoter FaMYB98 physically 169
interacts with FaERF9 and transient expression assays demonstrated a synergistic 170
effect on FaQR expression and furanone synthesis 171
172
Results 173
Changes in the content of both furanones and the activity of their biosynthetic 174
genes in strawberry fruit 175
lsquoYuexinrsquo fruits at four developmental and ripening stages (G green T turning IR 176
intermediate red R full red) were harvested (Figure 1) and determination of HDMF 177
levels indicated a major increase from about 065 μg per gram fruit at the IR stage to 178
346 μg at the R stage in the apical section implying that furaneol accumulation was 179
closely related to colour change and ripening (Figure 1) Furaneol levels were higher 180
in the apical section than in the basal section HDMF could not be detected at the IR 181
stage in the basal section but the amount increased at the R stage to 142 μg per gram 182
fruit Differences were also found for DMMF with the relative content in the apical 183
section 018 μg per gram at the R stage compared to 008 μg per gram in the basal 184
section at the same stage 185
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8
186
Measurement of mRNA levels by RT-qPCR indicated that the transcript levels of both 187
FaQR (GenBank AY1588361) and FaOMT (GenBank AF2204912) increased 188
throughout ripening (Figure 1) Comparison of the expression of these genes showed 189
that the transcript levels of FaQR and FaOMT significantly increased as early as in T 190
stage in basal fruit sections and for each gene over half of the peak transcript 191
abundance occurred as early as in IR stage in the apical section while for the basal 192
section it was in the R stage indicating a gradient of gene expression and volatile 193
production from apex to base of the fruit during ripening 194
195
Genome-wide identification of AP2ERF gene family in strawberry 196
Coding sequences of 120 non-redundant FaAP2ERF genes were isolated and 197
identified from lsquoYuexinrsquo strawberry and a systematic nomenclature for the AP2ERF 198
family genes was used to distinguish the members based on the structural features 199
defined previously (Supplemental Table S1) (Shigyo and Ito 2004 Nakano et al 200
2006 Licausi et al 2013) CD-search analysis showed that this superfamily is 201
consisted of 95 ERFs 18 AP2 and 6 RAV family members and 1 soloist member 202
(Supplemental Table S2) Phylogenetic analysis of the Fragaria times ananassa and 203
Arabidopsis AP2ERF members is shown in Supplemental Figure S1 with the 120 204
AP2ERF genes divided into three major groups (ERF AP2 RAV) and a soloist and 205
the ERF family being further divided into 10 groups (groups I to X in Supplemental 206
Table S1) 207
208
We performed a dual-luciferase assay to determine the ability of 116 FaAP2ERF 209
members to activate transcription from the promoter of FaQR The results indicated 210
about 12 members (mainly belonging to the ERF and RAV families) showed a 211
significant activation effect on the FaQR promoter while the remaining members 212
showed very limited effects (Figure 2) The relative activity of only the following 12 213
FaAP2ERF transcripts reached the threshold value set at 2 FaERF8FaERF9 214
(group II) FaERF27FaERF29FaERF31FaERF32 (group IV) 215
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9
FaERF37FaERF38 (group V) FaERF62FaERF64 (group VIII) FaERF68 216
(group IX) and FaRAV4 (Figure 2) Of these FaERF9 exhibited the highest 217
activation effect on the FaQR promoter (466-fold) (Figure 2) The strawberry 218
FaERF9 cDNA is 699 bp long and ExPASy Compute pIMw tool analysis indicated 219
that this gene encodes a 232-amino acid protein with a calculated molecular mass of 220
254 KD and a pI of 56 221
222
FaERF9 expression pattern and subcellular localization 223
To further explore the connections between AP2ERFs and furaneol biosynthesis we 224
obtained the transcript profiles of the AP2ERF genes in strawberry fruit samples at 225
different fruit developmental and ripening stages by reverse transcription quantitative 226
PCR (RT-qPCR) excluding genes with very low abundance in the fruit samples The 227
results presented as a heatmap (Supplemental Figure S2) demonstrate that these 228
genes displayed various expression patterns in both the apical and basal sections and 229
by analysing the expression patterns of the members indicated as activators in the 230
dual-luciferase assay we found that only a few genes including FaERF8 FaERF9 231
FaERF27 FaERF32 and FaERF37 were up-regulated during ripening stages and 232
their expression correlated with furaneol accumulation in the fruit (Figure 1) 233
Furthermore the expression patterns of the up-regulated genes in the apical and basal 234
sections showed that one ERF gene FaERF9 not only showed an up-regulation 235
pattern in both sections but its expression in the apical section occurred ahead of that 236
in the basal section (Figure 3) consistent with the actual changes in furaneol content 237
(Figure 1) and the expression pattern of FaQR (Figure 1) The subcellular localization 238
of FaERF9 was predicted to be in the nucleus using the WoLF PSORT program In 239
experimental tests 35S-FaERF9-GFP (green fluorescence protein) showed strong 240
fluorescence in the nucleus and the green signal merged with the red fluorescence 241
signal of mCherry-nucleus-marker in tobacco plants (Figure 3) 242
243
Transient overexpression of FaERF9 in strawberry 244
The expression of FaERF9 in agro-infiltrated fruits was analysed by performing 245
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10
RT-qPCR on the seventh day after infiltration by which time they had reached the IR 246
or R stage and the result showed that the transcript levels were significantly higher 247
(52-fold) than in control fruits (Figure 4) The expression of FaQR was examined in 248
the same fruits and the transcript abundance also increased 22-fold The relative 249
content of HDMF in the FaERF9-overexpressing fruits was 008 μg per gram fruit 250
and undetectable in the control fruits (Figure 4) The relative content of DMMF in the 251
overexpressing fruits was also significantly increased to 038 μg per gram fruit 252
compared to 004 μg per gram fruit in the control (Figure 4) These observations 253
provide direct evidence for a regulatory role for FaERF9 in promoting FaQR 254
biosynthesis and activity in ripening strawberry fruit Taken together these results 255
indicate that by activating the transcription of FaQR FaERF9 functions as a positive 256
regulator in furaneol biosynthesis 257
258
Correlation of FaERF9 expression and FaQR transcript profiles 259
GC-MS quantification showed that furanones are distributed in variable levels among 260
different strawberry cultivars (Supplemental Figure S3) The transcript profiles of 261
FaQR and FaERF9 in fruits of different cultivars were measured and linear 262
regression analysis was performed In the cultivars the changes in FaQR transcripts 263
correlated positively with those in FaERF9 transcripts (r = 079 plt001) (Figure 5) 264
In addition FaERF9 transcript levels also correlated with furanone content across 265
cultivars (Figure 5) 266
267
FaERF9 is an indirect regulator of the FaQR promoter and acts via 268
protein-protein interaction with FaMYB98 269
Although the results of the dual-luciferase assay expression analysis transient 270
overexpression and correlation analysis were all consistent with the suggestion that 271
FaERF9 regulates transcript abundance by acting on the FaQR promoter a yeast 272
one-hybrid assay indicated that FaERF9 cannot bind directly to the FaQR promoter 273
(Figure 6) This led us to speculate that activation may occur via a transcription 274
complex involving an additional as-yet unknown regulator which can bind directly to 275
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11
the FaQR promoter 276
277
In parallel with the investigation of the FaAP2ERF genes a cDNA library screening 278
was performed with a yeast one-hybrid assay using the promoter of FaQR as the bait 279
This screen identified several transcription factors that could physically bind to the 280
FaQR promoter but only one MYB could activate transcription from the FaQR 281
promoter (approximately 56-fold) relative to the control (Figure 6) in the 282
dual-luciferase assay This MYB showed 44 amino acid identity with MYB98 283
(GenBank ABA420611) a transcriptional regulator in the synergid cells in 284
Arabidopsis (Kasahara et al 2005) and it was designated as FaMYB98 The 285
specificity of FaMYB98 binding to the FaQR promoter was confirmed by EMSA 286
assay (Figure 7) and increasing the concentration of the cold probe reduced binding 287
In addition mutating the putative binding sites (Goacutemez-Maldonado et al 2004 288
Punwani et al 2007) as shown in Figure 7 eliminated FaMYB98 protein binding 289
When the combined effect of FaERF9 and FaMYB98 was analysed (Figure 8) a 290
synergistic 14-fold activation of the FaQR promoter was observed compared with the 291
activation by either FaERF9 or FaMYB98 which alone promoted transactivation 292
39-fold and 45-fold respectively In addition overexpression of both genes 293
(FaERF9-FaMYB98-SK) in strawberry fruits resulted in higher expression of 294
FaERF9 transcripts and higher furanone content than overexpression of FaERF9 295
(Supplemental Figure S4 Supplemental Table S3) Subcellular localization analysis 296
revealed that FaMYB98 was also localized in the nucleus (Supplemental Figure S5) 297
298
To investigate the potential interactions between FaERF9 and FaMYB98 the 299
DUALhunter system was used (Figure 9) Cells expressing the FaMYB98 and 300
FaERF9 protein pair using either FaMYB98 or FaERF9 as the bait grew on DDO 301
QDO and QDO supplemented with 1 mM 3-AT selective medium indicating 302
interaction between the two proteins This putative protein-protein interaction was 303
confirmed by BiFC assay and the combinations of FaMYB98-YFPNFaERF9-YFPC 304
and FaERF9-YFPNFaMYB98-YFPC exhibited strong coincident signals in the 305
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12
nucleus while negative controls produced no detectable fluorescence signal (Figure 306
10) In addition coexpression of FaERF9-YFPNFaERF9-YFPC as well as 307
FaMYB98-YFPNFaMYB98-YFPC also generated signals in the nucleus indicating 308
that FaERF9 and FaMYB98 both could form homodimers or possibly multimers in 309
the nucleus (Figure 10) 310
311
Discussion 312
The AP2ERF superfamily in strawberry 313
The AP2ERF superfamily of plant transcription factors is defined by the AP2ERF 314
domain and comprises the ERF AP2 and RAV families as well as one soloist member 315
(Riechmann et al 2000 Weirauch and Hughes 2011) The completion of multiple 316
plant genome sequences has enabled a genome-scale analysis of the AP2ERF family 317
which in recent years has been systematically studied in diverse fruit species such as 318
tomato grape peach and kiwi fruit (Zhuang et al 2009 Sharma et al 2010 Licausi 319
et al 2010 Yin et al 2010 Pirrello et al 2012 Zhang et al 2012 Zhang et al 320
2016) A few AP2ERF genes have been isolated and characterized in strawberry and 321
CBF orthologs (Owens et al 2002 Koehler et al 2012 Zhang et al 2014) have 322
been identified from different strawberry cultivars in several independent studies 323
Although they have distinct names eg Fragaria times ananassa CBF1 (FaCBF1) 324
FaCBF4 (GenBank HQ9105151) and CBF1 (GenBank EU1172142) according to 325
the phylogenetic tree generated in this study the orthologs of 326
CBF1CBF4CBF2CBF3 in Arabidopsis are similar to each other and to FaERF20 327
(Supplemental Figure S1) (Owens et al 2002 Koehler et al 2012 Zhang et al 328
2014) FaERF20 has 85 sequence similarity with FaCBF1 identified by Owens et 329
al (2002) 93 similarity with FaCBF4 amplified by Koehler et al (2012) and 75 330
similarity with CBF1 cloned by Zhang et al (2014) The AP2ERF genes 331
characterized in other studies (Jia et al 2011 GAO et al 2015 Chai and Shen 2016 332
Mu et al 2016) are also noted in Supplemental Table S1 333
334
Based on the computational analysis we have identified a total of 120 AP2ERF 335
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13
genes in octoploid strawberry (Supplemental Table S1) The number of predicted 336
AP2ERF genes (120) is comparable to those observed in other fruits including 337
tomato (112) Chinese plum (116) citrus (126) and peach (131) but lower than those 338
reported for grape (149) (Xie et al 2016) As shown in Supplemental Table S2 79 339
(95 genes) of the AP2ERF genes belong to the ERF family in strawberry constituting 340
the largest sub-family The members of this sub-family can be classified into 10 341
groups (group I to X) according to their sequence similarities to the Arabidopsis ERF 342
genes (Nakano et al 2006) The AP2 family encompasses the same number of genes 343
in Arabidopsis citrus and strawberry (eighteen) (Nakano et al 2006 Xie et al 2014) 344
and there are six RAV genes in strawberry which are highly conserved in dicots such 345
as Vitis vinifera Arabidopsis thaliana and Populus trichocarpa (Licausi et al 2010) 346
347
Role of FaERF9 in regulating the biosynthesis of HDMF a positive regulator 348
acting in an indirect manner 349
The large-scale screening of the AP2ERF superfamily in strawberry led to 350
identification of 11 ERFs and 1 RAV that trans-activated the FaQR promoter more 351
than two-fold with the highest activation caused by FaERF9 which trans-activated 352
the FaQR promoter (Figure 2) as well as up-regulating FaQR expression and furanone 353
production in transient overexpression assays (Figure 4) which has been extensively 354
used to explore the fruit-associated gene functions in strawberry (Han et al 2015 355
Medina-Puche et al 2015 Vallarino et al 2015 Carvalho et al 2016 Song et al 356
2016 Wang et al 2018) FaERF9 transcripts accumulate in the fruit apical section 357
before the basal section (Figure 3) a finding consistent with the actual changes in 358
furaneol content (Figure 1) and the expression of FaQR (Figure 1) The association 359
between FaERF9 transcripts and accumulation of furanones were also established 360
with different strawberry cultivars The correlation between FaERF9 and FaQR 361
expression as well as furanone content among cultivars supports a positive role of 362
FaERF9 in regulating furanone content (Figure 5) These results indicate that 363
FaERF9 transcript abundance may be a good indicator of the abundance of these 364
important flavour volatiles in fruits of different cultivars This should be considered as 365
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14
a method for high-throughput variety screening to replace direct measurement of 366
volatiles 367
368
FaERF9 is a member of the ERF group II family and is most closely related to the 369
Arabidopsis genes At1g44830 (ATERF014) At1g21910 (DREB26) and At1g77640 370
(Supplemental Figure S1) At1g44830 was observed to be strongly up-regulated in a 371
comprehensive microarray analysis of the root transcriptome following NaCl 372
exposure (Jiang and Deyholos 2006) At1g21910 (DREB26) was functionally 373
characterized as a trans-activator localized in the nucleus exhibiting tissue-specific 374
expression and participating in plant developmental processes as well as biotic andor 375
abiotic stress signalling (Krishnaswamy et al 2011) However none of these genes 376
have been reported as furanone regulators In strawberry another five genes 377
(FaERF6 FaERF7 FaERF8 FaERF10 and FaERF11) also belong to the same 378
group with FaERF8 also showing somewhat weaker activation activity towards the 379
FaQR promoter than FaERF9 The fact that FaERF9 could not bind directly to the 380
promoter of FaQR (Figure 6) indicates that it might function as an indirect regulator 381
of FaQR and furaneol biosynthesis 382
383
A FaERF9 and FaMYB98 complex is involved in regulating FaQR and furaneol 384
biosynthesis 385
The finding that FaERF9 could interact with FaMYB98 protein (Figures 9 and 386
Figure 10) and that FaMYB98 could physically bind to the FaQR promoter (Figure 6 387
and Figure 7) provides evidence for a regulatory mechanism whereby FaERF9 388
regulates FaQR and furaneol production as part of a complex with an MYB 389
transcription factor Since co-overexpression of FaERF9 and FaMYB98 resulted in 390
much higher activation activity towards FaQR we speculate that FaERF9 may 391
recruit FaMYB98 homologs in tobacco to activate the FaQR promoter (Figure 8) 392
FaOMT is another key gene for furanone biosynthesis and a potential target for 393
transcriptional activation However FaERF9 did not significantly activate the 394
FaOMT promoter in a dual-luciferase assay and the transcript level of FaOMT in the 395
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15
FaERF9-overexpressing fruits showed no significant difference from that in the 396
control (Supplemental Figure S6 Supplemental Figure S7) The FaOMT promoter 397
was significantly induced by FaMYB98 but no synergistic effect of FaERF9 and 398
FaMYB98 on the promoter was observed (Supplemental Figure S6) In previous 399
studies of the regulation of plant volatile compounds MYBs have been characterized 400
as being involved mainly in the regulation of the benzenoidphenylpropanoid pathway 401
that produces floral volatiles in petunia and eugenol in ripe strawberry fruit (Verdonk 402
et al 2005 Dal Cin et al 2011 Colquhoun et al 2011 Spitzer-Rimon et al 2012 403
Medina-Puche et al 2015) but their role in formation of volatiles from other 404
pathways has not been reported Our study demonstrates a role for MYB in the 405
synthesis of furaneol a carbohydrate-derived volatile compound and reveals the 406
synergistic interactions between an MYB and ERF in a transcription complex (Figure 407
8 Figure 9 and Figure 10) 408
409
Recent research has provided evidence for interactions between AP2ERF and MYB 410
transcription factors in regulating other aspects of fruit quality including texture 411
(EjAP2-1 and EjMYB Zeng et al 2015) and colour (PyERF3 and PyMYB114 Yao 412
et al 2017) A group VIII ERF has also recently been shown to interact with an MYB 413
to regulate floral scent production in petunia (Liu et al 2017) In strawberry fruit 414
DOF in combination with an MYB has been reported to be involved in the regulation 415
of eugenol production and the identification of this second transcription factor (DOF) 416
suggests that it is a good target in breeding for improved flavour (Molina-Hidalgo et 417
al 2017 Tieman 2017) Considering its important contribution to flavour in 418
strawberry and many other highly valued fruit crop species (pineapple tomato mango 419
etc) very little is known about regulation of furaneol synthesis Here we established 420
the role of FaERF9 in the regulation of HDMF synthesis by direct protein-protein 421
interactions with FaMYB98 to synergistically trans-activate FaQR The functional 422
identification of this complex enhances our knowledge of the regulation of volatile 423
compound synthesis and identifies a new AP2ERF-MYB complex Further 424
examination of the other ERFs that stimulated transcription from the FaQR promoter 425
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16
(Figure 2) may provide additional information about the complexity of this regulation 426
Overall this study provides important clues for understanding the transcriptional 427
regulation of HDMF synthesis and identifies specific transcription factors that are 428
likely to be good targets for molecular breeding for improved flavour 429
430
Conclusions 431
Screening of the AP2ERF superfamily in strawberry (Fragaria times ananassa) 432
identified candidate members capable of activating the FaQR promoter An ERF 433
transcription factor was identified as a positive regulator of HDMF synthesis in 434
strawberry fruit and the mechanism of activation was shown to involve an ERF-MYB 435
transcription complex that regulates transcription of FaQR leading to the biosynthesis 436
of HDMF the characteristic volatile compound which has a major influence on 437
strawberry aroma 438
439
Materials and Methods 440
441
Plant Materials and Growth conditions 442
The strawberry (Fragaria times ananassa cv lsquoYuexinrsquo an octoploid cultivar) fruit used in 443
this study were bred by Zhejiang Academy of Agricultural Sciences (Haining 444
Zhejiang) Fruits at various developmental and ripening stages including G (green) T 445
(turning) IR (intermediate red) and R (full red) were harvested (Figure 1) and 446
transported to the laboratory within 2 h Thirty-six fruits of uniform size and free of 447
visible defects were selected at each stage with twelve fruits in each biological 448
replicate After removing the calyces fruits were then divided into the basal and 449
apical sections which were sampled separately (Figure 1) They were rapidly cut into 450
pieces frozen immediately in liquid nitrogen and stored at -80deg C until use Red ripe 451
fruits of different strawberry cultivars (Fragaria times ananassa octoploid cultivars) 452
including lsquoYuelirsquo lsquoBenihoppersquo lsquoMengxiangrsquo lsquoAmaoursquo lsquo10-1-4rsquo lsquoAkihimersquo lsquoSweet 453
Charliersquo lsquo07-1-4rsquo lsquoDarselectrsquo lsquoYuexinrsquo and lsquoXuemeirsquo were also provided by Zhejiang 454
Academy of Agricultural Sciences For each cultivar the fruits of three biological 455
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17
replicates were sampled frozen in liquid nitrogen and stored at -80deg C for further use 456
457
Tobacco plants (Nicotiana benthamiana) used for dual-luciferase assays and 458
subcellular localization analysis in this study were grown in a growth chamber with a 459
lightdark cycle of 16 h8 h at 24degC 460
461
Detection of DMMF and HDMF 462
Automated HS-SPME-GC-MS was performed to detect both furanones in lsquoYuexinrsquo 463
strawberry fruit (Zorrilla-Fontanesi et al 2012) Samples were ground into a powder 464
under liquid nitrogen for analysis 465
466
For the detection of DMMF (Figure 1) 05 g (fresh weight) of each sample was 467
weighed in the vial to which was added 1 mL of EDTA solution (100 mM pH 75) 1 468
mL of CaCl2 solution (mv = 20) and 20 microL of 2-octanol as the internal standard 469
(007 μgμL) The mixture was homogenized and the vial closed and placed on the 470
sample tray for analysis by CombiPAL autosampler (CTC Analytic CA USA) The 471
fruit volatiles were sampled by headspace solid-phase microextraction with a 65-μm 472
polydimethylsiloxane-divinylbenzene fibre (PDMS-DVB) Initially vials were 473
pre-incubated at 50degC for 10 min under continuous agitation (500 rpm) then volatiles 474
were extracted for 30 min at the same temperature and agitation speed After that the 475
fibre was desorbed in the GC injection port for 5 min in splitless mode The 7890A 476
GC chromatograph was equipped with a DB-5ms column (60 m times 250 μm times 1 μm 477
JampW Scientific Folsom CA USA) with helium as the carrier gas at a constant flow 478
of 12 mLmin The GC was programmed at an initial temperature of 35degC for 2 min 479
with a ramp of 5degC min up to 250degC and held for 5 min The injection port interface 480
and MS source temperatures were 250degC 260degC and 230degC respectively The 481
ionization potential was set at 70 eV recorded by a 5975B mass spectrometer (Agilent 482
Technologies JampW Scientific Folsom CA USA) and the scanning speed was 7 483
scanss The same method was used to analyse HDMF and DMMF in fruits from 484
different cultivars (Supplemental Figure S3) except for the sample preparation 485
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18
procedure (Araguumlez et al 2013) briefly 05 g (fresh weight) of powdered fruit was 486
incubated at 30degC in a water bath for 5 min then 2 mL of NaCl (mv = 20) and 20 487
microL of 2-octanol as the internal standard (007 μgμL) were added and homogenized 488
489
For the detection of HDMF (Figure 1) and both furanones (Figure 4 and Supplemental 490
Table S3) a liquid-injection system equipped with CTC Pal ALS was used One gram 491
(fresh weight) of powdered fruit and 2 mL of NaCl (mv = 20) were homogenized in 492
a 10-mL tube and 300 μL of CH2Cl2 and 20 microL of 2-octanol (0766 μgμL) as the 493
internal standard were added to extract the volatiles the mixture was then 494
homogenized again The tubes were stored at room temperature for 20 min and 495
centrifuged at 12000 rpm for 5 min The subnatant was pipetted into a clean 15-mL 496
tube in which 20 mg of anhydrous sodium sulphate was added the tube was left 497
without shaking for half an hour Then 150 μL of the solution was transferred into a 498
GC vial and placed on the sample tray as described above Each sample (1 μL) was 499
injected using the autosampler and the analysis was accomplished by a 7890A 500
GC-MS system (Agilent Technologies JampW Scientific Folsom CA USA) equipped 501
with a DB-WAX column (30 m times 025 mm times 025 μm JampW) Helium (12 mLmin) 502
was used as a carrier gas The injection port (splitless injection mode) interface and 503
MS source temperatures were as described above The oven temperature was set at 504
60degC for 4 min then increased to 180degC at a rate of 4degCmin and maintained for 30 505
min DMMF was identified by comparison of electron ionization mass spectra and 506
retention time data with the data from the NISTEPANIH mass spectral library 507
(NIST-08 and Flavor) HDMF (Figure 1) was identified and qualified by comparison 508
with injected standard (Sigma) The quantitative analysis of both furanones (Figure 4 509
Supplemental Table S3 and Supplemental Figure S3) was determined using the peak 510
area of the internal standard as a reference based on total ion chromatogram (TIC) 511
512
RNA isolation and Reverse Transcription Quantitative PCR (RT-qPCR) 513
Total RNA from strawberry samples was isolated in this study using the CTAB 514
method (Chang et al 1993) Genomic DNA contamination was eliminated by 515
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
19
TURBO Dnase (Ambion) 1 μg of RNA was used to obtain cDNA using an IScriptTM 516
cDNA Synthesis Kit (Bio-Rad) The synthesized cDNA was diluted with water (120) 517
and 2 μL of diluted cDNA was used as the template for RT-qPCR Reactions were 518
performed in a total volume of 20 μL consisting of 10 μL of SYBR PCR supermix 519
(Bio-Rad) 1 μL of each primer (10 μM) 6 μL of DEPC-H2O and 2 μL of diluted 520
cDNA on CFX96 instrument (Bio-Rad) (Yin et al 2012) The oligonucleotide 521
primers for RT-qPCR analysis of genes including the AP2ERF FaQR and FaOMT 522
were designed according to the coding sequences of genes and the specificity was 523
verified before use (Min et al 2012) NCBIPrimer-BLAST was applied to design the 524
primers Relative expression levels were normalized to that of an internal controlmdashthe 525
interspacer 26S-18S strawberry RNA housekeeping gene FaRIB413 526
(Zorrilla-Fontanesi et al 2012) To investigate the differential expression of genes 527
during fruit development and ripening stages relative expression of each gene at the 528
R stage in the basal fruit section was set as 1 using the 2minus∆∆119862119879 method For transient 529
overexpression assay relative expression of control fruits with an empty vector (SK) 530
was set as 1 The primers used in RT-qPCR are listed in Supplemental Table S4 531
532
Gene isolation and analysis 533
Multiple database searches were performed to identify members of the strawberry 534
(Fragaria times ananassa) AP2ERF superfamily in the published strawberry databases 535
and annotations of Fragaria times ananassa and Fragaria times vesca by using the 536
AP2ERF DNA binding domain as a query sequence and 120 genes were identified 537
with AP2ERF domain(s) Based on the BLAST result primers (listed in 538
Supplemental Table S5) were used to amplify the coding full-length cDNAs of 539
AP2ERF genes The deduced amino acid sequences of AP2ERF proteins in 540
Arabidopsis thaliana used for construction of a phylogenetic tree were obtained from 541
the Arabidopsis Information Resource (TAIR) Alignment of the proteins was 542
performed using the neighbour-joining method in ClustalX (v181) and the 543
phylogenetic tree was constructed using FigTree (v131) 544
545
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20
FaMYB98 was obtained by yeast one-hybrid screening sequencing and the full-length 546
sequences were predicted by BLAST Primers were designed (listed in Supplemental 547
Table S5) to amplify the full-length coding sequence 548
549
The promoter of FaQR was cloned by Genome Walking as previously described (Yin 550
et al 2010) and conserved cis-element motifs in the promoter were manually 551
searched 552
553
Conserved domains within the FaAP2ERF proteins and FaMYB98 were analysed by 554
CD-search (httpswwwncbinlmnihgovStructurecddwrpsbcgi) and cellular 555
locations of proteins including FaERF9 and FaMYB98 were predicted with the 556
WoLF PSORT program (httpswwwgenscriptcomwolf-psorthtml) 557
558
Dual-Luciferase Assays 559
In accordance with a previous protocol (Yin et al 2010) the full-length cDNAs of 560
FaAP2ERF or FaMYB98 transcription factors were cloned into pGreen II 0029 561
62-SK vector and the promoter of FaQR was cloned into pGreen II 0800-LUC vector 562
A luciferase gene from Renillia (REN) driven by a 35S promoter in the LUC vector 563
acted as a positive control The above constructs were transiently expressed in 564
Nicotiana benthamiana leaves by Agrobacterium-mediated infiltration (strain 565
GV3101) and the activity of the TFs on the promoter was measured on the third day 566
after infiltration indicated by the ratio of enzyme activities of firefly luciferase (LUC) 567
and renilla luciferase (REN) using a Modulus Luminometer (Promega Madison WI 568
USA) To determine the activity of a specific transcription factor towards the 569
promoter we mixed the Agrobacterium culture with 1 mL of TF and 100 μL of 570
promoter and the LUCREN value of the empty vector SK on the promoter was set as 571
1 as a calibrator To test the combined effect of two transcription factors on the 572
promoter to the Agrobacterium culture mixture we added 05 mL of each TF and 100 573
μL of promoter the effect of the mixtures that contained each transcription factor (05 574
mL) and empty vector SK (05 mL) was also tested on the promoter as a control 575
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
21
576
Subcellular localization analysis 577
35S-FaERF9-GFP and 35S-FaMYB98-GFP were transiently expressed in tobacco (N 578
benthamiana) leaves by Agrobacterium infiltration (EHA105) using the same method 579
as described in the dual-luciferase assay above The transiently infected leaves were 580
imaged on the third day after infiltration using a Nikon A1-SHS confocal laser 581
scanning microscope The excitation wavelength for GFP fluorescence was 488 nm 582
and fluorescence was detected at 490ndash520 nm The primers used for GFP construction 583
are listed in Supplemental Table S6 584
585
Transient overexpression in strawberry fruit 586
Transient overexpression of FaERF9 and an overexpression binary vector (pGreen II 587
0029 62-SK-FaERF9-FaMYB98) were performed in strawberry fruit using the 588
FaERF9-SK construct described above for the dual-luciferase assays and the binary 589
vector constructed according to Liu et al 2013 The transfection of fruit was carried 590
out at the G stage (Hoffmann et al 2006) The FaERF9-SK construct and binary 591
vector were individually electroporated into Agrobacterium tumefaciens GV3101 and 592
the Agrobacterium culture suspended in infiltration buffer was infiltrated into the 593
whole fruit using a syringe As a control treatment fruits were infiltrated with 594
Agrobacterium carrying an empty vector SK under the same transfection conditions 595
Fruits were left attached to the plants and harvested on the seventh day after 596
infiltration Fruits of three biological replicates were sampled for further analysis 597
598
Yeast one-hybrid assay 599
In order to identify proteins that bind to the FaQR promoter the Matchmaker Gold 600
Yeast One-hybrid Library Screening System (Clontech USA) was used The sequence 601
of the FaQR promoter was cloned into the pAbAi vector and the construct was 602
integrated into the genome of the Y1HGold yeast strain A mixture of total RNA from 603
strawberry fruit at four stages (G T IR R) was used to construct the prey cDNA 604
library (TaKaRa) The background AbAr expression of Y1HGold FaQR-pAbAi strain 605
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
22
was tested according to the system user manual and then screening for protein-DNA 606
interactions was carried out Furthermore the full length of each transcription factor 607
was separately cloned into pGADT7 AD vector to confirm the screening results The 608
relationship between FaERF9 and FaQR promoter was also examined individually 609
Primers used in this assay are listed in Supplemental Table S6 610
611
Expression and purification of FaMYB98 recombinant protein 612
A 405-bp region spanning the DNA-binding domain of FaMYB98 was amplified 613
from FaMYB98 cDNA and cloned into a pET6timesHN vector (Clontech Palo CA USA) 614
to generate the recombinant N-terminal His-tagged protein the primers used are listed 615
in Supplemental Table S6 The resulting construct was sequenced and introduced into 616
Escherichia coli strain Rosetta 2(DE3)pLysS (Novagen) Ten millilitres of the 617
overnight culture was combined with 500 mL of an LB liquid medium (100 μgmL 618
ampicillin and 34 μgmL chloramphenicol) as described (Li et al 2017) Isopropyl 619
β-D-1-thiogalactopyranoside (IPTG) was added to a final concentration of 1 mM and 620
the bacterial culture was incubated at 18degC at 150 rpm for 18 h Then the cells were 621
harvested using a centrifuge and resuspended in 1times PBS buffer (Sangon Biotech) 622
after which they were disrupted by sonication and the supernatant was purified using 623
a HisTALONTM Gravity Column (Clontech) according to the user manual The PD-10 624
Desalting column (GE Healthcare) was then used for buffer change and sample 625
clean-up of proteins according to the gravity protocol SDS-PAGE was performed and 626
the protein was visualized using Coomassie brilliant blue 627
628
Electrophoretic mobility shift assay (EMSA) 629
A Lightshift Chemiluminescent EMSA kit (Thermo) was used to perform EMSA 630
experiments according to the manufacturerrsquos instructions Single-strand 631
oligonucleotides were synthesized and biotinylated by GeneBio Biotech (Hangzhou 632
China) The details of the EMSA assay are provided in Ge et al (2017) The probes 633
used for EMSAs are listed in Supplemental Table S6 634
635
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
23
636
Yeast two-hybrid assay 637
The DUALhunter system (Dualsystems Biotech Switzerland) was used to investigate 638
the interaction between FaERF9 and FaMYB98 Full-length coding sequences of 639
FaERF9 and FaMYB98 were respectively cloned into pDHB1 bait vector and 640
pPR3-N prey vector sequences were verified and the bait plasmid was 641
co-transformed with prey plasmid into NMY51 in the combinations below 642
FaMYB98-pDHB1pPR3-N FaMYB98-pDHB1FaERF9-pPR3-N 643
FaMYB98-pDHB1pOst1-NubI FaERF9-pDHB1pPR3-N 644
FaERF9-pDHB1FaMYB98-pPR3-N and FaERF9-pDHB1pOst1-NubI (Li et al 645
2017) Transformed cells were spread onto the following plates DDO (SD 646
medium-Trp-Leu) QDO (SD medium-Trp-Leu-His-Ade) and QDO+3-AT (QDO 647
medium supplemented with 1 mM 3-amino-124-triazole) The control plasmid 648
pOst1-NubI was used to determine whether the bait was functional the pPR3-N prey 649
vector plasmid was used to test whether the bait displayed non-specific background 650
and positive interactions were indicated by the growth of yeast on QDO and 651
QDO+3-AT plates The Primers used in the DUALhunter assay are listed in 652
Supplemental Table S6 653
654
Bimolecular fluorescence complementation (BiFC) assays 655
Full-length FaERF9 and FaMYB98 respectively were cloned into sequences 656
encoding the N- and C- fragments of YFP protein (Lv et al 2014) All constructs 657
were transiently expressed in tobacco (N benthamiana) leaves by Agrobacterium 658
infiltration (EHA105) The YFP fluorescence of transfected leaves was imaged 40 h 659
after infiltration by using a Nikon A1-SHS confocal laser scanning microscope The 660
excitation wavelength for YFP was 488 nm and fluorescence was detected at 520ndash661
540 nm Primers used are listed in Supplemental Table S6 662
663
Statistics 664
A Studentrsquos two-tailed t test ( plt005 plt001 and plt0001) was used to 665
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
24
determine significant differences between two groups in this study Microsoft Excel 666
was used to perform linear regressive analysis significant differences were 667
determined by SPSS Statistics 200 and scatter plots were prepared with Origin80 668
Least significant difference (LSD) at the 5 level was calculated using Microsoft 669
Excel Figures were prepared with Origin80 (Microcal Software Inc Northampton 670
MA USA) The online tool MetaboAnalyst 36 (httpwwwmetaboanalystca) was 671
used to analyse the transcript abundance of the AP2ERF genes 672
673
Accession numbers 674
Sequence data from this article have been deposited in GenBank under the accession 675
numbers MH332903-MH333022 for AP2ERF genes in Fragaria times ananassa and 676
MH333023 for FaMYB98 GenBank numbers for FaQR and FaOMT were 677
AY1588361 (Raab et al 2006) and AF2204912 (Wein et al 2002) 678
679
Supplemental Material 680
Supplemental Figure S1 Phylogenetic analysis of FaAP2ERF and Arabidopsis 681
AP2ERF proteins 682
Supplemental Figure S2 Analysis of FaAP2ERF gene expression patterns in 683
strawberry fruit during development and ripening 684
Supplemental Figure S3 Contents of furanones in fruit of strawberry cultivars 685
Supplemental Figure S4 Relative expression of FaERF9 in FaERF9-FaMYB98- 686
and FaERF9-overexpressing fruits 687
Supplemental Figure S5 Subcellular localization of FaMYB98 688
Supplemental Figure S6 The combined activation effects of FaERF9FaMYB98 on 689
the FaOMT promoter 690
Supplemental Figure S7 Relative expression of FaOMT in 691
FaERF9-overexpressing fruits 692
Supplemental Table S1 AP2ERF superfamily genes in Fragaria times ananassa 693
Supplemental Table S2 Classification of the AP2ERF superfamily members in 694
Fragaria times ananassa 695
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
25
Supplemental Table S3 Furanone content in FaERF9-FaMYB98- and 696
FaERF9-overexpressing fruits 697
Supplemental Table S4 Primers used for reverse transcription quantitative PCR 698
(RT-qPCR) 699
Supplemental Table S5 Primers used to amplify the full-length coding sequences of 700
AP2ERF genes and FaMYB98 in strawberry (Fragaria times ananassa) 701
Supplemental Table S6 Primers used for vector construction 702
703
Acknowledgments 704
This research was supported by the National Key Research and Development 705
Program (2016YFD0400101) the Project of the Science and Technology Department 706
of Zhejiang Province (2016C04001) and the 111 Project (B17039) 707
708
Figure legends 709
Figure 1 Changes in furanone content and furanone biosynthetic genes during 710
strawberry (Fragaria times ananassa Duch cv Yuexin) fruit development and ripening 711
A Fruits were collected at four ripening stages G (green stage) T (turning stage) IR 712
(intermediate red stage) R (full red stage) B Changes in the contents of furaneol 713
(HDMF) and mesifurane (DMMF) HDMF content was calculated using a standard 714
curve of HDMF while DMMF content was calculated with an internal standard as the 715
reference C Expression levels of FaQR and FaOMT The expression levels of each 716
gene were calculated relative to corresponding values in the basal section at the R 717
stage SEs were calculated from three replicates and LSD values represent the least 718
significant differences at p = 005 719
Figure 2 Regulatory effects of FaAP2ERF on the promoter of FaQR LUCREN 720
values of the empty vector on FaQR promoter were used as the calibrator set as 1 721
and SEs were calculated from five replicates statistical significance was determined 722
by Studentrsquos two-tailed t test ( plt0001) 723
Figure 3 Expression and the subcellular localization of FaERF9 A The expression 724
levels were calculated relative to the levels in the basal section at the R stage B 725
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
26
Subcellular localization analysis was performed in tobacco leaves The tobacco used 726
in the assay was stably transformed with a specific nucleus localized red fluorescence 727
protein construct and the red fluorescence indicates the nucleus-localized signal 728
(NLS) Scale bar = 25 microm SEs were calculated from three replicates 729
Figure 4 Transient overexpression of FaERF9 in strawberry fruit A Relative 730
expression of FaQR and FaERF9 in FaERF9-OX fruit 7 days after infiltration The 731
expression was calculated relative to the average value in control (SK) fruits B 732
HDMF and DMMF content in FaERF9-OX fruit The content of both furanones 733
were quantified using the peak area of the internal standard (2-octanol) as the 734
reference SEs were calculated from three replicates Statistical significance was 735
determined by Studentrsquos two-tailed t test ( plt005 plt001 plt0001) 736
Figure 5 Scatter plots of 11 strawberry cultivars A Linear regression analysis 737
between FaERF9 expression and FaQR expression B Linear regression analysis 738
between FaERF9 expression and furanone content The relative expression was 739
normalized to that of the housekeeping gene FaRIB413 and furanone content was 740
calculated with internal standard as the reference Significant differences were 741
determined by SPSS Statistics 200 742
Figure 6 Interactions of FaERF9 and FaMYB98 with the FaQR promoter A Yeast 743
one-hybrid analysis of the interaction of FaERF9 and FaQR promoter B Yeast 744
one-hybrid analysis of the interaction of FaMYB98 and FaQR promoter C 745
Regulatory effect of FaMYB98 on the FaQR promoter Auto-activation was tested on 746
SD-Ura (synthetically defined medium without uracil) in presence of Aureobasidin A 747
(AbA) and physical interaction was determined on SD-Leu (synthetically defined 748
medium without leucine) in presence of AbA LUCREN values of the empty vector 749
on FaQR promoter were used as the calibrator set as 1 and error bars were calculated 750
from five replicates Statistical significance was determined by Studentrsquos two-tailed t 751
test ( plt005 plt001 plt0001) 752
Figure 7 Electrophoretic mobility shift assay of FaMYB98 binding to FaQR 753
promoter A The probe sequence used for EMSA and mutated nucleotides are 754
indicated with lowercase letters B Purified DNA-binding domain of FaMYB98 755
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
27
protein and biotin-labelled DNA probe were mixed and analysed on 6 native 756
polyacrylamide gels and then photographed Presence or absence of specific probes is 757
marked by the symbol + or - 758
Figure 8 The combined activation effects of FaERF9FaMYB98 on the FaQR 759
promoter LUCREN values obtained with the empty vector and FaQR promoter were 760
used as the calibrator set as 1 and error bars were calculated from five replicates 761
Figure 9 Yeast two-hybrid analysis of the protein-protein interactions between 762
FaMYB98 and FaERF9 Positive interactions were determined by the growth of 763
yeast cells on selection plates Bait with pOST acted as positive controls and bait with 764
pPR3 as negative controls DDO synthetically defined medium without tryptophan 765
and leucine QDO synthetically defined medium without tryptophan leucine 766
histidine and adenine QDO+3AT QDO medium supplemented with 1 mM 767
3-aminotriazole 768
Figure 10 BiFC analysis of the protein-protein interactions between FaMYB98 and 769
FaERF9 The pairs of fusion proteins tested were FaMYB98-YFPN+FaERF9-YFPC 770
FaERF9-YFPN+FaMYB98-YFPC FaMYB98-YFPN+FaMYB98-YFPC and 771
FaERF9-YFPN+FaERF9-YFPC The other combinations were negative controls 772
The tobacco used in the assay was stably transformed with a specific 773
nucleus-localized red fluorescence protein construct and the red fluorescence 774
indicated the nucleus-localized signal (NLS) Fluorescence of the yellow fluorescence 775
protein (YFP) visualized the interaction in vivo Scale bar = 25 microm 776
777
Literature Cited 778
779
Agarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression 780
of PgDREB2A transcription factor enhances abiotic stress tolerance and activates 781
downstream stress-responsive genes Mol Biol Rep 37 1125-1135 782
Araguumlez I Osorio S Hoffmann T Rambla JL Medina-Escobar N Granell A 783
Botella MAacute Schwab W Valpuesta V (2013) Eugenol production in achenes and 784
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28
receptacles of strawberry fruits is catalyzed by synthases exhibiting distinct kinetics 785
Plant Physiol 163 946-958 786
Carvalho RF Carvalho SD OrsquoGrady K Folta KM (2016) Agroinfiltration of 787
strawberry fruit mdash a powerful transient expression system for gene validation Curr 788
Plant Biol 6 19-37 789
Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic 790
(Amsterdam) 210 34-40 791
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating 792
RNA from pine trees Plant Mol Biol Rep 11 113-116 793
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC 794
Clark DG (2011) PhMYB4 fine-tunes the floral volatile signature of 795
Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143 796
Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz 797
EA Taylor MG Smits-Kroon MT Schuurink RC Haring MA Giovannoni J 798
Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic 799
pathway by ectopic expression of a MYB transcription factor in tomato fruit Plant 800
Cell 23 2738-2753 801
Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan 802
XW Yang ZY (2017) Differential responses of four biosynthetic pathways of 803
aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under 804
interaction of light and temperature Food Chem 221 356-364 805
Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of 806
differentially-expressed genes during somatic embryogenesis in Fragaria times 807
ananassa Duch lsquoBenihopprsquo J Hortic Sci Biotechnol 90 671-681 808
Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 809
transcriptionally regulates chilling-induced lignification of loquat fruit via physical 810
interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136 811
Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM 812
(2004) Functional interactions between a glutamine synthetase promoter and MYB 813
proteins Plant J 39 513-526 814
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29
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) 815
Sucrose nonfermenting1-related protein kinase26 an ortholog of open stomata1 is 816
a negative regulator of strawberry fruit development and ripening Plant Physiol 817
167 915-930 818
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene 819
expression in strawberry fruit (Fragaria times ananassa) by agroinfiltration a rapid 820
assay for gene function analysis Plant J 48 818-826 821
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of 822
selected aroma-active compounds in strawberries by headspace solid-phase 823
microextraction gas chromatography and correlation with sensory descriptive 824
analysis J Food Sci 72 S487-S496 825
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid 826
plays an important role in the regulation of strawberry fruit ripening Plant Physiol 827
157 188-199 828
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of 829
NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes BMC 830
Plant Biol 6 20 831
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN 832
(2005) MYB98 is required for pollen tube guidance and synergid cell differentiation 833
in Arabidopsis Plant Cell 17 2981-2992 834
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional 835
characterization of enone oxidoreductases from strawberry and tomato fruit J 836
Agric Food Chem 55 6705-6711 837
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You 838
J-S Rohloff J Randall SK Alsheikh M (2012) Proteomic study of 839
low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ 840
in cold tolerance Plant Physiol 159 1787-1805 841
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional 842
characterization of four APETALA2-family genes (RAP26 RAP26L DREB19 843
and DREB26) in Arabidopsis Plant Mol Biol 75 107-127 844
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
30
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon 845
J Gupta V (2013) An oxidoreductase from lsquoAlphonsorsquo mango catalyzing 846
biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494 847
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in 848
strawberries Z Lebensm-Unters Forsch 195 120-123 849
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X 850
(2015) Label-free quantitative proteomics to investigate strawberry fruit proteome 851
changes under controlled atmosphere and low temperature storage J Proteomics 852
120 44-57 853
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 854
cooperates with CitWRKY1 to participate in citric acid degradation via 855
up-regulation of CitAco3 J Exp Bot 68 3419-3426 856
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription 857
factor CitERF71 activates the terpene synthase gene CitTPS16 involved in the 858
synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938 859
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and 860
transcriptomic analysis of the AP2ERF superfamily in Vitis vinifera BMC 861
Genomics 11 719 862
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive 863
Factor (AP2ERF) transcription factors mediators of stress responses and 864
developmental programs New Phytol 199 639-649 865
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 866
interacting with EOBI negatively regulates fragrance biosynthesis in petunia 867
flowers New Phytol 215 1490-1502 868
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu 869
CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 in regulating 870
anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) 871
during anthocyanin biosynthesis Plant Cell Tissue Organ Cult 115 285-298 872
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31
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao 873
CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphate signaling and 874
homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597 875
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC 876
Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL 877
Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor 878
regulates eugenol production in ripe strawberry fruit receptacles Plant Physiol 168 879
598-614 880
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics 881
and volatile constituents of strawberry (cv Cigaline) during maturation J Agric 882
Food Chem 52 1248-1254 883
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS 884
(2012) Ethylene-responsive transcription factors interact with promoters of ADH 885
and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 886
63 6393-6405 887
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM 888
Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-Franco A 889
Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific 890
transcription factor FaDOF2 regulates the production of eugenol in ripe fruit 891
receptacles J Exp Bot 68 4529-4543 892
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) 893
Comparison and verification of the genes involved in ethylene biosynthesis and 894
signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44 895
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the 896
ERF gene family in Arabidopsis and rice Plant Physiol 140 411-432 897
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in 898
sour cherry and strawberry and the heterologous expression of CBF1 in strawberry 899
J Am Soc Hortic Sci 127 489-494 900
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech 901
JC Ohme-Takagi M Regad F Bouzayen M (2012) Functional analysis and 902
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
32
binding affinity of tomato ethylene response factors provide insight on the 903
molecular bases of plant differential responses to ethylene BMC Plant Biol 12 190 904
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) 905
Methylpentoses are possible precursors of furanones in fruits Prikl Biokhim 906
Mikrobiol 28 123-127 907
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery 908
of synergid-expressed genes encoding filiform apparatus localized proteins Plant 909
Cell 19 2557-2568 910
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria 911
vesca L compared to those of cultivated berries Fragariatimes ananassa cv Senga 912
Sengana J Agric Food Chem 27 19-22 913
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W 914
Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of the strawberry 915
flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone 916
oxidoreductase Plant Cell 18 1023-1037 917
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L 918
Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim M Broun P Zhang 919
JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription 920
factors genome-wide comparative analysis among eukaryotes Science 290 921
2105-2110 922
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the 923
formation of 25-dimethyl-4-hydroxy-3(2H)-furanone in detached ripening 924
strawberry fruits J Agric Food Chem 46 1488-1493 925
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 926
25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in 927
strawberry fruits Phytochemistry 43 155-159 928
Schwab W (1998) Application of stable isotope ratio analysis explaining the 929
bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone in plants by a biological 930
maillard reaction J Agric Food Chem 46 2266ndash2269 931
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
33
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) 932
Molecules 18 6936-6951 933
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard 934
products Recent Res Dev Phytochem 1 643-673 935
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL 936
Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJ Sims CA 937
Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical 938
compositions a seasonal influence and effects on sensory perception PLoS One 9 939
e88446 940
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) 941
Identification phylogeny and transcript profiling of ERF family genes during 942
development and abiotic stress treatments in tomato Mol Genet Genomics 284 943
455-475 944
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) 945
CitAP210 activation of the terpene synthase CsTPS1 is associated with the 946
synthesis of (+)-valencene in lsquoNewhallrsquo orange J Exp Bot 67 4105-4115 947
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes 948
Dev Genes Evol 214 105-114 949
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K 950
Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the 951
key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151 952
Spitzer-Rimon B Farhi M Albo B Cnarsquoani A Ben Zvi MM Masci T Edelbaum 953
O Yu YX Shklarman E Ovadis M Vainstein A (2012) The R2R3-MYB-like 954
regulatory factor EOBI acting downstream of EOBII regulates scent production 955
by activating ODO1 and structural scent-related genes in petunia Plant Cell 24 956
5089-5105 957
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp 958
Bot 68 4407-4409 959
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla 960
JF Amaya I Giavalisco P Fernie AR Botella MA Valpuesta V (2015) Central 961
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
34
role of FaGAMYB in the transition of the strawberry receptacle from development 962
to ripening New Phytol 208 482-496 963
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 964
regulates fragrance biosynthesis in petunia flowers Plant Cell 17 1612-1624 965
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS 966
(2018) The potassium channel FaTPK1 plays a critical role in fruit quality 967
formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748 968
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) 969
Isolation cloning and expression of a multifunctional O-methyltransferase capable 970
of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma 971
compounds in strawberry fruits Plant J 31 755-765 972
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor 973
types their evolutionary origin and species distribution In A handbook of 974
transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular 975
Biochemistry 52 25-73 976
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of 977
odor (Buettner A Ed) Springer Cham 9-10 978
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS 979
(2014) Isolation classification and transcription profiles of the AP2ERF 980
transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271 981
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in 982
regulation of fruit quality Crit Rev Plant Sci 35 120-130 983
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ 984
Zhang SL Wu J (2017) Map-based cloning of the pear gene MYB114 identifies an 985
interaction with other transcription factors to coordinately regulate fruit 986
anthocyanin biosynthesis Plant J 92 437-451 987
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes 988
involved in regulating fruit ripening Plant Physiol 153 1280-1292 989
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
35
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) 990
Expression of ethylene response genes during persimmon fruit astringency removal 991
Planta 235 895-906 992
Zabetakis I Gramshaw JW Robinson DS (1999) 993
25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis and 994
biosynthesis-a review Food Chem 65 139-151 995
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci 996
Food Agric 74 421-434 997
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 998
an AP2ERF gene is a novel regulator of fruit lignification induced by chilling 999
injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1000
1325-1334 1001
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation 1002
classification and transcription profiles of the Ethylene Response Factors (ERFs) in 1003
ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215 1004
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML 1005
(2012) Genome-wide analysis of the AP2ERF superfamily in peach (Prunus 1006
persica) Genet Mol Res 11 4788-4809 1007
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and 1008
expression analysis of a CRTDRE-binding factor gene FaCBF1 from Fragaria times 1009
ananassa Acta Hortic 41 240-248 1010
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The 1011
Arabidopsis AP2ERF transcription factor RAP26 participates in ABA salt and 1012
osmotic stress responses Gene 457 1-12 1013
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B 1014
Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) Genome-wide 1015
analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic 1016
(Amsterdam) 123 73-81 1017
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF 1018
Valpuesta V Botella MA Granell A Amaya I (2012) Genetic analysis of 1019
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
36
strawberry fruit aroma and identification of O-methyltransferase FaOMT as the 1020
locus controlling natural variation in mesifurane content Plant Physiol 159 1021
851-870 1022
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
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wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
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Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery of synergid-expressed genes encoding filiformapparatus localized proteins Plant Cell 19 2557-2568
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria vesca L compared to those of cultivated berriesFragariatimes ananassa cv Senga Sengana J Agric Food Chem 27 19-22
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of thestrawberry flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone oxidoreductase Plant Cell 18 1023-1037
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim MBroun P Zhang JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription factors genome-wide comparative analysisamong eukaryotes Science 290 2105-2110
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the formation of 25-dimethyl-4-hydroxy-3(2H)-furanonein detached ripening strawberry fruits J Agric Food Chem 46 1488-1493
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in strawberry fruits Phytochemistry 43 155-159
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (1998) Application of stable isotope ratio analysis explaining the bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone inplants by a biological maillard reaction J Agric Food Chem 46 2266ndash2269
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) Molecules 18 6936-6951Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard products Recent Res Dev Phytochem 1 643-673Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJSims CA Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical compositions a seasonal influence and effects on sensoryperception PLoS One 9 e88446
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) Identification phylogeny and transcript profiling of ERFfamily genes during development and abiotic stress treatments in tomato Mol Genet Genomics 284 455-475
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) CitAP210 activation of the terpene synthase CsTPS1 isassociated with the synthesis of (+)-valencene in Newhall orange J Exp Bot 67 4105-4115
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes Dev Genes Evol 214 105-114Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Spitzer-Rimon B Farhi M Albo B Cnaani A Ben Zvi MM Masci T Edelbaum O Yu YX Shklarman E Ovadis M Vainstein A (2012) TheR2R3-MYB-like regulatory factor EOBI acting downstream of EOBII regulates scent production by activating ODO1 and structuralscent-related genes in petunia Plant Cell 24 5089-5105
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp Bot 68 4407-4409Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla JF Amaya I Giavalisco P Fernie AR Botella MAValpuesta V (2015) Central role of FaGAMYB in the transition of the strawberry receptacle from development to ripening New Phytol208 482-496
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 regulates fragrance biosynthesis in petunia flowers PlantCell 17 1612-1624
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS (2018) The potassium channel FaTPK1 plays a critical role infruit quality formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) Isolation cloning and expression of a multifunctional O- wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma compounds in strawberry fruitsPlant J 31 755-765
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor types their evolutionary origin and speciesdistribution In A handbook of transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular Biochemistry 52 25-73
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of odor (Buettner A Ed) Springer Cham 9-10Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS (2014) Isolation classification and transcription profiles ofthe AP2ERF transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in regulation of fruit quality Crit Rev Plant Sci 35 120-130
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ Zhang SL Wu J (2017) Map-based cloning of the pear geneMYB114 identifies an interaction with other transcription factors to coordinately regulate fruit anthocyanin biosynthesis Plant J 92437-451
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes involved in regulating fruit ripening Plant Physiol 1531280-1292
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) Expression of ethylene response genes during persimmonfruit astringency removal Planta 235 895-906
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zabetakis I Gramshaw JW Robinson DS (1999) 25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis andbiosynthesis-a review Food Chem 65 139-151
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci Food Agric 74 421-434Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 an AP2ERF gene is a novel regulator of fruit lignificationinduced by chilling injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1325-1334
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation classification and transcription profiles of the Ethylene ResponseFactors (ERFs) in ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML (2012) Genome-wide analysis of the AP2ERF superfamily inpeach (Prunus persica) Genet Mol Res 11 4788-4809
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and expression analysis of a CRTDRE-binding factor gene FaCBF1from Fragaria times ananassa Acta Hortic 41 240-248
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The Arabidopsis AP2ERF transcription factor RAP26 participatesin ABA salt and osmotic stress responses Gene 457 1-12
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Genome-wide analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic (Amsterdam) 123 73-81Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF Valpuesta V Botella MA Granell A Amaya I (2012) Geneticanalysis of strawberry fruit aroma and identification of O-methyltransferase FaOMT as the locus controlling natural variation inmesifurane content Plant Physiol 159 851-870
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
6
4-hydroxy-5-methyl-2-methylene-3(2H)-furanone (HMMF) and Fragaria times 126
ananassa quinone oxidoreductase (FaQR later renamed as FaEO) was identified as 127
the enzyme responsible for reduction of the α β-unsaturated bond of HMMF to form 128
the aroma-active compound HDMF (Raab et al 2006 Klein et al 2007) An 129
O-methyltransferase FaOMT subsequently generates DMMF by methylation of 130
HDMF (Wein et al 2002) HDMF can also be metabolized to 131
25-dimethyl-4-hydroxy-2H-furan-3-one glucoside (HDMF-glucoside) by a 132
UDP-dependent glycosyltransferase (UGT71K3) and further malonylated into 133
25-dimethyl-4-hydroxy-2H-furan-3-one 6rsquo-O-malonyl-β-D-glucopyranoside (HDMF 134
malonyl-glucoside) in strawberry fruit (Roscher et al 1996 Song et al 2016) The 135
biosynthetic pathway of HDMF in other plants is similar to that in strawberry Genes 136
with homology to FaQR have been identified in tomato (SlEO) and mango (MIEO) 137
(Klein et al 2007 Kulkarni et al 2013) 138
139
As an NADH-dependent enone oxidoreductase protein FaQR exhibits o-quinone 140
oxidoreductase activity (Raab et al 2006) FaQR mRNA accumulates in fruit 141
parenchyma tissues but is absent in vascular tissues and FaQR is mainly expressed in 142
the late stages of fruit growth and ripening paralleling furaneol production in the fruit 143
(Raab et al 2006) FaQR is responsive to environmental stimuli associated with 144
furaneol production and in the dark lsquoSweet Charliersquo strawberry fruits have higher 145
levels of FaQR expression and HDMF production at 25degC than at 15degC (Fu et al 146
2017) in contrast the concentration of furanones and the abundance of FaQR protein 147
under low-temperature storage is significantly lower than those under 148
room-temperature storage (Li et al 2015) Thus the regulation of FaQR is important 149
for manipulating furaneol content Although it is assumed that transcription factors 150
control expressions of genes involved in volatile production in plants no such factors 151
regulating FaQR or other furanone biosynthetic genes have been identified 152
153
Different members of the largely plant-specific AP2ERF gene family (Weirauch and 154
Hughes 2011) have diverse functions in plant growth development and stress 155
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
7
responses (Agarwal et al 2010 Zhu et al 2010 Licausi et al 2013) In recent years 156
several AP2ERF genes have been reported to regulate aspects of fruit quality (Xie et 157
al 2016) including fruit aroma For example CitAP210 is associated with the 158
synthesis of (+)-valencene in Newhall orange acting via regulation of CsTPS1 (Shen 159
et al 2016) CitERF71 was shown to physically bind to the CsTPS16 promoter and 160
contribute to the synthesis of E-geraniol in citrus fruit (Li et al 2017) These 161
observations raised the possibility that FaQR might also be a target for a member of 162
the AP2ERF family and that ERFs might also control furaneol biosynthesis 163
164
In this study screening of the Fragaria times ananassa AP2ERF gene family led to 165
identification of FaERF9 as an activator of FaQR however it did not bind directly 166
to the promoter A parallel search for proteins that directly bind the FaQR promoter 167
using yeast one-hybrid screening identified a second factor FaMYB98 which was 168
capable of physically interacting with the FaQR promoter FaMYB98 physically 169
interacts with FaERF9 and transient expression assays demonstrated a synergistic 170
effect on FaQR expression and furanone synthesis 171
172
Results 173
Changes in the content of both furanones and the activity of their biosynthetic 174
genes in strawberry fruit 175
lsquoYuexinrsquo fruits at four developmental and ripening stages (G green T turning IR 176
intermediate red R full red) were harvested (Figure 1) and determination of HDMF 177
levels indicated a major increase from about 065 μg per gram fruit at the IR stage to 178
346 μg at the R stage in the apical section implying that furaneol accumulation was 179
closely related to colour change and ripening (Figure 1) Furaneol levels were higher 180
in the apical section than in the basal section HDMF could not be detected at the IR 181
stage in the basal section but the amount increased at the R stage to 142 μg per gram 182
fruit Differences were also found for DMMF with the relative content in the apical 183
section 018 μg per gram at the R stage compared to 008 μg per gram in the basal 184
section at the same stage 185
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8
186
Measurement of mRNA levels by RT-qPCR indicated that the transcript levels of both 187
FaQR (GenBank AY1588361) and FaOMT (GenBank AF2204912) increased 188
throughout ripening (Figure 1) Comparison of the expression of these genes showed 189
that the transcript levels of FaQR and FaOMT significantly increased as early as in T 190
stage in basal fruit sections and for each gene over half of the peak transcript 191
abundance occurred as early as in IR stage in the apical section while for the basal 192
section it was in the R stage indicating a gradient of gene expression and volatile 193
production from apex to base of the fruit during ripening 194
195
Genome-wide identification of AP2ERF gene family in strawberry 196
Coding sequences of 120 non-redundant FaAP2ERF genes were isolated and 197
identified from lsquoYuexinrsquo strawberry and a systematic nomenclature for the AP2ERF 198
family genes was used to distinguish the members based on the structural features 199
defined previously (Supplemental Table S1) (Shigyo and Ito 2004 Nakano et al 200
2006 Licausi et al 2013) CD-search analysis showed that this superfamily is 201
consisted of 95 ERFs 18 AP2 and 6 RAV family members and 1 soloist member 202
(Supplemental Table S2) Phylogenetic analysis of the Fragaria times ananassa and 203
Arabidopsis AP2ERF members is shown in Supplemental Figure S1 with the 120 204
AP2ERF genes divided into three major groups (ERF AP2 RAV) and a soloist and 205
the ERF family being further divided into 10 groups (groups I to X in Supplemental 206
Table S1) 207
208
We performed a dual-luciferase assay to determine the ability of 116 FaAP2ERF 209
members to activate transcription from the promoter of FaQR The results indicated 210
about 12 members (mainly belonging to the ERF and RAV families) showed a 211
significant activation effect on the FaQR promoter while the remaining members 212
showed very limited effects (Figure 2) The relative activity of only the following 12 213
FaAP2ERF transcripts reached the threshold value set at 2 FaERF8FaERF9 214
(group II) FaERF27FaERF29FaERF31FaERF32 (group IV) 215
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9
FaERF37FaERF38 (group V) FaERF62FaERF64 (group VIII) FaERF68 216
(group IX) and FaRAV4 (Figure 2) Of these FaERF9 exhibited the highest 217
activation effect on the FaQR promoter (466-fold) (Figure 2) The strawberry 218
FaERF9 cDNA is 699 bp long and ExPASy Compute pIMw tool analysis indicated 219
that this gene encodes a 232-amino acid protein with a calculated molecular mass of 220
254 KD and a pI of 56 221
222
FaERF9 expression pattern and subcellular localization 223
To further explore the connections between AP2ERFs and furaneol biosynthesis we 224
obtained the transcript profiles of the AP2ERF genes in strawberry fruit samples at 225
different fruit developmental and ripening stages by reverse transcription quantitative 226
PCR (RT-qPCR) excluding genes with very low abundance in the fruit samples The 227
results presented as a heatmap (Supplemental Figure S2) demonstrate that these 228
genes displayed various expression patterns in both the apical and basal sections and 229
by analysing the expression patterns of the members indicated as activators in the 230
dual-luciferase assay we found that only a few genes including FaERF8 FaERF9 231
FaERF27 FaERF32 and FaERF37 were up-regulated during ripening stages and 232
their expression correlated with furaneol accumulation in the fruit (Figure 1) 233
Furthermore the expression patterns of the up-regulated genes in the apical and basal 234
sections showed that one ERF gene FaERF9 not only showed an up-regulation 235
pattern in both sections but its expression in the apical section occurred ahead of that 236
in the basal section (Figure 3) consistent with the actual changes in furaneol content 237
(Figure 1) and the expression pattern of FaQR (Figure 1) The subcellular localization 238
of FaERF9 was predicted to be in the nucleus using the WoLF PSORT program In 239
experimental tests 35S-FaERF9-GFP (green fluorescence protein) showed strong 240
fluorescence in the nucleus and the green signal merged with the red fluorescence 241
signal of mCherry-nucleus-marker in tobacco plants (Figure 3) 242
243
Transient overexpression of FaERF9 in strawberry 244
The expression of FaERF9 in agro-infiltrated fruits was analysed by performing 245
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
10
RT-qPCR on the seventh day after infiltration by which time they had reached the IR 246
or R stage and the result showed that the transcript levels were significantly higher 247
(52-fold) than in control fruits (Figure 4) The expression of FaQR was examined in 248
the same fruits and the transcript abundance also increased 22-fold The relative 249
content of HDMF in the FaERF9-overexpressing fruits was 008 μg per gram fruit 250
and undetectable in the control fruits (Figure 4) The relative content of DMMF in the 251
overexpressing fruits was also significantly increased to 038 μg per gram fruit 252
compared to 004 μg per gram fruit in the control (Figure 4) These observations 253
provide direct evidence for a regulatory role for FaERF9 in promoting FaQR 254
biosynthesis and activity in ripening strawberry fruit Taken together these results 255
indicate that by activating the transcription of FaQR FaERF9 functions as a positive 256
regulator in furaneol biosynthesis 257
258
Correlation of FaERF9 expression and FaQR transcript profiles 259
GC-MS quantification showed that furanones are distributed in variable levels among 260
different strawberry cultivars (Supplemental Figure S3) The transcript profiles of 261
FaQR and FaERF9 in fruits of different cultivars were measured and linear 262
regression analysis was performed In the cultivars the changes in FaQR transcripts 263
correlated positively with those in FaERF9 transcripts (r = 079 plt001) (Figure 5) 264
In addition FaERF9 transcript levels also correlated with furanone content across 265
cultivars (Figure 5) 266
267
FaERF9 is an indirect regulator of the FaQR promoter and acts via 268
protein-protein interaction with FaMYB98 269
Although the results of the dual-luciferase assay expression analysis transient 270
overexpression and correlation analysis were all consistent with the suggestion that 271
FaERF9 regulates transcript abundance by acting on the FaQR promoter a yeast 272
one-hybrid assay indicated that FaERF9 cannot bind directly to the FaQR promoter 273
(Figure 6) This led us to speculate that activation may occur via a transcription 274
complex involving an additional as-yet unknown regulator which can bind directly to 275
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
11
the FaQR promoter 276
277
In parallel with the investigation of the FaAP2ERF genes a cDNA library screening 278
was performed with a yeast one-hybrid assay using the promoter of FaQR as the bait 279
This screen identified several transcription factors that could physically bind to the 280
FaQR promoter but only one MYB could activate transcription from the FaQR 281
promoter (approximately 56-fold) relative to the control (Figure 6) in the 282
dual-luciferase assay This MYB showed 44 amino acid identity with MYB98 283
(GenBank ABA420611) a transcriptional regulator in the synergid cells in 284
Arabidopsis (Kasahara et al 2005) and it was designated as FaMYB98 The 285
specificity of FaMYB98 binding to the FaQR promoter was confirmed by EMSA 286
assay (Figure 7) and increasing the concentration of the cold probe reduced binding 287
In addition mutating the putative binding sites (Goacutemez-Maldonado et al 2004 288
Punwani et al 2007) as shown in Figure 7 eliminated FaMYB98 protein binding 289
When the combined effect of FaERF9 and FaMYB98 was analysed (Figure 8) a 290
synergistic 14-fold activation of the FaQR promoter was observed compared with the 291
activation by either FaERF9 or FaMYB98 which alone promoted transactivation 292
39-fold and 45-fold respectively In addition overexpression of both genes 293
(FaERF9-FaMYB98-SK) in strawberry fruits resulted in higher expression of 294
FaERF9 transcripts and higher furanone content than overexpression of FaERF9 295
(Supplemental Figure S4 Supplemental Table S3) Subcellular localization analysis 296
revealed that FaMYB98 was also localized in the nucleus (Supplemental Figure S5) 297
298
To investigate the potential interactions between FaERF9 and FaMYB98 the 299
DUALhunter system was used (Figure 9) Cells expressing the FaMYB98 and 300
FaERF9 protein pair using either FaMYB98 or FaERF9 as the bait grew on DDO 301
QDO and QDO supplemented with 1 mM 3-AT selective medium indicating 302
interaction between the two proteins This putative protein-protein interaction was 303
confirmed by BiFC assay and the combinations of FaMYB98-YFPNFaERF9-YFPC 304
and FaERF9-YFPNFaMYB98-YFPC exhibited strong coincident signals in the 305
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
12
nucleus while negative controls produced no detectable fluorescence signal (Figure 306
10) In addition coexpression of FaERF9-YFPNFaERF9-YFPC as well as 307
FaMYB98-YFPNFaMYB98-YFPC also generated signals in the nucleus indicating 308
that FaERF9 and FaMYB98 both could form homodimers or possibly multimers in 309
the nucleus (Figure 10) 310
311
Discussion 312
The AP2ERF superfamily in strawberry 313
The AP2ERF superfamily of plant transcription factors is defined by the AP2ERF 314
domain and comprises the ERF AP2 and RAV families as well as one soloist member 315
(Riechmann et al 2000 Weirauch and Hughes 2011) The completion of multiple 316
plant genome sequences has enabled a genome-scale analysis of the AP2ERF family 317
which in recent years has been systematically studied in diverse fruit species such as 318
tomato grape peach and kiwi fruit (Zhuang et al 2009 Sharma et al 2010 Licausi 319
et al 2010 Yin et al 2010 Pirrello et al 2012 Zhang et al 2012 Zhang et al 320
2016) A few AP2ERF genes have been isolated and characterized in strawberry and 321
CBF orthologs (Owens et al 2002 Koehler et al 2012 Zhang et al 2014) have 322
been identified from different strawberry cultivars in several independent studies 323
Although they have distinct names eg Fragaria times ananassa CBF1 (FaCBF1) 324
FaCBF4 (GenBank HQ9105151) and CBF1 (GenBank EU1172142) according to 325
the phylogenetic tree generated in this study the orthologs of 326
CBF1CBF4CBF2CBF3 in Arabidopsis are similar to each other and to FaERF20 327
(Supplemental Figure S1) (Owens et al 2002 Koehler et al 2012 Zhang et al 328
2014) FaERF20 has 85 sequence similarity with FaCBF1 identified by Owens et 329
al (2002) 93 similarity with FaCBF4 amplified by Koehler et al (2012) and 75 330
similarity with CBF1 cloned by Zhang et al (2014) The AP2ERF genes 331
characterized in other studies (Jia et al 2011 GAO et al 2015 Chai and Shen 2016 332
Mu et al 2016) are also noted in Supplemental Table S1 333
334
Based on the computational analysis we have identified a total of 120 AP2ERF 335
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13
genes in octoploid strawberry (Supplemental Table S1) The number of predicted 336
AP2ERF genes (120) is comparable to those observed in other fruits including 337
tomato (112) Chinese plum (116) citrus (126) and peach (131) but lower than those 338
reported for grape (149) (Xie et al 2016) As shown in Supplemental Table S2 79 339
(95 genes) of the AP2ERF genes belong to the ERF family in strawberry constituting 340
the largest sub-family The members of this sub-family can be classified into 10 341
groups (group I to X) according to their sequence similarities to the Arabidopsis ERF 342
genes (Nakano et al 2006) The AP2 family encompasses the same number of genes 343
in Arabidopsis citrus and strawberry (eighteen) (Nakano et al 2006 Xie et al 2014) 344
and there are six RAV genes in strawberry which are highly conserved in dicots such 345
as Vitis vinifera Arabidopsis thaliana and Populus trichocarpa (Licausi et al 2010) 346
347
Role of FaERF9 in regulating the biosynthesis of HDMF a positive regulator 348
acting in an indirect manner 349
The large-scale screening of the AP2ERF superfamily in strawberry led to 350
identification of 11 ERFs and 1 RAV that trans-activated the FaQR promoter more 351
than two-fold with the highest activation caused by FaERF9 which trans-activated 352
the FaQR promoter (Figure 2) as well as up-regulating FaQR expression and furanone 353
production in transient overexpression assays (Figure 4) which has been extensively 354
used to explore the fruit-associated gene functions in strawberry (Han et al 2015 355
Medina-Puche et al 2015 Vallarino et al 2015 Carvalho et al 2016 Song et al 356
2016 Wang et al 2018) FaERF9 transcripts accumulate in the fruit apical section 357
before the basal section (Figure 3) a finding consistent with the actual changes in 358
furaneol content (Figure 1) and the expression of FaQR (Figure 1) The association 359
between FaERF9 transcripts and accumulation of furanones were also established 360
with different strawberry cultivars The correlation between FaERF9 and FaQR 361
expression as well as furanone content among cultivars supports a positive role of 362
FaERF9 in regulating furanone content (Figure 5) These results indicate that 363
FaERF9 transcript abundance may be a good indicator of the abundance of these 364
important flavour volatiles in fruits of different cultivars This should be considered as 365
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14
a method for high-throughput variety screening to replace direct measurement of 366
volatiles 367
368
FaERF9 is a member of the ERF group II family and is most closely related to the 369
Arabidopsis genes At1g44830 (ATERF014) At1g21910 (DREB26) and At1g77640 370
(Supplemental Figure S1) At1g44830 was observed to be strongly up-regulated in a 371
comprehensive microarray analysis of the root transcriptome following NaCl 372
exposure (Jiang and Deyholos 2006) At1g21910 (DREB26) was functionally 373
characterized as a trans-activator localized in the nucleus exhibiting tissue-specific 374
expression and participating in plant developmental processes as well as biotic andor 375
abiotic stress signalling (Krishnaswamy et al 2011) However none of these genes 376
have been reported as furanone regulators In strawberry another five genes 377
(FaERF6 FaERF7 FaERF8 FaERF10 and FaERF11) also belong to the same 378
group with FaERF8 also showing somewhat weaker activation activity towards the 379
FaQR promoter than FaERF9 The fact that FaERF9 could not bind directly to the 380
promoter of FaQR (Figure 6) indicates that it might function as an indirect regulator 381
of FaQR and furaneol biosynthesis 382
383
A FaERF9 and FaMYB98 complex is involved in regulating FaQR and furaneol 384
biosynthesis 385
The finding that FaERF9 could interact with FaMYB98 protein (Figures 9 and 386
Figure 10) and that FaMYB98 could physically bind to the FaQR promoter (Figure 6 387
and Figure 7) provides evidence for a regulatory mechanism whereby FaERF9 388
regulates FaQR and furaneol production as part of a complex with an MYB 389
transcription factor Since co-overexpression of FaERF9 and FaMYB98 resulted in 390
much higher activation activity towards FaQR we speculate that FaERF9 may 391
recruit FaMYB98 homologs in tobacco to activate the FaQR promoter (Figure 8) 392
FaOMT is another key gene for furanone biosynthesis and a potential target for 393
transcriptional activation However FaERF9 did not significantly activate the 394
FaOMT promoter in a dual-luciferase assay and the transcript level of FaOMT in the 395
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15
FaERF9-overexpressing fruits showed no significant difference from that in the 396
control (Supplemental Figure S6 Supplemental Figure S7) The FaOMT promoter 397
was significantly induced by FaMYB98 but no synergistic effect of FaERF9 and 398
FaMYB98 on the promoter was observed (Supplemental Figure S6) In previous 399
studies of the regulation of plant volatile compounds MYBs have been characterized 400
as being involved mainly in the regulation of the benzenoidphenylpropanoid pathway 401
that produces floral volatiles in petunia and eugenol in ripe strawberry fruit (Verdonk 402
et al 2005 Dal Cin et al 2011 Colquhoun et al 2011 Spitzer-Rimon et al 2012 403
Medina-Puche et al 2015) but their role in formation of volatiles from other 404
pathways has not been reported Our study demonstrates a role for MYB in the 405
synthesis of furaneol a carbohydrate-derived volatile compound and reveals the 406
synergistic interactions between an MYB and ERF in a transcription complex (Figure 407
8 Figure 9 and Figure 10) 408
409
Recent research has provided evidence for interactions between AP2ERF and MYB 410
transcription factors in regulating other aspects of fruit quality including texture 411
(EjAP2-1 and EjMYB Zeng et al 2015) and colour (PyERF3 and PyMYB114 Yao 412
et al 2017) A group VIII ERF has also recently been shown to interact with an MYB 413
to regulate floral scent production in petunia (Liu et al 2017) In strawberry fruit 414
DOF in combination with an MYB has been reported to be involved in the regulation 415
of eugenol production and the identification of this second transcription factor (DOF) 416
suggests that it is a good target in breeding for improved flavour (Molina-Hidalgo et 417
al 2017 Tieman 2017) Considering its important contribution to flavour in 418
strawberry and many other highly valued fruit crop species (pineapple tomato mango 419
etc) very little is known about regulation of furaneol synthesis Here we established 420
the role of FaERF9 in the regulation of HDMF synthesis by direct protein-protein 421
interactions with FaMYB98 to synergistically trans-activate FaQR The functional 422
identification of this complex enhances our knowledge of the regulation of volatile 423
compound synthesis and identifies a new AP2ERF-MYB complex Further 424
examination of the other ERFs that stimulated transcription from the FaQR promoter 425
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
16
(Figure 2) may provide additional information about the complexity of this regulation 426
Overall this study provides important clues for understanding the transcriptional 427
regulation of HDMF synthesis and identifies specific transcription factors that are 428
likely to be good targets for molecular breeding for improved flavour 429
430
Conclusions 431
Screening of the AP2ERF superfamily in strawberry (Fragaria times ananassa) 432
identified candidate members capable of activating the FaQR promoter An ERF 433
transcription factor was identified as a positive regulator of HDMF synthesis in 434
strawberry fruit and the mechanism of activation was shown to involve an ERF-MYB 435
transcription complex that regulates transcription of FaQR leading to the biosynthesis 436
of HDMF the characteristic volatile compound which has a major influence on 437
strawberry aroma 438
439
Materials and Methods 440
441
Plant Materials and Growth conditions 442
The strawberry (Fragaria times ananassa cv lsquoYuexinrsquo an octoploid cultivar) fruit used in 443
this study were bred by Zhejiang Academy of Agricultural Sciences (Haining 444
Zhejiang) Fruits at various developmental and ripening stages including G (green) T 445
(turning) IR (intermediate red) and R (full red) were harvested (Figure 1) and 446
transported to the laboratory within 2 h Thirty-six fruits of uniform size and free of 447
visible defects were selected at each stage with twelve fruits in each biological 448
replicate After removing the calyces fruits were then divided into the basal and 449
apical sections which were sampled separately (Figure 1) They were rapidly cut into 450
pieces frozen immediately in liquid nitrogen and stored at -80deg C until use Red ripe 451
fruits of different strawberry cultivars (Fragaria times ananassa octoploid cultivars) 452
including lsquoYuelirsquo lsquoBenihoppersquo lsquoMengxiangrsquo lsquoAmaoursquo lsquo10-1-4rsquo lsquoAkihimersquo lsquoSweet 453
Charliersquo lsquo07-1-4rsquo lsquoDarselectrsquo lsquoYuexinrsquo and lsquoXuemeirsquo were also provided by Zhejiang 454
Academy of Agricultural Sciences For each cultivar the fruits of three biological 455
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17
replicates were sampled frozen in liquid nitrogen and stored at -80deg C for further use 456
457
Tobacco plants (Nicotiana benthamiana) used for dual-luciferase assays and 458
subcellular localization analysis in this study were grown in a growth chamber with a 459
lightdark cycle of 16 h8 h at 24degC 460
461
Detection of DMMF and HDMF 462
Automated HS-SPME-GC-MS was performed to detect both furanones in lsquoYuexinrsquo 463
strawberry fruit (Zorrilla-Fontanesi et al 2012) Samples were ground into a powder 464
under liquid nitrogen for analysis 465
466
For the detection of DMMF (Figure 1) 05 g (fresh weight) of each sample was 467
weighed in the vial to which was added 1 mL of EDTA solution (100 mM pH 75) 1 468
mL of CaCl2 solution (mv = 20) and 20 microL of 2-octanol as the internal standard 469
(007 μgμL) The mixture was homogenized and the vial closed and placed on the 470
sample tray for analysis by CombiPAL autosampler (CTC Analytic CA USA) The 471
fruit volatiles were sampled by headspace solid-phase microextraction with a 65-μm 472
polydimethylsiloxane-divinylbenzene fibre (PDMS-DVB) Initially vials were 473
pre-incubated at 50degC for 10 min under continuous agitation (500 rpm) then volatiles 474
were extracted for 30 min at the same temperature and agitation speed After that the 475
fibre was desorbed in the GC injection port for 5 min in splitless mode The 7890A 476
GC chromatograph was equipped with a DB-5ms column (60 m times 250 μm times 1 μm 477
JampW Scientific Folsom CA USA) with helium as the carrier gas at a constant flow 478
of 12 mLmin The GC was programmed at an initial temperature of 35degC for 2 min 479
with a ramp of 5degC min up to 250degC and held for 5 min The injection port interface 480
and MS source temperatures were 250degC 260degC and 230degC respectively The 481
ionization potential was set at 70 eV recorded by a 5975B mass spectrometer (Agilent 482
Technologies JampW Scientific Folsom CA USA) and the scanning speed was 7 483
scanss The same method was used to analyse HDMF and DMMF in fruits from 484
different cultivars (Supplemental Figure S3) except for the sample preparation 485
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18
procedure (Araguumlez et al 2013) briefly 05 g (fresh weight) of powdered fruit was 486
incubated at 30degC in a water bath for 5 min then 2 mL of NaCl (mv = 20) and 20 487
microL of 2-octanol as the internal standard (007 μgμL) were added and homogenized 488
489
For the detection of HDMF (Figure 1) and both furanones (Figure 4 and Supplemental 490
Table S3) a liquid-injection system equipped with CTC Pal ALS was used One gram 491
(fresh weight) of powdered fruit and 2 mL of NaCl (mv = 20) were homogenized in 492
a 10-mL tube and 300 μL of CH2Cl2 and 20 microL of 2-octanol (0766 μgμL) as the 493
internal standard were added to extract the volatiles the mixture was then 494
homogenized again The tubes were stored at room temperature for 20 min and 495
centrifuged at 12000 rpm for 5 min The subnatant was pipetted into a clean 15-mL 496
tube in which 20 mg of anhydrous sodium sulphate was added the tube was left 497
without shaking for half an hour Then 150 μL of the solution was transferred into a 498
GC vial and placed on the sample tray as described above Each sample (1 μL) was 499
injected using the autosampler and the analysis was accomplished by a 7890A 500
GC-MS system (Agilent Technologies JampW Scientific Folsom CA USA) equipped 501
with a DB-WAX column (30 m times 025 mm times 025 μm JampW) Helium (12 mLmin) 502
was used as a carrier gas The injection port (splitless injection mode) interface and 503
MS source temperatures were as described above The oven temperature was set at 504
60degC for 4 min then increased to 180degC at a rate of 4degCmin and maintained for 30 505
min DMMF was identified by comparison of electron ionization mass spectra and 506
retention time data with the data from the NISTEPANIH mass spectral library 507
(NIST-08 and Flavor) HDMF (Figure 1) was identified and qualified by comparison 508
with injected standard (Sigma) The quantitative analysis of both furanones (Figure 4 509
Supplemental Table S3 and Supplemental Figure S3) was determined using the peak 510
area of the internal standard as a reference based on total ion chromatogram (TIC) 511
512
RNA isolation and Reverse Transcription Quantitative PCR (RT-qPCR) 513
Total RNA from strawberry samples was isolated in this study using the CTAB 514
method (Chang et al 1993) Genomic DNA contamination was eliminated by 515
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19
TURBO Dnase (Ambion) 1 μg of RNA was used to obtain cDNA using an IScriptTM 516
cDNA Synthesis Kit (Bio-Rad) The synthesized cDNA was diluted with water (120) 517
and 2 μL of diluted cDNA was used as the template for RT-qPCR Reactions were 518
performed in a total volume of 20 μL consisting of 10 μL of SYBR PCR supermix 519
(Bio-Rad) 1 μL of each primer (10 μM) 6 μL of DEPC-H2O and 2 μL of diluted 520
cDNA on CFX96 instrument (Bio-Rad) (Yin et al 2012) The oligonucleotide 521
primers for RT-qPCR analysis of genes including the AP2ERF FaQR and FaOMT 522
were designed according to the coding sequences of genes and the specificity was 523
verified before use (Min et al 2012) NCBIPrimer-BLAST was applied to design the 524
primers Relative expression levels were normalized to that of an internal controlmdashthe 525
interspacer 26S-18S strawberry RNA housekeeping gene FaRIB413 526
(Zorrilla-Fontanesi et al 2012) To investigate the differential expression of genes 527
during fruit development and ripening stages relative expression of each gene at the 528
R stage in the basal fruit section was set as 1 using the 2minus∆∆119862119879 method For transient 529
overexpression assay relative expression of control fruits with an empty vector (SK) 530
was set as 1 The primers used in RT-qPCR are listed in Supplemental Table S4 531
532
Gene isolation and analysis 533
Multiple database searches were performed to identify members of the strawberry 534
(Fragaria times ananassa) AP2ERF superfamily in the published strawberry databases 535
and annotations of Fragaria times ananassa and Fragaria times vesca by using the 536
AP2ERF DNA binding domain as a query sequence and 120 genes were identified 537
with AP2ERF domain(s) Based on the BLAST result primers (listed in 538
Supplemental Table S5) were used to amplify the coding full-length cDNAs of 539
AP2ERF genes The deduced amino acid sequences of AP2ERF proteins in 540
Arabidopsis thaliana used for construction of a phylogenetic tree were obtained from 541
the Arabidopsis Information Resource (TAIR) Alignment of the proteins was 542
performed using the neighbour-joining method in ClustalX (v181) and the 543
phylogenetic tree was constructed using FigTree (v131) 544
545
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
20
FaMYB98 was obtained by yeast one-hybrid screening sequencing and the full-length 546
sequences were predicted by BLAST Primers were designed (listed in Supplemental 547
Table S5) to amplify the full-length coding sequence 548
549
The promoter of FaQR was cloned by Genome Walking as previously described (Yin 550
et al 2010) and conserved cis-element motifs in the promoter were manually 551
searched 552
553
Conserved domains within the FaAP2ERF proteins and FaMYB98 were analysed by 554
CD-search (httpswwwncbinlmnihgovStructurecddwrpsbcgi) and cellular 555
locations of proteins including FaERF9 and FaMYB98 were predicted with the 556
WoLF PSORT program (httpswwwgenscriptcomwolf-psorthtml) 557
558
Dual-Luciferase Assays 559
In accordance with a previous protocol (Yin et al 2010) the full-length cDNAs of 560
FaAP2ERF or FaMYB98 transcription factors were cloned into pGreen II 0029 561
62-SK vector and the promoter of FaQR was cloned into pGreen II 0800-LUC vector 562
A luciferase gene from Renillia (REN) driven by a 35S promoter in the LUC vector 563
acted as a positive control The above constructs were transiently expressed in 564
Nicotiana benthamiana leaves by Agrobacterium-mediated infiltration (strain 565
GV3101) and the activity of the TFs on the promoter was measured on the third day 566
after infiltration indicated by the ratio of enzyme activities of firefly luciferase (LUC) 567
and renilla luciferase (REN) using a Modulus Luminometer (Promega Madison WI 568
USA) To determine the activity of a specific transcription factor towards the 569
promoter we mixed the Agrobacterium culture with 1 mL of TF and 100 μL of 570
promoter and the LUCREN value of the empty vector SK on the promoter was set as 571
1 as a calibrator To test the combined effect of two transcription factors on the 572
promoter to the Agrobacterium culture mixture we added 05 mL of each TF and 100 573
μL of promoter the effect of the mixtures that contained each transcription factor (05 574
mL) and empty vector SK (05 mL) was also tested on the promoter as a control 575
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
21
576
Subcellular localization analysis 577
35S-FaERF9-GFP and 35S-FaMYB98-GFP were transiently expressed in tobacco (N 578
benthamiana) leaves by Agrobacterium infiltration (EHA105) using the same method 579
as described in the dual-luciferase assay above The transiently infected leaves were 580
imaged on the third day after infiltration using a Nikon A1-SHS confocal laser 581
scanning microscope The excitation wavelength for GFP fluorescence was 488 nm 582
and fluorescence was detected at 490ndash520 nm The primers used for GFP construction 583
are listed in Supplemental Table S6 584
585
Transient overexpression in strawberry fruit 586
Transient overexpression of FaERF9 and an overexpression binary vector (pGreen II 587
0029 62-SK-FaERF9-FaMYB98) were performed in strawberry fruit using the 588
FaERF9-SK construct described above for the dual-luciferase assays and the binary 589
vector constructed according to Liu et al 2013 The transfection of fruit was carried 590
out at the G stage (Hoffmann et al 2006) The FaERF9-SK construct and binary 591
vector were individually electroporated into Agrobacterium tumefaciens GV3101 and 592
the Agrobacterium culture suspended in infiltration buffer was infiltrated into the 593
whole fruit using a syringe As a control treatment fruits were infiltrated with 594
Agrobacterium carrying an empty vector SK under the same transfection conditions 595
Fruits were left attached to the plants and harvested on the seventh day after 596
infiltration Fruits of three biological replicates were sampled for further analysis 597
598
Yeast one-hybrid assay 599
In order to identify proteins that bind to the FaQR promoter the Matchmaker Gold 600
Yeast One-hybrid Library Screening System (Clontech USA) was used The sequence 601
of the FaQR promoter was cloned into the pAbAi vector and the construct was 602
integrated into the genome of the Y1HGold yeast strain A mixture of total RNA from 603
strawberry fruit at four stages (G T IR R) was used to construct the prey cDNA 604
library (TaKaRa) The background AbAr expression of Y1HGold FaQR-pAbAi strain 605
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
22
was tested according to the system user manual and then screening for protein-DNA 606
interactions was carried out Furthermore the full length of each transcription factor 607
was separately cloned into pGADT7 AD vector to confirm the screening results The 608
relationship between FaERF9 and FaQR promoter was also examined individually 609
Primers used in this assay are listed in Supplemental Table S6 610
611
Expression and purification of FaMYB98 recombinant protein 612
A 405-bp region spanning the DNA-binding domain of FaMYB98 was amplified 613
from FaMYB98 cDNA and cloned into a pET6timesHN vector (Clontech Palo CA USA) 614
to generate the recombinant N-terminal His-tagged protein the primers used are listed 615
in Supplemental Table S6 The resulting construct was sequenced and introduced into 616
Escherichia coli strain Rosetta 2(DE3)pLysS (Novagen) Ten millilitres of the 617
overnight culture was combined with 500 mL of an LB liquid medium (100 μgmL 618
ampicillin and 34 μgmL chloramphenicol) as described (Li et al 2017) Isopropyl 619
β-D-1-thiogalactopyranoside (IPTG) was added to a final concentration of 1 mM and 620
the bacterial culture was incubated at 18degC at 150 rpm for 18 h Then the cells were 621
harvested using a centrifuge and resuspended in 1times PBS buffer (Sangon Biotech) 622
after which they were disrupted by sonication and the supernatant was purified using 623
a HisTALONTM Gravity Column (Clontech) according to the user manual The PD-10 624
Desalting column (GE Healthcare) was then used for buffer change and sample 625
clean-up of proteins according to the gravity protocol SDS-PAGE was performed and 626
the protein was visualized using Coomassie brilliant blue 627
628
Electrophoretic mobility shift assay (EMSA) 629
A Lightshift Chemiluminescent EMSA kit (Thermo) was used to perform EMSA 630
experiments according to the manufacturerrsquos instructions Single-strand 631
oligonucleotides were synthesized and biotinylated by GeneBio Biotech (Hangzhou 632
China) The details of the EMSA assay are provided in Ge et al (2017) The probes 633
used for EMSAs are listed in Supplemental Table S6 634
635
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
23
636
Yeast two-hybrid assay 637
The DUALhunter system (Dualsystems Biotech Switzerland) was used to investigate 638
the interaction between FaERF9 and FaMYB98 Full-length coding sequences of 639
FaERF9 and FaMYB98 were respectively cloned into pDHB1 bait vector and 640
pPR3-N prey vector sequences were verified and the bait plasmid was 641
co-transformed with prey plasmid into NMY51 in the combinations below 642
FaMYB98-pDHB1pPR3-N FaMYB98-pDHB1FaERF9-pPR3-N 643
FaMYB98-pDHB1pOst1-NubI FaERF9-pDHB1pPR3-N 644
FaERF9-pDHB1FaMYB98-pPR3-N and FaERF9-pDHB1pOst1-NubI (Li et al 645
2017) Transformed cells were spread onto the following plates DDO (SD 646
medium-Trp-Leu) QDO (SD medium-Trp-Leu-His-Ade) and QDO+3-AT (QDO 647
medium supplemented with 1 mM 3-amino-124-triazole) The control plasmid 648
pOst1-NubI was used to determine whether the bait was functional the pPR3-N prey 649
vector plasmid was used to test whether the bait displayed non-specific background 650
and positive interactions were indicated by the growth of yeast on QDO and 651
QDO+3-AT plates The Primers used in the DUALhunter assay are listed in 652
Supplemental Table S6 653
654
Bimolecular fluorescence complementation (BiFC) assays 655
Full-length FaERF9 and FaMYB98 respectively were cloned into sequences 656
encoding the N- and C- fragments of YFP protein (Lv et al 2014) All constructs 657
were transiently expressed in tobacco (N benthamiana) leaves by Agrobacterium 658
infiltration (EHA105) The YFP fluorescence of transfected leaves was imaged 40 h 659
after infiltration by using a Nikon A1-SHS confocal laser scanning microscope The 660
excitation wavelength for YFP was 488 nm and fluorescence was detected at 520ndash661
540 nm Primers used are listed in Supplemental Table S6 662
663
Statistics 664
A Studentrsquos two-tailed t test ( plt005 plt001 and plt0001) was used to 665
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
24
determine significant differences between two groups in this study Microsoft Excel 666
was used to perform linear regressive analysis significant differences were 667
determined by SPSS Statistics 200 and scatter plots were prepared with Origin80 668
Least significant difference (LSD) at the 5 level was calculated using Microsoft 669
Excel Figures were prepared with Origin80 (Microcal Software Inc Northampton 670
MA USA) The online tool MetaboAnalyst 36 (httpwwwmetaboanalystca) was 671
used to analyse the transcript abundance of the AP2ERF genes 672
673
Accession numbers 674
Sequence data from this article have been deposited in GenBank under the accession 675
numbers MH332903-MH333022 for AP2ERF genes in Fragaria times ananassa and 676
MH333023 for FaMYB98 GenBank numbers for FaQR and FaOMT were 677
AY1588361 (Raab et al 2006) and AF2204912 (Wein et al 2002) 678
679
Supplemental Material 680
Supplemental Figure S1 Phylogenetic analysis of FaAP2ERF and Arabidopsis 681
AP2ERF proteins 682
Supplemental Figure S2 Analysis of FaAP2ERF gene expression patterns in 683
strawberry fruit during development and ripening 684
Supplemental Figure S3 Contents of furanones in fruit of strawberry cultivars 685
Supplemental Figure S4 Relative expression of FaERF9 in FaERF9-FaMYB98- 686
and FaERF9-overexpressing fruits 687
Supplemental Figure S5 Subcellular localization of FaMYB98 688
Supplemental Figure S6 The combined activation effects of FaERF9FaMYB98 on 689
the FaOMT promoter 690
Supplemental Figure S7 Relative expression of FaOMT in 691
FaERF9-overexpressing fruits 692
Supplemental Table S1 AP2ERF superfamily genes in Fragaria times ananassa 693
Supplemental Table S2 Classification of the AP2ERF superfamily members in 694
Fragaria times ananassa 695
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25
Supplemental Table S3 Furanone content in FaERF9-FaMYB98- and 696
FaERF9-overexpressing fruits 697
Supplemental Table S4 Primers used for reverse transcription quantitative PCR 698
(RT-qPCR) 699
Supplemental Table S5 Primers used to amplify the full-length coding sequences of 700
AP2ERF genes and FaMYB98 in strawberry (Fragaria times ananassa) 701
Supplemental Table S6 Primers used for vector construction 702
703
Acknowledgments 704
This research was supported by the National Key Research and Development 705
Program (2016YFD0400101) the Project of the Science and Technology Department 706
of Zhejiang Province (2016C04001) and the 111 Project (B17039) 707
708
Figure legends 709
Figure 1 Changes in furanone content and furanone biosynthetic genes during 710
strawberry (Fragaria times ananassa Duch cv Yuexin) fruit development and ripening 711
A Fruits were collected at four ripening stages G (green stage) T (turning stage) IR 712
(intermediate red stage) R (full red stage) B Changes in the contents of furaneol 713
(HDMF) and mesifurane (DMMF) HDMF content was calculated using a standard 714
curve of HDMF while DMMF content was calculated with an internal standard as the 715
reference C Expression levels of FaQR and FaOMT The expression levels of each 716
gene were calculated relative to corresponding values in the basal section at the R 717
stage SEs were calculated from three replicates and LSD values represent the least 718
significant differences at p = 005 719
Figure 2 Regulatory effects of FaAP2ERF on the promoter of FaQR LUCREN 720
values of the empty vector on FaQR promoter were used as the calibrator set as 1 721
and SEs were calculated from five replicates statistical significance was determined 722
by Studentrsquos two-tailed t test ( plt0001) 723
Figure 3 Expression and the subcellular localization of FaERF9 A The expression 724
levels were calculated relative to the levels in the basal section at the R stage B 725
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
26
Subcellular localization analysis was performed in tobacco leaves The tobacco used 726
in the assay was stably transformed with a specific nucleus localized red fluorescence 727
protein construct and the red fluorescence indicates the nucleus-localized signal 728
(NLS) Scale bar = 25 microm SEs were calculated from three replicates 729
Figure 4 Transient overexpression of FaERF9 in strawberry fruit A Relative 730
expression of FaQR and FaERF9 in FaERF9-OX fruit 7 days after infiltration The 731
expression was calculated relative to the average value in control (SK) fruits B 732
HDMF and DMMF content in FaERF9-OX fruit The content of both furanones 733
were quantified using the peak area of the internal standard (2-octanol) as the 734
reference SEs were calculated from three replicates Statistical significance was 735
determined by Studentrsquos two-tailed t test ( plt005 plt001 plt0001) 736
Figure 5 Scatter plots of 11 strawberry cultivars A Linear regression analysis 737
between FaERF9 expression and FaQR expression B Linear regression analysis 738
between FaERF9 expression and furanone content The relative expression was 739
normalized to that of the housekeeping gene FaRIB413 and furanone content was 740
calculated with internal standard as the reference Significant differences were 741
determined by SPSS Statistics 200 742
Figure 6 Interactions of FaERF9 and FaMYB98 with the FaQR promoter A Yeast 743
one-hybrid analysis of the interaction of FaERF9 and FaQR promoter B Yeast 744
one-hybrid analysis of the interaction of FaMYB98 and FaQR promoter C 745
Regulatory effect of FaMYB98 on the FaQR promoter Auto-activation was tested on 746
SD-Ura (synthetically defined medium without uracil) in presence of Aureobasidin A 747
(AbA) and physical interaction was determined on SD-Leu (synthetically defined 748
medium without leucine) in presence of AbA LUCREN values of the empty vector 749
on FaQR promoter were used as the calibrator set as 1 and error bars were calculated 750
from five replicates Statistical significance was determined by Studentrsquos two-tailed t 751
test ( plt005 plt001 plt0001) 752
Figure 7 Electrophoretic mobility shift assay of FaMYB98 binding to FaQR 753
promoter A The probe sequence used for EMSA and mutated nucleotides are 754
indicated with lowercase letters B Purified DNA-binding domain of FaMYB98 755
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
27
protein and biotin-labelled DNA probe were mixed and analysed on 6 native 756
polyacrylamide gels and then photographed Presence or absence of specific probes is 757
marked by the symbol + or - 758
Figure 8 The combined activation effects of FaERF9FaMYB98 on the FaQR 759
promoter LUCREN values obtained with the empty vector and FaQR promoter were 760
used as the calibrator set as 1 and error bars were calculated from five replicates 761
Figure 9 Yeast two-hybrid analysis of the protein-protein interactions between 762
FaMYB98 and FaERF9 Positive interactions were determined by the growth of 763
yeast cells on selection plates Bait with pOST acted as positive controls and bait with 764
pPR3 as negative controls DDO synthetically defined medium without tryptophan 765
and leucine QDO synthetically defined medium without tryptophan leucine 766
histidine and adenine QDO+3AT QDO medium supplemented with 1 mM 767
3-aminotriazole 768
Figure 10 BiFC analysis of the protein-protein interactions between FaMYB98 and 769
FaERF9 The pairs of fusion proteins tested were FaMYB98-YFPN+FaERF9-YFPC 770
FaERF9-YFPN+FaMYB98-YFPC FaMYB98-YFPN+FaMYB98-YFPC and 771
FaERF9-YFPN+FaERF9-YFPC The other combinations were negative controls 772
The tobacco used in the assay was stably transformed with a specific 773
nucleus-localized red fluorescence protein construct and the red fluorescence 774
indicated the nucleus-localized signal (NLS) Fluorescence of the yellow fluorescence 775
protein (YFP) visualized the interaction in vivo Scale bar = 25 microm 776
777
Literature Cited 778
779
Agarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression 780
of PgDREB2A transcription factor enhances abiotic stress tolerance and activates 781
downstream stress-responsive genes Mol Biol Rep 37 1125-1135 782
Araguumlez I Osorio S Hoffmann T Rambla JL Medina-Escobar N Granell A 783
Botella MAacute Schwab W Valpuesta V (2013) Eugenol production in achenes and 784
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
28
receptacles of strawberry fruits is catalyzed by synthases exhibiting distinct kinetics 785
Plant Physiol 163 946-958 786
Carvalho RF Carvalho SD OrsquoGrady K Folta KM (2016) Agroinfiltration of 787
strawberry fruit mdash a powerful transient expression system for gene validation Curr 788
Plant Biol 6 19-37 789
Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic 790
(Amsterdam) 210 34-40 791
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating 792
RNA from pine trees Plant Mol Biol Rep 11 113-116 793
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC 794
Clark DG (2011) PhMYB4 fine-tunes the floral volatile signature of 795
Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143 796
Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz 797
EA Taylor MG Smits-Kroon MT Schuurink RC Haring MA Giovannoni J 798
Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic 799
pathway by ectopic expression of a MYB transcription factor in tomato fruit Plant 800
Cell 23 2738-2753 801
Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan 802
XW Yang ZY (2017) Differential responses of four biosynthetic pathways of 803
aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under 804
interaction of light and temperature Food Chem 221 356-364 805
Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of 806
differentially-expressed genes during somatic embryogenesis in Fragaria times 807
ananassa Duch lsquoBenihopprsquo J Hortic Sci Biotechnol 90 671-681 808
Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 809
transcriptionally regulates chilling-induced lignification of loquat fruit via physical 810
interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136 811
Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM 812
(2004) Functional interactions between a glutamine synthetase promoter and MYB 813
proteins Plant J 39 513-526 814
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
29
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) 815
Sucrose nonfermenting1-related protein kinase26 an ortholog of open stomata1 is 816
a negative regulator of strawberry fruit development and ripening Plant Physiol 817
167 915-930 818
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene 819
expression in strawberry fruit (Fragaria times ananassa) by agroinfiltration a rapid 820
assay for gene function analysis Plant J 48 818-826 821
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of 822
selected aroma-active compounds in strawberries by headspace solid-phase 823
microextraction gas chromatography and correlation with sensory descriptive 824
analysis J Food Sci 72 S487-S496 825
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid 826
plays an important role in the regulation of strawberry fruit ripening Plant Physiol 827
157 188-199 828
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of 829
NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes BMC 830
Plant Biol 6 20 831
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN 832
(2005) MYB98 is required for pollen tube guidance and synergid cell differentiation 833
in Arabidopsis Plant Cell 17 2981-2992 834
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional 835
characterization of enone oxidoreductases from strawberry and tomato fruit J 836
Agric Food Chem 55 6705-6711 837
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You 838
J-S Rohloff J Randall SK Alsheikh M (2012) Proteomic study of 839
low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ 840
in cold tolerance Plant Physiol 159 1787-1805 841
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional 842
characterization of four APETALA2-family genes (RAP26 RAP26L DREB19 843
and DREB26) in Arabidopsis Plant Mol Biol 75 107-127 844
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
30
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon 845
J Gupta V (2013) An oxidoreductase from lsquoAlphonsorsquo mango catalyzing 846
biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494 847
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in 848
strawberries Z Lebensm-Unters Forsch 195 120-123 849
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X 850
(2015) Label-free quantitative proteomics to investigate strawberry fruit proteome 851
changes under controlled atmosphere and low temperature storage J Proteomics 852
120 44-57 853
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 854
cooperates with CitWRKY1 to participate in citric acid degradation via 855
up-regulation of CitAco3 J Exp Bot 68 3419-3426 856
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription 857
factor CitERF71 activates the terpene synthase gene CitTPS16 involved in the 858
synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938 859
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and 860
transcriptomic analysis of the AP2ERF superfamily in Vitis vinifera BMC 861
Genomics 11 719 862
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive 863
Factor (AP2ERF) transcription factors mediators of stress responses and 864
developmental programs New Phytol 199 639-649 865
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 866
interacting with EOBI negatively regulates fragrance biosynthesis in petunia 867
flowers New Phytol 215 1490-1502 868
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu 869
CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 in regulating 870
anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) 871
during anthocyanin biosynthesis Plant Cell Tissue Organ Cult 115 285-298 872
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
31
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao 873
CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphate signaling and 874
homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597 875
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC 876
Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL 877
Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor 878
regulates eugenol production in ripe strawberry fruit receptacles Plant Physiol 168 879
598-614 880
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics 881
and volatile constituents of strawberry (cv Cigaline) during maturation J Agric 882
Food Chem 52 1248-1254 883
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS 884
(2012) Ethylene-responsive transcription factors interact with promoters of ADH 885
and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 886
63 6393-6405 887
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM 888
Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-Franco A 889
Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific 890
transcription factor FaDOF2 regulates the production of eugenol in ripe fruit 891
receptacles J Exp Bot 68 4529-4543 892
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) 893
Comparison and verification of the genes involved in ethylene biosynthesis and 894
signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44 895
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the 896
ERF gene family in Arabidopsis and rice Plant Physiol 140 411-432 897
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in 898
sour cherry and strawberry and the heterologous expression of CBF1 in strawberry 899
J Am Soc Hortic Sci 127 489-494 900
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech 901
JC Ohme-Takagi M Regad F Bouzayen M (2012) Functional analysis and 902
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
32
binding affinity of tomato ethylene response factors provide insight on the 903
molecular bases of plant differential responses to ethylene BMC Plant Biol 12 190 904
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) 905
Methylpentoses are possible precursors of furanones in fruits Prikl Biokhim 906
Mikrobiol 28 123-127 907
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery 908
of synergid-expressed genes encoding filiform apparatus localized proteins Plant 909
Cell 19 2557-2568 910
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria 911
vesca L compared to those of cultivated berries Fragariatimes ananassa cv Senga 912
Sengana J Agric Food Chem 27 19-22 913
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W 914
Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of the strawberry 915
flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone 916
oxidoreductase Plant Cell 18 1023-1037 917
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L 918
Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim M Broun P Zhang 919
JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription 920
factors genome-wide comparative analysis among eukaryotes Science 290 921
2105-2110 922
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the 923
formation of 25-dimethyl-4-hydroxy-3(2H)-furanone in detached ripening 924
strawberry fruits J Agric Food Chem 46 1488-1493 925
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 926
25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in 927
strawberry fruits Phytochemistry 43 155-159 928
Schwab W (1998) Application of stable isotope ratio analysis explaining the 929
bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone in plants by a biological 930
maillard reaction J Agric Food Chem 46 2266ndash2269 931
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
33
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) 932
Molecules 18 6936-6951 933
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard 934
products Recent Res Dev Phytochem 1 643-673 935
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL 936
Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJ Sims CA 937
Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical 938
compositions a seasonal influence and effects on sensory perception PLoS One 9 939
e88446 940
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) 941
Identification phylogeny and transcript profiling of ERF family genes during 942
development and abiotic stress treatments in tomato Mol Genet Genomics 284 943
455-475 944
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) 945
CitAP210 activation of the terpene synthase CsTPS1 is associated with the 946
synthesis of (+)-valencene in lsquoNewhallrsquo orange J Exp Bot 67 4105-4115 947
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes 948
Dev Genes Evol 214 105-114 949
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K 950
Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the 951
key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151 952
Spitzer-Rimon B Farhi M Albo B Cnarsquoani A Ben Zvi MM Masci T Edelbaum 953
O Yu YX Shklarman E Ovadis M Vainstein A (2012) The R2R3-MYB-like 954
regulatory factor EOBI acting downstream of EOBII regulates scent production 955
by activating ODO1 and structural scent-related genes in petunia Plant Cell 24 956
5089-5105 957
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp 958
Bot 68 4407-4409 959
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla 960
JF Amaya I Giavalisco P Fernie AR Botella MA Valpuesta V (2015) Central 961
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
34
role of FaGAMYB in the transition of the strawberry receptacle from development 962
to ripening New Phytol 208 482-496 963
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 964
regulates fragrance biosynthesis in petunia flowers Plant Cell 17 1612-1624 965
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS 966
(2018) The potassium channel FaTPK1 plays a critical role in fruit quality 967
formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748 968
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) 969
Isolation cloning and expression of a multifunctional O-methyltransferase capable 970
of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma 971
compounds in strawberry fruits Plant J 31 755-765 972
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor 973
types their evolutionary origin and species distribution In A handbook of 974
transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular 975
Biochemistry 52 25-73 976
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of 977
odor (Buettner A Ed) Springer Cham 9-10 978
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS 979
(2014) Isolation classification and transcription profiles of the AP2ERF 980
transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271 981
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in 982
regulation of fruit quality Crit Rev Plant Sci 35 120-130 983
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ 984
Zhang SL Wu J (2017) Map-based cloning of the pear gene MYB114 identifies an 985
interaction with other transcription factors to coordinately regulate fruit 986
anthocyanin biosynthesis Plant J 92 437-451 987
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes 988
involved in regulating fruit ripening Plant Physiol 153 1280-1292 989
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35
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) 990
Expression of ethylene response genes during persimmon fruit astringency removal 991
Planta 235 895-906 992
Zabetakis I Gramshaw JW Robinson DS (1999) 993
25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis and 994
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Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci 996
Food Agric 74 421-434 997
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 998
an AP2ERF gene is a novel regulator of fruit lignification induced by chilling 999
injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1000
1325-1334 1001
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation 1002
classification and transcription profiles of the Ethylene Response Factors (ERFs) in 1003
ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215 1004
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML 1005
(2012) Genome-wide analysis of the AP2ERF superfamily in peach (Prunus 1006
persica) Genet Mol Res 11 4788-4809 1007
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and 1008
expression analysis of a CRTDRE-binding factor gene FaCBF1 from Fragaria times 1009
ananassa Acta Hortic 41 240-248 1010
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The 1011
Arabidopsis AP2ERF transcription factor RAP26 participates in ABA salt and 1012
osmotic stress responses Gene 457 1-12 1013
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B 1014
Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) Genome-wide 1015
analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic 1016
(Amsterdam) 123 73-81 1017
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF 1018
Valpuesta V Botella MA Granell A Amaya I (2012) Genetic analysis of 1019
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36
strawberry fruit aroma and identification of O-methyltransferase FaOMT as the 1020
locus controlling natural variation in mesifurane content Plant Physiol 159 1021
851-870 1022
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
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wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
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Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphatesignaling and homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597
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Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor regulates eugenol production in ripe strawberry fruitreceptacles Plant Physiol 168 598-614
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Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS (2012) Ethylene-responsive transcription factors interact withpromoters of ADH and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 63 6393-6405
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Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-FrancoA Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific transcription factor FaDOF2 regulates the production ofeugenol in ripe fruit receptacles J Exp Bot 68 4529-4543
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Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) Comparison and verification of the genes involved in ethylenebiosynthesis and signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice Plant Physiol140 411-432
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in sour cherry and strawberry and the heterologousexpression of CBF1 in strawberry J Am Soc Hortic Sci 127 489-494
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech JC Ohme-Takagi M Regad F Bouzayen M (2012)Functional analysis and binding affinity of tomato ethylene response factors provide insight on the molecular bases of plant differentialresponses to ethylene BMC Plant Biol 12 190
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) Methylpentoses are possible precursors of furanones in fruits PriklBiokhim Mikrobiol 28 123-127
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery of synergid-expressed genes encoding filiformapparatus localized proteins Plant Cell 19 2557-2568
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria vesca L compared to those of cultivated berriesFragariatimes ananassa cv Senga Sengana J Agric Food Chem 27 19-22
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of thestrawberry flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone oxidoreductase Plant Cell 18 1023-1037
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim MBroun P Zhang JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription factors genome-wide comparative analysisamong eukaryotes Science 290 2105-2110
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the formation of 25-dimethyl-4-hydroxy-3(2H)-furanonein detached ripening strawberry fruits J Agric Food Chem 46 1488-1493
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in strawberry fruits Phytochemistry 43 155-159
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (1998) Application of stable isotope ratio analysis explaining the bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone inplants by a biological maillard reaction J Agric Food Chem 46 2266ndash2269
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) Molecules 18 6936-6951Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard products Recent Res Dev Phytochem 1 643-673Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJSims CA Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical compositions a seasonal influence and effects on sensoryperception PLoS One 9 e88446
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) Identification phylogeny and transcript profiling of ERFfamily genes during development and abiotic stress treatments in tomato Mol Genet Genomics 284 455-475
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) CitAP210 activation of the terpene synthase CsTPS1 isassociated with the synthesis of (+)-valencene in Newhall orange J Exp Bot 67 4105-4115
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes Dev Genes Evol 214 105-114Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Spitzer-Rimon B Farhi M Albo B Cnaani A Ben Zvi MM Masci T Edelbaum O Yu YX Shklarman E Ovadis M Vainstein A (2012) TheR2R3-MYB-like regulatory factor EOBI acting downstream of EOBII regulates scent production by activating ODO1 and structuralscent-related genes in petunia Plant Cell 24 5089-5105
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp Bot 68 4407-4409Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla JF Amaya I Giavalisco P Fernie AR Botella MAValpuesta V (2015) Central role of FaGAMYB in the transition of the strawberry receptacle from development to ripening New Phytol208 482-496
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 regulates fragrance biosynthesis in petunia flowers PlantCell 17 1612-1624
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS (2018) The potassium channel FaTPK1 plays a critical role infruit quality formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) Isolation cloning and expression of a multifunctional O- wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma compounds in strawberry fruitsPlant J 31 755-765
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor types their evolutionary origin and speciesdistribution In A handbook of transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular Biochemistry 52 25-73
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of odor (Buettner A Ed) Springer Cham 9-10Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS (2014) Isolation classification and transcription profiles ofthe AP2ERF transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in regulation of fruit quality Crit Rev Plant Sci 35 120-130
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ Zhang SL Wu J (2017) Map-based cloning of the pear geneMYB114 identifies an interaction with other transcription factors to coordinately regulate fruit anthocyanin biosynthesis Plant J 92437-451
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes involved in regulating fruit ripening Plant Physiol 1531280-1292
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Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) Expression of ethylene response genes during persimmonfruit astringency removal Planta 235 895-906
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Zabetakis I Gramshaw JW Robinson DS (1999) 25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis andbiosynthesis-a review Food Chem 65 139-151
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Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci Food Agric 74 421-434Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 an AP2ERF gene is a novel regulator of fruit lignificationinduced by chilling injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1325-1334
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Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation classification and transcription profiles of the Ethylene ResponseFactors (ERFs) in ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215
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Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML (2012) Genome-wide analysis of the AP2ERF superfamily inpeach (Prunus persica) Genet Mol Res 11 4788-4809
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Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and expression analysis of a CRTDRE-binding factor gene FaCBF1from Fragaria times ananassa Acta Hortic 41 240-248
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The Arabidopsis AP2ERF transcription factor RAP26 participatesin ABA salt and osmotic stress responses Gene 457 1-12
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Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Genome-wide analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic (Amsterdam) 123 73-81Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF Valpuesta V Botella MA Granell A Amaya I (2012) Geneticanalysis of strawberry fruit aroma and identification of O-methyltransferase FaOMT as the locus controlling natural variation inmesifurane content Plant Physiol 159 851-870
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wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
7
responses (Agarwal et al 2010 Zhu et al 2010 Licausi et al 2013) In recent years 156
several AP2ERF genes have been reported to regulate aspects of fruit quality (Xie et 157
al 2016) including fruit aroma For example CitAP210 is associated with the 158
synthesis of (+)-valencene in Newhall orange acting via regulation of CsTPS1 (Shen 159
et al 2016) CitERF71 was shown to physically bind to the CsTPS16 promoter and 160
contribute to the synthesis of E-geraniol in citrus fruit (Li et al 2017) These 161
observations raised the possibility that FaQR might also be a target for a member of 162
the AP2ERF family and that ERFs might also control furaneol biosynthesis 163
164
In this study screening of the Fragaria times ananassa AP2ERF gene family led to 165
identification of FaERF9 as an activator of FaQR however it did not bind directly 166
to the promoter A parallel search for proteins that directly bind the FaQR promoter 167
using yeast one-hybrid screening identified a second factor FaMYB98 which was 168
capable of physically interacting with the FaQR promoter FaMYB98 physically 169
interacts with FaERF9 and transient expression assays demonstrated a synergistic 170
effect on FaQR expression and furanone synthesis 171
172
Results 173
Changes in the content of both furanones and the activity of their biosynthetic 174
genes in strawberry fruit 175
lsquoYuexinrsquo fruits at four developmental and ripening stages (G green T turning IR 176
intermediate red R full red) were harvested (Figure 1) and determination of HDMF 177
levels indicated a major increase from about 065 μg per gram fruit at the IR stage to 178
346 μg at the R stage in the apical section implying that furaneol accumulation was 179
closely related to colour change and ripening (Figure 1) Furaneol levels were higher 180
in the apical section than in the basal section HDMF could not be detected at the IR 181
stage in the basal section but the amount increased at the R stage to 142 μg per gram 182
fruit Differences were also found for DMMF with the relative content in the apical 183
section 018 μg per gram at the R stage compared to 008 μg per gram in the basal 184
section at the same stage 185
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8
186
Measurement of mRNA levels by RT-qPCR indicated that the transcript levels of both 187
FaQR (GenBank AY1588361) and FaOMT (GenBank AF2204912) increased 188
throughout ripening (Figure 1) Comparison of the expression of these genes showed 189
that the transcript levels of FaQR and FaOMT significantly increased as early as in T 190
stage in basal fruit sections and for each gene over half of the peak transcript 191
abundance occurred as early as in IR stage in the apical section while for the basal 192
section it was in the R stage indicating a gradient of gene expression and volatile 193
production from apex to base of the fruit during ripening 194
195
Genome-wide identification of AP2ERF gene family in strawberry 196
Coding sequences of 120 non-redundant FaAP2ERF genes were isolated and 197
identified from lsquoYuexinrsquo strawberry and a systematic nomenclature for the AP2ERF 198
family genes was used to distinguish the members based on the structural features 199
defined previously (Supplemental Table S1) (Shigyo and Ito 2004 Nakano et al 200
2006 Licausi et al 2013) CD-search analysis showed that this superfamily is 201
consisted of 95 ERFs 18 AP2 and 6 RAV family members and 1 soloist member 202
(Supplemental Table S2) Phylogenetic analysis of the Fragaria times ananassa and 203
Arabidopsis AP2ERF members is shown in Supplemental Figure S1 with the 120 204
AP2ERF genes divided into three major groups (ERF AP2 RAV) and a soloist and 205
the ERF family being further divided into 10 groups (groups I to X in Supplemental 206
Table S1) 207
208
We performed a dual-luciferase assay to determine the ability of 116 FaAP2ERF 209
members to activate transcription from the promoter of FaQR The results indicated 210
about 12 members (mainly belonging to the ERF and RAV families) showed a 211
significant activation effect on the FaQR promoter while the remaining members 212
showed very limited effects (Figure 2) The relative activity of only the following 12 213
FaAP2ERF transcripts reached the threshold value set at 2 FaERF8FaERF9 214
(group II) FaERF27FaERF29FaERF31FaERF32 (group IV) 215
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9
FaERF37FaERF38 (group V) FaERF62FaERF64 (group VIII) FaERF68 216
(group IX) and FaRAV4 (Figure 2) Of these FaERF9 exhibited the highest 217
activation effect on the FaQR promoter (466-fold) (Figure 2) The strawberry 218
FaERF9 cDNA is 699 bp long and ExPASy Compute pIMw tool analysis indicated 219
that this gene encodes a 232-amino acid protein with a calculated molecular mass of 220
254 KD and a pI of 56 221
222
FaERF9 expression pattern and subcellular localization 223
To further explore the connections between AP2ERFs and furaneol biosynthesis we 224
obtained the transcript profiles of the AP2ERF genes in strawberry fruit samples at 225
different fruit developmental and ripening stages by reverse transcription quantitative 226
PCR (RT-qPCR) excluding genes with very low abundance in the fruit samples The 227
results presented as a heatmap (Supplemental Figure S2) demonstrate that these 228
genes displayed various expression patterns in both the apical and basal sections and 229
by analysing the expression patterns of the members indicated as activators in the 230
dual-luciferase assay we found that only a few genes including FaERF8 FaERF9 231
FaERF27 FaERF32 and FaERF37 were up-regulated during ripening stages and 232
their expression correlated with furaneol accumulation in the fruit (Figure 1) 233
Furthermore the expression patterns of the up-regulated genes in the apical and basal 234
sections showed that one ERF gene FaERF9 not only showed an up-regulation 235
pattern in both sections but its expression in the apical section occurred ahead of that 236
in the basal section (Figure 3) consistent with the actual changes in furaneol content 237
(Figure 1) and the expression pattern of FaQR (Figure 1) The subcellular localization 238
of FaERF9 was predicted to be in the nucleus using the WoLF PSORT program In 239
experimental tests 35S-FaERF9-GFP (green fluorescence protein) showed strong 240
fluorescence in the nucleus and the green signal merged with the red fluorescence 241
signal of mCherry-nucleus-marker in tobacco plants (Figure 3) 242
243
Transient overexpression of FaERF9 in strawberry 244
The expression of FaERF9 in agro-infiltrated fruits was analysed by performing 245
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
10
RT-qPCR on the seventh day after infiltration by which time they had reached the IR 246
or R stage and the result showed that the transcript levels were significantly higher 247
(52-fold) than in control fruits (Figure 4) The expression of FaQR was examined in 248
the same fruits and the transcript abundance also increased 22-fold The relative 249
content of HDMF in the FaERF9-overexpressing fruits was 008 μg per gram fruit 250
and undetectable in the control fruits (Figure 4) The relative content of DMMF in the 251
overexpressing fruits was also significantly increased to 038 μg per gram fruit 252
compared to 004 μg per gram fruit in the control (Figure 4) These observations 253
provide direct evidence for a regulatory role for FaERF9 in promoting FaQR 254
biosynthesis and activity in ripening strawberry fruit Taken together these results 255
indicate that by activating the transcription of FaQR FaERF9 functions as a positive 256
regulator in furaneol biosynthesis 257
258
Correlation of FaERF9 expression and FaQR transcript profiles 259
GC-MS quantification showed that furanones are distributed in variable levels among 260
different strawberry cultivars (Supplemental Figure S3) The transcript profiles of 261
FaQR and FaERF9 in fruits of different cultivars were measured and linear 262
regression analysis was performed In the cultivars the changes in FaQR transcripts 263
correlated positively with those in FaERF9 transcripts (r = 079 plt001) (Figure 5) 264
In addition FaERF9 transcript levels also correlated with furanone content across 265
cultivars (Figure 5) 266
267
FaERF9 is an indirect regulator of the FaQR promoter and acts via 268
protein-protein interaction with FaMYB98 269
Although the results of the dual-luciferase assay expression analysis transient 270
overexpression and correlation analysis were all consistent with the suggestion that 271
FaERF9 regulates transcript abundance by acting on the FaQR promoter a yeast 272
one-hybrid assay indicated that FaERF9 cannot bind directly to the FaQR promoter 273
(Figure 6) This led us to speculate that activation may occur via a transcription 274
complex involving an additional as-yet unknown regulator which can bind directly to 275
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
11
the FaQR promoter 276
277
In parallel with the investigation of the FaAP2ERF genes a cDNA library screening 278
was performed with a yeast one-hybrid assay using the promoter of FaQR as the bait 279
This screen identified several transcription factors that could physically bind to the 280
FaQR promoter but only one MYB could activate transcription from the FaQR 281
promoter (approximately 56-fold) relative to the control (Figure 6) in the 282
dual-luciferase assay This MYB showed 44 amino acid identity with MYB98 283
(GenBank ABA420611) a transcriptional regulator in the synergid cells in 284
Arabidopsis (Kasahara et al 2005) and it was designated as FaMYB98 The 285
specificity of FaMYB98 binding to the FaQR promoter was confirmed by EMSA 286
assay (Figure 7) and increasing the concentration of the cold probe reduced binding 287
In addition mutating the putative binding sites (Goacutemez-Maldonado et al 2004 288
Punwani et al 2007) as shown in Figure 7 eliminated FaMYB98 protein binding 289
When the combined effect of FaERF9 and FaMYB98 was analysed (Figure 8) a 290
synergistic 14-fold activation of the FaQR promoter was observed compared with the 291
activation by either FaERF9 or FaMYB98 which alone promoted transactivation 292
39-fold and 45-fold respectively In addition overexpression of both genes 293
(FaERF9-FaMYB98-SK) in strawberry fruits resulted in higher expression of 294
FaERF9 transcripts and higher furanone content than overexpression of FaERF9 295
(Supplemental Figure S4 Supplemental Table S3) Subcellular localization analysis 296
revealed that FaMYB98 was also localized in the nucleus (Supplemental Figure S5) 297
298
To investigate the potential interactions between FaERF9 and FaMYB98 the 299
DUALhunter system was used (Figure 9) Cells expressing the FaMYB98 and 300
FaERF9 protein pair using either FaMYB98 or FaERF9 as the bait grew on DDO 301
QDO and QDO supplemented with 1 mM 3-AT selective medium indicating 302
interaction between the two proteins This putative protein-protein interaction was 303
confirmed by BiFC assay and the combinations of FaMYB98-YFPNFaERF9-YFPC 304
and FaERF9-YFPNFaMYB98-YFPC exhibited strong coincident signals in the 305
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
12
nucleus while negative controls produced no detectable fluorescence signal (Figure 306
10) In addition coexpression of FaERF9-YFPNFaERF9-YFPC as well as 307
FaMYB98-YFPNFaMYB98-YFPC also generated signals in the nucleus indicating 308
that FaERF9 and FaMYB98 both could form homodimers or possibly multimers in 309
the nucleus (Figure 10) 310
311
Discussion 312
The AP2ERF superfamily in strawberry 313
The AP2ERF superfamily of plant transcription factors is defined by the AP2ERF 314
domain and comprises the ERF AP2 and RAV families as well as one soloist member 315
(Riechmann et al 2000 Weirauch and Hughes 2011) The completion of multiple 316
plant genome sequences has enabled a genome-scale analysis of the AP2ERF family 317
which in recent years has been systematically studied in diverse fruit species such as 318
tomato grape peach and kiwi fruit (Zhuang et al 2009 Sharma et al 2010 Licausi 319
et al 2010 Yin et al 2010 Pirrello et al 2012 Zhang et al 2012 Zhang et al 320
2016) A few AP2ERF genes have been isolated and characterized in strawberry and 321
CBF orthologs (Owens et al 2002 Koehler et al 2012 Zhang et al 2014) have 322
been identified from different strawberry cultivars in several independent studies 323
Although they have distinct names eg Fragaria times ananassa CBF1 (FaCBF1) 324
FaCBF4 (GenBank HQ9105151) and CBF1 (GenBank EU1172142) according to 325
the phylogenetic tree generated in this study the orthologs of 326
CBF1CBF4CBF2CBF3 in Arabidopsis are similar to each other and to FaERF20 327
(Supplemental Figure S1) (Owens et al 2002 Koehler et al 2012 Zhang et al 328
2014) FaERF20 has 85 sequence similarity with FaCBF1 identified by Owens et 329
al (2002) 93 similarity with FaCBF4 amplified by Koehler et al (2012) and 75 330
similarity with CBF1 cloned by Zhang et al (2014) The AP2ERF genes 331
characterized in other studies (Jia et al 2011 GAO et al 2015 Chai and Shen 2016 332
Mu et al 2016) are also noted in Supplemental Table S1 333
334
Based on the computational analysis we have identified a total of 120 AP2ERF 335
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13
genes in octoploid strawberry (Supplemental Table S1) The number of predicted 336
AP2ERF genes (120) is comparable to those observed in other fruits including 337
tomato (112) Chinese plum (116) citrus (126) and peach (131) but lower than those 338
reported for grape (149) (Xie et al 2016) As shown in Supplemental Table S2 79 339
(95 genes) of the AP2ERF genes belong to the ERF family in strawberry constituting 340
the largest sub-family The members of this sub-family can be classified into 10 341
groups (group I to X) according to their sequence similarities to the Arabidopsis ERF 342
genes (Nakano et al 2006) The AP2 family encompasses the same number of genes 343
in Arabidopsis citrus and strawberry (eighteen) (Nakano et al 2006 Xie et al 2014) 344
and there are six RAV genes in strawberry which are highly conserved in dicots such 345
as Vitis vinifera Arabidopsis thaliana and Populus trichocarpa (Licausi et al 2010) 346
347
Role of FaERF9 in regulating the biosynthesis of HDMF a positive regulator 348
acting in an indirect manner 349
The large-scale screening of the AP2ERF superfamily in strawberry led to 350
identification of 11 ERFs and 1 RAV that trans-activated the FaQR promoter more 351
than two-fold with the highest activation caused by FaERF9 which trans-activated 352
the FaQR promoter (Figure 2) as well as up-regulating FaQR expression and furanone 353
production in transient overexpression assays (Figure 4) which has been extensively 354
used to explore the fruit-associated gene functions in strawberry (Han et al 2015 355
Medina-Puche et al 2015 Vallarino et al 2015 Carvalho et al 2016 Song et al 356
2016 Wang et al 2018) FaERF9 transcripts accumulate in the fruit apical section 357
before the basal section (Figure 3) a finding consistent with the actual changes in 358
furaneol content (Figure 1) and the expression of FaQR (Figure 1) The association 359
between FaERF9 transcripts and accumulation of furanones were also established 360
with different strawberry cultivars The correlation between FaERF9 and FaQR 361
expression as well as furanone content among cultivars supports a positive role of 362
FaERF9 in regulating furanone content (Figure 5) These results indicate that 363
FaERF9 transcript abundance may be a good indicator of the abundance of these 364
important flavour volatiles in fruits of different cultivars This should be considered as 365
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14
a method for high-throughput variety screening to replace direct measurement of 366
volatiles 367
368
FaERF9 is a member of the ERF group II family and is most closely related to the 369
Arabidopsis genes At1g44830 (ATERF014) At1g21910 (DREB26) and At1g77640 370
(Supplemental Figure S1) At1g44830 was observed to be strongly up-regulated in a 371
comprehensive microarray analysis of the root transcriptome following NaCl 372
exposure (Jiang and Deyholos 2006) At1g21910 (DREB26) was functionally 373
characterized as a trans-activator localized in the nucleus exhibiting tissue-specific 374
expression and participating in plant developmental processes as well as biotic andor 375
abiotic stress signalling (Krishnaswamy et al 2011) However none of these genes 376
have been reported as furanone regulators In strawberry another five genes 377
(FaERF6 FaERF7 FaERF8 FaERF10 and FaERF11) also belong to the same 378
group with FaERF8 also showing somewhat weaker activation activity towards the 379
FaQR promoter than FaERF9 The fact that FaERF9 could not bind directly to the 380
promoter of FaQR (Figure 6) indicates that it might function as an indirect regulator 381
of FaQR and furaneol biosynthesis 382
383
A FaERF9 and FaMYB98 complex is involved in regulating FaQR and furaneol 384
biosynthesis 385
The finding that FaERF9 could interact with FaMYB98 protein (Figures 9 and 386
Figure 10) and that FaMYB98 could physically bind to the FaQR promoter (Figure 6 387
and Figure 7) provides evidence for a regulatory mechanism whereby FaERF9 388
regulates FaQR and furaneol production as part of a complex with an MYB 389
transcription factor Since co-overexpression of FaERF9 and FaMYB98 resulted in 390
much higher activation activity towards FaQR we speculate that FaERF9 may 391
recruit FaMYB98 homologs in tobacco to activate the FaQR promoter (Figure 8) 392
FaOMT is another key gene for furanone biosynthesis and a potential target for 393
transcriptional activation However FaERF9 did not significantly activate the 394
FaOMT promoter in a dual-luciferase assay and the transcript level of FaOMT in the 395
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15
FaERF9-overexpressing fruits showed no significant difference from that in the 396
control (Supplemental Figure S6 Supplemental Figure S7) The FaOMT promoter 397
was significantly induced by FaMYB98 but no synergistic effect of FaERF9 and 398
FaMYB98 on the promoter was observed (Supplemental Figure S6) In previous 399
studies of the regulation of plant volatile compounds MYBs have been characterized 400
as being involved mainly in the regulation of the benzenoidphenylpropanoid pathway 401
that produces floral volatiles in petunia and eugenol in ripe strawberry fruit (Verdonk 402
et al 2005 Dal Cin et al 2011 Colquhoun et al 2011 Spitzer-Rimon et al 2012 403
Medina-Puche et al 2015) but their role in formation of volatiles from other 404
pathways has not been reported Our study demonstrates a role for MYB in the 405
synthesis of furaneol a carbohydrate-derived volatile compound and reveals the 406
synergistic interactions between an MYB and ERF in a transcription complex (Figure 407
8 Figure 9 and Figure 10) 408
409
Recent research has provided evidence for interactions between AP2ERF and MYB 410
transcription factors in regulating other aspects of fruit quality including texture 411
(EjAP2-1 and EjMYB Zeng et al 2015) and colour (PyERF3 and PyMYB114 Yao 412
et al 2017) A group VIII ERF has also recently been shown to interact with an MYB 413
to regulate floral scent production in petunia (Liu et al 2017) In strawberry fruit 414
DOF in combination with an MYB has been reported to be involved in the regulation 415
of eugenol production and the identification of this second transcription factor (DOF) 416
suggests that it is a good target in breeding for improved flavour (Molina-Hidalgo et 417
al 2017 Tieman 2017) Considering its important contribution to flavour in 418
strawberry and many other highly valued fruit crop species (pineapple tomato mango 419
etc) very little is known about regulation of furaneol synthesis Here we established 420
the role of FaERF9 in the regulation of HDMF synthesis by direct protein-protein 421
interactions with FaMYB98 to synergistically trans-activate FaQR The functional 422
identification of this complex enhances our knowledge of the regulation of volatile 423
compound synthesis and identifies a new AP2ERF-MYB complex Further 424
examination of the other ERFs that stimulated transcription from the FaQR promoter 425
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16
(Figure 2) may provide additional information about the complexity of this regulation 426
Overall this study provides important clues for understanding the transcriptional 427
regulation of HDMF synthesis and identifies specific transcription factors that are 428
likely to be good targets for molecular breeding for improved flavour 429
430
Conclusions 431
Screening of the AP2ERF superfamily in strawberry (Fragaria times ananassa) 432
identified candidate members capable of activating the FaQR promoter An ERF 433
transcription factor was identified as a positive regulator of HDMF synthesis in 434
strawberry fruit and the mechanism of activation was shown to involve an ERF-MYB 435
transcription complex that regulates transcription of FaQR leading to the biosynthesis 436
of HDMF the characteristic volatile compound which has a major influence on 437
strawberry aroma 438
439
Materials and Methods 440
441
Plant Materials and Growth conditions 442
The strawberry (Fragaria times ananassa cv lsquoYuexinrsquo an octoploid cultivar) fruit used in 443
this study were bred by Zhejiang Academy of Agricultural Sciences (Haining 444
Zhejiang) Fruits at various developmental and ripening stages including G (green) T 445
(turning) IR (intermediate red) and R (full red) were harvested (Figure 1) and 446
transported to the laboratory within 2 h Thirty-six fruits of uniform size and free of 447
visible defects were selected at each stage with twelve fruits in each biological 448
replicate After removing the calyces fruits were then divided into the basal and 449
apical sections which were sampled separately (Figure 1) They were rapidly cut into 450
pieces frozen immediately in liquid nitrogen and stored at -80deg C until use Red ripe 451
fruits of different strawberry cultivars (Fragaria times ananassa octoploid cultivars) 452
including lsquoYuelirsquo lsquoBenihoppersquo lsquoMengxiangrsquo lsquoAmaoursquo lsquo10-1-4rsquo lsquoAkihimersquo lsquoSweet 453
Charliersquo lsquo07-1-4rsquo lsquoDarselectrsquo lsquoYuexinrsquo and lsquoXuemeirsquo were also provided by Zhejiang 454
Academy of Agricultural Sciences For each cultivar the fruits of three biological 455
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17
replicates were sampled frozen in liquid nitrogen and stored at -80deg C for further use 456
457
Tobacco plants (Nicotiana benthamiana) used for dual-luciferase assays and 458
subcellular localization analysis in this study were grown in a growth chamber with a 459
lightdark cycle of 16 h8 h at 24degC 460
461
Detection of DMMF and HDMF 462
Automated HS-SPME-GC-MS was performed to detect both furanones in lsquoYuexinrsquo 463
strawberry fruit (Zorrilla-Fontanesi et al 2012) Samples were ground into a powder 464
under liquid nitrogen for analysis 465
466
For the detection of DMMF (Figure 1) 05 g (fresh weight) of each sample was 467
weighed in the vial to which was added 1 mL of EDTA solution (100 mM pH 75) 1 468
mL of CaCl2 solution (mv = 20) and 20 microL of 2-octanol as the internal standard 469
(007 μgμL) The mixture was homogenized and the vial closed and placed on the 470
sample tray for analysis by CombiPAL autosampler (CTC Analytic CA USA) The 471
fruit volatiles were sampled by headspace solid-phase microextraction with a 65-μm 472
polydimethylsiloxane-divinylbenzene fibre (PDMS-DVB) Initially vials were 473
pre-incubated at 50degC for 10 min under continuous agitation (500 rpm) then volatiles 474
were extracted for 30 min at the same temperature and agitation speed After that the 475
fibre was desorbed in the GC injection port for 5 min in splitless mode The 7890A 476
GC chromatograph was equipped with a DB-5ms column (60 m times 250 μm times 1 μm 477
JampW Scientific Folsom CA USA) with helium as the carrier gas at a constant flow 478
of 12 mLmin The GC was programmed at an initial temperature of 35degC for 2 min 479
with a ramp of 5degC min up to 250degC and held for 5 min The injection port interface 480
and MS source temperatures were 250degC 260degC and 230degC respectively The 481
ionization potential was set at 70 eV recorded by a 5975B mass spectrometer (Agilent 482
Technologies JampW Scientific Folsom CA USA) and the scanning speed was 7 483
scanss The same method was used to analyse HDMF and DMMF in fruits from 484
different cultivars (Supplemental Figure S3) except for the sample preparation 485
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18
procedure (Araguumlez et al 2013) briefly 05 g (fresh weight) of powdered fruit was 486
incubated at 30degC in a water bath for 5 min then 2 mL of NaCl (mv = 20) and 20 487
microL of 2-octanol as the internal standard (007 μgμL) were added and homogenized 488
489
For the detection of HDMF (Figure 1) and both furanones (Figure 4 and Supplemental 490
Table S3) a liquid-injection system equipped with CTC Pal ALS was used One gram 491
(fresh weight) of powdered fruit and 2 mL of NaCl (mv = 20) were homogenized in 492
a 10-mL tube and 300 μL of CH2Cl2 and 20 microL of 2-octanol (0766 μgμL) as the 493
internal standard were added to extract the volatiles the mixture was then 494
homogenized again The tubes were stored at room temperature for 20 min and 495
centrifuged at 12000 rpm for 5 min The subnatant was pipetted into a clean 15-mL 496
tube in which 20 mg of anhydrous sodium sulphate was added the tube was left 497
without shaking for half an hour Then 150 μL of the solution was transferred into a 498
GC vial and placed on the sample tray as described above Each sample (1 μL) was 499
injected using the autosampler and the analysis was accomplished by a 7890A 500
GC-MS system (Agilent Technologies JampW Scientific Folsom CA USA) equipped 501
with a DB-WAX column (30 m times 025 mm times 025 μm JampW) Helium (12 mLmin) 502
was used as a carrier gas The injection port (splitless injection mode) interface and 503
MS source temperatures were as described above The oven temperature was set at 504
60degC for 4 min then increased to 180degC at a rate of 4degCmin and maintained for 30 505
min DMMF was identified by comparison of electron ionization mass spectra and 506
retention time data with the data from the NISTEPANIH mass spectral library 507
(NIST-08 and Flavor) HDMF (Figure 1) was identified and qualified by comparison 508
with injected standard (Sigma) The quantitative analysis of both furanones (Figure 4 509
Supplemental Table S3 and Supplemental Figure S3) was determined using the peak 510
area of the internal standard as a reference based on total ion chromatogram (TIC) 511
512
RNA isolation and Reverse Transcription Quantitative PCR (RT-qPCR) 513
Total RNA from strawberry samples was isolated in this study using the CTAB 514
method (Chang et al 1993) Genomic DNA contamination was eliminated by 515
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19
TURBO Dnase (Ambion) 1 μg of RNA was used to obtain cDNA using an IScriptTM 516
cDNA Synthesis Kit (Bio-Rad) The synthesized cDNA was diluted with water (120) 517
and 2 μL of diluted cDNA was used as the template for RT-qPCR Reactions were 518
performed in a total volume of 20 μL consisting of 10 μL of SYBR PCR supermix 519
(Bio-Rad) 1 μL of each primer (10 μM) 6 μL of DEPC-H2O and 2 μL of diluted 520
cDNA on CFX96 instrument (Bio-Rad) (Yin et al 2012) The oligonucleotide 521
primers for RT-qPCR analysis of genes including the AP2ERF FaQR and FaOMT 522
were designed according to the coding sequences of genes and the specificity was 523
verified before use (Min et al 2012) NCBIPrimer-BLAST was applied to design the 524
primers Relative expression levels were normalized to that of an internal controlmdashthe 525
interspacer 26S-18S strawberry RNA housekeeping gene FaRIB413 526
(Zorrilla-Fontanesi et al 2012) To investigate the differential expression of genes 527
during fruit development and ripening stages relative expression of each gene at the 528
R stage in the basal fruit section was set as 1 using the 2minus∆∆119862119879 method For transient 529
overexpression assay relative expression of control fruits with an empty vector (SK) 530
was set as 1 The primers used in RT-qPCR are listed in Supplemental Table S4 531
532
Gene isolation and analysis 533
Multiple database searches were performed to identify members of the strawberry 534
(Fragaria times ananassa) AP2ERF superfamily in the published strawberry databases 535
and annotations of Fragaria times ananassa and Fragaria times vesca by using the 536
AP2ERF DNA binding domain as a query sequence and 120 genes were identified 537
with AP2ERF domain(s) Based on the BLAST result primers (listed in 538
Supplemental Table S5) were used to amplify the coding full-length cDNAs of 539
AP2ERF genes The deduced amino acid sequences of AP2ERF proteins in 540
Arabidopsis thaliana used for construction of a phylogenetic tree were obtained from 541
the Arabidopsis Information Resource (TAIR) Alignment of the proteins was 542
performed using the neighbour-joining method in ClustalX (v181) and the 543
phylogenetic tree was constructed using FigTree (v131) 544
545
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
20
FaMYB98 was obtained by yeast one-hybrid screening sequencing and the full-length 546
sequences were predicted by BLAST Primers were designed (listed in Supplemental 547
Table S5) to amplify the full-length coding sequence 548
549
The promoter of FaQR was cloned by Genome Walking as previously described (Yin 550
et al 2010) and conserved cis-element motifs in the promoter were manually 551
searched 552
553
Conserved domains within the FaAP2ERF proteins and FaMYB98 were analysed by 554
CD-search (httpswwwncbinlmnihgovStructurecddwrpsbcgi) and cellular 555
locations of proteins including FaERF9 and FaMYB98 were predicted with the 556
WoLF PSORT program (httpswwwgenscriptcomwolf-psorthtml) 557
558
Dual-Luciferase Assays 559
In accordance with a previous protocol (Yin et al 2010) the full-length cDNAs of 560
FaAP2ERF or FaMYB98 transcription factors were cloned into pGreen II 0029 561
62-SK vector and the promoter of FaQR was cloned into pGreen II 0800-LUC vector 562
A luciferase gene from Renillia (REN) driven by a 35S promoter in the LUC vector 563
acted as a positive control The above constructs were transiently expressed in 564
Nicotiana benthamiana leaves by Agrobacterium-mediated infiltration (strain 565
GV3101) and the activity of the TFs on the promoter was measured on the third day 566
after infiltration indicated by the ratio of enzyme activities of firefly luciferase (LUC) 567
and renilla luciferase (REN) using a Modulus Luminometer (Promega Madison WI 568
USA) To determine the activity of a specific transcription factor towards the 569
promoter we mixed the Agrobacterium culture with 1 mL of TF and 100 μL of 570
promoter and the LUCREN value of the empty vector SK on the promoter was set as 571
1 as a calibrator To test the combined effect of two transcription factors on the 572
promoter to the Agrobacterium culture mixture we added 05 mL of each TF and 100 573
μL of promoter the effect of the mixtures that contained each transcription factor (05 574
mL) and empty vector SK (05 mL) was also tested on the promoter as a control 575
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
21
576
Subcellular localization analysis 577
35S-FaERF9-GFP and 35S-FaMYB98-GFP were transiently expressed in tobacco (N 578
benthamiana) leaves by Agrobacterium infiltration (EHA105) using the same method 579
as described in the dual-luciferase assay above The transiently infected leaves were 580
imaged on the third day after infiltration using a Nikon A1-SHS confocal laser 581
scanning microscope The excitation wavelength for GFP fluorescence was 488 nm 582
and fluorescence was detected at 490ndash520 nm The primers used for GFP construction 583
are listed in Supplemental Table S6 584
585
Transient overexpression in strawberry fruit 586
Transient overexpression of FaERF9 and an overexpression binary vector (pGreen II 587
0029 62-SK-FaERF9-FaMYB98) were performed in strawberry fruit using the 588
FaERF9-SK construct described above for the dual-luciferase assays and the binary 589
vector constructed according to Liu et al 2013 The transfection of fruit was carried 590
out at the G stage (Hoffmann et al 2006) The FaERF9-SK construct and binary 591
vector were individually electroporated into Agrobacterium tumefaciens GV3101 and 592
the Agrobacterium culture suspended in infiltration buffer was infiltrated into the 593
whole fruit using a syringe As a control treatment fruits were infiltrated with 594
Agrobacterium carrying an empty vector SK under the same transfection conditions 595
Fruits were left attached to the plants and harvested on the seventh day after 596
infiltration Fruits of three biological replicates were sampled for further analysis 597
598
Yeast one-hybrid assay 599
In order to identify proteins that bind to the FaQR promoter the Matchmaker Gold 600
Yeast One-hybrid Library Screening System (Clontech USA) was used The sequence 601
of the FaQR promoter was cloned into the pAbAi vector and the construct was 602
integrated into the genome of the Y1HGold yeast strain A mixture of total RNA from 603
strawberry fruit at four stages (G T IR R) was used to construct the prey cDNA 604
library (TaKaRa) The background AbAr expression of Y1HGold FaQR-pAbAi strain 605
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
22
was tested according to the system user manual and then screening for protein-DNA 606
interactions was carried out Furthermore the full length of each transcription factor 607
was separately cloned into pGADT7 AD vector to confirm the screening results The 608
relationship between FaERF9 and FaQR promoter was also examined individually 609
Primers used in this assay are listed in Supplemental Table S6 610
611
Expression and purification of FaMYB98 recombinant protein 612
A 405-bp region spanning the DNA-binding domain of FaMYB98 was amplified 613
from FaMYB98 cDNA and cloned into a pET6timesHN vector (Clontech Palo CA USA) 614
to generate the recombinant N-terminal His-tagged protein the primers used are listed 615
in Supplemental Table S6 The resulting construct was sequenced and introduced into 616
Escherichia coli strain Rosetta 2(DE3)pLysS (Novagen) Ten millilitres of the 617
overnight culture was combined with 500 mL of an LB liquid medium (100 μgmL 618
ampicillin and 34 μgmL chloramphenicol) as described (Li et al 2017) Isopropyl 619
β-D-1-thiogalactopyranoside (IPTG) was added to a final concentration of 1 mM and 620
the bacterial culture was incubated at 18degC at 150 rpm for 18 h Then the cells were 621
harvested using a centrifuge and resuspended in 1times PBS buffer (Sangon Biotech) 622
after which they were disrupted by sonication and the supernatant was purified using 623
a HisTALONTM Gravity Column (Clontech) according to the user manual The PD-10 624
Desalting column (GE Healthcare) was then used for buffer change and sample 625
clean-up of proteins according to the gravity protocol SDS-PAGE was performed and 626
the protein was visualized using Coomassie brilliant blue 627
628
Electrophoretic mobility shift assay (EMSA) 629
A Lightshift Chemiluminescent EMSA kit (Thermo) was used to perform EMSA 630
experiments according to the manufacturerrsquos instructions Single-strand 631
oligonucleotides were synthesized and biotinylated by GeneBio Biotech (Hangzhou 632
China) The details of the EMSA assay are provided in Ge et al (2017) The probes 633
used for EMSAs are listed in Supplemental Table S6 634
635
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
23
636
Yeast two-hybrid assay 637
The DUALhunter system (Dualsystems Biotech Switzerland) was used to investigate 638
the interaction between FaERF9 and FaMYB98 Full-length coding sequences of 639
FaERF9 and FaMYB98 were respectively cloned into pDHB1 bait vector and 640
pPR3-N prey vector sequences were verified and the bait plasmid was 641
co-transformed with prey plasmid into NMY51 in the combinations below 642
FaMYB98-pDHB1pPR3-N FaMYB98-pDHB1FaERF9-pPR3-N 643
FaMYB98-pDHB1pOst1-NubI FaERF9-pDHB1pPR3-N 644
FaERF9-pDHB1FaMYB98-pPR3-N and FaERF9-pDHB1pOst1-NubI (Li et al 645
2017) Transformed cells were spread onto the following plates DDO (SD 646
medium-Trp-Leu) QDO (SD medium-Trp-Leu-His-Ade) and QDO+3-AT (QDO 647
medium supplemented with 1 mM 3-amino-124-triazole) The control plasmid 648
pOst1-NubI was used to determine whether the bait was functional the pPR3-N prey 649
vector plasmid was used to test whether the bait displayed non-specific background 650
and positive interactions were indicated by the growth of yeast on QDO and 651
QDO+3-AT plates The Primers used in the DUALhunter assay are listed in 652
Supplemental Table S6 653
654
Bimolecular fluorescence complementation (BiFC) assays 655
Full-length FaERF9 and FaMYB98 respectively were cloned into sequences 656
encoding the N- and C- fragments of YFP protein (Lv et al 2014) All constructs 657
were transiently expressed in tobacco (N benthamiana) leaves by Agrobacterium 658
infiltration (EHA105) The YFP fluorescence of transfected leaves was imaged 40 h 659
after infiltration by using a Nikon A1-SHS confocal laser scanning microscope The 660
excitation wavelength for YFP was 488 nm and fluorescence was detected at 520ndash661
540 nm Primers used are listed in Supplemental Table S6 662
663
Statistics 664
A Studentrsquos two-tailed t test ( plt005 plt001 and plt0001) was used to 665
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
24
determine significant differences between two groups in this study Microsoft Excel 666
was used to perform linear regressive analysis significant differences were 667
determined by SPSS Statistics 200 and scatter plots were prepared with Origin80 668
Least significant difference (LSD) at the 5 level was calculated using Microsoft 669
Excel Figures were prepared with Origin80 (Microcal Software Inc Northampton 670
MA USA) The online tool MetaboAnalyst 36 (httpwwwmetaboanalystca) was 671
used to analyse the transcript abundance of the AP2ERF genes 672
673
Accession numbers 674
Sequence data from this article have been deposited in GenBank under the accession 675
numbers MH332903-MH333022 for AP2ERF genes in Fragaria times ananassa and 676
MH333023 for FaMYB98 GenBank numbers for FaQR and FaOMT were 677
AY1588361 (Raab et al 2006) and AF2204912 (Wein et al 2002) 678
679
Supplemental Material 680
Supplemental Figure S1 Phylogenetic analysis of FaAP2ERF and Arabidopsis 681
AP2ERF proteins 682
Supplemental Figure S2 Analysis of FaAP2ERF gene expression patterns in 683
strawberry fruit during development and ripening 684
Supplemental Figure S3 Contents of furanones in fruit of strawberry cultivars 685
Supplemental Figure S4 Relative expression of FaERF9 in FaERF9-FaMYB98- 686
and FaERF9-overexpressing fruits 687
Supplemental Figure S5 Subcellular localization of FaMYB98 688
Supplemental Figure S6 The combined activation effects of FaERF9FaMYB98 on 689
the FaOMT promoter 690
Supplemental Figure S7 Relative expression of FaOMT in 691
FaERF9-overexpressing fruits 692
Supplemental Table S1 AP2ERF superfamily genes in Fragaria times ananassa 693
Supplemental Table S2 Classification of the AP2ERF superfamily members in 694
Fragaria times ananassa 695
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25
Supplemental Table S3 Furanone content in FaERF9-FaMYB98- and 696
FaERF9-overexpressing fruits 697
Supplemental Table S4 Primers used for reverse transcription quantitative PCR 698
(RT-qPCR) 699
Supplemental Table S5 Primers used to amplify the full-length coding sequences of 700
AP2ERF genes and FaMYB98 in strawberry (Fragaria times ananassa) 701
Supplemental Table S6 Primers used for vector construction 702
703
Acknowledgments 704
This research was supported by the National Key Research and Development 705
Program (2016YFD0400101) the Project of the Science and Technology Department 706
of Zhejiang Province (2016C04001) and the 111 Project (B17039) 707
708
Figure legends 709
Figure 1 Changes in furanone content and furanone biosynthetic genes during 710
strawberry (Fragaria times ananassa Duch cv Yuexin) fruit development and ripening 711
A Fruits were collected at four ripening stages G (green stage) T (turning stage) IR 712
(intermediate red stage) R (full red stage) B Changes in the contents of furaneol 713
(HDMF) and mesifurane (DMMF) HDMF content was calculated using a standard 714
curve of HDMF while DMMF content was calculated with an internal standard as the 715
reference C Expression levels of FaQR and FaOMT The expression levels of each 716
gene were calculated relative to corresponding values in the basal section at the R 717
stage SEs were calculated from three replicates and LSD values represent the least 718
significant differences at p = 005 719
Figure 2 Regulatory effects of FaAP2ERF on the promoter of FaQR LUCREN 720
values of the empty vector on FaQR promoter were used as the calibrator set as 1 721
and SEs were calculated from five replicates statistical significance was determined 722
by Studentrsquos two-tailed t test ( plt0001) 723
Figure 3 Expression and the subcellular localization of FaERF9 A The expression 724
levels were calculated relative to the levels in the basal section at the R stage B 725
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
26
Subcellular localization analysis was performed in tobacco leaves The tobacco used 726
in the assay was stably transformed with a specific nucleus localized red fluorescence 727
protein construct and the red fluorescence indicates the nucleus-localized signal 728
(NLS) Scale bar = 25 microm SEs were calculated from three replicates 729
Figure 4 Transient overexpression of FaERF9 in strawberry fruit A Relative 730
expression of FaQR and FaERF9 in FaERF9-OX fruit 7 days after infiltration The 731
expression was calculated relative to the average value in control (SK) fruits B 732
HDMF and DMMF content in FaERF9-OX fruit The content of both furanones 733
were quantified using the peak area of the internal standard (2-octanol) as the 734
reference SEs were calculated from three replicates Statistical significance was 735
determined by Studentrsquos two-tailed t test ( plt005 plt001 plt0001) 736
Figure 5 Scatter plots of 11 strawberry cultivars A Linear regression analysis 737
between FaERF9 expression and FaQR expression B Linear regression analysis 738
between FaERF9 expression and furanone content The relative expression was 739
normalized to that of the housekeeping gene FaRIB413 and furanone content was 740
calculated with internal standard as the reference Significant differences were 741
determined by SPSS Statistics 200 742
Figure 6 Interactions of FaERF9 and FaMYB98 with the FaQR promoter A Yeast 743
one-hybrid analysis of the interaction of FaERF9 and FaQR promoter B Yeast 744
one-hybrid analysis of the interaction of FaMYB98 and FaQR promoter C 745
Regulatory effect of FaMYB98 on the FaQR promoter Auto-activation was tested on 746
SD-Ura (synthetically defined medium without uracil) in presence of Aureobasidin A 747
(AbA) and physical interaction was determined on SD-Leu (synthetically defined 748
medium without leucine) in presence of AbA LUCREN values of the empty vector 749
on FaQR promoter were used as the calibrator set as 1 and error bars were calculated 750
from five replicates Statistical significance was determined by Studentrsquos two-tailed t 751
test ( plt005 plt001 plt0001) 752
Figure 7 Electrophoretic mobility shift assay of FaMYB98 binding to FaQR 753
promoter A The probe sequence used for EMSA and mutated nucleotides are 754
indicated with lowercase letters B Purified DNA-binding domain of FaMYB98 755
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
27
protein and biotin-labelled DNA probe were mixed and analysed on 6 native 756
polyacrylamide gels and then photographed Presence or absence of specific probes is 757
marked by the symbol + or - 758
Figure 8 The combined activation effects of FaERF9FaMYB98 on the FaQR 759
promoter LUCREN values obtained with the empty vector and FaQR promoter were 760
used as the calibrator set as 1 and error bars were calculated from five replicates 761
Figure 9 Yeast two-hybrid analysis of the protein-protein interactions between 762
FaMYB98 and FaERF9 Positive interactions were determined by the growth of 763
yeast cells on selection plates Bait with pOST acted as positive controls and bait with 764
pPR3 as negative controls DDO synthetically defined medium without tryptophan 765
and leucine QDO synthetically defined medium without tryptophan leucine 766
histidine and adenine QDO+3AT QDO medium supplemented with 1 mM 767
3-aminotriazole 768
Figure 10 BiFC analysis of the protein-protein interactions between FaMYB98 and 769
FaERF9 The pairs of fusion proteins tested were FaMYB98-YFPN+FaERF9-YFPC 770
FaERF9-YFPN+FaMYB98-YFPC FaMYB98-YFPN+FaMYB98-YFPC and 771
FaERF9-YFPN+FaERF9-YFPC The other combinations were negative controls 772
The tobacco used in the assay was stably transformed with a specific 773
nucleus-localized red fluorescence protein construct and the red fluorescence 774
indicated the nucleus-localized signal (NLS) Fluorescence of the yellow fluorescence 775
protein (YFP) visualized the interaction in vivo Scale bar = 25 microm 776
777
Literature Cited 778
779
Agarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression 780
of PgDREB2A transcription factor enhances abiotic stress tolerance and activates 781
downstream stress-responsive genes Mol Biol Rep 37 1125-1135 782
Araguumlez I Osorio S Hoffmann T Rambla JL Medina-Escobar N Granell A 783
Botella MAacute Schwab W Valpuesta V (2013) Eugenol production in achenes and 784
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
28
receptacles of strawberry fruits is catalyzed by synthases exhibiting distinct kinetics 785
Plant Physiol 163 946-958 786
Carvalho RF Carvalho SD OrsquoGrady K Folta KM (2016) Agroinfiltration of 787
strawberry fruit mdash a powerful transient expression system for gene validation Curr 788
Plant Biol 6 19-37 789
Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic 790
(Amsterdam) 210 34-40 791
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating 792
RNA from pine trees Plant Mol Biol Rep 11 113-116 793
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC 794
Clark DG (2011) PhMYB4 fine-tunes the floral volatile signature of 795
Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143 796
Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz 797
EA Taylor MG Smits-Kroon MT Schuurink RC Haring MA Giovannoni J 798
Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic 799
pathway by ectopic expression of a MYB transcription factor in tomato fruit Plant 800
Cell 23 2738-2753 801
Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan 802
XW Yang ZY (2017) Differential responses of four biosynthetic pathways of 803
aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under 804
interaction of light and temperature Food Chem 221 356-364 805
Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of 806
differentially-expressed genes during somatic embryogenesis in Fragaria times 807
ananassa Duch lsquoBenihopprsquo J Hortic Sci Biotechnol 90 671-681 808
Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 809
transcriptionally regulates chilling-induced lignification of loquat fruit via physical 810
interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136 811
Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM 812
(2004) Functional interactions between a glutamine synthetase promoter and MYB 813
proteins Plant J 39 513-526 814
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
29
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) 815
Sucrose nonfermenting1-related protein kinase26 an ortholog of open stomata1 is 816
a negative regulator of strawberry fruit development and ripening Plant Physiol 817
167 915-930 818
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene 819
expression in strawberry fruit (Fragaria times ananassa) by agroinfiltration a rapid 820
assay for gene function analysis Plant J 48 818-826 821
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of 822
selected aroma-active compounds in strawberries by headspace solid-phase 823
microextraction gas chromatography and correlation with sensory descriptive 824
analysis J Food Sci 72 S487-S496 825
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid 826
plays an important role in the regulation of strawberry fruit ripening Plant Physiol 827
157 188-199 828
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of 829
NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes BMC 830
Plant Biol 6 20 831
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN 832
(2005) MYB98 is required for pollen tube guidance and synergid cell differentiation 833
in Arabidopsis Plant Cell 17 2981-2992 834
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional 835
characterization of enone oxidoreductases from strawberry and tomato fruit J 836
Agric Food Chem 55 6705-6711 837
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You 838
J-S Rohloff J Randall SK Alsheikh M (2012) Proteomic study of 839
low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ 840
in cold tolerance Plant Physiol 159 1787-1805 841
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional 842
characterization of four APETALA2-family genes (RAP26 RAP26L DREB19 843
and DREB26) in Arabidopsis Plant Mol Biol 75 107-127 844
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
30
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon 845
J Gupta V (2013) An oxidoreductase from lsquoAlphonsorsquo mango catalyzing 846
biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494 847
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in 848
strawberries Z Lebensm-Unters Forsch 195 120-123 849
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X 850
(2015) Label-free quantitative proteomics to investigate strawberry fruit proteome 851
changes under controlled atmosphere and low temperature storage J Proteomics 852
120 44-57 853
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 854
cooperates with CitWRKY1 to participate in citric acid degradation via 855
up-regulation of CitAco3 J Exp Bot 68 3419-3426 856
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription 857
factor CitERF71 activates the terpene synthase gene CitTPS16 involved in the 858
synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938 859
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and 860
transcriptomic analysis of the AP2ERF superfamily in Vitis vinifera BMC 861
Genomics 11 719 862
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive 863
Factor (AP2ERF) transcription factors mediators of stress responses and 864
developmental programs New Phytol 199 639-649 865
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 866
interacting with EOBI negatively regulates fragrance biosynthesis in petunia 867
flowers New Phytol 215 1490-1502 868
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu 869
CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 in regulating 870
anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) 871
during anthocyanin biosynthesis Plant Cell Tissue Organ Cult 115 285-298 872
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
31
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao 873
CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphate signaling and 874
homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597 875
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC 876
Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL 877
Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor 878
regulates eugenol production in ripe strawberry fruit receptacles Plant Physiol 168 879
598-614 880
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics 881
and volatile constituents of strawberry (cv Cigaline) during maturation J Agric 882
Food Chem 52 1248-1254 883
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS 884
(2012) Ethylene-responsive transcription factors interact with promoters of ADH 885
and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 886
63 6393-6405 887
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM 888
Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-Franco A 889
Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific 890
transcription factor FaDOF2 regulates the production of eugenol in ripe fruit 891
receptacles J Exp Bot 68 4529-4543 892
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) 893
Comparison and verification of the genes involved in ethylene biosynthesis and 894
signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44 895
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the 896
ERF gene family in Arabidopsis and rice Plant Physiol 140 411-432 897
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in 898
sour cherry and strawberry and the heterologous expression of CBF1 in strawberry 899
J Am Soc Hortic Sci 127 489-494 900
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech 901
JC Ohme-Takagi M Regad F Bouzayen M (2012) Functional analysis and 902
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
32
binding affinity of tomato ethylene response factors provide insight on the 903
molecular bases of plant differential responses to ethylene BMC Plant Biol 12 190 904
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) 905
Methylpentoses are possible precursors of furanones in fruits Prikl Biokhim 906
Mikrobiol 28 123-127 907
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery 908
of synergid-expressed genes encoding filiform apparatus localized proteins Plant 909
Cell 19 2557-2568 910
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria 911
vesca L compared to those of cultivated berries Fragariatimes ananassa cv Senga 912
Sengana J Agric Food Chem 27 19-22 913
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W 914
Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of the strawberry 915
flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone 916
oxidoreductase Plant Cell 18 1023-1037 917
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L 918
Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim M Broun P Zhang 919
JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription 920
factors genome-wide comparative analysis among eukaryotes Science 290 921
2105-2110 922
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the 923
formation of 25-dimethyl-4-hydroxy-3(2H)-furanone in detached ripening 924
strawberry fruits J Agric Food Chem 46 1488-1493 925
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 926
25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in 927
strawberry fruits Phytochemistry 43 155-159 928
Schwab W (1998) Application of stable isotope ratio analysis explaining the 929
bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone in plants by a biological 930
maillard reaction J Agric Food Chem 46 2266ndash2269 931
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
33
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) 932
Molecules 18 6936-6951 933
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard 934
products Recent Res Dev Phytochem 1 643-673 935
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL 936
Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJ Sims CA 937
Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical 938
compositions a seasonal influence and effects on sensory perception PLoS One 9 939
e88446 940
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) 941
Identification phylogeny and transcript profiling of ERF family genes during 942
development and abiotic stress treatments in tomato Mol Genet Genomics 284 943
455-475 944
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) 945
CitAP210 activation of the terpene synthase CsTPS1 is associated with the 946
synthesis of (+)-valencene in lsquoNewhallrsquo orange J Exp Bot 67 4105-4115 947
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes 948
Dev Genes Evol 214 105-114 949
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K 950
Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the 951
key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151 952
Spitzer-Rimon B Farhi M Albo B Cnarsquoani A Ben Zvi MM Masci T Edelbaum 953
O Yu YX Shklarman E Ovadis M Vainstein A (2012) The R2R3-MYB-like 954
regulatory factor EOBI acting downstream of EOBII regulates scent production 955
by activating ODO1 and structural scent-related genes in petunia Plant Cell 24 956
5089-5105 957
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp 958
Bot 68 4407-4409 959
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla 960
JF Amaya I Giavalisco P Fernie AR Botella MA Valpuesta V (2015) Central 961
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
34
role of FaGAMYB in the transition of the strawberry receptacle from development 962
to ripening New Phytol 208 482-496 963
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 964
regulates fragrance biosynthesis in petunia flowers Plant Cell 17 1612-1624 965
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS 966
(2018) The potassium channel FaTPK1 plays a critical role in fruit quality 967
formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748 968
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) 969
Isolation cloning and expression of a multifunctional O-methyltransferase capable 970
of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma 971
compounds in strawberry fruits Plant J 31 755-765 972
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor 973
types their evolutionary origin and species distribution In A handbook of 974
transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular 975
Biochemistry 52 25-73 976
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of 977
odor (Buettner A Ed) Springer Cham 9-10 978
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS 979
(2014) Isolation classification and transcription profiles of the AP2ERF 980
transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271 981
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in 982
regulation of fruit quality Crit Rev Plant Sci 35 120-130 983
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ 984
Zhang SL Wu J (2017) Map-based cloning of the pear gene MYB114 identifies an 985
interaction with other transcription factors to coordinately regulate fruit 986
anthocyanin biosynthesis Plant J 92 437-451 987
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes 988
involved in regulating fruit ripening Plant Physiol 153 1280-1292 989
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
35
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) 990
Expression of ethylene response genes during persimmon fruit astringency removal 991
Planta 235 895-906 992
Zabetakis I Gramshaw JW Robinson DS (1999) 993
25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis and 994
biosynthesis-a review Food Chem 65 139-151 995
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci 996
Food Agric 74 421-434 997
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 998
an AP2ERF gene is a novel regulator of fruit lignification induced by chilling 999
injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1000
1325-1334 1001
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation 1002
classification and transcription profiles of the Ethylene Response Factors (ERFs) in 1003
ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215 1004
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML 1005
(2012) Genome-wide analysis of the AP2ERF superfamily in peach (Prunus 1006
persica) Genet Mol Res 11 4788-4809 1007
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and 1008
expression analysis of a CRTDRE-binding factor gene FaCBF1 from Fragaria times 1009
ananassa Acta Hortic 41 240-248 1010
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The 1011
Arabidopsis AP2ERF transcription factor RAP26 participates in ABA salt and 1012
osmotic stress responses Gene 457 1-12 1013
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B 1014
Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) Genome-wide 1015
analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic 1016
(Amsterdam) 123 73-81 1017
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF 1018
Valpuesta V Botella MA Granell A Amaya I (2012) Genetic analysis of 1019
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36
strawberry fruit aroma and identification of O-methyltransferase FaOMT as the 1020
locus controlling natural variation in mesifurane content Plant Physiol 159 1021
851-870 1022
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
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wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
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wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
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Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor regulates eugenol production in ripe strawberry fruitreceptacles Plant Physiol 168 598-614
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Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS (2012) Ethylene-responsive transcription factors interact withpromoters of ADH and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 63 6393-6405
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Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech JC Ohme-Takagi M Regad F Bouzayen M (2012)Functional analysis and binding affinity of tomato ethylene response factors provide insight on the molecular bases of plant differentialresponses to ethylene BMC Plant Biol 12 190
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) Methylpentoses are possible precursors of furanones in fruits PriklBiokhim Mikrobiol 28 123-127
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery of synergid-expressed genes encoding filiformapparatus localized proteins Plant Cell 19 2557-2568
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria vesca L compared to those of cultivated berriesFragariatimes ananassa cv Senga Sengana J Agric Food Chem 27 19-22
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of thestrawberry flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone oxidoreductase Plant Cell 18 1023-1037
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim MBroun P Zhang JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription factors genome-wide comparative analysisamong eukaryotes Science 290 2105-2110
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the formation of 25-dimethyl-4-hydroxy-3(2H)-furanonein detached ripening strawberry fruits J Agric Food Chem 46 1488-1493
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in strawberry fruits Phytochemistry 43 155-159
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (1998) Application of stable isotope ratio analysis explaining the bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone inplants by a biological maillard reaction J Agric Food Chem 46 2266ndash2269
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) Molecules 18 6936-6951Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard products Recent Res Dev Phytochem 1 643-673Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJSims CA Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical compositions a seasonal influence and effects on sensoryperception PLoS One 9 e88446
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) Identification phylogeny and transcript profiling of ERFfamily genes during development and abiotic stress treatments in tomato Mol Genet Genomics 284 455-475
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) CitAP210 activation of the terpene synthase CsTPS1 isassociated with the synthesis of (+)-valencene in Newhall orange J Exp Bot 67 4105-4115
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes Dev Genes Evol 214 105-114Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Spitzer-Rimon B Farhi M Albo B Cnaani A Ben Zvi MM Masci T Edelbaum O Yu YX Shklarman E Ovadis M Vainstein A (2012) TheR2R3-MYB-like regulatory factor EOBI acting downstream of EOBII regulates scent production by activating ODO1 and structuralscent-related genes in petunia Plant Cell 24 5089-5105
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp Bot 68 4407-4409Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla JF Amaya I Giavalisco P Fernie AR Botella MAValpuesta V (2015) Central role of FaGAMYB in the transition of the strawberry receptacle from development to ripening New Phytol208 482-496
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 regulates fragrance biosynthesis in petunia flowers PlantCell 17 1612-1624
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS (2018) The potassium channel FaTPK1 plays a critical role infruit quality formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) Isolation cloning and expression of a multifunctional O- wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma compounds in strawberry fruitsPlant J 31 755-765
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor types their evolutionary origin and speciesdistribution In A handbook of transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular Biochemistry 52 25-73
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of odor (Buettner A Ed) Springer Cham 9-10Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS (2014) Isolation classification and transcription profiles ofthe AP2ERF transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in regulation of fruit quality Crit Rev Plant Sci 35 120-130
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ Zhang SL Wu J (2017) Map-based cloning of the pear geneMYB114 identifies an interaction with other transcription factors to coordinately regulate fruit anthocyanin biosynthesis Plant J 92437-451
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes involved in regulating fruit ripening Plant Physiol 1531280-1292
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) Expression of ethylene response genes during persimmonfruit astringency removal Planta 235 895-906
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zabetakis I Gramshaw JW Robinson DS (1999) 25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis andbiosynthesis-a review Food Chem 65 139-151
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci Food Agric 74 421-434Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 an AP2ERF gene is a novel regulator of fruit lignificationinduced by chilling injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1325-1334
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Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation classification and transcription profiles of the Ethylene ResponseFactors (ERFs) in ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML (2012) Genome-wide analysis of the AP2ERF superfamily inpeach (Prunus persica) Genet Mol Res 11 4788-4809
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and expression analysis of a CRTDRE-binding factor gene FaCBF1from Fragaria times ananassa Acta Hortic 41 240-248
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Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The Arabidopsis AP2ERF transcription factor RAP26 participatesin ABA salt and osmotic stress responses Gene 457 1-12
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Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Genome-wide analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic (Amsterdam) 123 73-81Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
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8
186
Measurement of mRNA levels by RT-qPCR indicated that the transcript levels of both 187
FaQR (GenBank AY1588361) and FaOMT (GenBank AF2204912) increased 188
throughout ripening (Figure 1) Comparison of the expression of these genes showed 189
that the transcript levels of FaQR and FaOMT significantly increased as early as in T 190
stage in basal fruit sections and for each gene over half of the peak transcript 191
abundance occurred as early as in IR stage in the apical section while for the basal 192
section it was in the R stage indicating a gradient of gene expression and volatile 193
production from apex to base of the fruit during ripening 194
195
Genome-wide identification of AP2ERF gene family in strawberry 196
Coding sequences of 120 non-redundant FaAP2ERF genes were isolated and 197
identified from lsquoYuexinrsquo strawberry and a systematic nomenclature for the AP2ERF 198
family genes was used to distinguish the members based on the structural features 199
defined previously (Supplemental Table S1) (Shigyo and Ito 2004 Nakano et al 200
2006 Licausi et al 2013) CD-search analysis showed that this superfamily is 201
consisted of 95 ERFs 18 AP2 and 6 RAV family members and 1 soloist member 202
(Supplemental Table S2) Phylogenetic analysis of the Fragaria times ananassa and 203
Arabidopsis AP2ERF members is shown in Supplemental Figure S1 with the 120 204
AP2ERF genes divided into three major groups (ERF AP2 RAV) and a soloist and 205
the ERF family being further divided into 10 groups (groups I to X in Supplemental 206
Table S1) 207
208
We performed a dual-luciferase assay to determine the ability of 116 FaAP2ERF 209
members to activate transcription from the promoter of FaQR The results indicated 210
about 12 members (mainly belonging to the ERF and RAV families) showed a 211
significant activation effect on the FaQR promoter while the remaining members 212
showed very limited effects (Figure 2) The relative activity of only the following 12 213
FaAP2ERF transcripts reached the threshold value set at 2 FaERF8FaERF9 214
(group II) FaERF27FaERF29FaERF31FaERF32 (group IV) 215
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9
FaERF37FaERF38 (group V) FaERF62FaERF64 (group VIII) FaERF68 216
(group IX) and FaRAV4 (Figure 2) Of these FaERF9 exhibited the highest 217
activation effect on the FaQR promoter (466-fold) (Figure 2) The strawberry 218
FaERF9 cDNA is 699 bp long and ExPASy Compute pIMw tool analysis indicated 219
that this gene encodes a 232-amino acid protein with a calculated molecular mass of 220
254 KD and a pI of 56 221
222
FaERF9 expression pattern and subcellular localization 223
To further explore the connections between AP2ERFs and furaneol biosynthesis we 224
obtained the transcript profiles of the AP2ERF genes in strawberry fruit samples at 225
different fruit developmental and ripening stages by reverse transcription quantitative 226
PCR (RT-qPCR) excluding genes with very low abundance in the fruit samples The 227
results presented as a heatmap (Supplemental Figure S2) demonstrate that these 228
genes displayed various expression patterns in both the apical and basal sections and 229
by analysing the expression patterns of the members indicated as activators in the 230
dual-luciferase assay we found that only a few genes including FaERF8 FaERF9 231
FaERF27 FaERF32 and FaERF37 were up-regulated during ripening stages and 232
their expression correlated with furaneol accumulation in the fruit (Figure 1) 233
Furthermore the expression patterns of the up-regulated genes in the apical and basal 234
sections showed that one ERF gene FaERF9 not only showed an up-regulation 235
pattern in both sections but its expression in the apical section occurred ahead of that 236
in the basal section (Figure 3) consistent with the actual changes in furaneol content 237
(Figure 1) and the expression pattern of FaQR (Figure 1) The subcellular localization 238
of FaERF9 was predicted to be in the nucleus using the WoLF PSORT program In 239
experimental tests 35S-FaERF9-GFP (green fluorescence protein) showed strong 240
fluorescence in the nucleus and the green signal merged with the red fluorescence 241
signal of mCherry-nucleus-marker in tobacco plants (Figure 3) 242
243
Transient overexpression of FaERF9 in strawberry 244
The expression of FaERF9 in agro-infiltrated fruits was analysed by performing 245
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
10
RT-qPCR on the seventh day after infiltration by which time they had reached the IR 246
or R stage and the result showed that the transcript levels were significantly higher 247
(52-fold) than in control fruits (Figure 4) The expression of FaQR was examined in 248
the same fruits and the transcript abundance also increased 22-fold The relative 249
content of HDMF in the FaERF9-overexpressing fruits was 008 μg per gram fruit 250
and undetectable in the control fruits (Figure 4) The relative content of DMMF in the 251
overexpressing fruits was also significantly increased to 038 μg per gram fruit 252
compared to 004 μg per gram fruit in the control (Figure 4) These observations 253
provide direct evidence for a regulatory role for FaERF9 in promoting FaQR 254
biosynthesis and activity in ripening strawberry fruit Taken together these results 255
indicate that by activating the transcription of FaQR FaERF9 functions as a positive 256
regulator in furaneol biosynthesis 257
258
Correlation of FaERF9 expression and FaQR transcript profiles 259
GC-MS quantification showed that furanones are distributed in variable levels among 260
different strawberry cultivars (Supplemental Figure S3) The transcript profiles of 261
FaQR and FaERF9 in fruits of different cultivars were measured and linear 262
regression analysis was performed In the cultivars the changes in FaQR transcripts 263
correlated positively with those in FaERF9 transcripts (r = 079 plt001) (Figure 5) 264
In addition FaERF9 transcript levels also correlated with furanone content across 265
cultivars (Figure 5) 266
267
FaERF9 is an indirect regulator of the FaQR promoter and acts via 268
protein-protein interaction with FaMYB98 269
Although the results of the dual-luciferase assay expression analysis transient 270
overexpression and correlation analysis were all consistent with the suggestion that 271
FaERF9 regulates transcript abundance by acting on the FaQR promoter a yeast 272
one-hybrid assay indicated that FaERF9 cannot bind directly to the FaQR promoter 273
(Figure 6) This led us to speculate that activation may occur via a transcription 274
complex involving an additional as-yet unknown regulator which can bind directly to 275
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11
the FaQR promoter 276
277
In parallel with the investigation of the FaAP2ERF genes a cDNA library screening 278
was performed with a yeast one-hybrid assay using the promoter of FaQR as the bait 279
This screen identified several transcription factors that could physically bind to the 280
FaQR promoter but only one MYB could activate transcription from the FaQR 281
promoter (approximately 56-fold) relative to the control (Figure 6) in the 282
dual-luciferase assay This MYB showed 44 amino acid identity with MYB98 283
(GenBank ABA420611) a transcriptional regulator in the synergid cells in 284
Arabidopsis (Kasahara et al 2005) and it was designated as FaMYB98 The 285
specificity of FaMYB98 binding to the FaQR promoter was confirmed by EMSA 286
assay (Figure 7) and increasing the concentration of the cold probe reduced binding 287
In addition mutating the putative binding sites (Goacutemez-Maldonado et al 2004 288
Punwani et al 2007) as shown in Figure 7 eliminated FaMYB98 protein binding 289
When the combined effect of FaERF9 and FaMYB98 was analysed (Figure 8) a 290
synergistic 14-fold activation of the FaQR promoter was observed compared with the 291
activation by either FaERF9 or FaMYB98 which alone promoted transactivation 292
39-fold and 45-fold respectively In addition overexpression of both genes 293
(FaERF9-FaMYB98-SK) in strawberry fruits resulted in higher expression of 294
FaERF9 transcripts and higher furanone content than overexpression of FaERF9 295
(Supplemental Figure S4 Supplemental Table S3) Subcellular localization analysis 296
revealed that FaMYB98 was also localized in the nucleus (Supplemental Figure S5) 297
298
To investigate the potential interactions between FaERF9 and FaMYB98 the 299
DUALhunter system was used (Figure 9) Cells expressing the FaMYB98 and 300
FaERF9 protein pair using either FaMYB98 or FaERF9 as the bait grew on DDO 301
QDO and QDO supplemented with 1 mM 3-AT selective medium indicating 302
interaction between the two proteins This putative protein-protein interaction was 303
confirmed by BiFC assay and the combinations of FaMYB98-YFPNFaERF9-YFPC 304
and FaERF9-YFPNFaMYB98-YFPC exhibited strong coincident signals in the 305
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12
nucleus while negative controls produced no detectable fluorescence signal (Figure 306
10) In addition coexpression of FaERF9-YFPNFaERF9-YFPC as well as 307
FaMYB98-YFPNFaMYB98-YFPC also generated signals in the nucleus indicating 308
that FaERF9 and FaMYB98 both could form homodimers or possibly multimers in 309
the nucleus (Figure 10) 310
311
Discussion 312
The AP2ERF superfamily in strawberry 313
The AP2ERF superfamily of plant transcription factors is defined by the AP2ERF 314
domain and comprises the ERF AP2 and RAV families as well as one soloist member 315
(Riechmann et al 2000 Weirauch and Hughes 2011) The completion of multiple 316
plant genome sequences has enabled a genome-scale analysis of the AP2ERF family 317
which in recent years has been systematically studied in diverse fruit species such as 318
tomato grape peach and kiwi fruit (Zhuang et al 2009 Sharma et al 2010 Licausi 319
et al 2010 Yin et al 2010 Pirrello et al 2012 Zhang et al 2012 Zhang et al 320
2016) A few AP2ERF genes have been isolated and characterized in strawberry and 321
CBF orthologs (Owens et al 2002 Koehler et al 2012 Zhang et al 2014) have 322
been identified from different strawberry cultivars in several independent studies 323
Although they have distinct names eg Fragaria times ananassa CBF1 (FaCBF1) 324
FaCBF4 (GenBank HQ9105151) and CBF1 (GenBank EU1172142) according to 325
the phylogenetic tree generated in this study the orthologs of 326
CBF1CBF4CBF2CBF3 in Arabidopsis are similar to each other and to FaERF20 327
(Supplemental Figure S1) (Owens et al 2002 Koehler et al 2012 Zhang et al 328
2014) FaERF20 has 85 sequence similarity with FaCBF1 identified by Owens et 329
al (2002) 93 similarity with FaCBF4 amplified by Koehler et al (2012) and 75 330
similarity with CBF1 cloned by Zhang et al (2014) The AP2ERF genes 331
characterized in other studies (Jia et al 2011 GAO et al 2015 Chai and Shen 2016 332
Mu et al 2016) are also noted in Supplemental Table S1 333
334
Based on the computational analysis we have identified a total of 120 AP2ERF 335
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13
genes in octoploid strawberry (Supplemental Table S1) The number of predicted 336
AP2ERF genes (120) is comparable to those observed in other fruits including 337
tomato (112) Chinese plum (116) citrus (126) and peach (131) but lower than those 338
reported for grape (149) (Xie et al 2016) As shown in Supplemental Table S2 79 339
(95 genes) of the AP2ERF genes belong to the ERF family in strawberry constituting 340
the largest sub-family The members of this sub-family can be classified into 10 341
groups (group I to X) according to their sequence similarities to the Arabidopsis ERF 342
genes (Nakano et al 2006) The AP2 family encompasses the same number of genes 343
in Arabidopsis citrus and strawberry (eighteen) (Nakano et al 2006 Xie et al 2014) 344
and there are six RAV genes in strawberry which are highly conserved in dicots such 345
as Vitis vinifera Arabidopsis thaliana and Populus trichocarpa (Licausi et al 2010) 346
347
Role of FaERF9 in regulating the biosynthesis of HDMF a positive regulator 348
acting in an indirect manner 349
The large-scale screening of the AP2ERF superfamily in strawberry led to 350
identification of 11 ERFs and 1 RAV that trans-activated the FaQR promoter more 351
than two-fold with the highest activation caused by FaERF9 which trans-activated 352
the FaQR promoter (Figure 2) as well as up-regulating FaQR expression and furanone 353
production in transient overexpression assays (Figure 4) which has been extensively 354
used to explore the fruit-associated gene functions in strawberry (Han et al 2015 355
Medina-Puche et al 2015 Vallarino et al 2015 Carvalho et al 2016 Song et al 356
2016 Wang et al 2018) FaERF9 transcripts accumulate in the fruit apical section 357
before the basal section (Figure 3) a finding consistent with the actual changes in 358
furaneol content (Figure 1) and the expression of FaQR (Figure 1) The association 359
between FaERF9 transcripts and accumulation of furanones were also established 360
with different strawberry cultivars The correlation between FaERF9 and FaQR 361
expression as well as furanone content among cultivars supports a positive role of 362
FaERF9 in regulating furanone content (Figure 5) These results indicate that 363
FaERF9 transcript abundance may be a good indicator of the abundance of these 364
important flavour volatiles in fruits of different cultivars This should be considered as 365
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14
a method for high-throughput variety screening to replace direct measurement of 366
volatiles 367
368
FaERF9 is a member of the ERF group II family and is most closely related to the 369
Arabidopsis genes At1g44830 (ATERF014) At1g21910 (DREB26) and At1g77640 370
(Supplemental Figure S1) At1g44830 was observed to be strongly up-regulated in a 371
comprehensive microarray analysis of the root transcriptome following NaCl 372
exposure (Jiang and Deyholos 2006) At1g21910 (DREB26) was functionally 373
characterized as a trans-activator localized in the nucleus exhibiting tissue-specific 374
expression and participating in plant developmental processes as well as biotic andor 375
abiotic stress signalling (Krishnaswamy et al 2011) However none of these genes 376
have been reported as furanone regulators In strawberry another five genes 377
(FaERF6 FaERF7 FaERF8 FaERF10 and FaERF11) also belong to the same 378
group with FaERF8 also showing somewhat weaker activation activity towards the 379
FaQR promoter than FaERF9 The fact that FaERF9 could not bind directly to the 380
promoter of FaQR (Figure 6) indicates that it might function as an indirect regulator 381
of FaQR and furaneol biosynthesis 382
383
A FaERF9 and FaMYB98 complex is involved in regulating FaQR and furaneol 384
biosynthesis 385
The finding that FaERF9 could interact with FaMYB98 protein (Figures 9 and 386
Figure 10) and that FaMYB98 could physically bind to the FaQR promoter (Figure 6 387
and Figure 7) provides evidence for a regulatory mechanism whereby FaERF9 388
regulates FaQR and furaneol production as part of a complex with an MYB 389
transcription factor Since co-overexpression of FaERF9 and FaMYB98 resulted in 390
much higher activation activity towards FaQR we speculate that FaERF9 may 391
recruit FaMYB98 homologs in tobacco to activate the FaQR promoter (Figure 8) 392
FaOMT is another key gene for furanone biosynthesis and a potential target for 393
transcriptional activation However FaERF9 did not significantly activate the 394
FaOMT promoter in a dual-luciferase assay and the transcript level of FaOMT in the 395
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15
FaERF9-overexpressing fruits showed no significant difference from that in the 396
control (Supplemental Figure S6 Supplemental Figure S7) The FaOMT promoter 397
was significantly induced by FaMYB98 but no synergistic effect of FaERF9 and 398
FaMYB98 on the promoter was observed (Supplemental Figure S6) In previous 399
studies of the regulation of plant volatile compounds MYBs have been characterized 400
as being involved mainly in the regulation of the benzenoidphenylpropanoid pathway 401
that produces floral volatiles in petunia and eugenol in ripe strawberry fruit (Verdonk 402
et al 2005 Dal Cin et al 2011 Colquhoun et al 2011 Spitzer-Rimon et al 2012 403
Medina-Puche et al 2015) but their role in formation of volatiles from other 404
pathways has not been reported Our study demonstrates a role for MYB in the 405
synthesis of furaneol a carbohydrate-derived volatile compound and reveals the 406
synergistic interactions between an MYB and ERF in a transcription complex (Figure 407
8 Figure 9 and Figure 10) 408
409
Recent research has provided evidence for interactions between AP2ERF and MYB 410
transcription factors in regulating other aspects of fruit quality including texture 411
(EjAP2-1 and EjMYB Zeng et al 2015) and colour (PyERF3 and PyMYB114 Yao 412
et al 2017) A group VIII ERF has also recently been shown to interact with an MYB 413
to regulate floral scent production in petunia (Liu et al 2017) In strawberry fruit 414
DOF in combination with an MYB has been reported to be involved in the regulation 415
of eugenol production and the identification of this second transcription factor (DOF) 416
suggests that it is a good target in breeding for improved flavour (Molina-Hidalgo et 417
al 2017 Tieman 2017) Considering its important contribution to flavour in 418
strawberry and many other highly valued fruit crop species (pineapple tomato mango 419
etc) very little is known about regulation of furaneol synthesis Here we established 420
the role of FaERF9 in the regulation of HDMF synthesis by direct protein-protein 421
interactions with FaMYB98 to synergistically trans-activate FaQR The functional 422
identification of this complex enhances our knowledge of the regulation of volatile 423
compound synthesis and identifies a new AP2ERF-MYB complex Further 424
examination of the other ERFs that stimulated transcription from the FaQR promoter 425
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16
(Figure 2) may provide additional information about the complexity of this regulation 426
Overall this study provides important clues for understanding the transcriptional 427
regulation of HDMF synthesis and identifies specific transcription factors that are 428
likely to be good targets for molecular breeding for improved flavour 429
430
Conclusions 431
Screening of the AP2ERF superfamily in strawberry (Fragaria times ananassa) 432
identified candidate members capable of activating the FaQR promoter An ERF 433
transcription factor was identified as a positive regulator of HDMF synthesis in 434
strawberry fruit and the mechanism of activation was shown to involve an ERF-MYB 435
transcription complex that regulates transcription of FaQR leading to the biosynthesis 436
of HDMF the characteristic volatile compound which has a major influence on 437
strawberry aroma 438
439
Materials and Methods 440
441
Plant Materials and Growth conditions 442
The strawberry (Fragaria times ananassa cv lsquoYuexinrsquo an octoploid cultivar) fruit used in 443
this study were bred by Zhejiang Academy of Agricultural Sciences (Haining 444
Zhejiang) Fruits at various developmental and ripening stages including G (green) T 445
(turning) IR (intermediate red) and R (full red) were harvested (Figure 1) and 446
transported to the laboratory within 2 h Thirty-six fruits of uniform size and free of 447
visible defects were selected at each stage with twelve fruits in each biological 448
replicate After removing the calyces fruits were then divided into the basal and 449
apical sections which were sampled separately (Figure 1) They were rapidly cut into 450
pieces frozen immediately in liquid nitrogen and stored at -80deg C until use Red ripe 451
fruits of different strawberry cultivars (Fragaria times ananassa octoploid cultivars) 452
including lsquoYuelirsquo lsquoBenihoppersquo lsquoMengxiangrsquo lsquoAmaoursquo lsquo10-1-4rsquo lsquoAkihimersquo lsquoSweet 453
Charliersquo lsquo07-1-4rsquo lsquoDarselectrsquo lsquoYuexinrsquo and lsquoXuemeirsquo were also provided by Zhejiang 454
Academy of Agricultural Sciences For each cultivar the fruits of three biological 455
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17
replicates were sampled frozen in liquid nitrogen and stored at -80deg C for further use 456
457
Tobacco plants (Nicotiana benthamiana) used for dual-luciferase assays and 458
subcellular localization analysis in this study were grown in a growth chamber with a 459
lightdark cycle of 16 h8 h at 24degC 460
461
Detection of DMMF and HDMF 462
Automated HS-SPME-GC-MS was performed to detect both furanones in lsquoYuexinrsquo 463
strawberry fruit (Zorrilla-Fontanesi et al 2012) Samples were ground into a powder 464
under liquid nitrogen for analysis 465
466
For the detection of DMMF (Figure 1) 05 g (fresh weight) of each sample was 467
weighed in the vial to which was added 1 mL of EDTA solution (100 mM pH 75) 1 468
mL of CaCl2 solution (mv = 20) and 20 microL of 2-octanol as the internal standard 469
(007 μgμL) The mixture was homogenized and the vial closed and placed on the 470
sample tray for analysis by CombiPAL autosampler (CTC Analytic CA USA) The 471
fruit volatiles were sampled by headspace solid-phase microextraction with a 65-μm 472
polydimethylsiloxane-divinylbenzene fibre (PDMS-DVB) Initially vials were 473
pre-incubated at 50degC for 10 min under continuous agitation (500 rpm) then volatiles 474
were extracted for 30 min at the same temperature and agitation speed After that the 475
fibre was desorbed in the GC injection port for 5 min in splitless mode The 7890A 476
GC chromatograph was equipped with a DB-5ms column (60 m times 250 μm times 1 μm 477
JampW Scientific Folsom CA USA) with helium as the carrier gas at a constant flow 478
of 12 mLmin The GC was programmed at an initial temperature of 35degC for 2 min 479
with a ramp of 5degC min up to 250degC and held for 5 min The injection port interface 480
and MS source temperatures were 250degC 260degC and 230degC respectively The 481
ionization potential was set at 70 eV recorded by a 5975B mass spectrometer (Agilent 482
Technologies JampW Scientific Folsom CA USA) and the scanning speed was 7 483
scanss The same method was used to analyse HDMF and DMMF in fruits from 484
different cultivars (Supplemental Figure S3) except for the sample preparation 485
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18
procedure (Araguumlez et al 2013) briefly 05 g (fresh weight) of powdered fruit was 486
incubated at 30degC in a water bath for 5 min then 2 mL of NaCl (mv = 20) and 20 487
microL of 2-octanol as the internal standard (007 μgμL) were added and homogenized 488
489
For the detection of HDMF (Figure 1) and both furanones (Figure 4 and Supplemental 490
Table S3) a liquid-injection system equipped with CTC Pal ALS was used One gram 491
(fresh weight) of powdered fruit and 2 mL of NaCl (mv = 20) were homogenized in 492
a 10-mL tube and 300 μL of CH2Cl2 and 20 microL of 2-octanol (0766 μgμL) as the 493
internal standard were added to extract the volatiles the mixture was then 494
homogenized again The tubes were stored at room temperature for 20 min and 495
centrifuged at 12000 rpm for 5 min The subnatant was pipetted into a clean 15-mL 496
tube in which 20 mg of anhydrous sodium sulphate was added the tube was left 497
without shaking for half an hour Then 150 μL of the solution was transferred into a 498
GC vial and placed on the sample tray as described above Each sample (1 μL) was 499
injected using the autosampler and the analysis was accomplished by a 7890A 500
GC-MS system (Agilent Technologies JampW Scientific Folsom CA USA) equipped 501
with a DB-WAX column (30 m times 025 mm times 025 μm JampW) Helium (12 mLmin) 502
was used as a carrier gas The injection port (splitless injection mode) interface and 503
MS source temperatures were as described above The oven temperature was set at 504
60degC for 4 min then increased to 180degC at a rate of 4degCmin and maintained for 30 505
min DMMF was identified by comparison of electron ionization mass spectra and 506
retention time data with the data from the NISTEPANIH mass spectral library 507
(NIST-08 and Flavor) HDMF (Figure 1) was identified and qualified by comparison 508
with injected standard (Sigma) The quantitative analysis of both furanones (Figure 4 509
Supplemental Table S3 and Supplemental Figure S3) was determined using the peak 510
area of the internal standard as a reference based on total ion chromatogram (TIC) 511
512
RNA isolation and Reverse Transcription Quantitative PCR (RT-qPCR) 513
Total RNA from strawberry samples was isolated in this study using the CTAB 514
method (Chang et al 1993) Genomic DNA contamination was eliminated by 515
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
19
TURBO Dnase (Ambion) 1 μg of RNA was used to obtain cDNA using an IScriptTM 516
cDNA Synthesis Kit (Bio-Rad) The synthesized cDNA was diluted with water (120) 517
and 2 μL of diluted cDNA was used as the template for RT-qPCR Reactions were 518
performed in a total volume of 20 μL consisting of 10 μL of SYBR PCR supermix 519
(Bio-Rad) 1 μL of each primer (10 μM) 6 μL of DEPC-H2O and 2 μL of diluted 520
cDNA on CFX96 instrument (Bio-Rad) (Yin et al 2012) The oligonucleotide 521
primers for RT-qPCR analysis of genes including the AP2ERF FaQR and FaOMT 522
were designed according to the coding sequences of genes and the specificity was 523
verified before use (Min et al 2012) NCBIPrimer-BLAST was applied to design the 524
primers Relative expression levels were normalized to that of an internal controlmdashthe 525
interspacer 26S-18S strawberry RNA housekeeping gene FaRIB413 526
(Zorrilla-Fontanesi et al 2012) To investigate the differential expression of genes 527
during fruit development and ripening stages relative expression of each gene at the 528
R stage in the basal fruit section was set as 1 using the 2minus∆∆119862119879 method For transient 529
overexpression assay relative expression of control fruits with an empty vector (SK) 530
was set as 1 The primers used in RT-qPCR are listed in Supplemental Table S4 531
532
Gene isolation and analysis 533
Multiple database searches were performed to identify members of the strawberry 534
(Fragaria times ananassa) AP2ERF superfamily in the published strawberry databases 535
and annotations of Fragaria times ananassa and Fragaria times vesca by using the 536
AP2ERF DNA binding domain as a query sequence and 120 genes were identified 537
with AP2ERF domain(s) Based on the BLAST result primers (listed in 538
Supplemental Table S5) were used to amplify the coding full-length cDNAs of 539
AP2ERF genes The deduced amino acid sequences of AP2ERF proteins in 540
Arabidopsis thaliana used for construction of a phylogenetic tree were obtained from 541
the Arabidopsis Information Resource (TAIR) Alignment of the proteins was 542
performed using the neighbour-joining method in ClustalX (v181) and the 543
phylogenetic tree was constructed using FigTree (v131) 544
545
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
20
FaMYB98 was obtained by yeast one-hybrid screening sequencing and the full-length 546
sequences were predicted by BLAST Primers were designed (listed in Supplemental 547
Table S5) to amplify the full-length coding sequence 548
549
The promoter of FaQR was cloned by Genome Walking as previously described (Yin 550
et al 2010) and conserved cis-element motifs in the promoter were manually 551
searched 552
553
Conserved domains within the FaAP2ERF proteins and FaMYB98 were analysed by 554
CD-search (httpswwwncbinlmnihgovStructurecddwrpsbcgi) and cellular 555
locations of proteins including FaERF9 and FaMYB98 were predicted with the 556
WoLF PSORT program (httpswwwgenscriptcomwolf-psorthtml) 557
558
Dual-Luciferase Assays 559
In accordance with a previous protocol (Yin et al 2010) the full-length cDNAs of 560
FaAP2ERF or FaMYB98 transcription factors were cloned into pGreen II 0029 561
62-SK vector and the promoter of FaQR was cloned into pGreen II 0800-LUC vector 562
A luciferase gene from Renillia (REN) driven by a 35S promoter in the LUC vector 563
acted as a positive control The above constructs were transiently expressed in 564
Nicotiana benthamiana leaves by Agrobacterium-mediated infiltration (strain 565
GV3101) and the activity of the TFs on the promoter was measured on the third day 566
after infiltration indicated by the ratio of enzyme activities of firefly luciferase (LUC) 567
and renilla luciferase (REN) using a Modulus Luminometer (Promega Madison WI 568
USA) To determine the activity of a specific transcription factor towards the 569
promoter we mixed the Agrobacterium culture with 1 mL of TF and 100 μL of 570
promoter and the LUCREN value of the empty vector SK on the promoter was set as 571
1 as a calibrator To test the combined effect of two transcription factors on the 572
promoter to the Agrobacterium culture mixture we added 05 mL of each TF and 100 573
μL of promoter the effect of the mixtures that contained each transcription factor (05 574
mL) and empty vector SK (05 mL) was also tested on the promoter as a control 575
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
21
576
Subcellular localization analysis 577
35S-FaERF9-GFP and 35S-FaMYB98-GFP were transiently expressed in tobacco (N 578
benthamiana) leaves by Agrobacterium infiltration (EHA105) using the same method 579
as described in the dual-luciferase assay above The transiently infected leaves were 580
imaged on the third day after infiltration using a Nikon A1-SHS confocal laser 581
scanning microscope The excitation wavelength for GFP fluorescence was 488 nm 582
and fluorescence was detected at 490ndash520 nm The primers used for GFP construction 583
are listed in Supplemental Table S6 584
585
Transient overexpression in strawberry fruit 586
Transient overexpression of FaERF9 and an overexpression binary vector (pGreen II 587
0029 62-SK-FaERF9-FaMYB98) were performed in strawberry fruit using the 588
FaERF9-SK construct described above for the dual-luciferase assays and the binary 589
vector constructed according to Liu et al 2013 The transfection of fruit was carried 590
out at the G stage (Hoffmann et al 2006) The FaERF9-SK construct and binary 591
vector were individually electroporated into Agrobacterium tumefaciens GV3101 and 592
the Agrobacterium culture suspended in infiltration buffer was infiltrated into the 593
whole fruit using a syringe As a control treatment fruits were infiltrated with 594
Agrobacterium carrying an empty vector SK under the same transfection conditions 595
Fruits were left attached to the plants and harvested on the seventh day after 596
infiltration Fruits of three biological replicates were sampled for further analysis 597
598
Yeast one-hybrid assay 599
In order to identify proteins that bind to the FaQR promoter the Matchmaker Gold 600
Yeast One-hybrid Library Screening System (Clontech USA) was used The sequence 601
of the FaQR promoter was cloned into the pAbAi vector and the construct was 602
integrated into the genome of the Y1HGold yeast strain A mixture of total RNA from 603
strawberry fruit at four stages (G T IR R) was used to construct the prey cDNA 604
library (TaKaRa) The background AbAr expression of Y1HGold FaQR-pAbAi strain 605
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
22
was tested according to the system user manual and then screening for protein-DNA 606
interactions was carried out Furthermore the full length of each transcription factor 607
was separately cloned into pGADT7 AD vector to confirm the screening results The 608
relationship between FaERF9 and FaQR promoter was also examined individually 609
Primers used in this assay are listed in Supplemental Table S6 610
611
Expression and purification of FaMYB98 recombinant protein 612
A 405-bp region spanning the DNA-binding domain of FaMYB98 was amplified 613
from FaMYB98 cDNA and cloned into a pET6timesHN vector (Clontech Palo CA USA) 614
to generate the recombinant N-terminal His-tagged protein the primers used are listed 615
in Supplemental Table S6 The resulting construct was sequenced and introduced into 616
Escherichia coli strain Rosetta 2(DE3)pLysS (Novagen) Ten millilitres of the 617
overnight culture was combined with 500 mL of an LB liquid medium (100 μgmL 618
ampicillin and 34 μgmL chloramphenicol) as described (Li et al 2017) Isopropyl 619
β-D-1-thiogalactopyranoside (IPTG) was added to a final concentration of 1 mM and 620
the bacterial culture was incubated at 18degC at 150 rpm for 18 h Then the cells were 621
harvested using a centrifuge and resuspended in 1times PBS buffer (Sangon Biotech) 622
after which they were disrupted by sonication and the supernatant was purified using 623
a HisTALONTM Gravity Column (Clontech) according to the user manual The PD-10 624
Desalting column (GE Healthcare) was then used for buffer change and sample 625
clean-up of proteins according to the gravity protocol SDS-PAGE was performed and 626
the protein was visualized using Coomassie brilliant blue 627
628
Electrophoretic mobility shift assay (EMSA) 629
A Lightshift Chemiluminescent EMSA kit (Thermo) was used to perform EMSA 630
experiments according to the manufacturerrsquos instructions Single-strand 631
oligonucleotides were synthesized and biotinylated by GeneBio Biotech (Hangzhou 632
China) The details of the EMSA assay are provided in Ge et al (2017) The probes 633
used for EMSAs are listed in Supplemental Table S6 634
635
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
23
636
Yeast two-hybrid assay 637
The DUALhunter system (Dualsystems Biotech Switzerland) was used to investigate 638
the interaction between FaERF9 and FaMYB98 Full-length coding sequences of 639
FaERF9 and FaMYB98 were respectively cloned into pDHB1 bait vector and 640
pPR3-N prey vector sequences were verified and the bait plasmid was 641
co-transformed with prey plasmid into NMY51 in the combinations below 642
FaMYB98-pDHB1pPR3-N FaMYB98-pDHB1FaERF9-pPR3-N 643
FaMYB98-pDHB1pOst1-NubI FaERF9-pDHB1pPR3-N 644
FaERF9-pDHB1FaMYB98-pPR3-N and FaERF9-pDHB1pOst1-NubI (Li et al 645
2017) Transformed cells were spread onto the following plates DDO (SD 646
medium-Trp-Leu) QDO (SD medium-Trp-Leu-His-Ade) and QDO+3-AT (QDO 647
medium supplemented with 1 mM 3-amino-124-triazole) The control plasmid 648
pOst1-NubI was used to determine whether the bait was functional the pPR3-N prey 649
vector plasmid was used to test whether the bait displayed non-specific background 650
and positive interactions were indicated by the growth of yeast on QDO and 651
QDO+3-AT plates The Primers used in the DUALhunter assay are listed in 652
Supplemental Table S6 653
654
Bimolecular fluorescence complementation (BiFC) assays 655
Full-length FaERF9 and FaMYB98 respectively were cloned into sequences 656
encoding the N- and C- fragments of YFP protein (Lv et al 2014) All constructs 657
were transiently expressed in tobacco (N benthamiana) leaves by Agrobacterium 658
infiltration (EHA105) The YFP fluorescence of transfected leaves was imaged 40 h 659
after infiltration by using a Nikon A1-SHS confocal laser scanning microscope The 660
excitation wavelength for YFP was 488 nm and fluorescence was detected at 520ndash661
540 nm Primers used are listed in Supplemental Table S6 662
663
Statistics 664
A Studentrsquos two-tailed t test ( plt005 plt001 and plt0001) was used to 665
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
24
determine significant differences between two groups in this study Microsoft Excel 666
was used to perform linear regressive analysis significant differences were 667
determined by SPSS Statistics 200 and scatter plots were prepared with Origin80 668
Least significant difference (LSD) at the 5 level was calculated using Microsoft 669
Excel Figures were prepared with Origin80 (Microcal Software Inc Northampton 670
MA USA) The online tool MetaboAnalyst 36 (httpwwwmetaboanalystca) was 671
used to analyse the transcript abundance of the AP2ERF genes 672
673
Accession numbers 674
Sequence data from this article have been deposited in GenBank under the accession 675
numbers MH332903-MH333022 for AP2ERF genes in Fragaria times ananassa and 676
MH333023 for FaMYB98 GenBank numbers for FaQR and FaOMT were 677
AY1588361 (Raab et al 2006) and AF2204912 (Wein et al 2002) 678
679
Supplemental Material 680
Supplemental Figure S1 Phylogenetic analysis of FaAP2ERF and Arabidopsis 681
AP2ERF proteins 682
Supplemental Figure S2 Analysis of FaAP2ERF gene expression patterns in 683
strawberry fruit during development and ripening 684
Supplemental Figure S3 Contents of furanones in fruit of strawberry cultivars 685
Supplemental Figure S4 Relative expression of FaERF9 in FaERF9-FaMYB98- 686
and FaERF9-overexpressing fruits 687
Supplemental Figure S5 Subcellular localization of FaMYB98 688
Supplemental Figure S6 The combined activation effects of FaERF9FaMYB98 on 689
the FaOMT promoter 690
Supplemental Figure S7 Relative expression of FaOMT in 691
FaERF9-overexpressing fruits 692
Supplemental Table S1 AP2ERF superfamily genes in Fragaria times ananassa 693
Supplemental Table S2 Classification of the AP2ERF superfamily members in 694
Fragaria times ananassa 695
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
25
Supplemental Table S3 Furanone content in FaERF9-FaMYB98- and 696
FaERF9-overexpressing fruits 697
Supplemental Table S4 Primers used for reverse transcription quantitative PCR 698
(RT-qPCR) 699
Supplemental Table S5 Primers used to amplify the full-length coding sequences of 700
AP2ERF genes and FaMYB98 in strawberry (Fragaria times ananassa) 701
Supplemental Table S6 Primers used for vector construction 702
703
Acknowledgments 704
This research was supported by the National Key Research and Development 705
Program (2016YFD0400101) the Project of the Science and Technology Department 706
of Zhejiang Province (2016C04001) and the 111 Project (B17039) 707
708
Figure legends 709
Figure 1 Changes in furanone content and furanone biosynthetic genes during 710
strawberry (Fragaria times ananassa Duch cv Yuexin) fruit development and ripening 711
A Fruits were collected at four ripening stages G (green stage) T (turning stage) IR 712
(intermediate red stage) R (full red stage) B Changes in the contents of furaneol 713
(HDMF) and mesifurane (DMMF) HDMF content was calculated using a standard 714
curve of HDMF while DMMF content was calculated with an internal standard as the 715
reference C Expression levels of FaQR and FaOMT The expression levels of each 716
gene were calculated relative to corresponding values in the basal section at the R 717
stage SEs were calculated from three replicates and LSD values represent the least 718
significant differences at p = 005 719
Figure 2 Regulatory effects of FaAP2ERF on the promoter of FaQR LUCREN 720
values of the empty vector on FaQR promoter were used as the calibrator set as 1 721
and SEs were calculated from five replicates statistical significance was determined 722
by Studentrsquos two-tailed t test ( plt0001) 723
Figure 3 Expression and the subcellular localization of FaERF9 A The expression 724
levels were calculated relative to the levels in the basal section at the R stage B 725
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
26
Subcellular localization analysis was performed in tobacco leaves The tobacco used 726
in the assay was stably transformed with a specific nucleus localized red fluorescence 727
protein construct and the red fluorescence indicates the nucleus-localized signal 728
(NLS) Scale bar = 25 microm SEs were calculated from three replicates 729
Figure 4 Transient overexpression of FaERF9 in strawberry fruit A Relative 730
expression of FaQR and FaERF9 in FaERF9-OX fruit 7 days after infiltration The 731
expression was calculated relative to the average value in control (SK) fruits B 732
HDMF and DMMF content in FaERF9-OX fruit The content of both furanones 733
were quantified using the peak area of the internal standard (2-octanol) as the 734
reference SEs were calculated from three replicates Statistical significance was 735
determined by Studentrsquos two-tailed t test ( plt005 plt001 plt0001) 736
Figure 5 Scatter plots of 11 strawberry cultivars A Linear regression analysis 737
between FaERF9 expression and FaQR expression B Linear regression analysis 738
between FaERF9 expression and furanone content The relative expression was 739
normalized to that of the housekeeping gene FaRIB413 and furanone content was 740
calculated with internal standard as the reference Significant differences were 741
determined by SPSS Statistics 200 742
Figure 6 Interactions of FaERF9 and FaMYB98 with the FaQR promoter A Yeast 743
one-hybrid analysis of the interaction of FaERF9 and FaQR promoter B Yeast 744
one-hybrid analysis of the interaction of FaMYB98 and FaQR promoter C 745
Regulatory effect of FaMYB98 on the FaQR promoter Auto-activation was tested on 746
SD-Ura (synthetically defined medium without uracil) in presence of Aureobasidin A 747
(AbA) and physical interaction was determined on SD-Leu (synthetically defined 748
medium without leucine) in presence of AbA LUCREN values of the empty vector 749
on FaQR promoter were used as the calibrator set as 1 and error bars were calculated 750
from five replicates Statistical significance was determined by Studentrsquos two-tailed t 751
test ( plt005 plt001 plt0001) 752
Figure 7 Electrophoretic mobility shift assay of FaMYB98 binding to FaQR 753
promoter A The probe sequence used for EMSA and mutated nucleotides are 754
indicated with lowercase letters B Purified DNA-binding domain of FaMYB98 755
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
27
protein and biotin-labelled DNA probe were mixed and analysed on 6 native 756
polyacrylamide gels and then photographed Presence or absence of specific probes is 757
marked by the symbol + or - 758
Figure 8 The combined activation effects of FaERF9FaMYB98 on the FaQR 759
promoter LUCREN values obtained with the empty vector and FaQR promoter were 760
used as the calibrator set as 1 and error bars were calculated from five replicates 761
Figure 9 Yeast two-hybrid analysis of the protein-protein interactions between 762
FaMYB98 and FaERF9 Positive interactions were determined by the growth of 763
yeast cells on selection plates Bait with pOST acted as positive controls and bait with 764
pPR3 as negative controls DDO synthetically defined medium without tryptophan 765
and leucine QDO synthetically defined medium without tryptophan leucine 766
histidine and adenine QDO+3AT QDO medium supplemented with 1 mM 767
3-aminotriazole 768
Figure 10 BiFC analysis of the protein-protein interactions between FaMYB98 and 769
FaERF9 The pairs of fusion proteins tested were FaMYB98-YFPN+FaERF9-YFPC 770
FaERF9-YFPN+FaMYB98-YFPC FaMYB98-YFPN+FaMYB98-YFPC and 771
FaERF9-YFPN+FaERF9-YFPC The other combinations were negative controls 772
The tobacco used in the assay was stably transformed with a specific 773
nucleus-localized red fluorescence protein construct and the red fluorescence 774
indicated the nucleus-localized signal (NLS) Fluorescence of the yellow fluorescence 775
protein (YFP) visualized the interaction in vivo Scale bar = 25 microm 776
777
Literature Cited 778
779
Agarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression 780
of PgDREB2A transcription factor enhances abiotic stress tolerance and activates 781
downstream stress-responsive genes Mol Biol Rep 37 1125-1135 782
Araguumlez I Osorio S Hoffmann T Rambla JL Medina-Escobar N Granell A 783
Botella MAacute Schwab W Valpuesta V (2013) Eugenol production in achenes and 784
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28
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Plant Physiol 163 946-958 786
Carvalho RF Carvalho SD OrsquoGrady K Folta KM (2016) Agroinfiltration of 787
strawberry fruit mdash a powerful transient expression system for gene validation Curr 788
Plant Biol 6 19-37 789
Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic 790
(Amsterdam) 210 34-40 791
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating 792
RNA from pine trees Plant Mol Biol Rep 11 113-116 793
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC 794
Clark DG (2011) PhMYB4 fine-tunes the floral volatile signature of 795
Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143 796
Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz 797
EA Taylor MG Smits-Kroon MT Schuurink RC Haring MA Giovannoni J 798
Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic 799
pathway by ectopic expression of a MYB transcription factor in tomato fruit Plant 800
Cell 23 2738-2753 801
Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan 802
XW Yang ZY (2017) Differential responses of four biosynthetic pathways of 803
aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under 804
interaction of light and temperature Food Chem 221 356-364 805
Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of 806
differentially-expressed genes during somatic embryogenesis in Fragaria times 807
ananassa Duch lsquoBenihopprsquo J Hortic Sci Biotechnol 90 671-681 808
Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 809
transcriptionally regulates chilling-induced lignification of loquat fruit via physical 810
interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136 811
Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM 812
(2004) Functional interactions between a glutamine synthetase promoter and MYB 813
proteins Plant J 39 513-526 814
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29
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) 815
Sucrose nonfermenting1-related protein kinase26 an ortholog of open stomata1 is 816
a negative regulator of strawberry fruit development and ripening Plant Physiol 817
167 915-930 818
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene 819
expression in strawberry fruit (Fragaria times ananassa) by agroinfiltration a rapid 820
assay for gene function analysis Plant J 48 818-826 821
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of 822
selected aroma-active compounds in strawberries by headspace solid-phase 823
microextraction gas chromatography and correlation with sensory descriptive 824
analysis J Food Sci 72 S487-S496 825
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid 826
plays an important role in the regulation of strawberry fruit ripening Plant Physiol 827
157 188-199 828
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of 829
NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes BMC 830
Plant Biol 6 20 831
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN 832
(2005) MYB98 is required for pollen tube guidance and synergid cell differentiation 833
in Arabidopsis Plant Cell 17 2981-2992 834
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional 835
characterization of enone oxidoreductases from strawberry and tomato fruit J 836
Agric Food Chem 55 6705-6711 837
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You 838
J-S Rohloff J Randall SK Alsheikh M (2012) Proteomic study of 839
low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ 840
in cold tolerance Plant Physiol 159 1787-1805 841
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional 842
characterization of four APETALA2-family genes (RAP26 RAP26L DREB19 843
and DREB26) in Arabidopsis Plant Mol Biol 75 107-127 844
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
30
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon 845
J Gupta V (2013) An oxidoreductase from lsquoAlphonsorsquo mango catalyzing 846
biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494 847
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in 848
strawberries Z Lebensm-Unters Forsch 195 120-123 849
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X 850
(2015) Label-free quantitative proteomics to investigate strawberry fruit proteome 851
changes under controlled atmosphere and low temperature storage J Proteomics 852
120 44-57 853
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 854
cooperates with CitWRKY1 to participate in citric acid degradation via 855
up-regulation of CitAco3 J Exp Bot 68 3419-3426 856
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription 857
factor CitERF71 activates the terpene synthase gene CitTPS16 involved in the 858
synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938 859
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and 860
transcriptomic analysis of the AP2ERF superfamily in Vitis vinifera BMC 861
Genomics 11 719 862
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive 863
Factor (AP2ERF) transcription factors mediators of stress responses and 864
developmental programs New Phytol 199 639-649 865
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 866
interacting with EOBI negatively regulates fragrance biosynthesis in petunia 867
flowers New Phytol 215 1490-1502 868
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu 869
CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 in regulating 870
anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) 871
during anthocyanin biosynthesis Plant Cell Tissue Organ Cult 115 285-298 872
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
31
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao 873
CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphate signaling and 874
homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597 875
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC 876
Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL 877
Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor 878
regulates eugenol production in ripe strawberry fruit receptacles Plant Physiol 168 879
598-614 880
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics 881
and volatile constituents of strawberry (cv Cigaline) during maturation J Agric 882
Food Chem 52 1248-1254 883
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS 884
(2012) Ethylene-responsive transcription factors interact with promoters of ADH 885
and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 886
63 6393-6405 887
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM 888
Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-Franco A 889
Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific 890
transcription factor FaDOF2 regulates the production of eugenol in ripe fruit 891
receptacles J Exp Bot 68 4529-4543 892
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) 893
Comparison and verification of the genes involved in ethylene biosynthesis and 894
signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44 895
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the 896
ERF gene family in Arabidopsis and rice Plant Physiol 140 411-432 897
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in 898
sour cherry and strawberry and the heterologous expression of CBF1 in strawberry 899
J Am Soc Hortic Sci 127 489-494 900
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech 901
JC Ohme-Takagi M Regad F Bouzayen M (2012) Functional analysis and 902
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
32
binding affinity of tomato ethylene response factors provide insight on the 903
molecular bases of plant differential responses to ethylene BMC Plant Biol 12 190 904
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) 905
Methylpentoses are possible precursors of furanones in fruits Prikl Biokhim 906
Mikrobiol 28 123-127 907
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery 908
of synergid-expressed genes encoding filiform apparatus localized proteins Plant 909
Cell 19 2557-2568 910
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria 911
vesca L compared to those of cultivated berries Fragariatimes ananassa cv Senga 912
Sengana J Agric Food Chem 27 19-22 913
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W 914
Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of the strawberry 915
flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone 916
oxidoreductase Plant Cell 18 1023-1037 917
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L 918
Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim M Broun P Zhang 919
JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription 920
factors genome-wide comparative analysis among eukaryotes Science 290 921
2105-2110 922
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the 923
formation of 25-dimethyl-4-hydroxy-3(2H)-furanone in detached ripening 924
strawberry fruits J Agric Food Chem 46 1488-1493 925
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 926
25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in 927
strawberry fruits Phytochemistry 43 155-159 928
Schwab W (1998) Application of stable isotope ratio analysis explaining the 929
bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone in plants by a biological 930
maillard reaction J Agric Food Chem 46 2266ndash2269 931
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
33
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) 932
Molecules 18 6936-6951 933
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard 934
products Recent Res Dev Phytochem 1 643-673 935
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL 936
Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJ Sims CA 937
Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical 938
compositions a seasonal influence and effects on sensory perception PLoS One 9 939
e88446 940
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) 941
Identification phylogeny and transcript profiling of ERF family genes during 942
development and abiotic stress treatments in tomato Mol Genet Genomics 284 943
455-475 944
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) 945
CitAP210 activation of the terpene synthase CsTPS1 is associated with the 946
synthesis of (+)-valencene in lsquoNewhallrsquo orange J Exp Bot 67 4105-4115 947
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes 948
Dev Genes Evol 214 105-114 949
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K 950
Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the 951
key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151 952
Spitzer-Rimon B Farhi M Albo B Cnarsquoani A Ben Zvi MM Masci T Edelbaum 953
O Yu YX Shklarman E Ovadis M Vainstein A (2012) The R2R3-MYB-like 954
regulatory factor EOBI acting downstream of EOBII regulates scent production 955
by activating ODO1 and structural scent-related genes in petunia Plant Cell 24 956
5089-5105 957
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp 958
Bot 68 4407-4409 959
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla 960
JF Amaya I Giavalisco P Fernie AR Botella MA Valpuesta V (2015) Central 961
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
34
role of FaGAMYB in the transition of the strawberry receptacle from development 962
to ripening New Phytol 208 482-496 963
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 964
regulates fragrance biosynthesis in petunia flowers Plant Cell 17 1612-1624 965
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS 966
(2018) The potassium channel FaTPK1 plays a critical role in fruit quality 967
formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748 968
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) 969
Isolation cloning and expression of a multifunctional O-methyltransferase capable 970
of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma 971
compounds in strawberry fruits Plant J 31 755-765 972
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor 973
types their evolutionary origin and species distribution In A handbook of 974
transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular 975
Biochemistry 52 25-73 976
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of 977
odor (Buettner A Ed) Springer Cham 9-10 978
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS 979
(2014) Isolation classification and transcription profiles of the AP2ERF 980
transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271 981
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in 982
regulation of fruit quality Crit Rev Plant Sci 35 120-130 983
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ 984
Zhang SL Wu J (2017) Map-based cloning of the pear gene MYB114 identifies an 985
interaction with other transcription factors to coordinately regulate fruit 986
anthocyanin biosynthesis Plant J 92 437-451 987
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes 988
involved in regulating fruit ripening Plant Physiol 153 1280-1292 989
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
35
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) 990
Expression of ethylene response genes during persimmon fruit astringency removal 991
Planta 235 895-906 992
Zabetakis I Gramshaw JW Robinson DS (1999) 993
25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis and 994
biosynthesis-a review Food Chem 65 139-151 995
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci 996
Food Agric 74 421-434 997
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 998
an AP2ERF gene is a novel regulator of fruit lignification induced by chilling 999
injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1000
1325-1334 1001
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation 1002
classification and transcription profiles of the Ethylene Response Factors (ERFs) in 1003
ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215 1004
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML 1005
(2012) Genome-wide analysis of the AP2ERF superfamily in peach (Prunus 1006
persica) Genet Mol Res 11 4788-4809 1007
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and 1008
expression analysis of a CRTDRE-binding factor gene FaCBF1 from Fragaria times 1009
ananassa Acta Hortic 41 240-248 1010
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The 1011
Arabidopsis AP2ERF transcription factor RAP26 participates in ABA salt and 1012
osmotic stress responses Gene 457 1-12 1013
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B 1014
Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) Genome-wide 1015
analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic 1016
(Amsterdam) 123 73-81 1017
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF 1018
Valpuesta V Botella MA Granell A Amaya I (2012) Genetic analysis of 1019
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
36
strawberry fruit aroma and identification of O-methyltransferase FaOMT as the 1020
locus controlling natural variation in mesifurane content Plant Physiol 159 1021
851-870 1022
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Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes Dev Genes Evol 214 105-114Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Spitzer-Rimon B Farhi M Albo B Cnaani A Ben Zvi MM Masci T Edelbaum O Yu YX Shklarman E Ovadis M Vainstein A (2012) TheR2R3-MYB-like regulatory factor EOBI acting downstream of EOBII regulates scent production by activating ODO1 and structuralscent-related genes in petunia Plant Cell 24 5089-5105
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp Bot 68 4407-4409Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla JF Amaya I Giavalisco P Fernie AR Botella MAValpuesta V (2015) Central role of FaGAMYB in the transition of the strawberry receptacle from development to ripening New Phytol208 482-496
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Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 regulates fragrance biosynthesis in petunia flowers PlantCell 17 1612-1624
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Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS (2018) The potassium channel FaTPK1 plays a critical role infruit quality formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748
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Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) Isolation cloning and expression of a multifunctional O- wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma compounds in strawberry fruitsPlant J 31 755-765
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Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in regulation of fruit quality Crit Rev Plant Sci 35 120-130
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Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ Zhang SL Wu J (2017) Map-based cloning of the pear geneMYB114 identifies an interaction with other transcription factors to coordinately regulate fruit anthocyanin biosynthesis Plant J 92437-451
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Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes involved in regulating fruit ripening Plant Physiol 1531280-1292
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) Expression of ethylene response genes during persimmonfruit astringency removal Planta 235 895-906
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zabetakis I Gramshaw JW Robinson DS (1999) 25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis andbiosynthesis-a review Food Chem 65 139-151
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Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci Food Agric 74 421-434Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 an AP2ERF gene is a novel regulator of fruit lignificationinduced by chilling injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1325-1334
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Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation classification and transcription profiles of the Ethylene ResponseFactors (ERFs) in ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML (2012) Genome-wide analysis of the AP2ERF superfamily inpeach (Prunus persica) Genet Mol Res 11 4788-4809
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and expression analysis of a CRTDRE-binding factor gene FaCBF1from Fragaria times ananassa Acta Hortic 41 240-248
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The Arabidopsis AP2ERF transcription factor RAP26 participatesin ABA salt and osmotic stress responses Gene 457 1-12
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Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Genome-wide analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic (Amsterdam) 123 73-81Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF Valpuesta V Botella MA Granell A Amaya I (2012) Geneticanalysis of strawberry fruit aroma and identification of O-methyltransferase FaOMT as the locus controlling natural variation inmesifurane content Plant Physiol 159 851-870
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
9
FaERF37FaERF38 (group V) FaERF62FaERF64 (group VIII) FaERF68 216
(group IX) and FaRAV4 (Figure 2) Of these FaERF9 exhibited the highest 217
activation effect on the FaQR promoter (466-fold) (Figure 2) The strawberry 218
FaERF9 cDNA is 699 bp long and ExPASy Compute pIMw tool analysis indicated 219
that this gene encodes a 232-amino acid protein with a calculated molecular mass of 220
254 KD and a pI of 56 221
222
FaERF9 expression pattern and subcellular localization 223
To further explore the connections between AP2ERFs and furaneol biosynthesis we 224
obtained the transcript profiles of the AP2ERF genes in strawberry fruit samples at 225
different fruit developmental and ripening stages by reverse transcription quantitative 226
PCR (RT-qPCR) excluding genes with very low abundance in the fruit samples The 227
results presented as a heatmap (Supplemental Figure S2) demonstrate that these 228
genes displayed various expression patterns in both the apical and basal sections and 229
by analysing the expression patterns of the members indicated as activators in the 230
dual-luciferase assay we found that only a few genes including FaERF8 FaERF9 231
FaERF27 FaERF32 and FaERF37 were up-regulated during ripening stages and 232
their expression correlated with furaneol accumulation in the fruit (Figure 1) 233
Furthermore the expression patterns of the up-regulated genes in the apical and basal 234
sections showed that one ERF gene FaERF9 not only showed an up-regulation 235
pattern in both sections but its expression in the apical section occurred ahead of that 236
in the basal section (Figure 3) consistent with the actual changes in furaneol content 237
(Figure 1) and the expression pattern of FaQR (Figure 1) The subcellular localization 238
of FaERF9 was predicted to be in the nucleus using the WoLF PSORT program In 239
experimental tests 35S-FaERF9-GFP (green fluorescence protein) showed strong 240
fluorescence in the nucleus and the green signal merged with the red fluorescence 241
signal of mCherry-nucleus-marker in tobacco plants (Figure 3) 242
243
Transient overexpression of FaERF9 in strawberry 244
The expression of FaERF9 in agro-infiltrated fruits was analysed by performing 245
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10
RT-qPCR on the seventh day after infiltration by which time they had reached the IR 246
or R stage and the result showed that the transcript levels were significantly higher 247
(52-fold) than in control fruits (Figure 4) The expression of FaQR was examined in 248
the same fruits and the transcript abundance also increased 22-fold The relative 249
content of HDMF in the FaERF9-overexpressing fruits was 008 μg per gram fruit 250
and undetectable in the control fruits (Figure 4) The relative content of DMMF in the 251
overexpressing fruits was also significantly increased to 038 μg per gram fruit 252
compared to 004 μg per gram fruit in the control (Figure 4) These observations 253
provide direct evidence for a regulatory role for FaERF9 in promoting FaQR 254
biosynthesis and activity in ripening strawberry fruit Taken together these results 255
indicate that by activating the transcription of FaQR FaERF9 functions as a positive 256
regulator in furaneol biosynthesis 257
258
Correlation of FaERF9 expression and FaQR transcript profiles 259
GC-MS quantification showed that furanones are distributed in variable levels among 260
different strawberry cultivars (Supplemental Figure S3) The transcript profiles of 261
FaQR and FaERF9 in fruits of different cultivars were measured and linear 262
regression analysis was performed In the cultivars the changes in FaQR transcripts 263
correlated positively with those in FaERF9 transcripts (r = 079 plt001) (Figure 5) 264
In addition FaERF9 transcript levels also correlated with furanone content across 265
cultivars (Figure 5) 266
267
FaERF9 is an indirect regulator of the FaQR promoter and acts via 268
protein-protein interaction with FaMYB98 269
Although the results of the dual-luciferase assay expression analysis transient 270
overexpression and correlation analysis were all consistent with the suggestion that 271
FaERF9 regulates transcript abundance by acting on the FaQR promoter a yeast 272
one-hybrid assay indicated that FaERF9 cannot bind directly to the FaQR promoter 273
(Figure 6) This led us to speculate that activation may occur via a transcription 274
complex involving an additional as-yet unknown regulator which can bind directly to 275
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11
the FaQR promoter 276
277
In parallel with the investigation of the FaAP2ERF genes a cDNA library screening 278
was performed with a yeast one-hybrid assay using the promoter of FaQR as the bait 279
This screen identified several transcription factors that could physically bind to the 280
FaQR promoter but only one MYB could activate transcription from the FaQR 281
promoter (approximately 56-fold) relative to the control (Figure 6) in the 282
dual-luciferase assay This MYB showed 44 amino acid identity with MYB98 283
(GenBank ABA420611) a transcriptional regulator in the synergid cells in 284
Arabidopsis (Kasahara et al 2005) and it was designated as FaMYB98 The 285
specificity of FaMYB98 binding to the FaQR promoter was confirmed by EMSA 286
assay (Figure 7) and increasing the concentration of the cold probe reduced binding 287
In addition mutating the putative binding sites (Goacutemez-Maldonado et al 2004 288
Punwani et al 2007) as shown in Figure 7 eliminated FaMYB98 protein binding 289
When the combined effect of FaERF9 and FaMYB98 was analysed (Figure 8) a 290
synergistic 14-fold activation of the FaQR promoter was observed compared with the 291
activation by either FaERF9 or FaMYB98 which alone promoted transactivation 292
39-fold and 45-fold respectively In addition overexpression of both genes 293
(FaERF9-FaMYB98-SK) in strawberry fruits resulted in higher expression of 294
FaERF9 transcripts and higher furanone content than overexpression of FaERF9 295
(Supplemental Figure S4 Supplemental Table S3) Subcellular localization analysis 296
revealed that FaMYB98 was also localized in the nucleus (Supplemental Figure S5) 297
298
To investigate the potential interactions between FaERF9 and FaMYB98 the 299
DUALhunter system was used (Figure 9) Cells expressing the FaMYB98 and 300
FaERF9 protein pair using either FaMYB98 or FaERF9 as the bait grew on DDO 301
QDO and QDO supplemented with 1 mM 3-AT selective medium indicating 302
interaction between the two proteins This putative protein-protein interaction was 303
confirmed by BiFC assay and the combinations of FaMYB98-YFPNFaERF9-YFPC 304
and FaERF9-YFPNFaMYB98-YFPC exhibited strong coincident signals in the 305
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12
nucleus while negative controls produced no detectable fluorescence signal (Figure 306
10) In addition coexpression of FaERF9-YFPNFaERF9-YFPC as well as 307
FaMYB98-YFPNFaMYB98-YFPC also generated signals in the nucleus indicating 308
that FaERF9 and FaMYB98 both could form homodimers or possibly multimers in 309
the nucleus (Figure 10) 310
311
Discussion 312
The AP2ERF superfamily in strawberry 313
The AP2ERF superfamily of plant transcription factors is defined by the AP2ERF 314
domain and comprises the ERF AP2 and RAV families as well as one soloist member 315
(Riechmann et al 2000 Weirauch and Hughes 2011) The completion of multiple 316
plant genome sequences has enabled a genome-scale analysis of the AP2ERF family 317
which in recent years has been systematically studied in diverse fruit species such as 318
tomato grape peach and kiwi fruit (Zhuang et al 2009 Sharma et al 2010 Licausi 319
et al 2010 Yin et al 2010 Pirrello et al 2012 Zhang et al 2012 Zhang et al 320
2016) A few AP2ERF genes have been isolated and characterized in strawberry and 321
CBF orthologs (Owens et al 2002 Koehler et al 2012 Zhang et al 2014) have 322
been identified from different strawberry cultivars in several independent studies 323
Although they have distinct names eg Fragaria times ananassa CBF1 (FaCBF1) 324
FaCBF4 (GenBank HQ9105151) and CBF1 (GenBank EU1172142) according to 325
the phylogenetic tree generated in this study the orthologs of 326
CBF1CBF4CBF2CBF3 in Arabidopsis are similar to each other and to FaERF20 327
(Supplemental Figure S1) (Owens et al 2002 Koehler et al 2012 Zhang et al 328
2014) FaERF20 has 85 sequence similarity with FaCBF1 identified by Owens et 329
al (2002) 93 similarity with FaCBF4 amplified by Koehler et al (2012) and 75 330
similarity with CBF1 cloned by Zhang et al (2014) The AP2ERF genes 331
characterized in other studies (Jia et al 2011 GAO et al 2015 Chai and Shen 2016 332
Mu et al 2016) are also noted in Supplemental Table S1 333
334
Based on the computational analysis we have identified a total of 120 AP2ERF 335
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13
genes in octoploid strawberry (Supplemental Table S1) The number of predicted 336
AP2ERF genes (120) is comparable to those observed in other fruits including 337
tomato (112) Chinese plum (116) citrus (126) and peach (131) but lower than those 338
reported for grape (149) (Xie et al 2016) As shown in Supplemental Table S2 79 339
(95 genes) of the AP2ERF genes belong to the ERF family in strawberry constituting 340
the largest sub-family The members of this sub-family can be classified into 10 341
groups (group I to X) according to their sequence similarities to the Arabidopsis ERF 342
genes (Nakano et al 2006) The AP2 family encompasses the same number of genes 343
in Arabidopsis citrus and strawberry (eighteen) (Nakano et al 2006 Xie et al 2014) 344
and there are six RAV genes in strawberry which are highly conserved in dicots such 345
as Vitis vinifera Arabidopsis thaliana and Populus trichocarpa (Licausi et al 2010) 346
347
Role of FaERF9 in regulating the biosynthesis of HDMF a positive regulator 348
acting in an indirect manner 349
The large-scale screening of the AP2ERF superfamily in strawberry led to 350
identification of 11 ERFs and 1 RAV that trans-activated the FaQR promoter more 351
than two-fold with the highest activation caused by FaERF9 which trans-activated 352
the FaQR promoter (Figure 2) as well as up-regulating FaQR expression and furanone 353
production in transient overexpression assays (Figure 4) which has been extensively 354
used to explore the fruit-associated gene functions in strawberry (Han et al 2015 355
Medina-Puche et al 2015 Vallarino et al 2015 Carvalho et al 2016 Song et al 356
2016 Wang et al 2018) FaERF9 transcripts accumulate in the fruit apical section 357
before the basal section (Figure 3) a finding consistent with the actual changes in 358
furaneol content (Figure 1) and the expression of FaQR (Figure 1) The association 359
between FaERF9 transcripts and accumulation of furanones were also established 360
with different strawberry cultivars The correlation between FaERF9 and FaQR 361
expression as well as furanone content among cultivars supports a positive role of 362
FaERF9 in regulating furanone content (Figure 5) These results indicate that 363
FaERF9 transcript abundance may be a good indicator of the abundance of these 364
important flavour volatiles in fruits of different cultivars This should be considered as 365
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14
a method for high-throughput variety screening to replace direct measurement of 366
volatiles 367
368
FaERF9 is a member of the ERF group II family and is most closely related to the 369
Arabidopsis genes At1g44830 (ATERF014) At1g21910 (DREB26) and At1g77640 370
(Supplemental Figure S1) At1g44830 was observed to be strongly up-regulated in a 371
comprehensive microarray analysis of the root transcriptome following NaCl 372
exposure (Jiang and Deyholos 2006) At1g21910 (DREB26) was functionally 373
characterized as a trans-activator localized in the nucleus exhibiting tissue-specific 374
expression and participating in plant developmental processes as well as biotic andor 375
abiotic stress signalling (Krishnaswamy et al 2011) However none of these genes 376
have been reported as furanone regulators In strawberry another five genes 377
(FaERF6 FaERF7 FaERF8 FaERF10 and FaERF11) also belong to the same 378
group with FaERF8 also showing somewhat weaker activation activity towards the 379
FaQR promoter than FaERF9 The fact that FaERF9 could not bind directly to the 380
promoter of FaQR (Figure 6) indicates that it might function as an indirect regulator 381
of FaQR and furaneol biosynthesis 382
383
A FaERF9 and FaMYB98 complex is involved in regulating FaQR and furaneol 384
biosynthesis 385
The finding that FaERF9 could interact with FaMYB98 protein (Figures 9 and 386
Figure 10) and that FaMYB98 could physically bind to the FaQR promoter (Figure 6 387
and Figure 7) provides evidence for a regulatory mechanism whereby FaERF9 388
regulates FaQR and furaneol production as part of a complex with an MYB 389
transcription factor Since co-overexpression of FaERF9 and FaMYB98 resulted in 390
much higher activation activity towards FaQR we speculate that FaERF9 may 391
recruit FaMYB98 homologs in tobacco to activate the FaQR promoter (Figure 8) 392
FaOMT is another key gene for furanone biosynthesis and a potential target for 393
transcriptional activation However FaERF9 did not significantly activate the 394
FaOMT promoter in a dual-luciferase assay and the transcript level of FaOMT in the 395
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15
FaERF9-overexpressing fruits showed no significant difference from that in the 396
control (Supplemental Figure S6 Supplemental Figure S7) The FaOMT promoter 397
was significantly induced by FaMYB98 but no synergistic effect of FaERF9 and 398
FaMYB98 on the promoter was observed (Supplemental Figure S6) In previous 399
studies of the regulation of plant volatile compounds MYBs have been characterized 400
as being involved mainly in the regulation of the benzenoidphenylpropanoid pathway 401
that produces floral volatiles in petunia and eugenol in ripe strawberry fruit (Verdonk 402
et al 2005 Dal Cin et al 2011 Colquhoun et al 2011 Spitzer-Rimon et al 2012 403
Medina-Puche et al 2015) but their role in formation of volatiles from other 404
pathways has not been reported Our study demonstrates a role for MYB in the 405
synthesis of furaneol a carbohydrate-derived volatile compound and reveals the 406
synergistic interactions between an MYB and ERF in a transcription complex (Figure 407
8 Figure 9 and Figure 10) 408
409
Recent research has provided evidence for interactions between AP2ERF and MYB 410
transcription factors in regulating other aspects of fruit quality including texture 411
(EjAP2-1 and EjMYB Zeng et al 2015) and colour (PyERF3 and PyMYB114 Yao 412
et al 2017) A group VIII ERF has also recently been shown to interact with an MYB 413
to regulate floral scent production in petunia (Liu et al 2017) In strawberry fruit 414
DOF in combination with an MYB has been reported to be involved in the regulation 415
of eugenol production and the identification of this second transcription factor (DOF) 416
suggests that it is a good target in breeding for improved flavour (Molina-Hidalgo et 417
al 2017 Tieman 2017) Considering its important contribution to flavour in 418
strawberry and many other highly valued fruit crop species (pineapple tomato mango 419
etc) very little is known about regulation of furaneol synthesis Here we established 420
the role of FaERF9 in the regulation of HDMF synthesis by direct protein-protein 421
interactions with FaMYB98 to synergistically trans-activate FaQR The functional 422
identification of this complex enhances our knowledge of the regulation of volatile 423
compound synthesis and identifies a new AP2ERF-MYB complex Further 424
examination of the other ERFs that stimulated transcription from the FaQR promoter 425
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16
(Figure 2) may provide additional information about the complexity of this regulation 426
Overall this study provides important clues for understanding the transcriptional 427
regulation of HDMF synthesis and identifies specific transcription factors that are 428
likely to be good targets for molecular breeding for improved flavour 429
430
Conclusions 431
Screening of the AP2ERF superfamily in strawberry (Fragaria times ananassa) 432
identified candidate members capable of activating the FaQR promoter An ERF 433
transcription factor was identified as a positive regulator of HDMF synthesis in 434
strawberry fruit and the mechanism of activation was shown to involve an ERF-MYB 435
transcription complex that regulates transcription of FaQR leading to the biosynthesis 436
of HDMF the characteristic volatile compound which has a major influence on 437
strawberry aroma 438
439
Materials and Methods 440
441
Plant Materials and Growth conditions 442
The strawberry (Fragaria times ananassa cv lsquoYuexinrsquo an octoploid cultivar) fruit used in 443
this study were bred by Zhejiang Academy of Agricultural Sciences (Haining 444
Zhejiang) Fruits at various developmental and ripening stages including G (green) T 445
(turning) IR (intermediate red) and R (full red) were harvested (Figure 1) and 446
transported to the laboratory within 2 h Thirty-six fruits of uniform size and free of 447
visible defects were selected at each stage with twelve fruits in each biological 448
replicate After removing the calyces fruits were then divided into the basal and 449
apical sections which were sampled separately (Figure 1) They were rapidly cut into 450
pieces frozen immediately in liquid nitrogen and stored at -80deg C until use Red ripe 451
fruits of different strawberry cultivars (Fragaria times ananassa octoploid cultivars) 452
including lsquoYuelirsquo lsquoBenihoppersquo lsquoMengxiangrsquo lsquoAmaoursquo lsquo10-1-4rsquo lsquoAkihimersquo lsquoSweet 453
Charliersquo lsquo07-1-4rsquo lsquoDarselectrsquo lsquoYuexinrsquo and lsquoXuemeirsquo were also provided by Zhejiang 454
Academy of Agricultural Sciences For each cultivar the fruits of three biological 455
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17
replicates were sampled frozen in liquid nitrogen and stored at -80deg C for further use 456
457
Tobacco plants (Nicotiana benthamiana) used for dual-luciferase assays and 458
subcellular localization analysis in this study were grown in a growth chamber with a 459
lightdark cycle of 16 h8 h at 24degC 460
461
Detection of DMMF and HDMF 462
Automated HS-SPME-GC-MS was performed to detect both furanones in lsquoYuexinrsquo 463
strawberry fruit (Zorrilla-Fontanesi et al 2012) Samples were ground into a powder 464
under liquid nitrogen for analysis 465
466
For the detection of DMMF (Figure 1) 05 g (fresh weight) of each sample was 467
weighed in the vial to which was added 1 mL of EDTA solution (100 mM pH 75) 1 468
mL of CaCl2 solution (mv = 20) and 20 microL of 2-octanol as the internal standard 469
(007 μgμL) The mixture was homogenized and the vial closed and placed on the 470
sample tray for analysis by CombiPAL autosampler (CTC Analytic CA USA) The 471
fruit volatiles were sampled by headspace solid-phase microextraction with a 65-μm 472
polydimethylsiloxane-divinylbenzene fibre (PDMS-DVB) Initially vials were 473
pre-incubated at 50degC for 10 min under continuous agitation (500 rpm) then volatiles 474
were extracted for 30 min at the same temperature and agitation speed After that the 475
fibre was desorbed in the GC injection port for 5 min in splitless mode The 7890A 476
GC chromatograph was equipped with a DB-5ms column (60 m times 250 μm times 1 μm 477
JampW Scientific Folsom CA USA) with helium as the carrier gas at a constant flow 478
of 12 mLmin The GC was programmed at an initial temperature of 35degC for 2 min 479
with a ramp of 5degC min up to 250degC and held for 5 min The injection port interface 480
and MS source temperatures were 250degC 260degC and 230degC respectively The 481
ionization potential was set at 70 eV recorded by a 5975B mass spectrometer (Agilent 482
Technologies JampW Scientific Folsom CA USA) and the scanning speed was 7 483
scanss The same method was used to analyse HDMF and DMMF in fruits from 484
different cultivars (Supplemental Figure S3) except for the sample preparation 485
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18
procedure (Araguumlez et al 2013) briefly 05 g (fresh weight) of powdered fruit was 486
incubated at 30degC in a water bath for 5 min then 2 mL of NaCl (mv = 20) and 20 487
microL of 2-octanol as the internal standard (007 μgμL) were added and homogenized 488
489
For the detection of HDMF (Figure 1) and both furanones (Figure 4 and Supplemental 490
Table S3) a liquid-injection system equipped with CTC Pal ALS was used One gram 491
(fresh weight) of powdered fruit and 2 mL of NaCl (mv = 20) were homogenized in 492
a 10-mL tube and 300 μL of CH2Cl2 and 20 microL of 2-octanol (0766 μgμL) as the 493
internal standard were added to extract the volatiles the mixture was then 494
homogenized again The tubes were stored at room temperature for 20 min and 495
centrifuged at 12000 rpm for 5 min The subnatant was pipetted into a clean 15-mL 496
tube in which 20 mg of anhydrous sodium sulphate was added the tube was left 497
without shaking for half an hour Then 150 μL of the solution was transferred into a 498
GC vial and placed on the sample tray as described above Each sample (1 μL) was 499
injected using the autosampler and the analysis was accomplished by a 7890A 500
GC-MS system (Agilent Technologies JampW Scientific Folsom CA USA) equipped 501
with a DB-WAX column (30 m times 025 mm times 025 μm JampW) Helium (12 mLmin) 502
was used as a carrier gas The injection port (splitless injection mode) interface and 503
MS source temperatures were as described above The oven temperature was set at 504
60degC for 4 min then increased to 180degC at a rate of 4degCmin and maintained for 30 505
min DMMF was identified by comparison of electron ionization mass spectra and 506
retention time data with the data from the NISTEPANIH mass spectral library 507
(NIST-08 and Flavor) HDMF (Figure 1) was identified and qualified by comparison 508
with injected standard (Sigma) The quantitative analysis of both furanones (Figure 4 509
Supplemental Table S3 and Supplemental Figure S3) was determined using the peak 510
area of the internal standard as a reference based on total ion chromatogram (TIC) 511
512
RNA isolation and Reverse Transcription Quantitative PCR (RT-qPCR) 513
Total RNA from strawberry samples was isolated in this study using the CTAB 514
method (Chang et al 1993) Genomic DNA contamination was eliminated by 515
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19
TURBO Dnase (Ambion) 1 μg of RNA was used to obtain cDNA using an IScriptTM 516
cDNA Synthesis Kit (Bio-Rad) The synthesized cDNA was diluted with water (120) 517
and 2 μL of diluted cDNA was used as the template for RT-qPCR Reactions were 518
performed in a total volume of 20 μL consisting of 10 μL of SYBR PCR supermix 519
(Bio-Rad) 1 μL of each primer (10 μM) 6 μL of DEPC-H2O and 2 μL of diluted 520
cDNA on CFX96 instrument (Bio-Rad) (Yin et al 2012) The oligonucleotide 521
primers for RT-qPCR analysis of genes including the AP2ERF FaQR and FaOMT 522
were designed according to the coding sequences of genes and the specificity was 523
verified before use (Min et al 2012) NCBIPrimer-BLAST was applied to design the 524
primers Relative expression levels were normalized to that of an internal controlmdashthe 525
interspacer 26S-18S strawberry RNA housekeeping gene FaRIB413 526
(Zorrilla-Fontanesi et al 2012) To investigate the differential expression of genes 527
during fruit development and ripening stages relative expression of each gene at the 528
R stage in the basal fruit section was set as 1 using the 2minus∆∆119862119879 method For transient 529
overexpression assay relative expression of control fruits with an empty vector (SK) 530
was set as 1 The primers used in RT-qPCR are listed in Supplemental Table S4 531
532
Gene isolation and analysis 533
Multiple database searches were performed to identify members of the strawberry 534
(Fragaria times ananassa) AP2ERF superfamily in the published strawberry databases 535
and annotations of Fragaria times ananassa and Fragaria times vesca by using the 536
AP2ERF DNA binding domain as a query sequence and 120 genes were identified 537
with AP2ERF domain(s) Based on the BLAST result primers (listed in 538
Supplemental Table S5) were used to amplify the coding full-length cDNAs of 539
AP2ERF genes The deduced amino acid sequences of AP2ERF proteins in 540
Arabidopsis thaliana used for construction of a phylogenetic tree were obtained from 541
the Arabidopsis Information Resource (TAIR) Alignment of the proteins was 542
performed using the neighbour-joining method in ClustalX (v181) and the 543
phylogenetic tree was constructed using FigTree (v131) 544
545
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
20
FaMYB98 was obtained by yeast one-hybrid screening sequencing and the full-length 546
sequences were predicted by BLAST Primers were designed (listed in Supplemental 547
Table S5) to amplify the full-length coding sequence 548
549
The promoter of FaQR was cloned by Genome Walking as previously described (Yin 550
et al 2010) and conserved cis-element motifs in the promoter were manually 551
searched 552
553
Conserved domains within the FaAP2ERF proteins and FaMYB98 were analysed by 554
CD-search (httpswwwncbinlmnihgovStructurecddwrpsbcgi) and cellular 555
locations of proteins including FaERF9 and FaMYB98 were predicted with the 556
WoLF PSORT program (httpswwwgenscriptcomwolf-psorthtml) 557
558
Dual-Luciferase Assays 559
In accordance with a previous protocol (Yin et al 2010) the full-length cDNAs of 560
FaAP2ERF or FaMYB98 transcription factors were cloned into pGreen II 0029 561
62-SK vector and the promoter of FaQR was cloned into pGreen II 0800-LUC vector 562
A luciferase gene from Renillia (REN) driven by a 35S promoter in the LUC vector 563
acted as a positive control The above constructs were transiently expressed in 564
Nicotiana benthamiana leaves by Agrobacterium-mediated infiltration (strain 565
GV3101) and the activity of the TFs on the promoter was measured on the third day 566
after infiltration indicated by the ratio of enzyme activities of firefly luciferase (LUC) 567
and renilla luciferase (REN) using a Modulus Luminometer (Promega Madison WI 568
USA) To determine the activity of a specific transcription factor towards the 569
promoter we mixed the Agrobacterium culture with 1 mL of TF and 100 μL of 570
promoter and the LUCREN value of the empty vector SK on the promoter was set as 571
1 as a calibrator To test the combined effect of two transcription factors on the 572
promoter to the Agrobacterium culture mixture we added 05 mL of each TF and 100 573
μL of promoter the effect of the mixtures that contained each transcription factor (05 574
mL) and empty vector SK (05 mL) was also tested on the promoter as a control 575
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
21
576
Subcellular localization analysis 577
35S-FaERF9-GFP and 35S-FaMYB98-GFP were transiently expressed in tobacco (N 578
benthamiana) leaves by Agrobacterium infiltration (EHA105) using the same method 579
as described in the dual-luciferase assay above The transiently infected leaves were 580
imaged on the third day after infiltration using a Nikon A1-SHS confocal laser 581
scanning microscope The excitation wavelength for GFP fluorescence was 488 nm 582
and fluorescence was detected at 490ndash520 nm The primers used for GFP construction 583
are listed in Supplemental Table S6 584
585
Transient overexpression in strawberry fruit 586
Transient overexpression of FaERF9 and an overexpression binary vector (pGreen II 587
0029 62-SK-FaERF9-FaMYB98) were performed in strawberry fruit using the 588
FaERF9-SK construct described above for the dual-luciferase assays and the binary 589
vector constructed according to Liu et al 2013 The transfection of fruit was carried 590
out at the G stage (Hoffmann et al 2006) The FaERF9-SK construct and binary 591
vector were individually electroporated into Agrobacterium tumefaciens GV3101 and 592
the Agrobacterium culture suspended in infiltration buffer was infiltrated into the 593
whole fruit using a syringe As a control treatment fruits were infiltrated with 594
Agrobacterium carrying an empty vector SK under the same transfection conditions 595
Fruits were left attached to the plants and harvested on the seventh day after 596
infiltration Fruits of three biological replicates were sampled for further analysis 597
598
Yeast one-hybrid assay 599
In order to identify proteins that bind to the FaQR promoter the Matchmaker Gold 600
Yeast One-hybrid Library Screening System (Clontech USA) was used The sequence 601
of the FaQR promoter was cloned into the pAbAi vector and the construct was 602
integrated into the genome of the Y1HGold yeast strain A mixture of total RNA from 603
strawberry fruit at four stages (G T IR R) was used to construct the prey cDNA 604
library (TaKaRa) The background AbAr expression of Y1HGold FaQR-pAbAi strain 605
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
22
was tested according to the system user manual and then screening for protein-DNA 606
interactions was carried out Furthermore the full length of each transcription factor 607
was separately cloned into pGADT7 AD vector to confirm the screening results The 608
relationship between FaERF9 and FaQR promoter was also examined individually 609
Primers used in this assay are listed in Supplemental Table S6 610
611
Expression and purification of FaMYB98 recombinant protein 612
A 405-bp region spanning the DNA-binding domain of FaMYB98 was amplified 613
from FaMYB98 cDNA and cloned into a pET6timesHN vector (Clontech Palo CA USA) 614
to generate the recombinant N-terminal His-tagged protein the primers used are listed 615
in Supplemental Table S6 The resulting construct was sequenced and introduced into 616
Escherichia coli strain Rosetta 2(DE3)pLysS (Novagen) Ten millilitres of the 617
overnight culture was combined with 500 mL of an LB liquid medium (100 μgmL 618
ampicillin and 34 μgmL chloramphenicol) as described (Li et al 2017) Isopropyl 619
β-D-1-thiogalactopyranoside (IPTG) was added to a final concentration of 1 mM and 620
the bacterial culture was incubated at 18degC at 150 rpm for 18 h Then the cells were 621
harvested using a centrifuge and resuspended in 1times PBS buffer (Sangon Biotech) 622
after which they were disrupted by sonication and the supernatant was purified using 623
a HisTALONTM Gravity Column (Clontech) according to the user manual The PD-10 624
Desalting column (GE Healthcare) was then used for buffer change and sample 625
clean-up of proteins according to the gravity protocol SDS-PAGE was performed and 626
the protein was visualized using Coomassie brilliant blue 627
628
Electrophoretic mobility shift assay (EMSA) 629
A Lightshift Chemiluminescent EMSA kit (Thermo) was used to perform EMSA 630
experiments according to the manufacturerrsquos instructions Single-strand 631
oligonucleotides were synthesized and biotinylated by GeneBio Biotech (Hangzhou 632
China) The details of the EMSA assay are provided in Ge et al (2017) The probes 633
used for EMSAs are listed in Supplemental Table S6 634
635
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
23
636
Yeast two-hybrid assay 637
The DUALhunter system (Dualsystems Biotech Switzerland) was used to investigate 638
the interaction between FaERF9 and FaMYB98 Full-length coding sequences of 639
FaERF9 and FaMYB98 were respectively cloned into pDHB1 bait vector and 640
pPR3-N prey vector sequences were verified and the bait plasmid was 641
co-transformed with prey plasmid into NMY51 in the combinations below 642
FaMYB98-pDHB1pPR3-N FaMYB98-pDHB1FaERF9-pPR3-N 643
FaMYB98-pDHB1pOst1-NubI FaERF9-pDHB1pPR3-N 644
FaERF9-pDHB1FaMYB98-pPR3-N and FaERF9-pDHB1pOst1-NubI (Li et al 645
2017) Transformed cells were spread onto the following plates DDO (SD 646
medium-Trp-Leu) QDO (SD medium-Trp-Leu-His-Ade) and QDO+3-AT (QDO 647
medium supplemented with 1 mM 3-amino-124-triazole) The control plasmid 648
pOst1-NubI was used to determine whether the bait was functional the pPR3-N prey 649
vector plasmid was used to test whether the bait displayed non-specific background 650
and positive interactions were indicated by the growth of yeast on QDO and 651
QDO+3-AT plates The Primers used in the DUALhunter assay are listed in 652
Supplemental Table S6 653
654
Bimolecular fluorescence complementation (BiFC) assays 655
Full-length FaERF9 and FaMYB98 respectively were cloned into sequences 656
encoding the N- and C- fragments of YFP protein (Lv et al 2014) All constructs 657
were transiently expressed in tobacco (N benthamiana) leaves by Agrobacterium 658
infiltration (EHA105) The YFP fluorescence of transfected leaves was imaged 40 h 659
after infiltration by using a Nikon A1-SHS confocal laser scanning microscope The 660
excitation wavelength for YFP was 488 nm and fluorescence was detected at 520ndash661
540 nm Primers used are listed in Supplemental Table S6 662
663
Statistics 664
A Studentrsquos two-tailed t test ( plt005 plt001 and plt0001) was used to 665
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
24
determine significant differences between two groups in this study Microsoft Excel 666
was used to perform linear regressive analysis significant differences were 667
determined by SPSS Statistics 200 and scatter plots were prepared with Origin80 668
Least significant difference (LSD) at the 5 level was calculated using Microsoft 669
Excel Figures were prepared with Origin80 (Microcal Software Inc Northampton 670
MA USA) The online tool MetaboAnalyst 36 (httpwwwmetaboanalystca) was 671
used to analyse the transcript abundance of the AP2ERF genes 672
673
Accession numbers 674
Sequence data from this article have been deposited in GenBank under the accession 675
numbers MH332903-MH333022 for AP2ERF genes in Fragaria times ananassa and 676
MH333023 for FaMYB98 GenBank numbers for FaQR and FaOMT were 677
AY1588361 (Raab et al 2006) and AF2204912 (Wein et al 2002) 678
679
Supplemental Material 680
Supplemental Figure S1 Phylogenetic analysis of FaAP2ERF and Arabidopsis 681
AP2ERF proteins 682
Supplemental Figure S2 Analysis of FaAP2ERF gene expression patterns in 683
strawberry fruit during development and ripening 684
Supplemental Figure S3 Contents of furanones in fruit of strawberry cultivars 685
Supplemental Figure S4 Relative expression of FaERF9 in FaERF9-FaMYB98- 686
and FaERF9-overexpressing fruits 687
Supplemental Figure S5 Subcellular localization of FaMYB98 688
Supplemental Figure S6 The combined activation effects of FaERF9FaMYB98 on 689
the FaOMT promoter 690
Supplemental Figure S7 Relative expression of FaOMT in 691
FaERF9-overexpressing fruits 692
Supplemental Table S1 AP2ERF superfamily genes in Fragaria times ananassa 693
Supplemental Table S2 Classification of the AP2ERF superfamily members in 694
Fragaria times ananassa 695
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
25
Supplemental Table S3 Furanone content in FaERF9-FaMYB98- and 696
FaERF9-overexpressing fruits 697
Supplemental Table S4 Primers used for reverse transcription quantitative PCR 698
(RT-qPCR) 699
Supplemental Table S5 Primers used to amplify the full-length coding sequences of 700
AP2ERF genes and FaMYB98 in strawberry (Fragaria times ananassa) 701
Supplemental Table S6 Primers used for vector construction 702
703
Acknowledgments 704
This research was supported by the National Key Research and Development 705
Program (2016YFD0400101) the Project of the Science and Technology Department 706
of Zhejiang Province (2016C04001) and the 111 Project (B17039) 707
708
Figure legends 709
Figure 1 Changes in furanone content and furanone biosynthetic genes during 710
strawberry (Fragaria times ananassa Duch cv Yuexin) fruit development and ripening 711
A Fruits were collected at four ripening stages G (green stage) T (turning stage) IR 712
(intermediate red stage) R (full red stage) B Changes in the contents of furaneol 713
(HDMF) and mesifurane (DMMF) HDMF content was calculated using a standard 714
curve of HDMF while DMMF content was calculated with an internal standard as the 715
reference C Expression levels of FaQR and FaOMT The expression levels of each 716
gene were calculated relative to corresponding values in the basal section at the R 717
stage SEs were calculated from three replicates and LSD values represent the least 718
significant differences at p = 005 719
Figure 2 Regulatory effects of FaAP2ERF on the promoter of FaQR LUCREN 720
values of the empty vector on FaQR promoter were used as the calibrator set as 1 721
and SEs were calculated from five replicates statistical significance was determined 722
by Studentrsquos two-tailed t test ( plt0001) 723
Figure 3 Expression and the subcellular localization of FaERF9 A The expression 724
levels were calculated relative to the levels in the basal section at the R stage B 725
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
26
Subcellular localization analysis was performed in tobacco leaves The tobacco used 726
in the assay was stably transformed with a specific nucleus localized red fluorescence 727
protein construct and the red fluorescence indicates the nucleus-localized signal 728
(NLS) Scale bar = 25 microm SEs were calculated from three replicates 729
Figure 4 Transient overexpression of FaERF9 in strawberry fruit A Relative 730
expression of FaQR and FaERF9 in FaERF9-OX fruit 7 days after infiltration The 731
expression was calculated relative to the average value in control (SK) fruits B 732
HDMF and DMMF content in FaERF9-OX fruit The content of both furanones 733
were quantified using the peak area of the internal standard (2-octanol) as the 734
reference SEs were calculated from three replicates Statistical significance was 735
determined by Studentrsquos two-tailed t test ( plt005 plt001 plt0001) 736
Figure 5 Scatter plots of 11 strawberry cultivars A Linear regression analysis 737
between FaERF9 expression and FaQR expression B Linear regression analysis 738
between FaERF9 expression and furanone content The relative expression was 739
normalized to that of the housekeeping gene FaRIB413 and furanone content was 740
calculated with internal standard as the reference Significant differences were 741
determined by SPSS Statistics 200 742
Figure 6 Interactions of FaERF9 and FaMYB98 with the FaQR promoter A Yeast 743
one-hybrid analysis of the interaction of FaERF9 and FaQR promoter B Yeast 744
one-hybrid analysis of the interaction of FaMYB98 and FaQR promoter C 745
Regulatory effect of FaMYB98 on the FaQR promoter Auto-activation was tested on 746
SD-Ura (synthetically defined medium without uracil) in presence of Aureobasidin A 747
(AbA) and physical interaction was determined on SD-Leu (synthetically defined 748
medium without leucine) in presence of AbA LUCREN values of the empty vector 749
on FaQR promoter were used as the calibrator set as 1 and error bars were calculated 750
from five replicates Statistical significance was determined by Studentrsquos two-tailed t 751
test ( plt005 plt001 plt0001) 752
Figure 7 Electrophoretic mobility shift assay of FaMYB98 binding to FaQR 753
promoter A The probe sequence used for EMSA and mutated nucleotides are 754
indicated with lowercase letters B Purified DNA-binding domain of FaMYB98 755
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
27
protein and biotin-labelled DNA probe were mixed and analysed on 6 native 756
polyacrylamide gels and then photographed Presence or absence of specific probes is 757
marked by the symbol + or - 758
Figure 8 The combined activation effects of FaERF9FaMYB98 on the FaQR 759
promoter LUCREN values obtained with the empty vector and FaQR promoter were 760
used as the calibrator set as 1 and error bars were calculated from five replicates 761
Figure 9 Yeast two-hybrid analysis of the protein-protein interactions between 762
FaMYB98 and FaERF9 Positive interactions were determined by the growth of 763
yeast cells on selection plates Bait with pOST acted as positive controls and bait with 764
pPR3 as negative controls DDO synthetically defined medium without tryptophan 765
and leucine QDO synthetically defined medium without tryptophan leucine 766
histidine and adenine QDO+3AT QDO medium supplemented with 1 mM 767
3-aminotriazole 768
Figure 10 BiFC analysis of the protein-protein interactions between FaMYB98 and 769
FaERF9 The pairs of fusion proteins tested were FaMYB98-YFPN+FaERF9-YFPC 770
FaERF9-YFPN+FaMYB98-YFPC FaMYB98-YFPN+FaMYB98-YFPC and 771
FaERF9-YFPN+FaERF9-YFPC The other combinations were negative controls 772
The tobacco used in the assay was stably transformed with a specific 773
nucleus-localized red fluorescence protein construct and the red fluorescence 774
indicated the nucleus-localized signal (NLS) Fluorescence of the yellow fluorescence 775
protein (YFP) visualized the interaction in vivo Scale bar = 25 microm 776
777
Literature Cited 778
779
Agarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression 780
of PgDREB2A transcription factor enhances abiotic stress tolerance and activates 781
downstream stress-responsive genes Mol Biol Rep 37 1125-1135 782
Araguumlez I Osorio S Hoffmann T Rambla JL Medina-Escobar N Granell A 783
Botella MAacute Schwab W Valpuesta V (2013) Eugenol production in achenes and 784
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28
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Plant Physiol 163 946-958 786
Carvalho RF Carvalho SD OrsquoGrady K Folta KM (2016) Agroinfiltration of 787
strawberry fruit mdash a powerful transient expression system for gene validation Curr 788
Plant Biol 6 19-37 789
Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic 790
(Amsterdam) 210 34-40 791
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating 792
RNA from pine trees Plant Mol Biol Rep 11 113-116 793
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC 794
Clark DG (2011) PhMYB4 fine-tunes the floral volatile signature of 795
Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143 796
Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz 797
EA Taylor MG Smits-Kroon MT Schuurink RC Haring MA Giovannoni J 798
Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic 799
pathway by ectopic expression of a MYB transcription factor in tomato fruit Plant 800
Cell 23 2738-2753 801
Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan 802
XW Yang ZY (2017) Differential responses of four biosynthetic pathways of 803
aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under 804
interaction of light and temperature Food Chem 221 356-364 805
Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of 806
differentially-expressed genes during somatic embryogenesis in Fragaria times 807
ananassa Duch lsquoBenihopprsquo J Hortic Sci Biotechnol 90 671-681 808
Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 809
transcriptionally regulates chilling-induced lignification of loquat fruit via physical 810
interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136 811
Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM 812
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proteins Plant J 39 513-526 814
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29
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) 815
Sucrose nonfermenting1-related protein kinase26 an ortholog of open stomata1 is 816
a negative regulator of strawberry fruit development and ripening Plant Physiol 817
167 915-930 818
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene 819
expression in strawberry fruit (Fragaria times ananassa) by agroinfiltration a rapid 820
assay for gene function analysis Plant J 48 818-826 821
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of 822
selected aroma-active compounds in strawberries by headspace solid-phase 823
microextraction gas chromatography and correlation with sensory descriptive 824
analysis J Food Sci 72 S487-S496 825
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid 826
plays an important role in the regulation of strawberry fruit ripening Plant Physiol 827
157 188-199 828
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of 829
NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes BMC 830
Plant Biol 6 20 831
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN 832
(2005) MYB98 is required for pollen tube guidance and synergid cell differentiation 833
in Arabidopsis Plant Cell 17 2981-2992 834
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional 835
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Agric Food Chem 55 6705-6711 837
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You 838
J-S Rohloff J Randall SK Alsheikh M (2012) Proteomic study of 839
low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ 840
in cold tolerance Plant Physiol 159 1787-1805 841
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional 842
characterization of four APETALA2-family genes (RAP26 RAP26L DREB19 843
and DREB26) in Arabidopsis Plant Mol Biol 75 107-127 844
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30
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon 845
J Gupta V (2013) An oxidoreductase from lsquoAlphonsorsquo mango catalyzing 846
biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494 847
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in 848
strawberries Z Lebensm-Unters Forsch 195 120-123 849
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X 850
(2015) Label-free quantitative proteomics to investigate strawberry fruit proteome 851
changes under controlled atmosphere and low temperature storage J Proteomics 852
120 44-57 853
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 854
cooperates with CitWRKY1 to participate in citric acid degradation via 855
up-regulation of CitAco3 J Exp Bot 68 3419-3426 856
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription 857
factor CitERF71 activates the terpene synthase gene CitTPS16 involved in the 858
synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938 859
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and 860
transcriptomic analysis of the AP2ERF superfamily in Vitis vinifera BMC 861
Genomics 11 719 862
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive 863
Factor (AP2ERF) transcription factors mediators of stress responses and 864
developmental programs New Phytol 199 639-649 865
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 866
interacting with EOBI negatively regulates fragrance biosynthesis in petunia 867
flowers New Phytol 215 1490-1502 868
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu 869
CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 in regulating 870
anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) 871
during anthocyanin biosynthesis Plant Cell Tissue Organ Cult 115 285-298 872
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31
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao 873
CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphate signaling and 874
homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597 875
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC 876
Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL 877
Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor 878
regulates eugenol production in ripe strawberry fruit receptacles Plant Physiol 168 879
598-614 880
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics 881
and volatile constituents of strawberry (cv Cigaline) during maturation J Agric 882
Food Chem 52 1248-1254 883
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS 884
(2012) Ethylene-responsive transcription factors interact with promoters of ADH 885
and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 886
63 6393-6405 887
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM 888
Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-Franco A 889
Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific 890
transcription factor FaDOF2 regulates the production of eugenol in ripe fruit 891
receptacles J Exp Bot 68 4529-4543 892
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) 893
Comparison and verification of the genes involved in ethylene biosynthesis and 894
signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44 895
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the 896
ERF gene family in Arabidopsis and rice Plant Physiol 140 411-432 897
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in 898
sour cherry and strawberry and the heterologous expression of CBF1 in strawberry 899
J Am Soc Hortic Sci 127 489-494 900
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech 901
JC Ohme-Takagi M Regad F Bouzayen M (2012) Functional analysis and 902
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32
binding affinity of tomato ethylene response factors provide insight on the 903
molecular bases of plant differential responses to ethylene BMC Plant Biol 12 190 904
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) 905
Methylpentoses are possible precursors of furanones in fruits Prikl Biokhim 906
Mikrobiol 28 123-127 907
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery 908
of synergid-expressed genes encoding filiform apparatus localized proteins Plant 909
Cell 19 2557-2568 910
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria 911
vesca L compared to those of cultivated berries Fragariatimes ananassa cv Senga 912
Sengana J Agric Food Chem 27 19-22 913
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W 914
Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of the strawberry 915
flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone 916
oxidoreductase Plant Cell 18 1023-1037 917
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L 918
Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim M Broun P Zhang 919
JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription 920
factors genome-wide comparative analysis among eukaryotes Science 290 921
2105-2110 922
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the 923
formation of 25-dimethyl-4-hydroxy-3(2H)-furanone in detached ripening 924
strawberry fruits J Agric Food Chem 46 1488-1493 925
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 926
25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in 927
strawberry fruits Phytochemistry 43 155-159 928
Schwab W (1998) Application of stable isotope ratio analysis explaining the 929
bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone in plants by a biological 930
maillard reaction J Agric Food Chem 46 2266ndash2269 931
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33
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) 932
Molecules 18 6936-6951 933
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products Recent Res Dev Phytochem 1 643-673 935
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL 936
Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJ Sims CA 937
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compositions a seasonal influence and effects on sensory perception PLoS One 9 939
e88446 940
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) 941
Identification phylogeny and transcript profiling of ERF family genes during 942
development and abiotic stress treatments in tomato Mol Genet Genomics 284 943
455-475 944
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) 945
CitAP210 activation of the terpene synthase CsTPS1 is associated with the 946
synthesis of (+)-valencene in lsquoNewhallrsquo orange J Exp Bot 67 4105-4115 947
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes 948
Dev Genes Evol 214 105-114 949
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K 950
Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the 951
key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151 952
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O Yu YX Shklarman E Ovadis M Vainstein A (2012) The R2R3-MYB-like 954
regulatory factor EOBI acting downstream of EOBII regulates scent production 955
by activating ODO1 and structural scent-related genes in petunia Plant Cell 24 956
5089-5105 957
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp 958
Bot 68 4407-4409 959
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla 960
JF Amaya I Giavalisco P Fernie AR Botella MA Valpuesta V (2015) Central 961
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34
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to ripening New Phytol 208 482-496 963
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 964
regulates fragrance biosynthesis in petunia flowers Plant Cell 17 1612-1624 965
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS 966
(2018) The potassium channel FaTPK1 plays a critical role in fruit quality 967
formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748 968
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) 969
Isolation cloning and expression of a multifunctional O-methyltransferase capable 970
of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma 971
compounds in strawberry fruits Plant J 31 755-765 972
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor 973
types their evolutionary origin and species distribution In A handbook of 974
transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular 975
Biochemistry 52 25-73 976
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of 977
odor (Buettner A Ed) Springer Cham 9-10 978
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS 979
(2014) Isolation classification and transcription profiles of the AP2ERF 980
transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271 981
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in 982
regulation of fruit quality Crit Rev Plant Sci 35 120-130 983
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ 984
Zhang SL Wu J (2017) Map-based cloning of the pear gene MYB114 identifies an 985
interaction with other transcription factors to coordinately regulate fruit 986
anthocyanin biosynthesis Plant J 92 437-451 987
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes 988
involved in regulating fruit ripening Plant Physiol 153 1280-1292 989
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
35
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) 990
Expression of ethylene response genes during persimmon fruit astringency removal 991
Planta 235 895-906 992
Zabetakis I Gramshaw JW Robinson DS (1999) 993
25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis and 994
biosynthesis-a review Food Chem 65 139-151 995
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci 996
Food Agric 74 421-434 997
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 998
an AP2ERF gene is a novel regulator of fruit lignification induced by chilling 999
injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1000
1325-1334 1001
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation 1002
classification and transcription profiles of the Ethylene Response Factors (ERFs) in 1003
ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215 1004
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML 1005
(2012) Genome-wide analysis of the AP2ERF superfamily in peach (Prunus 1006
persica) Genet Mol Res 11 4788-4809 1007
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and 1008
expression analysis of a CRTDRE-binding factor gene FaCBF1 from Fragaria times 1009
ananassa Acta Hortic 41 240-248 1010
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The 1011
Arabidopsis AP2ERF transcription factor RAP26 participates in ABA salt and 1012
osmotic stress responses Gene 457 1-12 1013
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Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF 1018
Valpuesta V Botella MA Granell A Amaya I (2012) Genetic analysis of 1019
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36
strawberry fruit aroma and identification of O-methyltransferase FaOMT as the 1020
locus controlling natural variation in mesifurane content Plant Physiol 159 1021
851-870 1022
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10
RT-qPCR on the seventh day after infiltration by which time they had reached the IR 246
or R stage and the result showed that the transcript levels were significantly higher 247
(52-fold) than in control fruits (Figure 4) The expression of FaQR was examined in 248
the same fruits and the transcript abundance also increased 22-fold The relative 249
content of HDMF in the FaERF9-overexpressing fruits was 008 μg per gram fruit 250
and undetectable in the control fruits (Figure 4) The relative content of DMMF in the 251
overexpressing fruits was also significantly increased to 038 μg per gram fruit 252
compared to 004 μg per gram fruit in the control (Figure 4) These observations 253
provide direct evidence for a regulatory role for FaERF9 in promoting FaQR 254
biosynthesis and activity in ripening strawberry fruit Taken together these results 255
indicate that by activating the transcription of FaQR FaERF9 functions as a positive 256
regulator in furaneol biosynthesis 257
258
Correlation of FaERF9 expression and FaQR transcript profiles 259
GC-MS quantification showed that furanones are distributed in variable levels among 260
different strawberry cultivars (Supplemental Figure S3) The transcript profiles of 261
FaQR and FaERF9 in fruits of different cultivars were measured and linear 262
regression analysis was performed In the cultivars the changes in FaQR transcripts 263
correlated positively with those in FaERF9 transcripts (r = 079 plt001) (Figure 5) 264
In addition FaERF9 transcript levels also correlated with furanone content across 265
cultivars (Figure 5) 266
267
FaERF9 is an indirect regulator of the FaQR promoter and acts via 268
protein-protein interaction with FaMYB98 269
Although the results of the dual-luciferase assay expression analysis transient 270
overexpression and correlation analysis were all consistent with the suggestion that 271
FaERF9 regulates transcript abundance by acting on the FaQR promoter a yeast 272
one-hybrid assay indicated that FaERF9 cannot bind directly to the FaQR promoter 273
(Figure 6) This led us to speculate that activation may occur via a transcription 274
complex involving an additional as-yet unknown regulator which can bind directly to 275
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11
the FaQR promoter 276
277
In parallel with the investigation of the FaAP2ERF genes a cDNA library screening 278
was performed with a yeast one-hybrid assay using the promoter of FaQR as the bait 279
This screen identified several transcription factors that could physically bind to the 280
FaQR promoter but only one MYB could activate transcription from the FaQR 281
promoter (approximately 56-fold) relative to the control (Figure 6) in the 282
dual-luciferase assay This MYB showed 44 amino acid identity with MYB98 283
(GenBank ABA420611) a transcriptional regulator in the synergid cells in 284
Arabidopsis (Kasahara et al 2005) and it was designated as FaMYB98 The 285
specificity of FaMYB98 binding to the FaQR promoter was confirmed by EMSA 286
assay (Figure 7) and increasing the concentration of the cold probe reduced binding 287
In addition mutating the putative binding sites (Goacutemez-Maldonado et al 2004 288
Punwani et al 2007) as shown in Figure 7 eliminated FaMYB98 protein binding 289
When the combined effect of FaERF9 and FaMYB98 was analysed (Figure 8) a 290
synergistic 14-fold activation of the FaQR promoter was observed compared with the 291
activation by either FaERF9 or FaMYB98 which alone promoted transactivation 292
39-fold and 45-fold respectively In addition overexpression of both genes 293
(FaERF9-FaMYB98-SK) in strawberry fruits resulted in higher expression of 294
FaERF9 transcripts and higher furanone content than overexpression of FaERF9 295
(Supplemental Figure S4 Supplemental Table S3) Subcellular localization analysis 296
revealed that FaMYB98 was also localized in the nucleus (Supplemental Figure S5) 297
298
To investigate the potential interactions between FaERF9 and FaMYB98 the 299
DUALhunter system was used (Figure 9) Cells expressing the FaMYB98 and 300
FaERF9 protein pair using either FaMYB98 or FaERF9 as the bait grew on DDO 301
QDO and QDO supplemented with 1 mM 3-AT selective medium indicating 302
interaction between the two proteins This putative protein-protein interaction was 303
confirmed by BiFC assay and the combinations of FaMYB98-YFPNFaERF9-YFPC 304
and FaERF9-YFPNFaMYB98-YFPC exhibited strong coincident signals in the 305
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12
nucleus while negative controls produced no detectable fluorescence signal (Figure 306
10) In addition coexpression of FaERF9-YFPNFaERF9-YFPC as well as 307
FaMYB98-YFPNFaMYB98-YFPC also generated signals in the nucleus indicating 308
that FaERF9 and FaMYB98 both could form homodimers or possibly multimers in 309
the nucleus (Figure 10) 310
311
Discussion 312
The AP2ERF superfamily in strawberry 313
The AP2ERF superfamily of plant transcription factors is defined by the AP2ERF 314
domain and comprises the ERF AP2 and RAV families as well as one soloist member 315
(Riechmann et al 2000 Weirauch and Hughes 2011) The completion of multiple 316
plant genome sequences has enabled a genome-scale analysis of the AP2ERF family 317
which in recent years has been systematically studied in diverse fruit species such as 318
tomato grape peach and kiwi fruit (Zhuang et al 2009 Sharma et al 2010 Licausi 319
et al 2010 Yin et al 2010 Pirrello et al 2012 Zhang et al 2012 Zhang et al 320
2016) A few AP2ERF genes have been isolated and characterized in strawberry and 321
CBF orthologs (Owens et al 2002 Koehler et al 2012 Zhang et al 2014) have 322
been identified from different strawberry cultivars in several independent studies 323
Although they have distinct names eg Fragaria times ananassa CBF1 (FaCBF1) 324
FaCBF4 (GenBank HQ9105151) and CBF1 (GenBank EU1172142) according to 325
the phylogenetic tree generated in this study the orthologs of 326
CBF1CBF4CBF2CBF3 in Arabidopsis are similar to each other and to FaERF20 327
(Supplemental Figure S1) (Owens et al 2002 Koehler et al 2012 Zhang et al 328
2014) FaERF20 has 85 sequence similarity with FaCBF1 identified by Owens et 329
al (2002) 93 similarity with FaCBF4 amplified by Koehler et al (2012) and 75 330
similarity with CBF1 cloned by Zhang et al (2014) The AP2ERF genes 331
characterized in other studies (Jia et al 2011 GAO et al 2015 Chai and Shen 2016 332
Mu et al 2016) are also noted in Supplemental Table S1 333
334
Based on the computational analysis we have identified a total of 120 AP2ERF 335
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13
genes in octoploid strawberry (Supplemental Table S1) The number of predicted 336
AP2ERF genes (120) is comparable to those observed in other fruits including 337
tomato (112) Chinese plum (116) citrus (126) and peach (131) but lower than those 338
reported for grape (149) (Xie et al 2016) As shown in Supplemental Table S2 79 339
(95 genes) of the AP2ERF genes belong to the ERF family in strawberry constituting 340
the largest sub-family The members of this sub-family can be classified into 10 341
groups (group I to X) according to their sequence similarities to the Arabidopsis ERF 342
genes (Nakano et al 2006) The AP2 family encompasses the same number of genes 343
in Arabidopsis citrus and strawberry (eighteen) (Nakano et al 2006 Xie et al 2014) 344
and there are six RAV genes in strawberry which are highly conserved in dicots such 345
as Vitis vinifera Arabidopsis thaliana and Populus trichocarpa (Licausi et al 2010) 346
347
Role of FaERF9 in regulating the biosynthesis of HDMF a positive regulator 348
acting in an indirect manner 349
The large-scale screening of the AP2ERF superfamily in strawberry led to 350
identification of 11 ERFs and 1 RAV that trans-activated the FaQR promoter more 351
than two-fold with the highest activation caused by FaERF9 which trans-activated 352
the FaQR promoter (Figure 2) as well as up-regulating FaQR expression and furanone 353
production in transient overexpression assays (Figure 4) which has been extensively 354
used to explore the fruit-associated gene functions in strawberry (Han et al 2015 355
Medina-Puche et al 2015 Vallarino et al 2015 Carvalho et al 2016 Song et al 356
2016 Wang et al 2018) FaERF9 transcripts accumulate in the fruit apical section 357
before the basal section (Figure 3) a finding consistent with the actual changes in 358
furaneol content (Figure 1) and the expression of FaQR (Figure 1) The association 359
between FaERF9 transcripts and accumulation of furanones were also established 360
with different strawberry cultivars The correlation between FaERF9 and FaQR 361
expression as well as furanone content among cultivars supports a positive role of 362
FaERF9 in regulating furanone content (Figure 5) These results indicate that 363
FaERF9 transcript abundance may be a good indicator of the abundance of these 364
important flavour volatiles in fruits of different cultivars This should be considered as 365
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14
a method for high-throughput variety screening to replace direct measurement of 366
volatiles 367
368
FaERF9 is a member of the ERF group II family and is most closely related to the 369
Arabidopsis genes At1g44830 (ATERF014) At1g21910 (DREB26) and At1g77640 370
(Supplemental Figure S1) At1g44830 was observed to be strongly up-regulated in a 371
comprehensive microarray analysis of the root transcriptome following NaCl 372
exposure (Jiang and Deyholos 2006) At1g21910 (DREB26) was functionally 373
characterized as a trans-activator localized in the nucleus exhibiting tissue-specific 374
expression and participating in plant developmental processes as well as biotic andor 375
abiotic stress signalling (Krishnaswamy et al 2011) However none of these genes 376
have been reported as furanone regulators In strawberry another five genes 377
(FaERF6 FaERF7 FaERF8 FaERF10 and FaERF11) also belong to the same 378
group with FaERF8 also showing somewhat weaker activation activity towards the 379
FaQR promoter than FaERF9 The fact that FaERF9 could not bind directly to the 380
promoter of FaQR (Figure 6) indicates that it might function as an indirect regulator 381
of FaQR and furaneol biosynthesis 382
383
A FaERF9 and FaMYB98 complex is involved in regulating FaQR and furaneol 384
biosynthesis 385
The finding that FaERF9 could interact with FaMYB98 protein (Figures 9 and 386
Figure 10) and that FaMYB98 could physically bind to the FaQR promoter (Figure 6 387
and Figure 7) provides evidence for a regulatory mechanism whereby FaERF9 388
regulates FaQR and furaneol production as part of a complex with an MYB 389
transcription factor Since co-overexpression of FaERF9 and FaMYB98 resulted in 390
much higher activation activity towards FaQR we speculate that FaERF9 may 391
recruit FaMYB98 homologs in tobacco to activate the FaQR promoter (Figure 8) 392
FaOMT is another key gene for furanone biosynthesis and a potential target for 393
transcriptional activation However FaERF9 did not significantly activate the 394
FaOMT promoter in a dual-luciferase assay and the transcript level of FaOMT in the 395
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15
FaERF9-overexpressing fruits showed no significant difference from that in the 396
control (Supplemental Figure S6 Supplemental Figure S7) The FaOMT promoter 397
was significantly induced by FaMYB98 but no synergistic effect of FaERF9 and 398
FaMYB98 on the promoter was observed (Supplemental Figure S6) In previous 399
studies of the regulation of plant volatile compounds MYBs have been characterized 400
as being involved mainly in the regulation of the benzenoidphenylpropanoid pathway 401
that produces floral volatiles in petunia and eugenol in ripe strawberry fruit (Verdonk 402
et al 2005 Dal Cin et al 2011 Colquhoun et al 2011 Spitzer-Rimon et al 2012 403
Medina-Puche et al 2015) but their role in formation of volatiles from other 404
pathways has not been reported Our study demonstrates a role for MYB in the 405
synthesis of furaneol a carbohydrate-derived volatile compound and reveals the 406
synergistic interactions between an MYB and ERF in a transcription complex (Figure 407
8 Figure 9 and Figure 10) 408
409
Recent research has provided evidence for interactions between AP2ERF and MYB 410
transcription factors in regulating other aspects of fruit quality including texture 411
(EjAP2-1 and EjMYB Zeng et al 2015) and colour (PyERF3 and PyMYB114 Yao 412
et al 2017) A group VIII ERF has also recently been shown to interact with an MYB 413
to regulate floral scent production in petunia (Liu et al 2017) In strawberry fruit 414
DOF in combination with an MYB has been reported to be involved in the regulation 415
of eugenol production and the identification of this second transcription factor (DOF) 416
suggests that it is a good target in breeding for improved flavour (Molina-Hidalgo et 417
al 2017 Tieman 2017) Considering its important contribution to flavour in 418
strawberry and many other highly valued fruit crop species (pineapple tomato mango 419
etc) very little is known about regulation of furaneol synthesis Here we established 420
the role of FaERF9 in the regulation of HDMF synthesis by direct protein-protein 421
interactions with FaMYB98 to synergistically trans-activate FaQR The functional 422
identification of this complex enhances our knowledge of the regulation of volatile 423
compound synthesis and identifies a new AP2ERF-MYB complex Further 424
examination of the other ERFs that stimulated transcription from the FaQR promoter 425
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16
(Figure 2) may provide additional information about the complexity of this regulation 426
Overall this study provides important clues for understanding the transcriptional 427
regulation of HDMF synthesis and identifies specific transcription factors that are 428
likely to be good targets for molecular breeding for improved flavour 429
430
Conclusions 431
Screening of the AP2ERF superfamily in strawberry (Fragaria times ananassa) 432
identified candidate members capable of activating the FaQR promoter An ERF 433
transcription factor was identified as a positive regulator of HDMF synthesis in 434
strawberry fruit and the mechanism of activation was shown to involve an ERF-MYB 435
transcription complex that regulates transcription of FaQR leading to the biosynthesis 436
of HDMF the characteristic volatile compound which has a major influence on 437
strawberry aroma 438
439
Materials and Methods 440
441
Plant Materials and Growth conditions 442
The strawberry (Fragaria times ananassa cv lsquoYuexinrsquo an octoploid cultivar) fruit used in 443
this study were bred by Zhejiang Academy of Agricultural Sciences (Haining 444
Zhejiang) Fruits at various developmental and ripening stages including G (green) T 445
(turning) IR (intermediate red) and R (full red) were harvested (Figure 1) and 446
transported to the laboratory within 2 h Thirty-six fruits of uniform size and free of 447
visible defects were selected at each stage with twelve fruits in each biological 448
replicate After removing the calyces fruits were then divided into the basal and 449
apical sections which were sampled separately (Figure 1) They were rapidly cut into 450
pieces frozen immediately in liquid nitrogen and stored at -80deg C until use Red ripe 451
fruits of different strawberry cultivars (Fragaria times ananassa octoploid cultivars) 452
including lsquoYuelirsquo lsquoBenihoppersquo lsquoMengxiangrsquo lsquoAmaoursquo lsquo10-1-4rsquo lsquoAkihimersquo lsquoSweet 453
Charliersquo lsquo07-1-4rsquo lsquoDarselectrsquo lsquoYuexinrsquo and lsquoXuemeirsquo were also provided by Zhejiang 454
Academy of Agricultural Sciences For each cultivar the fruits of three biological 455
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17
replicates were sampled frozen in liquid nitrogen and stored at -80deg C for further use 456
457
Tobacco plants (Nicotiana benthamiana) used for dual-luciferase assays and 458
subcellular localization analysis in this study were grown in a growth chamber with a 459
lightdark cycle of 16 h8 h at 24degC 460
461
Detection of DMMF and HDMF 462
Automated HS-SPME-GC-MS was performed to detect both furanones in lsquoYuexinrsquo 463
strawberry fruit (Zorrilla-Fontanesi et al 2012) Samples were ground into a powder 464
under liquid nitrogen for analysis 465
466
For the detection of DMMF (Figure 1) 05 g (fresh weight) of each sample was 467
weighed in the vial to which was added 1 mL of EDTA solution (100 mM pH 75) 1 468
mL of CaCl2 solution (mv = 20) and 20 microL of 2-octanol as the internal standard 469
(007 μgμL) The mixture was homogenized and the vial closed and placed on the 470
sample tray for analysis by CombiPAL autosampler (CTC Analytic CA USA) The 471
fruit volatiles were sampled by headspace solid-phase microextraction with a 65-μm 472
polydimethylsiloxane-divinylbenzene fibre (PDMS-DVB) Initially vials were 473
pre-incubated at 50degC for 10 min under continuous agitation (500 rpm) then volatiles 474
were extracted for 30 min at the same temperature and agitation speed After that the 475
fibre was desorbed in the GC injection port for 5 min in splitless mode The 7890A 476
GC chromatograph was equipped with a DB-5ms column (60 m times 250 μm times 1 μm 477
JampW Scientific Folsom CA USA) with helium as the carrier gas at a constant flow 478
of 12 mLmin The GC was programmed at an initial temperature of 35degC for 2 min 479
with a ramp of 5degC min up to 250degC and held for 5 min The injection port interface 480
and MS source temperatures were 250degC 260degC and 230degC respectively The 481
ionization potential was set at 70 eV recorded by a 5975B mass spectrometer (Agilent 482
Technologies JampW Scientific Folsom CA USA) and the scanning speed was 7 483
scanss The same method was used to analyse HDMF and DMMF in fruits from 484
different cultivars (Supplemental Figure S3) except for the sample preparation 485
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18
procedure (Araguumlez et al 2013) briefly 05 g (fresh weight) of powdered fruit was 486
incubated at 30degC in a water bath for 5 min then 2 mL of NaCl (mv = 20) and 20 487
microL of 2-octanol as the internal standard (007 μgμL) were added and homogenized 488
489
For the detection of HDMF (Figure 1) and both furanones (Figure 4 and Supplemental 490
Table S3) a liquid-injection system equipped with CTC Pal ALS was used One gram 491
(fresh weight) of powdered fruit and 2 mL of NaCl (mv = 20) were homogenized in 492
a 10-mL tube and 300 μL of CH2Cl2 and 20 microL of 2-octanol (0766 μgμL) as the 493
internal standard were added to extract the volatiles the mixture was then 494
homogenized again The tubes were stored at room temperature for 20 min and 495
centrifuged at 12000 rpm for 5 min The subnatant was pipetted into a clean 15-mL 496
tube in which 20 mg of anhydrous sodium sulphate was added the tube was left 497
without shaking for half an hour Then 150 μL of the solution was transferred into a 498
GC vial and placed on the sample tray as described above Each sample (1 μL) was 499
injected using the autosampler and the analysis was accomplished by a 7890A 500
GC-MS system (Agilent Technologies JampW Scientific Folsom CA USA) equipped 501
with a DB-WAX column (30 m times 025 mm times 025 μm JampW) Helium (12 mLmin) 502
was used as a carrier gas The injection port (splitless injection mode) interface and 503
MS source temperatures were as described above The oven temperature was set at 504
60degC for 4 min then increased to 180degC at a rate of 4degCmin and maintained for 30 505
min DMMF was identified by comparison of electron ionization mass spectra and 506
retention time data with the data from the NISTEPANIH mass spectral library 507
(NIST-08 and Flavor) HDMF (Figure 1) was identified and qualified by comparison 508
with injected standard (Sigma) The quantitative analysis of both furanones (Figure 4 509
Supplemental Table S3 and Supplemental Figure S3) was determined using the peak 510
area of the internal standard as a reference based on total ion chromatogram (TIC) 511
512
RNA isolation and Reverse Transcription Quantitative PCR (RT-qPCR) 513
Total RNA from strawberry samples was isolated in this study using the CTAB 514
method (Chang et al 1993) Genomic DNA contamination was eliminated by 515
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
19
TURBO Dnase (Ambion) 1 μg of RNA was used to obtain cDNA using an IScriptTM 516
cDNA Synthesis Kit (Bio-Rad) The synthesized cDNA was diluted with water (120) 517
and 2 μL of diluted cDNA was used as the template for RT-qPCR Reactions were 518
performed in a total volume of 20 μL consisting of 10 μL of SYBR PCR supermix 519
(Bio-Rad) 1 μL of each primer (10 μM) 6 μL of DEPC-H2O and 2 μL of diluted 520
cDNA on CFX96 instrument (Bio-Rad) (Yin et al 2012) The oligonucleotide 521
primers for RT-qPCR analysis of genes including the AP2ERF FaQR and FaOMT 522
were designed according to the coding sequences of genes and the specificity was 523
verified before use (Min et al 2012) NCBIPrimer-BLAST was applied to design the 524
primers Relative expression levels were normalized to that of an internal controlmdashthe 525
interspacer 26S-18S strawberry RNA housekeeping gene FaRIB413 526
(Zorrilla-Fontanesi et al 2012) To investigate the differential expression of genes 527
during fruit development and ripening stages relative expression of each gene at the 528
R stage in the basal fruit section was set as 1 using the 2minus∆∆119862119879 method For transient 529
overexpression assay relative expression of control fruits with an empty vector (SK) 530
was set as 1 The primers used in RT-qPCR are listed in Supplemental Table S4 531
532
Gene isolation and analysis 533
Multiple database searches were performed to identify members of the strawberry 534
(Fragaria times ananassa) AP2ERF superfamily in the published strawberry databases 535
and annotations of Fragaria times ananassa and Fragaria times vesca by using the 536
AP2ERF DNA binding domain as a query sequence and 120 genes were identified 537
with AP2ERF domain(s) Based on the BLAST result primers (listed in 538
Supplemental Table S5) were used to amplify the coding full-length cDNAs of 539
AP2ERF genes The deduced amino acid sequences of AP2ERF proteins in 540
Arabidopsis thaliana used for construction of a phylogenetic tree were obtained from 541
the Arabidopsis Information Resource (TAIR) Alignment of the proteins was 542
performed using the neighbour-joining method in ClustalX (v181) and the 543
phylogenetic tree was constructed using FigTree (v131) 544
545
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
20
FaMYB98 was obtained by yeast one-hybrid screening sequencing and the full-length 546
sequences were predicted by BLAST Primers were designed (listed in Supplemental 547
Table S5) to amplify the full-length coding sequence 548
549
The promoter of FaQR was cloned by Genome Walking as previously described (Yin 550
et al 2010) and conserved cis-element motifs in the promoter were manually 551
searched 552
553
Conserved domains within the FaAP2ERF proteins and FaMYB98 were analysed by 554
CD-search (httpswwwncbinlmnihgovStructurecddwrpsbcgi) and cellular 555
locations of proteins including FaERF9 and FaMYB98 were predicted with the 556
WoLF PSORT program (httpswwwgenscriptcomwolf-psorthtml) 557
558
Dual-Luciferase Assays 559
In accordance with a previous protocol (Yin et al 2010) the full-length cDNAs of 560
FaAP2ERF or FaMYB98 transcription factors were cloned into pGreen II 0029 561
62-SK vector and the promoter of FaQR was cloned into pGreen II 0800-LUC vector 562
A luciferase gene from Renillia (REN) driven by a 35S promoter in the LUC vector 563
acted as a positive control The above constructs were transiently expressed in 564
Nicotiana benthamiana leaves by Agrobacterium-mediated infiltration (strain 565
GV3101) and the activity of the TFs on the promoter was measured on the third day 566
after infiltration indicated by the ratio of enzyme activities of firefly luciferase (LUC) 567
and renilla luciferase (REN) using a Modulus Luminometer (Promega Madison WI 568
USA) To determine the activity of a specific transcription factor towards the 569
promoter we mixed the Agrobacterium culture with 1 mL of TF and 100 μL of 570
promoter and the LUCREN value of the empty vector SK on the promoter was set as 571
1 as a calibrator To test the combined effect of two transcription factors on the 572
promoter to the Agrobacterium culture mixture we added 05 mL of each TF and 100 573
μL of promoter the effect of the mixtures that contained each transcription factor (05 574
mL) and empty vector SK (05 mL) was also tested on the promoter as a control 575
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
21
576
Subcellular localization analysis 577
35S-FaERF9-GFP and 35S-FaMYB98-GFP were transiently expressed in tobacco (N 578
benthamiana) leaves by Agrobacterium infiltration (EHA105) using the same method 579
as described in the dual-luciferase assay above The transiently infected leaves were 580
imaged on the third day after infiltration using a Nikon A1-SHS confocal laser 581
scanning microscope The excitation wavelength for GFP fluorescence was 488 nm 582
and fluorescence was detected at 490ndash520 nm The primers used for GFP construction 583
are listed in Supplemental Table S6 584
585
Transient overexpression in strawberry fruit 586
Transient overexpression of FaERF9 and an overexpression binary vector (pGreen II 587
0029 62-SK-FaERF9-FaMYB98) were performed in strawberry fruit using the 588
FaERF9-SK construct described above for the dual-luciferase assays and the binary 589
vector constructed according to Liu et al 2013 The transfection of fruit was carried 590
out at the G stage (Hoffmann et al 2006) The FaERF9-SK construct and binary 591
vector were individually electroporated into Agrobacterium tumefaciens GV3101 and 592
the Agrobacterium culture suspended in infiltration buffer was infiltrated into the 593
whole fruit using a syringe As a control treatment fruits were infiltrated with 594
Agrobacterium carrying an empty vector SK under the same transfection conditions 595
Fruits were left attached to the plants and harvested on the seventh day after 596
infiltration Fruits of three biological replicates were sampled for further analysis 597
598
Yeast one-hybrid assay 599
In order to identify proteins that bind to the FaQR promoter the Matchmaker Gold 600
Yeast One-hybrid Library Screening System (Clontech USA) was used The sequence 601
of the FaQR promoter was cloned into the pAbAi vector and the construct was 602
integrated into the genome of the Y1HGold yeast strain A mixture of total RNA from 603
strawberry fruit at four stages (G T IR R) was used to construct the prey cDNA 604
library (TaKaRa) The background AbAr expression of Y1HGold FaQR-pAbAi strain 605
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
22
was tested according to the system user manual and then screening for protein-DNA 606
interactions was carried out Furthermore the full length of each transcription factor 607
was separately cloned into pGADT7 AD vector to confirm the screening results The 608
relationship between FaERF9 and FaQR promoter was also examined individually 609
Primers used in this assay are listed in Supplemental Table S6 610
611
Expression and purification of FaMYB98 recombinant protein 612
A 405-bp region spanning the DNA-binding domain of FaMYB98 was amplified 613
from FaMYB98 cDNA and cloned into a pET6timesHN vector (Clontech Palo CA USA) 614
to generate the recombinant N-terminal His-tagged protein the primers used are listed 615
in Supplemental Table S6 The resulting construct was sequenced and introduced into 616
Escherichia coli strain Rosetta 2(DE3)pLysS (Novagen) Ten millilitres of the 617
overnight culture was combined with 500 mL of an LB liquid medium (100 μgmL 618
ampicillin and 34 μgmL chloramphenicol) as described (Li et al 2017) Isopropyl 619
β-D-1-thiogalactopyranoside (IPTG) was added to a final concentration of 1 mM and 620
the bacterial culture was incubated at 18degC at 150 rpm for 18 h Then the cells were 621
harvested using a centrifuge and resuspended in 1times PBS buffer (Sangon Biotech) 622
after which they were disrupted by sonication and the supernatant was purified using 623
a HisTALONTM Gravity Column (Clontech) according to the user manual The PD-10 624
Desalting column (GE Healthcare) was then used for buffer change and sample 625
clean-up of proteins according to the gravity protocol SDS-PAGE was performed and 626
the protein was visualized using Coomassie brilliant blue 627
628
Electrophoretic mobility shift assay (EMSA) 629
A Lightshift Chemiluminescent EMSA kit (Thermo) was used to perform EMSA 630
experiments according to the manufacturerrsquos instructions Single-strand 631
oligonucleotides were synthesized and biotinylated by GeneBio Biotech (Hangzhou 632
China) The details of the EMSA assay are provided in Ge et al (2017) The probes 633
used for EMSAs are listed in Supplemental Table S6 634
635
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
23
636
Yeast two-hybrid assay 637
The DUALhunter system (Dualsystems Biotech Switzerland) was used to investigate 638
the interaction between FaERF9 and FaMYB98 Full-length coding sequences of 639
FaERF9 and FaMYB98 were respectively cloned into pDHB1 bait vector and 640
pPR3-N prey vector sequences were verified and the bait plasmid was 641
co-transformed with prey plasmid into NMY51 in the combinations below 642
FaMYB98-pDHB1pPR3-N FaMYB98-pDHB1FaERF9-pPR3-N 643
FaMYB98-pDHB1pOst1-NubI FaERF9-pDHB1pPR3-N 644
FaERF9-pDHB1FaMYB98-pPR3-N and FaERF9-pDHB1pOst1-NubI (Li et al 645
2017) Transformed cells were spread onto the following plates DDO (SD 646
medium-Trp-Leu) QDO (SD medium-Trp-Leu-His-Ade) and QDO+3-AT (QDO 647
medium supplemented with 1 mM 3-amino-124-triazole) The control plasmid 648
pOst1-NubI was used to determine whether the bait was functional the pPR3-N prey 649
vector plasmid was used to test whether the bait displayed non-specific background 650
and positive interactions were indicated by the growth of yeast on QDO and 651
QDO+3-AT plates The Primers used in the DUALhunter assay are listed in 652
Supplemental Table S6 653
654
Bimolecular fluorescence complementation (BiFC) assays 655
Full-length FaERF9 and FaMYB98 respectively were cloned into sequences 656
encoding the N- and C- fragments of YFP protein (Lv et al 2014) All constructs 657
were transiently expressed in tobacco (N benthamiana) leaves by Agrobacterium 658
infiltration (EHA105) The YFP fluorescence of transfected leaves was imaged 40 h 659
after infiltration by using a Nikon A1-SHS confocal laser scanning microscope The 660
excitation wavelength for YFP was 488 nm and fluorescence was detected at 520ndash661
540 nm Primers used are listed in Supplemental Table S6 662
663
Statistics 664
A Studentrsquos two-tailed t test ( plt005 plt001 and plt0001) was used to 665
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
24
determine significant differences between two groups in this study Microsoft Excel 666
was used to perform linear regressive analysis significant differences were 667
determined by SPSS Statistics 200 and scatter plots were prepared with Origin80 668
Least significant difference (LSD) at the 5 level was calculated using Microsoft 669
Excel Figures were prepared with Origin80 (Microcal Software Inc Northampton 670
MA USA) The online tool MetaboAnalyst 36 (httpwwwmetaboanalystca) was 671
used to analyse the transcript abundance of the AP2ERF genes 672
673
Accession numbers 674
Sequence data from this article have been deposited in GenBank under the accession 675
numbers MH332903-MH333022 for AP2ERF genes in Fragaria times ananassa and 676
MH333023 for FaMYB98 GenBank numbers for FaQR and FaOMT were 677
AY1588361 (Raab et al 2006) and AF2204912 (Wein et al 2002) 678
679
Supplemental Material 680
Supplemental Figure S1 Phylogenetic analysis of FaAP2ERF and Arabidopsis 681
AP2ERF proteins 682
Supplemental Figure S2 Analysis of FaAP2ERF gene expression patterns in 683
strawberry fruit during development and ripening 684
Supplemental Figure S3 Contents of furanones in fruit of strawberry cultivars 685
Supplemental Figure S4 Relative expression of FaERF9 in FaERF9-FaMYB98- 686
and FaERF9-overexpressing fruits 687
Supplemental Figure S5 Subcellular localization of FaMYB98 688
Supplemental Figure S6 The combined activation effects of FaERF9FaMYB98 on 689
the FaOMT promoter 690
Supplemental Figure S7 Relative expression of FaOMT in 691
FaERF9-overexpressing fruits 692
Supplemental Table S1 AP2ERF superfamily genes in Fragaria times ananassa 693
Supplemental Table S2 Classification of the AP2ERF superfamily members in 694
Fragaria times ananassa 695
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
25
Supplemental Table S3 Furanone content in FaERF9-FaMYB98- and 696
FaERF9-overexpressing fruits 697
Supplemental Table S4 Primers used for reverse transcription quantitative PCR 698
(RT-qPCR) 699
Supplemental Table S5 Primers used to amplify the full-length coding sequences of 700
AP2ERF genes and FaMYB98 in strawberry (Fragaria times ananassa) 701
Supplemental Table S6 Primers used for vector construction 702
703
Acknowledgments 704
This research was supported by the National Key Research and Development 705
Program (2016YFD0400101) the Project of the Science and Technology Department 706
of Zhejiang Province (2016C04001) and the 111 Project (B17039) 707
708
Figure legends 709
Figure 1 Changes in furanone content and furanone biosynthetic genes during 710
strawberry (Fragaria times ananassa Duch cv Yuexin) fruit development and ripening 711
A Fruits were collected at four ripening stages G (green stage) T (turning stage) IR 712
(intermediate red stage) R (full red stage) B Changes in the contents of furaneol 713
(HDMF) and mesifurane (DMMF) HDMF content was calculated using a standard 714
curve of HDMF while DMMF content was calculated with an internal standard as the 715
reference C Expression levels of FaQR and FaOMT The expression levels of each 716
gene were calculated relative to corresponding values in the basal section at the R 717
stage SEs were calculated from three replicates and LSD values represent the least 718
significant differences at p = 005 719
Figure 2 Regulatory effects of FaAP2ERF on the promoter of FaQR LUCREN 720
values of the empty vector on FaQR promoter were used as the calibrator set as 1 721
and SEs were calculated from five replicates statistical significance was determined 722
by Studentrsquos two-tailed t test ( plt0001) 723
Figure 3 Expression and the subcellular localization of FaERF9 A The expression 724
levels were calculated relative to the levels in the basal section at the R stage B 725
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
26
Subcellular localization analysis was performed in tobacco leaves The tobacco used 726
in the assay was stably transformed with a specific nucleus localized red fluorescence 727
protein construct and the red fluorescence indicates the nucleus-localized signal 728
(NLS) Scale bar = 25 microm SEs were calculated from three replicates 729
Figure 4 Transient overexpression of FaERF9 in strawberry fruit A Relative 730
expression of FaQR and FaERF9 in FaERF9-OX fruit 7 days after infiltration The 731
expression was calculated relative to the average value in control (SK) fruits B 732
HDMF and DMMF content in FaERF9-OX fruit The content of both furanones 733
were quantified using the peak area of the internal standard (2-octanol) as the 734
reference SEs were calculated from three replicates Statistical significance was 735
determined by Studentrsquos two-tailed t test ( plt005 plt001 plt0001) 736
Figure 5 Scatter plots of 11 strawberry cultivars A Linear regression analysis 737
between FaERF9 expression and FaQR expression B Linear regression analysis 738
between FaERF9 expression and furanone content The relative expression was 739
normalized to that of the housekeeping gene FaRIB413 and furanone content was 740
calculated with internal standard as the reference Significant differences were 741
determined by SPSS Statistics 200 742
Figure 6 Interactions of FaERF9 and FaMYB98 with the FaQR promoter A Yeast 743
one-hybrid analysis of the interaction of FaERF9 and FaQR promoter B Yeast 744
one-hybrid analysis of the interaction of FaMYB98 and FaQR promoter C 745
Regulatory effect of FaMYB98 on the FaQR promoter Auto-activation was tested on 746
SD-Ura (synthetically defined medium without uracil) in presence of Aureobasidin A 747
(AbA) and physical interaction was determined on SD-Leu (synthetically defined 748
medium without leucine) in presence of AbA LUCREN values of the empty vector 749
on FaQR promoter were used as the calibrator set as 1 and error bars were calculated 750
from five replicates Statistical significance was determined by Studentrsquos two-tailed t 751
test ( plt005 plt001 plt0001) 752
Figure 7 Electrophoretic mobility shift assay of FaMYB98 binding to FaQR 753
promoter A The probe sequence used for EMSA and mutated nucleotides are 754
indicated with lowercase letters B Purified DNA-binding domain of FaMYB98 755
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
27
protein and biotin-labelled DNA probe were mixed and analysed on 6 native 756
polyacrylamide gels and then photographed Presence or absence of specific probes is 757
marked by the symbol + or - 758
Figure 8 The combined activation effects of FaERF9FaMYB98 on the FaQR 759
promoter LUCREN values obtained with the empty vector and FaQR promoter were 760
used as the calibrator set as 1 and error bars were calculated from five replicates 761
Figure 9 Yeast two-hybrid analysis of the protein-protein interactions between 762
FaMYB98 and FaERF9 Positive interactions were determined by the growth of 763
yeast cells on selection plates Bait with pOST acted as positive controls and bait with 764
pPR3 as negative controls DDO synthetically defined medium without tryptophan 765
and leucine QDO synthetically defined medium without tryptophan leucine 766
histidine and adenine QDO+3AT QDO medium supplemented with 1 mM 767
3-aminotriazole 768
Figure 10 BiFC analysis of the protein-protein interactions between FaMYB98 and 769
FaERF9 The pairs of fusion proteins tested were FaMYB98-YFPN+FaERF9-YFPC 770
FaERF9-YFPN+FaMYB98-YFPC FaMYB98-YFPN+FaMYB98-YFPC and 771
FaERF9-YFPN+FaERF9-YFPC The other combinations were negative controls 772
The tobacco used in the assay was stably transformed with a specific 773
nucleus-localized red fluorescence protein construct and the red fluorescence 774
indicated the nucleus-localized signal (NLS) Fluorescence of the yellow fluorescence 775
protein (YFP) visualized the interaction in vivo Scale bar = 25 microm 776
777
Literature Cited 778
779
Agarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression 780
of PgDREB2A transcription factor enhances abiotic stress tolerance and activates 781
downstream stress-responsive genes Mol Biol Rep 37 1125-1135 782
Araguumlez I Osorio S Hoffmann T Rambla JL Medina-Escobar N Granell A 783
Botella MAacute Schwab W Valpuesta V (2013) Eugenol production in achenes and 784
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
28
receptacles of strawberry fruits is catalyzed by synthases exhibiting distinct kinetics 785
Plant Physiol 163 946-958 786
Carvalho RF Carvalho SD OrsquoGrady K Folta KM (2016) Agroinfiltration of 787
strawberry fruit mdash a powerful transient expression system for gene validation Curr 788
Plant Biol 6 19-37 789
Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic 790
(Amsterdam) 210 34-40 791
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating 792
RNA from pine trees Plant Mol Biol Rep 11 113-116 793
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC 794
Clark DG (2011) PhMYB4 fine-tunes the floral volatile signature of 795
Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143 796
Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz 797
EA Taylor MG Smits-Kroon MT Schuurink RC Haring MA Giovannoni J 798
Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic 799
pathway by ectopic expression of a MYB transcription factor in tomato fruit Plant 800
Cell 23 2738-2753 801
Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan 802
XW Yang ZY (2017) Differential responses of four biosynthetic pathways of 803
aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under 804
interaction of light and temperature Food Chem 221 356-364 805
Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of 806
differentially-expressed genes during somatic embryogenesis in Fragaria times 807
ananassa Duch lsquoBenihopprsquo J Hortic Sci Biotechnol 90 671-681 808
Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 809
transcriptionally regulates chilling-induced lignification of loquat fruit via physical 810
interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136 811
Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM 812
(2004) Functional interactions between a glutamine synthetase promoter and MYB 813
proteins Plant J 39 513-526 814
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
29
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) 815
Sucrose nonfermenting1-related protein kinase26 an ortholog of open stomata1 is 816
a negative regulator of strawberry fruit development and ripening Plant Physiol 817
167 915-930 818
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene 819
expression in strawberry fruit (Fragaria times ananassa) by agroinfiltration a rapid 820
assay for gene function analysis Plant J 48 818-826 821
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of 822
selected aroma-active compounds in strawberries by headspace solid-phase 823
microextraction gas chromatography and correlation with sensory descriptive 824
analysis J Food Sci 72 S487-S496 825
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid 826
plays an important role in the regulation of strawberry fruit ripening Plant Physiol 827
157 188-199 828
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of 829
NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes BMC 830
Plant Biol 6 20 831
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN 832
(2005) MYB98 is required for pollen tube guidance and synergid cell differentiation 833
in Arabidopsis Plant Cell 17 2981-2992 834
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional 835
characterization of enone oxidoreductases from strawberry and tomato fruit J 836
Agric Food Chem 55 6705-6711 837
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You 838
J-S Rohloff J Randall SK Alsheikh M (2012) Proteomic study of 839
low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ 840
in cold tolerance Plant Physiol 159 1787-1805 841
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional 842
characterization of four APETALA2-family genes (RAP26 RAP26L DREB19 843
and DREB26) in Arabidopsis Plant Mol Biol 75 107-127 844
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
30
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon 845
J Gupta V (2013) An oxidoreductase from lsquoAlphonsorsquo mango catalyzing 846
biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494 847
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in 848
strawberries Z Lebensm-Unters Forsch 195 120-123 849
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X 850
(2015) Label-free quantitative proteomics to investigate strawberry fruit proteome 851
changes under controlled atmosphere and low temperature storage J Proteomics 852
120 44-57 853
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 854
cooperates with CitWRKY1 to participate in citric acid degradation via 855
up-regulation of CitAco3 J Exp Bot 68 3419-3426 856
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription 857
factor CitERF71 activates the terpene synthase gene CitTPS16 involved in the 858
synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938 859
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and 860
transcriptomic analysis of the AP2ERF superfamily in Vitis vinifera BMC 861
Genomics 11 719 862
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive 863
Factor (AP2ERF) transcription factors mediators of stress responses and 864
developmental programs New Phytol 199 639-649 865
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 866
interacting with EOBI negatively regulates fragrance biosynthesis in petunia 867
flowers New Phytol 215 1490-1502 868
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu 869
CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 in regulating 870
anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) 871
during anthocyanin biosynthesis Plant Cell Tissue Organ Cult 115 285-298 872
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
31
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao 873
CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphate signaling and 874
homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597 875
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC 876
Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL 877
Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor 878
regulates eugenol production in ripe strawberry fruit receptacles Plant Physiol 168 879
598-614 880
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics 881
and volatile constituents of strawberry (cv Cigaline) during maturation J Agric 882
Food Chem 52 1248-1254 883
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS 884
(2012) Ethylene-responsive transcription factors interact with promoters of ADH 885
and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 886
63 6393-6405 887
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM 888
Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-Franco A 889
Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific 890
transcription factor FaDOF2 regulates the production of eugenol in ripe fruit 891
receptacles J Exp Bot 68 4529-4543 892
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) 893
Comparison and verification of the genes involved in ethylene biosynthesis and 894
signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44 895
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the 896
ERF gene family in Arabidopsis and rice Plant Physiol 140 411-432 897
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in 898
sour cherry and strawberry and the heterologous expression of CBF1 in strawberry 899
J Am Soc Hortic Sci 127 489-494 900
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech 901
JC Ohme-Takagi M Regad F Bouzayen M (2012) Functional analysis and 902
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32
binding affinity of tomato ethylene response factors provide insight on the 903
molecular bases of plant differential responses to ethylene BMC Plant Biol 12 190 904
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) 905
Methylpentoses are possible precursors of furanones in fruits Prikl Biokhim 906
Mikrobiol 28 123-127 907
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery 908
of synergid-expressed genes encoding filiform apparatus localized proteins Plant 909
Cell 19 2557-2568 910
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria 911
vesca L compared to those of cultivated berries Fragariatimes ananassa cv Senga 912
Sengana J Agric Food Chem 27 19-22 913
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W 914
Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of the strawberry 915
flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone 916
oxidoreductase Plant Cell 18 1023-1037 917
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L 918
Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim M Broun P Zhang 919
JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription 920
factors genome-wide comparative analysis among eukaryotes Science 290 921
2105-2110 922
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the 923
formation of 25-dimethyl-4-hydroxy-3(2H)-furanone in detached ripening 924
strawberry fruits J Agric Food Chem 46 1488-1493 925
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 926
25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in 927
strawberry fruits Phytochemistry 43 155-159 928
Schwab W (1998) Application of stable isotope ratio analysis explaining the 929
bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone in plants by a biological 930
maillard reaction J Agric Food Chem 46 2266ndash2269 931
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33
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) 932
Molecules 18 6936-6951 933
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard 934
products Recent Res Dev Phytochem 1 643-673 935
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL 936
Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJ Sims CA 937
Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical 938
compositions a seasonal influence and effects on sensory perception PLoS One 9 939
e88446 940
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) 941
Identification phylogeny and transcript profiling of ERF family genes during 942
development and abiotic stress treatments in tomato Mol Genet Genomics 284 943
455-475 944
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) 945
CitAP210 activation of the terpene synthase CsTPS1 is associated with the 946
synthesis of (+)-valencene in lsquoNewhallrsquo orange J Exp Bot 67 4105-4115 947
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes 948
Dev Genes Evol 214 105-114 949
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K 950
Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the 951
key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151 952
Spitzer-Rimon B Farhi M Albo B Cnarsquoani A Ben Zvi MM Masci T Edelbaum 953
O Yu YX Shklarman E Ovadis M Vainstein A (2012) The R2R3-MYB-like 954
regulatory factor EOBI acting downstream of EOBII regulates scent production 955
by activating ODO1 and structural scent-related genes in petunia Plant Cell 24 956
5089-5105 957
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp 958
Bot 68 4407-4409 959
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla 960
JF Amaya I Giavalisco P Fernie AR Botella MA Valpuesta V (2015) Central 961
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34
role of FaGAMYB in the transition of the strawberry receptacle from development 962
to ripening New Phytol 208 482-496 963
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 964
regulates fragrance biosynthesis in petunia flowers Plant Cell 17 1612-1624 965
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS 966
(2018) The potassium channel FaTPK1 plays a critical role in fruit quality 967
formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748 968
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) 969
Isolation cloning and expression of a multifunctional O-methyltransferase capable 970
of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma 971
compounds in strawberry fruits Plant J 31 755-765 972
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor 973
types their evolutionary origin and species distribution In A handbook of 974
transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular 975
Biochemistry 52 25-73 976
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of 977
odor (Buettner A Ed) Springer Cham 9-10 978
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS 979
(2014) Isolation classification and transcription profiles of the AP2ERF 980
transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271 981
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in 982
regulation of fruit quality Crit Rev Plant Sci 35 120-130 983
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ 984
Zhang SL Wu J (2017) Map-based cloning of the pear gene MYB114 identifies an 985
interaction with other transcription factors to coordinately regulate fruit 986
anthocyanin biosynthesis Plant J 92 437-451 987
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes 988
involved in regulating fruit ripening Plant Physiol 153 1280-1292 989
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
35
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) 990
Expression of ethylene response genes during persimmon fruit astringency removal 991
Planta 235 895-906 992
Zabetakis I Gramshaw JW Robinson DS (1999) 993
25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis and 994
biosynthesis-a review Food Chem 65 139-151 995
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci 996
Food Agric 74 421-434 997
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 998
an AP2ERF gene is a novel regulator of fruit lignification induced by chilling 999
injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1000
1325-1334 1001
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation 1002
classification and transcription profiles of the Ethylene Response Factors (ERFs) in 1003
ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215 1004
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML 1005
(2012) Genome-wide analysis of the AP2ERF superfamily in peach (Prunus 1006
persica) Genet Mol Res 11 4788-4809 1007
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and 1008
expression analysis of a CRTDRE-binding factor gene FaCBF1 from Fragaria times 1009
ananassa Acta Hortic 41 240-248 1010
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The 1011
Arabidopsis AP2ERF transcription factor RAP26 participates in ABA salt and 1012
osmotic stress responses Gene 457 1-12 1013
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B 1014
Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) Genome-wide 1015
analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic 1016
(Amsterdam) 123 73-81 1017
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF 1018
Valpuesta V Botella MA Granell A Amaya I (2012) Genetic analysis of 1019
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
36
strawberry fruit aroma and identification of O-methyltransferase FaOMT as the 1020
locus controlling natural variation in mesifurane content Plant Physiol 159 1021
851-870 1022
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Parsed CitationsAgarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression of PgDREB2A transcription factor enhances abioticstress tolerance and activates downstream stress-responsive genes Mol Biol Rep 37 1125-1135
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Araguumlez I Osorio S Hoffmann T Rambla JL Medina-Escobar N Granell A Botella MAacute Schwab W Valpuesta V (2013) Eugenolproduction in achenes and receptacles of strawberry fruits is catalyzed by synthases exhibiting distinct kinetics Plant Physiol 163 946-958
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Carvalho RF Carvalho SD OGrady K Folta KM (2016) Agroinfiltration of strawberry fruit - a powerful transient expression system forgene validation Curr Plant Biol 6 19-37
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic (Amsterdam) 210 34-40Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating RNA from pine trees Plant Mol Biol Rep 11 113-116Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC Clark DG (2011) PhMYB4 fine-tunes the floral volatilesignature of Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz EA Taylor MG Smits-Kroon MT Schuurink RC HaringMA Giovannoni J Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic pathway by ectopic expression of aMYB transcription factor in tomato fruit Plant Cell 23 2738-2753
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan XW Yang ZY (2017) Differential responses of fourbiosynthetic pathways of aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under interaction of light andtemperature Food Chem 221 356-364
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of differentially-expressed genes during somatic embryogenesis inFragaria times ananassa Duch Benihopp J Hortic Sci Biotechnol 90 671-681
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 transcriptionally regulates chilling-induced lignification ofloquat fruit via physical interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM (2004) Functional interactions between a glutaminesynthetase promoter and MYB proteins Plant J 39 513-526
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) Sucrose nonfermenting1-related protein kinase26 anortholog of open stomata1 is a negative regulator of strawberry fruit development and ripening Plant Physiol 167 915-930
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene expression in strawberry fruit (Fragaria times ananassa) byagroinfiltration a rapid assay for gene function analysis Plant J 48 818-826
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of selected aroma-active compounds in strawberries byheadspace solid-phase microextraction gas chromatography and correlation with sensory descriptive analysis J Food Sci 72 S487-S496
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid plays an important role in the regulation of strawberry fruitripening Plant Physiol 157 188-199
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of NaCl-stressed Arabidopsis roots reveals novel classes ofresponsive genes BMC Plant Biol 6 20
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN (2005) MYB98 is required for pollen tube guidance andsynergid cell differentiation in Arabidopsis Plant Cell 17 2981-2992
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional characterization of enone oxidoreductases from strawberry andtomato fruit J Agric Food Chem 55 6705-6711
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You J-S Rohloff J Randall SK Alsheikh M (2012) Proteomicstudy of low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ in cold tolerance Plant Physiol 159 1787-1805
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional characterization of four APETALA2-family genes (RAP26 RAP26LDREB19 and DREB26) in Arabidopsis Plant Mol Biol 75 107-127
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon J Gupta V (2013) An oxidoreductase from Alphonsomango catalyzing biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
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methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma compounds in strawberry fruitsPlant J 31 755-765
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Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The Arabidopsis AP2ERF transcription factor RAP26 participatesin ABA salt and osmotic stress responses Gene 457 1-12
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Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Genome-wide analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic (Amsterdam) 123 73-81Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF Valpuesta V Botella MA Granell A Amaya I (2012) Geneticanalysis of strawberry fruit aroma and identification of O-methyltransferase FaOMT as the locus controlling natural variation inmesifurane content Plant Physiol 159 851-870
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wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
11
the FaQR promoter 276
277
In parallel with the investigation of the FaAP2ERF genes a cDNA library screening 278
was performed with a yeast one-hybrid assay using the promoter of FaQR as the bait 279
This screen identified several transcription factors that could physically bind to the 280
FaQR promoter but only one MYB could activate transcription from the FaQR 281
promoter (approximately 56-fold) relative to the control (Figure 6) in the 282
dual-luciferase assay This MYB showed 44 amino acid identity with MYB98 283
(GenBank ABA420611) a transcriptional regulator in the synergid cells in 284
Arabidopsis (Kasahara et al 2005) and it was designated as FaMYB98 The 285
specificity of FaMYB98 binding to the FaQR promoter was confirmed by EMSA 286
assay (Figure 7) and increasing the concentration of the cold probe reduced binding 287
In addition mutating the putative binding sites (Goacutemez-Maldonado et al 2004 288
Punwani et al 2007) as shown in Figure 7 eliminated FaMYB98 protein binding 289
When the combined effect of FaERF9 and FaMYB98 was analysed (Figure 8) a 290
synergistic 14-fold activation of the FaQR promoter was observed compared with the 291
activation by either FaERF9 or FaMYB98 which alone promoted transactivation 292
39-fold and 45-fold respectively In addition overexpression of both genes 293
(FaERF9-FaMYB98-SK) in strawberry fruits resulted in higher expression of 294
FaERF9 transcripts and higher furanone content than overexpression of FaERF9 295
(Supplemental Figure S4 Supplemental Table S3) Subcellular localization analysis 296
revealed that FaMYB98 was also localized in the nucleus (Supplemental Figure S5) 297
298
To investigate the potential interactions between FaERF9 and FaMYB98 the 299
DUALhunter system was used (Figure 9) Cells expressing the FaMYB98 and 300
FaERF9 protein pair using either FaMYB98 or FaERF9 as the bait grew on DDO 301
QDO and QDO supplemented with 1 mM 3-AT selective medium indicating 302
interaction between the two proteins This putative protein-protein interaction was 303
confirmed by BiFC assay and the combinations of FaMYB98-YFPNFaERF9-YFPC 304
and FaERF9-YFPNFaMYB98-YFPC exhibited strong coincident signals in the 305
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
12
nucleus while negative controls produced no detectable fluorescence signal (Figure 306
10) In addition coexpression of FaERF9-YFPNFaERF9-YFPC as well as 307
FaMYB98-YFPNFaMYB98-YFPC also generated signals in the nucleus indicating 308
that FaERF9 and FaMYB98 both could form homodimers or possibly multimers in 309
the nucleus (Figure 10) 310
311
Discussion 312
The AP2ERF superfamily in strawberry 313
The AP2ERF superfamily of plant transcription factors is defined by the AP2ERF 314
domain and comprises the ERF AP2 and RAV families as well as one soloist member 315
(Riechmann et al 2000 Weirauch and Hughes 2011) The completion of multiple 316
plant genome sequences has enabled a genome-scale analysis of the AP2ERF family 317
which in recent years has been systematically studied in diverse fruit species such as 318
tomato grape peach and kiwi fruit (Zhuang et al 2009 Sharma et al 2010 Licausi 319
et al 2010 Yin et al 2010 Pirrello et al 2012 Zhang et al 2012 Zhang et al 320
2016) A few AP2ERF genes have been isolated and characterized in strawberry and 321
CBF orthologs (Owens et al 2002 Koehler et al 2012 Zhang et al 2014) have 322
been identified from different strawberry cultivars in several independent studies 323
Although they have distinct names eg Fragaria times ananassa CBF1 (FaCBF1) 324
FaCBF4 (GenBank HQ9105151) and CBF1 (GenBank EU1172142) according to 325
the phylogenetic tree generated in this study the orthologs of 326
CBF1CBF4CBF2CBF3 in Arabidopsis are similar to each other and to FaERF20 327
(Supplemental Figure S1) (Owens et al 2002 Koehler et al 2012 Zhang et al 328
2014) FaERF20 has 85 sequence similarity with FaCBF1 identified by Owens et 329
al (2002) 93 similarity with FaCBF4 amplified by Koehler et al (2012) and 75 330
similarity with CBF1 cloned by Zhang et al (2014) The AP2ERF genes 331
characterized in other studies (Jia et al 2011 GAO et al 2015 Chai and Shen 2016 332
Mu et al 2016) are also noted in Supplemental Table S1 333
334
Based on the computational analysis we have identified a total of 120 AP2ERF 335
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13
genes in octoploid strawberry (Supplemental Table S1) The number of predicted 336
AP2ERF genes (120) is comparable to those observed in other fruits including 337
tomato (112) Chinese plum (116) citrus (126) and peach (131) but lower than those 338
reported for grape (149) (Xie et al 2016) As shown in Supplemental Table S2 79 339
(95 genes) of the AP2ERF genes belong to the ERF family in strawberry constituting 340
the largest sub-family The members of this sub-family can be classified into 10 341
groups (group I to X) according to their sequence similarities to the Arabidopsis ERF 342
genes (Nakano et al 2006) The AP2 family encompasses the same number of genes 343
in Arabidopsis citrus and strawberry (eighteen) (Nakano et al 2006 Xie et al 2014) 344
and there are six RAV genes in strawberry which are highly conserved in dicots such 345
as Vitis vinifera Arabidopsis thaliana and Populus trichocarpa (Licausi et al 2010) 346
347
Role of FaERF9 in regulating the biosynthesis of HDMF a positive regulator 348
acting in an indirect manner 349
The large-scale screening of the AP2ERF superfamily in strawberry led to 350
identification of 11 ERFs and 1 RAV that trans-activated the FaQR promoter more 351
than two-fold with the highest activation caused by FaERF9 which trans-activated 352
the FaQR promoter (Figure 2) as well as up-regulating FaQR expression and furanone 353
production in transient overexpression assays (Figure 4) which has been extensively 354
used to explore the fruit-associated gene functions in strawberry (Han et al 2015 355
Medina-Puche et al 2015 Vallarino et al 2015 Carvalho et al 2016 Song et al 356
2016 Wang et al 2018) FaERF9 transcripts accumulate in the fruit apical section 357
before the basal section (Figure 3) a finding consistent with the actual changes in 358
furaneol content (Figure 1) and the expression of FaQR (Figure 1) The association 359
between FaERF9 transcripts and accumulation of furanones were also established 360
with different strawberry cultivars The correlation between FaERF9 and FaQR 361
expression as well as furanone content among cultivars supports a positive role of 362
FaERF9 in regulating furanone content (Figure 5) These results indicate that 363
FaERF9 transcript abundance may be a good indicator of the abundance of these 364
important flavour volatiles in fruits of different cultivars This should be considered as 365
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14
a method for high-throughput variety screening to replace direct measurement of 366
volatiles 367
368
FaERF9 is a member of the ERF group II family and is most closely related to the 369
Arabidopsis genes At1g44830 (ATERF014) At1g21910 (DREB26) and At1g77640 370
(Supplemental Figure S1) At1g44830 was observed to be strongly up-regulated in a 371
comprehensive microarray analysis of the root transcriptome following NaCl 372
exposure (Jiang and Deyholos 2006) At1g21910 (DREB26) was functionally 373
characterized as a trans-activator localized in the nucleus exhibiting tissue-specific 374
expression and participating in plant developmental processes as well as biotic andor 375
abiotic stress signalling (Krishnaswamy et al 2011) However none of these genes 376
have been reported as furanone regulators In strawberry another five genes 377
(FaERF6 FaERF7 FaERF8 FaERF10 and FaERF11) also belong to the same 378
group with FaERF8 also showing somewhat weaker activation activity towards the 379
FaQR promoter than FaERF9 The fact that FaERF9 could not bind directly to the 380
promoter of FaQR (Figure 6) indicates that it might function as an indirect regulator 381
of FaQR and furaneol biosynthesis 382
383
A FaERF9 and FaMYB98 complex is involved in regulating FaQR and furaneol 384
biosynthesis 385
The finding that FaERF9 could interact with FaMYB98 protein (Figures 9 and 386
Figure 10) and that FaMYB98 could physically bind to the FaQR promoter (Figure 6 387
and Figure 7) provides evidence for a regulatory mechanism whereby FaERF9 388
regulates FaQR and furaneol production as part of a complex with an MYB 389
transcription factor Since co-overexpression of FaERF9 and FaMYB98 resulted in 390
much higher activation activity towards FaQR we speculate that FaERF9 may 391
recruit FaMYB98 homologs in tobacco to activate the FaQR promoter (Figure 8) 392
FaOMT is another key gene for furanone biosynthesis and a potential target for 393
transcriptional activation However FaERF9 did not significantly activate the 394
FaOMT promoter in a dual-luciferase assay and the transcript level of FaOMT in the 395
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15
FaERF9-overexpressing fruits showed no significant difference from that in the 396
control (Supplemental Figure S6 Supplemental Figure S7) The FaOMT promoter 397
was significantly induced by FaMYB98 but no synergistic effect of FaERF9 and 398
FaMYB98 on the promoter was observed (Supplemental Figure S6) In previous 399
studies of the regulation of plant volatile compounds MYBs have been characterized 400
as being involved mainly in the regulation of the benzenoidphenylpropanoid pathway 401
that produces floral volatiles in petunia and eugenol in ripe strawberry fruit (Verdonk 402
et al 2005 Dal Cin et al 2011 Colquhoun et al 2011 Spitzer-Rimon et al 2012 403
Medina-Puche et al 2015) but their role in formation of volatiles from other 404
pathways has not been reported Our study demonstrates a role for MYB in the 405
synthesis of furaneol a carbohydrate-derived volatile compound and reveals the 406
synergistic interactions between an MYB and ERF in a transcription complex (Figure 407
8 Figure 9 and Figure 10) 408
409
Recent research has provided evidence for interactions between AP2ERF and MYB 410
transcription factors in regulating other aspects of fruit quality including texture 411
(EjAP2-1 and EjMYB Zeng et al 2015) and colour (PyERF3 and PyMYB114 Yao 412
et al 2017) A group VIII ERF has also recently been shown to interact with an MYB 413
to regulate floral scent production in petunia (Liu et al 2017) In strawberry fruit 414
DOF in combination with an MYB has been reported to be involved in the regulation 415
of eugenol production and the identification of this second transcription factor (DOF) 416
suggests that it is a good target in breeding for improved flavour (Molina-Hidalgo et 417
al 2017 Tieman 2017) Considering its important contribution to flavour in 418
strawberry and many other highly valued fruit crop species (pineapple tomato mango 419
etc) very little is known about regulation of furaneol synthesis Here we established 420
the role of FaERF9 in the regulation of HDMF synthesis by direct protein-protein 421
interactions with FaMYB98 to synergistically trans-activate FaQR The functional 422
identification of this complex enhances our knowledge of the regulation of volatile 423
compound synthesis and identifies a new AP2ERF-MYB complex Further 424
examination of the other ERFs that stimulated transcription from the FaQR promoter 425
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16
(Figure 2) may provide additional information about the complexity of this regulation 426
Overall this study provides important clues for understanding the transcriptional 427
regulation of HDMF synthesis and identifies specific transcription factors that are 428
likely to be good targets for molecular breeding for improved flavour 429
430
Conclusions 431
Screening of the AP2ERF superfamily in strawberry (Fragaria times ananassa) 432
identified candidate members capable of activating the FaQR promoter An ERF 433
transcription factor was identified as a positive regulator of HDMF synthesis in 434
strawberry fruit and the mechanism of activation was shown to involve an ERF-MYB 435
transcription complex that regulates transcription of FaQR leading to the biosynthesis 436
of HDMF the characteristic volatile compound which has a major influence on 437
strawberry aroma 438
439
Materials and Methods 440
441
Plant Materials and Growth conditions 442
The strawberry (Fragaria times ananassa cv lsquoYuexinrsquo an octoploid cultivar) fruit used in 443
this study were bred by Zhejiang Academy of Agricultural Sciences (Haining 444
Zhejiang) Fruits at various developmental and ripening stages including G (green) T 445
(turning) IR (intermediate red) and R (full red) were harvested (Figure 1) and 446
transported to the laboratory within 2 h Thirty-six fruits of uniform size and free of 447
visible defects were selected at each stage with twelve fruits in each biological 448
replicate After removing the calyces fruits were then divided into the basal and 449
apical sections which were sampled separately (Figure 1) They were rapidly cut into 450
pieces frozen immediately in liquid nitrogen and stored at -80deg C until use Red ripe 451
fruits of different strawberry cultivars (Fragaria times ananassa octoploid cultivars) 452
including lsquoYuelirsquo lsquoBenihoppersquo lsquoMengxiangrsquo lsquoAmaoursquo lsquo10-1-4rsquo lsquoAkihimersquo lsquoSweet 453
Charliersquo lsquo07-1-4rsquo lsquoDarselectrsquo lsquoYuexinrsquo and lsquoXuemeirsquo were also provided by Zhejiang 454
Academy of Agricultural Sciences For each cultivar the fruits of three biological 455
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17
replicates were sampled frozen in liquid nitrogen and stored at -80deg C for further use 456
457
Tobacco plants (Nicotiana benthamiana) used for dual-luciferase assays and 458
subcellular localization analysis in this study were grown in a growth chamber with a 459
lightdark cycle of 16 h8 h at 24degC 460
461
Detection of DMMF and HDMF 462
Automated HS-SPME-GC-MS was performed to detect both furanones in lsquoYuexinrsquo 463
strawberry fruit (Zorrilla-Fontanesi et al 2012) Samples were ground into a powder 464
under liquid nitrogen for analysis 465
466
For the detection of DMMF (Figure 1) 05 g (fresh weight) of each sample was 467
weighed in the vial to which was added 1 mL of EDTA solution (100 mM pH 75) 1 468
mL of CaCl2 solution (mv = 20) and 20 microL of 2-octanol as the internal standard 469
(007 μgμL) The mixture was homogenized and the vial closed and placed on the 470
sample tray for analysis by CombiPAL autosampler (CTC Analytic CA USA) The 471
fruit volatiles were sampled by headspace solid-phase microextraction with a 65-μm 472
polydimethylsiloxane-divinylbenzene fibre (PDMS-DVB) Initially vials were 473
pre-incubated at 50degC for 10 min under continuous agitation (500 rpm) then volatiles 474
were extracted for 30 min at the same temperature and agitation speed After that the 475
fibre was desorbed in the GC injection port for 5 min in splitless mode The 7890A 476
GC chromatograph was equipped with a DB-5ms column (60 m times 250 μm times 1 μm 477
JampW Scientific Folsom CA USA) with helium as the carrier gas at a constant flow 478
of 12 mLmin The GC was programmed at an initial temperature of 35degC for 2 min 479
with a ramp of 5degC min up to 250degC and held for 5 min The injection port interface 480
and MS source temperatures were 250degC 260degC and 230degC respectively The 481
ionization potential was set at 70 eV recorded by a 5975B mass spectrometer (Agilent 482
Technologies JampW Scientific Folsom CA USA) and the scanning speed was 7 483
scanss The same method was used to analyse HDMF and DMMF in fruits from 484
different cultivars (Supplemental Figure S3) except for the sample preparation 485
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18
procedure (Araguumlez et al 2013) briefly 05 g (fresh weight) of powdered fruit was 486
incubated at 30degC in a water bath for 5 min then 2 mL of NaCl (mv = 20) and 20 487
microL of 2-octanol as the internal standard (007 μgμL) were added and homogenized 488
489
For the detection of HDMF (Figure 1) and both furanones (Figure 4 and Supplemental 490
Table S3) a liquid-injection system equipped with CTC Pal ALS was used One gram 491
(fresh weight) of powdered fruit and 2 mL of NaCl (mv = 20) were homogenized in 492
a 10-mL tube and 300 μL of CH2Cl2 and 20 microL of 2-octanol (0766 μgμL) as the 493
internal standard were added to extract the volatiles the mixture was then 494
homogenized again The tubes were stored at room temperature for 20 min and 495
centrifuged at 12000 rpm for 5 min The subnatant was pipetted into a clean 15-mL 496
tube in which 20 mg of anhydrous sodium sulphate was added the tube was left 497
without shaking for half an hour Then 150 μL of the solution was transferred into a 498
GC vial and placed on the sample tray as described above Each sample (1 μL) was 499
injected using the autosampler and the analysis was accomplished by a 7890A 500
GC-MS system (Agilent Technologies JampW Scientific Folsom CA USA) equipped 501
with a DB-WAX column (30 m times 025 mm times 025 μm JampW) Helium (12 mLmin) 502
was used as a carrier gas The injection port (splitless injection mode) interface and 503
MS source temperatures were as described above The oven temperature was set at 504
60degC for 4 min then increased to 180degC at a rate of 4degCmin and maintained for 30 505
min DMMF was identified by comparison of electron ionization mass spectra and 506
retention time data with the data from the NISTEPANIH mass spectral library 507
(NIST-08 and Flavor) HDMF (Figure 1) was identified and qualified by comparison 508
with injected standard (Sigma) The quantitative analysis of both furanones (Figure 4 509
Supplemental Table S3 and Supplemental Figure S3) was determined using the peak 510
area of the internal standard as a reference based on total ion chromatogram (TIC) 511
512
RNA isolation and Reverse Transcription Quantitative PCR (RT-qPCR) 513
Total RNA from strawberry samples was isolated in this study using the CTAB 514
method (Chang et al 1993) Genomic DNA contamination was eliminated by 515
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
19
TURBO Dnase (Ambion) 1 μg of RNA was used to obtain cDNA using an IScriptTM 516
cDNA Synthesis Kit (Bio-Rad) The synthesized cDNA was diluted with water (120) 517
and 2 μL of diluted cDNA was used as the template for RT-qPCR Reactions were 518
performed in a total volume of 20 μL consisting of 10 μL of SYBR PCR supermix 519
(Bio-Rad) 1 μL of each primer (10 μM) 6 μL of DEPC-H2O and 2 μL of diluted 520
cDNA on CFX96 instrument (Bio-Rad) (Yin et al 2012) The oligonucleotide 521
primers for RT-qPCR analysis of genes including the AP2ERF FaQR and FaOMT 522
were designed according to the coding sequences of genes and the specificity was 523
verified before use (Min et al 2012) NCBIPrimer-BLAST was applied to design the 524
primers Relative expression levels were normalized to that of an internal controlmdashthe 525
interspacer 26S-18S strawberry RNA housekeeping gene FaRIB413 526
(Zorrilla-Fontanesi et al 2012) To investigate the differential expression of genes 527
during fruit development and ripening stages relative expression of each gene at the 528
R stage in the basal fruit section was set as 1 using the 2minus∆∆119862119879 method For transient 529
overexpression assay relative expression of control fruits with an empty vector (SK) 530
was set as 1 The primers used in RT-qPCR are listed in Supplemental Table S4 531
532
Gene isolation and analysis 533
Multiple database searches were performed to identify members of the strawberry 534
(Fragaria times ananassa) AP2ERF superfamily in the published strawberry databases 535
and annotations of Fragaria times ananassa and Fragaria times vesca by using the 536
AP2ERF DNA binding domain as a query sequence and 120 genes were identified 537
with AP2ERF domain(s) Based on the BLAST result primers (listed in 538
Supplemental Table S5) were used to amplify the coding full-length cDNAs of 539
AP2ERF genes The deduced amino acid sequences of AP2ERF proteins in 540
Arabidopsis thaliana used for construction of a phylogenetic tree were obtained from 541
the Arabidopsis Information Resource (TAIR) Alignment of the proteins was 542
performed using the neighbour-joining method in ClustalX (v181) and the 543
phylogenetic tree was constructed using FigTree (v131) 544
545
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
20
FaMYB98 was obtained by yeast one-hybrid screening sequencing and the full-length 546
sequences were predicted by BLAST Primers were designed (listed in Supplemental 547
Table S5) to amplify the full-length coding sequence 548
549
The promoter of FaQR was cloned by Genome Walking as previously described (Yin 550
et al 2010) and conserved cis-element motifs in the promoter were manually 551
searched 552
553
Conserved domains within the FaAP2ERF proteins and FaMYB98 were analysed by 554
CD-search (httpswwwncbinlmnihgovStructurecddwrpsbcgi) and cellular 555
locations of proteins including FaERF9 and FaMYB98 were predicted with the 556
WoLF PSORT program (httpswwwgenscriptcomwolf-psorthtml) 557
558
Dual-Luciferase Assays 559
In accordance with a previous protocol (Yin et al 2010) the full-length cDNAs of 560
FaAP2ERF or FaMYB98 transcription factors were cloned into pGreen II 0029 561
62-SK vector and the promoter of FaQR was cloned into pGreen II 0800-LUC vector 562
A luciferase gene from Renillia (REN) driven by a 35S promoter in the LUC vector 563
acted as a positive control The above constructs were transiently expressed in 564
Nicotiana benthamiana leaves by Agrobacterium-mediated infiltration (strain 565
GV3101) and the activity of the TFs on the promoter was measured on the third day 566
after infiltration indicated by the ratio of enzyme activities of firefly luciferase (LUC) 567
and renilla luciferase (REN) using a Modulus Luminometer (Promega Madison WI 568
USA) To determine the activity of a specific transcription factor towards the 569
promoter we mixed the Agrobacterium culture with 1 mL of TF and 100 μL of 570
promoter and the LUCREN value of the empty vector SK on the promoter was set as 571
1 as a calibrator To test the combined effect of two transcription factors on the 572
promoter to the Agrobacterium culture mixture we added 05 mL of each TF and 100 573
μL of promoter the effect of the mixtures that contained each transcription factor (05 574
mL) and empty vector SK (05 mL) was also tested on the promoter as a control 575
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
21
576
Subcellular localization analysis 577
35S-FaERF9-GFP and 35S-FaMYB98-GFP were transiently expressed in tobacco (N 578
benthamiana) leaves by Agrobacterium infiltration (EHA105) using the same method 579
as described in the dual-luciferase assay above The transiently infected leaves were 580
imaged on the third day after infiltration using a Nikon A1-SHS confocal laser 581
scanning microscope The excitation wavelength for GFP fluorescence was 488 nm 582
and fluorescence was detected at 490ndash520 nm The primers used for GFP construction 583
are listed in Supplemental Table S6 584
585
Transient overexpression in strawberry fruit 586
Transient overexpression of FaERF9 and an overexpression binary vector (pGreen II 587
0029 62-SK-FaERF9-FaMYB98) were performed in strawberry fruit using the 588
FaERF9-SK construct described above for the dual-luciferase assays and the binary 589
vector constructed according to Liu et al 2013 The transfection of fruit was carried 590
out at the G stage (Hoffmann et al 2006) The FaERF9-SK construct and binary 591
vector were individually electroporated into Agrobacterium tumefaciens GV3101 and 592
the Agrobacterium culture suspended in infiltration buffer was infiltrated into the 593
whole fruit using a syringe As a control treatment fruits were infiltrated with 594
Agrobacterium carrying an empty vector SK under the same transfection conditions 595
Fruits were left attached to the plants and harvested on the seventh day after 596
infiltration Fruits of three biological replicates were sampled for further analysis 597
598
Yeast one-hybrid assay 599
In order to identify proteins that bind to the FaQR promoter the Matchmaker Gold 600
Yeast One-hybrid Library Screening System (Clontech USA) was used The sequence 601
of the FaQR promoter was cloned into the pAbAi vector and the construct was 602
integrated into the genome of the Y1HGold yeast strain A mixture of total RNA from 603
strawberry fruit at four stages (G T IR R) was used to construct the prey cDNA 604
library (TaKaRa) The background AbAr expression of Y1HGold FaQR-pAbAi strain 605
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
22
was tested according to the system user manual and then screening for protein-DNA 606
interactions was carried out Furthermore the full length of each transcription factor 607
was separately cloned into pGADT7 AD vector to confirm the screening results The 608
relationship between FaERF9 and FaQR promoter was also examined individually 609
Primers used in this assay are listed in Supplemental Table S6 610
611
Expression and purification of FaMYB98 recombinant protein 612
A 405-bp region spanning the DNA-binding domain of FaMYB98 was amplified 613
from FaMYB98 cDNA and cloned into a pET6timesHN vector (Clontech Palo CA USA) 614
to generate the recombinant N-terminal His-tagged protein the primers used are listed 615
in Supplemental Table S6 The resulting construct was sequenced and introduced into 616
Escherichia coli strain Rosetta 2(DE3)pLysS (Novagen) Ten millilitres of the 617
overnight culture was combined with 500 mL of an LB liquid medium (100 μgmL 618
ampicillin and 34 μgmL chloramphenicol) as described (Li et al 2017) Isopropyl 619
β-D-1-thiogalactopyranoside (IPTG) was added to a final concentration of 1 mM and 620
the bacterial culture was incubated at 18degC at 150 rpm for 18 h Then the cells were 621
harvested using a centrifuge and resuspended in 1times PBS buffer (Sangon Biotech) 622
after which they were disrupted by sonication and the supernatant was purified using 623
a HisTALONTM Gravity Column (Clontech) according to the user manual The PD-10 624
Desalting column (GE Healthcare) was then used for buffer change and sample 625
clean-up of proteins according to the gravity protocol SDS-PAGE was performed and 626
the protein was visualized using Coomassie brilliant blue 627
628
Electrophoretic mobility shift assay (EMSA) 629
A Lightshift Chemiluminescent EMSA kit (Thermo) was used to perform EMSA 630
experiments according to the manufacturerrsquos instructions Single-strand 631
oligonucleotides were synthesized and biotinylated by GeneBio Biotech (Hangzhou 632
China) The details of the EMSA assay are provided in Ge et al (2017) The probes 633
used for EMSAs are listed in Supplemental Table S6 634
635
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
23
636
Yeast two-hybrid assay 637
The DUALhunter system (Dualsystems Biotech Switzerland) was used to investigate 638
the interaction between FaERF9 and FaMYB98 Full-length coding sequences of 639
FaERF9 and FaMYB98 were respectively cloned into pDHB1 bait vector and 640
pPR3-N prey vector sequences were verified and the bait plasmid was 641
co-transformed with prey plasmid into NMY51 in the combinations below 642
FaMYB98-pDHB1pPR3-N FaMYB98-pDHB1FaERF9-pPR3-N 643
FaMYB98-pDHB1pOst1-NubI FaERF9-pDHB1pPR3-N 644
FaERF9-pDHB1FaMYB98-pPR3-N and FaERF9-pDHB1pOst1-NubI (Li et al 645
2017) Transformed cells were spread onto the following plates DDO (SD 646
medium-Trp-Leu) QDO (SD medium-Trp-Leu-His-Ade) and QDO+3-AT (QDO 647
medium supplemented with 1 mM 3-amino-124-triazole) The control plasmid 648
pOst1-NubI was used to determine whether the bait was functional the pPR3-N prey 649
vector plasmid was used to test whether the bait displayed non-specific background 650
and positive interactions were indicated by the growth of yeast on QDO and 651
QDO+3-AT plates The Primers used in the DUALhunter assay are listed in 652
Supplemental Table S6 653
654
Bimolecular fluorescence complementation (BiFC) assays 655
Full-length FaERF9 and FaMYB98 respectively were cloned into sequences 656
encoding the N- and C- fragments of YFP protein (Lv et al 2014) All constructs 657
were transiently expressed in tobacco (N benthamiana) leaves by Agrobacterium 658
infiltration (EHA105) The YFP fluorescence of transfected leaves was imaged 40 h 659
after infiltration by using a Nikon A1-SHS confocal laser scanning microscope The 660
excitation wavelength for YFP was 488 nm and fluorescence was detected at 520ndash661
540 nm Primers used are listed in Supplemental Table S6 662
663
Statistics 664
A Studentrsquos two-tailed t test ( plt005 plt001 and plt0001) was used to 665
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
24
determine significant differences between two groups in this study Microsoft Excel 666
was used to perform linear regressive analysis significant differences were 667
determined by SPSS Statistics 200 and scatter plots were prepared with Origin80 668
Least significant difference (LSD) at the 5 level was calculated using Microsoft 669
Excel Figures were prepared with Origin80 (Microcal Software Inc Northampton 670
MA USA) The online tool MetaboAnalyst 36 (httpwwwmetaboanalystca) was 671
used to analyse the transcript abundance of the AP2ERF genes 672
673
Accession numbers 674
Sequence data from this article have been deposited in GenBank under the accession 675
numbers MH332903-MH333022 for AP2ERF genes in Fragaria times ananassa and 676
MH333023 for FaMYB98 GenBank numbers for FaQR and FaOMT were 677
AY1588361 (Raab et al 2006) and AF2204912 (Wein et al 2002) 678
679
Supplemental Material 680
Supplemental Figure S1 Phylogenetic analysis of FaAP2ERF and Arabidopsis 681
AP2ERF proteins 682
Supplemental Figure S2 Analysis of FaAP2ERF gene expression patterns in 683
strawberry fruit during development and ripening 684
Supplemental Figure S3 Contents of furanones in fruit of strawberry cultivars 685
Supplemental Figure S4 Relative expression of FaERF9 in FaERF9-FaMYB98- 686
and FaERF9-overexpressing fruits 687
Supplemental Figure S5 Subcellular localization of FaMYB98 688
Supplemental Figure S6 The combined activation effects of FaERF9FaMYB98 on 689
the FaOMT promoter 690
Supplemental Figure S7 Relative expression of FaOMT in 691
FaERF9-overexpressing fruits 692
Supplemental Table S1 AP2ERF superfamily genes in Fragaria times ananassa 693
Supplemental Table S2 Classification of the AP2ERF superfamily members in 694
Fragaria times ananassa 695
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25
Supplemental Table S3 Furanone content in FaERF9-FaMYB98- and 696
FaERF9-overexpressing fruits 697
Supplemental Table S4 Primers used for reverse transcription quantitative PCR 698
(RT-qPCR) 699
Supplemental Table S5 Primers used to amplify the full-length coding sequences of 700
AP2ERF genes and FaMYB98 in strawberry (Fragaria times ananassa) 701
Supplemental Table S6 Primers used for vector construction 702
703
Acknowledgments 704
This research was supported by the National Key Research and Development 705
Program (2016YFD0400101) the Project of the Science and Technology Department 706
of Zhejiang Province (2016C04001) and the 111 Project (B17039) 707
708
Figure legends 709
Figure 1 Changes in furanone content and furanone biosynthetic genes during 710
strawberry (Fragaria times ananassa Duch cv Yuexin) fruit development and ripening 711
A Fruits were collected at four ripening stages G (green stage) T (turning stage) IR 712
(intermediate red stage) R (full red stage) B Changes in the contents of furaneol 713
(HDMF) and mesifurane (DMMF) HDMF content was calculated using a standard 714
curve of HDMF while DMMF content was calculated with an internal standard as the 715
reference C Expression levels of FaQR and FaOMT The expression levels of each 716
gene were calculated relative to corresponding values in the basal section at the R 717
stage SEs were calculated from three replicates and LSD values represent the least 718
significant differences at p = 005 719
Figure 2 Regulatory effects of FaAP2ERF on the promoter of FaQR LUCREN 720
values of the empty vector on FaQR promoter were used as the calibrator set as 1 721
and SEs were calculated from five replicates statistical significance was determined 722
by Studentrsquos two-tailed t test ( plt0001) 723
Figure 3 Expression and the subcellular localization of FaERF9 A The expression 724
levels were calculated relative to the levels in the basal section at the R stage B 725
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
26
Subcellular localization analysis was performed in tobacco leaves The tobacco used 726
in the assay was stably transformed with a specific nucleus localized red fluorescence 727
protein construct and the red fluorescence indicates the nucleus-localized signal 728
(NLS) Scale bar = 25 microm SEs were calculated from three replicates 729
Figure 4 Transient overexpression of FaERF9 in strawberry fruit A Relative 730
expression of FaQR and FaERF9 in FaERF9-OX fruit 7 days after infiltration The 731
expression was calculated relative to the average value in control (SK) fruits B 732
HDMF and DMMF content in FaERF9-OX fruit The content of both furanones 733
were quantified using the peak area of the internal standard (2-octanol) as the 734
reference SEs were calculated from three replicates Statistical significance was 735
determined by Studentrsquos two-tailed t test ( plt005 plt001 plt0001) 736
Figure 5 Scatter plots of 11 strawberry cultivars A Linear regression analysis 737
between FaERF9 expression and FaQR expression B Linear regression analysis 738
between FaERF9 expression and furanone content The relative expression was 739
normalized to that of the housekeeping gene FaRIB413 and furanone content was 740
calculated with internal standard as the reference Significant differences were 741
determined by SPSS Statistics 200 742
Figure 6 Interactions of FaERF9 and FaMYB98 with the FaQR promoter A Yeast 743
one-hybrid analysis of the interaction of FaERF9 and FaQR promoter B Yeast 744
one-hybrid analysis of the interaction of FaMYB98 and FaQR promoter C 745
Regulatory effect of FaMYB98 on the FaQR promoter Auto-activation was tested on 746
SD-Ura (synthetically defined medium without uracil) in presence of Aureobasidin A 747
(AbA) and physical interaction was determined on SD-Leu (synthetically defined 748
medium without leucine) in presence of AbA LUCREN values of the empty vector 749
on FaQR promoter were used as the calibrator set as 1 and error bars were calculated 750
from five replicates Statistical significance was determined by Studentrsquos two-tailed t 751
test ( plt005 plt001 plt0001) 752
Figure 7 Electrophoretic mobility shift assay of FaMYB98 binding to FaQR 753
promoter A The probe sequence used for EMSA and mutated nucleotides are 754
indicated with lowercase letters B Purified DNA-binding domain of FaMYB98 755
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
27
protein and biotin-labelled DNA probe were mixed and analysed on 6 native 756
polyacrylamide gels and then photographed Presence or absence of specific probes is 757
marked by the symbol + or - 758
Figure 8 The combined activation effects of FaERF9FaMYB98 on the FaQR 759
promoter LUCREN values obtained with the empty vector and FaQR promoter were 760
used as the calibrator set as 1 and error bars were calculated from five replicates 761
Figure 9 Yeast two-hybrid analysis of the protein-protein interactions between 762
FaMYB98 and FaERF9 Positive interactions were determined by the growth of 763
yeast cells on selection plates Bait with pOST acted as positive controls and bait with 764
pPR3 as negative controls DDO synthetically defined medium without tryptophan 765
and leucine QDO synthetically defined medium without tryptophan leucine 766
histidine and adenine QDO+3AT QDO medium supplemented with 1 mM 767
3-aminotriazole 768
Figure 10 BiFC analysis of the protein-protein interactions between FaMYB98 and 769
FaERF9 The pairs of fusion proteins tested were FaMYB98-YFPN+FaERF9-YFPC 770
FaERF9-YFPN+FaMYB98-YFPC FaMYB98-YFPN+FaMYB98-YFPC and 771
FaERF9-YFPN+FaERF9-YFPC The other combinations were negative controls 772
The tobacco used in the assay was stably transformed with a specific 773
nucleus-localized red fluorescence protein construct and the red fluorescence 774
indicated the nucleus-localized signal (NLS) Fluorescence of the yellow fluorescence 775
protein (YFP) visualized the interaction in vivo Scale bar = 25 microm 776
777
Literature Cited 778
779
Agarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression 780
of PgDREB2A transcription factor enhances abiotic stress tolerance and activates 781
downstream stress-responsive genes Mol Biol Rep 37 1125-1135 782
Araguumlez I Osorio S Hoffmann T Rambla JL Medina-Escobar N Granell A 783
Botella MAacute Schwab W Valpuesta V (2013) Eugenol production in achenes and 784
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
28
receptacles of strawberry fruits is catalyzed by synthases exhibiting distinct kinetics 785
Plant Physiol 163 946-958 786
Carvalho RF Carvalho SD OrsquoGrady K Folta KM (2016) Agroinfiltration of 787
strawberry fruit mdash a powerful transient expression system for gene validation Curr 788
Plant Biol 6 19-37 789
Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic 790
(Amsterdam) 210 34-40 791
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating 792
RNA from pine trees Plant Mol Biol Rep 11 113-116 793
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC 794
Clark DG (2011) PhMYB4 fine-tunes the floral volatile signature of 795
Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143 796
Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz 797
EA Taylor MG Smits-Kroon MT Schuurink RC Haring MA Giovannoni J 798
Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic 799
pathway by ectopic expression of a MYB transcription factor in tomato fruit Plant 800
Cell 23 2738-2753 801
Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan 802
XW Yang ZY (2017) Differential responses of four biosynthetic pathways of 803
aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under 804
interaction of light and temperature Food Chem 221 356-364 805
Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of 806
differentially-expressed genes during somatic embryogenesis in Fragaria times 807
ananassa Duch lsquoBenihopprsquo J Hortic Sci Biotechnol 90 671-681 808
Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 809
transcriptionally regulates chilling-induced lignification of loquat fruit via physical 810
interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136 811
Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM 812
(2004) Functional interactions between a glutamine synthetase promoter and MYB 813
proteins Plant J 39 513-526 814
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
29
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) 815
Sucrose nonfermenting1-related protein kinase26 an ortholog of open stomata1 is 816
a negative regulator of strawberry fruit development and ripening Plant Physiol 817
167 915-930 818
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene 819
expression in strawberry fruit (Fragaria times ananassa) by agroinfiltration a rapid 820
assay for gene function analysis Plant J 48 818-826 821
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of 822
selected aroma-active compounds in strawberries by headspace solid-phase 823
microextraction gas chromatography and correlation with sensory descriptive 824
analysis J Food Sci 72 S487-S496 825
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid 826
plays an important role in the regulation of strawberry fruit ripening Plant Physiol 827
157 188-199 828
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of 829
NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes BMC 830
Plant Biol 6 20 831
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN 832
(2005) MYB98 is required for pollen tube guidance and synergid cell differentiation 833
in Arabidopsis Plant Cell 17 2981-2992 834
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional 835
characterization of enone oxidoreductases from strawberry and tomato fruit J 836
Agric Food Chem 55 6705-6711 837
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You 838
J-S Rohloff J Randall SK Alsheikh M (2012) Proteomic study of 839
low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ 840
in cold tolerance Plant Physiol 159 1787-1805 841
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional 842
characterization of four APETALA2-family genes (RAP26 RAP26L DREB19 843
and DREB26) in Arabidopsis Plant Mol Biol 75 107-127 844
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
30
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon 845
J Gupta V (2013) An oxidoreductase from lsquoAlphonsorsquo mango catalyzing 846
biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494 847
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in 848
strawberries Z Lebensm-Unters Forsch 195 120-123 849
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X 850
(2015) Label-free quantitative proteomics to investigate strawberry fruit proteome 851
changes under controlled atmosphere and low temperature storage J Proteomics 852
120 44-57 853
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 854
cooperates with CitWRKY1 to participate in citric acid degradation via 855
up-regulation of CitAco3 J Exp Bot 68 3419-3426 856
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription 857
factor CitERF71 activates the terpene synthase gene CitTPS16 involved in the 858
synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938 859
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and 860
transcriptomic analysis of the AP2ERF superfamily in Vitis vinifera BMC 861
Genomics 11 719 862
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive 863
Factor (AP2ERF) transcription factors mediators of stress responses and 864
developmental programs New Phytol 199 639-649 865
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 866
interacting with EOBI negatively regulates fragrance biosynthesis in petunia 867
flowers New Phytol 215 1490-1502 868
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu 869
CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 in regulating 870
anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) 871
during anthocyanin biosynthesis Plant Cell Tissue Organ Cult 115 285-298 872
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
31
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao 873
CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphate signaling and 874
homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597 875
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC 876
Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL 877
Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor 878
regulates eugenol production in ripe strawberry fruit receptacles Plant Physiol 168 879
598-614 880
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics 881
and volatile constituents of strawberry (cv Cigaline) during maturation J Agric 882
Food Chem 52 1248-1254 883
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS 884
(2012) Ethylene-responsive transcription factors interact with promoters of ADH 885
and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 886
63 6393-6405 887
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM 888
Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-Franco A 889
Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific 890
transcription factor FaDOF2 regulates the production of eugenol in ripe fruit 891
receptacles J Exp Bot 68 4529-4543 892
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) 893
Comparison and verification of the genes involved in ethylene biosynthesis and 894
signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44 895
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the 896
ERF gene family in Arabidopsis and rice Plant Physiol 140 411-432 897
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in 898
sour cherry and strawberry and the heterologous expression of CBF1 in strawberry 899
J Am Soc Hortic Sci 127 489-494 900
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech 901
JC Ohme-Takagi M Regad F Bouzayen M (2012) Functional analysis and 902
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
32
binding affinity of tomato ethylene response factors provide insight on the 903
molecular bases of plant differential responses to ethylene BMC Plant Biol 12 190 904
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) 905
Methylpentoses are possible precursors of furanones in fruits Prikl Biokhim 906
Mikrobiol 28 123-127 907
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery 908
of synergid-expressed genes encoding filiform apparatus localized proteins Plant 909
Cell 19 2557-2568 910
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria 911
vesca L compared to those of cultivated berries Fragariatimes ananassa cv Senga 912
Sengana J Agric Food Chem 27 19-22 913
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W 914
Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of the strawberry 915
flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone 916
oxidoreductase Plant Cell 18 1023-1037 917
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L 918
Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim M Broun P Zhang 919
JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription 920
factors genome-wide comparative analysis among eukaryotes Science 290 921
2105-2110 922
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the 923
formation of 25-dimethyl-4-hydroxy-3(2H)-furanone in detached ripening 924
strawberry fruits J Agric Food Chem 46 1488-1493 925
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 926
25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in 927
strawberry fruits Phytochemistry 43 155-159 928
Schwab W (1998) Application of stable isotope ratio analysis explaining the 929
bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone in plants by a biological 930
maillard reaction J Agric Food Chem 46 2266ndash2269 931
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33
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) 932
Molecules 18 6936-6951 933
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard 934
products Recent Res Dev Phytochem 1 643-673 935
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL 936
Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJ Sims CA 937
Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical 938
compositions a seasonal influence and effects on sensory perception PLoS One 9 939
e88446 940
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) 941
Identification phylogeny and transcript profiling of ERF family genes during 942
development and abiotic stress treatments in tomato Mol Genet Genomics 284 943
455-475 944
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) 945
CitAP210 activation of the terpene synthase CsTPS1 is associated with the 946
synthesis of (+)-valencene in lsquoNewhallrsquo orange J Exp Bot 67 4105-4115 947
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes 948
Dev Genes Evol 214 105-114 949
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K 950
Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the 951
key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151 952
Spitzer-Rimon B Farhi M Albo B Cnarsquoani A Ben Zvi MM Masci T Edelbaum 953
O Yu YX Shklarman E Ovadis M Vainstein A (2012) The R2R3-MYB-like 954
regulatory factor EOBI acting downstream of EOBII regulates scent production 955
by activating ODO1 and structural scent-related genes in petunia Plant Cell 24 956
5089-5105 957
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp 958
Bot 68 4407-4409 959
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla 960
JF Amaya I Giavalisco P Fernie AR Botella MA Valpuesta V (2015) Central 961
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34
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Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 964
regulates fragrance biosynthesis in petunia flowers Plant Cell 17 1612-1624 965
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(2018) The potassium channel FaTPK1 plays a critical role in fruit quality 967
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Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ 984
Zhang SL Wu J (2017) Map-based cloning of the pear gene MYB114 identifies an 985
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involved in regulating fruit ripening Plant Physiol 153 1280-1292 989
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35
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Arabidopsis AP2ERF transcription factor RAP26 participates in ABA salt and 1012
osmotic stress responses Gene 457 1-12 1013
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B 1014
Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) Genome-wide 1015
analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic 1016
(Amsterdam) 123 73-81 1017
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF 1018
Valpuesta V Botella MA Granell A Amaya I (2012) Genetic analysis of 1019
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36
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locus controlling natural variation in mesifurane content Plant Physiol 159 1021
851-870 1022
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
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wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
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Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive Factor (AP2ERF) transcription factors mediators of stressresponses and developmental programs New Phytol 199 639-649
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 interacting with EOBI negatively regulates fragrancebiosynthesis in petunia flowers New Phytol 215 1490-1502
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 inregulating anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) during anthocyanin biosynthesis Plant CellTissue Organ Cult 115 285-298
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title wwwplantphysiolorgon February 25 2020 - Published by Downloaded from
Copyright copy 2018 American Society of Plant Biologists All rights reserved
Google Scholar Author Only Title Only Author and Title
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphatesignaling and homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor regulates eugenol production in ripe strawberry fruitreceptacles Plant Physiol 168 598-614
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics and volatile constituents of strawberry (cv Cigaline)during maturation J Agric Food Chem 52 1248-1254
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS (2012) Ethylene-responsive transcription factors interact withpromoters of ADH and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 63 6393-6405
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-FrancoA Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific transcription factor FaDOF2 regulates the production ofeugenol in ripe fruit receptacles J Exp Bot 68 4529-4543
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) Comparison and verification of the genes involved in ethylenebiosynthesis and signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice Plant Physiol140 411-432
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in sour cherry and strawberry and the heterologousexpression of CBF1 in strawberry J Am Soc Hortic Sci 127 489-494
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech JC Ohme-Takagi M Regad F Bouzayen M (2012)Functional analysis and binding affinity of tomato ethylene response factors provide insight on the molecular bases of plant differentialresponses to ethylene BMC Plant Biol 12 190
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) Methylpentoses are possible precursors of furanones in fruits PriklBiokhim Mikrobiol 28 123-127
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery of synergid-expressed genes encoding filiformapparatus localized proteins Plant Cell 19 2557-2568
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria vesca L compared to those of cultivated berriesFragariatimes ananassa cv Senga Sengana J Agric Food Chem 27 19-22
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of thestrawberry flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone oxidoreductase Plant Cell 18 1023-1037
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim MBroun P Zhang JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription factors genome-wide comparative analysisamong eukaryotes Science 290 2105-2110
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the formation of 25-dimethyl-4-hydroxy-3(2H)-furanonein detached ripening strawberry fruits J Agric Food Chem 46 1488-1493
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in strawberry fruits Phytochemistry 43 155-159
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (1998) Application of stable isotope ratio analysis explaining the bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone inplants by a biological maillard reaction J Agric Food Chem 46 2266ndash2269
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) Molecules 18 6936-6951Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard products Recent Res Dev Phytochem 1 643-673Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJSims CA Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical compositions a seasonal influence and effects on sensoryperception PLoS One 9 e88446
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) Identification phylogeny and transcript profiling of ERFfamily genes during development and abiotic stress treatments in tomato Mol Genet Genomics 284 455-475
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) CitAP210 activation of the terpene synthase CsTPS1 isassociated with the synthesis of (+)-valencene in Newhall orange J Exp Bot 67 4105-4115
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes Dev Genes Evol 214 105-114Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Spitzer-Rimon B Farhi M Albo B Cnaani A Ben Zvi MM Masci T Edelbaum O Yu YX Shklarman E Ovadis M Vainstein A (2012) TheR2R3-MYB-like regulatory factor EOBI acting downstream of EOBII regulates scent production by activating ODO1 and structuralscent-related genes in petunia Plant Cell 24 5089-5105
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp Bot 68 4407-4409Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla JF Amaya I Giavalisco P Fernie AR Botella MAValpuesta V (2015) Central role of FaGAMYB in the transition of the strawberry receptacle from development to ripening New Phytol208 482-496
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Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 regulates fragrance biosynthesis in petunia flowers PlantCell 17 1612-1624
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Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS (2018) The potassium channel FaTPK1 plays a critical role infruit quality formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) Isolation cloning and expression of a multifunctional O- wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma compounds in strawberry fruitsPlant J 31 755-765
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor types their evolutionary origin and speciesdistribution In A handbook of transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular Biochemistry 52 25-73
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of odor (Buettner A Ed) Springer Cham 9-10Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS (2014) Isolation classification and transcription profiles ofthe AP2ERF transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in regulation of fruit quality Crit Rev Plant Sci 35 120-130
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Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ Zhang SL Wu J (2017) Map-based cloning of the pear geneMYB114 identifies an interaction with other transcription factors to coordinately regulate fruit anthocyanin biosynthesis Plant J 92437-451
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Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes involved in regulating fruit ripening Plant Physiol 1531280-1292
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Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) Expression of ethylene response genes during persimmonfruit astringency removal Planta 235 895-906
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Zabetakis I Gramshaw JW Robinson DS (1999) 25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis andbiosynthesis-a review Food Chem 65 139-151
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Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci Food Agric 74 421-434Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 an AP2ERF gene is a novel regulator of fruit lignificationinduced by chilling injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1325-1334
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Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation classification and transcription profiles of the Ethylene ResponseFactors (ERFs) in ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215
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Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML (2012) Genome-wide analysis of the AP2ERF superfamily inpeach (Prunus persica) Genet Mol Res 11 4788-4809
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Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and expression analysis of a CRTDRE-binding factor gene FaCBF1from Fragaria times ananassa Acta Hortic 41 240-248
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The Arabidopsis AP2ERF transcription factor RAP26 participatesin ABA salt and osmotic stress responses Gene 457 1-12
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Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Genome-wide analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic (Amsterdam) 123 73-81Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF Valpuesta V Botella MA Granell A Amaya I (2012) Geneticanalysis of strawberry fruit aroma and identification of O-methyltransferase FaOMT as the locus controlling natural variation inmesifurane content Plant Physiol 159 851-870
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
12
nucleus while negative controls produced no detectable fluorescence signal (Figure 306
10) In addition coexpression of FaERF9-YFPNFaERF9-YFPC as well as 307
FaMYB98-YFPNFaMYB98-YFPC also generated signals in the nucleus indicating 308
that FaERF9 and FaMYB98 both could form homodimers or possibly multimers in 309
the nucleus (Figure 10) 310
311
Discussion 312
The AP2ERF superfamily in strawberry 313
The AP2ERF superfamily of plant transcription factors is defined by the AP2ERF 314
domain and comprises the ERF AP2 and RAV families as well as one soloist member 315
(Riechmann et al 2000 Weirauch and Hughes 2011) The completion of multiple 316
plant genome sequences has enabled a genome-scale analysis of the AP2ERF family 317
which in recent years has been systematically studied in diverse fruit species such as 318
tomato grape peach and kiwi fruit (Zhuang et al 2009 Sharma et al 2010 Licausi 319
et al 2010 Yin et al 2010 Pirrello et al 2012 Zhang et al 2012 Zhang et al 320
2016) A few AP2ERF genes have been isolated and characterized in strawberry and 321
CBF orthologs (Owens et al 2002 Koehler et al 2012 Zhang et al 2014) have 322
been identified from different strawberry cultivars in several independent studies 323
Although they have distinct names eg Fragaria times ananassa CBF1 (FaCBF1) 324
FaCBF4 (GenBank HQ9105151) and CBF1 (GenBank EU1172142) according to 325
the phylogenetic tree generated in this study the orthologs of 326
CBF1CBF4CBF2CBF3 in Arabidopsis are similar to each other and to FaERF20 327
(Supplemental Figure S1) (Owens et al 2002 Koehler et al 2012 Zhang et al 328
2014) FaERF20 has 85 sequence similarity with FaCBF1 identified by Owens et 329
al (2002) 93 similarity with FaCBF4 amplified by Koehler et al (2012) and 75 330
similarity with CBF1 cloned by Zhang et al (2014) The AP2ERF genes 331
characterized in other studies (Jia et al 2011 GAO et al 2015 Chai and Shen 2016 332
Mu et al 2016) are also noted in Supplemental Table S1 333
334
Based on the computational analysis we have identified a total of 120 AP2ERF 335
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13
genes in octoploid strawberry (Supplemental Table S1) The number of predicted 336
AP2ERF genes (120) is comparable to those observed in other fruits including 337
tomato (112) Chinese plum (116) citrus (126) and peach (131) but lower than those 338
reported for grape (149) (Xie et al 2016) As shown in Supplemental Table S2 79 339
(95 genes) of the AP2ERF genes belong to the ERF family in strawberry constituting 340
the largest sub-family The members of this sub-family can be classified into 10 341
groups (group I to X) according to their sequence similarities to the Arabidopsis ERF 342
genes (Nakano et al 2006) The AP2 family encompasses the same number of genes 343
in Arabidopsis citrus and strawberry (eighteen) (Nakano et al 2006 Xie et al 2014) 344
and there are six RAV genes in strawberry which are highly conserved in dicots such 345
as Vitis vinifera Arabidopsis thaliana and Populus trichocarpa (Licausi et al 2010) 346
347
Role of FaERF9 in regulating the biosynthesis of HDMF a positive regulator 348
acting in an indirect manner 349
The large-scale screening of the AP2ERF superfamily in strawberry led to 350
identification of 11 ERFs and 1 RAV that trans-activated the FaQR promoter more 351
than two-fold with the highest activation caused by FaERF9 which trans-activated 352
the FaQR promoter (Figure 2) as well as up-regulating FaQR expression and furanone 353
production in transient overexpression assays (Figure 4) which has been extensively 354
used to explore the fruit-associated gene functions in strawberry (Han et al 2015 355
Medina-Puche et al 2015 Vallarino et al 2015 Carvalho et al 2016 Song et al 356
2016 Wang et al 2018) FaERF9 transcripts accumulate in the fruit apical section 357
before the basal section (Figure 3) a finding consistent with the actual changes in 358
furaneol content (Figure 1) and the expression of FaQR (Figure 1) The association 359
between FaERF9 transcripts and accumulation of furanones were also established 360
with different strawberry cultivars The correlation between FaERF9 and FaQR 361
expression as well as furanone content among cultivars supports a positive role of 362
FaERF9 in regulating furanone content (Figure 5) These results indicate that 363
FaERF9 transcript abundance may be a good indicator of the abundance of these 364
important flavour volatiles in fruits of different cultivars This should be considered as 365
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14
a method for high-throughput variety screening to replace direct measurement of 366
volatiles 367
368
FaERF9 is a member of the ERF group II family and is most closely related to the 369
Arabidopsis genes At1g44830 (ATERF014) At1g21910 (DREB26) and At1g77640 370
(Supplemental Figure S1) At1g44830 was observed to be strongly up-regulated in a 371
comprehensive microarray analysis of the root transcriptome following NaCl 372
exposure (Jiang and Deyholos 2006) At1g21910 (DREB26) was functionally 373
characterized as a trans-activator localized in the nucleus exhibiting tissue-specific 374
expression and participating in plant developmental processes as well as biotic andor 375
abiotic stress signalling (Krishnaswamy et al 2011) However none of these genes 376
have been reported as furanone regulators In strawberry another five genes 377
(FaERF6 FaERF7 FaERF8 FaERF10 and FaERF11) also belong to the same 378
group with FaERF8 also showing somewhat weaker activation activity towards the 379
FaQR promoter than FaERF9 The fact that FaERF9 could not bind directly to the 380
promoter of FaQR (Figure 6) indicates that it might function as an indirect regulator 381
of FaQR and furaneol biosynthesis 382
383
A FaERF9 and FaMYB98 complex is involved in regulating FaQR and furaneol 384
biosynthesis 385
The finding that FaERF9 could interact with FaMYB98 protein (Figures 9 and 386
Figure 10) and that FaMYB98 could physically bind to the FaQR promoter (Figure 6 387
and Figure 7) provides evidence for a regulatory mechanism whereby FaERF9 388
regulates FaQR and furaneol production as part of a complex with an MYB 389
transcription factor Since co-overexpression of FaERF9 and FaMYB98 resulted in 390
much higher activation activity towards FaQR we speculate that FaERF9 may 391
recruit FaMYB98 homologs in tobacco to activate the FaQR promoter (Figure 8) 392
FaOMT is another key gene for furanone biosynthesis and a potential target for 393
transcriptional activation However FaERF9 did not significantly activate the 394
FaOMT promoter in a dual-luciferase assay and the transcript level of FaOMT in the 395
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15
FaERF9-overexpressing fruits showed no significant difference from that in the 396
control (Supplemental Figure S6 Supplemental Figure S7) The FaOMT promoter 397
was significantly induced by FaMYB98 but no synergistic effect of FaERF9 and 398
FaMYB98 on the promoter was observed (Supplemental Figure S6) In previous 399
studies of the regulation of plant volatile compounds MYBs have been characterized 400
as being involved mainly in the regulation of the benzenoidphenylpropanoid pathway 401
that produces floral volatiles in petunia and eugenol in ripe strawberry fruit (Verdonk 402
et al 2005 Dal Cin et al 2011 Colquhoun et al 2011 Spitzer-Rimon et al 2012 403
Medina-Puche et al 2015) but their role in formation of volatiles from other 404
pathways has not been reported Our study demonstrates a role for MYB in the 405
synthesis of furaneol a carbohydrate-derived volatile compound and reveals the 406
synergistic interactions between an MYB and ERF in a transcription complex (Figure 407
8 Figure 9 and Figure 10) 408
409
Recent research has provided evidence for interactions between AP2ERF and MYB 410
transcription factors in regulating other aspects of fruit quality including texture 411
(EjAP2-1 and EjMYB Zeng et al 2015) and colour (PyERF3 and PyMYB114 Yao 412
et al 2017) A group VIII ERF has also recently been shown to interact with an MYB 413
to regulate floral scent production in petunia (Liu et al 2017) In strawberry fruit 414
DOF in combination with an MYB has been reported to be involved in the regulation 415
of eugenol production and the identification of this second transcription factor (DOF) 416
suggests that it is a good target in breeding for improved flavour (Molina-Hidalgo et 417
al 2017 Tieman 2017) Considering its important contribution to flavour in 418
strawberry and many other highly valued fruit crop species (pineapple tomato mango 419
etc) very little is known about regulation of furaneol synthesis Here we established 420
the role of FaERF9 in the regulation of HDMF synthesis by direct protein-protein 421
interactions with FaMYB98 to synergistically trans-activate FaQR The functional 422
identification of this complex enhances our knowledge of the regulation of volatile 423
compound synthesis and identifies a new AP2ERF-MYB complex Further 424
examination of the other ERFs that stimulated transcription from the FaQR promoter 425
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16
(Figure 2) may provide additional information about the complexity of this regulation 426
Overall this study provides important clues for understanding the transcriptional 427
regulation of HDMF synthesis and identifies specific transcription factors that are 428
likely to be good targets for molecular breeding for improved flavour 429
430
Conclusions 431
Screening of the AP2ERF superfamily in strawberry (Fragaria times ananassa) 432
identified candidate members capable of activating the FaQR promoter An ERF 433
transcription factor was identified as a positive regulator of HDMF synthesis in 434
strawberry fruit and the mechanism of activation was shown to involve an ERF-MYB 435
transcription complex that regulates transcription of FaQR leading to the biosynthesis 436
of HDMF the characteristic volatile compound which has a major influence on 437
strawberry aroma 438
439
Materials and Methods 440
441
Plant Materials and Growth conditions 442
The strawberry (Fragaria times ananassa cv lsquoYuexinrsquo an octoploid cultivar) fruit used in 443
this study were bred by Zhejiang Academy of Agricultural Sciences (Haining 444
Zhejiang) Fruits at various developmental and ripening stages including G (green) T 445
(turning) IR (intermediate red) and R (full red) were harvested (Figure 1) and 446
transported to the laboratory within 2 h Thirty-six fruits of uniform size and free of 447
visible defects were selected at each stage with twelve fruits in each biological 448
replicate After removing the calyces fruits were then divided into the basal and 449
apical sections which were sampled separately (Figure 1) They were rapidly cut into 450
pieces frozen immediately in liquid nitrogen and stored at -80deg C until use Red ripe 451
fruits of different strawberry cultivars (Fragaria times ananassa octoploid cultivars) 452
including lsquoYuelirsquo lsquoBenihoppersquo lsquoMengxiangrsquo lsquoAmaoursquo lsquo10-1-4rsquo lsquoAkihimersquo lsquoSweet 453
Charliersquo lsquo07-1-4rsquo lsquoDarselectrsquo lsquoYuexinrsquo and lsquoXuemeirsquo were also provided by Zhejiang 454
Academy of Agricultural Sciences For each cultivar the fruits of three biological 455
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17
replicates were sampled frozen in liquid nitrogen and stored at -80deg C for further use 456
457
Tobacco plants (Nicotiana benthamiana) used for dual-luciferase assays and 458
subcellular localization analysis in this study were grown in a growth chamber with a 459
lightdark cycle of 16 h8 h at 24degC 460
461
Detection of DMMF and HDMF 462
Automated HS-SPME-GC-MS was performed to detect both furanones in lsquoYuexinrsquo 463
strawberry fruit (Zorrilla-Fontanesi et al 2012) Samples were ground into a powder 464
under liquid nitrogen for analysis 465
466
For the detection of DMMF (Figure 1) 05 g (fresh weight) of each sample was 467
weighed in the vial to which was added 1 mL of EDTA solution (100 mM pH 75) 1 468
mL of CaCl2 solution (mv = 20) and 20 microL of 2-octanol as the internal standard 469
(007 μgμL) The mixture was homogenized and the vial closed and placed on the 470
sample tray for analysis by CombiPAL autosampler (CTC Analytic CA USA) The 471
fruit volatiles were sampled by headspace solid-phase microextraction with a 65-μm 472
polydimethylsiloxane-divinylbenzene fibre (PDMS-DVB) Initially vials were 473
pre-incubated at 50degC for 10 min under continuous agitation (500 rpm) then volatiles 474
were extracted for 30 min at the same temperature and agitation speed After that the 475
fibre was desorbed in the GC injection port for 5 min in splitless mode The 7890A 476
GC chromatograph was equipped with a DB-5ms column (60 m times 250 μm times 1 μm 477
JampW Scientific Folsom CA USA) with helium as the carrier gas at a constant flow 478
of 12 mLmin The GC was programmed at an initial temperature of 35degC for 2 min 479
with a ramp of 5degC min up to 250degC and held for 5 min The injection port interface 480
and MS source temperatures were 250degC 260degC and 230degC respectively The 481
ionization potential was set at 70 eV recorded by a 5975B mass spectrometer (Agilent 482
Technologies JampW Scientific Folsom CA USA) and the scanning speed was 7 483
scanss The same method was used to analyse HDMF and DMMF in fruits from 484
different cultivars (Supplemental Figure S3) except for the sample preparation 485
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18
procedure (Araguumlez et al 2013) briefly 05 g (fresh weight) of powdered fruit was 486
incubated at 30degC in a water bath for 5 min then 2 mL of NaCl (mv = 20) and 20 487
microL of 2-octanol as the internal standard (007 μgμL) were added and homogenized 488
489
For the detection of HDMF (Figure 1) and both furanones (Figure 4 and Supplemental 490
Table S3) a liquid-injection system equipped with CTC Pal ALS was used One gram 491
(fresh weight) of powdered fruit and 2 mL of NaCl (mv = 20) were homogenized in 492
a 10-mL tube and 300 μL of CH2Cl2 and 20 microL of 2-octanol (0766 μgμL) as the 493
internal standard were added to extract the volatiles the mixture was then 494
homogenized again The tubes were stored at room temperature for 20 min and 495
centrifuged at 12000 rpm for 5 min The subnatant was pipetted into a clean 15-mL 496
tube in which 20 mg of anhydrous sodium sulphate was added the tube was left 497
without shaking for half an hour Then 150 μL of the solution was transferred into a 498
GC vial and placed on the sample tray as described above Each sample (1 μL) was 499
injected using the autosampler and the analysis was accomplished by a 7890A 500
GC-MS system (Agilent Technologies JampW Scientific Folsom CA USA) equipped 501
with a DB-WAX column (30 m times 025 mm times 025 μm JampW) Helium (12 mLmin) 502
was used as a carrier gas The injection port (splitless injection mode) interface and 503
MS source temperatures were as described above The oven temperature was set at 504
60degC for 4 min then increased to 180degC at a rate of 4degCmin and maintained for 30 505
min DMMF was identified by comparison of electron ionization mass spectra and 506
retention time data with the data from the NISTEPANIH mass spectral library 507
(NIST-08 and Flavor) HDMF (Figure 1) was identified and qualified by comparison 508
with injected standard (Sigma) The quantitative analysis of both furanones (Figure 4 509
Supplemental Table S3 and Supplemental Figure S3) was determined using the peak 510
area of the internal standard as a reference based on total ion chromatogram (TIC) 511
512
RNA isolation and Reverse Transcription Quantitative PCR (RT-qPCR) 513
Total RNA from strawberry samples was isolated in this study using the CTAB 514
method (Chang et al 1993) Genomic DNA contamination was eliminated by 515
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
19
TURBO Dnase (Ambion) 1 μg of RNA was used to obtain cDNA using an IScriptTM 516
cDNA Synthesis Kit (Bio-Rad) The synthesized cDNA was diluted with water (120) 517
and 2 μL of diluted cDNA was used as the template for RT-qPCR Reactions were 518
performed in a total volume of 20 μL consisting of 10 μL of SYBR PCR supermix 519
(Bio-Rad) 1 μL of each primer (10 μM) 6 μL of DEPC-H2O and 2 μL of diluted 520
cDNA on CFX96 instrument (Bio-Rad) (Yin et al 2012) The oligonucleotide 521
primers for RT-qPCR analysis of genes including the AP2ERF FaQR and FaOMT 522
were designed according to the coding sequences of genes and the specificity was 523
verified before use (Min et al 2012) NCBIPrimer-BLAST was applied to design the 524
primers Relative expression levels were normalized to that of an internal controlmdashthe 525
interspacer 26S-18S strawberry RNA housekeeping gene FaRIB413 526
(Zorrilla-Fontanesi et al 2012) To investigate the differential expression of genes 527
during fruit development and ripening stages relative expression of each gene at the 528
R stage in the basal fruit section was set as 1 using the 2minus∆∆119862119879 method For transient 529
overexpression assay relative expression of control fruits with an empty vector (SK) 530
was set as 1 The primers used in RT-qPCR are listed in Supplemental Table S4 531
532
Gene isolation and analysis 533
Multiple database searches were performed to identify members of the strawberry 534
(Fragaria times ananassa) AP2ERF superfamily in the published strawberry databases 535
and annotations of Fragaria times ananassa and Fragaria times vesca by using the 536
AP2ERF DNA binding domain as a query sequence and 120 genes were identified 537
with AP2ERF domain(s) Based on the BLAST result primers (listed in 538
Supplemental Table S5) were used to amplify the coding full-length cDNAs of 539
AP2ERF genes The deduced amino acid sequences of AP2ERF proteins in 540
Arabidopsis thaliana used for construction of a phylogenetic tree were obtained from 541
the Arabidopsis Information Resource (TAIR) Alignment of the proteins was 542
performed using the neighbour-joining method in ClustalX (v181) and the 543
phylogenetic tree was constructed using FigTree (v131) 544
545
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
20
FaMYB98 was obtained by yeast one-hybrid screening sequencing and the full-length 546
sequences were predicted by BLAST Primers were designed (listed in Supplemental 547
Table S5) to amplify the full-length coding sequence 548
549
The promoter of FaQR was cloned by Genome Walking as previously described (Yin 550
et al 2010) and conserved cis-element motifs in the promoter were manually 551
searched 552
553
Conserved domains within the FaAP2ERF proteins and FaMYB98 were analysed by 554
CD-search (httpswwwncbinlmnihgovStructurecddwrpsbcgi) and cellular 555
locations of proteins including FaERF9 and FaMYB98 were predicted with the 556
WoLF PSORT program (httpswwwgenscriptcomwolf-psorthtml) 557
558
Dual-Luciferase Assays 559
In accordance with a previous protocol (Yin et al 2010) the full-length cDNAs of 560
FaAP2ERF or FaMYB98 transcription factors were cloned into pGreen II 0029 561
62-SK vector and the promoter of FaQR was cloned into pGreen II 0800-LUC vector 562
A luciferase gene from Renillia (REN) driven by a 35S promoter in the LUC vector 563
acted as a positive control The above constructs were transiently expressed in 564
Nicotiana benthamiana leaves by Agrobacterium-mediated infiltration (strain 565
GV3101) and the activity of the TFs on the promoter was measured on the third day 566
after infiltration indicated by the ratio of enzyme activities of firefly luciferase (LUC) 567
and renilla luciferase (REN) using a Modulus Luminometer (Promega Madison WI 568
USA) To determine the activity of a specific transcription factor towards the 569
promoter we mixed the Agrobacterium culture with 1 mL of TF and 100 μL of 570
promoter and the LUCREN value of the empty vector SK on the promoter was set as 571
1 as a calibrator To test the combined effect of two transcription factors on the 572
promoter to the Agrobacterium culture mixture we added 05 mL of each TF and 100 573
μL of promoter the effect of the mixtures that contained each transcription factor (05 574
mL) and empty vector SK (05 mL) was also tested on the promoter as a control 575
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
21
576
Subcellular localization analysis 577
35S-FaERF9-GFP and 35S-FaMYB98-GFP were transiently expressed in tobacco (N 578
benthamiana) leaves by Agrobacterium infiltration (EHA105) using the same method 579
as described in the dual-luciferase assay above The transiently infected leaves were 580
imaged on the third day after infiltration using a Nikon A1-SHS confocal laser 581
scanning microscope The excitation wavelength for GFP fluorescence was 488 nm 582
and fluorescence was detected at 490ndash520 nm The primers used for GFP construction 583
are listed in Supplemental Table S6 584
585
Transient overexpression in strawberry fruit 586
Transient overexpression of FaERF9 and an overexpression binary vector (pGreen II 587
0029 62-SK-FaERF9-FaMYB98) were performed in strawberry fruit using the 588
FaERF9-SK construct described above for the dual-luciferase assays and the binary 589
vector constructed according to Liu et al 2013 The transfection of fruit was carried 590
out at the G stage (Hoffmann et al 2006) The FaERF9-SK construct and binary 591
vector were individually electroporated into Agrobacterium tumefaciens GV3101 and 592
the Agrobacterium culture suspended in infiltration buffer was infiltrated into the 593
whole fruit using a syringe As a control treatment fruits were infiltrated with 594
Agrobacterium carrying an empty vector SK under the same transfection conditions 595
Fruits were left attached to the plants and harvested on the seventh day after 596
infiltration Fruits of three biological replicates were sampled for further analysis 597
598
Yeast one-hybrid assay 599
In order to identify proteins that bind to the FaQR promoter the Matchmaker Gold 600
Yeast One-hybrid Library Screening System (Clontech USA) was used The sequence 601
of the FaQR promoter was cloned into the pAbAi vector and the construct was 602
integrated into the genome of the Y1HGold yeast strain A mixture of total RNA from 603
strawberry fruit at four stages (G T IR R) was used to construct the prey cDNA 604
library (TaKaRa) The background AbAr expression of Y1HGold FaQR-pAbAi strain 605
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
22
was tested according to the system user manual and then screening for protein-DNA 606
interactions was carried out Furthermore the full length of each transcription factor 607
was separately cloned into pGADT7 AD vector to confirm the screening results The 608
relationship between FaERF9 and FaQR promoter was also examined individually 609
Primers used in this assay are listed in Supplemental Table S6 610
611
Expression and purification of FaMYB98 recombinant protein 612
A 405-bp region spanning the DNA-binding domain of FaMYB98 was amplified 613
from FaMYB98 cDNA and cloned into a pET6timesHN vector (Clontech Palo CA USA) 614
to generate the recombinant N-terminal His-tagged protein the primers used are listed 615
in Supplemental Table S6 The resulting construct was sequenced and introduced into 616
Escherichia coli strain Rosetta 2(DE3)pLysS (Novagen) Ten millilitres of the 617
overnight culture was combined with 500 mL of an LB liquid medium (100 μgmL 618
ampicillin and 34 μgmL chloramphenicol) as described (Li et al 2017) Isopropyl 619
β-D-1-thiogalactopyranoside (IPTG) was added to a final concentration of 1 mM and 620
the bacterial culture was incubated at 18degC at 150 rpm for 18 h Then the cells were 621
harvested using a centrifuge and resuspended in 1times PBS buffer (Sangon Biotech) 622
after which they were disrupted by sonication and the supernatant was purified using 623
a HisTALONTM Gravity Column (Clontech) according to the user manual The PD-10 624
Desalting column (GE Healthcare) was then used for buffer change and sample 625
clean-up of proteins according to the gravity protocol SDS-PAGE was performed and 626
the protein was visualized using Coomassie brilliant blue 627
628
Electrophoretic mobility shift assay (EMSA) 629
A Lightshift Chemiluminescent EMSA kit (Thermo) was used to perform EMSA 630
experiments according to the manufacturerrsquos instructions Single-strand 631
oligonucleotides were synthesized and biotinylated by GeneBio Biotech (Hangzhou 632
China) The details of the EMSA assay are provided in Ge et al (2017) The probes 633
used for EMSAs are listed in Supplemental Table S6 634
635
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
23
636
Yeast two-hybrid assay 637
The DUALhunter system (Dualsystems Biotech Switzerland) was used to investigate 638
the interaction between FaERF9 and FaMYB98 Full-length coding sequences of 639
FaERF9 and FaMYB98 were respectively cloned into pDHB1 bait vector and 640
pPR3-N prey vector sequences were verified and the bait plasmid was 641
co-transformed with prey plasmid into NMY51 in the combinations below 642
FaMYB98-pDHB1pPR3-N FaMYB98-pDHB1FaERF9-pPR3-N 643
FaMYB98-pDHB1pOst1-NubI FaERF9-pDHB1pPR3-N 644
FaERF9-pDHB1FaMYB98-pPR3-N and FaERF9-pDHB1pOst1-NubI (Li et al 645
2017) Transformed cells were spread onto the following plates DDO (SD 646
medium-Trp-Leu) QDO (SD medium-Trp-Leu-His-Ade) and QDO+3-AT (QDO 647
medium supplemented with 1 mM 3-amino-124-triazole) The control plasmid 648
pOst1-NubI was used to determine whether the bait was functional the pPR3-N prey 649
vector plasmid was used to test whether the bait displayed non-specific background 650
and positive interactions were indicated by the growth of yeast on QDO and 651
QDO+3-AT plates The Primers used in the DUALhunter assay are listed in 652
Supplemental Table S6 653
654
Bimolecular fluorescence complementation (BiFC) assays 655
Full-length FaERF9 and FaMYB98 respectively were cloned into sequences 656
encoding the N- and C- fragments of YFP protein (Lv et al 2014) All constructs 657
were transiently expressed in tobacco (N benthamiana) leaves by Agrobacterium 658
infiltration (EHA105) The YFP fluorescence of transfected leaves was imaged 40 h 659
after infiltration by using a Nikon A1-SHS confocal laser scanning microscope The 660
excitation wavelength for YFP was 488 nm and fluorescence was detected at 520ndash661
540 nm Primers used are listed in Supplemental Table S6 662
663
Statistics 664
A Studentrsquos two-tailed t test ( plt005 plt001 and plt0001) was used to 665
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
24
determine significant differences between two groups in this study Microsoft Excel 666
was used to perform linear regressive analysis significant differences were 667
determined by SPSS Statistics 200 and scatter plots were prepared with Origin80 668
Least significant difference (LSD) at the 5 level was calculated using Microsoft 669
Excel Figures were prepared with Origin80 (Microcal Software Inc Northampton 670
MA USA) The online tool MetaboAnalyst 36 (httpwwwmetaboanalystca) was 671
used to analyse the transcript abundance of the AP2ERF genes 672
673
Accession numbers 674
Sequence data from this article have been deposited in GenBank under the accession 675
numbers MH332903-MH333022 for AP2ERF genes in Fragaria times ananassa and 676
MH333023 for FaMYB98 GenBank numbers for FaQR and FaOMT were 677
AY1588361 (Raab et al 2006) and AF2204912 (Wein et al 2002) 678
679
Supplemental Material 680
Supplemental Figure S1 Phylogenetic analysis of FaAP2ERF and Arabidopsis 681
AP2ERF proteins 682
Supplemental Figure S2 Analysis of FaAP2ERF gene expression patterns in 683
strawberry fruit during development and ripening 684
Supplemental Figure S3 Contents of furanones in fruit of strawberry cultivars 685
Supplemental Figure S4 Relative expression of FaERF9 in FaERF9-FaMYB98- 686
and FaERF9-overexpressing fruits 687
Supplemental Figure S5 Subcellular localization of FaMYB98 688
Supplemental Figure S6 The combined activation effects of FaERF9FaMYB98 on 689
the FaOMT promoter 690
Supplemental Figure S7 Relative expression of FaOMT in 691
FaERF9-overexpressing fruits 692
Supplemental Table S1 AP2ERF superfamily genes in Fragaria times ananassa 693
Supplemental Table S2 Classification of the AP2ERF superfamily members in 694
Fragaria times ananassa 695
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
25
Supplemental Table S3 Furanone content in FaERF9-FaMYB98- and 696
FaERF9-overexpressing fruits 697
Supplemental Table S4 Primers used for reverse transcription quantitative PCR 698
(RT-qPCR) 699
Supplemental Table S5 Primers used to amplify the full-length coding sequences of 700
AP2ERF genes and FaMYB98 in strawberry (Fragaria times ananassa) 701
Supplemental Table S6 Primers used for vector construction 702
703
Acknowledgments 704
This research was supported by the National Key Research and Development 705
Program (2016YFD0400101) the Project of the Science and Technology Department 706
of Zhejiang Province (2016C04001) and the 111 Project (B17039) 707
708
Figure legends 709
Figure 1 Changes in furanone content and furanone biosynthetic genes during 710
strawberry (Fragaria times ananassa Duch cv Yuexin) fruit development and ripening 711
A Fruits were collected at four ripening stages G (green stage) T (turning stage) IR 712
(intermediate red stage) R (full red stage) B Changes in the contents of furaneol 713
(HDMF) and mesifurane (DMMF) HDMF content was calculated using a standard 714
curve of HDMF while DMMF content was calculated with an internal standard as the 715
reference C Expression levels of FaQR and FaOMT The expression levels of each 716
gene were calculated relative to corresponding values in the basal section at the R 717
stage SEs were calculated from three replicates and LSD values represent the least 718
significant differences at p = 005 719
Figure 2 Regulatory effects of FaAP2ERF on the promoter of FaQR LUCREN 720
values of the empty vector on FaQR promoter were used as the calibrator set as 1 721
and SEs were calculated from five replicates statistical significance was determined 722
by Studentrsquos two-tailed t test ( plt0001) 723
Figure 3 Expression and the subcellular localization of FaERF9 A The expression 724
levels were calculated relative to the levels in the basal section at the R stage B 725
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
26
Subcellular localization analysis was performed in tobacco leaves The tobacco used 726
in the assay was stably transformed with a specific nucleus localized red fluorescence 727
protein construct and the red fluorescence indicates the nucleus-localized signal 728
(NLS) Scale bar = 25 microm SEs were calculated from three replicates 729
Figure 4 Transient overexpression of FaERF9 in strawberry fruit A Relative 730
expression of FaQR and FaERF9 in FaERF9-OX fruit 7 days after infiltration The 731
expression was calculated relative to the average value in control (SK) fruits B 732
HDMF and DMMF content in FaERF9-OX fruit The content of both furanones 733
were quantified using the peak area of the internal standard (2-octanol) as the 734
reference SEs were calculated from three replicates Statistical significance was 735
determined by Studentrsquos two-tailed t test ( plt005 plt001 plt0001) 736
Figure 5 Scatter plots of 11 strawberry cultivars A Linear regression analysis 737
between FaERF9 expression and FaQR expression B Linear regression analysis 738
between FaERF9 expression and furanone content The relative expression was 739
normalized to that of the housekeeping gene FaRIB413 and furanone content was 740
calculated with internal standard as the reference Significant differences were 741
determined by SPSS Statistics 200 742
Figure 6 Interactions of FaERF9 and FaMYB98 with the FaQR promoter A Yeast 743
one-hybrid analysis of the interaction of FaERF9 and FaQR promoter B Yeast 744
one-hybrid analysis of the interaction of FaMYB98 and FaQR promoter C 745
Regulatory effect of FaMYB98 on the FaQR promoter Auto-activation was tested on 746
SD-Ura (synthetically defined medium without uracil) in presence of Aureobasidin A 747
(AbA) and physical interaction was determined on SD-Leu (synthetically defined 748
medium without leucine) in presence of AbA LUCREN values of the empty vector 749
on FaQR promoter were used as the calibrator set as 1 and error bars were calculated 750
from five replicates Statistical significance was determined by Studentrsquos two-tailed t 751
test ( plt005 plt001 plt0001) 752
Figure 7 Electrophoretic mobility shift assay of FaMYB98 binding to FaQR 753
promoter A The probe sequence used for EMSA and mutated nucleotides are 754
indicated with lowercase letters B Purified DNA-binding domain of FaMYB98 755
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
27
protein and biotin-labelled DNA probe were mixed and analysed on 6 native 756
polyacrylamide gels and then photographed Presence or absence of specific probes is 757
marked by the symbol + or - 758
Figure 8 The combined activation effects of FaERF9FaMYB98 on the FaQR 759
promoter LUCREN values obtained with the empty vector and FaQR promoter were 760
used as the calibrator set as 1 and error bars were calculated from five replicates 761
Figure 9 Yeast two-hybrid analysis of the protein-protein interactions between 762
FaMYB98 and FaERF9 Positive interactions were determined by the growth of 763
yeast cells on selection plates Bait with pOST acted as positive controls and bait with 764
pPR3 as negative controls DDO synthetically defined medium without tryptophan 765
and leucine QDO synthetically defined medium without tryptophan leucine 766
histidine and adenine QDO+3AT QDO medium supplemented with 1 mM 767
3-aminotriazole 768
Figure 10 BiFC analysis of the protein-protein interactions between FaMYB98 and 769
FaERF9 The pairs of fusion proteins tested were FaMYB98-YFPN+FaERF9-YFPC 770
FaERF9-YFPN+FaMYB98-YFPC FaMYB98-YFPN+FaMYB98-YFPC and 771
FaERF9-YFPN+FaERF9-YFPC The other combinations were negative controls 772
The tobacco used in the assay was stably transformed with a specific 773
nucleus-localized red fluorescence protein construct and the red fluorescence 774
indicated the nucleus-localized signal (NLS) Fluorescence of the yellow fluorescence 775
protein (YFP) visualized the interaction in vivo Scale bar = 25 microm 776
777
Literature Cited 778
779
Agarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression 780
of PgDREB2A transcription factor enhances abiotic stress tolerance and activates 781
downstream stress-responsive genes Mol Biol Rep 37 1125-1135 782
Araguumlez I Osorio S Hoffmann T Rambla JL Medina-Escobar N Granell A 783
Botella MAacute Schwab W Valpuesta V (2013) Eugenol production in achenes and 784
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28
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Plant Physiol 163 946-958 786
Carvalho RF Carvalho SD OrsquoGrady K Folta KM (2016) Agroinfiltration of 787
strawberry fruit mdash a powerful transient expression system for gene validation Curr 788
Plant Biol 6 19-37 789
Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic 790
(Amsterdam) 210 34-40 791
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating 792
RNA from pine trees Plant Mol Biol Rep 11 113-116 793
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC 794
Clark DG (2011) PhMYB4 fine-tunes the floral volatile signature of 795
Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143 796
Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz 797
EA Taylor MG Smits-Kroon MT Schuurink RC Haring MA Giovannoni J 798
Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic 799
pathway by ectopic expression of a MYB transcription factor in tomato fruit Plant 800
Cell 23 2738-2753 801
Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan 802
XW Yang ZY (2017) Differential responses of four biosynthetic pathways of 803
aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under 804
interaction of light and temperature Food Chem 221 356-364 805
Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of 806
differentially-expressed genes during somatic embryogenesis in Fragaria times 807
ananassa Duch lsquoBenihopprsquo J Hortic Sci Biotechnol 90 671-681 808
Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 809
transcriptionally regulates chilling-induced lignification of loquat fruit via physical 810
interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136 811
Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM 812
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proteins Plant J 39 513-526 814
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29
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) 815
Sucrose nonfermenting1-related protein kinase26 an ortholog of open stomata1 is 816
a negative regulator of strawberry fruit development and ripening Plant Physiol 817
167 915-930 818
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene 819
expression in strawberry fruit (Fragaria times ananassa) by agroinfiltration a rapid 820
assay for gene function analysis Plant J 48 818-826 821
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of 822
selected aroma-active compounds in strawberries by headspace solid-phase 823
microextraction gas chromatography and correlation with sensory descriptive 824
analysis J Food Sci 72 S487-S496 825
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid 826
plays an important role in the regulation of strawberry fruit ripening Plant Physiol 827
157 188-199 828
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of 829
NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes BMC 830
Plant Biol 6 20 831
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN 832
(2005) MYB98 is required for pollen tube guidance and synergid cell differentiation 833
in Arabidopsis Plant Cell 17 2981-2992 834
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional 835
characterization of enone oxidoreductases from strawberry and tomato fruit J 836
Agric Food Chem 55 6705-6711 837
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You 838
J-S Rohloff J Randall SK Alsheikh M (2012) Proteomic study of 839
low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ 840
in cold tolerance Plant Physiol 159 1787-1805 841
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional 842
characterization of four APETALA2-family genes (RAP26 RAP26L DREB19 843
and DREB26) in Arabidopsis Plant Mol Biol 75 107-127 844
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30
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon 845
J Gupta V (2013) An oxidoreductase from lsquoAlphonsorsquo mango catalyzing 846
biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494 847
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in 848
strawberries Z Lebensm-Unters Forsch 195 120-123 849
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X 850
(2015) Label-free quantitative proteomics to investigate strawberry fruit proteome 851
changes under controlled atmosphere and low temperature storage J Proteomics 852
120 44-57 853
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 854
cooperates with CitWRKY1 to participate in citric acid degradation via 855
up-regulation of CitAco3 J Exp Bot 68 3419-3426 856
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription 857
factor CitERF71 activates the terpene synthase gene CitTPS16 involved in the 858
synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938 859
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and 860
transcriptomic analysis of the AP2ERF superfamily in Vitis vinifera BMC 861
Genomics 11 719 862
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive 863
Factor (AP2ERF) transcription factors mediators of stress responses and 864
developmental programs New Phytol 199 639-649 865
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 866
interacting with EOBI negatively regulates fragrance biosynthesis in petunia 867
flowers New Phytol 215 1490-1502 868
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu 869
CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 in regulating 870
anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) 871
during anthocyanin biosynthesis Plant Cell Tissue Organ Cult 115 285-298 872
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31
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao 873
CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphate signaling and 874
homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597 875
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC 876
Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL 877
Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor 878
regulates eugenol production in ripe strawberry fruit receptacles Plant Physiol 168 879
598-614 880
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics 881
and volatile constituents of strawberry (cv Cigaline) during maturation J Agric 882
Food Chem 52 1248-1254 883
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS 884
(2012) Ethylene-responsive transcription factors interact with promoters of ADH 885
and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 886
63 6393-6405 887
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM 888
Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-Franco A 889
Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific 890
transcription factor FaDOF2 regulates the production of eugenol in ripe fruit 891
receptacles J Exp Bot 68 4529-4543 892
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) 893
Comparison and verification of the genes involved in ethylene biosynthesis and 894
signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44 895
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the 896
ERF gene family in Arabidopsis and rice Plant Physiol 140 411-432 897
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in 898
sour cherry and strawberry and the heterologous expression of CBF1 in strawberry 899
J Am Soc Hortic Sci 127 489-494 900
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech 901
JC Ohme-Takagi M Regad F Bouzayen M (2012) Functional analysis and 902
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32
binding affinity of tomato ethylene response factors provide insight on the 903
molecular bases of plant differential responses to ethylene BMC Plant Biol 12 190 904
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) 905
Methylpentoses are possible precursors of furanones in fruits Prikl Biokhim 906
Mikrobiol 28 123-127 907
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery 908
of synergid-expressed genes encoding filiform apparatus localized proteins Plant 909
Cell 19 2557-2568 910
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria 911
vesca L compared to those of cultivated berries Fragariatimes ananassa cv Senga 912
Sengana J Agric Food Chem 27 19-22 913
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W 914
Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of the strawberry 915
flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone 916
oxidoreductase Plant Cell 18 1023-1037 917
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L 918
Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim M Broun P Zhang 919
JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription 920
factors genome-wide comparative analysis among eukaryotes Science 290 921
2105-2110 922
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the 923
formation of 25-dimethyl-4-hydroxy-3(2H)-furanone in detached ripening 924
strawberry fruits J Agric Food Chem 46 1488-1493 925
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 926
25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in 927
strawberry fruits Phytochemistry 43 155-159 928
Schwab W (1998) Application of stable isotope ratio analysis explaining the 929
bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone in plants by a biological 930
maillard reaction J Agric Food Chem 46 2266ndash2269 931
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33
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) 932
Molecules 18 6936-6951 933
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard 934
products Recent Res Dev Phytochem 1 643-673 935
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL 936
Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJ Sims CA 937
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compositions a seasonal influence and effects on sensory perception PLoS One 9 939
e88446 940
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) 941
Identification phylogeny and transcript profiling of ERF family genes during 942
development and abiotic stress treatments in tomato Mol Genet Genomics 284 943
455-475 944
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) 945
CitAP210 activation of the terpene synthase CsTPS1 is associated with the 946
synthesis of (+)-valencene in lsquoNewhallrsquo orange J Exp Bot 67 4105-4115 947
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes 948
Dev Genes Evol 214 105-114 949
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K 950
Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the 951
key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151 952
Spitzer-Rimon B Farhi M Albo B Cnarsquoani A Ben Zvi MM Masci T Edelbaum 953
O Yu YX Shklarman E Ovadis M Vainstein A (2012) The R2R3-MYB-like 954
regulatory factor EOBI acting downstream of EOBII regulates scent production 955
by activating ODO1 and structural scent-related genes in petunia Plant Cell 24 956
5089-5105 957
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp 958
Bot 68 4407-4409 959
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla 960
JF Amaya I Giavalisco P Fernie AR Botella MA Valpuesta V (2015) Central 961
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34
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to ripening New Phytol 208 482-496 963
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 964
regulates fragrance biosynthesis in petunia flowers Plant Cell 17 1612-1624 965
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS 966
(2018) The potassium channel FaTPK1 plays a critical role in fruit quality 967
formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748 968
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) 969
Isolation cloning and expression of a multifunctional O-methyltransferase capable 970
of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma 971
compounds in strawberry fruits Plant J 31 755-765 972
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor 973
types their evolutionary origin and species distribution In A handbook of 974
transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular 975
Biochemistry 52 25-73 976
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of 977
odor (Buettner A Ed) Springer Cham 9-10 978
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS 979
(2014) Isolation classification and transcription profiles of the AP2ERF 980
transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271 981
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in 982
regulation of fruit quality Crit Rev Plant Sci 35 120-130 983
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ 984
Zhang SL Wu J (2017) Map-based cloning of the pear gene MYB114 identifies an 985
interaction with other transcription factors to coordinately regulate fruit 986
anthocyanin biosynthesis Plant J 92 437-451 987
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes 988
involved in regulating fruit ripening Plant Physiol 153 1280-1292 989
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
35
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) 990
Expression of ethylene response genes during persimmon fruit astringency removal 991
Planta 235 895-906 992
Zabetakis I Gramshaw JW Robinson DS (1999) 993
25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis and 994
biosynthesis-a review Food Chem 65 139-151 995
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci 996
Food Agric 74 421-434 997
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 998
an AP2ERF gene is a novel regulator of fruit lignification induced by chilling 999
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13
genes in octoploid strawberry (Supplemental Table S1) The number of predicted 336
AP2ERF genes (120) is comparable to those observed in other fruits including 337
tomato (112) Chinese plum (116) citrus (126) and peach (131) but lower than those 338
reported for grape (149) (Xie et al 2016) As shown in Supplemental Table S2 79 339
(95 genes) of the AP2ERF genes belong to the ERF family in strawberry constituting 340
the largest sub-family The members of this sub-family can be classified into 10 341
groups (group I to X) according to their sequence similarities to the Arabidopsis ERF 342
genes (Nakano et al 2006) The AP2 family encompasses the same number of genes 343
in Arabidopsis citrus and strawberry (eighteen) (Nakano et al 2006 Xie et al 2014) 344
and there are six RAV genes in strawberry which are highly conserved in dicots such 345
as Vitis vinifera Arabidopsis thaliana and Populus trichocarpa (Licausi et al 2010) 346
347
Role of FaERF9 in regulating the biosynthesis of HDMF a positive regulator 348
acting in an indirect manner 349
The large-scale screening of the AP2ERF superfamily in strawberry led to 350
identification of 11 ERFs and 1 RAV that trans-activated the FaQR promoter more 351
than two-fold with the highest activation caused by FaERF9 which trans-activated 352
the FaQR promoter (Figure 2) as well as up-regulating FaQR expression and furanone 353
production in transient overexpression assays (Figure 4) which has been extensively 354
used to explore the fruit-associated gene functions in strawberry (Han et al 2015 355
Medina-Puche et al 2015 Vallarino et al 2015 Carvalho et al 2016 Song et al 356
2016 Wang et al 2018) FaERF9 transcripts accumulate in the fruit apical section 357
before the basal section (Figure 3) a finding consistent with the actual changes in 358
furaneol content (Figure 1) and the expression of FaQR (Figure 1) The association 359
between FaERF9 transcripts and accumulation of furanones were also established 360
with different strawberry cultivars The correlation between FaERF9 and FaQR 361
expression as well as furanone content among cultivars supports a positive role of 362
FaERF9 in regulating furanone content (Figure 5) These results indicate that 363
FaERF9 transcript abundance may be a good indicator of the abundance of these 364
important flavour volatiles in fruits of different cultivars This should be considered as 365
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14
a method for high-throughput variety screening to replace direct measurement of 366
volatiles 367
368
FaERF9 is a member of the ERF group II family and is most closely related to the 369
Arabidopsis genes At1g44830 (ATERF014) At1g21910 (DREB26) and At1g77640 370
(Supplemental Figure S1) At1g44830 was observed to be strongly up-regulated in a 371
comprehensive microarray analysis of the root transcriptome following NaCl 372
exposure (Jiang and Deyholos 2006) At1g21910 (DREB26) was functionally 373
characterized as a trans-activator localized in the nucleus exhibiting tissue-specific 374
expression and participating in plant developmental processes as well as biotic andor 375
abiotic stress signalling (Krishnaswamy et al 2011) However none of these genes 376
have been reported as furanone regulators In strawberry another five genes 377
(FaERF6 FaERF7 FaERF8 FaERF10 and FaERF11) also belong to the same 378
group with FaERF8 also showing somewhat weaker activation activity towards the 379
FaQR promoter than FaERF9 The fact that FaERF9 could not bind directly to the 380
promoter of FaQR (Figure 6) indicates that it might function as an indirect regulator 381
of FaQR and furaneol biosynthesis 382
383
A FaERF9 and FaMYB98 complex is involved in regulating FaQR and furaneol 384
biosynthesis 385
The finding that FaERF9 could interact with FaMYB98 protein (Figures 9 and 386
Figure 10) and that FaMYB98 could physically bind to the FaQR promoter (Figure 6 387
and Figure 7) provides evidence for a regulatory mechanism whereby FaERF9 388
regulates FaQR and furaneol production as part of a complex with an MYB 389
transcription factor Since co-overexpression of FaERF9 and FaMYB98 resulted in 390
much higher activation activity towards FaQR we speculate that FaERF9 may 391
recruit FaMYB98 homologs in tobacco to activate the FaQR promoter (Figure 8) 392
FaOMT is another key gene for furanone biosynthesis and a potential target for 393
transcriptional activation However FaERF9 did not significantly activate the 394
FaOMT promoter in a dual-luciferase assay and the transcript level of FaOMT in the 395
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15
FaERF9-overexpressing fruits showed no significant difference from that in the 396
control (Supplemental Figure S6 Supplemental Figure S7) The FaOMT promoter 397
was significantly induced by FaMYB98 but no synergistic effect of FaERF9 and 398
FaMYB98 on the promoter was observed (Supplemental Figure S6) In previous 399
studies of the regulation of plant volatile compounds MYBs have been characterized 400
as being involved mainly in the regulation of the benzenoidphenylpropanoid pathway 401
that produces floral volatiles in petunia and eugenol in ripe strawberry fruit (Verdonk 402
et al 2005 Dal Cin et al 2011 Colquhoun et al 2011 Spitzer-Rimon et al 2012 403
Medina-Puche et al 2015) but their role in formation of volatiles from other 404
pathways has not been reported Our study demonstrates a role for MYB in the 405
synthesis of furaneol a carbohydrate-derived volatile compound and reveals the 406
synergistic interactions between an MYB and ERF in a transcription complex (Figure 407
8 Figure 9 and Figure 10) 408
409
Recent research has provided evidence for interactions between AP2ERF and MYB 410
transcription factors in regulating other aspects of fruit quality including texture 411
(EjAP2-1 and EjMYB Zeng et al 2015) and colour (PyERF3 and PyMYB114 Yao 412
et al 2017) A group VIII ERF has also recently been shown to interact with an MYB 413
to regulate floral scent production in petunia (Liu et al 2017) In strawberry fruit 414
DOF in combination with an MYB has been reported to be involved in the regulation 415
of eugenol production and the identification of this second transcription factor (DOF) 416
suggests that it is a good target in breeding for improved flavour (Molina-Hidalgo et 417
al 2017 Tieman 2017) Considering its important contribution to flavour in 418
strawberry and many other highly valued fruit crop species (pineapple tomato mango 419
etc) very little is known about regulation of furaneol synthesis Here we established 420
the role of FaERF9 in the regulation of HDMF synthesis by direct protein-protein 421
interactions with FaMYB98 to synergistically trans-activate FaQR The functional 422
identification of this complex enhances our knowledge of the regulation of volatile 423
compound synthesis and identifies a new AP2ERF-MYB complex Further 424
examination of the other ERFs that stimulated transcription from the FaQR promoter 425
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16
(Figure 2) may provide additional information about the complexity of this regulation 426
Overall this study provides important clues for understanding the transcriptional 427
regulation of HDMF synthesis and identifies specific transcription factors that are 428
likely to be good targets for molecular breeding for improved flavour 429
430
Conclusions 431
Screening of the AP2ERF superfamily in strawberry (Fragaria times ananassa) 432
identified candidate members capable of activating the FaQR promoter An ERF 433
transcription factor was identified as a positive regulator of HDMF synthesis in 434
strawberry fruit and the mechanism of activation was shown to involve an ERF-MYB 435
transcription complex that regulates transcription of FaQR leading to the biosynthesis 436
of HDMF the characteristic volatile compound which has a major influence on 437
strawberry aroma 438
439
Materials and Methods 440
441
Plant Materials and Growth conditions 442
The strawberry (Fragaria times ananassa cv lsquoYuexinrsquo an octoploid cultivar) fruit used in 443
this study were bred by Zhejiang Academy of Agricultural Sciences (Haining 444
Zhejiang) Fruits at various developmental and ripening stages including G (green) T 445
(turning) IR (intermediate red) and R (full red) were harvested (Figure 1) and 446
transported to the laboratory within 2 h Thirty-six fruits of uniform size and free of 447
visible defects were selected at each stage with twelve fruits in each biological 448
replicate After removing the calyces fruits were then divided into the basal and 449
apical sections which were sampled separately (Figure 1) They were rapidly cut into 450
pieces frozen immediately in liquid nitrogen and stored at -80deg C until use Red ripe 451
fruits of different strawberry cultivars (Fragaria times ananassa octoploid cultivars) 452
including lsquoYuelirsquo lsquoBenihoppersquo lsquoMengxiangrsquo lsquoAmaoursquo lsquo10-1-4rsquo lsquoAkihimersquo lsquoSweet 453
Charliersquo lsquo07-1-4rsquo lsquoDarselectrsquo lsquoYuexinrsquo and lsquoXuemeirsquo were also provided by Zhejiang 454
Academy of Agricultural Sciences For each cultivar the fruits of three biological 455
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
17
replicates were sampled frozen in liquid nitrogen and stored at -80deg C for further use 456
457
Tobacco plants (Nicotiana benthamiana) used for dual-luciferase assays and 458
subcellular localization analysis in this study were grown in a growth chamber with a 459
lightdark cycle of 16 h8 h at 24degC 460
461
Detection of DMMF and HDMF 462
Automated HS-SPME-GC-MS was performed to detect both furanones in lsquoYuexinrsquo 463
strawberry fruit (Zorrilla-Fontanesi et al 2012) Samples were ground into a powder 464
under liquid nitrogen for analysis 465
466
For the detection of DMMF (Figure 1) 05 g (fresh weight) of each sample was 467
weighed in the vial to which was added 1 mL of EDTA solution (100 mM pH 75) 1 468
mL of CaCl2 solution (mv = 20) and 20 microL of 2-octanol as the internal standard 469
(007 μgμL) The mixture was homogenized and the vial closed and placed on the 470
sample tray for analysis by CombiPAL autosampler (CTC Analytic CA USA) The 471
fruit volatiles were sampled by headspace solid-phase microextraction with a 65-μm 472
polydimethylsiloxane-divinylbenzene fibre (PDMS-DVB) Initially vials were 473
pre-incubated at 50degC for 10 min under continuous agitation (500 rpm) then volatiles 474
were extracted for 30 min at the same temperature and agitation speed After that the 475
fibre was desorbed in the GC injection port for 5 min in splitless mode The 7890A 476
GC chromatograph was equipped with a DB-5ms column (60 m times 250 μm times 1 μm 477
JampW Scientific Folsom CA USA) with helium as the carrier gas at a constant flow 478
of 12 mLmin The GC was programmed at an initial temperature of 35degC for 2 min 479
with a ramp of 5degC min up to 250degC and held for 5 min The injection port interface 480
and MS source temperatures were 250degC 260degC and 230degC respectively The 481
ionization potential was set at 70 eV recorded by a 5975B mass spectrometer (Agilent 482
Technologies JampW Scientific Folsom CA USA) and the scanning speed was 7 483
scanss The same method was used to analyse HDMF and DMMF in fruits from 484
different cultivars (Supplemental Figure S3) except for the sample preparation 485
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
18
procedure (Araguumlez et al 2013) briefly 05 g (fresh weight) of powdered fruit was 486
incubated at 30degC in a water bath for 5 min then 2 mL of NaCl (mv = 20) and 20 487
microL of 2-octanol as the internal standard (007 μgμL) were added and homogenized 488
489
For the detection of HDMF (Figure 1) and both furanones (Figure 4 and Supplemental 490
Table S3) a liquid-injection system equipped with CTC Pal ALS was used One gram 491
(fresh weight) of powdered fruit and 2 mL of NaCl (mv = 20) were homogenized in 492
a 10-mL tube and 300 μL of CH2Cl2 and 20 microL of 2-octanol (0766 μgμL) as the 493
internal standard were added to extract the volatiles the mixture was then 494
homogenized again The tubes were stored at room temperature for 20 min and 495
centrifuged at 12000 rpm for 5 min The subnatant was pipetted into a clean 15-mL 496
tube in which 20 mg of anhydrous sodium sulphate was added the tube was left 497
without shaking for half an hour Then 150 μL of the solution was transferred into a 498
GC vial and placed on the sample tray as described above Each sample (1 μL) was 499
injected using the autosampler and the analysis was accomplished by a 7890A 500
GC-MS system (Agilent Technologies JampW Scientific Folsom CA USA) equipped 501
with a DB-WAX column (30 m times 025 mm times 025 μm JampW) Helium (12 mLmin) 502
was used as a carrier gas The injection port (splitless injection mode) interface and 503
MS source temperatures were as described above The oven temperature was set at 504
60degC for 4 min then increased to 180degC at a rate of 4degCmin and maintained for 30 505
min DMMF was identified by comparison of electron ionization mass spectra and 506
retention time data with the data from the NISTEPANIH mass spectral library 507
(NIST-08 and Flavor) HDMF (Figure 1) was identified and qualified by comparison 508
with injected standard (Sigma) The quantitative analysis of both furanones (Figure 4 509
Supplemental Table S3 and Supplemental Figure S3) was determined using the peak 510
area of the internal standard as a reference based on total ion chromatogram (TIC) 511
512
RNA isolation and Reverse Transcription Quantitative PCR (RT-qPCR) 513
Total RNA from strawberry samples was isolated in this study using the CTAB 514
method (Chang et al 1993) Genomic DNA contamination was eliminated by 515
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
19
TURBO Dnase (Ambion) 1 μg of RNA was used to obtain cDNA using an IScriptTM 516
cDNA Synthesis Kit (Bio-Rad) The synthesized cDNA was diluted with water (120) 517
and 2 μL of diluted cDNA was used as the template for RT-qPCR Reactions were 518
performed in a total volume of 20 μL consisting of 10 μL of SYBR PCR supermix 519
(Bio-Rad) 1 μL of each primer (10 μM) 6 μL of DEPC-H2O and 2 μL of diluted 520
cDNA on CFX96 instrument (Bio-Rad) (Yin et al 2012) The oligonucleotide 521
primers for RT-qPCR analysis of genes including the AP2ERF FaQR and FaOMT 522
were designed according to the coding sequences of genes and the specificity was 523
verified before use (Min et al 2012) NCBIPrimer-BLAST was applied to design the 524
primers Relative expression levels were normalized to that of an internal controlmdashthe 525
interspacer 26S-18S strawberry RNA housekeeping gene FaRIB413 526
(Zorrilla-Fontanesi et al 2012) To investigate the differential expression of genes 527
during fruit development and ripening stages relative expression of each gene at the 528
R stage in the basal fruit section was set as 1 using the 2minus∆∆119862119879 method For transient 529
overexpression assay relative expression of control fruits with an empty vector (SK) 530
was set as 1 The primers used in RT-qPCR are listed in Supplemental Table S4 531
532
Gene isolation and analysis 533
Multiple database searches were performed to identify members of the strawberry 534
(Fragaria times ananassa) AP2ERF superfamily in the published strawberry databases 535
and annotations of Fragaria times ananassa and Fragaria times vesca by using the 536
AP2ERF DNA binding domain as a query sequence and 120 genes were identified 537
with AP2ERF domain(s) Based on the BLAST result primers (listed in 538
Supplemental Table S5) were used to amplify the coding full-length cDNAs of 539
AP2ERF genes The deduced amino acid sequences of AP2ERF proteins in 540
Arabidopsis thaliana used for construction of a phylogenetic tree were obtained from 541
the Arabidopsis Information Resource (TAIR) Alignment of the proteins was 542
performed using the neighbour-joining method in ClustalX (v181) and the 543
phylogenetic tree was constructed using FigTree (v131) 544
545
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
20
FaMYB98 was obtained by yeast one-hybrid screening sequencing and the full-length 546
sequences were predicted by BLAST Primers were designed (listed in Supplemental 547
Table S5) to amplify the full-length coding sequence 548
549
The promoter of FaQR was cloned by Genome Walking as previously described (Yin 550
et al 2010) and conserved cis-element motifs in the promoter were manually 551
searched 552
553
Conserved domains within the FaAP2ERF proteins and FaMYB98 were analysed by 554
CD-search (httpswwwncbinlmnihgovStructurecddwrpsbcgi) and cellular 555
locations of proteins including FaERF9 and FaMYB98 were predicted with the 556
WoLF PSORT program (httpswwwgenscriptcomwolf-psorthtml) 557
558
Dual-Luciferase Assays 559
In accordance with a previous protocol (Yin et al 2010) the full-length cDNAs of 560
FaAP2ERF or FaMYB98 transcription factors were cloned into pGreen II 0029 561
62-SK vector and the promoter of FaQR was cloned into pGreen II 0800-LUC vector 562
A luciferase gene from Renillia (REN) driven by a 35S promoter in the LUC vector 563
acted as a positive control The above constructs were transiently expressed in 564
Nicotiana benthamiana leaves by Agrobacterium-mediated infiltration (strain 565
GV3101) and the activity of the TFs on the promoter was measured on the third day 566
after infiltration indicated by the ratio of enzyme activities of firefly luciferase (LUC) 567
and renilla luciferase (REN) using a Modulus Luminometer (Promega Madison WI 568
USA) To determine the activity of a specific transcription factor towards the 569
promoter we mixed the Agrobacterium culture with 1 mL of TF and 100 μL of 570
promoter and the LUCREN value of the empty vector SK on the promoter was set as 571
1 as a calibrator To test the combined effect of two transcription factors on the 572
promoter to the Agrobacterium culture mixture we added 05 mL of each TF and 100 573
μL of promoter the effect of the mixtures that contained each transcription factor (05 574
mL) and empty vector SK (05 mL) was also tested on the promoter as a control 575
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
21
576
Subcellular localization analysis 577
35S-FaERF9-GFP and 35S-FaMYB98-GFP were transiently expressed in tobacco (N 578
benthamiana) leaves by Agrobacterium infiltration (EHA105) using the same method 579
as described in the dual-luciferase assay above The transiently infected leaves were 580
imaged on the third day after infiltration using a Nikon A1-SHS confocal laser 581
scanning microscope The excitation wavelength for GFP fluorescence was 488 nm 582
and fluorescence was detected at 490ndash520 nm The primers used for GFP construction 583
are listed in Supplemental Table S6 584
585
Transient overexpression in strawberry fruit 586
Transient overexpression of FaERF9 and an overexpression binary vector (pGreen II 587
0029 62-SK-FaERF9-FaMYB98) were performed in strawberry fruit using the 588
FaERF9-SK construct described above for the dual-luciferase assays and the binary 589
vector constructed according to Liu et al 2013 The transfection of fruit was carried 590
out at the G stage (Hoffmann et al 2006) The FaERF9-SK construct and binary 591
vector were individually electroporated into Agrobacterium tumefaciens GV3101 and 592
the Agrobacterium culture suspended in infiltration buffer was infiltrated into the 593
whole fruit using a syringe As a control treatment fruits were infiltrated with 594
Agrobacterium carrying an empty vector SK under the same transfection conditions 595
Fruits were left attached to the plants and harvested on the seventh day after 596
infiltration Fruits of three biological replicates were sampled for further analysis 597
598
Yeast one-hybrid assay 599
In order to identify proteins that bind to the FaQR promoter the Matchmaker Gold 600
Yeast One-hybrid Library Screening System (Clontech USA) was used The sequence 601
of the FaQR promoter was cloned into the pAbAi vector and the construct was 602
integrated into the genome of the Y1HGold yeast strain A mixture of total RNA from 603
strawberry fruit at four stages (G T IR R) was used to construct the prey cDNA 604
library (TaKaRa) The background AbAr expression of Y1HGold FaQR-pAbAi strain 605
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
22
was tested according to the system user manual and then screening for protein-DNA 606
interactions was carried out Furthermore the full length of each transcription factor 607
was separately cloned into pGADT7 AD vector to confirm the screening results The 608
relationship between FaERF9 and FaQR promoter was also examined individually 609
Primers used in this assay are listed in Supplemental Table S6 610
611
Expression and purification of FaMYB98 recombinant protein 612
A 405-bp region spanning the DNA-binding domain of FaMYB98 was amplified 613
from FaMYB98 cDNA and cloned into a pET6timesHN vector (Clontech Palo CA USA) 614
to generate the recombinant N-terminal His-tagged protein the primers used are listed 615
in Supplemental Table S6 The resulting construct was sequenced and introduced into 616
Escherichia coli strain Rosetta 2(DE3)pLysS (Novagen) Ten millilitres of the 617
overnight culture was combined with 500 mL of an LB liquid medium (100 μgmL 618
ampicillin and 34 μgmL chloramphenicol) as described (Li et al 2017) Isopropyl 619
β-D-1-thiogalactopyranoside (IPTG) was added to a final concentration of 1 mM and 620
the bacterial culture was incubated at 18degC at 150 rpm for 18 h Then the cells were 621
harvested using a centrifuge and resuspended in 1times PBS buffer (Sangon Biotech) 622
after which they were disrupted by sonication and the supernatant was purified using 623
a HisTALONTM Gravity Column (Clontech) according to the user manual The PD-10 624
Desalting column (GE Healthcare) was then used for buffer change and sample 625
clean-up of proteins according to the gravity protocol SDS-PAGE was performed and 626
the protein was visualized using Coomassie brilliant blue 627
628
Electrophoretic mobility shift assay (EMSA) 629
A Lightshift Chemiluminescent EMSA kit (Thermo) was used to perform EMSA 630
experiments according to the manufacturerrsquos instructions Single-strand 631
oligonucleotides were synthesized and biotinylated by GeneBio Biotech (Hangzhou 632
China) The details of the EMSA assay are provided in Ge et al (2017) The probes 633
used for EMSAs are listed in Supplemental Table S6 634
635
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
23
636
Yeast two-hybrid assay 637
The DUALhunter system (Dualsystems Biotech Switzerland) was used to investigate 638
the interaction between FaERF9 and FaMYB98 Full-length coding sequences of 639
FaERF9 and FaMYB98 were respectively cloned into pDHB1 bait vector and 640
pPR3-N prey vector sequences were verified and the bait plasmid was 641
co-transformed with prey plasmid into NMY51 in the combinations below 642
FaMYB98-pDHB1pPR3-N FaMYB98-pDHB1FaERF9-pPR3-N 643
FaMYB98-pDHB1pOst1-NubI FaERF9-pDHB1pPR3-N 644
FaERF9-pDHB1FaMYB98-pPR3-N and FaERF9-pDHB1pOst1-NubI (Li et al 645
2017) Transformed cells were spread onto the following plates DDO (SD 646
medium-Trp-Leu) QDO (SD medium-Trp-Leu-His-Ade) and QDO+3-AT (QDO 647
medium supplemented with 1 mM 3-amino-124-triazole) The control plasmid 648
pOst1-NubI was used to determine whether the bait was functional the pPR3-N prey 649
vector plasmid was used to test whether the bait displayed non-specific background 650
and positive interactions were indicated by the growth of yeast on QDO and 651
QDO+3-AT plates The Primers used in the DUALhunter assay are listed in 652
Supplemental Table S6 653
654
Bimolecular fluorescence complementation (BiFC) assays 655
Full-length FaERF9 and FaMYB98 respectively were cloned into sequences 656
encoding the N- and C- fragments of YFP protein (Lv et al 2014) All constructs 657
were transiently expressed in tobacco (N benthamiana) leaves by Agrobacterium 658
infiltration (EHA105) The YFP fluorescence of transfected leaves was imaged 40 h 659
after infiltration by using a Nikon A1-SHS confocal laser scanning microscope The 660
excitation wavelength for YFP was 488 nm and fluorescence was detected at 520ndash661
540 nm Primers used are listed in Supplemental Table S6 662
663
Statistics 664
A Studentrsquos two-tailed t test ( plt005 plt001 and plt0001) was used to 665
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
24
determine significant differences between two groups in this study Microsoft Excel 666
was used to perform linear regressive analysis significant differences were 667
determined by SPSS Statistics 200 and scatter plots were prepared with Origin80 668
Least significant difference (LSD) at the 5 level was calculated using Microsoft 669
Excel Figures were prepared with Origin80 (Microcal Software Inc Northampton 670
MA USA) The online tool MetaboAnalyst 36 (httpwwwmetaboanalystca) was 671
used to analyse the transcript abundance of the AP2ERF genes 672
673
Accession numbers 674
Sequence data from this article have been deposited in GenBank under the accession 675
numbers MH332903-MH333022 for AP2ERF genes in Fragaria times ananassa and 676
MH333023 for FaMYB98 GenBank numbers for FaQR and FaOMT were 677
AY1588361 (Raab et al 2006) and AF2204912 (Wein et al 2002) 678
679
Supplemental Material 680
Supplemental Figure S1 Phylogenetic analysis of FaAP2ERF and Arabidopsis 681
AP2ERF proteins 682
Supplemental Figure S2 Analysis of FaAP2ERF gene expression patterns in 683
strawberry fruit during development and ripening 684
Supplemental Figure S3 Contents of furanones in fruit of strawberry cultivars 685
Supplemental Figure S4 Relative expression of FaERF9 in FaERF9-FaMYB98- 686
and FaERF9-overexpressing fruits 687
Supplemental Figure S5 Subcellular localization of FaMYB98 688
Supplemental Figure S6 The combined activation effects of FaERF9FaMYB98 on 689
the FaOMT promoter 690
Supplemental Figure S7 Relative expression of FaOMT in 691
FaERF9-overexpressing fruits 692
Supplemental Table S1 AP2ERF superfamily genes in Fragaria times ananassa 693
Supplemental Table S2 Classification of the AP2ERF superfamily members in 694
Fragaria times ananassa 695
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
25
Supplemental Table S3 Furanone content in FaERF9-FaMYB98- and 696
FaERF9-overexpressing fruits 697
Supplemental Table S4 Primers used for reverse transcription quantitative PCR 698
(RT-qPCR) 699
Supplemental Table S5 Primers used to amplify the full-length coding sequences of 700
AP2ERF genes and FaMYB98 in strawberry (Fragaria times ananassa) 701
Supplemental Table S6 Primers used for vector construction 702
703
Acknowledgments 704
This research was supported by the National Key Research and Development 705
Program (2016YFD0400101) the Project of the Science and Technology Department 706
of Zhejiang Province (2016C04001) and the 111 Project (B17039) 707
708
Figure legends 709
Figure 1 Changes in furanone content and furanone biosynthetic genes during 710
strawberry (Fragaria times ananassa Duch cv Yuexin) fruit development and ripening 711
A Fruits were collected at four ripening stages G (green stage) T (turning stage) IR 712
(intermediate red stage) R (full red stage) B Changes in the contents of furaneol 713
(HDMF) and mesifurane (DMMF) HDMF content was calculated using a standard 714
curve of HDMF while DMMF content was calculated with an internal standard as the 715
reference C Expression levels of FaQR and FaOMT The expression levels of each 716
gene were calculated relative to corresponding values in the basal section at the R 717
stage SEs were calculated from three replicates and LSD values represent the least 718
significant differences at p = 005 719
Figure 2 Regulatory effects of FaAP2ERF on the promoter of FaQR LUCREN 720
values of the empty vector on FaQR promoter were used as the calibrator set as 1 721
and SEs were calculated from five replicates statistical significance was determined 722
by Studentrsquos two-tailed t test ( plt0001) 723
Figure 3 Expression and the subcellular localization of FaERF9 A The expression 724
levels were calculated relative to the levels in the basal section at the R stage B 725
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
26
Subcellular localization analysis was performed in tobacco leaves The tobacco used 726
in the assay was stably transformed with a specific nucleus localized red fluorescence 727
protein construct and the red fluorescence indicates the nucleus-localized signal 728
(NLS) Scale bar = 25 microm SEs were calculated from three replicates 729
Figure 4 Transient overexpression of FaERF9 in strawberry fruit A Relative 730
expression of FaQR and FaERF9 in FaERF9-OX fruit 7 days after infiltration The 731
expression was calculated relative to the average value in control (SK) fruits B 732
HDMF and DMMF content in FaERF9-OX fruit The content of both furanones 733
were quantified using the peak area of the internal standard (2-octanol) as the 734
reference SEs were calculated from three replicates Statistical significance was 735
determined by Studentrsquos two-tailed t test ( plt005 plt001 plt0001) 736
Figure 5 Scatter plots of 11 strawberry cultivars A Linear regression analysis 737
between FaERF9 expression and FaQR expression B Linear regression analysis 738
between FaERF9 expression and furanone content The relative expression was 739
normalized to that of the housekeeping gene FaRIB413 and furanone content was 740
calculated with internal standard as the reference Significant differences were 741
determined by SPSS Statistics 200 742
Figure 6 Interactions of FaERF9 and FaMYB98 with the FaQR promoter A Yeast 743
one-hybrid analysis of the interaction of FaERF9 and FaQR promoter B Yeast 744
one-hybrid analysis of the interaction of FaMYB98 and FaQR promoter C 745
Regulatory effect of FaMYB98 on the FaQR promoter Auto-activation was tested on 746
SD-Ura (synthetically defined medium without uracil) in presence of Aureobasidin A 747
(AbA) and physical interaction was determined on SD-Leu (synthetically defined 748
medium without leucine) in presence of AbA LUCREN values of the empty vector 749
on FaQR promoter were used as the calibrator set as 1 and error bars were calculated 750
from five replicates Statistical significance was determined by Studentrsquos two-tailed t 751
test ( plt005 plt001 plt0001) 752
Figure 7 Electrophoretic mobility shift assay of FaMYB98 binding to FaQR 753
promoter A The probe sequence used for EMSA and mutated nucleotides are 754
indicated with lowercase letters B Purified DNA-binding domain of FaMYB98 755
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
27
protein and biotin-labelled DNA probe were mixed and analysed on 6 native 756
polyacrylamide gels and then photographed Presence or absence of specific probes is 757
marked by the symbol + or - 758
Figure 8 The combined activation effects of FaERF9FaMYB98 on the FaQR 759
promoter LUCREN values obtained with the empty vector and FaQR promoter were 760
used as the calibrator set as 1 and error bars were calculated from five replicates 761
Figure 9 Yeast two-hybrid analysis of the protein-protein interactions between 762
FaMYB98 and FaERF9 Positive interactions were determined by the growth of 763
yeast cells on selection plates Bait with pOST acted as positive controls and bait with 764
pPR3 as negative controls DDO synthetically defined medium without tryptophan 765
and leucine QDO synthetically defined medium without tryptophan leucine 766
histidine and adenine QDO+3AT QDO medium supplemented with 1 mM 767
3-aminotriazole 768
Figure 10 BiFC analysis of the protein-protein interactions between FaMYB98 and 769
FaERF9 The pairs of fusion proteins tested were FaMYB98-YFPN+FaERF9-YFPC 770
FaERF9-YFPN+FaMYB98-YFPC FaMYB98-YFPN+FaMYB98-YFPC and 771
FaERF9-YFPN+FaERF9-YFPC The other combinations were negative controls 772
The tobacco used in the assay was stably transformed with a specific 773
nucleus-localized red fluorescence protein construct and the red fluorescence 774
indicated the nucleus-localized signal (NLS) Fluorescence of the yellow fluorescence 775
protein (YFP) visualized the interaction in vivo Scale bar = 25 microm 776
777
Literature Cited 778
779
Agarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression 780
of PgDREB2A transcription factor enhances abiotic stress tolerance and activates 781
downstream stress-responsive genes Mol Biol Rep 37 1125-1135 782
Araguumlez I Osorio S Hoffmann T Rambla JL Medina-Escobar N Granell A 783
Botella MAacute Schwab W Valpuesta V (2013) Eugenol production in achenes and 784
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
28
receptacles of strawberry fruits is catalyzed by synthases exhibiting distinct kinetics 785
Plant Physiol 163 946-958 786
Carvalho RF Carvalho SD OrsquoGrady K Folta KM (2016) Agroinfiltration of 787
strawberry fruit mdash a powerful transient expression system for gene validation Curr 788
Plant Biol 6 19-37 789
Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic 790
(Amsterdam) 210 34-40 791
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating 792
RNA from pine trees Plant Mol Biol Rep 11 113-116 793
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC 794
Clark DG (2011) PhMYB4 fine-tunes the floral volatile signature of 795
Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143 796
Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz 797
EA Taylor MG Smits-Kroon MT Schuurink RC Haring MA Giovannoni J 798
Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic 799
pathway by ectopic expression of a MYB transcription factor in tomato fruit Plant 800
Cell 23 2738-2753 801
Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan 802
XW Yang ZY (2017) Differential responses of four biosynthetic pathways of 803
aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under 804
interaction of light and temperature Food Chem 221 356-364 805
Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of 806
differentially-expressed genes during somatic embryogenesis in Fragaria times 807
ananassa Duch lsquoBenihopprsquo J Hortic Sci Biotechnol 90 671-681 808
Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 809
transcriptionally regulates chilling-induced lignification of loquat fruit via physical 810
interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136 811
Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM 812
(2004) Functional interactions between a glutamine synthetase promoter and MYB 813
proteins Plant J 39 513-526 814
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
29
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) 815
Sucrose nonfermenting1-related protein kinase26 an ortholog of open stomata1 is 816
a negative regulator of strawberry fruit development and ripening Plant Physiol 817
167 915-930 818
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene 819
expression in strawberry fruit (Fragaria times ananassa) by agroinfiltration a rapid 820
assay for gene function analysis Plant J 48 818-826 821
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of 822
selected aroma-active compounds in strawberries by headspace solid-phase 823
microextraction gas chromatography and correlation with sensory descriptive 824
analysis J Food Sci 72 S487-S496 825
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid 826
plays an important role in the regulation of strawberry fruit ripening Plant Physiol 827
157 188-199 828
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of 829
NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes BMC 830
Plant Biol 6 20 831
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN 832
(2005) MYB98 is required for pollen tube guidance and synergid cell differentiation 833
in Arabidopsis Plant Cell 17 2981-2992 834
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional 835
characterization of enone oxidoreductases from strawberry and tomato fruit J 836
Agric Food Chem 55 6705-6711 837
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You 838
J-S Rohloff J Randall SK Alsheikh M (2012) Proteomic study of 839
low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ 840
in cold tolerance Plant Physiol 159 1787-1805 841
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional 842
characterization of four APETALA2-family genes (RAP26 RAP26L DREB19 843
and DREB26) in Arabidopsis Plant Mol Biol 75 107-127 844
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
30
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon 845
J Gupta V (2013) An oxidoreductase from lsquoAlphonsorsquo mango catalyzing 846
biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494 847
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in 848
strawberries Z Lebensm-Unters Forsch 195 120-123 849
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X 850
(2015) Label-free quantitative proteomics to investigate strawberry fruit proteome 851
changes under controlled atmosphere and low temperature storage J Proteomics 852
120 44-57 853
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 854
cooperates with CitWRKY1 to participate in citric acid degradation via 855
up-regulation of CitAco3 J Exp Bot 68 3419-3426 856
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription 857
factor CitERF71 activates the terpene synthase gene CitTPS16 involved in the 858
synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938 859
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and 860
transcriptomic analysis of the AP2ERF superfamily in Vitis vinifera BMC 861
Genomics 11 719 862
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive 863
Factor (AP2ERF) transcription factors mediators of stress responses and 864
developmental programs New Phytol 199 639-649 865
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 866
interacting with EOBI negatively regulates fragrance biosynthesis in petunia 867
flowers New Phytol 215 1490-1502 868
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu 869
CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 in regulating 870
anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) 871
during anthocyanin biosynthesis Plant Cell Tissue Organ Cult 115 285-298 872
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
31
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao 873
CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphate signaling and 874
homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597 875
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC 876
Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL 877
Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor 878
regulates eugenol production in ripe strawberry fruit receptacles Plant Physiol 168 879
598-614 880
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics 881
and volatile constituents of strawberry (cv Cigaline) during maturation J Agric 882
Food Chem 52 1248-1254 883
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS 884
(2012) Ethylene-responsive transcription factors interact with promoters of ADH 885
and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 886
63 6393-6405 887
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM 888
Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-Franco A 889
Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific 890
transcription factor FaDOF2 regulates the production of eugenol in ripe fruit 891
receptacles J Exp Bot 68 4529-4543 892
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) 893
Comparison and verification of the genes involved in ethylene biosynthesis and 894
signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44 895
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the 896
ERF gene family in Arabidopsis and rice Plant Physiol 140 411-432 897
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in 898
sour cherry and strawberry and the heterologous expression of CBF1 in strawberry 899
J Am Soc Hortic Sci 127 489-494 900
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech 901
JC Ohme-Takagi M Regad F Bouzayen M (2012) Functional analysis and 902
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
32
binding affinity of tomato ethylene response factors provide insight on the 903
molecular bases of plant differential responses to ethylene BMC Plant Biol 12 190 904
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) 905
Methylpentoses are possible precursors of furanones in fruits Prikl Biokhim 906
Mikrobiol 28 123-127 907
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery 908
of synergid-expressed genes encoding filiform apparatus localized proteins Plant 909
Cell 19 2557-2568 910
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria 911
vesca L compared to those of cultivated berries Fragariatimes ananassa cv Senga 912
Sengana J Agric Food Chem 27 19-22 913
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W 914
Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of the strawberry 915
flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone 916
oxidoreductase Plant Cell 18 1023-1037 917
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L 918
Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim M Broun P Zhang 919
JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription 920
factors genome-wide comparative analysis among eukaryotes Science 290 921
2105-2110 922
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the 923
formation of 25-dimethyl-4-hydroxy-3(2H)-furanone in detached ripening 924
strawberry fruits J Agric Food Chem 46 1488-1493 925
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 926
25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in 927
strawberry fruits Phytochemistry 43 155-159 928
Schwab W (1998) Application of stable isotope ratio analysis explaining the 929
bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone in plants by a biological 930
maillard reaction J Agric Food Chem 46 2266ndash2269 931
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33
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) 932
Molecules 18 6936-6951 933
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard 934
products Recent Res Dev Phytochem 1 643-673 935
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL 936
Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJ Sims CA 937
Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical 938
compositions a seasonal influence and effects on sensory perception PLoS One 9 939
e88446 940
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) 941
Identification phylogeny and transcript profiling of ERF family genes during 942
development and abiotic stress treatments in tomato Mol Genet Genomics 284 943
455-475 944
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) 945
CitAP210 activation of the terpene synthase CsTPS1 is associated with the 946
synthesis of (+)-valencene in lsquoNewhallrsquo orange J Exp Bot 67 4105-4115 947
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes 948
Dev Genes Evol 214 105-114 949
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K 950
Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the 951
key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151 952
Spitzer-Rimon B Farhi M Albo B Cnarsquoani A Ben Zvi MM Masci T Edelbaum 953
O Yu YX Shklarman E Ovadis M Vainstein A (2012) The R2R3-MYB-like 954
regulatory factor EOBI acting downstream of EOBII regulates scent production 955
by activating ODO1 and structural scent-related genes in petunia Plant Cell 24 956
5089-5105 957
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp 958
Bot 68 4407-4409 959
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla 960
JF Amaya I Giavalisco P Fernie AR Botella MA Valpuesta V (2015) Central 961
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34
role of FaGAMYB in the transition of the strawberry receptacle from development 962
to ripening New Phytol 208 482-496 963
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 964
regulates fragrance biosynthesis in petunia flowers Plant Cell 17 1612-1624 965
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS 966
(2018) The potassium channel FaTPK1 plays a critical role in fruit quality 967
formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748 968
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) 969
Isolation cloning and expression of a multifunctional O-methyltransferase capable 970
of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma 971
compounds in strawberry fruits Plant J 31 755-765 972
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor 973
types their evolutionary origin and species distribution In A handbook of 974
transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular 975
Biochemistry 52 25-73 976
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of 977
odor (Buettner A Ed) Springer Cham 9-10 978
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS 979
(2014) Isolation classification and transcription profiles of the AP2ERF 980
transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271 981
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in 982
regulation of fruit quality Crit Rev Plant Sci 35 120-130 983
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ 984
Zhang SL Wu J (2017) Map-based cloning of the pear gene MYB114 identifies an 985
interaction with other transcription factors to coordinately regulate fruit 986
anthocyanin biosynthesis Plant J 92 437-451 987
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes 988
involved in regulating fruit ripening Plant Physiol 153 1280-1292 989
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35
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) 990
Expression of ethylene response genes during persimmon fruit astringency removal 991
Planta 235 895-906 992
Zabetakis I Gramshaw JW Robinson DS (1999) 993
25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis and 994
biosynthesis-a review Food Chem 65 139-151 995
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci 996
Food Agric 74 421-434 997
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 998
an AP2ERF gene is a novel regulator of fruit lignification induced by chilling 999
injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1000
1325-1334 1001
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation 1002
classification and transcription profiles of the Ethylene Response Factors (ERFs) in 1003
ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215 1004
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML 1005
(2012) Genome-wide analysis of the AP2ERF superfamily in peach (Prunus 1006
persica) Genet Mol Res 11 4788-4809 1007
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and 1008
expression analysis of a CRTDRE-binding factor gene FaCBF1 from Fragaria times 1009
ananassa Acta Hortic 41 240-248 1010
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The 1011
Arabidopsis AP2ERF transcription factor RAP26 participates in ABA salt and 1012
osmotic stress responses Gene 457 1-12 1013
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B 1014
Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) Genome-wide 1015
analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic 1016
(Amsterdam) 123 73-81 1017
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF 1018
Valpuesta V Botella MA Granell A Amaya I (2012) Genetic analysis of 1019
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36
strawberry fruit aroma and identification of O-methyltransferase FaOMT as the 1020
locus controlling natural variation in mesifurane content Plant Physiol 159 1021
851-870 1022
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
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Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan XW Yang ZY (2017) Differential responses of fourbiosynthetic pathways of aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under interaction of light andtemperature Food Chem 221 356-364
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Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of differentially-expressed genes during somatic embryogenesis inFragaria times ananassa Duch Benihopp J Hortic Sci Biotechnol 90 671-681
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Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 transcriptionally regulates chilling-induced lignification ofloquat fruit via physical interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM (2004) Functional interactions between a glutaminesynthetase promoter and MYB proteins Plant J 39 513-526
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) Sucrose nonfermenting1-related protein kinase26 anortholog of open stomata1 is a negative regulator of strawberry fruit development and ripening Plant Physiol 167 915-930
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene expression in strawberry fruit (Fragaria times ananassa) byagroinfiltration a rapid assay for gene function analysis Plant J 48 818-826
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of selected aroma-active compounds in strawberries byheadspace solid-phase microextraction gas chromatography and correlation with sensory descriptive analysis J Food Sci 72 S487-S496
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid plays an important role in the regulation of strawberry fruitripening Plant Physiol 157 188-199
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of NaCl-stressed Arabidopsis roots reveals novel classes ofresponsive genes BMC Plant Biol 6 20
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN (2005) MYB98 is required for pollen tube guidance andsynergid cell differentiation in Arabidopsis Plant Cell 17 2981-2992
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional characterization of enone oxidoreductases from strawberry andtomato fruit J Agric Food Chem 55 6705-6711
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You J-S Rohloff J Randall SK Alsheikh M (2012) Proteomicstudy of low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ in cold tolerance Plant Physiol 159 1787-1805
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional characterization of four APETALA2-family genes (RAP26 RAP26LDREB19 and DREB26) in Arabidopsis Plant Mol Biol 75 107-127
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon J Gupta V (2013) An oxidoreductase from Alphonsomango catalyzing biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in strawberries Z Lebensm-Unters Forsch 195 120-123Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X (2015) Label-free quantitative proteomics to investigatestrawberry fruit proteome changes under controlled atmosphere and low temperature storage J Proteomics 120 44-57
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 cooperates with CitWRKY1 to participate in citric aciddegradation via up-regulation of CitAco3 J Exp Bot 68 3419-3426
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription factor CitERF71 activates the terpene synthase geneCitTPS16 involved in the synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and transcriptomic analysis of the AP2ERF superfamily inVitis vinifera BMC Genomics 11 719
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive Factor (AP2ERF) transcription factors mediators of stressresponses and developmental programs New Phytol 199 639-649
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 interacting with EOBI negatively regulates fragrancebiosynthesis in petunia flowers New Phytol 215 1490-1502
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 inregulating anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) during anthocyanin biosynthesis Plant CellTissue Organ Cult 115 285-298
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title wwwplantphysiolorgon February 25 2020 - Published by Downloaded from
Copyright copy 2018 American Society of Plant Biologists All rights reserved
Google Scholar Author Only Title Only Author and Title
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphatesignaling and homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor regulates eugenol production in ripe strawberry fruitreceptacles Plant Physiol 168 598-614
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics and volatile constituents of strawberry (cv Cigaline)during maturation J Agric Food Chem 52 1248-1254
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS (2012) Ethylene-responsive transcription factors interact withpromoters of ADH and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 63 6393-6405
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-FrancoA Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific transcription factor FaDOF2 regulates the production ofeugenol in ripe fruit receptacles J Exp Bot 68 4529-4543
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) Comparison and verification of the genes involved in ethylenebiosynthesis and signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice Plant Physiol140 411-432
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in sour cherry and strawberry and the heterologousexpression of CBF1 in strawberry J Am Soc Hortic Sci 127 489-494
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech JC Ohme-Takagi M Regad F Bouzayen M (2012)Functional analysis and binding affinity of tomato ethylene response factors provide insight on the molecular bases of plant differentialresponses to ethylene BMC Plant Biol 12 190
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) Methylpentoses are possible precursors of furanones in fruits PriklBiokhim Mikrobiol 28 123-127
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery of synergid-expressed genes encoding filiformapparatus localized proteins Plant Cell 19 2557-2568
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria vesca L compared to those of cultivated berriesFragariatimes ananassa cv Senga Sengana J Agric Food Chem 27 19-22
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Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of thestrawberry flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone oxidoreductase Plant Cell 18 1023-1037
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim MBroun P Zhang JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription factors genome-wide comparative analysisamong eukaryotes Science 290 2105-2110
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
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Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the formation of 25-dimethyl-4-hydroxy-3(2H)-furanonein detached ripening strawberry fruits J Agric Food Chem 46 1488-1493
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Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in strawberry fruits Phytochemistry 43 155-159
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (1998) Application of stable isotope ratio analysis explaining the bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone inplants by a biological maillard reaction J Agric Food Chem 46 2266ndash2269
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) Molecules 18 6936-6951Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard products Recent Res Dev Phytochem 1 643-673Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJSims CA Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical compositions a seasonal influence and effects on sensoryperception PLoS One 9 e88446
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) Identification phylogeny and transcript profiling of ERFfamily genes during development and abiotic stress treatments in tomato Mol Genet Genomics 284 455-475
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Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) CitAP210 activation of the terpene synthase CsTPS1 isassociated with the synthesis of (+)-valencene in Newhall orange J Exp Bot 67 4105-4115
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Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes Dev Genes Evol 214 105-114Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151
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Spitzer-Rimon B Farhi M Albo B Cnaani A Ben Zvi MM Masci T Edelbaum O Yu YX Shklarman E Ovadis M Vainstein A (2012) TheR2R3-MYB-like regulatory factor EOBI acting downstream of EOBII regulates scent production by activating ODO1 and structuralscent-related genes in petunia Plant Cell 24 5089-5105
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Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp Bot 68 4407-4409Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla JF Amaya I Giavalisco P Fernie AR Botella MAValpuesta V (2015) Central role of FaGAMYB in the transition of the strawberry receptacle from development to ripening New Phytol208 482-496
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Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) Isolation cloning and expression of a multifunctional O- wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma compounds in strawberry fruitsPlant J 31 755-765
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Genome-wide analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic (Amsterdam) 123 73-81Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
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wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
14
a method for high-throughput variety screening to replace direct measurement of 366
volatiles 367
368
FaERF9 is a member of the ERF group II family and is most closely related to the 369
Arabidopsis genes At1g44830 (ATERF014) At1g21910 (DREB26) and At1g77640 370
(Supplemental Figure S1) At1g44830 was observed to be strongly up-regulated in a 371
comprehensive microarray analysis of the root transcriptome following NaCl 372
exposure (Jiang and Deyholos 2006) At1g21910 (DREB26) was functionally 373
characterized as a trans-activator localized in the nucleus exhibiting tissue-specific 374
expression and participating in plant developmental processes as well as biotic andor 375
abiotic stress signalling (Krishnaswamy et al 2011) However none of these genes 376
have been reported as furanone regulators In strawberry another five genes 377
(FaERF6 FaERF7 FaERF8 FaERF10 and FaERF11) also belong to the same 378
group with FaERF8 also showing somewhat weaker activation activity towards the 379
FaQR promoter than FaERF9 The fact that FaERF9 could not bind directly to the 380
promoter of FaQR (Figure 6) indicates that it might function as an indirect regulator 381
of FaQR and furaneol biosynthesis 382
383
A FaERF9 and FaMYB98 complex is involved in regulating FaQR and furaneol 384
biosynthesis 385
The finding that FaERF9 could interact with FaMYB98 protein (Figures 9 and 386
Figure 10) and that FaMYB98 could physically bind to the FaQR promoter (Figure 6 387
and Figure 7) provides evidence for a regulatory mechanism whereby FaERF9 388
regulates FaQR and furaneol production as part of a complex with an MYB 389
transcription factor Since co-overexpression of FaERF9 and FaMYB98 resulted in 390
much higher activation activity towards FaQR we speculate that FaERF9 may 391
recruit FaMYB98 homologs in tobacco to activate the FaQR promoter (Figure 8) 392
FaOMT is another key gene for furanone biosynthesis and a potential target for 393
transcriptional activation However FaERF9 did not significantly activate the 394
FaOMT promoter in a dual-luciferase assay and the transcript level of FaOMT in the 395
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15
FaERF9-overexpressing fruits showed no significant difference from that in the 396
control (Supplemental Figure S6 Supplemental Figure S7) The FaOMT promoter 397
was significantly induced by FaMYB98 but no synergistic effect of FaERF9 and 398
FaMYB98 on the promoter was observed (Supplemental Figure S6) In previous 399
studies of the regulation of plant volatile compounds MYBs have been characterized 400
as being involved mainly in the regulation of the benzenoidphenylpropanoid pathway 401
that produces floral volatiles in petunia and eugenol in ripe strawberry fruit (Verdonk 402
et al 2005 Dal Cin et al 2011 Colquhoun et al 2011 Spitzer-Rimon et al 2012 403
Medina-Puche et al 2015) but their role in formation of volatiles from other 404
pathways has not been reported Our study demonstrates a role for MYB in the 405
synthesis of furaneol a carbohydrate-derived volatile compound and reveals the 406
synergistic interactions between an MYB and ERF in a transcription complex (Figure 407
8 Figure 9 and Figure 10) 408
409
Recent research has provided evidence for interactions between AP2ERF and MYB 410
transcription factors in regulating other aspects of fruit quality including texture 411
(EjAP2-1 and EjMYB Zeng et al 2015) and colour (PyERF3 and PyMYB114 Yao 412
et al 2017) A group VIII ERF has also recently been shown to interact with an MYB 413
to regulate floral scent production in petunia (Liu et al 2017) In strawberry fruit 414
DOF in combination with an MYB has been reported to be involved in the regulation 415
of eugenol production and the identification of this second transcription factor (DOF) 416
suggests that it is a good target in breeding for improved flavour (Molina-Hidalgo et 417
al 2017 Tieman 2017) Considering its important contribution to flavour in 418
strawberry and many other highly valued fruit crop species (pineapple tomato mango 419
etc) very little is known about regulation of furaneol synthesis Here we established 420
the role of FaERF9 in the regulation of HDMF synthesis by direct protein-protein 421
interactions with FaMYB98 to synergistically trans-activate FaQR The functional 422
identification of this complex enhances our knowledge of the regulation of volatile 423
compound synthesis and identifies a new AP2ERF-MYB complex Further 424
examination of the other ERFs that stimulated transcription from the FaQR promoter 425
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16
(Figure 2) may provide additional information about the complexity of this regulation 426
Overall this study provides important clues for understanding the transcriptional 427
regulation of HDMF synthesis and identifies specific transcription factors that are 428
likely to be good targets for molecular breeding for improved flavour 429
430
Conclusions 431
Screening of the AP2ERF superfamily in strawberry (Fragaria times ananassa) 432
identified candidate members capable of activating the FaQR promoter An ERF 433
transcription factor was identified as a positive regulator of HDMF synthesis in 434
strawberry fruit and the mechanism of activation was shown to involve an ERF-MYB 435
transcription complex that regulates transcription of FaQR leading to the biosynthesis 436
of HDMF the characteristic volatile compound which has a major influence on 437
strawberry aroma 438
439
Materials and Methods 440
441
Plant Materials and Growth conditions 442
The strawberry (Fragaria times ananassa cv lsquoYuexinrsquo an octoploid cultivar) fruit used in 443
this study were bred by Zhejiang Academy of Agricultural Sciences (Haining 444
Zhejiang) Fruits at various developmental and ripening stages including G (green) T 445
(turning) IR (intermediate red) and R (full red) were harvested (Figure 1) and 446
transported to the laboratory within 2 h Thirty-six fruits of uniform size and free of 447
visible defects were selected at each stage with twelve fruits in each biological 448
replicate After removing the calyces fruits were then divided into the basal and 449
apical sections which were sampled separately (Figure 1) They were rapidly cut into 450
pieces frozen immediately in liquid nitrogen and stored at -80deg C until use Red ripe 451
fruits of different strawberry cultivars (Fragaria times ananassa octoploid cultivars) 452
including lsquoYuelirsquo lsquoBenihoppersquo lsquoMengxiangrsquo lsquoAmaoursquo lsquo10-1-4rsquo lsquoAkihimersquo lsquoSweet 453
Charliersquo lsquo07-1-4rsquo lsquoDarselectrsquo lsquoYuexinrsquo and lsquoXuemeirsquo were also provided by Zhejiang 454
Academy of Agricultural Sciences For each cultivar the fruits of three biological 455
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17
replicates were sampled frozen in liquid nitrogen and stored at -80deg C for further use 456
457
Tobacco plants (Nicotiana benthamiana) used for dual-luciferase assays and 458
subcellular localization analysis in this study were grown in a growth chamber with a 459
lightdark cycle of 16 h8 h at 24degC 460
461
Detection of DMMF and HDMF 462
Automated HS-SPME-GC-MS was performed to detect both furanones in lsquoYuexinrsquo 463
strawberry fruit (Zorrilla-Fontanesi et al 2012) Samples were ground into a powder 464
under liquid nitrogen for analysis 465
466
For the detection of DMMF (Figure 1) 05 g (fresh weight) of each sample was 467
weighed in the vial to which was added 1 mL of EDTA solution (100 mM pH 75) 1 468
mL of CaCl2 solution (mv = 20) and 20 microL of 2-octanol as the internal standard 469
(007 μgμL) The mixture was homogenized and the vial closed and placed on the 470
sample tray for analysis by CombiPAL autosampler (CTC Analytic CA USA) The 471
fruit volatiles were sampled by headspace solid-phase microextraction with a 65-μm 472
polydimethylsiloxane-divinylbenzene fibre (PDMS-DVB) Initially vials were 473
pre-incubated at 50degC for 10 min under continuous agitation (500 rpm) then volatiles 474
were extracted for 30 min at the same temperature and agitation speed After that the 475
fibre was desorbed in the GC injection port for 5 min in splitless mode The 7890A 476
GC chromatograph was equipped with a DB-5ms column (60 m times 250 μm times 1 μm 477
JampW Scientific Folsom CA USA) with helium as the carrier gas at a constant flow 478
of 12 mLmin The GC was programmed at an initial temperature of 35degC for 2 min 479
with a ramp of 5degC min up to 250degC and held for 5 min The injection port interface 480
and MS source temperatures were 250degC 260degC and 230degC respectively The 481
ionization potential was set at 70 eV recorded by a 5975B mass spectrometer (Agilent 482
Technologies JampW Scientific Folsom CA USA) and the scanning speed was 7 483
scanss The same method was used to analyse HDMF and DMMF in fruits from 484
different cultivars (Supplemental Figure S3) except for the sample preparation 485
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
18
procedure (Araguumlez et al 2013) briefly 05 g (fresh weight) of powdered fruit was 486
incubated at 30degC in a water bath for 5 min then 2 mL of NaCl (mv = 20) and 20 487
microL of 2-octanol as the internal standard (007 μgμL) were added and homogenized 488
489
For the detection of HDMF (Figure 1) and both furanones (Figure 4 and Supplemental 490
Table S3) a liquid-injection system equipped with CTC Pal ALS was used One gram 491
(fresh weight) of powdered fruit and 2 mL of NaCl (mv = 20) were homogenized in 492
a 10-mL tube and 300 μL of CH2Cl2 and 20 microL of 2-octanol (0766 μgμL) as the 493
internal standard were added to extract the volatiles the mixture was then 494
homogenized again The tubes were stored at room temperature for 20 min and 495
centrifuged at 12000 rpm for 5 min The subnatant was pipetted into a clean 15-mL 496
tube in which 20 mg of anhydrous sodium sulphate was added the tube was left 497
without shaking for half an hour Then 150 μL of the solution was transferred into a 498
GC vial and placed on the sample tray as described above Each sample (1 μL) was 499
injected using the autosampler and the analysis was accomplished by a 7890A 500
GC-MS system (Agilent Technologies JampW Scientific Folsom CA USA) equipped 501
with a DB-WAX column (30 m times 025 mm times 025 μm JampW) Helium (12 mLmin) 502
was used as a carrier gas The injection port (splitless injection mode) interface and 503
MS source temperatures were as described above The oven temperature was set at 504
60degC for 4 min then increased to 180degC at a rate of 4degCmin and maintained for 30 505
min DMMF was identified by comparison of electron ionization mass spectra and 506
retention time data with the data from the NISTEPANIH mass spectral library 507
(NIST-08 and Flavor) HDMF (Figure 1) was identified and qualified by comparison 508
with injected standard (Sigma) The quantitative analysis of both furanones (Figure 4 509
Supplemental Table S3 and Supplemental Figure S3) was determined using the peak 510
area of the internal standard as a reference based on total ion chromatogram (TIC) 511
512
RNA isolation and Reverse Transcription Quantitative PCR (RT-qPCR) 513
Total RNA from strawberry samples was isolated in this study using the CTAB 514
method (Chang et al 1993) Genomic DNA contamination was eliminated by 515
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
19
TURBO Dnase (Ambion) 1 μg of RNA was used to obtain cDNA using an IScriptTM 516
cDNA Synthesis Kit (Bio-Rad) The synthesized cDNA was diluted with water (120) 517
and 2 μL of diluted cDNA was used as the template for RT-qPCR Reactions were 518
performed in a total volume of 20 μL consisting of 10 μL of SYBR PCR supermix 519
(Bio-Rad) 1 μL of each primer (10 μM) 6 μL of DEPC-H2O and 2 μL of diluted 520
cDNA on CFX96 instrument (Bio-Rad) (Yin et al 2012) The oligonucleotide 521
primers for RT-qPCR analysis of genes including the AP2ERF FaQR and FaOMT 522
were designed according to the coding sequences of genes and the specificity was 523
verified before use (Min et al 2012) NCBIPrimer-BLAST was applied to design the 524
primers Relative expression levels were normalized to that of an internal controlmdashthe 525
interspacer 26S-18S strawberry RNA housekeeping gene FaRIB413 526
(Zorrilla-Fontanesi et al 2012) To investigate the differential expression of genes 527
during fruit development and ripening stages relative expression of each gene at the 528
R stage in the basal fruit section was set as 1 using the 2minus∆∆119862119879 method For transient 529
overexpression assay relative expression of control fruits with an empty vector (SK) 530
was set as 1 The primers used in RT-qPCR are listed in Supplemental Table S4 531
532
Gene isolation and analysis 533
Multiple database searches were performed to identify members of the strawberry 534
(Fragaria times ananassa) AP2ERF superfamily in the published strawberry databases 535
and annotations of Fragaria times ananassa and Fragaria times vesca by using the 536
AP2ERF DNA binding domain as a query sequence and 120 genes were identified 537
with AP2ERF domain(s) Based on the BLAST result primers (listed in 538
Supplemental Table S5) were used to amplify the coding full-length cDNAs of 539
AP2ERF genes The deduced amino acid sequences of AP2ERF proteins in 540
Arabidopsis thaliana used for construction of a phylogenetic tree were obtained from 541
the Arabidopsis Information Resource (TAIR) Alignment of the proteins was 542
performed using the neighbour-joining method in ClustalX (v181) and the 543
phylogenetic tree was constructed using FigTree (v131) 544
545
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
20
FaMYB98 was obtained by yeast one-hybrid screening sequencing and the full-length 546
sequences were predicted by BLAST Primers were designed (listed in Supplemental 547
Table S5) to amplify the full-length coding sequence 548
549
The promoter of FaQR was cloned by Genome Walking as previously described (Yin 550
et al 2010) and conserved cis-element motifs in the promoter were manually 551
searched 552
553
Conserved domains within the FaAP2ERF proteins and FaMYB98 were analysed by 554
CD-search (httpswwwncbinlmnihgovStructurecddwrpsbcgi) and cellular 555
locations of proteins including FaERF9 and FaMYB98 were predicted with the 556
WoLF PSORT program (httpswwwgenscriptcomwolf-psorthtml) 557
558
Dual-Luciferase Assays 559
In accordance with a previous protocol (Yin et al 2010) the full-length cDNAs of 560
FaAP2ERF or FaMYB98 transcription factors were cloned into pGreen II 0029 561
62-SK vector and the promoter of FaQR was cloned into pGreen II 0800-LUC vector 562
A luciferase gene from Renillia (REN) driven by a 35S promoter in the LUC vector 563
acted as a positive control The above constructs were transiently expressed in 564
Nicotiana benthamiana leaves by Agrobacterium-mediated infiltration (strain 565
GV3101) and the activity of the TFs on the promoter was measured on the third day 566
after infiltration indicated by the ratio of enzyme activities of firefly luciferase (LUC) 567
and renilla luciferase (REN) using a Modulus Luminometer (Promega Madison WI 568
USA) To determine the activity of a specific transcription factor towards the 569
promoter we mixed the Agrobacterium culture with 1 mL of TF and 100 μL of 570
promoter and the LUCREN value of the empty vector SK on the promoter was set as 571
1 as a calibrator To test the combined effect of two transcription factors on the 572
promoter to the Agrobacterium culture mixture we added 05 mL of each TF and 100 573
μL of promoter the effect of the mixtures that contained each transcription factor (05 574
mL) and empty vector SK (05 mL) was also tested on the promoter as a control 575
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
21
576
Subcellular localization analysis 577
35S-FaERF9-GFP and 35S-FaMYB98-GFP were transiently expressed in tobacco (N 578
benthamiana) leaves by Agrobacterium infiltration (EHA105) using the same method 579
as described in the dual-luciferase assay above The transiently infected leaves were 580
imaged on the third day after infiltration using a Nikon A1-SHS confocal laser 581
scanning microscope The excitation wavelength for GFP fluorescence was 488 nm 582
and fluorescence was detected at 490ndash520 nm The primers used for GFP construction 583
are listed in Supplemental Table S6 584
585
Transient overexpression in strawberry fruit 586
Transient overexpression of FaERF9 and an overexpression binary vector (pGreen II 587
0029 62-SK-FaERF9-FaMYB98) were performed in strawberry fruit using the 588
FaERF9-SK construct described above for the dual-luciferase assays and the binary 589
vector constructed according to Liu et al 2013 The transfection of fruit was carried 590
out at the G stage (Hoffmann et al 2006) The FaERF9-SK construct and binary 591
vector were individually electroporated into Agrobacterium tumefaciens GV3101 and 592
the Agrobacterium culture suspended in infiltration buffer was infiltrated into the 593
whole fruit using a syringe As a control treatment fruits were infiltrated with 594
Agrobacterium carrying an empty vector SK under the same transfection conditions 595
Fruits were left attached to the plants and harvested on the seventh day after 596
infiltration Fruits of three biological replicates were sampled for further analysis 597
598
Yeast one-hybrid assay 599
In order to identify proteins that bind to the FaQR promoter the Matchmaker Gold 600
Yeast One-hybrid Library Screening System (Clontech USA) was used The sequence 601
of the FaQR promoter was cloned into the pAbAi vector and the construct was 602
integrated into the genome of the Y1HGold yeast strain A mixture of total RNA from 603
strawberry fruit at four stages (G T IR R) was used to construct the prey cDNA 604
library (TaKaRa) The background AbAr expression of Y1HGold FaQR-pAbAi strain 605
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
22
was tested according to the system user manual and then screening for protein-DNA 606
interactions was carried out Furthermore the full length of each transcription factor 607
was separately cloned into pGADT7 AD vector to confirm the screening results The 608
relationship between FaERF9 and FaQR promoter was also examined individually 609
Primers used in this assay are listed in Supplemental Table S6 610
611
Expression and purification of FaMYB98 recombinant protein 612
A 405-bp region spanning the DNA-binding domain of FaMYB98 was amplified 613
from FaMYB98 cDNA and cloned into a pET6timesHN vector (Clontech Palo CA USA) 614
to generate the recombinant N-terminal His-tagged protein the primers used are listed 615
in Supplemental Table S6 The resulting construct was sequenced and introduced into 616
Escherichia coli strain Rosetta 2(DE3)pLysS (Novagen) Ten millilitres of the 617
overnight culture was combined with 500 mL of an LB liquid medium (100 μgmL 618
ampicillin and 34 μgmL chloramphenicol) as described (Li et al 2017) Isopropyl 619
β-D-1-thiogalactopyranoside (IPTG) was added to a final concentration of 1 mM and 620
the bacterial culture was incubated at 18degC at 150 rpm for 18 h Then the cells were 621
harvested using a centrifuge and resuspended in 1times PBS buffer (Sangon Biotech) 622
after which they were disrupted by sonication and the supernatant was purified using 623
a HisTALONTM Gravity Column (Clontech) according to the user manual The PD-10 624
Desalting column (GE Healthcare) was then used for buffer change and sample 625
clean-up of proteins according to the gravity protocol SDS-PAGE was performed and 626
the protein was visualized using Coomassie brilliant blue 627
628
Electrophoretic mobility shift assay (EMSA) 629
A Lightshift Chemiluminescent EMSA kit (Thermo) was used to perform EMSA 630
experiments according to the manufacturerrsquos instructions Single-strand 631
oligonucleotides were synthesized and biotinylated by GeneBio Biotech (Hangzhou 632
China) The details of the EMSA assay are provided in Ge et al (2017) The probes 633
used for EMSAs are listed in Supplemental Table S6 634
635
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
23
636
Yeast two-hybrid assay 637
The DUALhunter system (Dualsystems Biotech Switzerland) was used to investigate 638
the interaction between FaERF9 and FaMYB98 Full-length coding sequences of 639
FaERF9 and FaMYB98 were respectively cloned into pDHB1 bait vector and 640
pPR3-N prey vector sequences were verified and the bait plasmid was 641
co-transformed with prey plasmid into NMY51 in the combinations below 642
FaMYB98-pDHB1pPR3-N FaMYB98-pDHB1FaERF9-pPR3-N 643
FaMYB98-pDHB1pOst1-NubI FaERF9-pDHB1pPR3-N 644
FaERF9-pDHB1FaMYB98-pPR3-N and FaERF9-pDHB1pOst1-NubI (Li et al 645
2017) Transformed cells were spread onto the following plates DDO (SD 646
medium-Trp-Leu) QDO (SD medium-Trp-Leu-His-Ade) and QDO+3-AT (QDO 647
medium supplemented with 1 mM 3-amino-124-triazole) The control plasmid 648
pOst1-NubI was used to determine whether the bait was functional the pPR3-N prey 649
vector plasmid was used to test whether the bait displayed non-specific background 650
and positive interactions were indicated by the growth of yeast on QDO and 651
QDO+3-AT plates The Primers used in the DUALhunter assay are listed in 652
Supplemental Table S6 653
654
Bimolecular fluorescence complementation (BiFC) assays 655
Full-length FaERF9 and FaMYB98 respectively were cloned into sequences 656
encoding the N- and C- fragments of YFP protein (Lv et al 2014) All constructs 657
were transiently expressed in tobacco (N benthamiana) leaves by Agrobacterium 658
infiltration (EHA105) The YFP fluorescence of transfected leaves was imaged 40 h 659
after infiltration by using a Nikon A1-SHS confocal laser scanning microscope The 660
excitation wavelength for YFP was 488 nm and fluorescence was detected at 520ndash661
540 nm Primers used are listed in Supplemental Table S6 662
663
Statistics 664
A Studentrsquos two-tailed t test ( plt005 plt001 and plt0001) was used to 665
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
24
determine significant differences between two groups in this study Microsoft Excel 666
was used to perform linear regressive analysis significant differences were 667
determined by SPSS Statistics 200 and scatter plots were prepared with Origin80 668
Least significant difference (LSD) at the 5 level was calculated using Microsoft 669
Excel Figures were prepared with Origin80 (Microcal Software Inc Northampton 670
MA USA) The online tool MetaboAnalyst 36 (httpwwwmetaboanalystca) was 671
used to analyse the transcript abundance of the AP2ERF genes 672
673
Accession numbers 674
Sequence data from this article have been deposited in GenBank under the accession 675
numbers MH332903-MH333022 for AP2ERF genes in Fragaria times ananassa and 676
MH333023 for FaMYB98 GenBank numbers for FaQR and FaOMT were 677
AY1588361 (Raab et al 2006) and AF2204912 (Wein et al 2002) 678
679
Supplemental Material 680
Supplemental Figure S1 Phylogenetic analysis of FaAP2ERF and Arabidopsis 681
AP2ERF proteins 682
Supplemental Figure S2 Analysis of FaAP2ERF gene expression patterns in 683
strawberry fruit during development and ripening 684
Supplemental Figure S3 Contents of furanones in fruit of strawberry cultivars 685
Supplemental Figure S4 Relative expression of FaERF9 in FaERF9-FaMYB98- 686
and FaERF9-overexpressing fruits 687
Supplemental Figure S5 Subcellular localization of FaMYB98 688
Supplemental Figure S6 The combined activation effects of FaERF9FaMYB98 on 689
the FaOMT promoter 690
Supplemental Figure S7 Relative expression of FaOMT in 691
FaERF9-overexpressing fruits 692
Supplemental Table S1 AP2ERF superfamily genes in Fragaria times ananassa 693
Supplemental Table S2 Classification of the AP2ERF superfamily members in 694
Fragaria times ananassa 695
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
25
Supplemental Table S3 Furanone content in FaERF9-FaMYB98- and 696
FaERF9-overexpressing fruits 697
Supplemental Table S4 Primers used for reverse transcription quantitative PCR 698
(RT-qPCR) 699
Supplemental Table S5 Primers used to amplify the full-length coding sequences of 700
AP2ERF genes and FaMYB98 in strawberry (Fragaria times ananassa) 701
Supplemental Table S6 Primers used for vector construction 702
703
Acknowledgments 704
This research was supported by the National Key Research and Development 705
Program (2016YFD0400101) the Project of the Science and Technology Department 706
of Zhejiang Province (2016C04001) and the 111 Project (B17039) 707
708
Figure legends 709
Figure 1 Changes in furanone content and furanone biosynthetic genes during 710
strawberry (Fragaria times ananassa Duch cv Yuexin) fruit development and ripening 711
A Fruits were collected at four ripening stages G (green stage) T (turning stage) IR 712
(intermediate red stage) R (full red stage) B Changes in the contents of furaneol 713
(HDMF) and mesifurane (DMMF) HDMF content was calculated using a standard 714
curve of HDMF while DMMF content was calculated with an internal standard as the 715
reference C Expression levels of FaQR and FaOMT The expression levels of each 716
gene were calculated relative to corresponding values in the basal section at the R 717
stage SEs were calculated from three replicates and LSD values represent the least 718
significant differences at p = 005 719
Figure 2 Regulatory effects of FaAP2ERF on the promoter of FaQR LUCREN 720
values of the empty vector on FaQR promoter were used as the calibrator set as 1 721
and SEs were calculated from five replicates statistical significance was determined 722
by Studentrsquos two-tailed t test ( plt0001) 723
Figure 3 Expression and the subcellular localization of FaERF9 A The expression 724
levels were calculated relative to the levels in the basal section at the R stage B 725
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
26
Subcellular localization analysis was performed in tobacco leaves The tobacco used 726
in the assay was stably transformed with a specific nucleus localized red fluorescence 727
protein construct and the red fluorescence indicates the nucleus-localized signal 728
(NLS) Scale bar = 25 microm SEs were calculated from three replicates 729
Figure 4 Transient overexpression of FaERF9 in strawberry fruit A Relative 730
expression of FaQR and FaERF9 in FaERF9-OX fruit 7 days after infiltration The 731
expression was calculated relative to the average value in control (SK) fruits B 732
HDMF and DMMF content in FaERF9-OX fruit The content of both furanones 733
were quantified using the peak area of the internal standard (2-octanol) as the 734
reference SEs were calculated from three replicates Statistical significance was 735
determined by Studentrsquos two-tailed t test ( plt005 plt001 plt0001) 736
Figure 5 Scatter plots of 11 strawberry cultivars A Linear regression analysis 737
between FaERF9 expression and FaQR expression B Linear regression analysis 738
between FaERF9 expression and furanone content The relative expression was 739
normalized to that of the housekeeping gene FaRIB413 and furanone content was 740
calculated with internal standard as the reference Significant differences were 741
determined by SPSS Statistics 200 742
Figure 6 Interactions of FaERF9 and FaMYB98 with the FaQR promoter A Yeast 743
one-hybrid analysis of the interaction of FaERF9 and FaQR promoter B Yeast 744
one-hybrid analysis of the interaction of FaMYB98 and FaQR promoter C 745
Regulatory effect of FaMYB98 on the FaQR promoter Auto-activation was tested on 746
SD-Ura (synthetically defined medium without uracil) in presence of Aureobasidin A 747
(AbA) and physical interaction was determined on SD-Leu (synthetically defined 748
medium without leucine) in presence of AbA LUCREN values of the empty vector 749
on FaQR promoter were used as the calibrator set as 1 and error bars were calculated 750
from five replicates Statistical significance was determined by Studentrsquos two-tailed t 751
test ( plt005 plt001 plt0001) 752
Figure 7 Electrophoretic mobility shift assay of FaMYB98 binding to FaQR 753
promoter A The probe sequence used for EMSA and mutated nucleotides are 754
indicated with lowercase letters B Purified DNA-binding domain of FaMYB98 755
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
27
protein and biotin-labelled DNA probe were mixed and analysed on 6 native 756
polyacrylamide gels and then photographed Presence or absence of specific probes is 757
marked by the symbol + or - 758
Figure 8 The combined activation effects of FaERF9FaMYB98 on the FaQR 759
promoter LUCREN values obtained with the empty vector and FaQR promoter were 760
used as the calibrator set as 1 and error bars were calculated from five replicates 761
Figure 9 Yeast two-hybrid analysis of the protein-protein interactions between 762
FaMYB98 and FaERF9 Positive interactions were determined by the growth of 763
yeast cells on selection plates Bait with pOST acted as positive controls and bait with 764
pPR3 as negative controls DDO synthetically defined medium without tryptophan 765
and leucine QDO synthetically defined medium without tryptophan leucine 766
histidine and adenine QDO+3AT QDO medium supplemented with 1 mM 767
3-aminotriazole 768
Figure 10 BiFC analysis of the protein-protein interactions between FaMYB98 and 769
FaERF9 The pairs of fusion proteins tested were FaMYB98-YFPN+FaERF9-YFPC 770
FaERF9-YFPN+FaMYB98-YFPC FaMYB98-YFPN+FaMYB98-YFPC and 771
FaERF9-YFPN+FaERF9-YFPC The other combinations were negative controls 772
The tobacco used in the assay was stably transformed with a specific 773
nucleus-localized red fluorescence protein construct and the red fluorescence 774
indicated the nucleus-localized signal (NLS) Fluorescence of the yellow fluorescence 775
protein (YFP) visualized the interaction in vivo Scale bar = 25 microm 776
777
Literature Cited 778
779
Agarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression 780
of PgDREB2A transcription factor enhances abiotic stress tolerance and activates 781
downstream stress-responsive genes Mol Biol Rep 37 1125-1135 782
Araguumlez I Osorio S Hoffmann T Rambla JL Medina-Escobar N Granell A 783
Botella MAacute Schwab W Valpuesta V (2013) Eugenol production in achenes and 784
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28
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Plant Physiol 163 946-958 786
Carvalho RF Carvalho SD OrsquoGrady K Folta KM (2016) Agroinfiltration of 787
strawberry fruit mdash a powerful transient expression system for gene validation Curr 788
Plant Biol 6 19-37 789
Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic 790
(Amsterdam) 210 34-40 791
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating 792
RNA from pine trees Plant Mol Biol Rep 11 113-116 793
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC 794
Clark DG (2011) PhMYB4 fine-tunes the floral volatile signature of 795
Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143 796
Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz 797
EA Taylor MG Smits-Kroon MT Schuurink RC Haring MA Giovannoni J 798
Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic 799
pathway by ectopic expression of a MYB transcription factor in tomato fruit Plant 800
Cell 23 2738-2753 801
Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan 802
XW Yang ZY (2017) Differential responses of four biosynthetic pathways of 803
aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under 804
interaction of light and temperature Food Chem 221 356-364 805
Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of 806
differentially-expressed genes during somatic embryogenesis in Fragaria times 807
ananassa Duch lsquoBenihopprsquo J Hortic Sci Biotechnol 90 671-681 808
Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 809
transcriptionally regulates chilling-induced lignification of loquat fruit via physical 810
interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136 811
Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM 812
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proteins Plant J 39 513-526 814
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29
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) 815
Sucrose nonfermenting1-related protein kinase26 an ortholog of open stomata1 is 816
a negative regulator of strawberry fruit development and ripening Plant Physiol 817
167 915-930 818
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene 819
expression in strawberry fruit (Fragaria times ananassa) by agroinfiltration a rapid 820
assay for gene function analysis Plant J 48 818-826 821
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of 822
selected aroma-active compounds in strawberries by headspace solid-phase 823
microextraction gas chromatography and correlation with sensory descriptive 824
analysis J Food Sci 72 S487-S496 825
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid 826
plays an important role in the regulation of strawberry fruit ripening Plant Physiol 827
157 188-199 828
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of 829
NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes BMC 830
Plant Biol 6 20 831
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN 832
(2005) MYB98 is required for pollen tube guidance and synergid cell differentiation 833
in Arabidopsis Plant Cell 17 2981-2992 834
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional 835
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Agric Food Chem 55 6705-6711 837
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You 838
J-S Rohloff J Randall SK Alsheikh M (2012) Proteomic study of 839
low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ 840
in cold tolerance Plant Physiol 159 1787-1805 841
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional 842
characterization of four APETALA2-family genes (RAP26 RAP26L DREB19 843
and DREB26) in Arabidopsis Plant Mol Biol 75 107-127 844
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30
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon 845
J Gupta V (2013) An oxidoreductase from lsquoAlphonsorsquo mango catalyzing 846
biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494 847
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in 848
strawberries Z Lebensm-Unters Forsch 195 120-123 849
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X 850
(2015) Label-free quantitative proteomics to investigate strawberry fruit proteome 851
changes under controlled atmosphere and low temperature storage J Proteomics 852
120 44-57 853
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 854
cooperates with CitWRKY1 to participate in citric acid degradation via 855
up-regulation of CitAco3 J Exp Bot 68 3419-3426 856
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription 857
factor CitERF71 activates the terpene synthase gene CitTPS16 involved in the 858
synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938 859
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and 860
transcriptomic analysis of the AP2ERF superfamily in Vitis vinifera BMC 861
Genomics 11 719 862
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive 863
Factor (AP2ERF) transcription factors mediators of stress responses and 864
developmental programs New Phytol 199 639-649 865
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 866
interacting with EOBI negatively regulates fragrance biosynthesis in petunia 867
flowers New Phytol 215 1490-1502 868
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu 869
CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 in regulating 870
anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) 871
during anthocyanin biosynthesis Plant Cell Tissue Organ Cult 115 285-298 872
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31
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao 873
CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphate signaling and 874
homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597 875
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC 876
Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL 877
Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor 878
regulates eugenol production in ripe strawberry fruit receptacles Plant Physiol 168 879
598-614 880
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics 881
and volatile constituents of strawberry (cv Cigaline) during maturation J Agric 882
Food Chem 52 1248-1254 883
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS 884
(2012) Ethylene-responsive transcription factors interact with promoters of ADH 885
and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 886
63 6393-6405 887
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM 888
Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-Franco A 889
Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific 890
transcription factor FaDOF2 regulates the production of eugenol in ripe fruit 891
receptacles J Exp Bot 68 4529-4543 892
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) 893
Comparison and verification of the genes involved in ethylene biosynthesis and 894
signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44 895
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the 896
ERF gene family in Arabidopsis and rice Plant Physiol 140 411-432 897
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in 898
sour cherry and strawberry and the heterologous expression of CBF1 in strawberry 899
J Am Soc Hortic Sci 127 489-494 900
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech 901
JC Ohme-Takagi M Regad F Bouzayen M (2012) Functional analysis and 902
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32
binding affinity of tomato ethylene response factors provide insight on the 903
molecular bases of plant differential responses to ethylene BMC Plant Biol 12 190 904
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) 905
Methylpentoses are possible precursors of furanones in fruits Prikl Biokhim 906
Mikrobiol 28 123-127 907
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery 908
of synergid-expressed genes encoding filiform apparatus localized proteins Plant 909
Cell 19 2557-2568 910
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria 911
vesca L compared to those of cultivated berries Fragariatimes ananassa cv Senga 912
Sengana J Agric Food Chem 27 19-22 913
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W 914
Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of the strawberry 915
flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone 916
oxidoreductase Plant Cell 18 1023-1037 917
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L 918
Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim M Broun P Zhang 919
JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription 920
factors genome-wide comparative analysis among eukaryotes Science 290 921
2105-2110 922
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the 923
formation of 25-dimethyl-4-hydroxy-3(2H)-furanone in detached ripening 924
strawberry fruits J Agric Food Chem 46 1488-1493 925
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 926
25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in 927
strawberry fruits Phytochemistry 43 155-159 928
Schwab W (1998) Application of stable isotope ratio analysis explaining the 929
bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone in plants by a biological 930
maillard reaction J Agric Food Chem 46 2266ndash2269 931
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33
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) 932
Molecules 18 6936-6951 933
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard 934
products Recent Res Dev Phytochem 1 643-673 935
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL 936
Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJ Sims CA 937
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compositions a seasonal influence and effects on sensory perception PLoS One 9 939
e88446 940
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) 941
Identification phylogeny and transcript profiling of ERF family genes during 942
development and abiotic stress treatments in tomato Mol Genet Genomics 284 943
455-475 944
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) 945
CitAP210 activation of the terpene synthase CsTPS1 is associated with the 946
synthesis of (+)-valencene in lsquoNewhallrsquo orange J Exp Bot 67 4105-4115 947
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes 948
Dev Genes Evol 214 105-114 949
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K 950
Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the 951
key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151 952
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O Yu YX Shklarman E Ovadis M Vainstein A (2012) The R2R3-MYB-like 954
regulatory factor EOBI acting downstream of EOBII regulates scent production 955
by activating ODO1 and structural scent-related genes in petunia Plant Cell 24 956
5089-5105 957
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp 958
Bot 68 4407-4409 959
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla 960
JF Amaya I Giavalisco P Fernie AR Botella MA Valpuesta V (2015) Central 961
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34
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to ripening New Phytol 208 482-496 963
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 964
regulates fragrance biosynthesis in petunia flowers Plant Cell 17 1612-1624 965
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS 966
(2018) The potassium channel FaTPK1 plays a critical role in fruit quality 967
formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748 968
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) 969
Isolation cloning and expression of a multifunctional O-methyltransferase capable 970
of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma 971
compounds in strawberry fruits Plant J 31 755-765 972
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor 973
types their evolutionary origin and species distribution In A handbook of 974
transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular 975
Biochemistry 52 25-73 976
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of 977
odor (Buettner A Ed) Springer Cham 9-10 978
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS 979
(2014) Isolation classification and transcription profiles of the AP2ERF 980
transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271 981
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in 982
regulation of fruit quality Crit Rev Plant Sci 35 120-130 983
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ 984
Zhang SL Wu J (2017) Map-based cloning of the pear gene MYB114 identifies an 985
interaction with other transcription factors to coordinately regulate fruit 986
anthocyanin biosynthesis Plant J 92 437-451 987
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes 988
involved in regulating fruit ripening Plant Physiol 153 1280-1292 989
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
35
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) 990
Expression of ethylene response genes during persimmon fruit astringency removal 991
Planta 235 895-906 992
Zabetakis I Gramshaw JW Robinson DS (1999) 993
25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis and 994
biosynthesis-a review Food Chem 65 139-151 995
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci 996
Food Agric 74 421-434 997
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 998
an AP2ERF gene is a novel regulator of fruit lignification induced by chilling 999
injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1000
1325-1334 1001
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation 1002
classification and transcription profiles of the Ethylene Response Factors (ERFs) in 1003
ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215 1004
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML 1005
(2012) Genome-wide analysis of the AP2ERF superfamily in peach (Prunus 1006
persica) Genet Mol Res 11 4788-4809 1007
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and 1008
expression analysis of a CRTDRE-binding factor gene FaCBF1 from Fragaria times 1009
ananassa Acta Hortic 41 240-248 1010
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The 1011
Arabidopsis AP2ERF transcription factor RAP26 participates in ABA salt and 1012
osmotic stress responses Gene 457 1-12 1013
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B 1014
Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) Genome-wide 1015
analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic 1016
(Amsterdam) 123 73-81 1017
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF 1018
Valpuesta V Botella MA Granell A Amaya I (2012) Genetic analysis of 1019
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36
strawberry fruit aroma and identification of O-methyltransferase FaOMT as the 1020
locus controlling natural variation in mesifurane content Plant Physiol 159 1021
851-870 1022
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Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Genome-wide analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic (Amsterdam) 123 73-81Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF Valpuesta V Botella MA Granell A Amaya I (2012) Geneticanalysis of strawberry fruit aroma and identification of O-methyltransferase FaOMT as the locus controlling natural variation inmesifurane content Plant Physiol 159 851-870
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
15
FaERF9-overexpressing fruits showed no significant difference from that in the 396
control (Supplemental Figure S6 Supplemental Figure S7) The FaOMT promoter 397
was significantly induced by FaMYB98 but no synergistic effect of FaERF9 and 398
FaMYB98 on the promoter was observed (Supplemental Figure S6) In previous 399
studies of the regulation of plant volatile compounds MYBs have been characterized 400
as being involved mainly in the regulation of the benzenoidphenylpropanoid pathway 401
that produces floral volatiles in petunia and eugenol in ripe strawberry fruit (Verdonk 402
et al 2005 Dal Cin et al 2011 Colquhoun et al 2011 Spitzer-Rimon et al 2012 403
Medina-Puche et al 2015) but their role in formation of volatiles from other 404
pathways has not been reported Our study demonstrates a role for MYB in the 405
synthesis of furaneol a carbohydrate-derived volatile compound and reveals the 406
synergistic interactions between an MYB and ERF in a transcription complex (Figure 407
8 Figure 9 and Figure 10) 408
409
Recent research has provided evidence for interactions between AP2ERF and MYB 410
transcription factors in regulating other aspects of fruit quality including texture 411
(EjAP2-1 and EjMYB Zeng et al 2015) and colour (PyERF3 and PyMYB114 Yao 412
et al 2017) A group VIII ERF has also recently been shown to interact with an MYB 413
to regulate floral scent production in petunia (Liu et al 2017) In strawberry fruit 414
DOF in combination with an MYB has been reported to be involved in the regulation 415
of eugenol production and the identification of this second transcription factor (DOF) 416
suggests that it is a good target in breeding for improved flavour (Molina-Hidalgo et 417
al 2017 Tieman 2017) Considering its important contribution to flavour in 418
strawberry and many other highly valued fruit crop species (pineapple tomato mango 419
etc) very little is known about regulation of furaneol synthesis Here we established 420
the role of FaERF9 in the regulation of HDMF synthesis by direct protein-protein 421
interactions with FaMYB98 to synergistically trans-activate FaQR The functional 422
identification of this complex enhances our knowledge of the regulation of volatile 423
compound synthesis and identifies a new AP2ERF-MYB complex Further 424
examination of the other ERFs that stimulated transcription from the FaQR promoter 425
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
16
(Figure 2) may provide additional information about the complexity of this regulation 426
Overall this study provides important clues for understanding the transcriptional 427
regulation of HDMF synthesis and identifies specific transcription factors that are 428
likely to be good targets for molecular breeding for improved flavour 429
430
Conclusions 431
Screening of the AP2ERF superfamily in strawberry (Fragaria times ananassa) 432
identified candidate members capable of activating the FaQR promoter An ERF 433
transcription factor was identified as a positive regulator of HDMF synthesis in 434
strawberry fruit and the mechanism of activation was shown to involve an ERF-MYB 435
transcription complex that regulates transcription of FaQR leading to the biosynthesis 436
of HDMF the characteristic volatile compound which has a major influence on 437
strawberry aroma 438
439
Materials and Methods 440
441
Plant Materials and Growth conditions 442
The strawberry (Fragaria times ananassa cv lsquoYuexinrsquo an octoploid cultivar) fruit used in 443
this study were bred by Zhejiang Academy of Agricultural Sciences (Haining 444
Zhejiang) Fruits at various developmental and ripening stages including G (green) T 445
(turning) IR (intermediate red) and R (full red) were harvested (Figure 1) and 446
transported to the laboratory within 2 h Thirty-six fruits of uniform size and free of 447
visible defects were selected at each stage with twelve fruits in each biological 448
replicate After removing the calyces fruits were then divided into the basal and 449
apical sections which were sampled separately (Figure 1) They were rapidly cut into 450
pieces frozen immediately in liquid nitrogen and stored at -80deg C until use Red ripe 451
fruits of different strawberry cultivars (Fragaria times ananassa octoploid cultivars) 452
including lsquoYuelirsquo lsquoBenihoppersquo lsquoMengxiangrsquo lsquoAmaoursquo lsquo10-1-4rsquo lsquoAkihimersquo lsquoSweet 453
Charliersquo lsquo07-1-4rsquo lsquoDarselectrsquo lsquoYuexinrsquo and lsquoXuemeirsquo were also provided by Zhejiang 454
Academy of Agricultural Sciences For each cultivar the fruits of three biological 455
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
17
replicates were sampled frozen in liquid nitrogen and stored at -80deg C for further use 456
457
Tobacco plants (Nicotiana benthamiana) used for dual-luciferase assays and 458
subcellular localization analysis in this study were grown in a growth chamber with a 459
lightdark cycle of 16 h8 h at 24degC 460
461
Detection of DMMF and HDMF 462
Automated HS-SPME-GC-MS was performed to detect both furanones in lsquoYuexinrsquo 463
strawberry fruit (Zorrilla-Fontanesi et al 2012) Samples were ground into a powder 464
under liquid nitrogen for analysis 465
466
For the detection of DMMF (Figure 1) 05 g (fresh weight) of each sample was 467
weighed in the vial to which was added 1 mL of EDTA solution (100 mM pH 75) 1 468
mL of CaCl2 solution (mv = 20) and 20 microL of 2-octanol as the internal standard 469
(007 μgμL) The mixture was homogenized and the vial closed and placed on the 470
sample tray for analysis by CombiPAL autosampler (CTC Analytic CA USA) The 471
fruit volatiles were sampled by headspace solid-phase microextraction with a 65-μm 472
polydimethylsiloxane-divinylbenzene fibre (PDMS-DVB) Initially vials were 473
pre-incubated at 50degC for 10 min under continuous agitation (500 rpm) then volatiles 474
were extracted for 30 min at the same temperature and agitation speed After that the 475
fibre was desorbed in the GC injection port for 5 min in splitless mode The 7890A 476
GC chromatograph was equipped with a DB-5ms column (60 m times 250 μm times 1 μm 477
JampW Scientific Folsom CA USA) with helium as the carrier gas at a constant flow 478
of 12 mLmin The GC was programmed at an initial temperature of 35degC for 2 min 479
with a ramp of 5degC min up to 250degC and held for 5 min The injection port interface 480
and MS source temperatures were 250degC 260degC and 230degC respectively The 481
ionization potential was set at 70 eV recorded by a 5975B mass spectrometer (Agilent 482
Technologies JampW Scientific Folsom CA USA) and the scanning speed was 7 483
scanss The same method was used to analyse HDMF and DMMF in fruits from 484
different cultivars (Supplemental Figure S3) except for the sample preparation 485
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18
procedure (Araguumlez et al 2013) briefly 05 g (fresh weight) of powdered fruit was 486
incubated at 30degC in a water bath for 5 min then 2 mL of NaCl (mv = 20) and 20 487
microL of 2-octanol as the internal standard (007 μgμL) were added and homogenized 488
489
For the detection of HDMF (Figure 1) and both furanones (Figure 4 and Supplemental 490
Table S3) a liquid-injection system equipped with CTC Pal ALS was used One gram 491
(fresh weight) of powdered fruit and 2 mL of NaCl (mv = 20) were homogenized in 492
a 10-mL tube and 300 μL of CH2Cl2 and 20 microL of 2-octanol (0766 μgμL) as the 493
internal standard were added to extract the volatiles the mixture was then 494
homogenized again The tubes were stored at room temperature for 20 min and 495
centrifuged at 12000 rpm for 5 min The subnatant was pipetted into a clean 15-mL 496
tube in which 20 mg of anhydrous sodium sulphate was added the tube was left 497
without shaking for half an hour Then 150 μL of the solution was transferred into a 498
GC vial and placed on the sample tray as described above Each sample (1 μL) was 499
injected using the autosampler and the analysis was accomplished by a 7890A 500
GC-MS system (Agilent Technologies JampW Scientific Folsom CA USA) equipped 501
with a DB-WAX column (30 m times 025 mm times 025 μm JampW) Helium (12 mLmin) 502
was used as a carrier gas The injection port (splitless injection mode) interface and 503
MS source temperatures were as described above The oven temperature was set at 504
60degC for 4 min then increased to 180degC at a rate of 4degCmin and maintained for 30 505
min DMMF was identified by comparison of electron ionization mass spectra and 506
retention time data with the data from the NISTEPANIH mass spectral library 507
(NIST-08 and Flavor) HDMF (Figure 1) was identified and qualified by comparison 508
with injected standard (Sigma) The quantitative analysis of both furanones (Figure 4 509
Supplemental Table S3 and Supplemental Figure S3) was determined using the peak 510
area of the internal standard as a reference based on total ion chromatogram (TIC) 511
512
RNA isolation and Reverse Transcription Quantitative PCR (RT-qPCR) 513
Total RNA from strawberry samples was isolated in this study using the CTAB 514
method (Chang et al 1993) Genomic DNA contamination was eliminated by 515
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
19
TURBO Dnase (Ambion) 1 μg of RNA was used to obtain cDNA using an IScriptTM 516
cDNA Synthesis Kit (Bio-Rad) The synthesized cDNA was diluted with water (120) 517
and 2 μL of diluted cDNA was used as the template for RT-qPCR Reactions were 518
performed in a total volume of 20 μL consisting of 10 μL of SYBR PCR supermix 519
(Bio-Rad) 1 μL of each primer (10 μM) 6 μL of DEPC-H2O and 2 μL of diluted 520
cDNA on CFX96 instrument (Bio-Rad) (Yin et al 2012) The oligonucleotide 521
primers for RT-qPCR analysis of genes including the AP2ERF FaQR and FaOMT 522
were designed according to the coding sequences of genes and the specificity was 523
verified before use (Min et al 2012) NCBIPrimer-BLAST was applied to design the 524
primers Relative expression levels were normalized to that of an internal controlmdashthe 525
interspacer 26S-18S strawberry RNA housekeeping gene FaRIB413 526
(Zorrilla-Fontanesi et al 2012) To investigate the differential expression of genes 527
during fruit development and ripening stages relative expression of each gene at the 528
R stage in the basal fruit section was set as 1 using the 2minus∆∆119862119879 method For transient 529
overexpression assay relative expression of control fruits with an empty vector (SK) 530
was set as 1 The primers used in RT-qPCR are listed in Supplemental Table S4 531
532
Gene isolation and analysis 533
Multiple database searches were performed to identify members of the strawberry 534
(Fragaria times ananassa) AP2ERF superfamily in the published strawberry databases 535
and annotations of Fragaria times ananassa and Fragaria times vesca by using the 536
AP2ERF DNA binding domain as a query sequence and 120 genes were identified 537
with AP2ERF domain(s) Based on the BLAST result primers (listed in 538
Supplemental Table S5) were used to amplify the coding full-length cDNAs of 539
AP2ERF genes The deduced amino acid sequences of AP2ERF proteins in 540
Arabidopsis thaliana used for construction of a phylogenetic tree were obtained from 541
the Arabidopsis Information Resource (TAIR) Alignment of the proteins was 542
performed using the neighbour-joining method in ClustalX (v181) and the 543
phylogenetic tree was constructed using FigTree (v131) 544
545
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20
FaMYB98 was obtained by yeast one-hybrid screening sequencing and the full-length 546
sequences were predicted by BLAST Primers were designed (listed in Supplemental 547
Table S5) to amplify the full-length coding sequence 548
549
The promoter of FaQR was cloned by Genome Walking as previously described (Yin 550
et al 2010) and conserved cis-element motifs in the promoter were manually 551
searched 552
553
Conserved domains within the FaAP2ERF proteins and FaMYB98 were analysed by 554
CD-search (httpswwwncbinlmnihgovStructurecddwrpsbcgi) and cellular 555
locations of proteins including FaERF9 and FaMYB98 were predicted with the 556
WoLF PSORT program (httpswwwgenscriptcomwolf-psorthtml) 557
558
Dual-Luciferase Assays 559
In accordance with a previous protocol (Yin et al 2010) the full-length cDNAs of 560
FaAP2ERF or FaMYB98 transcription factors were cloned into pGreen II 0029 561
62-SK vector and the promoter of FaQR was cloned into pGreen II 0800-LUC vector 562
A luciferase gene from Renillia (REN) driven by a 35S promoter in the LUC vector 563
acted as a positive control The above constructs were transiently expressed in 564
Nicotiana benthamiana leaves by Agrobacterium-mediated infiltration (strain 565
GV3101) and the activity of the TFs on the promoter was measured on the third day 566
after infiltration indicated by the ratio of enzyme activities of firefly luciferase (LUC) 567
and renilla luciferase (REN) using a Modulus Luminometer (Promega Madison WI 568
USA) To determine the activity of a specific transcription factor towards the 569
promoter we mixed the Agrobacterium culture with 1 mL of TF and 100 μL of 570
promoter and the LUCREN value of the empty vector SK on the promoter was set as 571
1 as a calibrator To test the combined effect of two transcription factors on the 572
promoter to the Agrobacterium culture mixture we added 05 mL of each TF and 100 573
μL of promoter the effect of the mixtures that contained each transcription factor (05 574
mL) and empty vector SK (05 mL) was also tested on the promoter as a control 575
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
21
576
Subcellular localization analysis 577
35S-FaERF9-GFP and 35S-FaMYB98-GFP were transiently expressed in tobacco (N 578
benthamiana) leaves by Agrobacterium infiltration (EHA105) using the same method 579
as described in the dual-luciferase assay above The transiently infected leaves were 580
imaged on the third day after infiltration using a Nikon A1-SHS confocal laser 581
scanning microscope The excitation wavelength for GFP fluorescence was 488 nm 582
and fluorescence was detected at 490ndash520 nm The primers used for GFP construction 583
are listed in Supplemental Table S6 584
585
Transient overexpression in strawberry fruit 586
Transient overexpression of FaERF9 and an overexpression binary vector (pGreen II 587
0029 62-SK-FaERF9-FaMYB98) were performed in strawberry fruit using the 588
FaERF9-SK construct described above for the dual-luciferase assays and the binary 589
vector constructed according to Liu et al 2013 The transfection of fruit was carried 590
out at the G stage (Hoffmann et al 2006) The FaERF9-SK construct and binary 591
vector were individually electroporated into Agrobacterium tumefaciens GV3101 and 592
the Agrobacterium culture suspended in infiltration buffer was infiltrated into the 593
whole fruit using a syringe As a control treatment fruits were infiltrated with 594
Agrobacterium carrying an empty vector SK under the same transfection conditions 595
Fruits were left attached to the plants and harvested on the seventh day after 596
infiltration Fruits of three biological replicates were sampled for further analysis 597
598
Yeast one-hybrid assay 599
In order to identify proteins that bind to the FaQR promoter the Matchmaker Gold 600
Yeast One-hybrid Library Screening System (Clontech USA) was used The sequence 601
of the FaQR promoter was cloned into the pAbAi vector and the construct was 602
integrated into the genome of the Y1HGold yeast strain A mixture of total RNA from 603
strawberry fruit at four stages (G T IR R) was used to construct the prey cDNA 604
library (TaKaRa) The background AbAr expression of Y1HGold FaQR-pAbAi strain 605
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
22
was tested according to the system user manual and then screening for protein-DNA 606
interactions was carried out Furthermore the full length of each transcription factor 607
was separately cloned into pGADT7 AD vector to confirm the screening results The 608
relationship between FaERF9 and FaQR promoter was also examined individually 609
Primers used in this assay are listed in Supplemental Table S6 610
611
Expression and purification of FaMYB98 recombinant protein 612
A 405-bp region spanning the DNA-binding domain of FaMYB98 was amplified 613
from FaMYB98 cDNA and cloned into a pET6timesHN vector (Clontech Palo CA USA) 614
to generate the recombinant N-terminal His-tagged protein the primers used are listed 615
in Supplemental Table S6 The resulting construct was sequenced and introduced into 616
Escherichia coli strain Rosetta 2(DE3)pLysS (Novagen) Ten millilitres of the 617
overnight culture was combined with 500 mL of an LB liquid medium (100 μgmL 618
ampicillin and 34 μgmL chloramphenicol) as described (Li et al 2017) Isopropyl 619
β-D-1-thiogalactopyranoside (IPTG) was added to a final concentration of 1 mM and 620
the bacterial culture was incubated at 18degC at 150 rpm for 18 h Then the cells were 621
harvested using a centrifuge and resuspended in 1times PBS buffer (Sangon Biotech) 622
after which they were disrupted by sonication and the supernatant was purified using 623
a HisTALONTM Gravity Column (Clontech) according to the user manual The PD-10 624
Desalting column (GE Healthcare) was then used for buffer change and sample 625
clean-up of proteins according to the gravity protocol SDS-PAGE was performed and 626
the protein was visualized using Coomassie brilliant blue 627
628
Electrophoretic mobility shift assay (EMSA) 629
A Lightshift Chemiluminescent EMSA kit (Thermo) was used to perform EMSA 630
experiments according to the manufacturerrsquos instructions Single-strand 631
oligonucleotides were synthesized and biotinylated by GeneBio Biotech (Hangzhou 632
China) The details of the EMSA assay are provided in Ge et al (2017) The probes 633
used for EMSAs are listed in Supplemental Table S6 634
635
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
23
636
Yeast two-hybrid assay 637
The DUALhunter system (Dualsystems Biotech Switzerland) was used to investigate 638
the interaction between FaERF9 and FaMYB98 Full-length coding sequences of 639
FaERF9 and FaMYB98 were respectively cloned into pDHB1 bait vector and 640
pPR3-N prey vector sequences were verified and the bait plasmid was 641
co-transformed with prey plasmid into NMY51 in the combinations below 642
FaMYB98-pDHB1pPR3-N FaMYB98-pDHB1FaERF9-pPR3-N 643
FaMYB98-pDHB1pOst1-NubI FaERF9-pDHB1pPR3-N 644
FaERF9-pDHB1FaMYB98-pPR3-N and FaERF9-pDHB1pOst1-NubI (Li et al 645
2017) Transformed cells were spread onto the following plates DDO (SD 646
medium-Trp-Leu) QDO (SD medium-Trp-Leu-His-Ade) and QDO+3-AT (QDO 647
medium supplemented with 1 mM 3-amino-124-triazole) The control plasmid 648
pOst1-NubI was used to determine whether the bait was functional the pPR3-N prey 649
vector plasmid was used to test whether the bait displayed non-specific background 650
and positive interactions were indicated by the growth of yeast on QDO and 651
QDO+3-AT plates The Primers used in the DUALhunter assay are listed in 652
Supplemental Table S6 653
654
Bimolecular fluorescence complementation (BiFC) assays 655
Full-length FaERF9 and FaMYB98 respectively were cloned into sequences 656
encoding the N- and C- fragments of YFP protein (Lv et al 2014) All constructs 657
were transiently expressed in tobacco (N benthamiana) leaves by Agrobacterium 658
infiltration (EHA105) The YFP fluorescence of transfected leaves was imaged 40 h 659
after infiltration by using a Nikon A1-SHS confocal laser scanning microscope The 660
excitation wavelength for YFP was 488 nm and fluorescence was detected at 520ndash661
540 nm Primers used are listed in Supplemental Table S6 662
663
Statistics 664
A Studentrsquos two-tailed t test ( plt005 plt001 and plt0001) was used to 665
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
24
determine significant differences between two groups in this study Microsoft Excel 666
was used to perform linear regressive analysis significant differences were 667
determined by SPSS Statistics 200 and scatter plots were prepared with Origin80 668
Least significant difference (LSD) at the 5 level was calculated using Microsoft 669
Excel Figures were prepared with Origin80 (Microcal Software Inc Northampton 670
MA USA) The online tool MetaboAnalyst 36 (httpwwwmetaboanalystca) was 671
used to analyse the transcript abundance of the AP2ERF genes 672
673
Accession numbers 674
Sequence data from this article have been deposited in GenBank under the accession 675
numbers MH332903-MH333022 for AP2ERF genes in Fragaria times ananassa and 676
MH333023 for FaMYB98 GenBank numbers for FaQR and FaOMT were 677
AY1588361 (Raab et al 2006) and AF2204912 (Wein et al 2002) 678
679
Supplemental Material 680
Supplemental Figure S1 Phylogenetic analysis of FaAP2ERF and Arabidopsis 681
AP2ERF proteins 682
Supplemental Figure S2 Analysis of FaAP2ERF gene expression patterns in 683
strawberry fruit during development and ripening 684
Supplemental Figure S3 Contents of furanones in fruit of strawberry cultivars 685
Supplemental Figure S4 Relative expression of FaERF9 in FaERF9-FaMYB98- 686
and FaERF9-overexpressing fruits 687
Supplemental Figure S5 Subcellular localization of FaMYB98 688
Supplemental Figure S6 The combined activation effects of FaERF9FaMYB98 on 689
the FaOMT promoter 690
Supplemental Figure S7 Relative expression of FaOMT in 691
FaERF9-overexpressing fruits 692
Supplemental Table S1 AP2ERF superfamily genes in Fragaria times ananassa 693
Supplemental Table S2 Classification of the AP2ERF superfamily members in 694
Fragaria times ananassa 695
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25
Supplemental Table S3 Furanone content in FaERF9-FaMYB98- and 696
FaERF9-overexpressing fruits 697
Supplemental Table S4 Primers used for reverse transcription quantitative PCR 698
(RT-qPCR) 699
Supplemental Table S5 Primers used to amplify the full-length coding sequences of 700
AP2ERF genes and FaMYB98 in strawberry (Fragaria times ananassa) 701
Supplemental Table S6 Primers used for vector construction 702
703
Acknowledgments 704
This research was supported by the National Key Research and Development 705
Program (2016YFD0400101) the Project of the Science and Technology Department 706
of Zhejiang Province (2016C04001) and the 111 Project (B17039) 707
708
Figure legends 709
Figure 1 Changes in furanone content and furanone biosynthetic genes during 710
strawberry (Fragaria times ananassa Duch cv Yuexin) fruit development and ripening 711
A Fruits were collected at four ripening stages G (green stage) T (turning stage) IR 712
(intermediate red stage) R (full red stage) B Changes in the contents of furaneol 713
(HDMF) and mesifurane (DMMF) HDMF content was calculated using a standard 714
curve of HDMF while DMMF content was calculated with an internal standard as the 715
reference C Expression levels of FaQR and FaOMT The expression levels of each 716
gene were calculated relative to corresponding values in the basal section at the R 717
stage SEs were calculated from three replicates and LSD values represent the least 718
significant differences at p = 005 719
Figure 2 Regulatory effects of FaAP2ERF on the promoter of FaQR LUCREN 720
values of the empty vector on FaQR promoter were used as the calibrator set as 1 721
and SEs were calculated from five replicates statistical significance was determined 722
by Studentrsquos two-tailed t test ( plt0001) 723
Figure 3 Expression and the subcellular localization of FaERF9 A The expression 724
levels were calculated relative to the levels in the basal section at the R stage B 725
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
26
Subcellular localization analysis was performed in tobacco leaves The tobacco used 726
in the assay was stably transformed with a specific nucleus localized red fluorescence 727
protein construct and the red fluorescence indicates the nucleus-localized signal 728
(NLS) Scale bar = 25 microm SEs were calculated from three replicates 729
Figure 4 Transient overexpression of FaERF9 in strawberry fruit A Relative 730
expression of FaQR and FaERF9 in FaERF9-OX fruit 7 days after infiltration The 731
expression was calculated relative to the average value in control (SK) fruits B 732
HDMF and DMMF content in FaERF9-OX fruit The content of both furanones 733
were quantified using the peak area of the internal standard (2-octanol) as the 734
reference SEs were calculated from three replicates Statistical significance was 735
determined by Studentrsquos two-tailed t test ( plt005 plt001 plt0001) 736
Figure 5 Scatter plots of 11 strawberry cultivars A Linear regression analysis 737
between FaERF9 expression and FaQR expression B Linear regression analysis 738
between FaERF9 expression and furanone content The relative expression was 739
normalized to that of the housekeeping gene FaRIB413 and furanone content was 740
calculated with internal standard as the reference Significant differences were 741
determined by SPSS Statistics 200 742
Figure 6 Interactions of FaERF9 and FaMYB98 with the FaQR promoter A Yeast 743
one-hybrid analysis of the interaction of FaERF9 and FaQR promoter B Yeast 744
one-hybrid analysis of the interaction of FaMYB98 and FaQR promoter C 745
Regulatory effect of FaMYB98 on the FaQR promoter Auto-activation was tested on 746
SD-Ura (synthetically defined medium without uracil) in presence of Aureobasidin A 747
(AbA) and physical interaction was determined on SD-Leu (synthetically defined 748
medium without leucine) in presence of AbA LUCREN values of the empty vector 749
on FaQR promoter were used as the calibrator set as 1 and error bars were calculated 750
from five replicates Statistical significance was determined by Studentrsquos two-tailed t 751
test ( plt005 plt001 plt0001) 752
Figure 7 Electrophoretic mobility shift assay of FaMYB98 binding to FaQR 753
promoter A The probe sequence used for EMSA and mutated nucleotides are 754
indicated with lowercase letters B Purified DNA-binding domain of FaMYB98 755
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
27
protein and biotin-labelled DNA probe were mixed and analysed on 6 native 756
polyacrylamide gels and then photographed Presence or absence of specific probes is 757
marked by the symbol + or - 758
Figure 8 The combined activation effects of FaERF9FaMYB98 on the FaQR 759
promoter LUCREN values obtained with the empty vector and FaQR promoter were 760
used as the calibrator set as 1 and error bars were calculated from five replicates 761
Figure 9 Yeast two-hybrid analysis of the protein-protein interactions between 762
FaMYB98 and FaERF9 Positive interactions were determined by the growth of 763
yeast cells on selection plates Bait with pOST acted as positive controls and bait with 764
pPR3 as negative controls DDO synthetically defined medium without tryptophan 765
and leucine QDO synthetically defined medium without tryptophan leucine 766
histidine and adenine QDO+3AT QDO medium supplemented with 1 mM 767
3-aminotriazole 768
Figure 10 BiFC analysis of the protein-protein interactions between FaMYB98 and 769
FaERF9 The pairs of fusion proteins tested were FaMYB98-YFPN+FaERF9-YFPC 770
FaERF9-YFPN+FaMYB98-YFPC FaMYB98-YFPN+FaMYB98-YFPC and 771
FaERF9-YFPN+FaERF9-YFPC The other combinations were negative controls 772
The tobacco used in the assay was stably transformed with a specific 773
nucleus-localized red fluorescence protein construct and the red fluorescence 774
indicated the nucleus-localized signal (NLS) Fluorescence of the yellow fluorescence 775
protein (YFP) visualized the interaction in vivo Scale bar = 25 microm 776
777
Literature Cited 778
779
Agarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression 780
of PgDREB2A transcription factor enhances abiotic stress tolerance and activates 781
downstream stress-responsive genes Mol Biol Rep 37 1125-1135 782
Araguumlez I Osorio S Hoffmann T Rambla JL Medina-Escobar N Granell A 783
Botella MAacute Schwab W Valpuesta V (2013) Eugenol production in achenes and 784
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28
receptacles of strawberry fruits is catalyzed by synthases exhibiting distinct kinetics 785
Plant Physiol 163 946-958 786
Carvalho RF Carvalho SD OrsquoGrady K Folta KM (2016) Agroinfiltration of 787
strawberry fruit mdash a powerful transient expression system for gene validation Curr 788
Plant Biol 6 19-37 789
Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic 790
(Amsterdam) 210 34-40 791
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating 792
RNA from pine trees Plant Mol Biol Rep 11 113-116 793
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC 794
Clark DG (2011) PhMYB4 fine-tunes the floral volatile signature of 795
Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143 796
Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz 797
EA Taylor MG Smits-Kroon MT Schuurink RC Haring MA Giovannoni J 798
Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic 799
pathway by ectopic expression of a MYB transcription factor in tomato fruit Plant 800
Cell 23 2738-2753 801
Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan 802
XW Yang ZY (2017) Differential responses of four biosynthetic pathways of 803
aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under 804
interaction of light and temperature Food Chem 221 356-364 805
Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of 806
differentially-expressed genes during somatic embryogenesis in Fragaria times 807
ananassa Duch lsquoBenihopprsquo J Hortic Sci Biotechnol 90 671-681 808
Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 809
transcriptionally regulates chilling-induced lignification of loquat fruit via physical 810
interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136 811
Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM 812
(2004) Functional interactions between a glutamine synthetase promoter and MYB 813
proteins Plant J 39 513-526 814
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
29
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) 815
Sucrose nonfermenting1-related protein kinase26 an ortholog of open stomata1 is 816
a negative regulator of strawberry fruit development and ripening Plant Physiol 817
167 915-930 818
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene 819
expression in strawberry fruit (Fragaria times ananassa) by agroinfiltration a rapid 820
assay for gene function analysis Plant J 48 818-826 821
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of 822
selected aroma-active compounds in strawberries by headspace solid-phase 823
microextraction gas chromatography and correlation with sensory descriptive 824
analysis J Food Sci 72 S487-S496 825
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid 826
plays an important role in the regulation of strawberry fruit ripening Plant Physiol 827
157 188-199 828
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of 829
NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes BMC 830
Plant Biol 6 20 831
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN 832
(2005) MYB98 is required for pollen tube guidance and synergid cell differentiation 833
in Arabidopsis Plant Cell 17 2981-2992 834
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional 835
characterization of enone oxidoreductases from strawberry and tomato fruit J 836
Agric Food Chem 55 6705-6711 837
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You 838
J-S Rohloff J Randall SK Alsheikh M (2012) Proteomic study of 839
low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ 840
in cold tolerance Plant Physiol 159 1787-1805 841
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional 842
characterization of four APETALA2-family genes (RAP26 RAP26L DREB19 843
and DREB26) in Arabidopsis Plant Mol Biol 75 107-127 844
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
30
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon 845
J Gupta V (2013) An oxidoreductase from lsquoAlphonsorsquo mango catalyzing 846
biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494 847
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in 848
strawberries Z Lebensm-Unters Forsch 195 120-123 849
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X 850
(2015) Label-free quantitative proteomics to investigate strawberry fruit proteome 851
changes under controlled atmosphere and low temperature storage J Proteomics 852
120 44-57 853
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 854
cooperates with CitWRKY1 to participate in citric acid degradation via 855
up-regulation of CitAco3 J Exp Bot 68 3419-3426 856
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription 857
factor CitERF71 activates the terpene synthase gene CitTPS16 involved in the 858
synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938 859
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and 860
transcriptomic analysis of the AP2ERF superfamily in Vitis vinifera BMC 861
Genomics 11 719 862
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive 863
Factor (AP2ERF) transcription factors mediators of stress responses and 864
developmental programs New Phytol 199 639-649 865
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 866
interacting with EOBI negatively regulates fragrance biosynthesis in petunia 867
flowers New Phytol 215 1490-1502 868
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu 869
CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 in regulating 870
anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) 871
during anthocyanin biosynthesis Plant Cell Tissue Organ Cult 115 285-298 872
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
31
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao 873
CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphate signaling and 874
homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597 875
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC 876
Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL 877
Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor 878
regulates eugenol production in ripe strawberry fruit receptacles Plant Physiol 168 879
598-614 880
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics 881
and volatile constituents of strawberry (cv Cigaline) during maturation J Agric 882
Food Chem 52 1248-1254 883
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS 884
(2012) Ethylene-responsive transcription factors interact with promoters of ADH 885
and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 886
63 6393-6405 887
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM 888
Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-Franco A 889
Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific 890
transcription factor FaDOF2 regulates the production of eugenol in ripe fruit 891
receptacles J Exp Bot 68 4529-4543 892
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) 893
Comparison and verification of the genes involved in ethylene biosynthesis and 894
signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44 895
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the 896
ERF gene family in Arabidopsis and rice Plant Physiol 140 411-432 897
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in 898
sour cherry and strawberry and the heterologous expression of CBF1 in strawberry 899
J Am Soc Hortic Sci 127 489-494 900
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech 901
JC Ohme-Takagi M Regad F Bouzayen M (2012) Functional analysis and 902
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
32
binding affinity of tomato ethylene response factors provide insight on the 903
molecular bases of plant differential responses to ethylene BMC Plant Biol 12 190 904
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) 905
Methylpentoses are possible precursors of furanones in fruits Prikl Biokhim 906
Mikrobiol 28 123-127 907
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery 908
of synergid-expressed genes encoding filiform apparatus localized proteins Plant 909
Cell 19 2557-2568 910
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria 911
vesca L compared to those of cultivated berries Fragariatimes ananassa cv Senga 912
Sengana J Agric Food Chem 27 19-22 913
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W 914
Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of the strawberry 915
flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone 916
oxidoreductase Plant Cell 18 1023-1037 917
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L 918
Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim M Broun P Zhang 919
JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription 920
factors genome-wide comparative analysis among eukaryotes Science 290 921
2105-2110 922
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the 923
formation of 25-dimethyl-4-hydroxy-3(2H)-furanone in detached ripening 924
strawberry fruits J Agric Food Chem 46 1488-1493 925
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 926
25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in 927
strawberry fruits Phytochemistry 43 155-159 928
Schwab W (1998) Application of stable isotope ratio analysis explaining the 929
bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone in plants by a biological 930
maillard reaction J Agric Food Chem 46 2266ndash2269 931
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
33
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) 932
Molecules 18 6936-6951 933
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard 934
products Recent Res Dev Phytochem 1 643-673 935
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL 936
Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJ Sims CA 937
Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical 938
compositions a seasonal influence and effects on sensory perception PLoS One 9 939
e88446 940
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) 941
Identification phylogeny and transcript profiling of ERF family genes during 942
development and abiotic stress treatments in tomato Mol Genet Genomics 284 943
455-475 944
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) 945
CitAP210 activation of the terpene synthase CsTPS1 is associated with the 946
synthesis of (+)-valencene in lsquoNewhallrsquo orange J Exp Bot 67 4105-4115 947
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes 948
Dev Genes Evol 214 105-114 949
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K 950
Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the 951
key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151 952
Spitzer-Rimon B Farhi M Albo B Cnarsquoani A Ben Zvi MM Masci T Edelbaum 953
O Yu YX Shklarman E Ovadis M Vainstein A (2012) The R2R3-MYB-like 954
regulatory factor EOBI acting downstream of EOBII regulates scent production 955
by activating ODO1 and structural scent-related genes in petunia Plant Cell 24 956
5089-5105 957
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp 958
Bot 68 4407-4409 959
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla 960
JF Amaya I Giavalisco P Fernie AR Botella MA Valpuesta V (2015) Central 961
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34
role of FaGAMYB in the transition of the strawberry receptacle from development 962
to ripening New Phytol 208 482-496 963
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 964
regulates fragrance biosynthesis in petunia flowers Plant Cell 17 1612-1624 965
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS 966
(2018) The potassium channel FaTPK1 plays a critical role in fruit quality 967
formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748 968
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) 969
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Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of 977
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Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS 979
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Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in 982
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Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ 984
Zhang SL Wu J (2017) Map-based cloning of the pear gene MYB114 identifies an 985
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involved in regulating fruit ripening Plant Physiol 153 1280-1292 989
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35
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injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1000
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Arabidopsis AP2ERF transcription factor RAP26 participates in ABA salt and 1012
osmotic stress responses Gene 457 1-12 1013
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B 1014
Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) Genome-wide 1015
analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic 1016
(Amsterdam) 123 73-81 1017
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF 1018
Valpuesta V Botella MA Granell A Amaya I (2012) Genetic analysis of 1019
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36
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locus controlling natural variation in mesifurane content Plant Physiol 159 1021
851-870 1022
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
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wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
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Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive Factor (AP2ERF) transcription factors mediators of stressresponses and developmental programs New Phytol 199 639-649
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Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphatesignaling and homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597
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Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor regulates eugenol production in ripe strawberry fruitreceptacles Plant Physiol 168 598-614
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics and volatile constituents of strawberry (cv Cigaline)during maturation J Agric Food Chem 52 1248-1254
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS (2012) Ethylene-responsive transcription factors interact withpromoters of ADH and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 63 6393-6405
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-FrancoA Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific transcription factor FaDOF2 regulates the production ofeugenol in ripe fruit receptacles J Exp Bot 68 4529-4543
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) Comparison and verification of the genes involved in ethylenebiosynthesis and signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice Plant Physiol140 411-432
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in sour cherry and strawberry and the heterologousexpression of CBF1 in strawberry J Am Soc Hortic Sci 127 489-494
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech JC Ohme-Takagi M Regad F Bouzayen M (2012)Functional analysis and binding affinity of tomato ethylene response factors provide insight on the molecular bases of plant differentialresponses to ethylene BMC Plant Biol 12 190
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) Methylpentoses are possible precursors of furanones in fruits PriklBiokhim Mikrobiol 28 123-127
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery of synergid-expressed genes encoding filiformapparatus localized proteins Plant Cell 19 2557-2568
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria vesca L compared to those of cultivated berriesFragariatimes ananassa cv Senga Sengana J Agric Food Chem 27 19-22
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of thestrawberry flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone oxidoreductase Plant Cell 18 1023-1037
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim MBroun P Zhang JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription factors genome-wide comparative analysisamong eukaryotes Science 290 2105-2110
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the formation of 25-dimethyl-4-hydroxy-3(2H)-furanonein detached ripening strawberry fruits J Agric Food Chem 46 1488-1493
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in strawberry fruits Phytochemistry 43 155-159
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (1998) Application of stable isotope ratio analysis explaining the bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone inplants by a biological maillard reaction J Agric Food Chem 46 2266ndash2269
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) Molecules 18 6936-6951Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard products Recent Res Dev Phytochem 1 643-673Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJSims CA Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical compositions a seasonal influence and effects on sensoryperception PLoS One 9 e88446
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) Identification phylogeny and transcript profiling of ERFfamily genes during development and abiotic stress treatments in tomato Mol Genet Genomics 284 455-475
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) CitAP210 activation of the terpene synthase CsTPS1 isassociated with the synthesis of (+)-valencene in Newhall orange J Exp Bot 67 4105-4115
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes Dev Genes Evol 214 105-114Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Spitzer-Rimon B Farhi M Albo B Cnaani A Ben Zvi MM Masci T Edelbaum O Yu YX Shklarman E Ovadis M Vainstein A (2012) TheR2R3-MYB-like regulatory factor EOBI acting downstream of EOBII regulates scent production by activating ODO1 and structuralscent-related genes in petunia Plant Cell 24 5089-5105
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp Bot 68 4407-4409Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla JF Amaya I Giavalisco P Fernie AR Botella MAValpuesta V (2015) Central role of FaGAMYB in the transition of the strawberry receptacle from development to ripening New Phytol208 482-496
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 regulates fragrance biosynthesis in petunia flowers PlantCell 17 1612-1624
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS (2018) The potassium channel FaTPK1 plays a critical role infruit quality formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) Isolation cloning and expression of a multifunctional O- wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma compounds in strawberry fruitsPlant J 31 755-765
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor types their evolutionary origin and speciesdistribution In A handbook of transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular Biochemistry 52 25-73
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of odor (Buettner A Ed) Springer Cham 9-10Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS (2014) Isolation classification and transcription profiles ofthe AP2ERF transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in regulation of fruit quality Crit Rev Plant Sci 35 120-130
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ Zhang SL Wu J (2017) Map-based cloning of the pear geneMYB114 identifies an interaction with other transcription factors to coordinately regulate fruit anthocyanin biosynthesis Plant J 92437-451
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes involved in regulating fruit ripening Plant Physiol 1531280-1292
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Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) Expression of ethylene response genes during persimmonfruit astringency removal Planta 235 895-906
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Zabetakis I Gramshaw JW Robinson DS (1999) 25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis andbiosynthesis-a review Food Chem 65 139-151
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Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci Food Agric 74 421-434Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 an AP2ERF gene is a novel regulator of fruit lignificationinduced by chilling injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1325-1334
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Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation classification and transcription profiles of the Ethylene ResponseFactors (ERFs) in ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215
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Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML (2012) Genome-wide analysis of the AP2ERF superfamily inpeach (Prunus persica) Genet Mol Res 11 4788-4809
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Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and expression analysis of a CRTDRE-binding factor gene FaCBF1from Fragaria times ananassa Acta Hortic 41 240-248
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The Arabidopsis AP2ERF transcription factor RAP26 participatesin ABA salt and osmotic stress responses Gene 457 1-12
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Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Genome-wide analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic (Amsterdam) 123 73-81Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
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wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
16
(Figure 2) may provide additional information about the complexity of this regulation 426
Overall this study provides important clues for understanding the transcriptional 427
regulation of HDMF synthesis and identifies specific transcription factors that are 428
likely to be good targets for molecular breeding for improved flavour 429
430
Conclusions 431
Screening of the AP2ERF superfamily in strawberry (Fragaria times ananassa) 432
identified candidate members capable of activating the FaQR promoter An ERF 433
transcription factor was identified as a positive regulator of HDMF synthesis in 434
strawberry fruit and the mechanism of activation was shown to involve an ERF-MYB 435
transcription complex that regulates transcription of FaQR leading to the biosynthesis 436
of HDMF the characteristic volatile compound which has a major influence on 437
strawberry aroma 438
439
Materials and Methods 440
441
Plant Materials and Growth conditions 442
The strawberry (Fragaria times ananassa cv lsquoYuexinrsquo an octoploid cultivar) fruit used in 443
this study were bred by Zhejiang Academy of Agricultural Sciences (Haining 444
Zhejiang) Fruits at various developmental and ripening stages including G (green) T 445
(turning) IR (intermediate red) and R (full red) were harvested (Figure 1) and 446
transported to the laboratory within 2 h Thirty-six fruits of uniform size and free of 447
visible defects were selected at each stage with twelve fruits in each biological 448
replicate After removing the calyces fruits were then divided into the basal and 449
apical sections which were sampled separately (Figure 1) They were rapidly cut into 450
pieces frozen immediately in liquid nitrogen and stored at -80deg C until use Red ripe 451
fruits of different strawberry cultivars (Fragaria times ananassa octoploid cultivars) 452
including lsquoYuelirsquo lsquoBenihoppersquo lsquoMengxiangrsquo lsquoAmaoursquo lsquo10-1-4rsquo lsquoAkihimersquo lsquoSweet 453
Charliersquo lsquo07-1-4rsquo lsquoDarselectrsquo lsquoYuexinrsquo and lsquoXuemeirsquo were also provided by Zhejiang 454
Academy of Agricultural Sciences For each cultivar the fruits of three biological 455
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
17
replicates were sampled frozen in liquid nitrogen and stored at -80deg C for further use 456
457
Tobacco plants (Nicotiana benthamiana) used for dual-luciferase assays and 458
subcellular localization analysis in this study were grown in a growth chamber with a 459
lightdark cycle of 16 h8 h at 24degC 460
461
Detection of DMMF and HDMF 462
Automated HS-SPME-GC-MS was performed to detect both furanones in lsquoYuexinrsquo 463
strawberry fruit (Zorrilla-Fontanesi et al 2012) Samples were ground into a powder 464
under liquid nitrogen for analysis 465
466
For the detection of DMMF (Figure 1) 05 g (fresh weight) of each sample was 467
weighed in the vial to which was added 1 mL of EDTA solution (100 mM pH 75) 1 468
mL of CaCl2 solution (mv = 20) and 20 microL of 2-octanol as the internal standard 469
(007 μgμL) The mixture was homogenized and the vial closed and placed on the 470
sample tray for analysis by CombiPAL autosampler (CTC Analytic CA USA) The 471
fruit volatiles were sampled by headspace solid-phase microextraction with a 65-μm 472
polydimethylsiloxane-divinylbenzene fibre (PDMS-DVB) Initially vials were 473
pre-incubated at 50degC for 10 min under continuous agitation (500 rpm) then volatiles 474
were extracted for 30 min at the same temperature and agitation speed After that the 475
fibre was desorbed in the GC injection port for 5 min in splitless mode The 7890A 476
GC chromatograph was equipped with a DB-5ms column (60 m times 250 μm times 1 μm 477
JampW Scientific Folsom CA USA) with helium as the carrier gas at a constant flow 478
of 12 mLmin The GC was programmed at an initial temperature of 35degC for 2 min 479
with a ramp of 5degC min up to 250degC and held for 5 min The injection port interface 480
and MS source temperatures were 250degC 260degC and 230degC respectively The 481
ionization potential was set at 70 eV recorded by a 5975B mass spectrometer (Agilent 482
Technologies JampW Scientific Folsom CA USA) and the scanning speed was 7 483
scanss The same method was used to analyse HDMF and DMMF in fruits from 484
different cultivars (Supplemental Figure S3) except for the sample preparation 485
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
18
procedure (Araguumlez et al 2013) briefly 05 g (fresh weight) of powdered fruit was 486
incubated at 30degC in a water bath for 5 min then 2 mL of NaCl (mv = 20) and 20 487
microL of 2-octanol as the internal standard (007 μgμL) were added and homogenized 488
489
For the detection of HDMF (Figure 1) and both furanones (Figure 4 and Supplemental 490
Table S3) a liquid-injection system equipped with CTC Pal ALS was used One gram 491
(fresh weight) of powdered fruit and 2 mL of NaCl (mv = 20) were homogenized in 492
a 10-mL tube and 300 μL of CH2Cl2 and 20 microL of 2-octanol (0766 μgμL) as the 493
internal standard were added to extract the volatiles the mixture was then 494
homogenized again The tubes were stored at room temperature for 20 min and 495
centrifuged at 12000 rpm for 5 min The subnatant was pipetted into a clean 15-mL 496
tube in which 20 mg of anhydrous sodium sulphate was added the tube was left 497
without shaking for half an hour Then 150 μL of the solution was transferred into a 498
GC vial and placed on the sample tray as described above Each sample (1 μL) was 499
injected using the autosampler and the analysis was accomplished by a 7890A 500
GC-MS system (Agilent Technologies JampW Scientific Folsom CA USA) equipped 501
with a DB-WAX column (30 m times 025 mm times 025 μm JampW) Helium (12 mLmin) 502
was used as a carrier gas The injection port (splitless injection mode) interface and 503
MS source temperatures were as described above The oven temperature was set at 504
60degC for 4 min then increased to 180degC at a rate of 4degCmin and maintained for 30 505
min DMMF was identified by comparison of electron ionization mass spectra and 506
retention time data with the data from the NISTEPANIH mass spectral library 507
(NIST-08 and Flavor) HDMF (Figure 1) was identified and qualified by comparison 508
with injected standard (Sigma) The quantitative analysis of both furanones (Figure 4 509
Supplemental Table S3 and Supplemental Figure S3) was determined using the peak 510
area of the internal standard as a reference based on total ion chromatogram (TIC) 511
512
RNA isolation and Reverse Transcription Quantitative PCR (RT-qPCR) 513
Total RNA from strawberry samples was isolated in this study using the CTAB 514
method (Chang et al 1993) Genomic DNA contamination was eliminated by 515
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
19
TURBO Dnase (Ambion) 1 μg of RNA was used to obtain cDNA using an IScriptTM 516
cDNA Synthesis Kit (Bio-Rad) The synthesized cDNA was diluted with water (120) 517
and 2 μL of diluted cDNA was used as the template for RT-qPCR Reactions were 518
performed in a total volume of 20 μL consisting of 10 μL of SYBR PCR supermix 519
(Bio-Rad) 1 μL of each primer (10 μM) 6 μL of DEPC-H2O and 2 μL of diluted 520
cDNA on CFX96 instrument (Bio-Rad) (Yin et al 2012) The oligonucleotide 521
primers for RT-qPCR analysis of genes including the AP2ERF FaQR and FaOMT 522
were designed according to the coding sequences of genes and the specificity was 523
verified before use (Min et al 2012) NCBIPrimer-BLAST was applied to design the 524
primers Relative expression levels were normalized to that of an internal controlmdashthe 525
interspacer 26S-18S strawberry RNA housekeeping gene FaRIB413 526
(Zorrilla-Fontanesi et al 2012) To investigate the differential expression of genes 527
during fruit development and ripening stages relative expression of each gene at the 528
R stage in the basal fruit section was set as 1 using the 2minus∆∆119862119879 method For transient 529
overexpression assay relative expression of control fruits with an empty vector (SK) 530
was set as 1 The primers used in RT-qPCR are listed in Supplemental Table S4 531
532
Gene isolation and analysis 533
Multiple database searches were performed to identify members of the strawberry 534
(Fragaria times ananassa) AP2ERF superfamily in the published strawberry databases 535
and annotations of Fragaria times ananassa and Fragaria times vesca by using the 536
AP2ERF DNA binding domain as a query sequence and 120 genes were identified 537
with AP2ERF domain(s) Based on the BLAST result primers (listed in 538
Supplemental Table S5) were used to amplify the coding full-length cDNAs of 539
AP2ERF genes The deduced amino acid sequences of AP2ERF proteins in 540
Arabidopsis thaliana used for construction of a phylogenetic tree were obtained from 541
the Arabidopsis Information Resource (TAIR) Alignment of the proteins was 542
performed using the neighbour-joining method in ClustalX (v181) and the 543
phylogenetic tree was constructed using FigTree (v131) 544
545
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
20
FaMYB98 was obtained by yeast one-hybrid screening sequencing and the full-length 546
sequences were predicted by BLAST Primers were designed (listed in Supplemental 547
Table S5) to amplify the full-length coding sequence 548
549
The promoter of FaQR was cloned by Genome Walking as previously described (Yin 550
et al 2010) and conserved cis-element motifs in the promoter were manually 551
searched 552
553
Conserved domains within the FaAP2ERF proteins and FaMYB98 were analysed by 554
CD-search (httpswwwncbinlmnihgovStructurecddwrpsbcgi) and cellular 555
locations of proteins including FaERF9 and FaMYB98 were predicted with the 556
WoLF PSORT program (httpswwwgenscriptcomwolf-psorthtml) 557
558
Dual-Luciferase Assays 559
In accordance with a previous protocol (Yin et al 2010) the full-length cDNAs of 560
FaAP2ERF or FaMYB98 transcription factors were cloned into pGreen II 0029 561
62-SK vector and the promoter of FaQR was cloned into pGreen II 0800-LUC vector 562
A luciferase gene from Renillia (REN) driven by a 35S promoter in the LUC vector 563
acted as a positive control The above constructs were transiently expressed in 564
Nicotiana benthamiana leaves by Agrobacterium-mediated infiltration (strain 565
GV3101) and the activity of the TFs on the promoter was measured on the third day 566
after infiltration indicated by the ratio of enzyme activities of firefly luciferase (LUC) 567
and renilla luciferase (REN) using a Modulus Luminometer (Promega Madison WI 568
USA) To determine the activity of a specific transcription factor towards the 569
promoter we mixed the Agrobacterium culture with 1 mL of TF and 100 μL of 570
promoter and the LUCREN value of the empty vector SK on the promoter was set as 571
1 as a calibrator To test the combined effect of two transcription factors on the 572
promoter to the Agrobacterium culture mixture we added 05 mL of each TF and 100 573
μL of promoter the effect of the mixtures that contained each transcription factor (05 574
mL) and empty vector SK (05 mL) was also tested on the promoter as a control 575
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
21
576
Subcellular localization analysis 577
35S-FaERF9-GFP and 35S-FaMYB98-GFP were transiently expressed in tobacco (N 578
benthamiana) leaves by Agrobacterium infiltration (EHA105) using the same method 579
as described in the dual-luciferase assay above The transiently infected leaves were 580
imaged on the third day after infiltration using a Nikon A1-SHS confocal laser 581
scanning microscope The excitation wavelength for GFP fluorescence was 488 nm 582
and fluorescence was detected at 490ndash520 nm The primers used for GFP construction 583
are listed in Supplemental Table S6 584
585
Transient overexpression in strawberry fruit 586
Transient overexpression of FaERF9 and an overexpression binary vector (pGreen II 587
0029 62-SK-FaERF9-FaMYB98) were performed in strawberry fruit using the 588
FaERF9-SK construct described above for the dual-luciferase assays and the binary 589
vector constructed according to Liu et al 2013 The transfection of fruit was carried 590
out at the G stage (Hoffmann et al 2006) The FaERF9-SK construct and binary 591
vector were individually electroporated into Agrobacterium tumefaciens GV3101 and 592
the Agrobacterium culture suspended in infiltration buffer was infiltrated into the 593
whole fruit using a syringe As a control treatment fruits were infiltrated with 594
Agrobacterium carrying an empty vector SK under the same transfection conditions 595
Fruits were left attached to the plants and harvested on the seventh day after 596
infiltration Fruits of three biological replicates were sampled for further analysis 597
598
Yeast one-hybrid assay 599
In order to identify proteins that bind to the FaQR promoter the Matchmaker Gold 600
Yeast One-hybrid Library Screening System (Clontech USA) was used The sequence 601
of the FaQR promoter was cloned into the pAbAi vector and the construct was 602
integrated into the genome of the Y1HGold yeast strain A mixture of total RNA from 603
strawberry fruit at four stages (G T IR R) was used to construct the prey cDNA 604
library (TaKaRa) The background AbAr expression of Y1HGold FaQR-pAbAi strain 605
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
22
was tested according to the system user manual and then screening for protein-DNA 606
interactions was carried out Furthermore the full length of each transcription factor 607
was separately cloned into pGADT7 AD vector to confirm the screening results The 608
relationship between FaERF9 and FaQR promoter was also examined individually 609
Primers used in this assay are listed in Supplemental Table S6 610
611
Expression and purification of FaMYB98 recombinant protein 612
A 405-bp region spanning the DNA-binding domain of FaMYB98 was amplified 613
from FaMYB98 cDNA and cloned into a pET6timesHN vector (Clontech Palo CA USA) 614
to generate the recombinant N-terminal His-tagged protein the primers used are listed 615
in Supplemental Table S6 The resulting construct was sequenced and introduced into 616
Escherichia coli strain Rosetta 2(DE3)pLysS (Novagen) Ten millilitres of the 617
overnight culture was combined with 500 mL of an LB liquid medium (100 μgmL 618
ampicillin and 34 μgmL chloramphenicol) as described (Li et al 2017) Isopropyl 619
β-D-1-thiogalactopyranoside (IPTG) was added to a final concentration of 1 mM and 620
the bacterial culture was incubated at 18degC at 150 rpm for 18 h Then the cells were 621
harvested using a centrifuge and resuspended in 1times PBS buffer (Sangon Biotech) 622
after which they were disrupted by sonication and the supernatant was purified using 623
a HisTALONTM Gravity Column (Clontech) according to the user manual The PD-10 624
Desalting column (GE Healthcare) was then used for buffer change and sample 625
clean-up of proteins according to the gravity protocol SDS-PAGE was performed and 626
the protein was visualized using Coomassie brilliant blue 627
628
Electrophoretic mobility shift assay (EMSA) 629
A Lightshift Chemiluminescent EMSA kit (Thermo) was used to perform EMSA 630
experiments according to the manufacturerrsquos instructions Single-strand 631
oligonucleotides were synthesized and biotinylated by GeneBio Biotech (Hangzhou 632
China) The details of the EMSA assay are provided in Ge et al (2017) The probes 633
used for EMSAs are listed in Supplemental Table S6 634
635
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
23
636
Yeast two-hybrid assay 637
The DUALhunter system (Dualsystems Biotech Switzerland) was used to investigate 638
the interaction between FaERF9 and FaMYB98 Full-length coding sequences of 639
FaERF9 and FaMYB98 were respectively cloned into pDHB1 bait vector and 640
pPR3-N prey vector sequences were verified and the bait plasmid was 641
co-transformed with prey plasmid into NMY51 in the combinations below 642
FaMYB98-pDHB1pPR3-N FaMYB98-pDHB1FaERF9-pPR3-N 643
FaMYB98-pDHB1pOst1-NubI FaERF9-pDHB1pPR3-N 644
FaERF9-pDHB1FaMYB98-pPR3-N and FaERF9-pDHB1pOst1-NubI (Li et al 645
2017) Transformed cells were spread onto the following plates DDO (SD 646
medium-Trp-Leu) QDO (SD medium-Trp-Leu-His-Ade) and QDO+3-AT (QDO 647
medium supplemented with 1 mM 3-amino-124-triazole) The control plasmid 648
pOst1-NubI was used to determine whether the bait was functional the pPR3-N prey 649
vector plasmid was used to test whether the bait displayed non-specific background 650
and positive interactions were indicated by the growth of yeast on QDO and 651
QDO+3-AT plates The Primers used in the DUALhunter assay are listed in 652
Supplemental Table S6 653
654
Bimolecular fluorescence complementation (BiFC) assays 655
Full-length FaERF9 and FaMYB98 respectively were cloned into sequences 656
encoding the N- and C- fragments of YFP protein (Lv et al 2014) All constructs 657
were transiently expressed in tobacco (N benthamiana) leaves by Agrobacterium 658
infiltration (EHA105) The YFP fluorescence of transfected leaves was imaged 40 h 659
after infiltration by using a Nikon A1-SHS confocal laser scanning microscope The 660
excitation wavelength for YFP was 488 nm and fluorescence was detected at 520ndash661
540 nm Primers used are listed in Supplemental Table S6 662
663
Statistics 664
A Studentrsquos two-tailed t test ( plt005 plt001 and plt0001) was used to 665
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
24
determine significant differences between two groups in this study Microsoft Excel 666
was used to perform linear regressive analysis significant differences were 667
determined by SPSS Statistics 200 and scatter plots were prepared with Origin80 668
Least significant difference (LSD) at the 5 level was calculated using Microsoft 669
Excel Figures were prepared with Origin80 (Microcal Software Inc Northampton 670
MA USA) The online tool MetaboAnalyst 36 (httpwwwmetaboanalystca) was 671
used to analyse the transcript abundance of the AP2ERF genes 672
673
Accession numbers 674
Sequence data from this article have been deposited in GenBank under the accession 675
numbers MH332903-MH333022 for AP2ERF genes in Fragaria times ananassa and 676
MH333023 for FaMYB98 GenBank numbers for FaQR and FaOMT were 677
AY1588361 (Raab et al 2006) and AF2204912 (Wein et al 2002) 678
679
Supplemental Material 680
Supplemental Figure S1 Phylogenetic analysis of FaAP2ERF and Arabidopsis 681
AP2ERF proteins 682
Supplemental Figure S2 Analysis of FaAP2ERF gene expression patterns in 683
strawberry fruit during development and ripening 684
Supplemental Figure S3 Contents of furanones in fruit of strawberry cultivars 685
Supplemental Figure S4 Relative expression of FaERF9 in FaERF9-FaMYB98- 686
and FaERF9-overexpressing fruits 687
Supplemental Figure S5 Subcellular localization of FaMYB98 688
Supplemental Figure S6 The combined activation effects of FaERF9FaMYB98 on 689
the FaOMT promoter 690
Supplemental Figure S7 Relative expression of FaOMT in 691
FaERF9-overexpressing fruits 692
Supplemental Table S1 AP2ERF superfamily genes in Fragaria times ananassa 693
Supplemental Table S2 Classification of the AP2ERF superfamily members in 694
Fragaria times ananassa 695
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
25
Supplemental Table S3 Furanone content in FaERF9-FaMYB98- and 696
FaERF9-overexpressing fruits 697
Supplemental Table S4 Primers used for reverse transcription quantitative PCR 698
(RT-qPCR) 699
Supplemental Table S5 Primers used to amplify the full-length coding sequences of 700
AP2ERF genes and FaMYB98 in strawberry (Fragaria times ananassa) 701
Supplemental Table S6 Primers used for vector construction 702
703
Acknowledgments 704
This research was supported by the National Key Research and Development 705
Program (2016YFD0400101) the Project of the Science and Technology Department 706
of Zhejiang Province (2016C04001) and the 111 Project (B17039) 707
708
Figure legends 709
Figure 1 Changes in furanone content and furanone biosynthetic genes during 710
strawberry (Fragaria times ananassa Duch cv Yuexin) fruit development and ripening 711
A Fruits were collected at four ripening stages G (green stage) T (turning stage) IR 712
(intermediate red stage) R (full red stage) B Changes in the contents of furaneol 713
(HDMF) and mesifurane (DMMF) HDMF content was calculated using a standard 714
curve of HDMF while DMMF content was calculated with an internal standard as the 715
reference C Expression levels of FaQR and FaOMT The expression levels of each 716
gene were calculated relative to corresponding values in the basal section at the R 717
stage SEs were calculated from three replicates and LSD values represent the least 718
significant differences at p = 005 719
Figure 2 Regulatory effects of FaAP2ERF on the promoter of FaQR LUCREN 720
values of the empty vector on FaQR promoter were used as the calibrator set as 1 721
and SEs were calculated from five replicates statistical significance was determined 722
by Studentrsquos two-tailed t test ( plt0001) 723
Figure 3 Expression and the subcellular localization of FaERF9 A The expression 724
levels were calculated relative to the levels in the basal section at the R stage B 725
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
26
Subcellular localization analysis was performed in tobacco leaves The tobacco used 726
in the assay was stably transformed with a specific nucleus localized red fluorescence 727
protein construct and the red fluorescence indicates the nucleus-localized signal 728
(NLS) Scale bar = 25 microm SEs were calculated from three replicates 729
Figure 4 Transient overexpression of FaERF9 in strawberry fruit A Relative 730
expression of FaQR and FaERF9 in FaERF9-OX fruit 7 days after infiltration The 731
expression was calculated relative to the average value in control (SK) fruits B 732
HDMF and DMMF content in FaERF9-OX fruit The content of both furanones 733
were quantified using the peak area of the internal standard (2-octanol) as the 734
reference SEs were calculated from three replicates Statistical significance was 735
determined by Studentrsquos two-tailed t test ( plt005 plt001 plt0001) 736
Figure 5 Scatter plots of 11 strawberry cultivars A Linear regression analysis 737
between FaERF9 expression and FaQR expression B Linear regression analysis 738
between FaERF9 expression and furanone content The relative expression was 739
normalized to that of the housekeeping gene FaRIB413 and furanone content was 740
calculated with internal standard as the reference Significant differences were 741
determined by SPSS Statistics 200 742
Figure 6 Interactions of FaERF9 and FaMYB98 with the FaQR promoter A Yeast 743
one-hybrid analysis of the interaction of FaERF9 and FaQR promoter B Yeast 744
one-hybrid analysis of the interaction of FaMYB98 and FaQR promoter C 745
Regulatory effect of FaMYB98 on the FaQR promoter Auto-activation was tested on 746
SD-Ura (synthetically defined medium without uracil) in presence of Aureobasidin A 747
(AbA) and physical interaction was determined on SD-Leu (synthetically defined 748
medium without leucine) in presence of AbA LUCREN values of the empty vector 749
on FaQR promoter were used as the calibrator set as 1 and error bars were calculated 750
from five replicates Statistical significance was determined by Studentrsquos two-tailed t 751
test ( plt005 plt001 plt0001) 752
Figure 7 Electrophoretic mobility shift assay of FaMYB98 binding to FaQR 753
promoter A The probe sequence used for EMSA and mutated nucleotides are 754
indicated with lowercase letters B Purified DNA-binding domain of FaMYB98 755
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
27
protein and biotin-labelled DNA probe were mixed and analysed on 6 native 756
polyacrylamide gels and then photographed Presence or absence of specific probes is 757
marked by the symbol + or - 758
Figure 8 The combined activation effects of FaERF9FaMYB98 on the FaQR 759
promoter LUCREN values obtained with the empty vector and FaQR promoter were 760
used as the calibrator set as 1 and error bars were calculated from five replicates 761
Figure 9 Yeast two-hybrid analysis of the protein-protein interactions between 762
FaMYB98 and FaERF9 Positive interactions were determined by the growth of 763
yeast cells on selection plates Bait with pOST acted as positive controls and bait with 764
pPR3 as negative controls DDO synthetically defined medium without tryptophan 765
and leucine QDO synthetically defined medium without tryptophan leucine 766
histidine and adenine QDO+3AT QDO medium supplemented with 1 mM 767
3-aminotriazole 768
Figure 10 BiFC analysis of the protein-protein interactions between FaMYB98 and 769
FaERF9 The pairs of fusion proteins tested were FaMYB98-YFPN+FaERF9-YFPC 770
FaERF9-YFPN+FaMYB98-YFPC FaMYB98-YFPN+FaMYB98-YFPC and 771
FaERF9-YFPN+FaERF9-YFPC The other combinations were negative controls 772
The tobacco used in the assay was stably transformed with a specific 773
nucleus-localized red fluorescence protein construct and the red fluorescence 774
indicated the nucleus-localized signal (NLS) Fluorescence of the yellow fluorescence 775
protein (YFP) visualized the interaction in vivo Scale bar = 25 microm 776
777
Literature Cited 778
779
Agarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression 780
of PgDREB2A transcription factor enhances abiotic stress tolerance and activates 781
downstream stress-responsive genes Mol Biol Rep 37 1125-1135 782
Araguumlez I Osorio S Hoffmann T Rambla JL Medina-Escobar N Granell A 783
Botella MAacute Schwab W Valpuesta V (2013) Eugenol production in achenes and 784
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
28
receptacles of strawberry fruits is catalyzed by synthases exhibiting distinct kinetics 785
Plant Physiol 163 946-958 786
Carvalho RF Carvalho SD OrsquoGrady K Folta KM (2016) Agroinfiltration of 787
strawberry fruit mdash a powerful transient expression system for gene validation Curr 788
Plant Biol 6 19-37 789
Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic 790
(Amsterdam) 210 34-40 791
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating 792
RNA from pine trees Plant Mol Biol Rep 11 113-116 793
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC 794
Clark DG (2011) PhMYB4 fine-tunes the floral volatile signature of 795
Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143 796
Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz 797
EA Taylor MG Smits-Kroon MT Schuurink RC Haring MA Giovannoni J 798
Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic 799
pathway by ectopic expression of a MYB transcription factor in tomato fruit Plant 800
Cell 23 2738-2753 801
Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan 802
XW Yang ZY (2017) Differential responses of four biosynthetic pathways of 803
aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under 804
interaction of light and temperature Food Chem 221 356-364 805
Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of 806
differentially-expressed genes during somatic embryogenesis in Fragaria times 807
ananassa Duch lsquoBenihopprsquo J Hortic Sci Biotechnol 90 671-681 808
Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 809
transcriptionally regulates chilling-induced lignification of loquat fruit via physical 810
interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136 811
Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM 812
(2004) Functional interactions between a glutamine synthetase promoter and MYB 813
proteins Plant J 39 513-526 814
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
29
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) 815
Sucrose nonfermenting1-related protein kinase26 an ortholog of open stomata1 is 816
a negative regulator of strawberry fruit development and ripening Plant Physiol 817
167 915-930 818
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene 819
expression in strawberry fruit (Fragaria times ananassa) by agroinfiltration a rapid 820
assay for gene function analysis Plant J 48 818-826 821
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of 822
selected aroma-active compounds in strawberries by headspace solid-phase 823
microextraction gas chromatography and correlation with sensory descriptive 824
analysis J Food Sci 72 S487-S496 825
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid 826
plays an important role in the regulation of strawberry fruit ripening Plant Physiol 827
157 188-199 828
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of 829
NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes BMC 830
Plant Biol 6 20 831
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN 832
(2005) MYB98 is required for pollen tube guidance and synergid cell differentiation 833
in Arabidopsis Plant Cell 17 2981-2992 834
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional 835
characterization of enone oxidoreductases from strawberry and tomato fruit J 836
Agric Food Chem 55 6705-6711 837
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You 838
J-S Rohloff J Randall SK Alsheikh M (2012) Proteomic study of 839
low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ 840
in cold tolerance Plant Physiol 159 1787-1805 841
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional 842
characterization of four APETALA2-family genes (RAP26 RAP26L DREB19 843
and DREB26) in Arabidopsis Plant Mol Biol 75 107-127 844
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
30
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon 845
J Gupta V (2013) An oxidoreductase from lsquoAlphonsorsquo mango catalyzing 846
biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494 847
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in 848
strawberries Z Lebensm-Unters Forsch 195 120-123 849
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X 850
(2015) Label-free quantitative proteomics to investigate strawberry fruit proteome 851
changes under controlled atmosphere and low temperature storage J Proteomics 852
120 44-57 853
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 854
cooperates with CitWRKY1 to participate in citric acid degradation via 855
up-regulation of CitAco3 J Exp Bot 68 3419-3426 856
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription 857
factor CitERF71 activates the terpene synthase gene CitTPS16 involved in the 858
synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938 859
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and 860
transcriptomic analysis of the AP2ERF superfamily in Vitis vinifera BMC 861
Genomics 11 719 862
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive 863
Factor (AP2ERF) transcription factors mediators of stress responses and 864
developmental programs New Phytol 199 639-649 865
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 866
interacting with EOBI negatively regulates fragrance biosynthesis in petunia 867
flowers New Phytol 215 1490-1502 868
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu 869
CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 in regulating 870
anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) 871
during anthocyanin biosynthesis Plant Cell Tissue Organ Cult 115 285-298 872
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
31
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao 873
CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphate signaling and 874
homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597 875
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC 876
Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL 877
Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor 878
regulates eugenol production in ripe strawberry fruit receptacles Plant Physiol 168 879
598-614 880
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics 881
and volatile constituents of strawberry (cv Cigaline) during maturation J Agric 882
Food Chem 52 1248-1254 883
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS 884
(2012) Ethylene-responsive transcription factors interact with promoters of ADH 885
and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 886
63 6393-6405 887
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM 888
Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-Franco A 889
Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific 890
transcription factor FaDOF2 regulates the production of eugenol in ripe fruit 891
receptacles J Exp Bot 68 4529-4543 892
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) 893
Comparison and verification of the genes involved in ethylene biosynthesis and 894
signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44 895
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the 896
ERF gene family in Arabidopsis and rice Plant Physiol 140 411-432 897
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in 898
sour cherry and strawberry and the heterologous expression of CBF1 in strawberry 899
J Am Soc Hortic Sci 127 489-494 900
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech 901
JC Ohme-Takagi M Regad F Bouzayen M (2012) Functional analysis and 902
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32
binding affinity of tomato ethylene response factors provide insight on the 903
molecular bases of plant differential responses to ethylene BMC Plant Biol 12 190 904
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) 905
Methylpentoses are possible precursors of furanones in fruits Prikl Biokhim 906
Mikrobiol 28 123-127 907
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery 908
of synergid-expressed genes encoding filiform apparatus localized proteins Plant 909
Cell 19 2557-2568 910
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria 911
vesca L compared to those of cultivated berries Fragariatimes ananassa cv Senga 912
Sengana J Agric Food Chem 27 19-22 913
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W 914
Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of the strawberry 915
flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone 916
oxidoreductase Plant Cell 18 1023-1037 917
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L 918
Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim M Broun P Zhang 919
JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription 920
factors genome-wide comparative analysis among eukaryotes Science 290 921
2105-2110 922
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the 923
formation of 25-dimethyl-4-hydroxy-3(2H)-furanone in detached ripening 924
strawberry fruits J Agric Food Chem 46 1488-1493 925
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 926
25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in 927
strawberry fruits Phytochemistry 43 155-159 928
Schwab W (1998) Application of stable isotope ratio analysis explaining the 929
bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone in plants by a biological 930
maillard reaction J Agric Food Chem 46 2266ndash2269 931
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33
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) 932
Molecules 18 6936-6951 933
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard 934
products Recent Res Dev Phytochem 1 643-673 935
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL 936
Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJ Sims CA 937
Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical 938
compositions a seasonal influence and effects on sensory perception PLoS One 9 939
e88446 940
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) 941
Identification phylogeny and transcript profiling of ERF family genes during 942
development and abiotic stress treatments in tomato Mol Genet Genomics 284 943
455-475 944
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) 945
CitAP210 activation of the terpene synthase CsTPS1 is associated with the 946
synthesis of (+)-valencene in lsquoNewhallrsquo orange J Exp Bot 67 4105-4115 947
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes 948
Dev Genes Evol 214 105-114 949
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K 950
Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the 951
key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151 952
Spitzer-Rimon B Farhi M Albo B Cnarsquoani A Ben Zvi MM Masci T Edelbaum 953
O Yu YX Shklarman E Ovadis M Vainstein A (2012) The R2R3-MYB-like 954
regulatory factor EOBI acting downstream of EOBII regulates scent production 955
by activating ODO1 and structural scent-related genes in petunia Plant Cell 24 956
5089-5105 957
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp 958
Bot 68 4407-4409 959
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla 960
JF Amaya I Giavalisco P Fernie AR Botella MA Valpuesta V (2015) Central 961
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34
role of FaGAMYB in the transition of the strawberry receptacle from development 962
to ripening New Phytol 208 482-496 963
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 964
regulates fragrance biosynthesis in petunia flowers Plant Cell 17 1612-1624 965
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS 966
(2018) The potassium channel FaTPK1 plays a critical role in fruit quality 967
formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748 968
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) 969
Isolation cloning and expression of a multifunctional O-methyltransferase capable 970
of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma 971
compounds in strawberry fruits Plant J 31 755-765 972
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor 973
types their evolutionary origin and species distribution In A handbook of 974
transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular 975
Biochemistry 52 25-73 976
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of 977
odor (Buettner A Ed) Springer Cham 9-10 978
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS 979
(2014) Isolation classification and transcription profiles of the AP2ERF 980
transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271 981
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in 982
regulation of fruit quality Crit Rev Plant Sci 35 120-130 983
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ 984
Zhang SL Wu J (2017) Map-based cloning of the pear gene MYB114 identifies an 985
interaction with other transcription factors to coordinately regulate fruit 986
anthocyanin biosynthesis Plant J 92 437-451 987
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes 988
involved in regulating fruit ripening Plant Physiol 153 1280-1292 989
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35
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) 990
Expression of ethylene response genes during persimmon fruit astringency removal 991
Planta 235 895-906 992
Zabetakis I Gramshaw JW Robinson DS (1999) 993
25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis and 994
biosynthesis-a review Food Chem 65 139-151 995
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci 996
Food Agric 74 421-434 997
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 998
an AP2ERF gene is a novel regulator of fruit lignification induced by chilling 999
injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1000
1325-1334 1001
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation 1002
classification and transcription profiles of the Ethylene Response Factors (ERFs) in 1003
ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215 1004
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML 1005
(2012) Genome-wide analysis of the AP2ERF superfamily in peach (Prunus 1006
persica) Genet Mol Res 11 4788-4809 1007
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and 1008
expression analysis of a CRTDRE-binding factor gene FaCBF1 from Fragaria times 1009
ananassa Acta Hortic 41 240-248 1010
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The 1011
Arabidopsis AP2ERF transcription factor RAP26 participates in ABA salt and 1012
osmotic stress responses Gene 457 1-12 1013
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B 1014
Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) Genome-wide 1015
analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic 1016
(Amsterdam) 123 73-81 1017
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF 1018
Valpuesta V Botella MA Granell A Amaya I (2012) Genetic analysis of 1019
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
36
strawberry fruit aroma and identification of O-methyltransferase FaOMT as the 1020
locus controlling natural variation in mesifurane content Plant Physiol 159 1021
851-870 1022
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Parsed CitationsAgarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression of PgDREB2A transcription factor enhances abioticstress tolerance and activates downstream stress-responsive genes Mol Biol Rep 37 1125-1135
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Araguumlez I Osorio S Hoffmann T Rambla JL Medina-Escobar N Granell A Botella MAacute Schwab W Valpuesta V (2013) Eugenolproduction in achenes and receptacles of strawberry fruits is catalyzed by synthases exhibiting distinct kinetics Plant Physiol 163 946-958
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Carvalho RF Carvalho SD OGrady K Folta KM (2016) Agroinfiltration of strawberry fruit - a powerful transient expression system forgene validation Curr Plant Biol 6 19-37
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic (Amsterdam) 210 34-40Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating RNA from pine trees Plant Mol Biol Rep 11 113-116Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC Clark DG (2011) PhMYB4 fine-tunes the floral volatilesignature of Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz EA Taylor MG Smits-Kroon MT Schuurink RC HaringMA Giovannoni J Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic pathway by ectopic expression of aMYB transcription factor in tomato fruit Plant Cell 23 2738-2753
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan XW Yang ZY (2017) Differential responses of fourbiosynthetic pathways of aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under interaction of light andtemperature Food Chem 221 356-364
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of differentially-expressed genes during somatic embryogenesis inFragaria times ananassa Duch Benihopp J Hortic Sci Biotechnol 90 671-681
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 transcriptionally regulates chilling-induced lignification ofloquat fruit via physical interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM (2004) Functional interactions between a glutaminesynthetase promoter and MYB proteins Plant J 39 513-526
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) Sucrose nonfermenting1-related protein kinase26 anortholog of open stomata1 is a negative regulator of strawberry fruit development and ripening Plant Physiol 167 915-930
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene expression in strawberry fruit (Fragaria times ananassa) byagroinfiltration a rapid assay for gene function analysis Plant J 48 818-826
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of selected aroma-active compounds in strawberries byheadspace solid-phase microextraction gas chromatography and correlation with sensory descriptive analysis J Food Sci 72 S487-S496
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid plays an important role in the regulation of strawberry fruitripening Plant Physiol 157 188-199
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of NaCl-stressed Arabidopsis roots reveals novel classes ofresponsive genes BMC Plant Biol 6 20
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN (2005) MYB98 is required for pollen tube guidance andsynergid cell differentiation in Arabidopsis Plant Cell 17 2981-2992
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional characterization of enone oxidoreductases from strawberry andtomato fruit J Agric Food Chem 55 6705-6711
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You J-S Rohloff J Randall SK Alsheikh M (2012) Proteomicstudy of low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ in cold tolerance Plant Physiol 159 1787-1805
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional characterization of four APETALA2-family genes (RAP26 RAP26LDREB19 and DREB26) in Arabidopsis Plant Mol Biol 75 107-127
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon J Gupta V (2013) An oxidoreductase from Alphonsomango catalyzing biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in strawberries Z Lebensm-Unters Forsch 195 120-123Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X (2015) Label-free quantitative proteomics to investigatestrawberry fruit proteome changes under controlled atmosphere and low temperature storage J Proteomics 120 44-57
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 cooperates with CitWRKY1 to participate in citric aciddegradation via up-regulation of CitAco3 J Exp Bot 68 3419-3426
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription factor CitERF71 activates the terpene synthase geneCitTPS16 involved in the synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and transcriptomic analysis of the AP2ERF superfamily inVitis vinifera BMC Genomics 11 719
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive Factor (AP2ERF) transcription factors mediators of stressresponses and developmental programs New Phytol 199 639-649
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 interacting with EOBI negatively regulates fragrancebiosynthesis in petunia flowers New Phytol 215 1490-1502
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 inregulating anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) during anthocyanin biosynthesis Plant CellTissue Organ Cult 115 285-298
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title wwwplantphysiolorgon February 25 2020 - Published by Downloaded from
Copyright copy 2018 American Society of Plant Biologists All rights reserved
Google Scholar Author Only Title Only Author and Title
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphatesignaling and homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597
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Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor regulates eugenol production in ripe strawberry fruitreceptacles Plant Physiol 168 598-614
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Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics and volatile constituents of strawberry (cv Cigaline)during maturation J Agric Food Chem 52 1248-1254
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Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS (2012) Ethylene-responsive transcription factors interact withpromoters of ADH and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 63 6393-6405
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-FrancoA Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific transcription factor FaDOF2 regulates the production ofeugenol in ripe fruit receptacles J Exp Bot 68 4529-4543
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Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) Comparison and verification of the genes involved in ethylenebiosynthesis and signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44
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Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice Plant Physiol140 411-432
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Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in sour cherry and strawberry and the heterologousexpression of CBF1 in strawberry J Am Soc Hortic Sci 127 489-494
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Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech JC Ohme-Takagi M Regad F Bouzayen M (2012)Functional analysis and binding affinity of tomato ethylene response factors provide insight on the molecular bases of plant differentialresponses to ethylene BMC Plant Biol 12 190
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Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery of synergid-expressed genes encoding filiformapparatus localized proteins Plant Cell 19 2557-2568
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Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria vesca L compared to those of cultivated berriesFragariatimes ananassa cv Senga Sengana J Agric Food Chem 27 19-22
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Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of thestrawberry flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone oxidoreductase Plant Cell 18 1023-1037
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Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the formation of 25-dimethyl-4-hydroxy-3(2H)-furanonein detached ripening strawberry fruits J Agric Food Chem 46 1488-1493
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Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in strawberry fruits Phytochemistry 43 155-159
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Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes Dev Genes Evol 214 105-114Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
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Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla JF Amaya I Giavalisco P Fernie AR Botella MAValpuesta V (2015) Central role of FaGAMYB in the transition of the strawberry receptacle from development to ripening New Phytol208 482-496
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methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma compounds in strawberry fruitsPlant J 31 755-765
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Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) Expression of ethylene response genes during persimmonfruit astringency removal Planta 235 895-906
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Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 an AP2ERF gene is a novel regulator of fruit lignificationinduced by chilling injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1325-1334
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Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Genome-wide analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic (Amsterdam) 123 73-81Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF Valpuesta V Botella MA Granell A Amaya I (2012) Geneticanalysis of strawberry fruit aroma and identification of O-methyltransferase FaOMT as the locus controlling natural variation inmesifurane content Plant Physiol 159 851-870
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wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
17
replicates were sampled frozen in liquid nitrogen and stored at -80deg C for further use 456
457
Tobacco plants (Nicotiana benthamiana) used for dual-luciferase assays and 458
subcellular localization analysis in this study were grown in a growth chamber with a 459
lightdark cycle of 16 h8 h at 24degC 460
461
Detection of DMMF and HDMF 462
Automated HS-SPME-GC-MS was performed to detect both furanones in lsquoYuexinrsquo 463
strawberry fruit (Zorrilla-Fontanesi et al 2012) Samples were ground into a powder 464
under liquid nitrogen for analysis 465
466
For the detection of DMMF (Figure 1) 05 g (fresh weight) of each sample was 467
weighed in the vial to which was added 1 mL of EDTA solution (100 mM pH 75) 1 468
mL of CaCl2 solution (mv = 20) and 20 microL of 2-octanol as the internal standard 469
(007 μgμL) The mixture was homogenized and the vial closed and placed on the 470
sample tray for analysis by CombiPAL autosampler (CTC Analytic CA USA) The 471
fruit volatiles were sampled by headspace solid-phase microextraction with a 65-μm 472
polydimethylsiloxane-divinylbenzene fibre (PDMS-DVB) Initially vials were 473
pre-incubated at 50degC for 10 min under continuous agitation (500 rpm) then volatiles 474
were extracted for 30 min at the same temperature and agitation speed After that the 475
fibre was desorbed in the GC injection port for 5 min in splitless mode The 7890A 476
GC chromatograph was equipped with a DB-5ms column (60 m times 250 μm times 1 μm 477
JampW Scientific Folsom CA USA) with helium as the carrier gas at a constant flow 478
of 12 mLmin The GC was programmed at an initial temperature of 35degC for 2 min 479
with a ramp of 5degC min up to 250degC and held for 5 min The injection port interface 480
and MS source temperatures were 250degC 260degC and 230degC respectively The 481
ionization potential was set at 70 eV recorded by a 5975B mass spectrometer (Agilent 482
Technologies JampW Scientific Folsom CA USA) and the scanning speed was 7 483
scanss The same method was used to analyse HDMF and DMMF in fruits from 484
different cultivars (Supplemental Figure S3) except for the sample preparation 485
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
18
procedure (Araguumlez et al 2013) briefly 05 g (fresh weight) of powdered fruit was 486
incubated at 30degC in a water bath for 5 min then 2 mL of NaCl (mv = 20) and 20 487
microL of 2-octanol as the internal standard (007 μgμL) were added and homogenized 488
489
For the detection of HDMF (Figure 1) and both furanones (Figure 4 and Supplemental 490
Table S3) a liquid-injection system equipped with CTC Pal ALS was used One gram 491
(fresh weight) of powdered fruit and 2 mL of NaCl (mv = 20) were homogenized in 492
a 10-mL tube and 300 μL of CH2Cl2 and 20 microL of 2-octanol (0766 μgμL) as the 493
internal standard were added to extract the volatiles the mixture was then 494
homogenized again The tubes were stored at room temperature for 20 min and 495
centrifuged at 12000 rpm for 5 min The subnatant was pipetted into a clean 15-mL 496
tube in which 20 mg of anhydrous sodium sulphate was added the tube was left 497
without shaking for half an hour Then 150 μL of the solution was transferred into a 498
GC vial and placed on the sample tray as described above Each sample (1 μL) was 499
injected using the autosampler and the analysis was accomplished by a 7890A 500
GC-MS system (Agilent Technologies JampW Scientific Folsom CA USA) equipped 501
with a DB-WAX column (30 m times 025 mm times 025 μm JampW) Helium (12 mLmin) 502
was used as a carrier gas The injection port (splitless injection mode) interface and 503
MS source temperatures were as described above The oven temperature was set at 504
60degC for 4 min then increased to 180degC at a rate of 4degCmin and maintained for 30 505
min DMMF was identified by comparison of electron ionization mass spectra and 506
retention time data with the data from the NISTEPANIH mass spectral library 507
(NIST-08 and Flavor) HDMF (Figure 1) was identified and qualified by comparison 508
with injected standard (Sigma) The quantitative analysis of both furanones (Figure 4 509
Supplemental Table S3 and Supplemental Figure S3) was determined using the peak 510
area of the internal standard as a reference based on total ion chromatogram (TIC) 511
512
RNA isolation and Reverse Transcription Quantitative PCR (RT-qPCR) 513
Total RNA from strawberry samples was isolated in this study using the CTAB 514
method (Chang et al 1993) Genomic DNA contamination was eliminated by 515
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
19
TURBO Dnase (Ambion) 1 μg of RNA was used to obtain cDNA using an IScriptTM 516
cDNA Synthesis Kit (Bio-Rad) The synthesized cDNA was diluted with water (120) 517
and 2 μL of diluted cDNA was used as the template for RT-qPCR Reactions were 518
performed in a total volume of 20 μL consisting of 10 μL of SYBR PCR supermix 519
(Bio-Rad) 1 μL of each primer (10 μM) 6 μL of DEPC-H2O and 2 μL of diluted 520
cDNA on CFX96 instrument (Bio-Rad) (Yin et al 2012) The oligonucleotide 521
primers for RT-qPCR analysis of genes including the AP2ERF FaQR and FaOMT 522
were designed according to the coding sequences of genes and the specificity was 523
verified before use (Min et al 2012) NCBIPrimer-BLAST was applied to design the 524
primers Relative expression levels were normalized to that of an internal controlmdashthe 525
interspacer 26S-18S strawberry RNA housekeeping gene FaRIB413 526
(Zorrilla-Fontanesi et al 2012) To investigate the differential expression of genes 527
during fruit development and ripening stages relative expression of each gene at the 528
R stage in the basal fruit section was set as 1 using the 2minus∆∆119862119879 method For transient 529
overexpression assay relative expression of control fruits with an empty vector (SK) 530
was set as 1 The primers used in RT-qPCR are listed in Supplemental Table S4 531
532
Gene isolation and analysis 533
Multiple database searches were performed to identify members of the strawberry 534
(Fragaria times ananassa) AP2ERF superfamily in the published strawberry databases 535
and annotations of Fragaria times ananassa and Fragaria times vesca by using the 536
AP2ERF DNA binding domain as a query sequence and 120 genes were identified 537
with AP2ERF domain(s) Based on the BLAST result primers (listed in 538
Supplemental Table S5) were used to amplify the coding full-length cDNAs of 539
AP2ERF genes The deduced amino acid sequences of AP2ERF proteins in 540
Arabidopsis thaliana used for construction of a phylogenetic tree were obtained from 541
the Arabidopsis Information Resource (TAIR) Alignment of the proteins was 542
performed using the neighbour-joining method in ClustalX (v181) and the 543
phylogenetic tree was constructed using FigTree (v131) 544
545
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
20
FaMYB98 was obtained by yeast one-hybrid screening sequencing and the full-length 546
sequences were predicted by BLAST Primers were designed (listed in Supplemental 547
Table S5) to amplify the full-length coding sequence 548
549
The promoter of FaQR was cloned by Genome Walking as previously described (Yin 550
et al 2010) and conserved cis-element motifs in the promoter were manually 551
searched 552
553
Conserved domains within the FaAP2ERF proteins and FaMYB98 were analysed by 554
CD-search (httpswwwncbinlmnihgovStructurecddwrpsbcgi) and cellular 555
locations of proteins including FaERF9 and FaMYB98 were predicted with the 556
WoLF PSORT program (httpswwwgenscriptcomwolf-psorthtml) 557
558
Dual-Luciferase Assays 559
In accordance with a previous protocol (Yin et al 2010) the full-length cDNAs of 560
FaAP2ERF or FaMYB98 transcription factors were cloned into pGreen II 0029 561
62-SK vector and the promoter of FaQR was cloned into pGreen II 0800-LUC vector 562
A luciferase gene from Renillia (REN) driven by a 35S promoter in the LUC vector 563
acted as a positive control The above constructs were transiently expressed in 564
Nicotiana benthamiana leaves by Agrobacterium-mediated infiltration (strain 565
GV3101) and the activity of the TFs on the promoter was measured on the third day 566
after infiltration indicated by the ratio of enzyme activities of firefly luciferase (LUC) 567
and renilla luciferase (REN) using a Modulus Luminometer (Promega Madison WI 568
USA) To determine the activity of a specific transcription factor towards the 569
promoter we mixed the Agrobacterium culture with 1 mL of TF and 100 μL of 570
promoter and the LUCREN value of the empty vector SK on the promoter was set as 571
1 as a calibrator To test the combined effect of two transcription factors on the 572
promoter to the Agrobacterium culture mixture we added 05 mL of each TF and 100 573
μL of promoter the effect of the mixtures that contained each transcription factor (05 574
mL) and empty vector SK (05 mL) was also tested on the promoter as a control 575
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
21
576
Subcellular localization analysis 577
35S-FaERF9-GFP and 35S-FaMYB98-GFP were transiently expressed in tobacco (N 578
benthamiana) leaves by Agrobacterium infiltration (EHA105) using the same method 579
as described in the dual-luciferase assay above The transiently infected leaves were 580
imaged on the third day after infiltration using a Nikon A1-SHS confocal laser 581
scanning microscope The excitation wavelength for GFP fluorescence was 488 nm 582
and fluorescence was detected at 490ndash520 nm The primers used for GFP construction 583
are listed in Supplemental Table S6 584
585
Transient overexpression in strawberry fruit 586
Transient overexpression of FaERF9 and an overexpression binary vector (pGreen II 587
0029 62-SK-FaERF9-FaMYB98) were performed in strawberry fruit using the 588
FaERF9-SK construct described above for the dual-luciferase assays and the binary 589
vector constructed according to Liu et al 2013 The transfection of fruit was carried 590
out at the G stage (Hoffmann et al 2006) The FaERF9-SK construct and binary 591
vector were individually electroporated into Agrobacterium tumefaciens GV3101 and 592
the Agrobacterium culture suspended in infiltration buffer was infiltrated into the 593
whole fruit using a syringe As a control treatment fruits were infiltrated with 594
Agrobacterium carrying an empty vector SK under the same transfection conditions 595
Fruits were left attached to the plants and harvested on the seventh day after 596
infiltration Fruits of three biological replicates were sampled for further analysis 597
598
Yeast one-hybrid assay 599
In order to identify proteins that bind to the FaQR promoter the Matchmaker Gold 600
Yeast One-hybrid Library Screening System (Clontech USA) was used The sequence 601
of the FaQR promoter was cloned into the pAbAi vector and the construct was 602
integrated into the genome of the Y1HGold yeast strain A mixture of total RNA from 603
strawberry fruit at four stages (G T IR R) was used to construct the prey cDNA 604
library (TaKaRa) The background AbAr expression of Y1HGold FaQR-pAbAi strain 605
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
22
was tested according to the system user manual and then screening for protein-DNA 606
interactions was carried out Furthermore the full length of each transcription factor 607
was separately cloned into pGADT7 AD vector to confirm the screening results The 608
relationship between FaERF9 and FaQR promoter was also examined individually 609
Primers used in this assay are listed in Supplemental Table S6 610
611
Expression and purification of FaMYB98 recombinant protein 612
A 405-bp region spanning the DNA-binding domain of FaMYB98 was amplified 613
from FaMYB98 cDNA and cloned into a pET6timesHN vector (Clontech Palo CA USA) 614
to generate the recombinant N-terminal His-tagged protein the primers used are listed 615
in Supplemental Table S6 The resulting construct was sequenced and introduced into 616
Escherichia coli strain Rosetta 2(DE3)pLysS (Novagen) Ten millilitres of the 617
overnight culture was combined with 500 mL of an LB liquid medium (100 μgmL 618
ampicillin and 34 μgmL chloramphenicol) as described (Li et al 2017) Isopropyl 619
β-D-1-thiogalactopyranoside (IPTG) was added to a final concentration of 1 mM and 620
the bacterial culture was incubated at 18degC at 150 rpm for 18 h Then the cells were 621
harvested using a centrifuge and resuspended in 1times PBS buffer (Sangon Biotech) 622
after which they were disrupted by sonication and the supernatant was purified using 623
a HisTALONTM Gravity Column (Clontech) according to the user manual The PD-10 624
Desalting column (GE Healthcare) was then used for buffer change and sample 625
clean-up of proteins according to the gravity protocol SDS-PAGE was performed and 626
the protein was visualized using Coomassie brilliant blue 627
628
Electrophoretic mobility shift assay (EMSA) 629
A Lightshift Chemiluminescent EMSA kit (Thermo) was used to perform EMSA 630
experiments according to the manufacturerrsquos instructions Single-strand 631
oligonucleotides were synthesized and biotinylated by GeneBio Biotech (Hangzhou 632
China) The details of the EMSA assay are provided in Ge et al (2017) The probes 633
used for EMSAs are listed in Supplemental Table S6 634
635
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
23
636
Yeast two-hybrid assay 637
The DUALhunter system (Dualsystems Biotech Switzerland) was used to investigate 638
the interaction between FaERF9 and FaMYB98 Full-length coding sequences of 639
FaERF9 and FaMYB98 were respectively cloned into pDHB1 bait vector and 640
pPR3-N prey vector sequences were verified and the bait plasmid was 641
co-transformed with prey plasmid into NMY51 in the combinations below 642
FaMYB98-pDHB1pPR3-N FaMYB98-pDHB1FaERF9-pPR3-N 643
FaMYB98-pDHB1pOst1-NubI FaERF9-pDHB1pPR3-N 644
FaERF9-pDHB1FaMYB98-pPR3-N and FaERF9-pDHB1pOst1-NubI (Li et al 645
2017) Transformed cells were spread onto the following plates DDO (SD 646
medium-Trp-Leu) QDO (SD medium-Trp-Leu-His-Ade) and QDO+3-AT (QDO 647
medium supplemented with 1 mM 3-amino-124-triazole) The control plasmid 648
pOst1-NubI was used to determine whether the bait was functional the pPR3-N prey 649
vector plasmid was used to test whether the bait displayed non-specific background 650
and positive interactions were indicated by the growth of yeast on QDO and 651
QDO+3-AT plates The Primers used in the DUALhunter assay are listed in 652
Supplemental Table S6 653
654
Bimolecular fluorescence complementation (BiFC) assays 655
Full-length FaERF9 and FaMYB98 respectively were cloned into sequences 656
encoding the N- and C- fragments of YFP protein (Lv et al 2014) All constructs 657
were transiently expressed in tobacco (N benthamiana) leaves by Agrobacterium 658
infiltration (EHA105) The YFP fluorescence of transfected leaves was imaged 40 h 659
after infiltration by using a Nikon A1-SHS confocal laser scanning microscope The 660
excitation wavelength for YFP was 488 nm and fluorescence was detected at 520ndash661
540 nm Primers used are listed in Supplemental Table S6 662
663
Statistics 664
A Studentrsquos two-tailed t test ( plt005 plt001 and plt0001) was used to 665
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
24
determine significant differences between two groups in this study Microsoft Excel 666
was used to perform linear regressive analysis significant differences were 667
determined by SPSS Statistics 200 and scatter plots were prepared with Origin80 668
Least significant difference (LSD) at the 5 level was calculated using Microsoft 669
Excel Figures were prepared with Origin80 (Microcal Software Inc Northampton 670
MA USA) The online tool MetaboAnalyst 36 (httpwwwmetaboanalystca) was 671
used to analyse the transcript abundance of the AP2ERF genes 672
673
Accession numbers 674
Sequence data from this article have been deposited in GenBank under the accession 675
numbers MH332903-MH333022 for AP2ERF genes in Fragaria times ananassa and 676
MH333023 for FaMYB98 GenBank numbers for FaQR and FaOMT were 677
AY1588361 (Raab et al 2006) and AF2204912 (Wein et al 2002) 678
679
Supplemental Material 680
Supplemental Figure S1 Phylogenetic analysis of FaAP2ERF and Arabidopsis 681
AP2ERF proteins 682
Supplemental Figure S2 Analysis of FaAP2ERF gene expression patterns in 683
strawberry fruit during development and ripening 684
Supplemental Figure S3 Contents of furanones in fruit of strawberry cultivars 685
Supplemental Figure S4 Relative expression of FaERF9 in FaERF9-FaMYB98- 686
and FaERF9-overexpressing fruits 687
Supplemental Figure S5 Subcellular localization of FaMYB98 688
Supplemental Figure S6 The combined activation effects of FaERF9FaMYB98 on 689
the FaOMT promoter 690
Supplemental Figure S7 Relative expression of FaOMT in 691
FaERF9-overexpressing fruits 692
Supplemental Table S1 AP2ERF superfamily genes in Fragaria times ananassa 693
Supplemental Table S2 Classification of the AP2ERF superfamily members in 694
Fragaria times ananassa 695
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
25
Supplemental Table S3 Furanone content in FaERF9-FaMYB98- and 696
FaERF9-overexpressing fruits 697
Supplemental Table S4 Primers used for reverse transcription quantitative PCR 698
(RT-qPCR) 699
Supplemental Table S5 Primers used to amplify the full-length coding sequences of 700
AP2ERF genes and FaMYB98 in strawberry (Fragaria times ananassa) 701
Supplemental Table S6 Primers used for vector construction 702
703
Acknowledgments 704
This research was supported by the National Key Research and Development 705
Program (2016YFD0400101) the Project of the Science and Technology Department 706
of Zhejiang Province (2016C04001) and the 111 Project (B17039) 707
708
Figure legends 709
Figure 1 Changes in furanone content and furanone biosynthetic genes during 710
strawberry (Fragaria times ananassa Duch cv Yuexin) fruit development and ripening 711
A Fruits were collected at four ripening stages G (green stage) T (turning stage) IR 712
(intermediate red stage) R (full red stage) B Changes in the contents of furaneol 713
(HDMF) and mesifurane (DMMF) HDMF content was calculated using a standard 714
curve of HDMF while DMMF content was calculated with an internal standard as the 715
reference C Expression levels of FaQR and FaOMT The expression levels of each 716
gene were calculated relative to corresponding values in the basal section at the R 717
stage SEs were calculated from three replicates and LSD values represent the least 718
significant differences at p = 005 719
Figure 2 Regulatory effects of FaAP2ERF on the promoter of FaQR LUCREN 720
values of the empty vector on FaQR promoter were used as the calibrator set as 1 721
and SEs were calculated from five replicates statistical significance was determined 722
by Studentrsquos two-tailed t test ( plt0001) 723
Figure 3 Expression and the subcellular localization of FaERF9 A The expression 724
levels were calculated relative to the levels in the basal section at the R stage B 725
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
26
Subcellular localization analysis was performed in tobacco leaves The tobacco used 726
in the assay was stably transformed with a specific nucleus localized red fluorescence 727
protein construct and the red fluorescence indicates the nucleus-localized signal 728
(NLS) Scale bar = 25 microm SEs were calculated from three replicates 729
Figure 4 Transient overexpression of FaERF9 in strawberry fruit A Relative 730
expression of FaQR and FaERF9 in FaERF9-OX fruit 7 days after infiltration The 731
expression was calculated relative to the average value in control (SK) fruits B 732
HDMF and DMMF content in FaERF9-OX fruit The content of both furanones 733
were quantified using the peak area of the internal standard (2-octanol) as the 734
reference SEs were calculated from three replicates Statistical significance was 735
determined by Studentrsquos two-tailed t test ( plt005 plt001 plt0001) 736
Figure 5 Scatter plots of 11 strawberry cultivars A Linear regression analysis 737
between FaERF9 expression and FaQR expression B Linear regression analysis 738
between FaERF9 expression and furanone content The relative expression was 739
normalized to that of the housekeeping gene FaRIB413 and furanone content was 740
calculated with internal standard as the reference Significant differences were 741
determined by SPSS Statistics 200 742
Figure 6 Interactions of FaERF9 and FaMYB98 with the FaQR promoter A Yeast 743
one-hybrid analysis of the interaction of FaERF9 and FaQR promoter B Yeast 744
one-hybrid analysis of the interaction of FaMYB98 and FaQR promoter C 745
Regulatory effect of FaMYB98 on the FaQR promoter Auto-activation was tested on 746
SD-Ura (synthetically defined medium without uracil) in presence of Aureobasidin A 747
(AbA) and physical interaction was determined on SD-Leu (synthetically defined 748
medium without leucine) in presence of AbA LUCREN values of the empty vector 749
on FaQR promoter were used as the calibrator set as 1 and error bars were calculated 750
from five replicates Statistical significance was determined by Studentrsquos two-tailed t 751
test ( plt005 plt001 plt0001) 752
Figure 7 Electrophoretic mobility shift assay of FaMYB98 binding to FaQR 753
promoter A The probe sequence used for EMSA and mutated nucleotides are 754
indicated with lowercase letters B Purified DNA-binding domain of FaMYB98 755
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
27
protein and biotin-labelled DNA probe were mixed and analysed on 6 native 756
polyacrylamide gels and then photographed Presence or absence of specific probes is 757
marked by the symbol + or - 758
Figure 8 The combined activation effects of FaERF9FaMYB98 on the FaQR 759
promoter LUCREN values obtained with the empty vector and FaQR promoter were 760
used as the calibrator set as 1 and error bars were calculated from five replicates 761
Figure 9 Yeast two-hybrid analysis of the protein-protein interactions between 762
FaMYB98 and FaERF9 Positive interactions were determined by the growth of 763
yeast cells on selection plates Bait with pOST acted as positive controls and bait with 764
pPR3 as negative controls DDO synthetically defined medium without tryptophan 765
and leucine QDO synthetically defined medium without tryptophan leucine 766
histidine and adenine QDO+3AT QDO medium supplemented with 1 mM 767
3-aminotriazole 768
Figure 10 BiFC analysis of the protein-protein interactions between FaMYB98 and 769
FaERF9 The pairs of fusion proteins tested were FaMYB98-YFPN+FaERF9-YFPC 770
FaERF9-YFPN+FaMYB98-YFPC FaMYB98-YFPN+FaMYB98-YFPC and 771
FaERF9-YFPN+FaERF9-YFPC The other combinations were negative controls 772
The tobacco used in the assay was stably transformed with a specific 773
nucleus-localized red fluorescence protein construct and the red fluorescence 774
indicated the nucleus-localized signal (NLS) Fluorescence of the yellow fluorescence 775
protein (YFP) visualized the interaction in vivo Scale bar = 25 microm 776
777
Literature Cited 778
779
Agarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression 780
of PgDREB2A transcription factor enhances abiotic stress tolerance and activates 781
downstream stress-responsive genes Mol Biol Rep 37 1125-1135 782
Araguumlez I Osorio S Hoffmann T Rambla JL Medina-Escobar N Granell A 783
Botella MAacute Schwab W Valpuesta V (2013) Eugenol production in achenes and 784
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
28
receptacles of strawberry fruits is catalyzed by synthases exhibiting distinct kinetics 785
Plant Physiol 163 946-958 786
Carvalho RF Carvalho SD OrsquoGrady K Folta KM (2016) Agroinfiltration of 787
strawberry fruit mdash a powerful transient expression system for gene validation Curr 788
Plant Biol 6 19-37 789
Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic 790
(Amsterdam) 210 34-40 791
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating 792
RNA from pine trees Plant Mol Biol Rep 11 113-116 793
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC 794
Clark DG (2011) PhMYB4 fine-tunes the floral volatile signature of 795
Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143 796
Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz 797
EA Taylor MG Smits-Kroon MT Schuurink RC Haring MA Giovannoni J 798
Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic 799
pathway by ectopic expression of a MYB transcription factor in tomato fruit Plant 800
Cell 23 2738-2753 801
Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan 802
XW Yang ZY (2017) Differential responses of four biosynthetic pathways of 803
aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under 804
interaction of light and temperature Food Chem 221 356-364 805
Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of 806
differentially-expressed genes during somatic embryogenesis in Fragaria times 807
ananassa Duch lsquoBenihopprsquo J Hortic Sci Biotechnol 90 671-681 808
Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 809
transcriptionally regulates chilling-induced lignification of loquat fruit via physical 810
interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136 811
Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM 812
(2004) Functional interactions between a glutamine synthetase promoter and MYB 813
proteins Plant J 39 513-526 814
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29
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) 815
Sucrose nonfermenting1-related protein kinase26 an ortholog of open stomata1 is 816
a negative regulator of strawberry fruit development and ripening Plant Physiol 817
167 915-930 818
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene 819
expression in strawberry fruit (Fragaria times ananassa) by agroinfiltration a rapid 820
assay for gene function analysis Plant J 48 818-826 821
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of 822
selected aroma-active compounds in strawberries by headspace solid-phase 823
microextraction gas chromatography and correlation with sensory descriptive 824
analysis J Food Sci 72 S487-S496 825
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid 826
plays an important role in the regulation of strawberry fruit ripening Plant Physiol 827
157 188-199 828
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of 829
NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes BMC 830
Plant Biol 6 20 831
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN 832
(2005) MYB98 is required for pollen tube guidance and synergid cell differentiation 833
in Arabidopsis Plant Cell 17 2981-2992 834
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional 835
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Agric Food Chem 55 6705-6711 837
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You 838
J-S Rohloff J Randall SK Alsheikh M (2012) Proteomic study of 839
low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ 840
in cold tolerance Plant Physiol 159 1787-1805 841
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional 842
characterization of four APETALA2-family genes (RAP26 RAP26L DREB19 843
and DREB26) in Arabidopsis Plant Mol Biol 75 107-127 844
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30
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon 845
J Gupta V (2013) An oxidoreductase from lsquoAlphonsorsquo mango catalyzing 846
biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494 847
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in 848
strawberries Z Lebensm-Unters Forsch 195 120-123 849
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X 850
(2015) Label-free quantitative proteomics to investigate strawberry fruit proteome 851
changes under controlled atmosphere and low temperature storage J Proteomics 852
120 44-57 853
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 854
cooperates with CitWRKY1 to participate in citric acid degradation via 855
up-regulation of CitAco3 J Exp Bot 68 3419-3426 856
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription 857
factor CitERF71 activates the terpene synthase gene CitTPS16 involved in the 858
synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938 859
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and 860
transcriptomic analysis of the AP2ERF superfamily in Vitis vinifera BMC 861
Genomics 11 719 862
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive 863
Factor (AP2ERF) transcription factors mediators of stress responses and 864
developmental programs New Phytol 199 639-649 865
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 866
interacting with EOBI negatively regulates fragrance biosynthesis in petunia 867
flowers New Phytol 215 1490-1502 868
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu 869
CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 in regulating 870
anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) 871
during anthocyanin biosynthesis Plant Cell Tissue Organ Cult 115 285-298 872
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31
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao 873
CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphate signaling and 874
homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597 875
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC 876
Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL 877
Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor 878
regulates eugenol production in ripe strawberry fruit receptacles Plant Physiol 168 879
598-614 880
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics 881
and volatile constituents of strawberry (cv Cigaline) during maturation J Agric 882
Food Chem 52 1248-1254 883
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS 884
(2012) Ethylene-responsive transcription factors interact with promoters of ADH 885
and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 886
63 6393-6405 887
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM 888
Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-Franco A 889
Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific 890
transcription factor FaDOF2 regulates the production of eugenol in ripe fruit 891
receptacles J Exp Bot 68 4529-4543 892
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) 893
Comparison and verification of the genes involved in ethylene biosynthesis and 894
signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44 895
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the 896
ERF gene family in Arabidopsis and rice Plant Physiol 140 411-432 897
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in 898
sour cherry and strawberry and the heterologous expression of CBF1 in strawberry 899
J Am Soc Hortic Sci 127 489-494 900
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech 901
JC Ohme-Takagi M Regad F Bouzayen M (2012) Functional analysis and 902
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32
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molecular bases of plant differential responses to ethylene BMC Plant Biol 12 190 904
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) 905
Methylpentoses are possible precursors of furanones in fruits Prikl Biokhim 906
Mikrobiol 28 123-127 907
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery 908
of synergid-expressed genes encoding filiform apparatus localized proteins Plant 909
Cell 19 2557-2568 910
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria 911
vesca L compared to those of cultivated berries Fragariatimes ananassa cv Senga 912
Sengana J Agric Food Chem 27 19-22 913
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W 914
Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of the strawberry 915
flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone 916
oxidoreductase Plant Cell 18 1023-1037 917
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L 918
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factors genome-wide comparative analysis among eukaryotes Science 290 921
2105-2110 922
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the 923
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strawberry fruits J Agric Food Chem 46 1488-1493 925
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 926
25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in 927
strawberry fruits Phytochemistry 43 155-159 928
Schwab W (1998) Application of stable isotope ratio analysis explaining the 929
bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone in plants by a biological 930
maillard reaction J Agric Food Chem 46 2266ndash2269 931
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33
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Molecules 18 6936-6951 933
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products Recent Res Dev Phytochem 1 643-673 935
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compositions a seasonal influence and effects on sensory perception PLoS One 9 939
e88446 940
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Identification phylogeny and transcript profiling of ERF family genes during 942
development and abiotic stress treatments in tomato Mol Genet Genomics 284 943
455-475 944
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) 945
CitAP210 activation of the terpene synthase CsTPS1 is associated with the 946
synthesis of (+)-valencene in lsquoNewhallrsquo orange J Exp Bot 67 4105-4115 947
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes 948
Dev Genes Evol 214 105-114 949
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key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151 952
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regulatory factor EOBI acting downstream of EOBII regulates scent production 955
by activating ODO1 and structural scent-related genes in petunia Plant Cell 24 956
5089-5105 957
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp 958
Bot 68 4407-4409 959
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla 960
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34
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to ripening New Phytol 208 482-496 963
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regulates fragrance biosynthesis in petunia flowers Plant Cell 17 1612-1624 965
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS 966
(2018) The potassium channel FaTPK1 plays a critical role in fruit quality 967
formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748 968
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) 969
Isolation cloning and expression of a multifunctional O-methyltransferase capable 970
of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma 971
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types their evolutionary origin and species distribution In A handbook of 974
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Biochemistry 52 25-73 976
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of 977
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Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS 979
(2014) Isolation classification and transcription profiles of the AP2ERF 980
transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271 981
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in 982
regulation of fruit quality Crit Rev Plant Sci 35 120-130 983
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ 984
Zhang SL Wu J (2017) Map-based cloning of the pear gene MYB114 identifies an 985
interaction with other transcription factors to coordinately regulate fruit 986
anthocyanin biosynthesis Plant J 92 437-451 987
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes 988
involved in regulating fruit ripening Plant Physiol 153 1280-1292 989
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
35
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) 990
Expression of ethylene response genes during persimmon fruit astringency removal 991
Planta 235 895-906 992
Zabetakis I Gramshaw JW Robinson DS (1999) 993
25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis and 994
biosynthesis-a review Food Chem 65 139-151 995
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci 996
Food Agric 74 421-434 997
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 998
an AP2ERF gene is a novel regulator of fruit lignification induced by chilling 999
injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1000
1325-1334 1001
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation 1002
classification and transcription profiles of the Ethylene Response Factors (ERFs) in 1003
ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215 1004
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML 1005
(2012) Genome-wide analysis of the AP2ERF superfamily in peach (Prunus 1006
persica) Genet Mol Res 11 4788-4809 1007
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and 1008
expression analysis of a CRTDRE-binding factor gene FaCBF1 from Fragaria times 1009
ananassa Acta Hortic 41 240-248 1010
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The 1011
Arabidopsis AP2ERF transcription factor RAP26 participates in ABA salt and 1012
osmotic stress responses Gene 457 1-12 1013
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B 1014
Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) Genome-wide 1015
analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic 1016
(Amsterdam) 123 73-81 1017
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF 1018
Valpuesta V Botella MA Granell A Amaya I (2012) Genetic analysis of 1019
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36
strawberry fruit aroma and identification of O-methyltransferase FaOMT as the 1020
locus controlling natural variation in mesifurane content Plant Physiol 159 1021
851-870 1022
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wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Parsed CitationsAgarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression of PgDREB2A transcription factor enhances abioticstress tolerance and activates downstream stress-responsive genes Mol Biol Rep 37 1125-1135
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Araguumlez I Osorio S Hoffmann T Rambla JL Medina-Escobar N Granell A Botella MAacute Schwab W Valpuesta V (2013) Eugenolproduction in achenes and receptacles of strawberry fruits is catalyzed by synthases exhibiting distinct kinetics Plant Physiol 163 946-958
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18
procedure (Araguumlez et al 2013) briefly 05 g (fresh weight) of powdered fruit was 486
incubated at 30degC in a water bath for 5 min then 2 mL of NaCl (mv = 20) and 20 487
microL of 2-octanol as the internal standard (007 μgμL) were added and homogenized 488
489
For the detection of HDMF (Figure 1) and both furanones (Figure 4 and Supplemental 490
Table S3) a liquid-injection system equipped with CTC Pal ALS was used One gram 491
(fresh weight) of powdered fruit and 2 mL of NaCl (mv = 20) were homogenized in 492
a 10-mL tube and 300 μL of CH2Cl2 and 20 microL of 2-octanol (0766 μgμL) as the 493
internal standard were added to extract the volatiles the mixture was then 494
homogenized again The tubes were stored at room temperature for 20 min and 495
centrifuged at 12000 rpm for 5 min The subnatant was pipetted into a clean 15-mL 496
tube in which 20 mg of anhydrous sodium sulphate was added the tube was left 497
without shaking for half an hour Then 150 μL of the solution was transferred into a 498
GC vial and placed on the sample tray as described above Each sample (1 μL) was 499
injected using the autosampler and the analysis was accomplished by a 7890A 500
GC-MS system (Agilent Technologies JampW Scientific Folsom CA USA) equipped 501
with a DB-WAX column (30 m times 025 mm times 025 μm JampW) Helium (12 mLmin) 502
was used as a carrier gas The injection port (splitless injection mode) interface and 503
MS source temperatures were as described above The oven temperature was set at 504
60degC for 4 min then increased to 180degC at a rate of 4degCmin and maintained for 30 505
min DMMF was identified by comparison of electron ionization mass spectra and 506
retention time data with the data from the NISTEPANIH mass spectral library 507
(NIST-08 and Flavor) HDMF (Figure 1) was identified and qualified by comparison 508
with injected standard (Sigma) The quantitative analysis of both furanones (Figure 4 509
Supplemental Table S3 and Supplemental Figure S3) was determined using the peak 510
area of the internal standard as a reference based on total ion chromatogram (TIC) 511
512
RNA isolation and Reverse Transcription Quantitative PCR (RT-qPCR) 513
Total RNA from strawberry samples was isolated in this study using the CTAB 514
method (Chang et al 1993) Genomic DNA contamination was eliminated by 515
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19
TURBO Dnase (Ambion) 1 μg of RNA was used to obtain cDNA using an IScriptTM 516
cDNA Synthesis Kit (Bio-Rad) The synthesized cDNA was diluted with water (120) 517
and 2 μL of diluted cDNA was used as the template for RT-qPCR Reactions were 518
performed in a total volume of 20 μL consisting of 10 μL of SYBR PCR supermix 519
(Bio-Rad) 1 μL of each primer (10 μM) 6 μL of DEPC-H2O and 2 μL of diluted 520
cDNA on CFX96 instrument (Bio-Rad) (Yin et al 2012) The oligonucleotide 521
primers for RT-qPCR analysis of genes including the AP2ERF FaQR and FaOMT 522
were designed according to the coding sequences of genes and the specificity was 523
verified before use (Min et al 2012) NCBIPrimer-BLAST was applied to design the 524
primers Relative expression levels were normalized to that of an internal controlmdashthe 525
interspacer 26S-18S strawberry RNA housekeeping gene FaRIB413 526
(Zorrilla-Fontanesi et al 2012) To investigate the differential expression of genes 527
during fruit development and ripening stages relative expression of each gene at the 528
R stage in the basal fruit section was set as 1 using the 2minus∆∆119862119879 method For transient 529
overexpression assay relative expression of control fruits with an empty vector (SK) 530
was set as 1 The primers used in RT-qPCR are listed in Supplemental Table S4 531
532
Gene isolation and analysis 533
Multiple database searches were performed to identify members of the strawberry 534
(Fragaria times ananassa) AP2ERF superfamily in the published strawberry databases 535
and annotations of Fragaria times ananassa and Fragaria times vesca by using the 536
AP2ERF DNA binding domain as a query sequence and 120 genes were identified 537
with AP2ERF domain(s) Based on the BLAST result primers (listed in 538
Supplemental Table S5) were used to amplify the coding full-length cDNAs of 539
AP2ERF genes The deduced amino acid sequences of AP2ERF proteins in 540
Arabidopsis thaliana used for construction of a phylogenetic tree were obtained from 541
the Arabidopsis Information Resource (TAIR) Alignment of the proteins was 542
performed using the neighbour-joining method in ClustalX (v181) and the 543
phylogenetic tree was constructed using FigTree (v131) 544
545
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20
FaMYB98 was obtained by yeast one-hybrid screening sequencing and the full-length 546
sequences were predicted by BLAST Primers were designed (listed in Supplemental 547
Table S5) to amplify the full-length coding sequence 548
549
The promoter of FaQR was cloned by Genome Walking as previously described (Yin 550
et al 2010) and conserved cis-element motifs in the promoter were manually 551
searched 552
553
Conserved domains within the FaAP2ERF proteins and FaMYB98 were analysed by 554
CD-search (httpswwwncbinlmnihgovStructurecddwrpsbcgi) and cellular 555
locations of proteins including FaERF9 and FaMYB98 were predicted with the 556
WoLF PSORT program (httpswwwgenscriptcomwolf-psorthtml) 557
558
Dual-Luciferase Assays 559
In accordance with a previous protocol (Yin et al 2010) the full-length cDNAs of 560
FaAP2ERF or FaMYB98 transcription factors were cloned into pGreen II 0029 561
62-SK vector and the promoter of FaQR was cloned into pGreen II 0800-LUC vector 562
A luciferase gene from Renillia (REN) driven by a 35S promoter in the LUC vector 563
acted as a positive control The above constructs were transiently expressed in 564
Nicotiana benthamiana leaves by Agrobacterium-mediated infiltration (strain 565
GV3101) and the activity of the TFs on the promoter was measured on the third day 566
after infiltration indicated by the ratio of enzyme activities of firefly luciferase (LUC) 567
and renilla luciferase (REN) using a Modulus Luminometer (Promega Madison WI 568
USA) To determine the activity of a specific transcription factor towards the 569
promoter we mixed the Agrobacterium culture with 1 mL of TF and 100 μL of 570
promoter and the LUCREN value of the empty vector SK on the promoter was set as 571
1 as a calibrator To test the combined effect of two transcription factors on the 572
promoter to the Agrobacterium culture mixture we added 05 mL of each TF and 100 573
μL of promoter the effect of the mixtures that contained each transcription factor (05 574
mL) and empty vector SK (05 mL) was also tested on the promoter as a control 575
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21
576
Subcellular localization analysis 577
35S-FaERF9-GFP and 35S-FaMYB98-GFP were transiently expressed in tobacco (N 578
benthamiana) leaves by Agrobacterium infiltration (EHA105) using the same method 579
as described in the dual-luciferase assay above The transiently infected leaves were 580
imaged on the third day after infiltration using a Nikon A1-SHS confocal laser 581
scanning microscope The excitation wavelength for GFP fluorescence was 488 nm 582
and fluorescence was detected at 490ndash520 nm The primers used for GFP construction 583
are listed in Supplemental Table S6 584
585
Transient overexpression in strawberry fruit 586
Transient overexpression of FaERF9 and an overexpression binary vector (pGreen II 587
0029 62-SK-FaERF9-FaMYB98) were performed in strawberry fruit using the 588
FaERF9-SK construct described above for the dual-luciferase assays and the binary 589
vector constructed according to Liu et al 2013 The transfection of fruit was carried 590
out at the G stage (Hoffmann et al 2006) The FaERF9-SK construct and binary 591
vector were individually electroporated into Agrobacterium tumefaciens GV3101 and 592
the Agrobacterium culture suspended in infiltration buffer was infiltrated into the 593
whole fruit using a syringe As a control treatment fruits were infiltrated with 594
Agrobacterium carrying an empty vector SK under the same transfection conditions 595
Fruits were left attached to the plants and harvested on the seventh day after 596
infiltration Fruits of three biological replicates were sampled for further analysis 597
598
Yeast one-hybrid assay 599
In order to identify proteins that bind to the FaQR promoter the Matchmaker Gold 600
Yeast One-hybrid Library Screening System (Clontech USA) was used The sequence 601
of the FaQR promoter was cloned into the pAbAi vector and the construct was 602
integrated into the genome of the Y1HGold yeast strain A mixture of total RNA from 603
strawberry fruit at four stages (G T IR R) was used to construct the prey cDNA 604
library (TaKaRa) The background AbAr expression of Y1HGold FaQR-pAbAi strain 605
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22
was tested according to the system user manual and then screening for protein-DNA 606
interactions was carried out Furthermore the full length of each transcription factor 607
was separately cloned into pGADT7 AD vector to confirm the screening results The 608
relationship between FaERF9 and FaQR promoter was also examined individually 609
Primers used in this assay are listed in Supplemental Table S6 610
611
Expression and purification of FaMYB98 recombinant protein 612
A 405-bp region spanning the DNA-binding domain of FaMYB98 was amplified 613
from FaMYB98 cDNA and cloned into a pET6timesHN vector (Clontech Palo CA USA) 614
to generate the recombinant N-terminal His-tagged protein the primers used are listed 615
in Supplemental Table S6 The resulting construct was sequenced and introduced into 616
Escherichia coli strain Rosetta 2(DE3)pLysS (Novagen) Ten millilitres of the 617
overnight culture was combined with 500 mL of an LB liquid medium (100 μgmL 618
ampicillin and 34 μgmL chloramphenicol) as described (Li et al 2017) Isopropyl 619
β-D-1-thiogalactopyranoside (IPTG) was added to a final concentration of 1 mM and 620
the bacterial culture was incubated at 18degC at 150 rpm for 18 h Then the cells were 621
harvested using a centrifuge and resuspended in 1times PBS buffer (Sangon Biotech) 622
after which they were disrupted by sonication and the supernatant was purified using 623
a HisTALONTM Gravity Column (Clontech) according to the user manual The PD-10 624
Desalting column (GE Healthcare) was then used for buffer change and sample 625
clean-up of proteins according to the gravity protocol SDS-PAGE was performed and 626
the protein was visualized using Coomassie brilliant blue 627
628
Electrophoretic mobility shift assay (EMSA) 629
A Lightshift Chemiluminescent EMSA kit (Thermo) was used to perform EMSA 630
experiments according to the manufacturerrsquos instructions Single-strand 631
oligonucleotides were synthesized and biotinylated by GeneBio Biotech (Hangzhou 632
China) The details of the EMSA assay are provided in Ge et al (2017) The probes 633
used for EMSAs are listed in Supplemental Table S6 634
635
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
23
636
Yeast two-hybrid assay 637
The DUALhunter system (Dualsystems Biotech Switzerland) was used to investigate 638
the interaction between FaERF9 and FaMYB98 Full-length coding sequences of 639
FaERF9 and FaMYB98 were respectively cloned into pDHB1 bait vector and 640
pPR3-N prey vector sequences were verified and the bait plasmid was 641
co-transformed with prey plasmid into NMY51 in the combinations below 642
FaMYB98-pDHB1pPR3-N FaMYB98-pDHB1FaERF9-pPR3-N 643
FaMYB98-pDHB1pOst1-NubI FaERF9-pDHB1pPR3-N 644
FaERF9-pDHB1FaMYB98-pPR3-N and FaERF9-pDHB1pOst1-NubI (Li et al 645
2017) Transformed cells were spread onto the following plates DDO (SD 646
medium-Trp-Leu) QDO (SD medium-Trp-Leu-His-Ade) and QDO+3-AT (QDO 647
medium supplemented with 1 mM 3-amino-124-triazole) The control plasmid 648
pOst1-NubI was used to determine whether the bait was functional the pPR3-N prey 649
vector plasmid was used to test whether the bait displayed non-specific background 650
and positive interactions were indicated by the growth of yeast on QDO and 651
QDO+3-AT plates The Primers used in the DUALhunter assay are listed in 652
Supplemental Table S6 653
654
Bimolecular fluorescence complementation (BiFC) assays 655
Full-length FaERF9 and FaMYB98 respectively were cloned into sequences 656
encoding the N- and C- fragments of YFP protein (Lv et al 2014) All constructs 657
were transiently expressed in tobacco (N benthamiana) leaves by Agrobacterium 658
infiltration (EHA105) The YFP fluorescence of transfected leaves was imaged 40 h 659
after infiltration by using a Nikon A1-SHS confocal laser scanning microscope The 660
excitation wavelength for YFP was 488 nm and fluorescence was detected at 520ndash661
540 nm Primers used are listed in Supplemental Table S6 662
663
Statistics 664
A Studentrsquos two-tailed t test ( plt005 plt001 and plt0001) was used to 665
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
24
determine significant differences between two groups in this study Microsoft Excel 666
was used to perform linear regressive analysis significant differences were 667
determined by SPSS Statistics 200 and scatter plots were prepared with Origin80 668
Least significant difference (LSD) at the 5 level was calculated using Microsoft 669
Excel Figures were prepared with Origin80 (Microcal Software Inc Northampton 670
MA USA) The online tool MetaboAnalyst 36 (httpwwwmetaboanalystca) was 671
used to analyse the transcript abundance of the AP2ERF genes 672
673
Accession numbers 674
Sequence data from this article have been deposited in GenBank under the accession 675
numbers MH332903-MH333022 for AP2ERF genes in Fragaria times ananassa and 676
MH333023 for FaMYB98 GenBank numbers for FaQR and FaOMT were 677
AY1588361 (Raab et al 2006) and AF2204912 (Wein et al 2002) 678
679
Supplemental Material 680
Supplemental Figure S1 Phylogenetic analysis of FaAP2ERF and Arabidopsis 681
AP2ERF proteins 682
Supplemental Figure S2 Analysis of FaAP2ERF gene expression patterns in 683
strawberry fruit during development and ripening 684
Supplemental Figure S3 Contents of furanones in fruit of strawberry cultivars 685
Supplemental Figure S4 Relative expression of FaERF9 in FaERF9-FaMYB98- 686
and FaERF9-overexpressing fruits 687
Supplemental Figure S5 Subcellular localization of FaMYB98 688
Supplemental Figure S6 The combined activation effects of FaERF9FaMYB98 on 689
the FaOMT promoter 690
Supplemental Figure S7 Relative expression of FaOMT in 691
FaERF9-overexpressing fruits 692
Supplemental Table S1 AP2ERF superfamily genes in Fragaria times ananassa 693
Supplemental Table S2 Classification of the AP2ERF superfamily members in 694
Fragaria times ananassa 695
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
25
Supplemental Table S3 Furanone content in FaERF9-FaMYB98- and 696
FaERF9-overexpressing fruits 697
Supplemental Table S4 Primers used for reverse transcription quantitative PCR 698
(RT-qPCR) 699
Supplemental Table S5 Primers used to amplify the full-length coding sequences of 700
AP2ERF genes and FaMYB98 in strawberry (Fragaria times ananassa) 701
Supplemental Table S6 Primers used for vector construction 702
703
Acknowledgments 704
This research was supported by the National Key Research and Development 705
Program (2016YFD0400101) the Project of the Science and Technology Department 706
of Zhejiang Province (2016C04001) and the 111 Project (B17039) 707
708
Figure legends 709
Figure 1 Changes in furanone content and furanone biosynthetic genes during 710
strawberry (Fragaria times ananassa Duch cv Yuexin) fruit development and ripening 711
A Fruits were collected at four ripening stages G (green stage) T (turning stage) IR 712
(intermediate red stage) R (full red stage) B Changes in the contents of furaneol 713
(HDMF) and mesifurane (DMMF) HDMF content was calculated using a standard 714
curve of HDMF while DMMF content was calculated with an internal standard as the 715
reference C Expression levels of FaQR and FaOMT The expression levels of each 716
gene were calculated relative to corresponding values in the basal section at the R 717
stage SEs were calculated from three replicates and LSD values represent the least 718
significant differences at p = 005 719
Figure 2 Regulatory effects of FaAP2ERF on the promoter of FaQR LUCREN 720
values of the empty vector on FaQR promoter were used as the calibrator set as 1 721
and SEs were calculated from five replicates statistical significance was determined 722
by Studentrsquos two-tailed t test ( plt0001) 723
Figure 3 Expression and the subcellular localization of FaERF9 A The expression 724
levels were calculated relative to the levels in the basal section at the R stage B 725
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
26
Subcellular localization analysis was performed in tobacco leaves The tobacco used 726
in the assay was stably transformed with a specific nucleus localized red fluorescence 727
protein construct and the red fluorescence indicates the nucleus-localized signal 728
(NLS) Scale bar = 25 microm SEs were calculated from three replicates 729
Figure 4 Transient overexpression of FaERF9 in strawberry fruit A Relative 730
expression of FaQR and FaERF9 in FaERF9-OX fruit 7 days after infiltration The 731
expression was calculated relative to the average value in control (SK) fruits B 732
HDMF and DMMF content in FaERF9-OX fruit The content of both furanones 733
were quantified using the peak area of the internal standard (2-octanol) as the 734
reference SEs were calculated from three replicates Statistical significance was 735
determined by Studentrsquos two-tailed t test ( plt005 plt001 plt0001) 736
Figure 5 Scatter plots of 11 strawberry cultivars A Linear regression analysis 737
between FaERF9 expression and FaQR expression B Linear regression analysis 738
between FaERF9 expression and furanone content The relative expression was 739
normalized to that of the housekeeping gene FaRIB413 and furanone content was 740
calculated with internal standard as the reference Significant differences were 741
determined by SPSS Statistics 200 742
Figure 6 Interactions of FaERF9 and FaMYB98 with the FaQR promoter A Yeast 743
one-hybrid analysis of the interaction of FaERF9 and FaQR promoter B Yeast 744
one-hybrid analysis of the interaction of FaMYB98 and FaQR promoter C 745
Regulatory effect of FaMYB98 on the FaQR promoter Auto-activation was tested on 746
SD-Ura (synthetically defined medium without uracil) in presence of Aureobasidin A 747
(AbA) and physical interaction was determined on SD-Leu (synthetically defined 748
medium without leucine) in presence of AbA LUCREN values of the empty vector 749
on FaQR promoter were used as the calibrator set as 1 and error bars were calculated 750
from five replicates Statistical significance was determined by Studentrsquos two-tailed t 751
test ( plt005 plt001 plt0001) 752
Figure 7 Electrophoretic mobility shift assay of FaMYB98 binding to FaQR 753
promoter A The probe sequence used for EMSA and mutated nucleotides are 754
indicated with lowercase letters B Purified DNA-binding domain of FaMYB98 755
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
27
protein and biotin-labelled DNA probe were mixed and analysed on 6 native 756
polyacrylamide gels and then photographed Presence or absence of specific probes is 757
marked by the symbol + or - 758
Figure 8 The combined activation effects of FaERF9FaMYB98 on the FaQR 759
promoter LUCREN values obtained with the empty vector and FaQR promoter were 760
used as the calibrator set as 1 and error bars were calculated from five replicates 761
Figure 9 Yeast two-hybrid analysis of the protein-protein interactions between 762
FaMYB98 and FaERF9 Positive interactions were determined by the growth of 763
yeast cells on selection plates Bait with pOST acted as positive controls and bait with 764
pPR3 as negative controls DDO synthetically defined medium without tryptophan 765
and leucine QDO synthetically defined medium without tryptophan leucine 766
histidine and adenine QDO+3AT QDO medium supplemented with 1 mM 767
3-aminotriazole 768
Figure 10 BiFC analysis of the protein-protein interactions between FaMYB98 and 769
FaERF9 The pairs of fusion proteins tested were FaMYB98-YFPN+FaERF9-YFPC 770
FaERF9-YFPN+FaMYB98-YFPC FaMYB98-YFPN+FaMYB98-YFPC and 771
FaERF9-YFPN+FaERF9-YFPC The other combinations were negative controls 772
The tobacco used in the assay was stably transformed with a specific 773
nucleus-localized red fluorescence protein construct and the red fluorescence 774
indicated the nucleus-localized signal (NLS) Fluorescence of the yellow fluorescence 775
protein (YFP) visualized the interaction in vivo Scale bar = 25 microm 776
777
Literature Cited 778
779
Agarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression 780
of PgDREB2A transcription factor enhances abiotic stress tolerance and activates 781
downstream stress-responsive genes Mol Biol Rep 37 1125-1135 782
Araguumlez I Osorio S Hoffmann T Rambla JL Medina-Escobar N Granell A 783
Botella MAacute Schwab W Valpuesta V (2013) Eugenol production in achenes and 784
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
28
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Plant Physiol 163 946-958 786
Carvalho RF Carvalho SD OrsquoGrady K Folta KM (2016) Agroinfiltration of 787
strawberry fruit mdash a powerful transient expression system for gene validation Curr 788
Plant Biol 6 19-37 789
Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic 790
(Amsterdam) 210 34-40 791
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating 792
RNA from pine trees Plant Mol Biol Rep 11 113-116 793
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC 794
Clark DG (2011) PhMYB4 fine-tunes the floral volatile signature of 795
Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143 796
Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz 797
EA Taylor MG Smits-Kroon MT Schuurink RC Haring MA Giovannoni J 798
Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic 799
pathway by ectopic expression of a MYB transcription factor in tomato fruit Plant 800
Cell 23 2738-2753 801
Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan 802
XW Yang ZY (2017) Differential responses of four biosynthetic pathways of 803
aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under 804
interaction of light and temperature Food Chem 221 356-364 805
Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of 806
differentially-expressed genes during somatic embryogenesis in Fragaria times 807
ananassa Duch lsquoBenihopprsquo J Hortic Sci Biotechnol 90 671-681 808
Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 809
transcriptionally regulates chilling-induced lignification of loquat fruit via physical 810
interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136 811
Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM 812
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proteins Plant J 39 513-526 814
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29
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) 815
Sucrose nonfermenting1-related protein kinase26 an ortholog of open stomata1 is 816
a negative regulator of strawberry fruit development and ripening Plant Physiol 817
167 915-930 818
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene 819
expression in strawberry fruit (Fragaria times ananassa) by agroinfiltration a rapid 820
assay for gene function analysis Plant J 48 818-826 821
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of 822
selected aroma-active compounds in strawberries by headspace solid-phase 823
microextraction gas chromatography and correlation with sensory descriptive 824
analysis J Food Sci 72 S487-S496 825
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid 826
plays an important role in the regulation of strawberry fruit ripening Plant Physiol 827
157 188-199 828
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of 829
NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes BMC 830
Plant Biol 6 20 831
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN 832
(2005) MYB98 is required for pollen tube guidance and synergid cell differentiation 833
in Arabidopsis Plant Cell 17 2981-2992 834
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional 835
characterization of enone oxidoreductases from strawberry and tomato fruit J 836
Agric Food Chem 55 6705-6711 837
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You 838
J-S Rohloff J Randall SK Alsheikh M (2012) Proteomic study of 839
low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ 840
in cold tolerance Plant Physiol 159 1787-1805 841
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional 842
characterization of four APETALA2-family genes (RAP26 RAP26L DREB19 843
and DREB26) in Arabidopsis Plant Mol Biol 75 107-127 844
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30
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon 845
J Gupta V (2013) An oxidoreductase from lsquoAlphonsorsquo mango catalyzing 846
biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494 847
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in 848
strawberries Z Lebensm-Unters Forsch 195 120-123 849
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X 850
(2015) Label-free quantitative proteomics to investigate strawberry fruit proteome 851
changes under controlled atmosphere and low temperature storage J Proteomics 852
120 44-57 853
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 854
cooperates with CitWRKY1 to participate in citric acid degradation via 855
up-regulation of CitAco3 J Exp Bot 68 3419-3426 856
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription 857
factor CitERF71 activates the terpene synthase gene CitTPS16 involved in the 858
synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938 859
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and 860
transcriptomic analysis of the AP2ERF superfamily in Vitis vinifera BMC 861
Genomics 11 719 862
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive 863
Factor (AP2ERF) transcription factors mediators of stress responses and 864
developmental programs New Phytol 199 639-649 865
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 866
interacting with EOBI negatively regulates fragrance biosynthesis in petunia 867
flowers New Phytol 215 1490-1502 868
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu 869
CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 in regulating 870
anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) 871
during anthocyanin biosynthesis Plant Cell Tissue Organ Cult 115 285-298 872
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31
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao 873
CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphate signaling and 874
homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597 875
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC 876
Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL 877
Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor 878
regulates eugenol production in ripe strawberry fruit receptacles Plant Physiol 168 879
598-614 880
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics 881
and volatile constituents of strawberry (cv Cigaline) during maturation J Agric 882
Food Chem 52 1248-1254 883
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS 884
(2012) Ethylene-responsive transcription factors interact with promoters of ADH 885
and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 886
63 6393-6405 887
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM 888
Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-Franco A 889
Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific 890
transcription factor FaDOF2 regulates the production of eugenol in ripe fruit 891
receptacles J Exp Bot 68 4529-4543 892
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) 893
Comparison and verification of the genes involved in ethylene biosynthesis and 894
signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44 895
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the 896
ERF gene family in Arabidopsis and rice Plant Physiol 140 411-432 897
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in 898
sour cherry and strawberry and the heterologous expression of CBF1 in strawberry 899
J Am Soc Hortic Sci 127 489-494 900
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech 901
JC Ohme-Takagi M Regad F Bouzayen M (2012) Functional analysis and 902
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32
binding affinity of tomato ethylene response factors provide insight on the 903
molecular bases of plant differential responses to ethylene BMC Plant Biol 12 190 904
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) 905
Methylpentoses are possible precursors of furanones in fruits Prikl Biokhim 906
Mikrobiol 28 123-127 907
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery 908
of synergid-expressed genes encoding filiform apparatus localized proteins Plant 909
Cell 19 2557-2568 910
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria 911
vesca L compared to those of cultivated berries Fragariatimes ananassa cv Senga 912
Sengana J Agric Food Chem 27 19-22 913
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W 914
Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of the strawberry 915
flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone 916
oxidoreductase Plant Cell 18 1023-1037 917
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L 918
Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim M Broun P Zhang 919
JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription 920
factors genome-wide comparative analysis among eukaryotes Science 290 921
2105-2110 922
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the 923
formation of 25-dimethyl-4-hydroxy-3(2H)-furanone in detached ripening 924
strawberry fruits J Agric Food Chem 46 1488-1493 925
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 926
25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in 927
strawberry fruits Phytochemistry 43 155-159 928
Schwab W (1998) Application of stable isotope ratio analysis explaining the 929
bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone in plants by a biological 930
maillard reaction J Agric Food Chem 46 2266ndash2269 931
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
33
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) 932
Molecules 18 6936-6951 933
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard 934
products Recent Res Dev Phytochem 1 643-673 935
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL 936
Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJ Sims CA 937
Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical 938
compositions a seasonal influence and effects on sensory perception PLoS One 9 939
e88446 940
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) 941
Identification phylogeny and transcript profiling of ERF family genes during 942
development and abiotic stress treatments in tomato Mol Genet Genomics 284 943
455-475 944
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) 945
CitAP210 activation of the terpene synthase CsTPS1 is associated with the 946
synthesis of (+)-valencene in lsquoNewhallrsquo orange J Exp Bot 67 4105-4115 947
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes 948
Dev Genes Evol 214 105-114 949
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K 950
Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the 951
key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151 952
Spitzer-Rimon B Farhi M Albo B Cnarsquoani A Ben Zvi MM Masci T Edelbaum 953
O Yu YX Shklarman E Ovadis M Vainstein A (2012) The R2R3-MYB-like 954
regulatory factor EOBI acting downstream of EOBII regulates scent production 955
by activating ODO1 and structural scent-related genes in petunia Plant Cell 24 956
5089-5105 957
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp 958
Bot 68 4407-4409 959
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla 960
JF Amaya I Giavalisco P Fernie AR Botella MA Valpuesta V (2015) Central 961
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34
role of FaGAMYB in the transition of the strawberry receptacle from development 962
to ripening New Phytol 208 482-496 963
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 964
regulates fragrance biosynthesis in petunia flowers Plant Cell 17 1612-1624 965
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS 966
(2018) The potassium channel FaTPK1 plays a critical role in fruit quality 967
formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748 968
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) 969
Isolation cloning and expression of a multifunctional O-methyltransferase capable 970
of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma 971
compounds in strawberry fruits Plant J 31 755-765 972
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor 973
types their evolutionary origin and species distribution In A handbook of 974
transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular 975
Biochemistry 52 25-73 976
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of 977
odor (Buettner A Ed) Springer Cham 9-10 978
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS 979
(2014) Isolation classification and transcription profiles of the AP2ERF 980
transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271 981
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in 982
regulation of fruit quality Crit Rev Plant Sci 35 120-130 983
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ 984
Zhang SL Wu J (2017) Map-based cloning of the pear gene MYB114 identifies an 985
interaction with other transcription factors to coordinately regulate fruit 986
anthocyanin biosynthesis Plant J 92 437-451 987
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes 988
involved in regulating fruit ripening Plant Physiol 153 1280-1292 989
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
35
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) 990
Expression of ethylene response genes during persimmon fruit astringency removal 991
Planta 235 895-906 992
Zabetakis I Gramshaw JW Robinson DS (1999) 993
25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis and 994
biosynthesis-a review Food Chem 65 139-151 995
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci 996
Food Agric 74 421-434 997
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 998
an AP2ERF gene is a novel regulator of fruit lignification induced by chilling 999
injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1000
1325-1334 1001
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation 1002
classification and transcription profiles of the Ethylene Response Factors (ERFs) in 1003
ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215 1004
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML 1005
(2012) Genome-wide analysis of the AP2ERF superfamily in peach (Prunus 1006
persica) Genet Mol Res 11 4788-4809 1007
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and 1008
expression analysis of a CRTDRE-binding factor gene FaCBF1 from Fragaria times 1009
ananassa Acta Hortic 41 240-248 1010
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The 1011
Arabidopsis AP2ERF transcription factor RAP26 participates in ABA salt and 1012
osmotic stress responses Gene 457 1-12 1013
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B 1014
Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) Genome-wide 1015
analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic 1016
(Amsterdam) 123 73-81 1017
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF 1018
Valpuesta V Botella MA Granell A Amaya I (2012) Genetic analysis of 1019
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36
strawberry fruit aroma and identification of O-methyltransferase FaOMT as the 1020
locus controlling natural variation in mesifurane content Plant Physiol 159 1021
851-870 1022
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Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 an AP2ERF gene is a novel regulator of fruit lignificationinduced by chilling injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1325-1334
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Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML (2012) Genome-wide analysis of the AP2ERF superfamily inpeach (Prunus persica) Genet Mol Res 11 4788-4809
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Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and expression analysis of a CRTDRE-binding factor gene FaCBF1from Fragaria times ananassa Acta Hortic 41 240-248
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
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Genome-wide analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic (Amsterdam) 123 73-81Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF Valpuesta V Botella MA Granell A Amaya I (2012) Geneticanalysis of strawberry fruit aroma and identification of O-methyltransferase FaOMT as the locus controlling natural variation inmesifurane content Plant Physiol 159 851-870
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
19
TURBO Dnase (Ambion) 1 μg of RNA was used to obtain cDNA using an IScriptTM 516
cDNA Synthesis Kit (Bio-Rad) The synthesized cDNA was diluted with water (120) 517
and 2 μL of diluted cDNA was used as the template for RT-qPCR Reactions were 518
performed in a total volume of 20 μL consisting of 10 μL of SYBR PCR supermix 519
(Bio-Rad) 1 μL of each primer (10 μM) 6 μL of DEPC-H2O and 2 μL of diluted 520
cDNA on CFX96 instrument (Bio-Rad) (Yin et al 2012) The oligonucleotide 521
primers for RT-qPCR analysis of genes including the AP2ERF FaQR and FaOMT 522
were designed according to the coding sequences of genes and the specificity was 523
verified before use (Min et al 2012) NCBIPrimer-BLAST was applied to design the 524
primers Relative expression levels were normalized to that of an internal controlmdashthe 525
interspacer 26S-18S strawberry RNA housekeeping gene FaRIB413 526
(Zorrilla-Fontanesi et al 2012) To investigate the differential expression of genes 527
during fruit development and ripening stages relative expression of each gene at the 528
R stage in the basal fruit section was set as 1 using the 2minus∆∆119862119879 method For transient 529
overexpression assay relative expression of control fruits with an empty vector (SK) 530
was set as 1 The primers used in RT-qPCR are listed in Supplemental Table S4 531
532
Gene isolation and analysis 533
Multiple database searches were performed to identify members of the strawberry 534
(Fragaria times ananassa) AP2ERF superfamily in the published strawberry databases 535
and annotations of Fragaria times ananassa and Fragaria times vesca by using the 536
AP2ERF DNA binding domain as a query sequence and 120 genes were identified 537
with AP2ERF domain(s) Based on the BLAST result primers (listed in 538
Supplemental Table S5) were used to amplify the coding full-length cDNAs of 539
AP2ERF genes The deduced amino acid sequences of AP2ERF proteins in 540
Arabidopsis thaliana used for construction of a phylogenetic tree were obtained from 541
the Arabidopsis Information Resource (TAIR) Alignment of the proteins was 542
performed using the neighbour-joining method in ClustalX (v181) and the 543
phylogenetic tree was constructed using FigTree (v131) 544
545
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20
FaMYB98 was obtained by yeast one-hybrid screening sequencing and the full-length 546
sequences were predicted by BLAST Primers were designed (listed in Supplemental 547
Table S5) to amplify the full-length coding sequence 548
549
The promoter of FaQR was cloned by Genome Walking as previously described (Yin 550
et al 2010) and conserved cis-element motifs in the promoter were manually 551
searched 552
553
Conserved domains within the FaAP2ERF proteins and FaMYB98 were analysed by 554
CD-search (httpswwwncbinlmnihgovStructurecddwrpsbcgi) and cellular 555
locations of proteins including FaERF9 and FaMYB98 were predicted with the 556
WoLF PSORT program (httpswwwgenscriptcomwolf-psorthtml) 557
558
Dual-Luciferase Assays 559
In accordance with a previous protocol (Yin et al 2010) the full-length cDNAs of 560
FaAP2ERF or FaMYB98 transcription factors were cloned into pGreen II 0029 561
62-SK vector and the promoter of FaQR was cloned into pGreen II 0800-LUC vector 562
A luciferase gene from Renillia (REN) driven by a 35S promoter in the LUC vector 563
acted as a positive control The above constructs were transiently expressed in 564
Nicotiana benthamiana leaves by Agrobacterium-mediated infiltration (strain 565
GV3101) and the activity of the TFs on the promoter was measured on the third day 566
after infiltration indicated by the ratio of enzyme activities of firefly luciferase (LUC) 567
and renilla luciferase (REN) using a Modulus Luminometer (Promega Madison WI 568
USA) To determine the activity of a specific transcription factor towards the 569
promoter we mixed the Agrobacterium culture with 1 mL of TF and 100 μL of 570
promoter and the LUCREN value of the empty vector SK on the promoter was set as 571
1 as a calibrator To test the combined effect of two transcription factors on the 572
promoter to the Agrobacterium culture mixture we added 05 mL of each TF and 100 573
μL of promoter the effect of the mixtures that contained each transcription factor (05 574
mL) and empty vector SK (05 mL) was also tested on the promoter as a control 575
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21
576
Subcellular localization analysis 577
35S-FaERF9-GFP and 35S-FaMYB98-GFP were transiently expressed in tobacco (N 578
benthamiana) leaves by Agrobacterium infiltration (EHA105) using the same method 579
as described in the dual-luciferase assay above The transiently infected leaves were 580
imaged on the third day after infiltration using a Nikon A1-SHS confocal laser 581
scanning microscope The excitation wavelength for GFP fluorescence was 488 nm 582
and fluorescence was detected at 490ndash520 nm The primers used for GFP construction 583
are listed in Supplemental Table S6 584
585
Transient overexpression in strawberry fruit 586
Transient overexpression of FaERF9 and an overexpression binary vector (pGreen II 587
0029 62-SK-FaERF9-FaMYB98) were performed in strawberry fruit using the 588
FaERF9-SK construct described above for the dual-luciferase assays and the binary 589
vector constructed according to Liu et al 2013 The transfection of fruit was carried 590
out at the G stage (Hoffmann et al 2006) The FaERF9-SK construct and binary 591
vector were individually electroporated into Agrobacterium tumefaciens GV3101 and 592
the Agrobacterium culture suspended in infiltration buffer was infiltrated into the 593
whole fruit using a syringe As a control treatment fruits were infiltrated with 594
Agrobacterium carrying an empty vector SK under the same transfection conditions 595
Fruits were left attached to the plants and harvested on the seventh day after 596
infiltration Fruits of three biological replicates were sampled for further analysis 597
598
Yeast one-hybrid assay 599
In order to identify proteins that bind to the FaQR promoter the Matchmaker Gold 600
Yeast One-hybrid Library Screening System (Clontech USA) was used The sequence 601
of the FaQR promoter was cloned into the pAbAi vector and the construct was 602
integrated into the genome of the Y1HGold yeast strain A mixture of total RNA from 603
strawberry fruit at four stages (G T IR R) was used to construct the prey cDNA 604
library (TaKaRa) The background AbAr expression of Y1HGold FaQR-pAbAi strain 605
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
22
was tested according to the system user manual and then screening for protein-DNA 606
interactions was carried out Furthermore the full length of each transcription factor 607
was separately cloned into pGADT7 AD vector to confirm the screening results The 608
relationship between FaERF9 and FaQR promoter was also examined individually 609
Primers used in this assay are listed in Supplemental Table S6 610
611
Expression and purification of FaMYB98 recombinant protein 612
A 405-bp region spanning the DNA-binding domain of FaMYB98 was amplified 613
from FaMYB98 cDNA and cloned into a pET6timesHN vector (Clontech Palo CA USA) 614
to generate the recombinant N-terminal His-tagged protein the primers used are listed 615
in Supplemental Table S6 The resulting construct was sequenced and introduced into 616
Escherichia coli strain Rosetta 2(DE3)pLysS (Novagen) Ten millilitres of the 617
overnight culture was combined with 500 mL of an LB liquid medium (100 μgmL 618
ampicillin and 34 μgmL chloramphenicol) as described (Li et al 2017) Isopropyl 619
β-D-1-thiogalactopyranoside (IPTG) was added to a final concentration of 1 mM and 620
the bacterial culture was incubated at 18degC at 150 rpm for 18 h Then the cells were 621
harvested using a centrifuge and resuspended in 1times PBS buffer (Sangon Biotech) 622
after which they were disrupted by sonication and the supernatant was purified using 623
a HisTALONTM Gravity Column (Clontech) according to the user manual The PD-10 624
Desalting column (GE Healthcare) was then used for buffer change and sample 625
clean-up of proteins according to the gravity protocol SDS-PAGE was performed and 626
the protein was visualized using Coomassie brilliant blue 627
628
Electrophoretic mobility shift assay (EMSA) 629
A Lightshift Chemiluminescent EMSA kit (Thermo) was used to perform EMSA 630
experiments according to the manufacturerrsquos instructions Single-strand 631
oligonucleotides were synthesized and biotinylated by GeneBio Biotech (Hangzhou 632
China) The details of the EMSA assay are provided in Ge et al (2017) The probes 633
used for EMSAs are listed in Supplemental Table S6 634
635
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
23
636
Yeast two-hybrid assay 637
The DUALhunter system (Dualsystems Biotech Switzerland) was used to investigate 638
the interaction between FaERF9 and FaMYB98 Full-length coding sequences of 639
FaERF9 and FaMYB98 were respectively cloned into pDHB1 bait vector and 640
pPR3-N prey vector sequences were verified and the bait plasmid was 641
co-transformed with prey plasmid into NMY51 in the combinations below 642
FaMYB98-pDHB1pPR3-N FaMYB98-pDHB1FaERF9-pPR3-N 643
FaMYB98-pDHB1pOst1-NubI FaERF9-pDHB1pPR3-N 644
FaERF9-pDHB1FaMYB98-pPR3-N and FaERF9-pDHB1pOst1-NubI (Li et al 645
2017) Transformed cells were spread onto the following plates DDO (SD 646
medium-Trp-Leu) QDO (SD medium-Trp-Leu-His-Ade) and QDO+3-AT (QDO 647
medium supplemented with 1 mM 3-amino-124-triazole) The control plasmid 648
pOst1-NubI was used to determine whether the bait was functional the pPR3-N prey 649
vector plasmid was used to test whether the bait displayed non-specific background 650
and positive interactions were indicated by the growth of yeast on QDO and 651
QDO+3-AT plates The Primers used in the DUALhunter assay are listed in 652
Supplemental Table S6 653
654
Bimolecular fluorescence complementation (BiFC) assays 655
Full-length FaERF9 and FaMYB98 respectively were cloned into sequences 656
encoding the N- and C- fragments of YFP protein (Lv et al 2014) All constructs 657
were transiently expressed in tobacco (N benthamiana) leaves by Agrobacterium 658
infiltration (EHA105) The YFP fluorescence of transfected leaves was imaged 40 h 659
after infiltration by using a Nikon A1-SHS confocal laser scanning microscope The 660
excitation wavelength for YFP was 488 nm and fluorescence was detected at 520ndash661
540 nm Primers used are listed in Supplemental Table S6 662
663
Statistics 664
A Studentrsquos two-tailed t test ( plt005 plt001 and plt0001) was used to 665
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
24
determine significant differences between two groups in this study Microsoft Excel 666
was used to perform linear regressive analysis significant differences were 667
determined by SPSS Statistics 200 and scatter plots were prepared with Origin80 668
Least significant difference (LSD) at the 5 level was calculated using Microsoft 669
Excel Figures were prepared with Origin80 (Microcal Software Inc Northampton 670
MA USA) The online tool MetaboAnalyst 36 (httpwwwmetaboanalystca) was 671
used to analyse the transcript abundance of the AP2ERF genes 672
673
Accession numbers 674
Sequence data from this article have been deposited in GenBank under the accession 675
numbers MH332903-MH333022 for AP2ERF genes in Fragaria times ananassa and 676
MH333023 for FaMYB98 GenBank numbers for FaQR and FaOMT were 677
AY1588361 (Raab et al 2006) and AF2204912 (Wein et al 2002) 678
679
Supplemental Material 680
Supplemental Figure S1 Phylogenetic analysis of FaAP2ERF and Arabidopsis 681
AP2ERF proteins 682
Supplemental Figure S2 Analysis of FaAP2ERF gene expression patterns in 683
strawberry fruit during development and ripening 684
Supplemental Figure S3 Contents of furanones in fruit of strawberry cultivars 685
Supplemental Figure S4 Relative expression of FaERF9 in FaERF9-FaMYB98- 686
and FaERF9-overexpressing fruits 687
Supplemental Figure S5 Subcellular localization of FaMYB98 688
Supplemental Figure S6 The combined activation effects of FaERF9FaMYB98 on 689
the FaOMT promoter 690
Supplemental Figure S7 Relative expression of FaOMT in 691
FaERF9-overexpressing fruits 692
Supplemental Table S1 AP2ERF superfamily genes in Fragaria times ananassa 693
Supplemental Table S2 Classification of the AP2ERF superfamily members in 694
Fragaria times ananassa 695
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
25
Supplemental Table S3 Furanone content in FaERF9-FaMYB98- and 696
FaERF9-overexpressing fruits 697
Supplemental Table S4 Primers used for reverse transcription quantitative PCR 698
(RT-qPCR) 699
Supplemental Table S5 Primers used to amplify the full-length coding sequences of 700
AP2ERF genes and FaMYB98 in strawberry (Fragaria times ananassa) 701
Supplemental Table S6 Primers used for vector construction 702
703
Acknowledgments 704
This research was supported by the National Key Research and Development 705
Program (2016YFD0400101) the Project of the Science and Technology Department 706
of Zhejiang Province (2016C04001) and the 111 Project (B17039) 707
708
Figure legends 709
Figure 1 Changes in furanone content and furanone biosynthetic genes during 710
strawberry (Fragaria times ananassa Duch cv Yuexin) fruit development and ripening 711
A Fruits were collected at four ripening stages G (green stage) T (turning stage) IR 712
(intermediate red stage) R (full red stage) B Changes in the contents of furaneol 713
(HDMF) and mesifurane (DMMF) HDMF content was calculated using a standard 714
curve of HDMF while DMMF content was calculated with an internal standard as the 715
reference C Expression levels of FaQR and FaOMT The expression levels of each 716
gene were calculated relative to corresponding values in the basal section at the R 717
stage SEs were calculated from three replicates and LSD values represent the least 718
significant differences at p = 005 719
Figure 2 Regulatory effects of FaAP2ERF on the promoter of FaQR LUCREN 720
values of the empty vector on FaQR promoter were used as the calibrator set as 1 721
and SEs were calculated from five replicates statistical significance was determined 722
by Studentrsquos two-tailed t test ( plt0001) 723
Figure 3 Expression and the subcellular localization of FaERF9 A The expression 724
levels were calculated relative to the levels in the basal section at the R stage B 725
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
26
Subcellular localization analysis was performed in tobacco leaves The tobacco used 726
in the assay was stably transformed with a specific nucleus localized red fluorescence 727
protein construct and the red fluorescence indicates the nucleus-localized signal 728
(NLS) Scale bar = 25 microm SEs were calculated from three replicates 729
Figure 4 Transient overexpression of FaERF9 in strawberry fruit A Relative 730
expression of FaQR and FaERF9 in FaERF9-OX fruit 7 days after infiltration The 731
expression was calculated relative to the average value in control (SK) fruits B 732
HDMF and DMMF content in FaERF9-OX fruit The content of both furanones 733
were quantified using the peak area of the internal standard (2-octanol) as the 734
reference SEs were calculated from three replicates Statistical significance was 735
determined by Studentrsquos two-tailed t test ( plt005 plt001 plt0001) 736
Figure 5 Scatter plots of 11 strawberry cultivars A Linear regression analysis 737
between FaERF9 expression and FaQR expression B Linear regression analysis 738
between FaERF9 expression and furanone content The relative expression was 739
normalized to that of the housekeeping gene FaRIB413 and furanone content was 740
calculated with internal standard as the reference Significant differences were 741
determined by SPSS Statistics 200 742
Figure 6 Interactions of FaERF9 and FaMYB98 with the FaQR promoter A Yeast 743
one-hybrid analysis of the interaction of FaERF9 and FaQR promoter B Yeast 744
one-hybrid analysis of the interaction of FaMYB98 and FaQR promoter C 745
Regulatory effect of FaMYB98 on the FaQR promoter Auto-activation was tested on 746
SD-Ura (synthetically defined medium without uracil) in presence of Aureobasidin A 747
(AbA) and physical interaction was determined on SD-Leu (synthetically defined 748
medium without leucine) in presence of AbA LUCREN values of the empty vector 749
on FaQR promoter were used as the calibrator set as 1 and error bars were calculated 750
from five replicates Statistical significance was determined by Studentrsquos two-tailed t 751
test ( plt005 plt001 plt0001) 752
Figure 7 Electrophoretic mobility shift assay of FaMYB98 binding to FaQR 753
promoter A The probe sequence used for EMSA and mutated nucleotides are 754
indicated with lowercase letters B Purified DNA-binding domain of FaMYB98 755
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
27
protein and biotin-labelled DNA probe were mixed and analysed on 6 native 756
polyacrylamide gels and then photographed Presence or absence of specific probes is 757
marked by the symbol + or - 758
Figure 8 The combined activation effects of FaERF9FaMYB98 on the FaQR 759
promoter LUCREN values obtained with the empty vector and FaQR promoter were 760
used as the calibrator set as 1 and error bars were calculated from five replicates 761
Figure 9 Yeast two-hybrid analysis of the protein-protein interactions between 762
FaMYB98 and FaERF9 Positive interactions were determined by the growth of 763
yeast cells on selection plates Bait with pOST acted as positive controls and bait with 764
pPR3 as negative controls DDO synthetically defined medium without tryptophan 765
and leucine QDO synthetically defined medium without tryptophan leucine 766
histidine and adenine QDO+3AT QDO medium supplemented with 1 mM 767
3-aminotriazole 768
Figure 10 BiFC analysis of the protein-protein interactions between FaMYB98 and 769
FaERF9 The pairs of fusion proteins tested were FaMYB98-YFPN+FaERF9-YFPC 770
FaERF9-YFPN+FaMYB98-YFPC FaMYB98-YFPN+FaMYB98-YFPC and 771
FaERF9-YFPN+FaERF9-YFPC The other combinations were negative controls 772
The tobacco used in the assay was stably transformed with a specific 773
nucleus-localized red fluorescence protein construct and the red fluorescence 774
indicated the nucleus-localized signal (NLS) Fluorescence of the yellow fluorescence 775
protein (YFP) visualized the interaction in vivo Scale bar = 25 microm 776
777
Literature Cited 778
779
Agarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression 780
of PgDREB2A transcription factor enhances abiotic stress tolerance and activates 781
downstream stress-responsive genes Mol Biol Rep 37 1125-1135 782
Araguumlez I Osorio S Hoffmann T Rambla JL Medina-Escobar N Granell A 783
Botella MAacute Schwab W Valpuesta V (2013) Eugenol production in achenes and 784
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
28
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Plant Physiol 163 946-958 786
Carvalho RF Carvalho SD OrsquoGrady K Folta KM (2016) Agroinfiltration of 787
strawberry fruit mdash a powerful transient expression system for gene validation Curr 788
Plant Biol 6 19-37 789
Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic 790
(Amsterdam) 210 34-40 791
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating 792
RNA from pine trees Plant Mol Biol Rep 11 113-116 793
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC 794
Clark DG (2011) PhMYB4 fine-tunes the floral volatile signature of 795
Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143 796
Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz 797
EA Taylor MG Smits-Kroon MT Schuurink RC Haring MA Giovannoni J 798
Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic 799
pathway by ectopic expression of a MYB transcription factor in tomato fruit Plant 800
Cell 23 2738-2753 801
Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan 802
XW Yang ZY (2017) Differential responses of four biosynthetic pathways of 803
aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under 804
interaction of light and temperature Food Chem 221 356-364 805
Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of 806
differentially-expressed genes during somatic embryogenesis in Fragaria times 807
ananassa Duch lsquoBenihopprsquo J Hortic Sci Biotechnol 90 671-681 808
Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 809
transcriptionally regulates chilling-induced lignification of loquat fruit via physical 810
interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136 811
Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM 812
(2004) Functional interactions between a glutamine synthetase promoter and MYB 813
proteins Plant J 39 513-526 814
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29
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) 815
Sucrose nonfermenting1-related protein kinase26 an ortholog of open stomata1 is 816
a negative regulator of strawberry fruit development and ripening Plant Physiol 817
167 915-930 818
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene 819
expression in strawberry fruit (Fragaria times ananassa) by agroinfiltration a rapid 820
assay for gene function analysis Plant J 48 818-826 821
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of 822
selected aroma-active compounds in strawberries by headspace solid-phase 823
microextraction gas chromatography and correlation with sensory descriptive 824
analysis J Food Sci 72 S487-S496 825
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid 826
plays an important role in the regulation of strawberry fruit ripening Plant Physiol 827
157 188-199 828
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of 829
NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes BMC 830
Plant Biol 6 20 831
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN 832
(2005) MYB98 is required for pollen tube guidance and synergid cell differentiation 833
in Arabidopsis Plant Cell 17 2981-2992 834
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional 835
characterization of enone oxidoreductases from strawberry and tomato fruit J 836
Agric Food Chem 55 6705-6711 837
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You 838
J-S Rohloff J Randall SK Alsheikh M (2012) Proteomic study of 839
low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ 840
in cold tolerance Plant Physiol 159 1787-1805 841
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional 842
characterization of four APETALA2-family genes (RAP26 RAP26L DREB19 843
and DREB26) in Arabidopsis Plant Mol Biol 75 107-127 844
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
30
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon 845
J Gupta V (2013) An oxidoreductase from lsquoAlphonsorsquo mango catalyzing 846
biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494 847
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in 848
strawberries Z Lebensm-Unters Forsch 195 120-123 849
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X 850
(2015) Label-free quantitative proteomics to investigate strawberry fruit proteome 851
changes under controlled atmosphere and low temperature storage J Proteomics 852
120 44-57 853
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 854
cooperates with CitWRKY1 to participate in citric acid degradation via 855
up-regulation of CitAco3 J Exp Bot 68 3419-3426 856
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription 857
factor CitERF71 activates the terpene synthase gene CitTPS16 involved in the 858
synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938 859
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and 860
transcriptomic analysis of the AP2ERF superfamily in Vitis vinifera BMC 861
Genomics 11 719 862
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive 863
Factor (AP2ERF) transcription factors mediators of stress responses and 864
developmental programs New Phytol 199 639-649 865
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 866
interacting with EOBI negatively regulates fragrance biosynthesis in petunia 867
flowers New Phytol 215 1490-1502 868
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu 869
CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 in regulating 870
anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) 871
during anthocyanin biosynthesis Plant Cell Tissue Organ Cult 115 285-298 872
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
31
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao 873
CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphate signaling and 874
homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597 875
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC 876
Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL 877
Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor 878
regulates eugenol production in ripe strawberry fruit receptacles Plant Physiol 168 879
598-614 880
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics 881
and volatile constituents of strawberry (cv Cigaline) during maturation J Agric 882
Food Chem 52 1248-1254 883
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS 884
(2012) Ethylene-responsive transcription factors interact with promoters of ADH 885
and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 886
63 6393-6405 887
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM 888
Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-Franco A 889
Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific 890
transcription factor FaDOF2 regulates the production of eugenol in ripe fruit 891
receptacles J Exp Bot 68 4529-4543 892
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) 893
Comparison and verification of the genes involved in ethylene biosynthesis and 894
signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44 895
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the 896
ERF gene family in Arabidopsis and rice Plant Physiol 140 411-432 897
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in 898
sour cherry and strawberry and the heterologous expression of CBF1 in strawberry 899
J Am Soc Hortic Sci 127 489-494 900
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech 901
JC Ohme-Takagi M Regad F Bouzayen M (2012) Functional analysis and 902
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
32
binding affinity of tomato ethylene response factors provide insight on the 903
molecular bases of plant differential responses to ethylene BMC Plant Biol 12 190 904
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) 905
Methylpentoses are possible precursors of furanones in fruits Prikl Biokhim 906
Mikrobiol 28 123-127 907
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery 908
of synergid-expressed genes encoding filiform apparatus localized proteins Plant 909
Cell 19 2557-2568 910
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria 911
vesca L compared to those of cultivated berries Fragariatimes ananassa cv Senga 912
Sengana J Agric Food Chem 27 19-22 913
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W 914
Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of the strawberry 915
flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone 916
oxidoreductase Plant Cell 18 1023-1037 917
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L 918
Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim M Broun P Zhang 919
JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription 920
factors genome-wide comparative analysis among eukaryotes Science 290 921
2105-2110 922
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the 923
formation of 25-dimethyl-4-hydroxy-3(2H)-furanone in detached ripening 924
strawberry fruits J Agric Food Chem 46 1488-1493 925
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 926
25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in 927
strawberry fruits Phytochemistry 43 155-159 928
Schwab W (1998) Application of stable isotope ratio analysis explaining the 929
bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone in plants by a biological 930
maillard reaction J Agric Food Chem 46 2266ndash2269 931
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
33
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) 932
Molecules 18 6936-6951 933
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard 934
products Recent Res Dev Phytochem 1 643-673 935
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL 936
Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJ Sims CA 937
Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical 938
compositions a seasonal influence and effects on sensory perception PLoS One 9 939
e88446 940
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) 941
Identification phylogeny and transcript profiling of ERF family genes during 942
development and abiotic stress treatments in tomato Mol Genet Genomics 284 943
455-475 944
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) 945
CitAP210 activation of the terpene synthase CsTPS1 is associated with the 946
synthesis of (+)-valencene in lsquoNewhallrsquo orange J Exp Bot 67 4105-4115 947
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes 948
Dev Genes Evol 214 105-114 949
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K 950
Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the 951
key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151 952
Spitzer-Rimon B Farhi M Albo B Cnarsquoani A Ben Zvi MM Masci T Edelbaum 953
O Yu YX Shklarman E Ovadis M Vainstein A (2012) The R2R3-MYB-like 954
regulatory factor EOBI acting downstream of EOBII regulates scent production 955
by activating ODO1 and structural scent-related genes in petunia Plant Cell 24 956
5089-5105 957
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp 958
Bot 68 4407-4409 959
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla 960
JF Amaya I Giavalisco P Fernie AR Botella MA Valpuesta V (2015) Central 961
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
34
role of FaGAMYB in the transition of the strawberry receptacle from development 962
to ripening New Phytol 208 482-496 963
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 964
regulates fragrance biosynthesis in petunia flowers Plant Cell 17 1612-1624 965
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS 966
(2018) The potassium channel FaTPK1 plays a critical role in fruit quality 967
formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748 968
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) 969
Isolation cloning and expression of a multifunctional O-methyltransferase capable 970
of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma 971
compounds in strawberry fruits Plant J 31 755-765 972
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor 973
types their evolutionary origin and species distribution In A handbook of 974
transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular 975
Biochemistry 52 25-73 976
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of 977
odor (Buettner A Ed) Springer Cham 9-10 978
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS 979
(2014) Isolation classification and transcription profiles of the AP2ERF 980
transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271 981
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in 982
regulation of fruit quality Crit Rev Plant Sci 35 120-130 983
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ 984
Zhang SL Wu J (2017) Map-based cloning of the pear gene MYB114 identifies an 985
interaction with other transcription factors to coordinately regulate fruit 986
anthocyanin biosynthesis Plant J 92 437-451 987
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes 988
involved in regulating fruit ripening Plant Physiol 153 1280-1292 989
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
35
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) 990
Expression of ethylene response genes during persimmon fruit astringency removal 991
Planta 235 895-906 992
Zabetakis I Gramshaw JW Robinson DS (1999) 993
25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis and 994
biosynthesis-a review Food Chem 65 139-151 995
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci 996
Food Agric 74 421-434 997
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 998
an AP2ERF gene is a novel regulator of fruit lignification induced by chilling 999
injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1000
1325-1334 1001
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation 1002
classification and transcription profiles of the Ethylene Response Factors (ERFs) in 1003
ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215 1004
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML 1005
(2012) Genome-wide analysis of the AP2ERF superfamily in peach (Prunus 1006
persica) Genet Mol Res 11 4788-4809 1007
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and 1008
expression analysis of a CRTDRE-binding factor gene FaCBF1 from Fragaria times 1009
ananassa Acta Hortic 41 240-248 1010
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The 1011
Arabidopsis AP2ERF transcription factor RAP26 participates in ABA salt and 1012
osmotic stress responses Gene 457 1-12 1013
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B 1014
Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) Genome-wide 1015
analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic 1016
(Amsterdam) 123 73-81 1017
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF 1018
Valpuesta V Botella MA Granell A Amaya I (2012) Genetic analysis of 1019
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
36
strawberry fruit aroma and identification of O-methyltransferase FaOMT as the 1020
locus controlling natural variation in mesifurane content Plant Physiol 159 1021
851-870 1022
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Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) Isolation cloning and expression of a multifunctional O- wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma compounds in strawberry fruitsPlant J 31 755-765
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Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS (2014) Isolation classification and transcription profiles ofthe AP2ERF transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in regulation of fruit quality Crit Rev Plant Sci 35 120-130
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ Zhang SL Wu J (2017) Map-based cloning of the pear geneMYB114 identifies an interaction with other transcription factors to coordinately regulate fruit anthocyanin biosynthesis Plant J 92437-451
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes involved in regulating fruit ripening Plant Physiol 1531280-1292
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) Expression of ethylene response genes during persimmonfruit astringency removal Planta 235 895-906
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zabetakis I Gramshaw JW Robinson DS (1999) 25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis andbiosynthesis-a review Food Chem 65 139-151
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci Food Agric 74 421-434Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 an AP2ERF gene is a novel regulator of fruit lignificationinduced by chilling injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1325-1334
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation classification and transcription profiles of the Ethylene ResponseFactors (ERFs) in ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML (2012) Genome-wide analysis of the AP2ERF superfamily inpeach (Prunus persica) Genet Mol Res 11 4788-4809
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and expression analysis of a CRTDRE-binding factor gene FaCBF1from Fragaria times ananassa Acta Hortic 41 240-248
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The Arabidopsis AP2ERF transcription factor RAP26 participatesin ABA salt and osmotic stress responses Gene 457 1-12
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Genome-wide analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic (Amsterdam) 123 73-81Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF Valpuesta V Botella MA Granell A Amaya I (2012) Geneticanalysis of strawberry fruit aroma and identification of O-methyltransferase FaOMT as the locus controlling natural variation inmesifurane content Plant Physiol 159 851-870
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
20
FaMYB98 was obtained by yeast one-hybrid screening sequencing and the full-length 546
sequences were predicted by BLAST Primers were designed (listed in Supplemental 547
Table S5) to amplify the full-length coding sequence 548
549
The promoter of FaQR was cloned by Genome Walking as previously described (Yin 550
et al 2010) and conserved cis-element motifs in the promoter were manually 551
searched 552
553
Conserved domains within the FaAP2ERF proteins and FaMYB98 were analysed by 554
CD-search (httpswwwncbinlmnihgovStructurecddwrpsbcgi) and cellular 555
locations of proteins including FaERF9 and FaMYB98 were predicted with the 556
WoLF PSORT program (httpswwwgenscriptcomwolf-psorthtml) 557
558
Dual-Luciferase Assays 559
In accordance with a previous protocol (Yin et al 2010) the full-length cDNAs of 560
FaAP2ERF or FaMYB98 transcription factors were cloned into pGreen II 0029 561
62-SK vector and the promoter of FaQR was cloned into pGreen II 0800-LUC vector 562
A luciferase gene from Renillia (REN) driven by a 35S promoter in the LUC vector 563
acted as a positive control The above constructs were transiently expressed in 564
Nicotiana benthamiana leaves by Agrobacterium-mediated infiltration (strain 565
GV3101) and the activity of the TFs on the promoter was measured on the third day 566
after infiltration indicated by the ratio of enzyme activities of firefly luciferase (LUC) 567
and renilla luciferase (REN) using a Modulus Luminometer (Promega Madison WI 568
USA) To determine the activity of a specific transcription factor towards the 569
promoter we mixed the Agrobacterium culture with 1 mL of TF and 100 μL of 570
promoter and the LUCREN value of the empty vector SK on the promoter was set as 571
1 as a calibrator To test the combined effect of two transcription factors on the 572
promoter to the Agrobacterium culture mixture we added 05 mL of each TF and 100 573
μL of promoter the effect of the mixtures that contained each transcription factor (05 574
mL) and empty vector SK (05 mL) was also tested on the promoter as a control 575
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
21
576
Subcellular localization analysis 577
35S-FaERF9-GFP and 35S-FaMYB98-GFP were transiently expressed in tobacco (N 578
benthamiana) leaves by Agrobacterium infiltration (EHA105) using the same method 579
as described in the dual-luciferase assay above The transiently infected leaves were 580
imaged on the third day after infiltration using a Nikon A1-SHS confocal laser 581
scanning microscope The excitation wavelength for GFP fluorescence was 488 nm 582
and fluorescence was detected at 490ndash520 nm The primers used for GFP construction 583
are listed in Supplemental Table S6 584
585
Transient overexpression in strawberry fruit 586
Transient overexpression of FaERF9 and an overexpression binary vector (pGreen II 587
0029 62-SK-FaERF9-FaMYB98) were performed in strawberry fruit using the 588
FaERF9-SK construct described above for the dual-luciferase assays and the binary 589
vector constructed according to Liu et al 2013 The transfection of fruit was carried 590
out at the G stage (Hoffmann et al 2006) The FaERF9-SK construct and binary 591
vector were individually electroporated into Agrobacterium tumefaciens GV3101 and 592
the Agrobacterium culture suspended in infiltration buffer was infiltrated into the 593
whole fruit using a syringe As a control treatment fruits were infiltrated with 594
Agrobacterium carrying an empty vector SK under the same transfection conditions 595
Fruits were left attached to the plants and harvested on the seventh day after 596
infiltration Fruits of three biological replicates were sampled for further analysis 597
598
Yeast one-hybrid assay 599
In order to identify proteins that bind to the FaQR promoter the Matchmaker Gold 600
Yeast One-hybrid Library Screening System (Clontech USA) was used The sequence 601
of the FaQR promoter was cloned into the pAbAi vector and the construct was 602
integrated into the genome of the Y1HGold yeast strain A mixture of total RNA from 603
strawberry fruit at four stages (G T IR R) was used to construct the prey cDNA 604
library (TaKaRa) The background AbAr expression of Y1HGold FaQR-pAbAi strain 605
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
22
was tested according to the system user manual and then screening for protein-DNA 606
interactions was carried out Furthermore the full length of each transcription factor 607
was separately cloned into pGADT7 AD vector to confirm the screening results The 608
relationship between FaERF9 and FaQR promoter was also examined individually 609
Primers used in this assay are listed in Supplemental Table S6 610
611
Expression and purification of FaMYB98 recombinant protein 612
A 405-bp region spanning the DNA-binding domain of FaMYB98 was amplified 613
from FaMYB98 cDNA and cloned into a pET6timesHN vector (Clontech Palo CA USA) 614
to generate the recombinant N-terminal His-tagged protein the primers used are listed 615
in Supplemental Table S6 The resulting construct was sequenced and introduced into 616
Escherichia coli strain Rosetta 2(DE3)pLysS (Novagen) Ten millilitres of the 617
overnight culture was combined with 500 mL of an LB liquid medium (100 μgmL 618
ampicillin and 34 μgmL chloramphenicol) as described (Li et al 2017) Isopropyl 619
β-D-1-thiogalactopyranoside (IPTG) was added to a final concentration of 1 mM and 620
the bacterial culture was incubated at 18degC at 150 rpm for 18 h Then the cells were 621
harvested using a centrifuge and resuspended in 1times PBS buffer (Sangon Biotech) 622
after which they were disrupted by sonication and the supernatant was purified using 623
a HisTALONTM Gravity Column (Clontech) according to the user manual The PD-10 624
Desalting column (GE Healthcare) was then used for buffer change and sample 625
clean-up of proteins according to the gravity protocol SDS-PAGE was performed and 626
the protein was visualized using Coomassie brilliant blue 627
628
Electrophoretic mobility shift assay (EMSA) 629
A Lightshift Chemiluminescent EMSA kit (Thermo) was used to perform EMSA 630
experiments according to the manufacturerrsquos instructions Single-strand 631
oligonucleotides were synthesized and biotinylated by GeneBio Biotech (Hangzhou 632
China) The details of the EMSA assay are provided in Ge et al (2017) The probes 633
used for EMSAs are listed in Supplemental Table S6 634
635
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
23
636
Yeast two-hybrid assay 637
The DUALhunter system (Dualsystems Biotech Switzerland) was used to investigate 638
the interaction between FaERF9 and FaMYB98 Full-length coding sequences of 639
FaERF9 and FaMYB98 were respectively cloned into pDHB1 bait vector and 640
pPR3-N prey vector sequences were verified and the bait plasmid was 641
co-transformed with prey plasmid into NMY51 in the combinations below 642
FaMYB98-pDHB1pPR3-N FaMYB98-pDHB1FaERF9-pPR3-N 643
FaMYB98-pDHB1pOst1-NubI FaERF9-pDHB1pPR3-N 644
FaERF9-pDHB1FaMYB98-pPR3-N and FaERF9-pDHB1pOst1-NubI (Li et al 645
2017) Transformed cells were spread onto the following plates DDO (SD 646
medium-Trp-Leu) QDO (SD medium-Trp-Leu-His-Ade) and QDO+3-AT (QDO 647
medium supplemented with 1 mM 3-amino-124-triazole) The control plasmid 648
pOst1-NubI was used to determine whether the bait was functional the pPR3-N prey 649
vector plasmid was used to test whether the bait displayed non-specific background 650
and positive interactions were indicated by the growth of yeast on QDO and 651
QDO+3-AT plates The Primers used in the DUALhunter assay are listed in 652
Supplemental Table S6 653
654
Bimolecular fluorescence complementation (BiFC) assays 655
Full-length FaERF9 and FaMYB98 respectively were cloned into sequences 656
encoding the N- and C- fragments of YFP protein (Lv et al 2014) All constructs 657
were transiently expressed in tobacco (N benthamiana) leaves by Agrobacterium 658
infiltration (EHA105) The YFP fluorescence of transfected leaves was imaged 40 h 659
after infiltration by using a Nikon A1-SHS confocal laser scanning microscope The 660
excitation wavelength for YFP was 488 nm and fluorescence was detected at 520ndash661
540 nm Primers used are listed in Supplemental Table S6 662
663
Statistics 664
A Studentrsquos two-tailed t test ( plt005 plt001 and plt0001) was used to 665
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
24
determine significant differences between two groups in this study Microsoft Excel 666
was used to perform linear regressive analysis significant differences were 667
determined by SPSS Statistics 200 and scatter plots were prepared with Origin80 668
Least significant difference (LSD) at the 5 level was calculated using Microsoft 669
Excel Figures were prepared with Origin80 (Microcal Software Inc Northampton 670
MA USA) The online tool MetaboAnalyst 36 (httpwwwmetaboanalystca) was 671
used to analyse the transcript abundance of the AP2ERF genes 672
673
Accession numbers 674
Sequence data from this article have been deposited in GenBank under the accession 675
numbers MH332903-MH333022 for AP2ERF genes in Fragaria times ananassa and 676
MH333023 for FaMYB98 GenBank numbers for FaQR and FaOMT were 677
AY1588361 (Raab et al 2006) and AF2204912 (Wein et al 2002) 678
679
Supplemental Material 680
Supplemental Figure S1 Phylogenetic analysis of FaAP2ERF and Arabidopsis 681
AP2ERF proteins 682
Supplemental Figure S2 Analysis of FaAP2ERF gene expression patterns in 683
strawberry fruit during development and ripening 684
Supplemental Figure S3 Contents of furanones in fruit of strawberry cultivars 685
Supplemental Figure S4 Relative expression of FaERF9 in FaERF9-FaMYB98- 686
and FaERF9-overexpressing fruits 687
Supplemental Figure S5 Subcellular localization of FaMYB98 688
Supplemental Figure S6 The combined activation effects of FaERF9FaMYB98 on 689
the FaOMT promoter 690
Supplemental Figure S7 Relative expression of FaOMT in 691
FaERF9-overexpressing fruits 692
Supplemental Table S1 AP2ERF superfamily genes in Fragaria times ananassa 693
Supplemental Table S2 Classification of the AP2ERF superfamily members in 694
Fragaria times ananassa 695
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
25
Supplemental Table S3 Furanone content in FaERF9-FaMYB98- and 696
FaERF9-overexpressing fruits 697
Supplemental Table S4 Primers used for reverse transcription quantitative PCR 698
(RT-qPCR) 699
Supplemental Table S5 Primers used to amplify the full-length coding sequences of 700
AP2ERF genes and FaMYB98 in strawberry (Fragaria times ananassa) 701
Supplemental Table S6 Primers used for vector construction 702
703
Acknowledgments 704
This research was supported by the National Key Research and Development 705
Program (2016YFD0400101) the Project of the Science and Technology Department 706
of Zhejiang Province (2016C04001) and the 111 Project (B17039) 707
708
Figure legends 709
Figure 1 Changes in furanone content and furanone biosynthetic genes during 710
strawberry (Fragaria times ananassa Duch cv Yuexin) fruit development and ripening 711
A Fruits were collected at four ripening stages G (green stage) T (turning stage) IR 712
(intermediate red stage) R (full red stage) B Changes in the contents of furaneol 713
(HDMF) and mesifurane (DMMF) HDMF content was calculated using a standard 714
curve of HDMF while DMMF content was calculated with an internal standard as the 715
reference C Expression levels of FaQR and FaOMT The expression levels of each 716
gene were calculated relative to corresponding values in the basal section at the R 717
stage SEs were calculated from three replicates and LSD values represent the least 718
significant differences at p = 005 719
Figure 2 Regulatory effects of FaAP2ERF on the promoter of FaQR LUCREN 720
values of the empty vector on FaQR promoter were used as the calibrator set as 1 721
and SEs were calculated from five replicates statistical significance was determined 722
by Studentrsquos two-tailed t test ( plt0001) 723
Figure 3 Expression and the subcellular localization of FaERF9 A The expression 724
levels were calculated relative to the levels in the basal section at the R stage B 725
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
26
Subcellular localization analysis was performed in tobacco leaves The tobacco used 726
in the assay was stably transformed with a specific nucleus localized red fluorescence 727
protein construct and the red fluorescence indicates the nucleus-localized signal 728
(NLS) Scale bar = 25 microm SEs were calculated from three replicates 729
Figure 4 Transient overexpression of FaERF9 in strawberry fruit A Relative 730
expression of FaQR and FaERF9 in FaERF9-OX fruit 7 days after infiltration The 731
expression was calculated relative to the average value in control (SK) fruits B 732
HDMF and DMMF content in FaERF9-OX fruit The content of both furanones 733
were quantified using the peak area of the internal standard (2-octanol) as the 734
reference SEs were calculated from three replicates Statistical significance was 735
determined by Studentrsquos two-tailed t test ( plt005 plt001 plt0001) 736
Figure 5 Scatter plots of 11 strawberry cultivars A Linear regression analysis 737
between FaERF9 expression and FaQR expression B Linear regression analysis 738
between FaERF9 expression and furanone content The relative expression was 739
normalized to that of the housekeeping gene FaRIB413 and furanone content was 740
calculated with internal standard as the reference Significant differences were 741
determined by SPSS Statistics 200 742
Figure 6 Interactions of FaERF9 and FaMYB98 with the FaQR promoter A Yeast 743
one-hybrid analysis of the interaction of FaERF9 and FaQR promoter B Yeast 744
one-hybrid analysis of the interaction of FaMYB98 and FaQR promoter C 745
Regulatory effect of FaMYB98 on the FaQR promoter Auto-activation was tested on 746
SD-Ura (synthetically defined medium without uracil) in presence of Aureobasidin A 747
(AbA) and physical interaction was determined on SD-Leu (synthetically defined 748
medium without leucine) in presence of AbA LUCREN values of the empty vector 749
on FaQR promoter were used as the calibrator set as 1 and error bars were calculated 750
from five replicates Statistical significance was determined by Studentrsquos two-tailed t 751
test ( plt005 plt001 plt0001) 752
Figure 7 Electrophoretic mobility shift assay of FaMYB98 binding to FaQR 753
promoter A The probe sequence used for EMSA and mutated nucleotides are 754
indicated with lowercase letters B Purified DNA-binding domain of FaMYB98 755
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
27
protein and biotin-labelled DNA probe were mixed and analysed on 6 native 756
polyacrylamide gels and then photographed Presence or absence of specific probes is 757
marked by the symbol + or - 758
Figure 8 The combined activation effects of FaERF9FaMYB98 on the FaQR 759
promoter LUCREN values obtained with the empty vector and FaQR promoter were 760
used as the calibrator set as 1 and error bars were calculated from five replicates 761
Figure 9 Yeast two-hybrid analysis of the protein-protein interactions between 762
FaMYB98 and FaERF9 Positive interactions were determined by the growth of 763
yeast cells on selection plates Bait with pOST acted as positive controls and bait with 764
pPR3 as negative controls DDO synthetically defined medium without tryptophan 765
and leucine QDO synthetically defined medium without tryptophan leucine 766
histidine and adenine QDO+3AT QDO medium supplemented with 1 mM 767
3-aminotriazole 768
Figure 10 BiFC analysis of the protein-protein interactions between FaMYB98 and 769
FaERF9 The pairs of fusion proteins tested were FaMYB98-YFPN+FaERF9-YFPC 770
FaERF9-YFPN+FaMYB98-YFPC FaMYB98-YFPN+FaMYB98-YFPC and 771
FaERF9-YFPN+FaERF9-YFPC The other combinations were negative controls 772
The tobacco used in the assay was stably transformed with a specific 773
nucleus-localized red fluorescence protein construct and the red fluorescence 774
indicated the nucleus-localized signal (NLS) Fluorescence of the yellow fluorescence 775
protein (YFP) visualized the interaction in vivo Scale bar = 25 microm 776
777
Literature Cited 778
779
Agarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression 780
of PgDREB2A transcription factor enhances abiotic stress tolerance and activates 781
downstream stress-responsive genes Mol Biol Rep 37 1125-1135 782
Araguumlez I Osorio S Hoffmann T Rambla JL Medina-Escobar N Granell A 783
Botella MAacute Schwab W Valpuesta V (2013) Eugenol production in achenes and 784
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
28
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Plant Physiol 163 946-958 786
Carvalho RF Carvalho SD OrsquoGrady K Folta KM (2016) Agroinfiltration of 787
strawberry fruit mdash a powerful transient expression system for gene validation Curr 788
Plant Biol 6 19-37 789
Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic 790
(Amsterdam) 210 34-40 791
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating 792
RNA from pine trees Plant Mol Biol Rep 11 113-116 793
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC 794
Clark DG (2011) PhMYB4 fine-tunes the floral volatile signature of 795
Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143 796
Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz 797
EA Taylor MG Smits-Kroon MT Schuurink RC Haring MA Giovannoni J 798
Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic 799
pathway by ectopic expression of a MYB transcription factor in tomato fruit Plant 800
Cell 23 2738-2753 801
Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan 802
XW Yang ZY (2017) Differential responses of four biosynthetic pathways of 803
aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under 804
interaction of light and temperature Food Chem 221 356-364 805
Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of 806
differentially-expressed genes during somatic embryogenesis in Fragaria times 807
ananassa Duch lsquoBenihopprsquo J Hortic Sci Biotechnol 90 671-681 808
Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 809
transcriptionally regulates chilling-induced lignification of loquat fruit via physical 810
interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136 811
Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM 812
(2004) Functional interactions between a glutamine synthetase promoter and MYB 813
proteins Plant J 39 513-526 814
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29
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) 815
Sucrose nonfermenting1-related protein kinase26 an ortholog of open stomata1 is 816
a negative regulator of strawberry fruit development and ripening Plant Physiol 817
167 915-930 818
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene 819
expression in strawberry fruit (Fragaria times ananassa) by agroinfiltration a rapid 820
assay for gene function analysis Plant J 48 818-826 821
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of 822
selected aroma-active compounds in strawberries by headspace solid-phase 823
microextraction gas chromatography and correlation with sensory descriptive 824
analysis J Food Sci 72 S487-S496 825
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid 826
plays an important role in the regulation of strawberry fruit ripening Plant Physiol 827
157 188-199 828
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of 829
NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes BMC 830
Plant Biol 6 20 831
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN 832
(2005) MYB98 is required for pollen tube guidance and synergid cell differentiation 833
in Arabidopsis Plant Cell 17 2981-2992 834
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional 835
characterization of enone oxidoreductases from strawberry and tomato fruit J 836
Agric Food Chem 55 6705-6711 837
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You 838
J-S Rohloff J Randall SK Alsheikh M (2012) Proteomic study of 839
low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ 840
in cold tolerance Plant Physiol 159 1787-1805 841
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional 842
characterization of four APETALA2-family genes (RAP26 RAP26L DREB19 843
and DREB26) in Arabidopsis Plant Mol Biol 75 107-127 844
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
30
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon 845
J Gupta V (2013) An oxidoreductase from lsquoAlphonsorsquo mango catalyzing 846
biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494 847
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in 848
strawberries Z Lebensm-Unters Forsch 195 120-123 849
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X 850
(2015) Label-free quantitative proteomics to investigate strawberry fruit proteome 851
changes under controlled atmosphere and low temperature storage J Proteomics 852
120 44-57 853
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 854
cooperates with CitWRKY1 to participate in citric acid degradation via 855
up-regulation of CitAco3 J Exp Bot 68 3419-3426 856
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription 857
factor CitERF71 activates the terpene synthase gene CitTPS16 involved in the 858
synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938 859
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and 860
transcriptomic analysis of the AP2ERF superfamily in Vitis vinifera BMC 861
Genomics 11 719 862
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive 863
Factor (AP2ERF) transcription factors mediators of stress responses and 864
developmental programs New Phytol 199 639-649 865
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 866
interacting with EOBI negatively regulates fragrance biosynthesis in petunia 867
flowers New Phytol 215 1490-1502 868
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu 869
CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 in regulating 870
anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) 871
during anthocyanin biosynthesis Plant Cell Tissue Organ Cult 115 285-298 872
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
31
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao 873
CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphate signaling and 874
homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597 875
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC 876
Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL 877
Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor 878
regulates eugenol production in ripe strawberry fruit receptacles Plant Physiol 168 879
598-614 880
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics 881
and volatile constituents of strawberry (cv Cigaline) during maturation J Agric 882
Food Chem 52 1248-1254 883
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS 884
(2012) Ethylene-responsive transcription factors interact with promoters of ADH 885
and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 886
63 6393-6405 887
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM 888
Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-Franco A 889
Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific 890
transcription factor FaDOF2 regulates the production of eugenol in ripe fruit 891
receptacles J Exp Bot 68 4529-4543 892
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) 893
Comparison and verification of the genes involved in ethylene biosynthesis and 894
signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44 895
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the 896
ERF gene family in Arabidopsis and rice Plant Physiol 140 411-432 897
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in 898
sour cherry and strawberry and the heterologous expression of CBF1 in strawberry 899
J Am Soc Hortic Sci 127 489-494 900
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech 901
JC Ohme-Takagi M Regad F Bouzayen M (2012) Functional analysis and 902
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32
binding affinity of tomato ethylene response factors provide insight on the 903
molecular bases of plant differential responses to ethylene BMC Plant Biol 12 190 904
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) 905
Methylpentoses are possible precursors of furanones in fruits Prikl Biokhim 906
Mikrobiol 28 123-127 907
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery 908
of synergid-expressed genes encoding filiform apparatus localized proteins Plant 909
Cell 19 2557-2568 910
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria 911
vesca L compared to those of cultivated berries Fragariatimes ananassa cv Senga 912
Sengana J Agric Food Chem 27 19-22 913
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W 914
Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of the strawberry 915
flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone 916
oxidoreductase Plant Cell 18 1023-1037 917
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L 918
Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim M Broun P Zhang 919
JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription 920
factors genome-wide comparative analysis among eukaryotes Science 290 921
2105-2110 922
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the 923
formation of 25-dimethyl-4-hydroxy-3(2H)-furanone in detached ripening 924
strawberry fruits J Agric Food Chem 46 1488-1493 925
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 926
25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in 927
strawberry fruits Phytochemistry 43 155-159 928
Schwab W (1998) Application of stable isotope ratio analysis explaining the 929
bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone in plants by a biological 930
maillard reaction J Agric Food Chem 46 2266ndash2269 931
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
33
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) 932
Molecules 18 6936-6951 933
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard 934
products Recent Res Dev Phytochem 1 643-673 935
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL 936
Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJ Sims CA 937
Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical 938
compositions a seasonal influence and effects on sensory perception PLoS One 9 939
e88446 940
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) 941
Identification phylogeny and transcript profiling of ERF family genes during 942
development and abiotic stress treatments in tomato Mol Genet Genomics 284 943
455-475 944
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) 945
CitAP210 activation of the terpene synthase CsTPS1 is associated with the 946
synthesis of (+)-valencene in lsquoNewhallrsquo orange J Exp Bot 67 4105-4115 947
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes 948
Dev Genes Evol 214 105-114 949
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K 950
Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the 951
key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151 952
Spitzer-Rimon B Farhi M Albo B Cnarsquoani A Ben Zvi MM Masci T Edelbaum 953
O Yu YX Shklarman E Ovadis M Vainstein A (2012) The R2R3-MYB-like 954
regulatory factor EOBI acting downstream of EOBII regulates scent production 955
by activating ODO1 and structural scent-related genes in petunia Plant Cell 24 956
5089-5105 957
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp 958
Bot 68 4407-4409 959
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla 960
JF Amaya I Giavalisco P Fernie AR Botella MA Valpuesta V (2015) Central 961
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
34
role of FaGAMYB in the transition of the strawberry receptacle from development 962
to ripening New Phytol 208 482-496 963
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 964
regulates fragrance biosynthesis in petunia flowers Plant Cell 17 1612-1624 965
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS 966
(2018) The potassium channel FaTPK1 plays a critical role in fruit quality 967
formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748 968
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) 969
Isolation cloning and expression of a multifunctional O-methyltransferase capable 970
of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma 971
compounds in strawberry fruits Plant J 31 755-765 972
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor 973
types their evolutionary origin and species distribution In A handbook of 974
transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular 975
Biochemistry 52 25-73 976
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of 977
odor (Buettner A Ed) Springer Cham 9-10 978
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS 979
(2014) Isolation classification and transcription profiles of the AP2ERF 980
transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271 981
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in 982
regulation of fruit quality Crit Rev Plant Sci 35 120-130 983
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ 984
Zhang SL Wu J (2017) Map-based cloning of the pear gene MYB114 identifies an 985
interaction with other transcription factors to coordinately regulate fruit 986
anthocyanin biosynthesis Plant J 92 437-451 987
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes 988
involved in regulating fruit ripening Plant Physiol 153 1280-1292 989
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
35
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) 990
Expression of ethylene response genes during persimmon fruit astringency removal 991
Planta 235 895-906 992
Zabetakis I Gramshaw JW Robinson DS (1999) 993
25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis and 994
biosynthesis-a review Food Chem 65 139-151 995
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci 996
Food Agric 74 421-434 997
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 998
an AP2ERF gene is a novel regulator of fruit lignification induced by chilling 999
injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1000
1325-1334 1001
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation 1002
classification and transcription profiles of the Ethylene Response Factors (ERFs) in 1003
ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215 1004
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML 1005
(2012) Genome-wide analysis of the AP2ERF superfamily in peach (Prunus 1006
persica) Genet Mol Res 11 4788-4809 1007
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and 1008
expression analysis of a CRTDRE-binding factor gene FaCBF1 from Fragaria times 1009
ananassa Acta Hortic 41 240-248 1010
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The 1011
Arabidopsis AP2ERF transcription factor RAP26 participates in ABA salt and 1012
osmotic stress responses Gene 457 1-12 1013
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B 1014
Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) Genome-wide 1015
analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic 1016
(Amsterdam) 123 73-81 1017
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF 1018
Valpuesta V Botella MA Granell A Amaya I (2012) Genetic analysis of 1019
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
36
strawberry fruit aroma and identification of O-methyltransferase FaOMT as the 1020
locus controlling natural variation in mesifurane content Plant Physiol 159 1021
851-870 1022
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methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma compounds in strawberry fruitsPlant J 31 755-765
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Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS (2014) Isolation classification and transcription profiles ofthe AP2ERF transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in regulation of fruit quality Crit Rev Plant Sci 35 120-130
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
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Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes involved in regulating fruit ripening Plant Physiol 1531280-1292
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) Expression of ethylene response genes during persimmonfruit astringency removal Planta 235 895-906
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zabetakis I Gramshaw JW Robinson DS (1999) 25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis andbiosynthesis-a review Food Chem 65 139-151
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci Food Agric 74 421-434Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 an AP2ERF gene is a novel regulator of fruit lignificationinduced by chilling injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1325-1334
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation classification and transcription profiles of the Ethylene ResponseFactors (ERFs) in ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML (2012) Genome-wide analysis of the AP2ERF superfamily inpeach (Prunus persica) Genet Mol Res 11 4788-4809
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and expression analysis of a CRTDRE-binding factor gene FaCBF1from Fragaria times ananassa Acta Hortic 41 240-248
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The Arabidopsis AP2ERF transcription factor RAP26 participatesin ABA salt and osmotic stress responses Gene 457 1-12
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Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Genome-wide analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic (Amsterdam) 123 73-81Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF Valpuesta V Botella MA Granell A Amaya I (2012) Geneticanalysis of strawberry fruit aroma and identification of O-methyltransferase FaOMT as the locus controlling natural variation inmesifurane content Plant Physiol 159 851-870
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
21
576
Subcellular localization analysis 577
35S-FaERF9-GFP and 35S-FaMYB98-GFP were transiently expressed in tobacco (N 578
benthamiana) leaves by Agrobacterium infiltration (EHA105) using the same method 579
as described in the dual-luciferase assay above The transiently infected leaves were 580
imaged on the third day after infiltration using a Nikon A1-SHS confocal laser 581
scanning microscope The excitation wavelength for GFP fluorescence was 488 nm 582
and fluorescence was detected at 490ndash520 nm The primers used for GFP construction 583
are listed in Supplemental Table S6 584
585
Transient overexpression in strawberry fruit 586
Transient overexpression of FaERF9 and an overexpression binary vector (pGreen II 587
0029 62-SK-FaERF9-FaMYB98) were performed in strawberry fruit using the 588
FaERF9-SK construct described above for the dual-luciferase assays and the binary 589
vector constructed according to Liu et al 2013 The transfection of fruit was carried 590
out at the G stage (Hoffmann et al 2006) The FaERF9-SK construct and binary 591
vector were individually electroporated into Agrobacterium tumefaciens GV3101 and 592
the Agrobacterium culture suspended in infiltration buffer was infiltrated into the 593
whole fruit using a syringe As a control treatment fruits were infiltrated with 594
Agrobacterium carrying an empty vector SK under the same transfection conditions 595
Fruits were left attached to the plants and harvested on the seventh day after 596
infiltration Fruits of three biological replicates were sampled for further analysis 597
598
Yeast one-hybrid assay 599
In order to identify proteins that bind to the FaQR promoter the Matchmaker Gold 600
Yeast One-hybrid Library Screening System (Clontech USA) was used The sequence 601
of the FaQR promoter was cloned into the pAbAi vector and the construct was 602
integrated into the genome of the Y1HGold yeast strain A mixture of total RNA from 603
strawberry fruit at four stages (G T IR R) was used to construct the prey cDNA 604
library (TaKaRa) The background AbAr expression of Y1HGold FaQR-pAbAi strain 605
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
22
was tested according to the system user manual and then screening for protein-DNA 606
interactions was carried out Furthermore the full length of each transcription factor 607
was separately cloned into pGADT7 AD vector to confirm the screening results The 608
relationship between FaERF9 and FaQR promoter was also examined individually 609
Primers used in this assay are listed in Supplemental Table S6 610
611
Expression and purification of FaMYB98 recombinant protein 612
A 405-bp region spanning the DNA-binding domain of FaMYB98 was amplified 613
from FaMYB98 cDNA and cloned into a pET6timesHN vector (Clontech Palo CA USA) 614
to generate the recombinant N-terminal His-tagged protein the primers used are listed 615
in Supplemental Table S6 The resulting construct was sequenced and introduced into 616
Escherichia coli strain Rosetta 2(DE3)pLysS (Novagen) Ten millilitres of the 617
overnight culture was combined with 500 mL of an LB liquid medium (100 μgmL 618
ampicillin and 34 μgmL chloramphenicol) as described (Li et al 2017) Isopropyl 619
β-D-1-thiogalactopyranoside (IPTG) was added to a final concentration of 1 mM and 620
the bacterial culture was incubated at 18degC at 150 rpm for 18 h Then the cells were 621
harvested using a centrifuge and resuspended in 1times PBS buffer (Sangon Biotech) 622
after which they were disrupted by sonication and the supernatant was purified using 623
a HisTALONTM Gravity Column (Clontech) according to the user manual The PD-10 624
Desalting column (GE Healthcare) was then used for buffer change and sample 625
clean-up of proteins according to the gravity protocol SDS-PAGE was performed and 626
the protein was visualized using Coomassie brilliant blue 627
628
Electrophoretic mobility shift assay (EMSA) 629
A Lightshift Chemiluminescent EMSA kit (Thermo) was used to perform EMSA 630
experiments according to the manufacturerrsquos instructions Single-strand 631
oligonucleotides were synthesized and biotinylated by GeneBio Biotech (Hangzhou 632
China) The details of the EMSA assay are provided in Ge et al (2017) The probes 633
used for EMSAs are listed in Supplemental Table S6 634
635
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
23
636
Yeast two-hybrid assay 637
The DUALhunter system (Dualsystems Biotech Switzerland) was used to investigate 638
the interaction between FaERF9 and FaMYB98 Full-length coding sequences of 639
FaERF9 and FaMYB98 were respectively cloned into pDHB1 bait vector and 640
pPR3-N prey vector sequences were verified and the bait plasmid was 641
co-transformed with prey plasmid into NMY51 in the combinations below 642
FaMYB98-pDHB1pPR3-N FaMYB98-pDHB1FaERF9-pPR3-N 643
FaMYB98-pDHB1pOst1-NubI FaERF9-pDHB1pPR3-N 644
FaERF9-pDHB1FaMYB98-pPR3-N and FaERF9-pDHB1pOst1-NubI (Li et al 645
2017) Transformed cells were spread onto the following plates DDO (SD 646
medium-Trp-Leu) QDO (SD medium-Trp-Leu-His-Ade) and QDO+3-AT (QDO 647
medium supplemented with 1 mM 3-amino-124-triazole) The control plasmid 648
pOst1-NubI was used to determine whether the bait was functional the pPR3-N prey 649
vector plasmid was used to test whether the bait displayed non-specific background 650
and positive interactions were indicated by the growth of yeast on QDO and 651
QDO+3-AT plates The Primers used in the DUALhunter assay are listed in 652
Supplemental Table S6 653
654
Bimolecular fluorescence complementation (BiFC) assays 655
Full-length FaERF9 and FaMYB98 respectively were cloned into sequences 656
encoding the N- and C- fragments of YFP protein (Lv et al 2014) All constructs 657
were transiently expressed in tobacco (N benthamiana) leaves by Agrobacterium 658
infiltration (EHA105) The YFP fluorescence of transfected leaves was imaged 40 h 659
after infiltration by using a Nikon A1-SHS confocal laser scanning microscope The 660
excitation wavelength for YFP was 488 nm and fluorescence was detected at 520ndash661
540 nm Primers used are listed in Supplemental Table S6 662
663
Statistics 664
A Studentrsquos two-tailed t test ( plt005 plt001 and plt0001) was used to 665
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
24
determine significant differences between two groups in this study Microsoft Excel 666
was used to perform linear regressive analysis significant differences were 667
determined by SPSS Statistics 200 and scatter plots were prepared with Origin80 668
Least significant difference (LSD) at the 5 level was calculated using Microsoft 669
Excel Figures were prepared with Origin80 (Microcal Software Inc Northampton 670
MA USA) The online tool MetaboAnalyst 36 (httpwwwmetaboanalystca) was 671
used to analyse the transcript abundance of the AP2ERF genes 672
673
Accession numbers 674
Sequence data from this article have been deposited in GenBank under the accession 675
numbers MH332903-MH333022 for AP2ERF genes in Fragaria times ananassa and 676
MH333023 for FaMYB98 GenBank numbers for FaQR and FaOMT were 677
AY1588361 (Raab et al 2006) and AF2204912 (Wein et al 2002) 678
679
Supplemental Material 680
Supplemental Figure S1 Phylogenetic analysis of FaAP2ERF and Arabidopsis 681
AP2ERF proteins 682
Supplemental Figure S2 Analysis of FaAP2ERF gene expression patterns in 683
strawberry fruit during development and ripening 684
Supplemental Figure S3 Contents of furanones in fruit of strawberry cultivars 685
Supplemental Figure S4 Relative expression of FaERF9 in FaERF9-FaMYB98- 686
and FaERF9-overexpressing fruits 687
Supplemental Figure S5 Subcellular localization of FaMYB98 688
Supplemental Figure S6 The combined activation effects of FaERF9FaMYB98 on 689
the FaOMT promoter 690
Supplemental Figure S7 Relative expression of FaOMT in 691
FaERF9-overexpressing fruits 692
Supplemental Table S1 AP2ERF superfamily genes in Fragaria times ananassa 693
Supplemental Table S2 Classification of the AP2ERF superfamily members in 694
Fragaria times ananassa 695
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
25
Supplemental Table S3 Furanone content in FaERF9-FaMYB98- and 696
FaERF9-overexpressing fruits 697
Supplemental Table S4 Primers used for reverse transcription quantitative PCR 698
(RT-qPCR) 699
Supplemental Table S5 Primers used to amplify the full-length coding sequences of 700
AP2ERF genes and FaMYB98 in strawberry (Fragaria times ananassa) 701
Supplemental Table S6 Primers used for vector construction 702
703
Acknowledgments 704
This research was supported by the National Key Research and Development 705
Program (2016YFD0400101) the Project of the Science and Technology Department 706
of Zhejiang Province (2016C04001) and the 111 Project (B17039) 707
708
Figure legends 709
Figure 1 Changes in furanone content and furanone biosynthetic genes during 710
strawberry (Fragaria times ananassa Duch cv Yuexin) fruit development and ripening 711
A Fruits were collected at four ripening stages G (green stage) T (turning stage) IR 712
(intermediate red stage) R (full red stage) B Changes in the contents of furaneol 713
(HDMF) and mesifurane (DMMF) HDMF content was calculated using a standard 714
curve of HDMF while DMMF content was calculated with an internal standard as the 715
reference C Expression levels of FaQR and FaOMT The expression levels of each 716
gene were calculated relative to corresponding values in the basal section at the R 717
stage SEs were calculated from three replicates and LSD values represent the least 718
significant differences at p = 005 719
Figure 2 Regulatory effects of FaAP2ERF on the promoter of FaQR LUCREN 720
values of the empty vector on FaQR promoter were used as the calibrator set as 1 721
and SEs were calculated from five replicates statistical significance was determined 722
by Studentrsquos two-tailed t test ( plt0001) 723
Figure 3 Expression and the subcellular localization of FaERF9 A The expression 724
levels were calculated relative to the levels in the basal section at the R stage B 725
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
26
Subcellular localization analysis was performed in tobacco leaves The tobacco used 726
in the assay was stably transformed with a specific nucleus localized red fluorescence 727
protein construct and the red fluorescence indicates the nucleus-localized signal 728
(NLS) Scale bar = 25 microm SEs were calculated from three replicates 729
Figure 4 Transient overexpression of FaERF9 in strawberry fruit A Relative 730
expression of FaQR and FaERF9 in FaERF9-OX fruit 7 days after infiltration The 731
expression was calculated relative to the average value in control (SK) fruits B 732
HDMF and DMMF content in FaERF9-OX fruit The content of both furanones 733
were quantified using the peak area of the internal standard (2-octanol) as the 734
reference SEs were calculated from three replicates Statistical significance was 735
determined by Studentrsquos two-tailed t test ( plt005 plt001 plt0001) 736
Figure 5 Scatter plots of 11 strawberry cultivars A Linear regression analysis 737
between FaERF9 expression and FaQR expression B Linear regression analysis 738
between FaERF9 expression and furanone content The relative expression was 739
normalized to that of the housekeeping gene FaRIB413 and furanone content was 740
calculated with internal standard as the reference Significant differences were 741
determined by SPSS Statistics 200 742
Figure 6 Interactions of FaERF9 and FaMYB98 with the FaQR promoter A Yeast 743
one-hybrid analysis of the interaction of FaERF9 and FaQR promoter B Yeast 744
one-hybrid analysis of the interaction of FaMYB98 and FaQR promoter C 745
Regulatory effect of FaMYB98 on the FaQR promoter Auto-activation was tested on 746
SD-Ura (synthetically defined medium without uracil) in presence of Aureobasidin A 747
(AbA) and physical interaction was determined on SD-Leu (synthetically defined 748
medium without leucine) in presence of AbA LUCREN values of the empty vector 749
on FaQR promoter were used as the calibrator set as 1 and error bars were calculated 750
from five replicates Statistical significance was determined by Studentrsquos two-tailed t 751
test ( plt005 plt001 plt0001) 752
Figure 7 Electrophoretic mobility shift assay of FaMYB98 binding to FaQR 753
promoter A The probe sequence used for EMSA and mutated nucleotides are 754
indicated with lowercase letters B Purified DNA-binding domain of FaMYB98 755
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
27
protein and biotin-labelled DNA probe were mixed and analysed on 6 native 756
polyacrylamide gels and then photographed Presence or absence of specific probes is 757
marked by the symbol + or - 758
Figure 8 The combined activation effects of FaERF9FaMYB98 on the FaQR 759
promoter LUCREN values obtained with the empty vector and FaQR promoter were 760
used as the calibrator set as 1 and error bars were calculated from five replicates 761
Figure 9 Yeast two-hybrid analysis of the protein-protein interactions between 762
FaMYB98 and FaERF9 Positive interactions were determined by the growth of 763
yeast cells on selection plates Bait with pOST acted as positive controls and bait with 764
pPR3 as negative controls DDO synthetically defined medium without tryptophan 765
and leucine QDO synthetically defined medium without tryptophan leucine 766
histidine and adenine QDO+3AT QDO medium supplemented with 1 mM 767
3-aminotriazole 768
Figure 10 BiFC analysis of the protein-protein interactions between FaMYB98 and 769
FaERF9 The pairs of fusion proteins tested were FaMYB98-YFPN+FaERF9-YFPC 770
FaERF9-YFPN+FaMYB98-YFPC FaMYB98-YFPN+FaMYB98-YFPC and 771
FaERF9-YFPN+FaERF9-YFPC The other combinations were negative controls 772
The tobacco used in the assay was stably transformed with a specific 773
nucleus-localized red fluorescence protein construct and the red fluorescence 774
indicated the nucleus-localized signal (NLS) Fluorescence of the yellow fluorescence 775
protein (YFP) visualized the interaction in vivo Scale bar = 25 microm 776
777
Literature Cited 778
779
Agarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression 780
of PgDREB2A transcription factor enhances abiotic stress tolerance and activates 781
downstream stress-responsive genes Mol Biol Rep 37 1125-1135 782
Araguumlez I Osorio S Hoffmann T Rambla JL Medina-Escobar N Granell A 783
Botella MAacute Schwab W Valpuesta V (2013) Eugenol production in achenes and 784
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28
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Plant Physiol 163 946-958 786
Carvalho RF Carvalho SD OrsquoGrady K Folta KM (2016) Agroinfiltration of 787
strawberry fruit mdash a powerful transient expression system for gene validation Curr 788
Plant Biol 6 19-37 789
Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic 790
(Amsterdam) 210 34-40 791
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating 792
RNA from pine trees Plant Mol Biol Rep 11 113-116 793
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC 794
Clark DG (2011) PhMYB4 fine-tunes the floral volatile signature of 795
Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143 796
Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz 797
EA Taylor MG Smits-Kroon MT Schuurink RC Haring MA Giovannoni J 798
Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic 799
pathway by ectopic expression of a MYB transcription factor in tomato fruit Plant 800
Cell 23 2738-2753 801
Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan 802
XW Yang ZY (2017) Differential responses of four biosynthetic pathways of 803
aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under 804
interaction of light and temperature Food Chem 221 356-364 805
Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of 806
differentially-expressed genes during somatic embryogenesis in Fragaria times 807
ananassa Duch lsquoBenihopprsquo J Hortic Sci Biotechnol 90 671-681 808
Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 809
transcriptionally regulates chilling-induced lignification of loquat fruit via physical 810
interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136 811
Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM 812
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proteins Plant J 39 513-526 814
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29
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) 815
Sucrose nonfermenting1-related protein kinase26 an ortholog of open stomata1 is 816
a negative regulator of strawberry fruit development and ripening Plant Physiol 817
167 915-930 818
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene 819
expression in strawberry fruit (Fragaria times ananassa) by agroinfiltration a rapid 820
assay for gene function analysis Plant J 48 818-826 821
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of 822
selected aroma-active compounds in strawberries by headspace solid-phase 823
microextraction gas chromatography and correlation with sensory descriptive 824
analysis J Food Sci 72 S487-S496 825
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid 826
plays an important role in the regulation of strawberry fruit ripening Plant Physiol 827
157 188-199 828
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of 829
NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes BMC 830
Plant Biol 6 20 831
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN 832
(2005) MYB98 is required for pollen tube guidance and synergid cell differentiation 833
in Arabidopsis Plant Cell 17 2981-2992 834
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional 835
characterization of enone oxidoreductases from strawberry and tomato fruit J 836
Agric Food Chem 55 6705-6711 837
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You 838
J-S Rohloff J Randall SK Alsheikh M (2012) Proteomic study of 839
low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ 840
in cold tolerance Plant Physiol 159 1787-1805 841
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional 842
characterization of four APETALA2-family genes (RAP26 RAP26L DREB19 843
and DREB26) in Arabidopsis Plant Mol Biol 75 107-127 844
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30
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon 845
J Gupta V (2013) An oxidoreductase from lsquoAlphonsorsquo mango catalyzing 846
biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494 847
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in 848
strawberries Z Lebensm-Unters Forsch 195 120-123 849
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X 850
(2015) Label-free quantitative proteomics to investigate strawberry fruit proteome 851
changes under controlled atmosphere and low temperature storage J Proteomics 852
120 44-57 853
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 854
cooperates with CitWRKY1 to participate in citric acid degradation via 855
up-regulation of CitAco3 J Exp Bot 68 3419-3426 856
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription 857
factor CitERF71 activates the terpene synthase gene CitTPS16 involved in the 858
synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938 859
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and 860
transcriptomic analysis of the AP2ERF superfamily in Vitis vinifera BMC 861
Genomics 11 719 862
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive 863
Factor (AP2ERF) transcription factors mediators of stress responses and 864
developmental programs New Phytol 199 639-649 865
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 866
interacting with EOBI negatively regulates fragrance biosynthesis in petunia 867
flowers New Phytol 215 1490-1502 868
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu 869
CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 in regulating 870
anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) 871
during anthocyanin biosynthesis Plant Cell Tissue Organ Cult 115 285-298 872
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31
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao 873
CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphate signaling and 874
homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597 875
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC 876
Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL 877
Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor 878
regulates eugenol production in ripe strawberry fruit receptacles Plant Physiol 168 879
598-614 880
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics 881
and volatile constituents of strawberry (cv Cigaline) during maturation J Agric 882
Food Chem 52 1248-1254 883
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS 884
(2012) Ethylene-responsive transcription factors interact with promoters of ADH 885
and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 886
63 6393-6405 887
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM 888
Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-Franco A 889
Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific 890
transcription factor FaDOF2 regulates the production of eugenol in ripe fruit 891
receptacles J Exp Bot 68 4529-4543 892
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) 893
Comparison and verification of the genes involved in ethylene biosynthesis and 894
signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44 895
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the 896
ERF gene family in Arabidopsis and rice Plant Physiol 140 411-432 897
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in 898
sour cherry and strawberry and the heterologous expression of CBF1 in strawberry 899
J Am Soc Hortic Sci 127 489-494 900
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech 901
JC Ohme-Takagi M Regad F Bouzayen M (2012) Functional analysis and 902
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32
binding affinity of tomato ethylene response factors provide insight on the 903
molecular bases of plant differential responses to ethylene BMC Plant Biol 12 190 904
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) 905
Methylpentoses are possible precursors of furanones in fruits Prikl Biokhim 906
Mikrobiol 28 123-127 907
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery 908
of synergid-expressed genes encoding filiform apparatus localized proteins Plant 909
Cell 19 2557-2568 910
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria 911
vesca L compared to those of cultivated berries Fragariatimes ananassa cv Senga 912
Sengana J Agric Food Chem 27 19-22 913
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W 914
Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of the strawberry 915
flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone 916
oxidoreductase Plant Cell 18 1023-1037 917
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L 918
Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim M Broun P Zhang 919
JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription 920
factors genome-wide comparative analysis among eukaryotes Science 290 921
2105-2110 922
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the 923
formation of 25-dimethyl-4-hydroxy-3(2H)-furanone in detached ripening 924
strawberry fruits J Agric Food Chem 46 1488-1493 925
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 926
25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in 927
strawberry fruits Phytochemistry 43 155-159 928
Schwab W (1998) Application of stable isotope ratio analysis explaining the 929
bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone in plants by a biological 930
maillard reaction J Agric Food Chem 46 2266ndash2269 931
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33
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) 932
Molecules 18 6936-6951 933
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard 934
products Recent Res Dev Phytochem 1 643-673 935
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL 936
Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJ Sims CA 937
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compositions a seasonal influence and effects on sensory perception PLoS One 9 939
e88446 940
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) 941
Identification phylogeny and transcript profiling of ERF family genes during 942
development and abiotic stress treatments in tomato Mol Genet Genomics 284 943
455-475 944
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) 945
CitAP210 activation of the terpene synthase CsTPS1 is associated with the 946
synthesis of (+)-valencene in lsquoNewhallrsquo orange J Exp Bot 67 4105-4115 947
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes 948
Dev Genes Evol 214 105-114 949
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K 950
Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the 951
key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151 952
Spitzer-Rimon B Farhi M Albo B Cnarsquoani A Ben Zvi MM Masci T Edelbaum 953
O Yu YX Shklarman E Ovadis M Vainstein A (2012) The R2R3-MYB-like 954
regulatory factor EOBI acting downstream of EOBII regulates scent production 955
by activating ODO1 and structural scent-related genes in petunia Plant Cell 24 956
5089-5105 957
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp 958
Bot 68 4407-4409 959
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla 960
JF Amaya I Giavalisco P Fernie AR Botella MA Valpuesta V (2015) Central 961
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34
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to ripening New Phytol 208 482-496 963
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 964
regulates fragrance biosynthesis in petunia flowers Plant Cell 17 1612-1624 965
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS 966
(2018) The potassium channel FaTPK1 plays a critical role in fruit quality 967
formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748 968
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) 969
Isolation cloning and expression of a multifunctional O-methyltransferase capable 970
of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma 971
compounds in strawberry fruits Plant J 31 755-765 972
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor 973
types their evolutionary origin and species distribution In A handbook of 974
transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular 975
Biochemistry 52 25-73 976
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of 977
odor (Buettner A Ed) Springer Cham 9-10 978
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS 979
(2014) Isolation classification and transcription profiles of the AP2ERF 980
transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271 981
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in 982
regulation of fruit quality Crit Rev Plant Sci 35 120-130 983
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ 984
Zhang SL Wu J (2017) Map-based cloning of the pear gene MYB114 identifies an 985
interaction with other transcription factors to coordinately regulate fruit 986
anthocyanin biosynthesis Plant J 92 437-451 987
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes 988
involved in regulating fruit ripening Plant Physiol 153 1280-1292 989
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
35
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) 990
Expression of ethylene response genes during persimmon fruit astringency removal 991
Planta 235 895-906 992
Zabetakis I Gramshaw JW Robinson DS (1999) 993
25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis and 994
biosynthesis-a review Food Chem 65 139-151 995
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci 996
Food Agric 74 421-434 997
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 998
an AP2ERF gene is a novel regulator of fruit lignification induced by chilling 999
injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1000
1325-1334 1001
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation 1002
classification and transcription profiles of the Ethylene Response Factors (ERFs) in 1003
ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215 1004
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML 1005
(2012) Genome-wide analysis of the AP2ERF superfamily in peach (Prunus 1006
persica) Genet Mol Res 11 4788-4809 1007
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and 1008
expression analysis of a CRTDRE-binding factor gene FaCBF1 from Fragaria times 1009
ananassa Acta Hortic 41 240-248 1010
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The 1011
Arabidopsis AP2ERF transcription factor RAP26 participates in ABA salt and 1012
osmotic stress responses Gene 457 1-12 1013
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B 1014
Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) Genome-wide 1015
analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic 1016
(Amsterdam) 123 73-81 1017
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF 1018
Valpuesta V Botella MA Granell A Amaya I (2012) Genetic analysis of 1019
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
36
strawberry fruit aroma and identification of O-methyltransferase FaOMT as the 1020
locus controlling natural variation in mesifurane content Plant Physiol 159 1021
851-870 1022
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methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma compounds in strawberry fruitsPlant J 31 755-765
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Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
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Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and expression analysis of a CRTDRE-binding factor gene FaCBF1from Fragaria times ananassa Acta Hortic 41 240-248
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The Arabidopsis AP2ERF transcription factor RAP26 participatesin ABA salt and osmotic stress responses Gene 457 1-12
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Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Genome-wide analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic (Amsterdam) 123 73-81Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF Valpuesta V Botella MA Granell A Amaya I (2012) Geneticanalysis of strawberry fruit aroma and identification of O-methyltransferase FaOMT as the locus controlling natural variation inmesifurane content Plant Physiol 159 851-870
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
22
was tested according to the system user manual and then screening for protein-DNA 606
interactions was carried out Furthermore the full length of each transcription factor 607
was separately cloned into pGADT7 AD vector to confirm the screening results The 608
relationship between FaERF9 and FaQR promoter was also examined individually 609
Primers used in this assay are listed in Supplemental Table S6 610
611
Expression and purification of FaMYB98 recombinant protein 612
A 405-bp region spanning the DNA-binding domain of FaMYB98 was amplified 613
from FaMYB98 cDNA and cloned into a pET6timesHN vector (Clontech Palo CA USA) 614
to generate the recombinant N-terminal His-tagged protein the primers used are listed 615
in Supplemental Table S6 The resulting construct was sequenced and introduced into 616
Escherichia coli strain Rosetta 2(DE3)pLysS (Novagen) Ten millilitres of the 617
overnight culture was combined with 500 mL of an LB liquid medium (100 μgmL 618
ampicillin and 34 μgmL chloramphenicol) as described (Li et al 2017) Isopropyl 619
β-D-1-thiogalactopyranoside (IPTG) was added to a final concentration of 1 mM and 620
the bacterial culture was incubated at 18degC at 150 rpm for 18 h Then the cells were 621
harvested using a centrifuge and resuspended in 1times PBS buffer (Sangon Biotech) 622
after which they were disrupted by sonication and the supernatant was purified using 623
a HisTALONTM Gravity Column (Clontech) according to the user manual The PD-10 624
Desalting column (GE Healthcare) was then used for buffer change and sample 625
clean-up of proteins according to the gravity protocol SDS-PAGE was performed and 626
the protein was visualized using Coomassie brilliant blue 627
628
Electrophoretic mobility shift assay (EMSA) 629
A Lightshift Chemiluminescent EMSA kit (Thermo) was used to perform EMSA 630
experiments according to the manufacturerrsquos instructions Single-strand 631
oligonucleotides were synthesized and biotinylated by GeneBio Biotech (Hangzhou 632
China) The details of the EMSA assay are provided in Ge et al (2017) The probes 633
used for EMSAs are listed in Supplemental Table S6 634
635
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
23
636
Yeast two-hybrid assay 637
The DUALhunter system (Dualsystems Biotech Switzerland) was used to investigate 638
the interaction between FaERF9 and FaMYB98 Full-length coding sequences of 639
FaERF9 and FaMYB98 were respectively cloned into pDHB1 bait vector and 640
pPR3-N prey vector sequences were verified and the bait plasmid was 641
co-transformed with prey plasmid into NMY51 in the combinations below 642
FaMYB98-pDHB1pPR3-N FaMYB98-pDHB1FaERF9-pPR3-N 643
FaMYB98-pDHB1pOst1-NubI FaERF9-pDHB1pPR3-N 644
FaERF9-pDHB1FaMYB98-pPR3-N and FaERF9-pDHB1pOst1-NubI (Li et al 645
2017) Transformed cells were spread onto the following plates DDO (SD 646
medium-Trp-Leu) QDO (SD medium-Trp-Leu-His-Ade) and QDO+3-AT (QDO 647
medium supplemented with 1 mM 3-amino-124-triazole) The control plasmid 648
pOst1-NubI was used to determine whether the bait was functional the pPR3-N prey 649
vector plasmid was used to test whether the bait displayed non-specific background 650
and positive interactions were indicated by the growth of yeast on QDO and 651
QDO+3-AT plates The Primers used in the DUALhunter assay are listed in 652
Supplemental Table S6 653
654
Bimolecular fluorescence complementation (BiFC) assays 655
Full-length FaERF9 and FaMYB98 respectively were cloned into sequences 656
encoding the N- and C- fragments of YFP protein (Lv et al 2014) All constructs 657
were transiently expressed in tobacco (N benthamiana) leaves by Agrobacterium 658
infiltration (EHA105) The YFP fluorescence of transfected leaves was imaged 40 h 659
after infiltration by using a Nikon A1-SHS confocal laser scanning microscope The 660
excitation wavelength for YFP was 488 nm and fluorescence was detected at 520ndash661
540 nm Primers used are listed in Supplemental Table S6 662
663
Statistics 664
A Studentrsquos two-tailed t test ( plt005 plt001 and plt0001) was used to 665
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
24
determine significant differences between two groups in this study Microsoft Excel 666
was used to perform linear regressive analysis significant differences were 667
determined by SPSS Statistics 200 and scatter plots were prepared with Origin80 668
Least significant difference (LSD) at the 5 level was calculated using Microsoft 669
Excel Figures were prepared with Origin80 (Microcal Software Inc Northampton 670
MA USA) The online tool MetaboAnalyst 36 (httpwwwmetaboanalystca) was 671
used to analyse the transcript abundance of the AP2ERF genes 672
673
Accession numbers 674
Sequence data from this article have been deposited in GenBank under the accession 675
numbers MH332903-MH333022 for AP2ERF genes in Fragaria times ananassa and 676
MH333023 for FaMYB98 GenBank numbers for FaQR and FaOMT were 677
AY1588361 (Raab et al 2006) and AF2204912 (Wein et al 2002) 678
679
Supplemental Material 680
Supplemental Figure S1 Phylogenetic analysis of FaAP2ERF and Arabidopsis 681
AP2ERF proteins 682
Supplemental Figure S2 Analysis of FaAP2ERF gene expression patterns in 683
strawberry fruit during development and ripening 684
Supplemental Figure S3 Contents of furanones in fruit of strawberry cultivars 685
Supplemental Figure S4 Relative expression of FaERF9 in FaERF9-FaMYB98- 686
and FaERF9-overexpressing fruits 687
Supplemental Figure S5 Subcellular localization of FaMYB98 688
Supplemental Figure S6 The combined activation effects of FaERF9FaMYB98 on 689
the FaOMT promoter 690
Supplemental Figure S7 Relative expression of FaOMT in 691
FaERF9-overexpressing fruits 692
Supplemental Table S1 AP2ERF superfamily genes in Fragaria times ananassa 693
Supplemental Table S2 Classification of the AP2ERF superfamily members in 694
Fragaria times ananassa 695
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
25
Supplemental Table S3 Furanone content in FaERF9-FaMYB98- and 696
FaERF9-overexpressing fruits 697
Supplemental Table S4 Primers used for reverse transcription quantitative PCR 698
(RT-qPCR) 699
Supplemental Table S5 Primers used to amplify the full-length coding sequences of 700
AP2ERF genes and FaMYB98 in strawberry (Fragaria times ananassa) 701
Supplemental Table S6 Primers used for vector construction 702
703
Acknowledgments 704
This research was supported by the National Key Research and Development 705
Program (2016YFD0400101) the Project of the Science and Technology Department 706
of Zhejiang Province (2016C04001) and the 111 Project (B17039) 707
708
Figure legends 709
Figure 1 Changes in furanone content and furanone biosynthetic genes during 710
strawberry (Fragaria times ananassa Duch cv Yuexin) fruit development and ripening 711
A Fruits were collected at four ripening stages G (green stage) T (turning stage) IR 712
(intermediate red stage) R (full red stage) B Changes in the contents of furaneol 713
(HDMF) and mesifurane (DMMF) HDMF content was calculated using a standard 714
curve of HDMF while DMMF content was calculated with an internal standard as the 715
reference C Expression levels of FaQR and FaOMT The expression levels of each 716
gene were calculated relative to corresponding values in the basal section at the R 717
stage SEs were calculated from three replicates and LSD values represent the least 718
significant differences at p = 005 719
Figure 2 Regulatory effects of FaAP2ERF on the promoter of FaQR LUCREN 720
values of the empty vector on FaQR promoter were used as the calibrator set as 1 721
and SEs were calculated from five replicates statistical significance was determined 722
by Studentrsquos two-tailed t test ( plt0001) 723
Figure 3 Expression and the subcellular localization of FaERF9 A The expression 724
levels were calculated relative to the levels in the basal section at the R stage B 725
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
26
Subcellular localization analysis was performed in tobacco leaves The tobacco used 726
in the assay was stably transformed with a specific nucleus localized red fluorescence 727
protein construct and the red fluorescence indicates the nucleus-localized signal 728
(NLS) Scale bar = 25 microm SEs were calculated from three replicates 729
Figure 4 Transient overexpression of FaERF9 in strawberry fruit A Relative 730
expression of FaQR and FaERF9 in FaERF9-OX fruit 7 days after infiltration The 731
expression was calculated relative to the average value in control (SK) fruits B 732
HDMF and DMMF content in FaERF9-OX fruit The content of both furanones 733
were quantified using the peak area of the internal standard (2-octanol) as the 734
reference SEs were calculated from three replicates Statistical significance was 735
determined by Studentrsquos two-tailed t test ( plt005 plt001 plt0001) 736
Figure 5 Scatter plots of 11 strawberry cultivars A Linear regression analysis 737
between FaERF9 expression and FaQR expression B Linear regression analysis 738
between FaERF9 expression and furanone content The relative expression was 739
normalized to that of the housekeeping gene FaRIB413 and furanone content was 740
calculated with internal standard as the reference Significant differences were 741
determined by SPSS Statistics 200 742
Figure 6 Interactions of FaERF9 and FaMYB98 with the FaQR promoter A Yeast 743
one-hybrid analysis of the interaction of FaERF9 and FaQR promoter B Yeast 744
one-hybrid analysis of the interaction of FaMYB98 and FaQR promoter C 745
Regulatory effect of FaMYB98 on the FaQR promoter Auto-activation was tested on 746
SD-Ura (synthetically defined medium without uracil) in presence of Aureobasidin A 747
(AbA) and physical interaction was determined on SD-Leu (synthetically defined 748
medium without leucine) in presence of AbA LUCREN values of the empty vector 749
on FaQR promoter were used as the calibrator set as 1 and error bars were calculated 750
from five replicates Statistical significance was determined by Studentrsquos two-tailed t 751
test ( plt005 plt001 plt0001) 752
Figure 7 Electrophoretic mobility shift assay of FaMYB98 binding to FaQR 753
promoter A The probe sequence used for EMSA and mutated nucleotides are 754
indicated with lowercase letters B Purified DNA-binding domain of FaMYB98 755
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
27
protein and biotin-labelled DNA probe were mixed and analysed on 6 native 756
polyacrylamide gels and then photographed Presence or absence of specific probes is 757
marked by the symbol + or - 758
Figure 8 The combined activation effects of FaERF9FaMYB98 on the FaQR 759
promoter LUCREN values obtained with the empty vector and FaQR promoter were 760
used as the calibrator set as 1 and error bars were calculated from five replicates 761
Figure 9 Yeast two-hybrid analysis of the protein-protein interactions between 762
FaMYB98 and FaERF9 Positive interactions were determined by the growth of 763
yeast cells on selection plates Bait with pOST acted as positive controls and bait with 764
pPR3 as negative controls DDO synthetically defined medium without tryptophan 765
and leucine QDO synthetically defined medium without tryptophan leucine 766
histidine and adenine QDO+3AT QDO medium supplemented with 1 mM 767
3-aminotriazole 768
Figure 10 BiFC analysis of the protein-protein interactions between FaMYB98 and 769
FaERF9 The pairs of fusion proteins tested were FaMYB98-YFPN+FaERF9-YFPC 770
FaERF9-YFPN+FaMYB98-YFPC FaMYB98-YFPN+FaMYB98-YFPC and 771
FaERF9-YFPN+FaERF9-YFPC The other combinations were negative controls 772
The tobacco used in the assay was stably transformed with a specific 773
nucleus-localized red fluorescence protein construct and the red fluorescence 774
indicated the nucleus-localized signal (NLS) Fluorescence of the yellow fluorescence 775
protein (YFP) visualized the interaction in vivo Scale bar = 25 microm 776
777
Literature Cited 778
779
Agarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression 780
of PgDREB2A transcription factor enhances abiotic stress tolerance and activates 781
downstream stress-responsive genes Mol Biol Rep 37 1125-1135 782
Araguumlez I Osorio S Hoffmann T Rambla JL Medina-Escobar N Granell A 783
Botella MAacute Schwab W Valpuesta V (2013) Eugenol production in achenes and 784
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
28
receptacles of strawberry fruits is catalyzed by synthases exhibiting distinct kinetics 785
Plant Physiol 163 946-958 786
Carvalho RF Carvalho SD OrsquoGrady K Folta KM (2016) Agroinfiltration of 787
strawberry fruit mdash a powerful transient expression system for gene validation Curr 788
Plant Biol 6 19-37 789
Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic 790
(Amsterdam) 210 34-40 791
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating 792
RNA from pine trees Plant Mol Biol Rep 11 113-116 793
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC 794
Clark DG (2011) PhMYB4 fine-tunes the floral volatile signature of 795
Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143 796
Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz 797
EA Taylor MG Smits-Kroon MT Schuurink RC Haring MA Giovannoni J 798
Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic 799
pathway by ectopic expression of a MYB transcription factor in tomato fruit Plant 800
Cell 23 2738-2753 801
Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan 802
XW Yang ZY (2017) Differential responses of four biosynthetic pathways of 803
aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under 804
interaction of light and temperature Food Chem 221 356-364 805
Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of 806
differentially-expressed genes during somatic embryogenesis in Fragaria times 807
ananassa Duch lsquoBenihopprsquo J Hortic Sci Biotechnol 90 671-681 808
Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 809
transcriptionally regulates chilling-induced lignification of loquat fruit via physical 810
interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136 811
Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM 812
(2004) Functional interactions between a glutamine synthetase promoter and MYB 813
proteins Plant J 39 513-526 814
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29
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) 815
Sucrose nonfermenting1-related protein kinase26 an ortholog of open stomata1 is 816
a negative regulator of strawberry fruit development and ripening Plant Physiol 817
167 915-930 818
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene 819
expression in strawberry fruit (Fragaria times ananassa) by agroinfiltration a rapid 820
assay for gene function analysis Plant J 48 818-826 821
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of 822
selected aroma-active compounds in strawberries by headspace solid-phase 823
microextraction gas chromatography and correlation with sensory descriptive 824
analysis J Food Sci 72 S487-S496 825
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid 826
plays an important role in the regulation of strawberry fruit ripening Plant Physiol 827
157 188-199 828
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of 829
NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes BMC 830
Plant Biol 6 20 831
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN 832
(2005) MYB98 is required for pollen tube guidance and synergid cell differentiation 833
in Arabidopsis Plant Cell 17 2981-2992 834
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional 835
characterization of enone oxidoreductases from strawberry and tomato fruit J 836
Agric Food Chem 55 6705-6711 837
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You 838
J-S Rohloff J Randall SK Alsheikh M (2012) Proteomic study of 839
low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ 840
in cold tolerance Plant Physiol 159 1787-1805 841
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional 842
characterization of four APETALA2-family genes (RAP26 RAP26L DREB19 843
and DREB26) in Arabidopsis Plant Mol Biol 75 107-127 844
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30
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon 845
J Gupta V (2013) An oxidoreductase from lsquoAlphonsorsquo mango catalyzing 846
biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494 847
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in 848
strawberries Z Lebensm-Unters Forsch 195 120-123 849
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X 850
(2015) Label-free quantitative proteomics to investigate strawberry fruit proteome 851
changes under controlled atmosphere and low temperature storage J Proteomics 852
120 44-57 853
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 854
cooperates with CitWRKY1 to participate in citric acid degradation via 855
up-regulation of CitAco3 J Exp Bot 68 3419-3426 856
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription 857
factor CitERF71 activates the terpene synthase gene CitTPS16 involved in the 858
synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938 859
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and 860
transcriptomic analysis of the AP2ERF superfamily in Vitis vinifera BMC 861
Genomics 11 719 862
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive 863
Factor (AP2ERF) transcription factors mediators of stress responses and 864
developmental programs New Phytol 199 639-649 865
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 866
interacting with EOBI negatively regulates fragrance biosynthesis in petunia 867
flowers New Phytol 215 1490-1502 868
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu 869
CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 in regulating 870
anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) 871
during anthocyanin biosynthesis Plant Cell Tissue Organ Cult 115 285-298 872
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31
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao 873
CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphate signaling and 874
homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597 875
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC 876
Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL 877
Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor 878
regulates eugenol production in ripe strawberry fruit receptacles Plant Physiol 168 879
598-614 880
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics 881
and volatile constituents of strawberry (cv Cigaline) during maturation J Agric 882
Food Chem 52 1248-1254 883
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS 884
(2012) Ethylene-responsive transcription factors interact with promoters of ADH 885
and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 886
63 6393-6405 887
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM 888
Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-Franco A 889
Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific 890
transcription factor FaDOF2 regulates the production of eugenol in ripe fruit 891
receptacles J Exp Bot 68 4529-4543 892
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) 893
Comparison and verification of the genes involved in ethylene biosynthesis and 894
signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44 895
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the 896
ERF gene family in Arabidopsis and rice Plant Physiol 140 411-432 897
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in 898
sour cherry and strawberry and the heterologous expression of CBF1 in strawberry 899
J Am Soc Hortic Sci 127 489-494 900
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech 901
JC Ohme-Takagi M Regad F Bouzayen M (2012) Functional analysis and 902
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32
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molecular bases of plant differential responses to ethylene BMC Plant Biol 12 190 904
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) 905
Methylpentoses are possible precursors of furanones in fruits Prikl Biokhim 906
Mikrobiol 28 123-127 907
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery 908
of synergid-expressed genes encoding filiform apparatus localized proteins Plant 909
Cell 19 2557-2568 910
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria 911
vesca L compared to those of cultivated berries Fragariatimes ananassa cv Senga 912
Sengana J Agric Food Chem 27 19-22 913
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W 914
Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of the strawberry 915
flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone 916
oxidoreductase Plant Cell 18 1023-1037 917
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L 918
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factors genome-wide comparative analysis among eukaryotes Science 290 921
2105-2110 922
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the 923
formation of 25-dimethyl-4-hydroxy-3(2H)-furanone in detached ripening 924
strawberry fruits J Agric Food Chem 46 1488-1493 925
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 926
25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in 927
strawberry fruits Phytochemistry 43 155-159 928
Schwab W (1998) Application of stable isotope ratio analysis explaining the 929
bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone in plants by a biological 930
maillard reaction J Agric Food Chem 46 2266ndash2269 931
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33
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) 932
Molecules 18 6936-6951 933
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products Recent Res Dev Phytochem 1 643-673 935
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compositions a seasonal influence and effects on sensory perception PLoS One 9 939
e88446 940
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) 941
Identification phylogeny and transcript profiling of ERF family genes during 942
development and abiotic stress treatments in tomato Mol Genet Genomics 284 943
455-475 944
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) 945
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synthesis of (+)-valencene in lsquoNewhallrsquo orange J Exp Bot 67 4105-4115 947
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes 948
Dev Genes Evol 214 105-114 949
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key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151 952
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O Yu YX Shklarman E Ovadis M Vainstein A (2012) The R2R3-MYB-like 954
regulatory factor EOBI acting downstream of EOBII regulates scent production 955
by activating ODO1 and structural scent-related genes in petunia Plant Cell 24 956
5089-5105 957
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp 958
Bot 68 4407-4409 959
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla 960
JF Amaya I Giavalisco P Fernie AR Botella MA Valpuesta V (2015) Central 961
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34
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to ripening New Phytol 208 482-496 963
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regulates fragrance biosynthesis in petunia flowers Plant Cell 17 1612-1624 965
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS 966
(2018) The potassium channel FaTPK1 plays a critical role in fruit quality 967
formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748 968
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) 969
Isolation cloning and expression of a multifunctional O-methyltransferase capable 970
of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma 971
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types their evolutionary origin and species distribution In A handbook of 974
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Biochemistry 52 25-73 976
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of 977
odor (Buettner A Ed) Springer Cham 9-10 978
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS 979
(2014) Isolation classification and transcription profiles of the AP2ERF 980
transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271 981
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in 982
regulation of fruit quality Crit Rev Plant Sci 35 120-130 983
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ 984
Zhang SL Wu J (2017) Map-based cloning of the pear gene MYB114 identifies an 985
interaction with other transcription factors to coordinately regulate fruit 986
anthocyanin biosynthesis Plant J 92 437-451 987
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes 988
involved in regulating fruit ripening Plant Physiol 153 1280-1292 989
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35
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) 990
Expression of ethylene response genes during persimmon fruit astringency removal 991
Planta 235 895-906 992
Zabetakis I Gramshaw JW Robinson DS (1999) 993
25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis and 994
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Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci 996
Food Agric 74 421-434 997
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 998
an AP2ERF gene is a novel regulator of fruit lignification induced by chilling 999
injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1000
1325-1334 1001
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation 1002
classification and transcription profiles of the Ethylene Response Factors (ERFs) in 1003
ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215 1004
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML 1005
(2012) Genome-wide analysis of the AP2ERF superfamily in peach (Prunus 1006
persica) Genet Mol Res 11 4788-4809 1007
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and 1008
expression analysis of a CRTDRE-binding factor gene FaCBF1 from Fragaria times 1009
ananassa Acta Hortic 41 240-248 1010
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The 1011
Arabidopsis AP2ERF transcription factor RAP26 participates in ABA salt and 1012
osmotic stress responses Gene 457 1-12 1013
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B 1014
Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) Genome-wide 1015
analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic 1016
(Amsterdam) 123 73-81 1017
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF 1018
Valpuesta V Botella MA Granell A Amaya I (2012) Genetic analysis of 1019
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36
strawberry fruit aroma and identification of O-methyltransferase FaOMT as the 1020
locus controlling natural variation in mesifurane content Plant Physiol 159 1021
851-870 1022
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Parsed CitationsAgarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression of PgDREB2A transcription factor enhances abioticstress tolerance and activates downstream stress-responsive genes Mol Biol Rep 37 1125-1135
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Araguumlez I Osorio S Hoffmann T Rambla JL Medina-Escobar N Granell A Botella MAacute Schwab W Valpuesta V (2013) Eugenolproduction in achenes and receptacles of strawberry fruits is catalyzed by synthases exhibiting distinct kinetics Plant Physiol 163 946-958
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Carvalho RF Carvalho SD OGrady K Folta KM (2016) Agroinfiltration of strawberry fruit - a powerful transient expression system forgene validation Curr Plant Biol 6 19-37
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic (Amsterdam) 210 34-40Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating RNA from pine trees Plant Mol Biol Rep 11 113-116Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
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wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
23
636
Yeast two-hybrid assay 637
The DUALhunter system (Dualsystems Biotech Switzerland) was used to investigate 638
the interaction between FaERF9 and FaMYB98 Full-length coding sequences of 639
FaERF9 and FaMYB98 were respectively cloned into pDHB1 bait vector and 640
pPR3-N prey vector sequences were verified and the bait plasmid was 641
co-transformed with prey plasmid into NMY51 in the combinations below 642
FaMYB98-pDHB1pPR3-N FaMYB98-pDHB1FaERF9-pPR3-N 643
FaMYB98-pDHB1pOst1-NubI FaERF9-pDHB1pPR3-N 644
FaERF9-pDHB1FaMYB98-pPR3-N and FaERF9-pDHB1pOst1-NubI (Li et al 645
2017) Transformed cells were spread onto the following plates DDO (SD 646
medium-Trp-Leu) QDO (SD medium-Trp-Leu-His-Ade) and QDO+3-AT (QDO 647
medium supplemented with 1 mM 3-amino-124-triazole) The control plasmid 648
pOst1-NubI was used to determine whether the bait was functional the pPR3-N prey 649
vector plasmid was used to test whether the bait displayed non-specific background 650
and positive interactions were indicated by the growth of yeast on QDO and 651
QDO+3-AT plates The Primers used in the DUALhunter assay are listed in 652
Supplemental Table S6 653
654
Bimolecular fluorescence complementation (BiFC) assays 655
Full-length FaERF9 and FaMYB98 respectively were cloned into sequences 656
encoding the N- and C- fragments of YFP protein (Lv et al 2014) All constructs 657
were transiently expressed in tobacco (N benthamiana) leaves by Agrobacterium 658
infiltration (EHA105) The YFP fluorescence of transfected leaves was imaged 40 h 659
after infiltration by using a Nikon A1-SHS confocal laser scanning microscope The 660
excitation wavelength for YFP was 488 nm and fluorescence was detected at 520ndash661
540 nm Primers used are listed in Supplemental Table S6 662
663
Statistics 664
A Studentrsquos two-tailed t test ( plt005 plt001 and plt0001) was used to 665
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
24
determine significant differences between two groups in this study Microsoft Excel 666
was used to perform linear regressive analysis significant differences were 667
determined by SPSS Statistics 200 and scatter plots were prepared with Origin80 668
Least significant difference (LSD) at the 5 level was calculated using Microsoft 669
Excel Figures were prepared with Origin80 (Microcal Software Inc Northampton 670
MA USA) The online tool MetaboAnalyst 36 (httpwwwmetaboanalystca) was 671
used to analyse the transcript abundance of the AP2ERF genes 672
673
Accession numbers 674
Sequence data from this article have been deposited in GenBank under the accession 675
numbers MH332903-MH333022 for AP2ERF genes in Fragaria times ananassa and 676
MH333023 for FaMYB98 GenBank numbers for FaQR and FaOMT were 677
AY1588361 (Raab et al 2006) and AF2204912 (Wein et al 2002) 678
679
Supplemental Material 680
Supplemental Figure S1 Phylogenetic analysis of FaAP2ERF and Arabidopsis 681
AP2ERF proteins 682
Supplemental Figure S2 Analysis of FaAP2ERF gene expression patterns in 683
strawberry fruit during development and ripening 684
Supplemental Figure S3 Contents of furanones in fruit of strawberry cultivars 685
Supplemental Figure S4 Relative expression of FaERF9 in FaERF9-FaMYB98- 686
and FaERF9-overexpressing fruits 687
Supplemental Figure S5 Subcellular localization of FaMYB98 688
Supplemental Figure S6 The combined activation effects of FaERF9FaMYB98 on 689
the FaOMT promoter 690
Supplemental Figure S7 Relative expression of FaOMT in 691
FaERF9-overexpressing fruits 692
Supplemental Table S1 AP2ERF superfamily genes in Fragaria times ananassa 693
Supplemental Table S2 Classification of the AP2ERF superfamily members in 694
Fragaria times ananassa 695
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
25
Supplemental Table S3 Furanone content in FaERF9-FaMYB98- and 696
FaERF9-overexpressing fruits 697
Supplemental Table S4 Primers used for reverse transcription quantitative PCR 698
(RT-qPCR) 699
Supplemental Table S5 Primers used to amplify the full-length coding sequences of 700
AP2ERF genes and FaMYB98 in strawberry (Fragaria times ananassa) 701
Supplemental Table S6 Primers used for vector construction 702
703
Acknowledgments 704
This research was supported by the National Key Research and Development 705
Program (2016YFD0400101) the Project of the Science and Technology Department 706
of Zhejiang Province (2016C04001) and the 111 Project (B17039) 707
708
Figure legends 709
Figure 1 Changes in furanone content and furanone biosynthetic genes during 710
strawberry (Fragaria times ananassa Duch cv Yuexin) fruit development and ripening 711
A Fruits were collected at four ripening stages G (green stage) T (turning stage) IR 712
(intermediate red stage) R (full red stage) B Changes in the contents of furaneol 713
(HDMF) and mesifurane (DMMF) HDMF content was calculated using a standard 714
curve of HDMF while DMMF content was calculated with an internal standard as the 715
reference C Expression levels of FaQR and FaOMT The expression levels of each 716
gene were calculated relative to corresponding values in the basal section at the R 717
stage SEs were calculated from three replicates and LSD values represent the least 718
significant differences at p = 005 719
Figure 2 Regulatory effects of FaAP2ERF on the promoter of FaQR LUCREN 720
values of the empty vector on FaQR promoter were used as the calibrator set as 1 721
and SEs were calculated from five replicates statistical significance was determined 722
by Studentrsquos two-tailed t test ( plt0001) 723
Figure 3 Expression and the subcellular localization of FaERF9 A The expression 724
levels were calculated relative to the levels in the basal section at the R stage B 725
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
26
Subcellular localization analysis was performed in tobacco leaves The tobacco used 726
in the assay was stably transformed with a specific nucleus localized red fluorescence 727
protein construct and the red fluorescence indicates the nucleus-localized signal 728
(NLS) Scale bar = 25 microm SEs were calculated from three replicates 729
Figure 4 Transient overexpression of FaERF9 in strawberry fruit A Relative 730
expression of FaQR and FaERF9 in FaERF9-OX fruit 7 days after infiltration The 731
expression was calculated relative to the average value in control (SK) fruits B 732
HDMF and DMMF content in FaERF9-OX fruit The content of both furanones 733
were quantified using the peak area of the internal standard (2-octanol) as the 734
reference SEs were calculated from three replicates Statistical significance was 735
determined by Studentrsquos two-tailed t test ( plt005 plt001 plt0001) 736
Figure 5 Scatter plots of 11 strawberry cultivars A Linear regression analysis 737
between FaERF9 expression and FaQR expression B Linear regression analysis 738
between FaERF9 expression and furanone content The relative expression was 739
normalized to that of the housekeeping gene FaRIB413 and furanone content was 740
calculated with internal standard as the reference Significant differences were 741
determined by SPSS Statistics 200 742
Figure 6 Interactions of FaERF9 and FaMYB98 with the FaQR promoter A Yeast 743
one-hybrid analysis of the interaction of FaERF9 and FaQR promoter B Yeast 744
one-hybrid analysis of the interaction of FaMYB98 and FaQR promoter C 745
Regulatory effect of FaMYB98 on the FaQR promoter Auto-activation was tested on 746
SD-Ura (synthetically defined medium without uracil) in presence of Aureobasidin A 747
(AbA) and physical interaction was determined on SD-Leu (synthetically defined 748
medium without leucine) in presence of AbA LUCREN values of the empty vector 749
on FaQR promoter were used as the calibrator set as 1 and error bars were calculated 750
from five replicates Statistical significance was determined by Studentrsquos two-tailed t 751
test ( plt005 plt001 plt0001) 752
Figure 7 Electrophoretic mobility shift assay of FaMYB98 binding to FaQR 753
promoter A The probe sequence used for EMSA and mutated nucleotides are 754
indicated with lowercase letters B Purified DNA-binding domain of FaMYB98 755
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
27
protein and biotin-labelled DNA probe were mixed and analysed on 6 native 756
polyacrylamide gels and then photographed Presence or absence of specific probes is 757
marked by the symbol + or - 758
Figure 8 The combined activation effects of FaERF9FaMYB98 on the FaQR 759
promoter LUCREN values obtained with the empty vector and FaQR promoter were 760
used as the calibrator set as 1 and error bars were calculated from five replicates 761
Figure 9 Yeast two-hybrid analysis of the protein-protein interactions between 762
FaMYB98 and FaERF9 Positive interactions were determined by the growth of 763
yeast cells on selection plates Bait with pOST acted as positive controls and bait with 764
pPR3 as negative controls DDO synthetically defined medium without tryptophan 765
and leucine QDO synthetically defined medium without tryptophan leucine 766
histidine and adenine QDO+3AT QDO medium supplemented with 1 mM 767
3-aminotriazole 768
Figure 10 BiFC analysis of the protein-protein interactions between FaMYB98 and 769
FaERF9 The pairs of fusion proteins tested were FaMYB98-YFPN+FaERF9-YFPC 770
FaERF9-YFPN+FaMYB98-YFPC FaMYB98-YFPN+FaMYB98-YFPC and 771
FaERF9-YFPN+FaERF9-YFPC The other combinations were negative controls 772
The tobacco used in the assay was stably transformed with a specific 773
nucleus-localized red fluorescence protein construct and the red fluorescence 774
indicated the nucleus-localized signal (NLS) Fluorescence of the yellow fluorescence 775
protein (YFP) visualized the interaction in vivo Scale bar = 25 microm 776
777
Literature Cited 778
779
Agarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression 780
of PgDREB2A transcription factor enhances abiotic stress tolerance and activates 781
downstream stress-responsive genes Mol Biol Rep 37 1125-1135 782
Araguumlez I Osorio S Hoffmann T Rambla JL Medina-Escobar N Granell A 783
Botella MAacute Schwab W Valpuesta V (2013) Eugenol production in achenes and 784
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
28
receptacles of strawberry fruits is catalyzed by synthases exhibiting distinct kinetics 785
Plant Physiol 163 946-958 786
Carvalho RF Carvalho SD OrsquoGrady K Folta KM (2016) Agroinfiltration of 787
strawberry fruit mdash a powerful transient expression system for gene validation Curr 788
Plant Biol 6 19-37 789
Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic 790
(Amsterdam) 210 34-40 791
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating 792
RNA from pine trees Plant Mol Biol Rep 11 113-116 793
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC 794
Clark DG (2011) PhMYB4 fine-tunes the floral volatile signature of 795
Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143 796
Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz 797
EA Taylor MG Smits-Kroon MT Schuurink RC Haring MA Giovannoni J 798
Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic 799
pathway by ectopic expression of a MYB transcription factor in tomato fruit Plant 800
Cell 23 2738-2753 801
Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan 802
XW Yang ZY (2017) Differential responses of four biosynthetic pathways of 803
aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under 804
interaction of light and temperature Food Chem 221 356-364 805
Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of 806
differentially-expressed genes during somatic embryogenesis in Fragaria times 807
ananassa Duch lsquoBenihopprsquo J Hortic Sci Biotechnol 90 671-681 808
Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 809
transcriptionally regulates chilling-induced lignification of loquat fruit via physical 810
interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136 811
Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM 812
(2004) Functional interactions between a glutamine synthetase promoter and MYB 813
proteins Plant J 39 513-526 814
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
29
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) 815
Sucrose nonfermenting1-related protein kinase26 an ortholog of open stomata1 is 816
a negative regulator of strawberry fruit development and ripening Plant Physiol 817
167 915-930 818
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene 819
expression in strawberry fruit (Fragaria times ananassa) by agroinfiltration a rapid 820
assay for gene function analysis Plant J 48 818-826 821
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of 822
selected aroma-active compounds in strawberries by headspace solid-phase 823
microextraction gas chromatography and correlation with sensory descriptive 824
analysis J Food Sci 72 S487-S496 825
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid 826
plays an important role in the regulation of strawberry fruit ripening Plant Physiol 827
157 188-199 828
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of 829
NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes BMC 830
Plant Biol 6 20 831
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN 832
(2005) MYB98 is required for pollen tube guidance and synergid cell differentiation 833
in Arabidopsis Plant Cell 17 2981-2992 834
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional 835
characterization of enone oxidoreductases from strawberry and tomato fruit J 836
Agric Food Chem 55 6705-6711 837
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You 838
J-S Rohloff J Randall SK Alsheikh M (2012) Proteomic study of 839
low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ 840
in cold tolerance Plant Physiol 159 1787-1805 841
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional 842
characterization of four APETALA2-family genes (RAP26 RAP26L DREB19 843
and DREB26) in Arabidopsis Plant Mol Biol 75 107-127 844
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
30
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon 845
J Gupta V (2013) An oxidoreductase from lsquoAlphonsorsquo mango catalyzing 846
biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494 847
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in 848
strawberries Z Lebensm-Unters Forsch 195 120-123 849
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X 850
(2015) Label-free quantitative proteomics to investigate strawberry fruit proteome 851
changes under controlled atmosphere and low temperature storage J Proteomics 852
120 44-57 853
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 854
cooperates with CitWRKY1 to participate in citric acid degradation via 855
up-regulation of CitAco3 J Exp Bot 68 3419-3426 856
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription 857
factor CitERF71 activates the terpene synthase gene CitTPS16 involved in the 858
synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938 859
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and 860
transcriptomic analysis of the AP2ERF superfamily in Vitis vinifera BMC 861
Genomics 11 719 862
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive 863
Factor (AP2ERF) transcription factors mediators of stress responses and 864
developmental programs New Phytol 199 639-649 865
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 866
interacting with EOBI negatively regulates fragrance biosynthesis in petunia 867
flowers New Phytol 215 1490-1502 868
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu 869
CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 in regulating 870
anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) 871
during anthocyanin biosynthesis Plant Cell Tissue Organ Cult 115 285-298 872
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
31
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao 873
CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphate signaling and 874
homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597 875
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC 876
Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL 877
Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor 878
regulates eugenol production in ripe strawberry fruit receptacles Plant Physiol 168 879
598-614 880
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics 881
and volatile constituents of strawberry (cv Cigaline) during maturation J Agric 882
Food Chem 52 1248-1254 883
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS 884
(2012) Ethylene-responsive transcription factors interact with promoters of ADH 885
and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 886
63 6393-6405 887
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM 888
Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-Franco A 889
Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific 890
transcription factor FaDOF2 regulates the production of eugenol in ripe fruit 891
receptacles J Exp Bot 68 4529-4543 892
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) 893
Comparison and verification of the genes involved in ethylene biosynthesis and 894
signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44 895
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the 896
ERF gene family in Arabidopsis and rice Plant Physiol 140 411-432 897
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in 898
sour cherry and strawberry and the heterologous expression of CBF1 in strawberry 899
J Am Soc Hortic Sci 127 489-494 900
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech 901
JC Ohme-Takagi M Regad F Bouzayen M (2012) Functional analysis and 902
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32
binding affinity of tomato ethylene response factors provide insight on the 903
molecular bases of plant differential responses to ethylene BMC Plant Biol 12 190 904
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) 905
Methylpentoses are possible precursors of furanones in fruits Prikl Biokhim 906
Mikrobiol 28 123-127 907
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery 908
of synergid-expressed genes encoding filiform apparatus localized proteins Plant 909
Cell 19 2557-2568 910
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria 911
vesca L compared to those of cultivated berries Fragariatimes ananassa cv Senga 912
Sengana J Agric Food Chem 27 19-22 913
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W 914
Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of the strawberry 915
flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone 916
oxidoreductase Plant Cell 18 1023-1037 917
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L 918
Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim M Broun P Zhang 919
JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription 920
factors genome-wide comparative analysis among eukaryotes Science 290 921
2105-2110 922
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the 923
formation of 25-dimethyl-4-hydroxy-3(2H)-furanone in detached ripening 924
strawberry fruits J Agric Food Chem 46 1488-1493 925
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 926
25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in 927
strawberry fruits Phytochemistry 43 155-159 928
Schwab W (1998) Application of stable isotope ratio analysis explaining the 929
bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone in plants by a biological 930
maillard reaction J Agric Food Chem 46 2266ndash2269 931
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33
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) 932
Molecules 18 6936-6951 933
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard 934
products Recent Res Dev Phytochem 1 643-673 935
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL 936
Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJ Sims CA 937
Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical 938
compositions a seasonal influence and effects on sensory perception PLoS One 9 939
e88446 940
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) 941
Identification phylogeny and transcript profiling of ERF family genes during 942
development and abiotic stress treatments in tomato Mol Genet Genomics 284 943
455-475 944
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) 945
CitAP210 activation of the terpene synthase CsTPS1 is associated with the 946
synthesis of (+)-valencene in lsquoNewhallrsquo orange J Exp Bot 67 4105-4115 947
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes 948
Dev Genes Evol 214 105-114 949
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K 950
Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the 951
key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151 952
Spitzer-Rimon B Farhi M Albo B Cnarsquoani A Ben Zvi MM Masci T Edelbaum 953
O Yu YX Shklarman E Ovadis M Vainstein A (2012) The R2R3-MYB-like 954
regulatory factor EOBI acting downstream of EOBII regulates scent production 955
by activating ODO1 and structural scent-related genes in petunia Plant Cell 24 956
5089-5105 957
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp 958
Bot 68 4407-4409 959
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla 960
JF Amaya I Giavalisco P Fernie AR Botella MA Valpuesta V (2015) Central 961
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34
role of FaGAMYB in the transition of the strawberry receptacle from development 962
to ripening New Phytol 208 482-496 963
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 964
regulates fragrance biosynthesis in petunia flowers Plant Cell 17 1612-1624 965
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS 966
(2018) The potassium channel FaTPK1 plays a critical role in fruit quality 967
formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748 968
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) 969
Isolation cloning and expression of a multifunctional O-methyltransferase capable 970
of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma 971
compounds in strawberry fruits Plant J 31 755-765 972
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor 973
types their evolutionary origin and species distribution In A handbook of 974
transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular 975
Biochemistry 52 25-73 976
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of 977
odor (Buettner A Ed) Springer Cham 9-10 978
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS 979
(2014) Isolation classification and transcription profiles of the AP2ERF 980
transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271 981
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in 982
regulation of fruit quality Crit Rev Plant Sci 35 120-130 983
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ 984
Zhang SL Wu J (2017) Map-based cloning of the pear gene MYB114 identifies an 985
interaction with other transcription factors to coordinately regulate fruit 986
anthocyanin biosynthesis Plant J 92 437-451 987
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes 988
involved in regulating fruit ripening Plant Physiol 153 1280-1292 989
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35
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) 990
Expression of ethylene response genes during persimmon fruit astringency removal 991
Planta 235 895-906 992
Zabetakis I Gramshaw JW Robinson DS (1999) 993
25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis and 994
biosynthesis-a review Food Chem 65 139-151 995
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci 996
Food Agric 74 421-434 997
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 998
an AP2ERF gene is a novel regulator of fruit lignification induced by chilling 999
injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1000
1325-1334 1001
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation 1002
classification and transcription profiles of the Ethylene Response Factors (ERFs) in 1003
ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215 1004
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML 1005
(2012) Genome-wide analysis of the AP2ERF superfamily in peach (Prunus 1006
persica) Genet Mol Res 11 4788-4809 1007
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and 1008
expression analysis of a CRTDRE-binding factor gene FaCBF1 from Fragaria times 1009
ananassa Acta Hortic 41 240-248 1010
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The 1011
Arabidopsis AP2ERF transcription factor RAP26 participates in ABA salt and 1012
osmotic stress responses Gene 457 1-12 1013
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B 1014
Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) Genome-wide 1015
analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic 1016
(Amsterdam) 123 73-81 1017
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF 1018
Valpuesta V Botella MA Granell A Amaya I (2012) Genetic analysis of 1019
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
36
strawberry fruit aroma and identification of O-methyltransferase FaOMT as the 1020
locus controlling natural variation in mesifurane content Plant Physiol 159 1021
851-870 1022
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Parsed CitationsAgarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression of PgDREB2A transcription factor enhances abioticstress tolerance and activates downstream stress-responsive genes Mol Biol Rep 37 1125-1135
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Araguumlez I Osorio S Hoffmann T Rambla JL Medina-Escobar N Granell A Botella MAacute Schwab W Valpuesta V (2013) Eugenolproduction in achenes and receptacles of strawberry fruits is catalyzed by synthases exhibiting distinct kinetics Plant Physiol 163 946-958
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Carvalho RF Carvalho SD OGrady K Folta KM (2016) Agroinfiltration of strawberry fruit - a powerful transient expression system forgene validation Curr Plant Biol 6 19-37
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic (Amsterdam) 210 34-40Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating RNA from pine trees Plant Mol Biol Rep 11 113-116Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC Clark DG (2011) PhMYB4 fine-tunes the floral volatilesignature of Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz EA Taylor MG Smits-Kroon MT Schuurink RC HaringMA Giovannoni J Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic pathway by ectopic expression of aMYB transcription factor in tomato fruit Plant Cell 23 2738-2753
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan XW Yang ZY (2017) Differential responses of fourbiosynthetic pathways of aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under interaction of light andtemperature Food Chem 221 356-364
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of differentially-expressed genes during somatic embryogenesis inFragaria times ananassa Duch Benihopp J Hortic Sci Biotechnol 90 671-681
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 transcriptionally regulates chilling-induced lignification ofloquat fruit via physical interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM (2004) Functional interactions between a glutaminesynthetase promoter and MYB proteins Plant J 39 513-526
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) Sucrose nonfermenting1-related protein kinase26 anortholog of open stomata1 is a negative regulator of strawberry fruit development and ripening Plant Physiol 167 915-930
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene expression in strawberry fruit (Fragaria times ananassa) byagroinfiltration a rapid assay for gene function analysis Plant J 48 818-826
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of selected aroma-active compounds in strawberries byheadspace solid-phase microextraction gas chromatography and correlation with sensory descriptive analysis J Food Sci 72 S487-S496
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid plays an important role in the regulation of strawberry fruitripening Plant Physiol 157 188-199
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of NaCl-stressed Arabidopsis roots reveals novel classes ofresponsive genes BMC Plant Biol 6 20
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN (2005) MYB98 is required for pollen tube guidance andsynergid cell differentiation in Arabidopsis Plant Cell 17 2981-2992
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional characterization of enone oxidoreductases from strawberry andtomato fruit J Agric Food Chem 55 6705-6711
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You J-S Rohloff J Randall SK Alsheikh M (2012) Proteomicstudy of low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ in cold tolerance Plant Physiol 159 1787-1805
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional characterization of four APETALA2-family genes (RAP26 RAP26LDREB19 and DREB26) in Arabidopsis Plant Mol Biol 75 107-127
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon J Gupta V (2013) An oxidoreductase from Alphonsomango catalyzing biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in strawberries Z Lebensm-Unters Forsch 195 120-123Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X (2015) Label-free quantitative proteomics to investigatestrawberry fruit proteome changes under controlled atmosphere and low temperature storage J Proteomics 120 44-57
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 cooperates with CitWRKY1 to participate in citric aciddegradation via up-regulation of CitAco3 J Exp Bot 68 3419-3426
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription factor CitERF71 activates the terpene synthase geneCitTPS16 involved in the synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and transcriptomic analysis of the AP2ERF superfamily inVitis vinifera BMC Genomics 11 719
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive Factor (AP2ERF) transcription factors mediators of stressresponses and developmental programs New Phytol 199 639-649
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 interacting with EOBI negatively regulates fragrancebiosynthesis in petunia flowers New Phytol 215 1490-1502
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
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24
determine significant differences between two groups in this study Microsoft Excel 666
was used to perform linear regressive analysis significant differences were 667
determined by SPSS Statistics 200 and scatter plots were prepared with Origin80 668
Least significant difference (LSD) at the 5 level was calculated using Microsoft 669
Excel Figures were prepared with Origin80 (Microcal Software Inc Northampton 670
MA USA) The online tool MetaboAnalyst 36 (httpwwwmetaboanalystca) was 671
used to analyse the transcript abundance of the AP2ERF genes 672
673
Accession numbers 674
Sequence data from this article have been deposited in GenBank under the accession 675
numbers MH332903-MH333022 for AP2ERF genes in Fragaria times ananassa and 676
MH333023 for FaMYB98 GenBank numbers for FaQR and FaOMT were 677
AY1588361 (Raab et al 2006) and AF2204912 (Wein et al 2002) 678
679
Supplemental Material 680
Supplemental Figure S1 Phylogenetic analysis of FaAP2ERF and Arabidopsis 681
AP2ERF proteins 682
Supplemental Figure S2 Analysis of FaAP2ERF gene expression patterns in 683
strawberry fruit during development and ripening 684
Supplemental Figure S3 Contents of furanones in fruit of strawberry cultivars 685
Supplemental Figure S4 Relative expression of FaERF9 in FaERF9-FaMYB98- 686
and FaERF9-overexpressing fruits 687
Supplemental Figure S5 Subcellular localization of FaMYB98 688
Supplemental Figure S6 The combined activation effects of FaERF9FaMYB98 on 689
the FaOMT promoter 690
Supplemental Figure S7 Relative expression of FaOMT in 691
FaERF9-overexpressing fruits 692
Supplemental Table S1 AP2ERF superfamily genes in Fragaria times ananassa 693
Supplemental Table S2 Classification of the AP2ERF superfamily members in 694
Fragaria times ananassa 695
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
25
Supplemental Table S3 Furanone content in FaERF9-FaMYB98- and 696
FaERF9-overexpressing fruits 697
Supplemental Table S4 Primers used for reverse transcription quantitative PCR 698
(RT-qPCR) 699
Supplemental Table S5 Primers used to amplify the full-length coding sequences of 700
AP2ERF genes and FaMYB98 in strawberry (Fragaria times ananassa) 701
Supplemental Table S6 Primers used for vector construction 702
703
Acknowledgments 704
This research was supported by the National Key Research and Development 705
Program (2016YFD0400101) the Project of the Science and Technology Department 706
of Zhejiang Province (2016C04001) and the 111 Project (B17039) 707
708
Figure legends 709
Figure 1 Changes in furanone content and furanone biosynthetic genes during 710
strawberry (Fragaria times ananassa Duch cv Yuexin) fruit development and ripening 711
A Fruits were collected at four ripening stages G (green stage) T (turning stage) IR 712
(intermediate red stage) R (full red stage) B Changes in the contents of furaneol 713
(HDMF) and mesifurane (DMMF) HDMF content was calculated using a standard 714
curve of HDMF while DMMF content was calculated with an internal standard as the 715
reference C Expression levels of FaQR and FaOMT The expression levels of each 716
gene were calculated relative to corresponding values in the basal section at the R 717
stage SEs were calculated from three replicates and LSD values represent the least 718
significant differences at p = 005 719
Figure 2 Regulatory effects of FaAP2ERF on the promoter of FaQR LUCREN 720
values of the empty vector on FaQR promoter were used as the calibrator set as 1 721
and SEs were calculated from five replicates statistical significance was determined 722
by Studentrsquos two-tailed t test ( plt0001) 723
Figure 3 Expression and the subcellular localization of FaERF9 A The expression 724
levels were calculated relative to the levels in the basal section at the R stage B 725
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
26
Subcellular localization analysis was performed in tobacco leaves The tobacco used 726
in the assay was stably transformed with a specific nucleus localized red fluorescence 727
protein construct and the red fluorescence indicates the nucleus-localized signal 728
(NLS) Scale bar = 25 microm SEs were calculated from three replicates 729
Figure 4 Transient overexpression of FaERF9 in strawberry fruit A Relative 730
expression of FaQR and FaERF9 in FaERF9-OX fruit 7 days after infiltration The 731
expression was calculated relative to the average value in control (SK) fruits B 732
HDMF and DMMF content in FaERF9-OX fruit The content of both furanones 733
were quantified using the peak area of the internal standard (2-octanol) as the 734
reference SEs were calculated from three replicates Statistical significance was 735
determined by Studentrsquos two-tailed t test ( plt005 plt001 plt0001) 736
Figure 5 Scatter plots of 11 strawberry cultivars A Linear regression analysis 737
between FaERF9 expression and FaQR expression B Linear regression analysis 738
between FaERF9 expression and furanone content The relative expression was 739
normalized to that of the housekeeping gene FaRIB413 and furanone content was 740
calculated with internal standard as the reference Significant differences were 741
determined by SPSS Statistics 200 742
Figure 6 Interactions of FaERF9 and FaMYB98 with the FaQR promoter A Yeast 743
one-hybrid analysis of the interaction of FaERF9 and FaQR promoter B Yeast 744
one-hybrid analysis of the interaction of FaMYB98 and FaQR promoter C 745
Regulatory effect of FaMYB98 on the FaQR promoter Auto-activation was tested on 746
SD-Ura (synthetically defined medium without uracil) in presence of Aureobasidin A 747
(AbA) and physical interaction was determined on SD-Leu (synthetically defined 748
medium without leucine) in presence of AbA LUCREN values of the empty vector 749
on FaQR promoter were used as the calibrator set as 1 and error bars were calculated 750
from five replicates Statistical significance was determined by Studentrsquos two-tailed t 751
test ( plt005 plt001 plt0001) 752
Figure 7 Electrophoretic mobility shift assay of FaMYB98 binding to FaQR 753
promoter A The probe sequence used for EMSA and mutated nucleotides are 754
indicated with lowercase letters B Purified DNA-binding domain of FaMYB98 755
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
27
protein and biotin-labelled DNA probe were mixed and analysed on 6 native 756
polyacrylamide gels and then photographed Presence or absence of specific probes is 757
marked by the symbol + or - 758
Figure 8 The combined activation effects of FaERF9FaMYB98 on the FaQR 759
promoter LUCREN values obtained with the empty vector and FaQR promoter were 760
used as the calibrator set as 1 and error bars were calculated from five replicates 761
Figure 9 Yeast two-hybrid analysis of the protein-protein interactions between 762
FaMYB98 and FaERF9 Positive interactions were determined by the growth of 763
yeast cells on selection plates Bait with pOST acted as positive controls and bait with 764
pPR3 as negative controls DDO synthetically defined medium without tryptophan 765
and leucine QDO synthetically defined medium without tryptophan leucine 766
histidine and adenine QDO+3AT QDO medium supplemented with 1 mM 767
3-aminotriazole 768
Figure 10 BiFC analysis of the protein-protein interactions between FaMYB98 and 769
FaERF9 The pairs of fusion proteins tested were FaMYB98-YFPN+FaERF9-YFPC 770
FaERF9-YFPN+FaMYB98-YFPC FaMYB98-YFPN+FaMYB98-YFPC and 771
FaERF9-YFPN+FaERF9-YFPC The other combinations were negative controls 772
The tobacco used in the assay was stably transformed with a specific 773
nucleus-localized red fluorescence protein construct and the red fluorescence 774
indicated the nucleus-localized signal (NLS) Fluorescence of the yellow fluorescence 775
protein (YFP) visualized the interaction in vivo Scale bar = 25 microm 776
777
Literature Cited 778
779
Agarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression 780
of PgDREB2A transcription factor enhances abiotic stress tolerance and activates 781
downstream stress-responsive genes Mol Biol Rep 37 1125-1135 782
Araguumlez I Osorio S Hoffmann T Rambla JL Medina-Escobar N Granell A 783
Botella MAacute Schwab W Valpuesta V (2013) Eugenol production in achenes and 784
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receptacles of strawberry fruits is catalyzed by synthases exhibiting distinct kinetics 785
Plant Physiol 163 946-958 786
Carvalho RF Carvalho SD OrsquoGrady K Folta KM (2016) Agroinfiltration of 787
strawberry fruit mdash a powerful transient expression system for gene validation Curr 788
Plant Biol 6 19-37 789
Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic 790
(Amsterdam) 210 34-40 791
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating 792
RNA from pine trees Plant Mol Biol Rep 11 113-116 793
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC 794
Clark DG (2011) PhMYB4 fine-tunes the floral volatile signature of 795
Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143 796
Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz 797
EA Taylor MG Smits-Kroon MT Schuurink RC Haring MA Giovannoni J 798
Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic 799
pathway by ectopic expression of a MYB transcription factor in tomato fruit Plant 800
Cell 23 2738-2753 801
Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan 802
XW Yang ZY (2017) Differential responses of four biosynthetic pathways of 803
aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under 804
interaction of light and temperature Food Chem 221 356-364 805
Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of 806
differentially-expressed genes during somatic embryogenesis in Fragaria times 807
ananassa Duch lsquoBenihopprsquo J Hortic Sci Biotechnol 90 671-681 808
Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 809
transcriptionally regulates chilling-induced lignification of loquat fruit via physical 810
interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136 811
Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM 812
(2004) Functional interactions between a glutamine synthetase promoter and MYB 813
proteins Plant J 39 513-526 814
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Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) 815
Sucrose nonfermenting1-related protein kinase26 an ortholog of open stomata1 is 816
a negative regulator of strawberry fruit development and ripening Plant Physiol 817
167 915-930 818
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene 819
expression in strawberry fruit (Fragaria times ananassa) by agroinfiltration a rapid 820
assay for gene function analysis Plant J 48 818-826 821
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of 822
selected aroma-active compounds in strawberries by headspace solid-phase 823
microextraction gas chromatography and correlation with sensory descriptive 824
analysis J Food Sci 72 S487-S496 825
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid 826
plays an important role in the regulation of strawberry fruit ripening Plant Physiol 827
157 188-199 828
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of 829
NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes BMC 830
Plant Biol 6 20 831
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN 832
(2005) MYB98 is required for pollen tube guidance and synergid cell differentiation 833
in Arabidopsis Plant Cell 17 2981-2992 834
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional 835
characterization of enone oxidoreductases from strawberry and tomato fruit J 836
Agric Food Chem 55 6705-6711 837
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You 838
J-S Rohloff J Randall SK Alsheikh M (2012) Proteomic study of 839
low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ 840
in cold tolerance Plant Physiol 159 1787-1805 841
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional 842
characterization of four APETALA2-family genes (RAP26 RAP26L DREB19 843
and DREB26) in Arabidopsis Plant Mol Biol 75 107-127 844
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30
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon 845
J Gupta V (2013) An oxidoreductase from lsquoAlphonsorsquo mango catalyzing 846
biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494 847
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in 848
strawberries Z Lebensm-Unters Forsch 195 120-123 849
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X 850
(2015) Label-free quantitative proteomics to investigate strawberry fruit proteome 851
changes under controlled atmosphere and low temperature storage J Proteomics 852
120 44-57 853
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 854
cooperates with CitWRKY1 to participate in citric acid degradation via 855
up-regulation of CitAco3 J Exp Bot 68 3419-3426 856
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription 857
factor CitERF71 activates the terpene synthase gene CitTPS16 involved in the 858
synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938 859
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and 860
transcriptomic analysis of the AP2ERF superfamily in Vitis vinifera BMC 861
Genomics 11 719 862
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive 863
Factor (AP2ERF) transcription factors mediators of stress responses and 864
developmental programs New Phytol 199 639-649 865
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 866
interacting with EOBI negatively regulates fragrance biosynthesis in petunia 867
flowers New Phytol 215 1490-1502 868
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu 869
CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 in regulating 870
anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) 871
during anthocyanin biosynthesis Plant Cell Tissue Organ Cult 115 285-298 872
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
31
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao 873
CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphate signaling and 874
homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597 875
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC 876
Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL 877
Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor 878
regulates eugenol production in ripe strawberry fruit receptacles Plant Physiol 168 879
598-614 880
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics 881
and volatile constituents of strawberry (cv Cigaline) during maturation J Agric 882
Food Chem 52 1248-1254 883
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS 884
(2012) Ethylene-responsive transcription factors interact with promoters of ADH 885
and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 886
63 6393-6405 887
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM 888
Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-Franco A 889
Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific 890
transcription factor FaDOF2 regulates the production of eugenol in ripe fruit 891
receptacles J Exp Bot 68 4529-4543 892
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) 893
Comparison and verification of the genes involved in ethylene biosynthesis and 894
signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44 895
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the 896
ERF gene family in Arabidopsis and rice Plant Physiol 140 411-432 897
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in 898
sour cherry and strawberry and the heterologous expression of CBF1 in strawberry 899
J Am Soc Hortic Sci 127 489-494 900
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech 901
JC Ohme-Takagi M Regad F Bouzayen M (2012) Functional analysis and 902
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
32
binding affinity of tomato ethylene response factors provide insight on the 903
molecular bases of plant differential responses to ethylene BMC Plant Biol 12 190 904
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) 905
Methylpentoses are possible precursors of furanones in fruits Prikl Biokhim 906
Mikrobiol 28 123-127 907
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery 908
of synergid-expressed genes encoding filiform apparatus localized proteins Plant 909
Cell 19 2557-2568 910
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria 911
vesca L compared to those of cultivated berries Fragariatimes ananassa cv Senga 912
Sengana J Agric Food Chem 27 19-22 913
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W 914
Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of the strawberry 915
flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone 916
oxidoreductase Plant Cell 18 1023-1037 917
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L 918
Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim M Broun P Zhang 919
JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription 920
factors genome-wide comparative analysis among eukaryotes Science 290 921
2105-2110 922
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the 923
formation of 25-dimethyl-4-hydroxy-3(2H)-furanone in detached ripening 924
strawberry fruits J Agric Food Chem 46 1488-1493 925
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 926
25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in 927
strawberry fruits Phytochemistry 43 155-159 928
Schwab W (1998) Application of stable isotope ratio analysis explaining the 929
bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone in plants by a biological 930
maillard reaction J Agric Food Chem 46 2266ndash2269 931
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
33
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) 932
Molecules 18 6936-6951 933
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard 934
products Recent Res Dev Phytochem 1 643-673 935
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL 936
Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJ Sims CA 937
Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical 938
compositions a seasonal influence and effects on sensory perception PLoS One 9 939
e88446 940
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) 941
Identification phylogeny and transcript profiling of ERF family genes during 942
development and abiotic stress treatments in tomato Mol Genet Genomics 284 943
455-475 944
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) 945
CitAP210 activation of the terpene synthase CsTPS1 is associated with the 946
synthesis of (+)-valencene in lsquoNewhallrsquo orange J Exp Bot 67 4105-4115 947
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes 948
Dev Genes Evol 214 105-114 949
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K 950
Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the 951
key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151 952
Spitzer-Rimon B Farhi M Albo B Cnarsquoani A Ben Zvi MM Masci T Edelbaum 953
O Yu YX Shklarman E Ovadis M Vainstein A (2012) The R2R3-MYB-like 954
regulatory factor EOBI acting downstream of EOBII regulates scent production 955
by activating ODO1 and structural scent-related genes in petunia Plant Cell 24 956
5089-5105 957
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp 958
Bot 68 4407-4409 959
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla 960
JF Amaya I Giavalisco P Fernie AR Botella MA Valpuesta V (2015) Central 961
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34
role of FaGAMYB in the transition of the strawberry receptacle from development 962
to ripening New Phytol 208 482-496 963
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 964
regulates fragrance biosynthesis in petunia flowers Plant Cell 17 1612-1624 965
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS 966
(2018) The potassium channel FaTPK1 plays a critical role in fruit quality 967
formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748 968
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) 969
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Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of 977
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Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS 979
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Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in 982
regulation of fruit quality Crit Rev Plant Sci 35 120-130 983
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ 984
Zhang SL Wu J (2017) Map-based cloning of the pear gene MYB114 identifies an 985
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Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes 988
involved in regulating fruit ripening Plant Physiol 153 1280-1292 989
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35
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) 990
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injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1000
1325-1334 1001
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation 1002
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expression analysis of a CRTDRE-binding factor gene FaCBF1 from Fragaria times 1009
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Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The 1011
Arabidopsis AP2ERF transcription factor RAP26 participates in ABA salt and 1012
osmotic stress responses Gene 457 1-12 1013
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B 1014
Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) Genome-wide 1015
analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic 1016
(Amsterdam) 123 73-81 1017
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF 1018
Valpuesta V Botella MA Granell A Amaya I (2012) Genetic analysis of 1019
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36
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locus controlling natural variation in mesifurane content Plant Physiol 159 1021
851-870 1022
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
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wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
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Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive Factor (AP2ERF) transcription factors mediators of stressresponses and developmental programs New Phytol 199 639-649
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Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 interacting with EOBI negatively regulates fragrancebiosynthesis in petunia flowers New Phytol 215 1490-1502
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Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 inregulating anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) during anthocyanin biosynthesis Plant CellTissue Organ Cult 115 285-298
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Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphatesignaling and homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor regulates eugenol production in ripe strawberry fruitreceptacles Plant Physiol 168 598-614
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics and volatile constituents of strawberry (cv Cigaline)during maturation J Agric Food Chem 52 1248-1254
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS (2012) Ethylene-responsive transcription factors interact withpromoters of ADH and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 63 6393-6405
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-FrancoA Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific transcription factor FaDOF2 regulates the production ofeugenol in ripe fruit receptacles J Exp Bot 68 4529-4543
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) Comparison and verification of the genes involved in ethylenebiosynthesis and signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice Plant Physiol140 411-432
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in sour cherry and strawberry and the heterologousexpression of CBF1 in strawberry J Am Soc Hortic Sci 127 489-494
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech JC Ohme-Takagi M Regad F Bouzayen M (2012)Functional analysis and binding affinity of tomato ethylene response factors provide insight on the molecular bases of plant differentialresponses to ethylene BMC Plant Biol 12 190
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) Methylpentoses are possible precursors of furanones in fruits PriklBiokhim Mikrobiol 28 123-127
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery of synergid-expressed genes encoding filiformapparatus localized proteins Plant Cell 19 2557-2568
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria vesca L compared to those of cultivated berriesFragariatimes ananassa cv Senga Sengana J Agric Food Chem 27 19-22
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of thestrawberry flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone oxidoreductase Plant Cell 18 1023-1037
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim MBroun P Zhang JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription factors genome-wide comparative analysisamong eukaryotes Science 290 2105-2110
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the formation of 25-dimethyl-4-hydroxy-3(2H)-furanonein detached ripening strawberry fruits J Agric Food Chem 46 1488-1493
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in strawberry fruits Phytochemistry 43 155-159
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (1998) Application of stable isotope ratio analysis explaining the bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone inplants by a biological maillard reaction J Agric Food Chem 46 2266ndash2269
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) Molecules 18 6936-6951Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard products Recent Res Dev Phytochem 1 643-673Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJSims CA Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical compositions a seasonal influence and effects on sensoryperception PLoS One 9 e88446
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) Identification phylogeny and transcript profiling of ERFfamily genes during development and abiotic stress treatments in tomato Mol Genet Genomics 284 455-475
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) CitAP210 activation of the terpene synthase CsTPS1 isassociated with the synthesis of (+)-valencene in Newhall orange J Exp Bot 67 4105-4115
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes Dev Genes Evol 214 105-114Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Spitzer-Rimon B Farhi M Albo B Cnaani A Ben Zvi MM Masci T Edelbaum O Yu YX Shklarman E Ovadis M Vainstein A (2012) TheR2R3-MYB-like regulatory factor EOBI acting downstream of EOBII regulates scent production by activating ODO1 and structuralscent-related genes in petunia Plant Cell 24 5089-5105
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp Bot 68 4407-4409Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla JF Amaya I Giavalisco P Fernie AR Botella MAValpuesta V (2015) Central role of FaGAMYB in the transition of the strawberry receptacle from development to ripening New Phytol208 482-496
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 regulates fragrance biosynthesis in petunia flowers PlantCell 17 1612-1624
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS (2018) The potassium channel FaTPK1 plays a critical role infruit quality formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748
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Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) Isolation cloning and expression of a multifunctional O- wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma compounds in strawberry fruitsPlant J 31 755-765
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Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor types their evolutionary origin and speciesdistribution In A handbook of transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular Biochemistry 52 25-73
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of odor (Buettner A Ed) Springer Cham 9-10Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS (2014) Isolation classification and transcription profiles ofthe AP2ERF transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in regulation of fruit quality Crit Rev Plant Sci 35 120-130
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ Zhang SL Wu J (2017) Map-based cloning of the pear geneMYB114 identifies an interaction with other transcription factors to coordinately regulate fruit anthocyanin biosynthesis Plant J 92437-451
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes involved in regulating fruit ripening Plant Physiol 1531280-1292
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Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) Expression of ethylene response genes during persimmonfruit astringency removal Planta 235 895-906
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zabetakis I Gramshaw JW Robinson DS (1999) 25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis andbiosynthesis-a review Food Chem 65 139-151
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci Food Agric 74 421-434Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 an AP2ERF gene is a novel regulator of fruit lignificationinduced by chilling injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1325-1334
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Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation classification and transcription profiles of the Ethylene ResponseFactors (ERFs) in ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215
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Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML (2012) Genome-wide analysis of the AP2ERF superfamily inpeach (Prunus persica) Genet Mol Res 11 4788-4809
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Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and expression analysis of a CRTDRE-binding factor gene FaCBF1from Fragaria times ananassa Acta Hortic 41 240-248
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The Arabidopsis AP2ERF transcription factor RAP26 participatesin ABA salt and osmotic stress responses Gene 457 1-12
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Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Genome-wide analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic (Amsterdam) 123 73-81Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF Valpuesta V Botella MA Granell A Amaya I (2012) Geneticanalysis of strawberry fruit aroma and identification of O-methyltransferase FaOMT as the locus controlling natural variation inmesifurane content Plant Physiol 159 851-870
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wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
25
Supplemental Table S3 Furanone content in FaERF9-FaMYB98- and 696
FaERF9-overexpressing fruits 697
Supplemental Table S4 Primers used for reverse transcription quantitative PCR 698
(RT-qPCR) 699
Supplemental Table S5 Primers used to amplify the full-length coding sequences of 700
AP2ERF genes and FaMYB98 in strawberry (Fragaria times ananassa) 701
Supplemental Table S6 Primers used for vector construction 702
703
Acknowledgments 704
This research was supported by the National Key Research and Development 705
Program (2016YFD0400101) the Project of the Science and Technology Department 706
of Zhejiang Province (2016C04001) and the 111 Project (B17039) 707
708
Figure legends 709
Figure 1 Changes in furanone content and furanone biosynthetic genes during 710
strawberry (Fragaria times ananassa Duch cv Yuexin) fruit development and ripening 711
A Fruits were collected at four ripening stages G (green stage) T (turning stage) IR 712
(intermediate red stage) R (full red stage) B Changes in the contents of furaneol 713
(HDMF) and mesifurane (DMMF) HDMF content was calculated using a standard 714
curve of HDMF while DMMF content was calculated with an internal standard as the 715
reference C Expression levels of FaQR and FaOMT The expression levels of each 716
gene were calculated relative to corresponding values in the basal section at the R 717
stage SEs were calculated from three replicates and LSD values represent the least 718
significant differences at p = 005 719
Figure 2 Regulatory effects of FaAP2ERF on the promoter of FaQR LUCREN 720
values of the empty vector on FaQR promoter were used as the calibrator set as 1 721
and SEs were calculated from five replicates statistical significance was determined 722
by Studentrsquos two-tailed t test ( plt0001) 723
Figure 3 Expression and the subcellular localization of FaERF9 A The expression 724
levels were calculated relative to the levels in the basal section at the R stage B 725
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
26
Subcellular localization analysis was performed in tobacco leaves The tobacco used 726
in the assay was stably transformed with a specific nucleus localized red fluorescence 727
protein construct and the red fluorescence indicates the nucleus-localized signal 728
(NLS) Scale bar = 25 microm SEs were calculated from three replicates 729
Figure 4 Transient overexpression of FaERF9 in strawberry fruit A Relative 730
expression of FaQR and FaERF9 in FaERF9-OX fruit 7 days after infiltration The 731
expression was calculated relative to the average value in control (SK) fruits B 732
HDMF and DMMF content in FaERF9-OX fruit The content of both furanones 733
were quantified using the peak area of the internal standard (2-octanol) as the 734
reference SEs were calculated from three replicates Statistical significance was 735
determined by Studentrsquos two-tailed t test ( plt005 plt001 plt0001) 736
Figure 5 Scatter plots of 11 strawberry cultivars A Linear regression analysis 737
between FaERF9 expression and FaQR expression B Linear regression analysis 738
between FaERF9 expression and furanone content The relative expression was 739
normalized to that of the housekeeping gene FaRIB413 and furanone content was 740
calculated with internal standard as the reference Significant differences were 741
determined by SPSS Statistics 200 742
Figure 6 Interactions of FaERF9 and FaMYB98 with the FaQR promoter A Yeast 743
one-hybrid analysis of the interaction of FaERF9 and FaQR promoter B Yeast 744
one-hybrid analysis of the interaction of FaMYB98 and FaQR promoter C 745
Regulatory effect of FaMYB98 on the FaQR promoter Auto-activation was tested on 746
SD-Ura (synthetically defined medium without uracil) in presence of Aureobasidin A 747
(AbA) and physical interaction was determined on SD-Leu (synthetically defined 748
medium without leucine) in presence of AbA LUCREN values of the empty vector 749
on FaQR promoter were used as the calibrator set as 1 and error bars were calculated 750
from five replicates Statistical significance was determined by Studentrsquos two-tailed t 751
test ( plt005 plt001 plt0001) 752
Figure 7 Electrophoretic mobility shift assay of FaMYB98 binding to FaQR 753
promoter A The probe sequence used for EMSA and mutated nucleotides are 754
indicated with lowercase letters B Purified DNA-binding domain of FaMYB98 755
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
27
protein and biotin-labelled DNA probe were mixed and analysed on 6 native 756
polyacrylamide gels and then photographed Presence or absence of specific probes is 757
marked by the symbol + or - 758
Figure 8 The combined activation effects of FaERF9FaMYB98 on the FaQR 759
promoter LUCREN values obtained with the empty vector and FaQR promoter were 760
used as the calibrator set as 1 and error bars were calculated from five replicates 761
Figure 9 Yeast two-hybrid analysis of the protein-protein interactions between 762
FaMYB98 and FaERF9 Positive interactions were determined by the growth of 763
yeast cells on selection plates Bait with pOST acted as positive controls and bait with 764
pPR3 as negative controls DDO synthetically defined medium without tryptophan 765
and leucine QDO synthetically defined medium without tryptophan leucine 766
histidine and adenine QDO+3AT QDO medium supplemented with 1 mM 767
3-aminotriazole 768
Figure 10 BiFC analysis of the protein-protein interactions between FaMYB98 and 769
FaERF9 The pairs of fusion proteins tested were FaMYB98-YFPN+FaERF9-YFPC 770
FaERF9-YFPN+FaMYB98-YFPC FaMYB98-YFPN+FaMYB98-YFPC and 771
FaERF9-YFPN+FaERF9-YFPC The other combinations were negative controls 772
The tobacco used in the assay was stably transformed with a specific 773
nucleus-localized red fluorescence protein construct and the red fluorescence 774
indicated the nucleus-localized signal (NLS) Fluorescence of the yellow fluorescence 775
protein (YFP) visualized the interaction in vivo Scale bar = 25 microm 776
777
Literature Cited 778
779
Agarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression 780
of PgDREB2A transcription factor enhances abiotic stress tolerance and activates 781
downstream stress-responsive genes Mol Biol Rep 37 1125-1135 782
Araguumlez I Osorio S Hoffmann T Rambla JL Medina-Escobar N Granell A 783
Botella MAacute Schwab W Valpuesta V (2013) Eugenol production in achenes and 784
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28
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Plant Physiol 163 946-958 786
Carvalho RF Carvalho SD OrsquoGrady K Folta KM (2016) Agroinfiltration of 787
strawberry fruit mdash a powerful transient expression system for gene validation Curr 788
Plant Biol 6 19-37 789
Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic 790
(Amsterdam) 210 34-40 791
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating 792
RNA from pine trees Plant Mol Biol Rep 11 113-116 793
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC 794
Clark DG (2011) PhMYB4 fine-tunes the floral volatile signature of 795
Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143 796
Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz 797
EA Taylor MG Smits-Kroon MT Schuurink RC Haring MA Giovannoni J 798
Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic 799
pathway by ectopic expression of a MYB transcription factor in tomato fruit Plant 800
Cell 23 2738-2753 801
Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan 802
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aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under 804
interaction of light and temperature Food Chem 221 356-364 805
Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of 806
differentially-expressed genes during somatic embryogenesis in Fragaria times 807
ananassa Duch lsquoBenihopprsquo J Hortic Sci Biotechnol 90 671-681 808
Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 809
transcriptionally regulates chilling-induced lignification of loquat fruit via physical 810
interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136 811
Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM 812
(2004) Functional interactions between a glutamine synthetase promoter and MYB 813
proteins Plant J 39 513-526 814
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29
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) 815
Sucrose nonfermenting1-related protein kinase26 an ortholog of open stomata1 is 816
a negative regulator of strawberry fruit development and ripening Plant Physiol 817
167 915-930 818
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene 819
expression in strawberry fruit (Fragaria times ananassa) by agroinfiltration a rapid 820
assay for gene function analysis Plant J 48 818-826 821
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of 822
selected aroma-active compounds in strawberries by headspace solid-phase 823
microextraction gas chromatography and correlation with sensory descriptive 824
analysis J Food Sci 72 S487-S496 825
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid 826
plays an important role in the regulation of strawberry fruit ripening Plant Physiol 827
157 188-199 828
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of 829
NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes BMC 830
Plant Biol 6 20 831
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN 832
(2005) MYB98 is required for pollen tube guidance and synergid cell differentiation 833
in Arabidopsis Plant Cell 17 2981-2992 834
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional 835
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Agric Food Chem 55 6705-6711 837
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You 838
J-S Rohloff J Randall SK Alsheikh M (2012) Proteomic study of 839
low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ 840
in cold tolerance Plant Physiol 159 1787-1805 841
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional 842
characterization of four APETALA2-family genes (RAP26 RAP26L DREB19 843
and DREB26) in Arabidopsis Plant Mol Biol 75 107-127 844
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Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon 845
J Gupta V (2013) An oxidoreductase from lsquoAlphonsorsquo mango catalyzing 846
biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494 847
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in 848
strawberries Z Lebensm-Unters Forsch 195 120-123 849
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X 850
(2015) Label-free quantitative proteomics to investigate strawberry fruit proteome 851
changes under controlled atmosphere and low temperature storage J Proteomics 852
120 44-57 853
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 854
cooperates with CitWRKY1 to participate in citric acid degradation via 855
up-regulation of CitAco3 J Exp Bot 68 3419-3426 856
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription 857
factor CitERF71 activates the terpene synthase gene CitTPS16 involved in the 858
synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938 859
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and 860
transcriptomic analysis of the AP2ERF superfamily in Vitis vinifera BMC 861
Genomics 11 719 862
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive 863
Factor (AP2ERF) transcription factors mediators of stress responses and 864
developmental programs New Phytol 199 639-649 865
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 866
interacting with EOBI negatively regulates fragrance biosynthesis in petunia 867
flowers New Phytol 215 1490-1502 868
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu 869
CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 in regulating 870
anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) 871
during anthocyanin biosynthesis Plant Cell Tissue Organ Cult 115 285-298 872
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31
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao 873
CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphate signaling and 874
homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597 875
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC 876
Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL 877
Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor 878
regulates eugenol production in ripe strawberry fruit receptacles Plant Physiol 168 879
598-614 880
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics 881
and volatile constituents of strawberry (cv Cigaline) during maturation J Agric 882
Food Chem 52 1248-1254 883
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS 884
(2012) Ethylene-responsive transcription factors interact with promoters of ADH 885
and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 886
63 6393-6405 887
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM 888
Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-Franco A 889
Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific 890
transcription factor FaDOF2 regulates the production of eugenol in ripe fruit 891
receptacles J Exp Bot 68 4529-4543 892
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) 893
Comparison and verification of the genes involved in ethylene biosynthesis and 894
signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44 895
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the 896
ERF gene family in Arabidopsis and rice Plant Physiol 140 411-432 897
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in 898
sour cherry and strawberry and the heterologous expression of CBF1 in strawberry 899
J Am Soc Hortic Sci 127 489-494 900
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech 901
JC Ohme-Takagi M Regad F Bouzayen M (2012) Functional analysis and 902
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32
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molecular bases of plant differential responses to ethylene BMC Plant Biol 12 190 904
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Methylpentoses are possible precursors of furanones in fruits Prikl Biokhim 906
Mikrobiol 28 123-127 907
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery 908
of synergid-expressed genes encoding filiform apparatus localized proteins Plant 909
Cell 19 2557-2568 910
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria 911
vesca L compared to those of cultivated berries Fragariatimes ananassa cv Senga 912
Sengana J Agric Food Chem 27 19-22 913
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W 914
Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of the strawberry 915
flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone 916
oxidoreductase Plant Cell 18 1023-1037 917
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L 918
Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim M Broun P Zhang 919
JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription 920
factors genome-wide comparative analysis among eukaryotes Science 290 921
2105-2110 922
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the 923
formation of 25-dimethyl-4-hydroxy-3(2H)-furanone in detached ripening 924
strawberry fruits J Agric Food Chem 46 1488-1493 925
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 926
25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in 927
strawberry fruits Phytochemistry 43 155-159 928
Schwab W (1998) Application of stable isotope ratio analysis explaining the 929
bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone in plants by a biological 930
maillard reaction J Agric Food Chem 46 2266ndash2269 931
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33
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) 932
Molecules 18 6936-6951 933
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard 934
products Recent Res Dev Phytochem 1 643-673 935
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL 936
Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJ Sims CA 937
Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical 938
compositions a seasonal influence and effects on sensory perception PLoS One 9 939
e88446 940
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) 941
Identification phylogeny and transcript profiling of ERF family genes during 942
development and abiotic stress treatments in tomato Mol Genet Genomics 284 943
455-475 944
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) 945
CitAP210 activation of the terpene synthase CsTPS1 is associated with the 946
synthesis of (+)-valencene in lsquoNewhallrsquo orange J Exp Bot 67 4105-4115 947
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes 948
Dev Genes Evol 214 105-114 949
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K 950
Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the 951
key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151 952
Spitzer-Rimon B Farhi M Albo B Cnarsquoani A Ben Zvi MM Masci T Edelbaum 953
O Yu YX Shklarman E Ovadis M Vainstein A (2012) The R2R3-MYB-like 954
regulatory factor EOBI acting downstream of EOBII regulates scent production 955
by activating ODO1 and structural scent-related genes in petunia Plant Cell 24 956
5089-5105 957
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp 958
Bot 68 4407-4409 959
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla 960
JF Amaya I Giavalisco P Fernie AR Botella MA Valpuesta V (2015) Central 961
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34
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to ripening New Phytol 208 482-496 963
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 964
regulates fragrance biosynthesis in petunia flowers Plant Cell 17 1612-1624 965
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS 966
(2018) The potassium channel FaTPK1 plays a critical role in fruit quality 967
formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748 968
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) 969
Isolation cloning and expression of a multifunctional O-methyltransferase capable 970
of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma 971
compounds in strawberry fruits Plant J 31 755-765 972
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor 973
types their evolutionary origin and species distribution In A handbook of 974
transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular 975
Biochemistry 52 25-73 976
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of 977
odor (Buettner A Ed) Springer Cham 9-10 978
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS 979
(2014) Isolation classification and transcription profiles of the AP2ERF 980
transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271 981
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in 982
regulation of fruit quality Crit Rev Plant Sci 35 120-130 983
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ 984
Zhang SL Wu J (2017) Map-based cloning of the pear gene MYB114 identifies an 985
interaction with other transcription factors to coordinately regulate fruit 986
anthocyanin biosynthesis Plant J 92 437-451 987
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes 988
involved in regulating fruit ripening Plant Physiol 153 1280-1292 989
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35
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) 990
Expression of ethylene response genes during persimmon fruit astringency removal 991
Planta 235 895-906 992
Zabetakis I Gramshaw JW Robinson DS (1999) 993
25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis and 994
biosynthesis-a review Food Chem 65 139-151 995
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci 996
Food Agric 74 421-434 997
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 998
an AP2ERF gene is a novel regulator of fruit lignification induced by chilling 999
injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1000
1325-1334 1001
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation 1002
classification and transcription profiles of the Ethylene Response Factors (ERFs) in 1003
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expression analysis of a CRTDRE-binding factor gene FaCBF1 from Fragaria times 1009
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osmotic stress responses Gene 457 1-12 1013
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B 1014
Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) Genome-wide 1015
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Valpuesta V Botella MA Granell A Amaya I (2012) Genetic analysis of 1019
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36
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851-870 1022
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Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
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Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Genome-wide analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic (Amsterdam) 123 73-81Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
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Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
26
Subcellular localization analysis was performed in tobacco leaves The tobacco used 726
in the assay was stably transformed with a specific nucleus localized red fluorescence 727
protein construct and the red fluorescence indicates the nucleus-localized signal 728
(NLS) Scale bar = 25 microm SEs were calculated from three replicates 729
Figure 4 Transient overexpression of FaERF9 in strawberry fruit A Relative 730
expression of FaQR and FaERF9 in FaERF9-OX fruit 7 days after infiltration The 731
expression was calculated relative to the average value in control (SK) fruits B 732
HDMF and DMMF content in FaERF9-OX fruit The content of both furanones 733
were quantified using the peak area of the internal standard (2-octanol) as the 734
reference SEs were calculated from three replicates Statistical significance was 735
determined by Studentrsquos two-tailed t test ( plt005 plt001 plt0001) 736
Figure 5 Scatter plots of 11 strawberry cultivars A Linear regression analysis 737
between FaERF9 expression and FaQR expression B Linear regression analysis 738
between FaERF9 expression and furanone content The relative expression was 739
normalized to that of the housekeeping gene FaRIB413 and furanone content was 740
calculated with internal standard as the reference Significant differences were 741
determined by SPSS Statistics 200 742
Figure 6 Interactions of FaERF9 and FaMYB98 with the FaQR promoter A Yeast 743
one-hybrid analysis of the interaction of FaERF9 and FaQR promoter B Yeast 744
one-hybrid analysis of the interaction of FaMYB98 and FaQR promoter C 745
Regulatory effect of FaMYB98 on the FaQR promoter Auto-activation was tested on 746
SD-Ura (synthetically defined medium without uracil) in presence of Aureobasidin A 747
(AbA) and physical interaction was determined on SD-Leu (synthetically defined 748
medium without leucine) in presence of AbA LUCREN values of the empty vector 749
on FaQR promoter were used as the calibrator set as 1 and error bars were calculated 750
from five replicates Statistical significance was determined by Studentrsquos two-tailed t 751
test ( plt005 plt001 plt0001) 752
Figure 7 Electrophoretic mobility shift assay of FaMYB98 binding to FaQR 753
promoter A The probe sequence used for EMSA and mutated nucleotides are 754
indicated with lowercase letters B Purified DNA-binding domain of FaMYB98 755
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
27
protein and biotin-labelled DNA probe were mixed and analysed on 6 native 756
polyacrylamide gels and then photographed Presence or absence of specific probes is 757
marked by the symbol + or - 758
Figure 8 The combined activation effects of FaERF9FaMYB98 on the FaQR 759
promoter LUCREN values obtained with the empty vector and FaQR promoter were 760
used as the calibrator set as 1 and error bars were calculated from five replicates 761
Figure 9 Yeast two-hybrid analysis of the protein-protein interactions between 762
FaMYB98 and FaERF9 Positive interactions were determined by the growth of 763
yeast cells on selection plates Bait with pOST acted as positive controls and bait with 764
pPR3 as negative controls DDO synthetically defined medium without tryptophan 765
and leucine QDO synthetically defined medium without tryptophan leucine 766
histidine and adenine QDO+3AT QDO medium supplemented with 1 mM 767
3-aminotriazole 768
Figure 10 BiFC analysis of the protein-protein interactions between FaMYB98 and 769
FaERF9 The pairs of fusion proteins tested were FaMYB98-YFPN+FaERF9-YFPC 770
FaERF9-YFPN+FaMYB98-YFPC FaMYB98-YFPN+FaMYB98-YFPC and 771
FaERF9-YFPN+FaERF9-YFPC The other combinations were negative controls 772
The tobacco used in the assay was stably transformed with a specific 773
nucleus-localized red fluorescence protein construct and the red fluorescence 774
indicated the nucleus-localized signal (NLS) Fluorescence of the yellow fluorescence 775
protein (YFP) visualized the interaction in vivo Scale bar = 25 microm 776
777
Literature Cited 778
779
Agarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression 780
of PgDREB2A transcription factor enhances abiotic stress tolerance and activates 781
downstream stress-responsive genes Mol Biol Rep 37 1125-1135 782
Araguumlez I Osorio S Hoffmann T Rambla JL Medina-Escobar N Granell A 783
Botella MAacute Schwab W Valpuesta V (2013) Eugenol production in achenes and 784
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
28
receptacles of strawberry fruits is catalyzed by synthases exhibiting distinct kinetics 785
Plant Physiol 163 946-958 786
Carvalho RF Carvalho SD OrsquoGrady K Folta KM (2016) Agroinfiltration of 787
strawberry fruit mdash a powerful transient expression system for gene validation Curr 788
Plant Biol 6 19-37 789
Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic 790
(Amsterdam) 210 34-40 791
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating 792
RNA from pine trees Plant Mol Biol Rep 11 113-116 793
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC 794
Clark DG (2011) PhMYB4 fine-tunes the floral volatile signature of 795
Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143 796
Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz 797
EA Taylor MG Smits-Kroon MT Schuurink RC Haring MA Giovannoni J 798
Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic 799
pathway by ectopic expression of a MYB transcription factor in tomato fruit Plant 800
Cell 23 2738-2753 801
Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan 802
XW Yang ZY (2017) Differential responses of four biosynthetic pathways of 803
aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under 804
interaction of light and temperature Food Chem 221 356-364 805
Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of 806
differentially-expressed genes during somatic embryogenesis in Fragaria times 807
ananassa Duch lsquoBenihopprsquo J Hortic Sci Biotechnol 90 671-681 808
Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 809
transcriptionally regulates chilling-induced lignification of loquat fruit via physical 810
interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136 811
Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM 812
(2004) Functional interactions between a glutamine synthetase promoter and MYB 813
proteins Plant J 39 513-526 814
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
29
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) 815
Sucrose nonfermenting1-related protein kinase26 an ortholog of open stomata1 is 816
a negative regulator of strawberry fruit development and ripening Plant Physiol 817
167 915-930 818
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene 819
expression in strawberry fruit (Fragaria times ananassa) by agroinfiltration a rapid 820
assay for gene function analysis Plant J 48 818-826 821
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of 822
selected aroma-active compounds in strawberries by headspace solid-phase 823
microextraction gas chromatography and correlation with sensory descriptive 824
analysis J Food Sci 72 S487-S496 825
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid 826
plays an important role in the regulation of strawberry fruit ripening Plant Physiol 827
157 188-199 828
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of 829
NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes BMC 830
Plant Biol 6 20 831
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN 832
(2005) MYB98 is required for pollen tube guidance and synergid cell differentiation 833
in Arabidopsis Plant Cell 17 2981-2992 834
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional 835
characterization of enone oxidoreductases from strawberry and tomato fruit J 836
Agric Food Chem 55 6705-6711 837
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You 838
J-S Rohloff J Randall SK Alsheikh M (2012) Proteomic study of 839
low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ 840
in cold tolerance Plant Physiol 159 1787-1805 841
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional 842
characterization of four APETALA2-family genes (RAP26 RAP26L DREB19 843
and DREB26) in Arabidopsis Plant Mol Biol 75 107-127 844
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
30
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon 845
J Gupta V (2013) An oxidoreductase from lsquoAlphonsorsquo mango catalyzing 846
biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494 847
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in 848
strawberries Z Lebensm-Unters Forsch 195 120-123 849
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X 850
(2015) Label-free quantitative proteomics to investigate strawberry fruit proteome 851
changes under controlled atmosphere and low temperature storage J Proteomics 852
120 44-57 853
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 854
cooperates with CitWRKY1 to participate in citric acid degradation via 855
up-regulation of CitAco3 J Exp Bot 68 3419-3426 856
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription 857
factor CitERF71 activates the terpene synthase gene CitTPS16 involved in the 858
synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938 859
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and 860
transcriptomic analysis of the AP2ERF superfamily in Vitis vinifera BMC 861
Genomics 11 719 862
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive 863
Factor (AP2ERF) transcription factors mediators of stress responses and 864
developmental programs New Phytol 199 639-649 865
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 866
interacting with EOBI negatively regulates fragrance biosynthesis in petunia 867
flowers New Phytol 215 1490-1502 868
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu 869
CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 in regulating 870
anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) 871
during anthocyanin biosynthesis Plant Cell Tissue Organ Cult 115 285-298 872
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
31
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao 873
CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphate signaling and 874
homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597 875
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC 876
Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL 877
Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor 878
regulates eugenol production in ripe strawberry fruit receptacles Plant Physiol 168 879
598-614 880
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics 881
and volatile constituents of strawberry (cv Cigaline) during maturation J Agric 882
Food Chem 52 1248-1254 883
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS 884
(2012) Ethylene-responsive transcription factors interact with promoters of ADH 885
and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 886
63 6393-6405 887
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM 888
Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-Franco A 889
Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific 890
transcription factor FaDOF2 regulates the production of eugenol in ripe fruit 891
receptacles J Exp Bot 68 4529-4543 892
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) 893
Comparison and verification of the genes involved in ethylene biosynthesis and 894
signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44 895
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the 896
ERF gene family in Arabidopsis and rice Plant Physiol 140 411-432 897
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in 898
sour cherry and strawberry and the heterologous expression of CBF1 in strawberry 899
J Am Soc Hortic Sci 127 489-494 900
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech 901
JC Ohme-Takagi M Regad F Bouzayen M (2012) Functional analysis and 902
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32
binding affinity of tomato ethylene response factors provide insight on the 903
molecular bases of plant differential responses to ethylene BMC Plant Biol 12 190 904
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) 905
Methylpentoses are possible precursors of furanones in fruits Prikl Biokhim 906
Mikrobiol 28 123-127 907
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery 908
of synergid-expressed genes encoding filiform apparatus localized proteins Plant 909
Cell 19 2557-2568 910
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria 911
vesca L compared to those of cultivated berries Fragariatimes ananassa cv Senga 912
Sengana J Agric Food Chem 27 19-22 913
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W 914
Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of the strawberry 915
flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone 916
oxidoreductase Plant Cell 18 1023-1037 917
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L 918
Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim M Broun P Zhang 919
JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription 920
factors genome-wide comparative analysis among eukaryotes Science 290 921
2105-2110 922
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the 923
formation of 25-dimethyl-4-hydroxy-3(2H)-furanone in detached ripening 924
strawberry fruits J Agric Food Chem 46 1488-1493 925
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 926
25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in 927
strawberry fruits Phytochemistry 43 155-159 928
Schwab W (1998) Application of stable isotope ratio analysis explaining the 929
bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone in plants by a biological 930
maillard reaction J Agric Food Chem 46 2266ndash2269 931
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33
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) 932
Molecules 18 6936-6951 933
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard 934
products Recent Res Dev Phytochem 1 643-673 935
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL 936
Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJ Sims CA 937
Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical 938
compositions a seasonal influence and effects on sensory perception PLoS One 9 939
e88446 940
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) 941
Identification phylogeny and transcript profiling of ERF family genes during 942
development and abiotic stress treatments in tomato Mol Genet Genomics 284 943
455-475 944
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) 945
CitAP210 activation of the terpene synthase CsTPS1 is associated with the 946
synthesis of (+)-valencene in lsquoNewhallrsquo orange J Exp Bot 67 4105-4115 947
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes 948
Dev Genes Evol 214 105-114 949
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K 950
Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the 951
key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151 952
Spitzer-Rimon B Farhi M Albo B Cnarsquoani A Ben Zvi MM Masci T Edelbaum 953
O Yu YX Shklarman E Ovadis M Vainstein A (2012) The R2R3-MYB-like 954
regulatory factor EOBI acting downstream of EOBII regulates scent production 955
by activating ODO1 and structural scent-related genes in petunia Plant Cell 24 956
5089-5105 957
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp 958
Bot 68 4407-4409 959
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla 960
JF Amaya I Giavalisco P Fernie AR Botella MA Valpuesta V (2015) Central 961
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34
role of FaGAMYB in the transition of the strawberry receptacle from development 962
to ripening New Phytol 208 482-496 963
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 964
regulates fragrance biosynthesis in petunia flowers Plant Cell 17 1612-1624 965
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS 966
(2018) The potassium channel FaTPK1 plays a critical role in fruit quality 967
formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748 968
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) 969
Isolation cloning and expression of a multifunctional O-methyltransferase capable 970
of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma 971
compounds in strawberry fruits Plant J 31 755-765 972
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor 973
types their evolutionary origin and species distribution In A handbook of 974
transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular 975
Biochemistry 52 25-73 976
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of 977
odor (Buettner A Ed) Springer Cham 9-10 978
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS 979
(2014) Isolation classification and transcription profiles of the AP2ERF 980
transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271 981
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in 982
regulation of fruit quality Crit Rev Plant Sci 35 120-130 983
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ 984
Zhang SL Wu J (2017) Map-based cloning of the pear gene MYB114 identifies an 985
interaction with other transcription factors to coordinately regulate fruit 986
anthocyanin biosynthesis Plant J 92 437-451 987
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes 988
involved in regulating fruit ripening Plant Physiol 153 1280-1292 989
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35
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) 990
Expression of ethylene response genes during persimmon fruit astringency removal 991
Planta 235 895-906 992
Zabetakis I Gramshaw JW Robinson DS (1999) 993
25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis and 994
biosynthesis-a review Food Chem 65 139-151 995
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci 996
Food Agric 74 421-434 997
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 998
an AP2ERF gene is a novel regulator of fruit lignification induced by chilling 999
injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1000
1325-1334 1001
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation 1002
classification and transcription profiles of the Ethylene Response Factors (ERFs) in 1003
ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215 1004
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML 1005
(2012) Genome-wide analysis of the AP2ERF superfamily in peach (Prunus 1006
persica) Genet Mol Res 11 4788-4809 1007
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and 1008
expression analysis of a CRTDRE-binding factor gene FaCBF1 from Fragaria times 1009
ananassa Acta Hortic 41 240-248 1010
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The 1011
Arabidopsis AP2ERF transcription factor RAP26 participates in ABA salt and 1012
osmotic stress responses Gene 457 1-12 1013
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B 1014
Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) Genome-wide 1015
analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic 1016
(Amsterdam) 123 73-81 1017
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF 1018
Valpuesta V Botella MA Granell A Amaya I (2012) Genetic analysis of 1019
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36
strawberry fruit aroma and identification of O-methyltransferase FaOMT as the 1020
locus controlling natural variation in mesifurane content Plant Physiol 159 1021
851-870 1022
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
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Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating RNA from pine trees Plant Mol Biol Rep 11 113-116Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC Clark DG (2011) PhMYB4 fine-tunes the floral volatilesignature of Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143
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Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz EA Taylor MG Smits-Kroon MT Schuurink RC HaringMA Giovannoni J Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic pathway by ectopic expression of aMYB transcription factor in tomato fruit Plant Cell 23 2738-2753
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan XW Yang ZY (2017) Differential responses of fourbiosynthetic pathways of aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under interaction of light andtemperature Food Chem 221 356-364
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of differentially-expressed genes during somatic embryogenesis inFragaria times ananassa Duch Benihopp J Hortic Sci Biotechnol 90 671-681
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 transcriptionally regulates chilling-induced lignification ofloquat fruit via physical interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM (2004) Functional interactions between a glutaminesynthetase promoter and MYB proteins Plant J 39 513-526
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) Sucrose nonfermenting1-related protein kinase26 anortholog of open stomata1 is a negative regulator of strawberry fruit development and ripening Plant Physiol 167 915-930
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene expression in strawberry fruit (Fragaria times ananassa) byagroinfiltration a rapid assay for gene function analysis Plant J 48 818-826
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of selected aroma-active compounds in strawberries byheadspace solid-phase microextraction gas chromatography and correlation with sensory descriptive analysis J Food Sci 72 S487-S496
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid plays an important role in the regulation of strawberry fruitripening Plant Physiol 157 188-199
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of NaCl-stressed Arabidopsis roots reveals novel classes ofresponsive genes BMC Plant Biol 6 20
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN (2005) MYB98 is required for pollen tube guidance andsynergid cell differentiation in Arabidopsis Plant Cell 17 2981-2992
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional characterization of enone oxidoreductases from strawberry andtomato fruit J Agric Food Chem 55 6705-6711
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You J-S Rohloff J Randall SK Alsheikh M (2012) Proteomicstudy of low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ in cold tolerance Plant Physiol 159 1787-1805
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional characterization of four APETALA2-family genes (RAP26 RAP26LDREB19 and DREB26) in Arabidopsis Plant Mol Biol 75 107-127
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon J Gupta V (2013) An oxidoreductase from Alphonsomango catalyzing biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in strawberries Z Lebensm-Unters Forsch 195 120-123Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X (2015) Label-free quantitative proteomics to investigatestrawberry fruit proteome changes under controlled atmosphere and low temperature storage J Proteomics 120 44-57
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 cooperates with CitWRKY1 to participate in citric aciddegradation via up-regulation of CitAco3 J Exp Bot 68 3419-3426
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription factor CitERF71 activates the terpene synthase geneCitTPS16 involved in the synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and transcriptomic analysis of the AP2ERF superfamily inVitis vinifera BMC Genomics 11 719
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive Factor (AP2ERF) transcription factors mediators of stressresponses and developmental programs New Phytol 199 639-649
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 interacting with EOBI negatively regulates fragrancebiosynthesis in petunia flowers New Phytol 215 1490-1502
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 inregulating anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) during anthocyanin biosynthesis Plant CellTissue Organ Cult 115 285-298
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title wwwplantphysiolorgon February 25 2020 - Published by Downloaded from
Copyright copy 2018 American Society of Plant Biologists All rights reserved
Google Scholar Author Only Title Only Author and Title
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphatesignaling and homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor regulates eugenol production in ripe strawberry fruitreceptacles Plant Physiol 168 598-614
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics and volatile constituents of strawberry (cv Cigaline)during maturation J Agric Food Chem 52 1248-1254
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS (2012) Ethylene-responsive transcription factors interact withpromoters of ADH and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 63 6393-6405
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-FrancoA Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific transcription factor FaDOF2 regulates the production ofeugenol in ripe fruit receptacles J Exp Bot 68 4529-4543
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) Comparison and verification of the genes involved in ethylenebiosynthesis and signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice Plant Physiol140 411-432
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in sour cherry and strawberry and the heterologousexpression of CBF1 in strawberry J Am Soc Hortic Sci 127 489-494
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech JC Ohme-Takagi M Regad F Bouzayen M (2012)Functional analysis and binding affinity of tomato ethylene response factors provide insight on the molecular bases of plant differentialresponses to ethylene BMC Plant Biol 12 190
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) Methylpentoses are possible precursors of furanones in fruits PriklBiokhim Mikrobiol 28 123-127
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery of synergid-expressed genes encoding filiformapparatus localized proteins Plant Cell 19 2557-2568
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria vesca L compared to those of cultivated berriesFragariatimes ananassa cv Senga Sengana J Agric Food Chem 27 19-22
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of thestrawberry flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone oxidoreductase Plant Cell 18 1023-1037
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim MBroun P Zhang JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription factors genome-wide comparative analysisamong eukaryotes Science 290 2105-2110
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the formation of 25-dimethyl-4-hydroxy-3(2H)-furanonein detached ripening strawberry fruits J Agric Food Chem 46 1488-1493
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in strawberry fruits Phytochemistry 43 155-159
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (1998) Application of stable isotope ratio analysis explaining the bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone inplants by a biological maillard reaction J Agric Food Chem 46 2266ndash2269
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) Molecules 18 6936-6951Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard products Recent Res Dev Phytochem 1 643-673Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJSims CA Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical compositions a seasonal influence and effects on sensoryperception PLoS One 9 e88446
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) Identification phylogeny and transcript profiling of ERFfamily genes during development and abiotic stress treatments in tomato Mol Genet Genomics 284 455-475
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) CitAP210 activation of the terpene synthase CsTPS1 isassociated with the synthesis of (+)-valencene in Newhall orange J Exp Bot 67 4105-4115
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes Dev Genes Evol 214 105-114Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Spitzer-Rimon B Farhi M Albo B Cnaani A Ben Zvi MM Masci T Edelbaum O Yu YX Shklarman E Ovadis M Vainstein A (2012) TheR2R3-MYB-like regulatory factor EOBI acting downstream of EOBII regulates scent production by activating ODO1 and structuralscent-related genes in petunia Plant Cell 24 5089-5105
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp Bot 68 4407-4409Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla JF Amaya I Giavalisco P Fernie AR Botella MAValpuesta V (2015) Central role of FaGAMYB in the transition of the strawberry receptacle from development to ripening New Phytol208 482-496
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 regulates fragrance biosynthesis in petunia flowers PlantCell 17 1612-1624
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS (2018) The potassium channel FaTPK1 plays a critical role infruit quality formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) Isolation cloning and expression of a multifunctional O- wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma compounds in strawberry fruitsPlant J 31 755-765
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor types their evolutionary origin and speciesdistribution In A handbook of transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular Biochemistry 52 25-73
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of odor (Buettner A Ed) Springer Cham 9-10Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS (2014) Isolation classification and transcription profiles ofthe AP2ERF transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in regulation of fruit quality Crit Rev Plant Sci 35 120-130
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ Zhang SL Wu J (2017) Map-based cloning of the pear geneMYB114 identifies an interaction with other transcription factors to coordinately regulate fruit anthocyanin biosynthesis Plant J 92437-451
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes involved in regulating fruit ripening Plant Physiol 1531280-1292
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) Expression of ethylene response genes during persimmonfruit astringency removal Planta 235 895-906
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zabetakis I Gramshaw JW Robinson DS (1999) 25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis andbiosynthesis-a review Food Chem 65 139-151
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Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci Food Agric 74 421-434Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 an AP2ERF gene is a novel regulator of fruit lignificationinduced by chilling injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1325-1334
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation classification and transcription profiles of the Ethylene ResponseFactors (ERFs) in ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML (2012) Genome-wide analysis of the AP2ERF superfamily inpeach (Prunus persica) Genet Mol Res 11 4788-4809
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and expression analysis of a CRTDRE-binding factor gene FaCBF1from Fragaria times ananassa Acta Hortic 41 240-248
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The Arabidopsis AP2ERF transcription factor RAP26 participatesin ABA salt and osmotic stress responses Gene 457 1-12
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Genome-wide analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic (Amsterdam) 123 73-81Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF Valpuesta V Botella MA Granell A Amaya I (2012) Geneticanalysis of strawberry fruit aroma and identification of O-methyltransferase FaOMT as the locus controlling natural variation inmesifurane content Plant Physiol 159 851-870
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
27
protein and biotin-labelled DNA probe were mixed and analysed on 6 native 756
polyacrylamide gels and then photographed Presence or absence of specific probes is 757
marked by the symbol + or - 758
Figure 8 The combined activation effects of FaERF9FaMYB98 on the FaQR 759
promoter LUCREN values obtained with the empty vector and FaQR promoter were 760
used as the calibrator set as 1 and error bars were calculated from five replicates 761
Figure 9 Yeast two-hybrid analysis of the protein-protein interactions between 762
FaMYB98 and FaERF9 Positive interactions were determined by the growth of 763
yeast cells on selection plates Bait with pOST acted as positive controls and bait with 764
pPR3 as negative controls DDO synthetically defined medium without tryptophan 765
and leucine QDO synthetically defined medium without tryptophan leucine 766
histidine and adenine QDO+3AT QDO medium supplemented with 1 mM 767
3-aminotriazole 768
Figure 10 BiFC analysis of the protein-protein interactions between FaMYB98 and 769
FaERF9 The pairs of fusion proteins tested were FaMYB98-YFPN+FaERF9-YFPC 770
FaERF9-YFPN+FaMYB98-YFPC FaMYB98-YFPN+FaMYB98-YFPC and 771
FaERF9-YFPN+FaERF9-YFPC The other combinations were negative controls 772
The tobacco used in the assay was stably transformed with a specific 773
nucleus-localized red fluorescence protein construct and the red fluorescence 774
indicated the nucleus-localized signal (NLS) Fluorescence of the yellow fluorescence 775
protein (YFP) visualized the interaction in vivo Scale bar = 25 microm 776
777
Literature Cited 778
779
Agarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression 780
of PgDREB2A transcription factor enhances abiotic stress tolerance and activates 781
downstream stress-responsive genes Mol Biol Rep 37 1125-1135 782
Araguumlez I Osorio S Hoffmann T Rambla JL Medina-Escobar N Granell A 783
Botella MAacute Schwab W Valpuesta V (2013) Eugenol production in achenes and 784
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28
receptacles of strawberry fruits is catalyzed by synthases exhibiting distinct kinetics 785
Plant Physiol 163 946-958 786
Carvalho RF Carvalho SD OrsquoGrady K Folta KM (2016) Agroinfiltration of 787
strawberry fruit mdash a powerful transient expression system for gene validation Curr 788
Plant Biol 6 19-37 789
Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic 790
(Amsterdam) 210 34-40 791
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating 792
RNA from pine trees Plant Mol Biol Rep 11 113-116 793
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC 794
Clark DG (2011) PhMYB4 fine-tunes the floral volatile signature of 795
Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143 796
Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz 797
EA Taylor MG Smits-Kroon MT Schuurink RC Haring MA Giovannoni J 798
Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic 799
pathway by ectopic expression of a MYB transcription factor in tomato fruit Plant 800
Cell 23 2738-2753 801
Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan 802
XW Yang ZY (2017) Differential responses of four biosynthetic pathways of 803
aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under 804
interaction of light and temperature Food Chem 221 356-364 805
Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of 806
differentially-expressed genes during somatic embryogenesis in Fragaria times 807
ananassa Duch lsquoBenihopprsquo J Hortic Sci Biotechnol 90 671-681 808
Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 809
transcriptionally regulates chilling-induced lignification of loquat fruit via physical 810
interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136 811
Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM 812
(2004) Functional interactions between a glutamine synthetase promoter and MYB 813
proteins Plant J 39 513-526 814
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29
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) 815
Sucrose nonfermenting1-related protein kinase26 an ortholog of open stomata1 is 816
a negative regulator of strawberry fruit development and ripening Plant Physiol 817
167 915-930 818
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene 819
expression in strawberry fruit (Fragaria times ananassa) by agroinfiltration a rapid 820
assay for gene function analysis Plant J 48 818-826 821
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of 822
selected aroma-active compounds in strawberries by headspace solid-phase 823
microextraction gas chromatography and correlation with sensory descriptive 824
analysis J Food Sci 72 S487-S496 825
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid 826
plays an important role in the regulation of strawberry fruit ripening Plant Physiol 827
157 188-199 828
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of 829
NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes BMC 830
Plant Biol 6 20 831
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN 832
(2005) MYB98 is required for pollen tube guidance and synergid cell differentiation 833
in Arabidopsis Plant Cell 17 2981-2992 834
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional 835
characterization of enone oxidoreductases from strawberry and tomato fruit J 836
Agric Food Chem 55 6705-6711 837
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You 838
J-S Rohloff J Randall SK Alsheikh M (2012) Proteomic study of 839
low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ 840
in cold tolerance Plant Physiol 159 1787-1805 841
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional 842
characterization of four APETALA2-family genes (RAP26 RAP26L DREB19 843
and DREB26) in Arabidopsis Plant Mol Biol 75 107-127 844
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30
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon 845
J Gupta V (2013) An oxidoreductase from lsquoAlphonsorsquo mango catalyzing 846
biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494 847
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in 848
strawberries Z Lebensm-Unters Forsch 195 120-123 849
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X 850
(2015) Label-free quantitative proteomics to investigate strawberry fruit proteome 851
changes under controlled atmosphere and low temperature storage J Proteomics 852
120 44-57 853
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 854
cooperates with CitWRKY1 to participate in citric acid degradation via 855
up-regulation of CitAco3 J Exp Bot 68 3419-3426 856
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription 857
factor CitERF71 activates the terpene synthase gene CitTPS16 involved in the 858
synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938 859
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and 860
transcriptomic analysis of the AP2ERF superfamily in Vitis vinifera BMC 861
Genomics 11 719 862
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive 863
Factor (AP2ERF) transcription factors mediators of stress responses and 864
developmental programs New Phytol 199 639-649 865
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 866
interacting with EOBI negatively regulates fragrance biosynthesis in petunia 867
flowers New Phytol 215 1490-1502 868
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu 869
CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 in regulating 870
anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) 871
during anthocyanin biosynthesis Plant Cell Tissue Organ Cult 115 285-298 872
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
31
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao 873
CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphate signaling and 874
homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597 875
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC 876
Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL 877
Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor 878
regulates eugenol production in ripe strawberry fruit receptacles Plant Physiol 168 879
598-614 880
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics 881
and volatile constituents of strawberry (cv Cigaline) during maturation J Agric 882
Food Chem 52 1248-1254 883
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS 884
(2012) Ethylene-responsive transcription factors interact with promoters of ADH 885
and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 886
63 6393-6405 887
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM 888
Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-Franco A 889
Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific 890
transcription factor FaDOF2 regulates the production of eugenol in ripe fruit 891
receptacles J Exp Bot 68 4529-4543 892
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) 893
Comparison and verification of the genes involved in ethylene biosynthesis and 894
signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44 895
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the 896
ERF gene family in Arabidopsis and rice Plant Physiol 140 411-432 897
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in 898
sour cherry and strawberry and the heterologous expression of CBF1 in strawberry 899
J Am Soc Hortic Sci 127 489-494 900
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech 901
JC Ohme-Takagi M Regad F Bouzayen M (2012) Functional analysis and 902
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
32
binding affinity of tomato ethylene response factors provide insight on the 903
molecular bases of plant differential responses to ethylene BMC Plant Biol 12 190 904
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) 905
Methylpentoses are possible precursors of furanones in fruits Prikl Biokhim 906
Mikrobiol 28 123-127 907
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery 908
of synergid-expressed genes encoding filiform apparatus localized proteins Plant 909
Cell 19 2557-2568 910
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria 911
vesca L compared to those of cultivated berries Fragariatimes ananassa cv Senga 912
Sengana J Agric Food Chem 27 19-22 913
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W 914
Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of the strawberry 915
flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone 916
oxidoreductase Plant Cell 18 1023-1037 917
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L 918
Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim M Broun P Zhang 919
JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription 920
factors genome-wide comparative analysis among eukaryotes Science 290 921
2105-2110 922
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the 923
formation of 25-dimethyl-4-hydroxy-3(2H)-furanone in detached ripening 924
strawberry fruits J Agric Food Chem 46 1488-1493 925
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 926
25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in 927
strawberry fruits Phytochemistry 43 155-159 928
Schwab W (1998) Application of stable isotope ratio analysis explaining the 929
bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone in plants by a biological 930
maillard reaction J Agric Food Chem 46 2266ndash2269 931
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
33
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) 932
Molecules 18 6936-6951 933
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard 934
products Recent Res Dev Phytochem 1 643-673 935
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL 936
Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJ Sims CA 937
Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical 938
compositions a seasonal influence and effects on sensory perception PLoS One 9 939
e88446 940
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) 941
Identification phylogeny and transcript profiling of ERF family genes during 942
development and abiotic stress treatments in tomato Mol Genet Genomics 284 943
455-475 944
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) 945
CitAP210 activation of the terpene synthase CsTPS1 is associated with the 946
synthesis of (+)-valencene in lsquoNewhallrsquo orange J Exp Bot 67 4105-4115 947
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes 948
Dev Genes Evol 214 105-114 949
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K 950
Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the 951
key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151 952
Spitzer-Rimon B Farhi M Albo B Cnarsquoani A Ben Zvi MM Masci T Edelbaum 953
O Yu YX Shklarman E Ovadis M Vainstein A (2012) The R2R3-MYB-like 954
regulatory factor EOBI acting downstream of EOBII regulates scent production 955
by activating ODO1 and structural scent-related genes in petunia Plant Cell 24 956
5089-5105 957
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp 958
Bot 68 4407-4409 959
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla 960
JF Amaya I Giavalisco P Fernie AR Botella MA Valpuesta V (2015) Central 961
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
34
role of FaGAMYB in the transition of the strawberry receptacle from development 962
to ripening New Phytol 208 482-496 963
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 964
regulates fragrance biosynthesis in petunia flowers Plant Cell 17 1612-1624 965
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS 966
(2018) The potassium channel FaTPK1 plays a critical role in fruit quality 967
formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748 968
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) 969
Isolation cloning and expression of a multifunctional O-methyltransferase capable 970
of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma 971
compounds in strawberry fruits Plant J 31 755-765 972
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor 973
types their evolutionary origin and species distribution In A handbook of 974
transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular 975
Biochemistry 52 25-73 976
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of 977
odor (Buettner A Ed) Springer Cham 9-10 978
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS 979
(2014) Isolation classification and transcription profiles of the AP2ERF 980
transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271 981
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in 982
regulation of fruit quality Crit Rev Plant Sci 35 120-130 983
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ 984
Zhang SL Wu J (2017) Map-based cloning of the pear gene MYB114 identifies an 985
interaction with other transcription factors to coordinately regulate fruit 986
anthocyanin biosynthesis Plant J 92 437-451 987
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes 988
involved in regulating fruit ripening Plant Physiol 153 1280-1292 989
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35
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) 990
Expression of ethylene response genes during persimmon fruit astringency removal 991
Planta 235 895-906 992
Zabetakis I Gramshaw JW Robinson DS (1999) 993
25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis and 994
biosynthesis-a review Food Chem 65 139-151 995
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci 996
Food Agric 74 421-434 997
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 998
an AP2ERF gene is a novel regulator of fruit lignification induced by chilling 999
injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1000
1325-1334 1001
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation 1002
classification and transcription profiles of the Ethylene Response Factors (ERFs) in 1003
ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215 1004
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML 1005
(2012) Genome-wide analysis of the AP2ERF superfamily in peach (Prunus 1006
persica) Genet Mol Res 11 4788-4809 1007
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and 1008
expression analysis of a CRTDRE-binding factor gene FaCBF1 from Fragaria times 1009
ananassa Acta Hortic 41 240-248 1010
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The 1011
Arabidopsis AP2ERF transcription factor RAP26 participates in ABA salt and 1012
osmotic stress responses Gene 457 1-12 1013
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B 1014
Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) Genome-wide 1015
analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic 1016
(Amsterdam) 123 73-81 1017
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF 1018
Valpuesta V Botella MA Granell A Amaya I (2012) Genetic analysis of 1019
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strawberry fruit aroma and identification of O-methyltransferase FaOMT as the 1020
locus controlling natural variation in mesifurane content Plant Physiol 159 1021
851-870 1022
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Genome-wide analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic (Amsterdam) 123 73-81Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF Valpuesta V Botella MA Granell A Amaya I (2012) Geneticanalysis of strawberry fruit aroma and identification of O-methyltransferase FaOMT as the locus controlling natural variation inmesifurane content Plant Physiol 159 851-870
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28
receptacles of strawberry fruits is catalyzed by synthases exhibiting distinct kinetics 785
Plant Physiol 163 946-958 786
Carvalho RF Carvalho SD OrsquoGrady K Folta KM (2016) Agroinfiltration of 787
strawberry fruit mdash a powerful transient expression system for gene validation Curr 788
Plant Biol 6 19-37 789
Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic 790
(Amsterdam) 210 34-40 791
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating 792
RNA from pine trees Plant Mol Biol Rep 11 113-116 793
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC 794
Clark DG (2011) PhMYB4 fine-tunes the floral volatile signature of 795
Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143 796
Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz 797
EA Taylor MG Smits-Kroon MT Schuurink RC Haring MA Giovannoni J 798
Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic 799
pathway by ectopic expression of a MYB transcription factor in tomato fruit Plant 800
Cell 23 2738-2753 801
Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan 802
XW Yang ZY (2017) Differential responses of four biosynthetic pathways of 803
aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under 804
interaction of light and temperature Food Chem 221 356-364 805
Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of 806
differentially-expressed genes during somatic embryogenesis in Fragaria times 807
ananassa Duch lsquoBenihopprsquo J Hortic Sci Biotechnol 90 671-681 808
Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 809
transcriptionally regulates chilling-induced lignification of loquat fruit via physical 810
interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136 811
Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM 812
(2004) Functional interactions between a glutamine synthetase promoter and MYB 813
proteins Plant J 39 513-526 814
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
29
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) 815
Sucrose nonfermenting1-related protein kinase26 an ortholog of open stomata1 is 816
a negative regulator of strawberry fruit development and ripening Plant Physiol 817
167 915-930 818
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene 819
expression in strawberry fruit (Fragaria times ananassa) by agroinfiltration a rapid 820
assay for gene function analysis Plant J 48 818-826 821
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of 822
selected aroma-active compounds in strawberries by headspace solid-phase 823
microextraction gas chromatography and correlation with sensory descriptive 824
analysis J Food Sci 72 S487-S496 825
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid 826
plays an important role in the regulation of strawberry fruit ripening Plant Physiol 827
157 188-199 828
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of 829
NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes BMC 830
Plant Biol 6 20 831
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN 832
(2005) MYB98 is required for pollen tube guidance and synergid cell differentiation 833
in Arabidopsis Plant Cell 17 2981-2992 834
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional 835
characterization of enone oxidoreductases from strawberry and tomato fruit J 836
Agric Food Chem 55 6705-6711 837
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You 838
J-S Rohloff J Randall SK Alsheikh M (2012) Proteomic study of 839
low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ 840
in cold tolerance Plant Physiol 159 1787-1805 841
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional 842
characterization of four APETALA2-family genes (RAP26 RAP26L DREB19 843
and DREB26) in Arabidopsis Plant Mol Biol 75 107-127 844
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
30
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon 845
J Gupta V (2013) An oxidoreductase from lsquoAlphonsorsquo mango catalyzing 846
biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494 847
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in 848
strawberries Z Lebensm-Unters Forsch 195 120-123 849
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X 850
(2015) Label-free quantitative proteomics to investigate strawberry fruit proteome 851
changes under controlled atmosphere and low temperature storage J Proteomics 852
120 44-57 853
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 854
cooperates with CitWRKY1 to participate in citric acid degradation via 855
up-regulation of CitAco3 J Exp Bot 68 3419-3426 856
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription 857
factor CitERF71 activates the terpene synthase gene CitTPS16 involved in the 858
synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938 859
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and 860
transcriptomic analysis of the AP2ERF superfamily in Vitis vinifera BMC 861
Genomics 11 719 862
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive 863
Factor (AP2ERF) transcription factors mediators of stress responses and 864
developmental programs New Phytol 199 639-649 865
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 866
interacting with EOBI negatively regulates fragrance biosynthesis in petunia 867
flowers New Phytol 215 1490-1502 868
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu 869
CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 in regulating 870
anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) 871
during anthocyanin biosynthesis Plant Cell Tissue Organ Cult 115 285-298 872
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
31
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao 873
CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphate signaling and 874
homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597 875
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC 876
Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL 877
Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor 878
regulates eugenol production in ripe strawberry fruit receptacles Plant Physiol 168 879
598-614 880
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics 881
and volatile constituents of strawberry (cv Cigaline) during maturation J Agric 882
Food Chem 52 1248-1254 883
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS 884
(2012) Ethylene-responsive transcription factors interact with promoters of ADH 885
and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 886
63 6393-6405 887
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM 888
Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-Franco A 889
Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific 890
transcription factor FaDOF2 regulates the production of eugenol in ripe fruit 891
receptacles J Exp Bot 68 4529-4543 892
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) 893
Comparison and verification of the genes involved in ethylene biosynthesis and 894
signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44 895
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the 896
ERF gene family in Arabidopsis and rice Plant Physiol 140 411-432 897
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in 898
sour cherry and strawberry and the heterologous expression of CBF1 in strawberry 899
J Am Soc Hortic Sci 127 489-494 900
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech 901
JC Ohme-Takagi M Regad F Bouzayen M (2012) Functional analysis and 902
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
32
binding affinity of tomato ethylene response factors provide insight on the 903
molecular bases of plant differential responses to ethylene BMC Plant Biol 12 190 904
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) 905
Methylpentoses are possible precursors of furanones in fruits Prikl Biokhim 906
Mikrobiol 28 123-127 907
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery 908
of synergid-expressed genes encoding filiform apparatus localized proteins Plant 909
Cell 19 2557-2568 910
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria 911
vesca L compared to those of cultivated berries Fragariatimes ananassa cv Senga 912
Sengana J Agric Food Chem 27 19-22 913
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W 914
Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of the strawberry 915
flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone 916
oxidoreductase Plant Cell 18 1023-1037 917
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L 918
Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim M Broun P Zhang 919
JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription 920
factors genome-wide comparative analysis among eukaryotes Science 290 921
2105-2110 922
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the 923
formation of 25-dimethyl-4-hydroxy-3(2H)-furanone in detached ripening 924
strawberry fruits J Agric Food Chem 46 1488-1493 925
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 926
25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in 927
strawberry fruits Phytochemistry 43 155-159 928
Schwab W (1998) Application of stable isotope ratio analysis explaining the 929
bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone in plants by a biological 930
maillard reaction J Agric Food Chem 46 2266ndash2269 931
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33
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) 932
Molecules 18 6936-6951 933
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard 934
products Recent Res Dev Phytochem 1 643-673 935
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL 936
Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJ Sims CA 937
Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical 938
compositions a seasonal influence and effects on sensory perception PLoS One 9 939
e88446 940
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) 941
Identification phylogeny and transcript profiling of ERF family genes during 942
development and abiotic stress treatments in tomato Mol Genet Genomics 284 943
455-475 944
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) 945
CitAP210 activation of the terpene synthase CsTPS1 is associated with the 946
synthesis of (+)-valencene in lsquoNewhallrsquo orange J Exp Bot 67 4105-4115 947
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes 948
Dev Genes Evol 214 105-114 949
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K 950
Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the 951
key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151 952
Spitzer-Rimon B Farhi M Albo B Cnarsquoani A Ben Zvi MM Masci T Edelbaum 953
O Yu YX Shklarman E Ovadis M Vainstein A (2012) The R2R3-MYB-like 954
regulatory factor EOBI acting downstream of EOBII regulates scent production 955
by activating ODO1 and structural scent-related genes in petunia Plant Cell 24 956
5089-5105 957
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp 958
Bot 68 4407-4409 959
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla 960
JF Amaya I Giavalisco P Fernie AR Botella MA Valpuesta V (2015) Central 961
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34
role of FaGAMYB in the transition of the strawberry receptacle from development 962
to ripening New Phytol 208 482-496 963
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 964
regulates fragrance biosynthesis in petunia flowers Plant Cell 17 1612-1624 965
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS 966
(2018) The potassium channel FaTPK1 plays a critical role in fruit quality 967
formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748 968
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) 969
Isolation cloning and expression of a multifunctional O-methyltransferase capable 970
of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma 971
compounds in strawberry fruits Plant J 31 755-765 972
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor 973
types their evolutionary origin and species distribution In A handbook of 974
transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular 975
Biochemistry 52 25-73 976
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of 977
odor (Buettner A Ed) Springer Cham 9-10 978
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS 979
(2014) Isolation classification and transcription profiles of the AP2ERF 980
transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271 981
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in 982
regulation of fruit quality Crit Rev Plant Sci 35 120-130 983
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ 984
Zhang SL Wu J (2017) Map-based cloning of the pear gene MYB114 identifies an 985
interaction with other transcription factors to coordinately regulate fruit 986
anthocyanin biosynthesis Plant J 92 437-451 987
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes 988
involved in regulating fruit ripening Plant Physiol 153 1280-1292 989
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35
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) 990
Expression of ethylene response genes during persimmon fruit astringency removal 991
Planta 235 895-906 992
Zabetakis I Gramshaw JW Robinson DS (1999) 993
25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis and 994
biosynthesis-a review Food Chem 65 139-151 995
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci 996
Food Agric 74 421-434 997
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 998
an AP2ERF gene is a novel regulator of fruit lignification induced by chilling 999
injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1000
1325-1334 1001
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation 1002
classification and transcription profiles of the Ethylene Response Factors (ERFs) in 1003
ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215 1004
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML 1005
(2012) Genome-wide analysis of the AP2ERF superfamily in peach (Prunus 1006
persica) Genet Mol Res 11 4788-4809 1007
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and 1008
expression analysis of a CRTDRE-binding factor gene FaCBF1 from Fragaria times 1009
ananassa Acta Hortic 41 240-248 1010
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The 1011
Arabidopsis AP2ERF transcription factor RAP26 participates in ABA salt and 1012
osmotic stress responses Gene 457 1-12 1013
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B 1014
Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) Genome-wide 1015
analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic 1016
(Amsterdam) 123 73-81 1017
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF 1018
Valpuesta V Botella MA Granell A Amaya I (2012) Genetic analysis of 1019
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36
strawberry fruit aroma and identification of O-methyltransferase FaOMT as the 1020
locus controlling natural variation in mesifurane content Plant Physiol 159 1021
851-870 1022
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
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Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid plays an important role in the regulation of strawberry fruitripening Plant Physiol 157 188-199
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Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of NaCl-stressed Arabidopsis roots reveals novel classes ofresponsive genes BMC Plant Biol 6 20
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Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN (2005) MYB98 is required for pollen tube guidance andsynergid cell differentiation in Arabidopsis Plant Cell 17 2981-2992
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional characterization of enone oxidoreductases from strawberry andtomato fruit J Agric Food Chem 55 6705-6711
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You J-S Rohloff J Randall SK Alsheikh M (2012) Proteomicstudy of low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ in cold tolerance Plant Physiol 159 1787-1805
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional characterization of four APETALA2-family genes (RAP26 RAP26LDREB19 and DREB26) in Arabidopsis Plant Mol Biol 75 107-127
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon J Gupta V (2013) An oxidoreductase from Alphonsomango catalyzing biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in strawberries Z Lebensm-Unters Forsch 195 120-123Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X (2015) Label-free quantitative proteomics to investigatestrawberry fruit proteome changes under controlled atmosphere and low temperature storage J Proteomics 120 44-57
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 cooperates with CitWRKY1 to participate in citric aciddegradation via up-regulation of CitAco3 J Exp Bot 68 3419-3426
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription factor CitERF71 activates the terpene synthase geneCitTPS16 involved in the synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and transcriptomic analysis of the AP2ERF superfamily inVitis vinifera BMC Genomics 11 719
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive Factor (AP2ERF) transcription factors mediators of stressresponses and developmental programs New Phytol 199 639-649
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 interacting with EOBI negatively regulates fragrancebiosynthesis in petunia flowers New Phytol 215 1490-1502
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 inregulating anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) during anthocyanin biosynthesis Plant CellTissue Organ Cult 115 285-298
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title wwwplantphysiolorgon February 25 2020 - Published by Downloaded from
Copyright copy 2018 American Society of Plant Biologists All rights reserved
Google Scholar Author Only Title Only Author and Title
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphatesignaling and homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor regulates eugenol production in ripe strawberry fruitreceptacles Plant Physiol 168 598-614
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics and volatile constituents of strawberry (cv Cigaline)during maturation J Agric Food Chem 52 1248-1254
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS (2012) Ethylene-responsive transcription factors interact withpromoters of ADH and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 63 6393-6405
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-FrancoA Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific transcription factor FaDOF2 regulates the production ofeugenol in ripe fruit receptacles J Exp Bot 68 4529-4543
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) Comparison and verification of the genes involved in ethylenebiosynthesis and signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice Plant Physiol140 411-432
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in sour cherry and strawberry and the heterologousexpression of CBF1 in strawberry J Am Soc Hortic Sci 127 489-494
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech JC Ohme-Takagi M Regad F Bouzayen M (2012)Functional analysis and binding affinity of tomato ethylene response factors provide insight on the molecular bases of plant differentialresponses to ethylene BMC Plant Biol 12 190
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) Methylpentoses are possible precursors of furanones in fruits PriklBiokhim Mikrobiol 28 123-127
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery of synergid-expressed genes encoding filiformapparatus localized proteins Plant Cell 19 2557-2568
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria vesca L compared to those of cultivated berriesFragariatimes ananassa cv Senga Sengana J Agric Food Chem 27 19-22
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of thestrawberry flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone oxidoreductase Plant Cell 18 1023-1037
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim MBroun P Zhang JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription factors genome-wide comparative analysisamong eukaryotes Science 290 2105-2110
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the formation of 25-dimethyl-4-hydroxy-3(2H)-furanonein detached ripening strawberry fruits J Agric Food Chem 46 1488-1493
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in strawberry fruits Phytochemistry 43 155-159
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (1998) Application of stable isotope ratio analysis explaining the bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone inplants by a biological maillard reaction J Agric Food Chem 46 2266ndash2269
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) Molecules 18 6936-6951Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard products Recent Res Dev Phytochem 1 643-673Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJSims CA Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical compositions a seasonal influence and effects on sensoryperception PLoS One 9 e88446
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) Identification phylogeny and transcript profiling of ERFfamily genes during development and abiotic stress treatments in tomato Mol Genet Genomics 284 455-475
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) CitAP210 activation of the terpene synthase CsTPS1 isassociated with the synthesis of (+)-valencene in Newhall orange J Exp Bot 67 4105-4115
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes Dev Genes Evol 214 105-114Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Spitzer-Rimon B Farhi M Albo B Cnaani A Ben Zvi MM Masci T Edelbaum O Yu YX Shklarman E Ovadis M Vainstein A (2012) TheR2R3-MYB-like regulatory factor EOBI acting downstream of EOBII regulates scent production by activating ODO1 and structuralscent-related genes in petunia Plant Cell 24 5089-5105
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp Bot 68 4407-4409Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla JF Amaya I Giavalisco P Fernie AR Botella MAValpuesta V (2015) Central role of FaGAMYB in the transition of the strawberry receptacle from development to ripening New Phytol208 482-496
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 regulates fragrance biosynthesis in petunia flowers PlantCell 17 1612-1624
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS (2018) The potassium channel FaTPK1 plays a critical role infruit quality formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) Isolation cloning and expression of a multifunctional O- wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma compounds in strawberry fruitsPlant J 31 755-765
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor types their evolutionary origin and speciesdistribution In A handbook of transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular Biochemistry 52 25-73
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of odor (Buettner A Ed) Springer Cham 9-10Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS (2014) Isolation classification and transcription profiles ofthe AP2ERF transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in regulation of fruit quality Crit Rev Plant Sci 35 120-130
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ Zhang SL Wu J (2017) Map-based cloning of the pear geneMYB114 identifies an interaction with other transcription factors to coordinately regulate fruit anthocyanin biosynthesis Plant J 92437-451
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes involved in regulating fruit ripening Plant Physiol 1531280-1292
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) Expression of ethylene response genes during persimmonfruit astringency removal Planta 235 895-906
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zabetakis I Gramshaw JW Robinson DS (1999) 25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis andbiosynthesis-a review Food Chem 65 139-151
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci Food Agric 74 421-434Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 an AP2ERF gene is a novel regulator of fruit lignificationinduced by chilling injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1325-1334
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation classification and transcription profiles of the Ethylene ResponseFactors (ERFs) in ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML (2012) Genome-wide analysis of the AP2ERF superfamily inpeach (Prunus persica) Genet Mol Res 11 4788-4809
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and expression analysis of a CRTDRE-binding factor gene FaCBF1from Fragaria times ananassa Acta Hortic 41 240-248
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The Arabidopsis AP2ERF transcription factor RAP26 participatesin ABA salt and osmotic stress responses Gene 457 1-12
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Genome-wide analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic (Amsterdam) 123 73-81Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF Valpuesta V Botella MA Granell A Amaya I (2012) Geneticanalysis of strawberry fruit aroma and identification of O-methyltransferase FaOMT as the locus controlling natural variation inmesifurane content Plant Physiol 159 851-870
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
29
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) 815
Sucrose nonfermenting1-related protein kinase26 an ortholog of open stomata1 is 816
a negative regulator of strawberry fruit development and ripening Plant Physiol 817
167 915-930 818
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene 819
expression in strawberry fruit (Fragaria times ananassa) by agroinfiltration a rapid 820
assay for gene function analysis Plant J 48 818-826 821
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of 822
selected aroma-active compounds in strawberries by headspace solid-phase 823
microextraction gas chromatography and correlation with sensory descriptive 824
analysis J Food Sci 72 S487-S496 825
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid 826
plays an important role in the regulation of strawberry fruit ripening Plant Physiol 827
157 188-199 828
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of 829
NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes BMC 830
Plant Biol 6 20 831
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN 832
(2005) MYB98 is required for pollen tube guidance and synergid cell differentiation 833
in Arabidopsis Plant Cell 17 2981-2992 834
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional 835
characterization of enone oxidoreductases from strawberry and tomato fruit J 836
Agric Food Chem 55 6705-6711 837
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You 838
J-S Rohloff J Randall SK Alsheikh M (2012) Proteomic study of 839
low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ 840
in cold tolerance Plant Physiol 159 1787-1805 841
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional 842
characterization of four APETALA2-family genes (RAP26 RAP26L DREB19 843
and DREB26) in Arabidopsis Plant Mol Biol 75 107-127 844
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30
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon 845
J Gupta V (2013) An oxidoreductase from lsquoAlphonsorsquo mango catalyzing 846
biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494 847
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in 848
strawberries Z Lebensm-Unters Forsch 195 120-123 849
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X 850
(2015) Label-free quantitative proteomics to investigate strawberry fruit proteome 851
changes under controlled atmosphere and low temperature storage J Proteomics 852
120 44-57 853
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 854
cooperates with CitWRKY1 to participate in citric acid degradation via 855
up-regulation of CitAco3 J Exp Bot 68 3419-3426 856
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription 857
factor CitERF71 activates the terpene synthase gene CitTPS16 involved in the 858
synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938 859
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and 860
transcriptomic analysis of the AP2ERF superfamily in Vitis vinifera BMC 861
Genomics 11 719 862
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive 863
Factor (AP2ERF) transcription factors mediators of stress responses and 864
developmental programs New Phytol 199 639-649 865
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 866
interacting with EOBI negatively regulates fragrance biosynthesis in petunia 867
flowers New Phytol 215 1490-1502 868
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu 869
CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 in regulating 870
anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) 871
during anthocyanin biosynthesis Plant Cell Tissue Organ Cult 115 285-298 872
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31
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao 873
CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphate signaling and 874
homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597 875
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC 876
Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL 877
Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor 878
regulates eugenol production in ripe strawberry fruit receptacles Plant Physiol 168 879
598-614 880
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics 881
and volatile constituents of strawberry (cv Cigaline) during maturation J Agric 882
Food Chem 52 1248-1254 883
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS 884
(2012) Ethylene-responsive transcription factors interact with promoters of ADH 885
and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 886
63 6393-6405 887
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM 888
Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-Franco A 889
Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific 890
transcription factor FaDOF2 regulates the production of eugenol in ripe fruit 891
receptacles J Exp Bot 68 4529-4543 892
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) 893
Comparison and verification of the genes involved in ethylene biosynthesis and 894
signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44 895
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the 896
ERF gene family in Arabidopsis and rice Plant Physiol 140 411-432 897
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in 898
sour cherry and strawberry and the heterologous expression of CBF1 in strawberry 899
J Am Soc Hortic Sci 127 489-494 900
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech 901
JC Ohme-Takagi M Regad F Bouzayen M (2012) Functional analysis and 902
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32
binding affinity of tomato ethylene response factors provide insight on the 903
molecular bases of plant differential responses to ethylene BMC Plant Biol 12 190 904
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) 905
Methylpentoses are possible precursors of furanones in fruits Prikl Biokhim 906
Mikrobiol 28 123-127 907
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery 908
of synergid-expressed genes encoding filiform apparatus localized proteins Plant 909
Cell 19 2557-2568 910
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria 911
vesca L compared to those of cultivated berries Fragariatimes ananassa cv Senga 912
Sengana J Agric Food Chem 27 19-22 913
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W 914
Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of the strawberry 915
flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone 916
oxidoreductase Plant Cell 18 1023-1037 917
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L 918
Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim M Broun P Zhang 919
JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription 920
factors genome-wide comparative analysis among eukaryotes Science 290 921
2105-2110 922
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the 923
formation of 25-dimethyl-4-hydroxy-3(2H)-furanone in detached ripening 924
strawberry fruits J Agric Food Chem 46 1488-1493 925
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 926
25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in 927
strawberry fruits Phytochemistry 43 155-159 928
Schwab W (1998) Application of stable isotope ratio analysis explaining the 929
bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone in plants by a biological 930
maillard reaction J Agric Food Chem 46 2266ndash2269 931
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
33
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) 932
Molecules 18 6936-6951 933
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard 934
products Recent Res Dev Phytochem 1 643-673 935
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL 936
Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJ Sims CA 937
Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical 938
compositions a seasonal influence and effects on sensory perception PLoS One 9 939
e88446 940
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) 941
Identification phylogeny and transcript profiling of ERF family genes during 942
development and abiotic stress treatments in tomato Mol Genet Genomics 284 943
455-475 944
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) 945
CitAP210 activation of the terpene synthase CsTPS1 is associated with the 946
synthesis of (+)-valencene in lsquoNewhallrsquo orange J Exp Bot 67 4105-4115 947
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes 948
Dev Genes Evol 214 105-114 949
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K 950
Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the 951
key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151 952
Spitzer-Rimon B Farhi M Albo B Cnarsquoani A Ben Zvi MM Masci T Edelbaum 953
O Yu YX Shklarman E Ovadis M Vainstein A (2012) The R2R3-MYB-like 954
regulatory factor EOBI acting downstream of EOBII regulates scent production 955
by activating ODO1 and structural scent-related genes in petunia Plant Cell 24 956
5089-5105 957
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp 958
Bot 68 4407-4409 959
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla 960
JF Amaya I Giavalisco P Fernie AR Botella MA Valpuesta V (2015) Central 961
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
34
role of FaGAMYB in the transition of the strawberry receptacle from development 962
to ripening New Phytol 208 482-496 963
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 964
regulates fragrance biosynthesis in petunia flowers Plant Cell 17 1612-1624 965
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS 966
(2018) The potassium channel FaTPK1 plays a critical role in fruit quality 967
formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748 968
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) 969
Isolation cloning and expression of a multifunctional O-methyltransferase capable 970
of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma 971
compounds in strawberry fruits Plant J 31 755-765 972
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor 973
types their evolutionary origin and species distribution In A handbook of 974
transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular 975
Biochemistry 52 25-73 976
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of 977
odor (Buettner A Ed) Springer Cham 9-10 978
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS 979
(2014) Isolation classification and transcription profiles of the AP2ERF 980
transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271 981
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in 982
regulation of fruit quality Crit Rev Plant Sci 35 120-130 983
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ 984
Zhang SL Wu J (2017) Map-based cloning of the pear gene MYB114 identifies an 985
interaction with other transcription factors to coordinately regulate fruit 986
anthocyanin biosynthesis Plant J 92 437-451 987
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes 988
involved in regulating fruit ripening Plant Physiol 153 1280-1292 989
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
35
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) 990
Expression of ethylene response genes during persimmon fruit astringency removal 991
Planta 235 895-906 992
Zabetakis I Gramshaw JW Robinson DS (1999) 993
25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis and 994
biosynthesis-a review Food Chem 65 139-151 995
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci 996
Food Agric 74 421-434 997
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 998
an AP2ERF gene is a novel regulator of fruit lignification induced by chilling 999
injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1000
1325-1334 1001
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation 1002
classification and transcription profiles of the Ethylene Response Factors (ERFs) in 1003
ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215 1004
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML 1005
(2012) Genome-wide analysis of the AP2ERF superfamily in peach (Prunus 1006
persica) Genet Mol Res 11 4788-4809 1007
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and 1008
expression analysis of a CRTDRE-binding factor gene FaCBF1 from Fragaria times 1009
ananassa Acta Hortic 41 240-248 1010
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The 1011
Arabidopsis AP2ERF transcription factor RAP26 participates in ABA salt and 1012
osmotic stress responses Gene 457 1-12 1013
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B 1014
Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) Genome-wide 1015
analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic 1016
(Amsterdam) 123 73-81 1017
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF 1018
Valpuesta V Botella MA Granell A Amaya I (2012) Genetic analysis of 1019
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
36
strawberry fruit aroma and identification of O-methyltransferase FaOMT as the 1020
locus controlling natural variation in mesifurane content Plant Physiol 159 1021
851-870 1022
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Parsed CitationsAgarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression of PgDREB2A transcription factor enhances abioticstress tolerance and activates downstream stress-responsive genes Mol Biol Rep 37 1125-1135
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Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating RNA from pine trees Plant Mol Biol Rep 11 113-116Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
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Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz EA Taylor MG Smits-Kroon MT Schuurink RC HaringMA Giovannoni J Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic pathway by ectopic expression of aMYB transcription factor in tomato fruit Plant Cell 23 2738-2753
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Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan XW Yang ZY (2017) Differential responses of fourbiosynthetic pathways of aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under interaction of light andtemperature Food Chem 221 356-364
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Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of differentially-expressed genes during somatic embryogenesis inFragaria times ananassa Duch Benihopp J Hortic Sci Biotechnol 90 671-681
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Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 transcriptionally regulates chilling-induced lignification ofloquat fruit via physical interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136
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Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM (2004) Functional interactions between a glutaminesynthetase promoter and MYB proteins Plant J 39 513-526
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) Sucrose nonfermenting1-related protein kinase26 anortholog of open stomata1 is a negative regulator of strawberry fruit development and ripening Plant Physiol 167 915-930
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene expression in strawberry fruit (Fragaria times ananassa) byagroinfiltration a rapid assay for gene function analysis Plant J 48 818-826
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of selected aroma-active compounds in strawberries byheadspace solid-phase microextraction gas chromatography and correlation with sensory descriptive analysis J Food Sci 72 S487-S496
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid plays an important role in the regulation of strawberry fruitripening Plant Physiol 157 188-199
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of NaCl-stressed Arabidopsis roots reveals novel classes ofresponsive genes BMC Plant Biol 6 20
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN (2005) MYB98 is required for pollen tube guidance andsynergid cell differentiation in Arabidopsis Plant Cell 17 2981-2992
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional characterization of enone oxidoreductases from strawberry andtomato fruit J Agric Food Chem 55 6705-6711
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You J-S Rohloff J Randall SK Alsheikh M (2012) Proteomicstudy of low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ in cold tolerance Plant Physiol 159 1787-1805
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional characterization of four APETALA2-family genes (RAP26 RAP26LDREB19 and DREB26) in Arabidopsis Plant Mol Biol 75 107-127
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon J Gupta V (2013) An oxidoreductase from Alphonsomango catalyzing biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in strawberries Z Lebensm-Unters Forsch 195 120-123Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X (2015) Label-free quantitative proteomics to investigatestrawberry fruit proteome changes under controlled atmosphere and low temperature storage J Proteomics 120 44-57
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 cooperates with CitWRKY1 to participate in citric aciddegradation via up-regulation of CitAco3 J Exp Bot 68 3419-3426
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription factor CitERF71 activates the terpene synthase geneCitTPS16 involved in the synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and transcriptomic analysis of the AP2ERF superfamily inVitis vinifera BMC Genomics 11 719
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive Factor (AP2ERF) transcription factors mediators of stressresponses and developmental programs New Phytol 199 639-649
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 interacting with EOBI negatively regulates fragrancebiosynthesis in petunia flowers New Phytol 215 1490-1502
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 inregulating anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) during anthocyanin biosynthesis Plant CellTissue Organ Cult 115 285-298
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title wwwplantphysiolorgon February 25 2020 - Published by Downloaded from
Copyright copy 2018 American Society of Plant Biologists All rights reserved
Google Scholar Author Only Title Only Author and Title
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphatesignaling and homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor regulates eugenol production in ripe strawberry fruitreceptacles Plant Physiol 168 598-614
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics and volatile constituents of strawberry (cv Cigaline)during maturation J Agric Food Chem 52 1248-1254
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS (2012) Ethylene-responsive transcription factors interact withpromoters of ADH and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 63 6393-6405
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-FrancoA Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific transcription factor FaDOF2 regulates the production ofeugenol in ripe fruit receptacles J Exp Bot 68 4529-4543
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) Comparison and verification of the genes involved in ethylenebiosynthesis and signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice Plant Physiol140 411-432
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in sour cherry and strawberry and the heterologousexpression of CBF1 in strawberry J Am Soc Hortic Sci 127 489-494
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech JC Ohme-Takagi M Regad F Bouzayen M (2012)Functional analysis and binding affinity of tomato ethylene response factors provide insight on the molecular bases of plant differentialresponses to ethylene BMC Plant Biol 12 190
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) Methylpentoses are possible precursors of furanones in fruits PriklBiokhim Mikrobiol 28 123-127
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery of synergid-expressed genes encoding filiformapparatus localized proteins Plant Cell 19 2557-2568
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria vesca L compared to those of cultivated berriesFragariatimes ananassa cv Senga Sengana J Agric Food Chem 27 19-22
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of thestrawberry flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone oxidoreductase Plant Cell 18 1023-1037
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim MBroun P Zhang JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription factors genome-wide comparative analysisamong eukaryotes Science 290 2105-2110
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the formation of 25-dimethyl-4-hydroxy-3(2H)-furanonein detached ripening strawberry fruits J Agric Food Chem 46 1488-1493
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in strawberry fruits Phytochemistry 43 155-159
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (1998) Application of stable isotope ratio analysis explaining the bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone inplants by a biological maillard reaction J Agric Food Chem 46 2266ndash2269
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) Molecules 18 6936-6951Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard products Recent Res Dev Phytochem 1 643-673Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJSims CA Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical compositions a seasonal influence and effects on sensoryperception PLoS One 9 e88446
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) Identification phylogeny and transcript profiling of ERFfamily genes during development and abiotic stress treatments in tomato Mol Genet Genomics 284 455-475
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) CitAP210 activation of the terpene synthase CsTPS1 isassociated with the synthesis of (+)-valencene in Newhall orange J Exp Bot 67 4105-4115
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes Dev Genes Evol 214 105-114Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Spitzer-Rimon B Farhi M Albo B Cnaani A Ben Zvi MM Masci T Edelbaum O Yu YX Shklarman E Ovadis M Vainstein A (2012) TheR2R3-MYB-like regulatory factor EOBI acting downstream of EOBII regulates scent production by activating ODO1 and structuralscent-related genes in petunia Plant Cell 24 5089-5105
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp Bot 68 4407-4409Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla JF Amaya I Giavalisco P Fernie AR Botella MAValpuesta V (2015) Central role of FaGAMYB in the transition of the strawberry receptacle from development to ripening New Phytol208 482-496
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 regulates fragrance biosynthesis in petunia flowers PlantCell 17 1612-1624
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS (2018) The potassium channel FaTPK1 plays a critical role infruit quality formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) Isolation cloning and expression of a multifunctional O- wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma compounds in strawberry fruitsPlant J 31 755-765
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor types their evolutionary origin and speciesdistribution In A handbook of transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular Biochemistry 52 25-73
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of odor (Buettner A Ed) Springer Cham 9-10Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS (2014) Isolation classification and transcription profiles ofthe AP2ERF transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in regulation of fruit quality Crit Rev Plant Sci 35 120-130
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ Zhang SL Wu J (2017) Map-based cloning of the pear geneMYB114 identifies an interaction with other transcription factors to coordinately regulate fruit anthocyanin biosynthesis Plant J 92437-451
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes involved in regulating fruit ripening Plant Physiol 1531280-1292
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) Expression of ethylene response genes during persimmonfruit astringency removal Planta 235 895-906
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Zabetakis I Gramshaw JW Robinson DS (1999) 25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis andbiosynthesis-a review Food Chem 65 139-151
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Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci Food Agric 74 421-434Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 an AP2ERF gene is a novel regulator of fruit lignificationinduced by chilling injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1325-1334
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation classification and transcription profiles of the Ethylene ResponseFactors (ERFs) in ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML (2012) Genome-wide analysis of the AP2ERF superfamily inpeach (Prunus persica) Genet Mol Res 11 4788-4809
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and expression analysis of a CRTDRE-binding factor gene FaCBF1from Fragaria times ananassa Acta Hortic 41 240-248
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The Arabidopsis AP2ERF transcription factor RAP26 participatesin ABA salt and osmotic stress responses Gene 457 1-12
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Genome-wide analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic (Amsterdam) 123 73-81Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF Valpuesta V Botella MA Granell A Amaya I (2012) Geneticanalysis of strawberry fruit aroma and identification of O-methyltransferase FaOMT as the locus controlling natural variation inmesifurane content Plant Physiol 159 851-870
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
30
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon 845
J Gupta V (2013) An oxidoreductase from lsquoAlphonsorsquo mango catalyzing 846
biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494 847
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in 848
strawberries Z Lebensm-Unters Forsch 195 120-123 849
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X 850
(2015) Label-free quantitative proteomics to investigate strawberry fruit proteome 851
changes under controlled atmosphere and low temperature storage J Proteomics 852
120 44-57 853
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 854
cooperates with CitWRKY1 to participate in citric acid degradation via 855
up-regulation of CitAco3 J Exp Bot 68 3419-3426 856
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription 857
factor CitERF71 activates the terpene synthase gene CitTPS16 involved in the 858
synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938 859
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and 860
transcriptomic analysis of the AP2ERF superfamily in Vitis vinifera BMC 861
Genomics 11 719 862
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive 863
Factor (AP2ERF) transcription factors mediators of stress responses and 864
developmental programs New Phytol 199 639-649 865
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 866
interacting with EOBI negatively regulates fragrance biosynthesis in petunia 867
flowers New Phytol 215 1490-1502 868
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu 869
CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 in regulating 870
anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) 871
during anthocyanin biosynthesis Plant Cell Tissue Organ Cult 115 285-298 872
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
31
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao 873
CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphate signaling and 874
homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597 875
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC 876
Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL 877
Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor 878
regulates eugenol production in ripe strawberry fruit receptacles Plant Physiol 168 879
598-614 880
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics 881
and volatile constituents of strawberry (cv Cigaline) during maturation J Agric 882
Food Chem 52 1248-1254 883
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS 884
(2012) Ethylene-responsive transcription factors interact with promoters of ADH 885
and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 886
63 6393-6405 887
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM 888
Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-Franco A 889
Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific 890
transcription factor FaDOF2 regulates the production of eugenol in ripe fruit 891
receptacles J Exp Bot 68 4529-4543 892
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) 893
Comparison and verification of the genes involved in ethylene biosynthesis and 894
signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44 895
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the 896
ERF gene family in Arabidopsis and rice Plant Physiol 140 411-432 897
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in 898
sour cherry and strawberry and the heterologous expression of CBF1 in strawberry 899
J Am Soc Hortic Sci 127 489-494 900
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech 901
JC Ohme-Takagi M Regad F Bouzayen M (2012) Functional analysis and 902
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
32
binding affinity of tomato ethylene response factors provide insight on the 903
molecular bases of plant differential responses to ethylene BMC Plant Biol 12 190 904
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) 905
Methylpentoses are possible precursors of furanones in fruits Prikl Biokhim 906
Mikrobiol 28 123-127 907
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery 908
of synergid-expressed genes encoding filiform apparatus localized proteins Plant 909
Cell 19 2557-2568 910
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria 911
vesca L compared to those of cultivated berries Fragariatimes ananassa cv Senga 912
Sengana J Agric Food Chem 27 19-22 913
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W 914
Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of the strawberry 915
flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone 916
oxidoreductase Plant Cell 18 1023-1037 917
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L 918
Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim M Broun P Zhang 919
JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription 920
factors genome-wide comparative analysis among eukaryotes Science 290 921
2105-2110 922
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the 923
formation of 25-dimethyl-4-hydroxy-3(2H)-furanone in detached ripening 924
strawberry fruits J Agric Food Chem 46 1488-1493 925
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 926
25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in 927
strawberry fruits Phytochemistry 43 155-159 928
Schwab W (1998) Application of stable isotope ratio analysis explaining the 929
bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone in plants by a biological 930
maillard reaction J Agric Food Chem 46 2266ndash2269 931
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
33
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) 932
Molecules 18 6936-6951 933
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard 934
products Recent Res Dev Phytochem 1 643-673 935
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL 936
Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJ Sims CA 937
Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical 938
compositions a seasonal influence and effects on sensory perception PLoS One 9 939
e88446 940
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) 941
Identification phylogeny and transcript profiling of ERF family genes during 942
development and abiotic stress treatments in tomato Mol Genet Genomics 284 943
455-475 944
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) 945
CitAP210 activation of the terpene synthase CsTPS1 is associated with the 946
synthesis of (+)-valencene in lsquoNewhallrsquo orange J Exp Bot 67 4105-4115 947
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes 948
Dev Genes Evol 214 105-114 949
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K 950
Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the 951
key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151 952
Spitzer-Rimon B Farhi M Albo B Cnarsquoani A Ben Zvi MM Masci T Edelbaum 953
O Yu YX Shklarman E Ovadis M Vainstein A (2012) The R2R3-MYB-like 954
regulatory factor EOBI acting downstream of EOBII regulates scent production 955
by activating ODO1 and structural scent-related genes in petunia Plant Cell 24 956
5089-5105 957
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp 958
Bot 68 4407-4409 959
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla 960
JF Amaya I Giavalisco P Fernie AR Botella MA Valpuesta V (2015) Central 961
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
34
role of FaGAMYB in the transition of the strawberry receptacle from development 962
to ripening New Phytol 208 482-496 963
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 964
regulates fragrance biosynthesis in petunia flowers Plant Cell 17 1612-1624 965
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS 966
(2018) The potassium channel FaTPK1 plays a critical role in fruit quality 967
formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748 968
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) 969
Isolation cloning and expression of a multifunctional O-methyltransferase capable 970
of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma 971
compounds in strawberry fruits Plant J 31 755-765 972
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor 973
types their evolutionary origin and species distribution In A handbook of 974
transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular 975
Biochemistry 52 25-73 976
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of 977
odor (Buettner A Ed) Springer Cham 9-10 978
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS 979
(2014) Isolation classification and transcription profiles of the AP2ERF 980
transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271 981
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in 982
regulation of fruit quality Crit Rev Plant Sci 35 120-130 983
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ 984
Zhang SL Wu J (2017) Map-based cloning of the pear gene MYB114 identifies an 985
interaction with other transcription factors to coordinately regulate fruit 986
anthocyanin biosynthesis Plant J 92 437-451 987
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes 988
involved in regulating fruit ripening Plant Physiol 153 1280-1292 989
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35
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) 990
Expression of ethylene response genes during persimmon fruit astringency removal 991
Planta 235 895-906 992
Zabetakis I Gramshaw JW Robinson DS (1999) 993
25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis and 994
biosynthesis-a review Food Chem 65 139-151 995
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci 996
Food Agric 74 421-434 997
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 998
an AP2ERF gene is a novel regulator of fruit lignification induced by chilling 999
injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1000
1325-1334 1001
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation 1002
classification and transcription profiles of the Ethylene Response Factors (ERFs) in 1003
ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215 1004
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML 1005
(2012) Genome-wide analysis of the AP2ERF superfamily in peach (Prunus 1006
persica) Genet Mol Res 11 4788-4809 1007
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and 1008
expression analysis of a CRTDRE-binding factor gene FaCBF1 from Fragaria times 1009
ananassa Acta Hortic 41 240-248 1010
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The 1011
Arabidopsis AP2ERF transcription factor RAP26 participates in ABA salt and 1012
osmotic stress responses Gene 457 1-12 1013
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B 1014
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locus controlling natural variation in mesifurane content Plant Physiol 159 1021
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Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF Valpuesta V Botella MA Granell A Amaya I (2012) Geneticanalysis of strawberry fruit aroma and identification of O-methyltransferase FaOMT as the locus controlling natural variation inmesifurane content Plant Physiol 159 851-870
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31
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao 873
CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphate signaling and 874
homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597 875
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC 876
Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL 877
Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor 878
regulates eugenol production in ripe strawberry fruit receptacles Plant Physiol 168 879
598-614 880
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics 881
and volatile constituents of strawberry (cv Cigaline) during maturation J Agric 882
Food Chem 52 1248-1254 883
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS 884
(2012) Ethylene-responsive transcription factors interact with promoters of ADH 885
and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 886
63 6393-6405 887
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM 888
Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-Franco A 889
Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific 890
transcription factor FaDOF2 regulates the production of eugenol in ripe fruit 891
receptacles J Exp Bot 68 4529-4543 892
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) 893
Comparison and verification of the genes involved in ethylene biosynthesis and 894
signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44 895
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the 896
ERF gene family in Arabidopsis and rice Plant Physiol 140 411-432 897
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in 898
sour cherry and strawberry and the heterologous expression of CBF1 in strawberry 899
J Am Soc Hortic Sci 127 489-494 900
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech 901
JC Ohme-Takagi M Regad F Bouzayen M (2012) Functional analysis and 902
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32
binding affinity of tomato ethylene response factors provide insight on the 903
molecular bases of plant differential responses to ethylene BMC Plant Biol 12 190 904
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) 905
Methylpentoses are possible precursors of furanones in fruits Prikl Biokhim 906
Mikrobiol 28 123-127 907
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery 908
of synergid-expressed genes encoding filiform apparatus localized proteins Plant 909
Cell 19 2557-2568 910
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria 911
vesca L compared to those of cultivated berries Fragariatimes ananassa cv Senga 912
Sengana J Agric Food Chem 27 19-22 913
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W 914
Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of the strawberry 915
flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone 916
oxidoreductase Plant Cell 18 1023-1037 917
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L 918
Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim M Broun P Zhang 919
JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription 920
factors genome-wide comparative analysis among eukaryotes Science 290 921
2105-2110 922
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the 923
formation of 25-dimethyl-4-hydroxy-3(2H)-furanone in detached ripening 924
strawberry fruits J Agric Food Chem 46 1488-1493 925
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 926
25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in 927
strawberry fruits Phytochemistry 43 155-159 928
Schwab W (1998) Application of stable isotope ratio analysis explaining the 929
bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone in plants by a biological 930
maillard reaction J Agric Food Chem 46 2266ndash2269 931
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
33
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) 932
Molecules 18 6936-6951 933
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard 934
products Recent Res Dev Phytochem 1 643-673 935
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL 936
Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJ Sims CA 937
Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical 938
compositions a seasonal influence and effects on sensory perception PLoS One 9 939
e88446 940
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) 941
Identification phylogeny and transcript profiling of ERF family genes during 942
development and abiotic stress treatments in tomato Mol Genet Genomics 284 943
455-475 944
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) 945
CitAP210 activation of the terpene synthase CsTPS1 is associated with the 946
synthesis of (+)-valencene in lsquoNewhallrsquo orange J Exp Bot 67 4105-4115 947
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes 948
Dev Genes Evol 214 105-114 949
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K 950
Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the 951
key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151 952
Spitzer-Rimon B Farhi M Albo B Cnarsquoani A Ben Zvi MM Masci T Edelbaum 953
O Yu YX Shklarman E Ovadis M Vainstein A (2012) The R2R3-MYB-like 954
regulatory factor EOBI acting downstream of EOBII regulates scent production 955
by activating ODO1 and structural scent-related genes in petunia Plant Cell 24 956
5089-5105 957
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp 958
Bot 68 4407-4409 959
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla 960
JF Amaya I Giavalisco P Fernie AR Botella MA Valpuesta V (2015) Central 961
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
34
role of FaGAMYB in the transition of the strawberry receptacle from development 962
to ripening New Phytol 208 482-496 963
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 964
regulates fragrance biosynthesis in petunia flowers Plant Cell 17 1612-1624 965
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS 966
(2018) The potassium channel FaTPK1 plays a critical role in fruit quality 967
formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748 968
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) 969
Isolation cloning and expression of a multifunctional O-methyltransferase capable 970
of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma 971
compounds in strawberry fruits Plant J 31 755-765 972
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor 973
types their evolutionary origin and species distribution In A handbook of 974
transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular 975
Biochemistry 52 25-73 976
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of 977
odor (Buettner A Ed) Springer Cham 9-10 978
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS 979
(2014) Isolation classification and transcription profiles of the AP2ERF 980
transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271 981
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in 982
regulation of fruit quality Crit Rev Plant Sci 35 120-130 983
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ 984
Zhang SL Wu J (2017) Map-based cloning of the pear gene MYB114 identifies an 985
interaction with other transcription factors to coordinately regulate fruit 986
anthocyanin biosynthesis Plant J 92 437-451 987
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes 988
involved in regulating fruit ripening Plant Physiol 153 1280-1292 989
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
35
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) 990
Expression of ethylene response genes during persimmon fruit astringency removal 991
Planta 235 895-906 992
Zabetakis I Gramshaw JW Robinson DS (1999) 993
25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis and 994
biosynthesis-a review Food Chem 65 139-151 995
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci 996
Food Agric 74 421-434 997
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 998
an AP2ERF gene is a novel regulator of fruit lignification induced by chilling 999
injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1000
1325-1334 1001
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation 1002
classification and transcription profiles of the Ethylene Response Factors (ERFs) in 1003
ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215 1004
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML 1005
(2012) Genome-wide analysis of the AP2ERF superfamily in peach (Prunus 1006
persica) Genet Mol Res 11 4788-4809 1007
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and 1008
expression analysis of a CRTDRE-binding factor gene FaCBF1 from Fragaria times 1009
ananassa Acta Hortic 41 240-248 1010
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The 1011
Arabidopsis AP2ERF transcription factor RAP26 participates in ABA salt and 1012
osmotic stress responses Gene 457 1-12 1013
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B 1014
Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) Genome-wide 1015
analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic 1016
(Amsterdam) 123 73-81 1017
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF 1018
Valpuesta V Botella MA Granell A Amaya I (2012) Genetic analysis of 1019
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
36
strawberry fruit aroma and identification of O-methyltransferase FaOMT as the 1020
locus controlling natural variation in mesifurane content Plant Physiol 159 1021
851-870 1022
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
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wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
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Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim MBroun P Zhang JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription factors genome-wide comparative analysisamong eukaryotes Science 290 2105-2110
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the formation of 25-dimethyl-4-hydroxy-3(2H)-furanonein detached ripening strawberry fruits J Agric Food Chem 46 1488-1493
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in strawberry fruits Phytochemistry 43 155-159
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (1998) Application of stable isotope ratio analysis explaining the bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone inplants by a biological maillard reaction J Agric Food Chem 46 2266ndash2269
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) Molecules 18 6936-6951Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard products Recent Res Dev Phytochem 1 643-673Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJSims CA Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical compositions a seasonal influence and effects on sensoryperception PLoS One 9 e88446
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) Identification phylogeny and transcript profiling of ERFfamily genes during development and abiotic stress treatments in tomato Mol Genet Genomics 284 455-475
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) CitAP210 activation of the terpene synthase CsTPS1 isassociated with the synthesis of (+)-valencene in Newhall orange J Exp Bot 67 4105-4115
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes Dev Genes Evol 214 105-114Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Spitzer-Rimon B Farhi M Albo B Cnaani A Ben Zvi MM Masci T Edelbaum O Yu YX Shklarman E Ovadis M Vainstein A (2012) TheR2R3-MYB-like regulatory factor EOBI acting downstream of EOBII regulates scent production by activating ODO1 and structuralscent-related genes in petunia Plant Cell 24 5089-5105
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp Bot 68 4407-4409Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla JF Amaya I Giavalisco P Fernie AR Botella MAValpuesta V (2015) Central role of FaGAMYB in the transition of the strawberry receptacle from development to ripening New Phytol208 482-496
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 regulates fragrance biosynthesis in petunia flowers PlantCell 17 1612-1624
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS (2018) The potassium channel FaTPK1 plays a critical role infruit quality formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) Isolation cloning and expression of a multifunctional O- wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma compounds in strawberry fruitsPlant J 31 755-765
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor types their evolutionary origin and speciesdistribution In A handbook of transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular Biochemistry 52 25-73
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of odor (Buettner A Ed) Springer Cham 9-10Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS (2014) Isolation classification and transcription profiles ofthe AP2ERF transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in regulation of fruit quality Crit Rev Plant Sci 35 120-130
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ Zhang SL Wu J (2017) Map-based cloning of the pear geneMYB114 identifies an interaction with other transcription factors to coordinately regulate fruit anthocyanin biosynthesis Plant J 92437-451
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes involved in regulating fruit ripening Plant Physiol 1531280-1292
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) Expression of ethylene response genes during persimmonfruit astringency removal Planta 235 895-906
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zabetakis I Gramshaw JW Robinson DS (1999) 25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis andbiosynthesis-a review Food Chem 65 139-151
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci Food Agric 74 421-434Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 an AP2ERF gene is a novel regulator of fruit lignificationinduced by chilling injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1325-1334
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation classification and transcription profiles of the Ethylene ResponseFactors (ERFs) in ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML (2012) Genome-wide analysis of the AP2ERF superfamily inpeach (Prunus persica) Genet Mol Res 11 4788-4809
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and expression analysis of a CRTDRE-binding factor gene FaCBF1from Fragaria times ananassa Acta Hortic 41 240-248
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The Arabidopsis AP2ERF transcription factor RAP26 participatesin ABA salt and osmotic stress responses Gene 457 1-12
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Genome-wide analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic (Amsterdam) 123 73-81Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF Valpuesta V Botella MA Granell A Amaya I (2012) Geneticanalysis of strawberry fruit aroma and identification of O-methyltransferase FaOMT as the locus controlling natural variation inmesifurane content Plant Physiol 159 851-870
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
32
binding affinity of tomato ethylene response factors provide insight on the 903
molecular bases of plant differential responses to ethylene BMC Plant Biol 12 190 904
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) 905
Methylpentoses are possible precursors of furanones in fruits Prikl Biokhim 906
Mikrobiol 28 123-127 907
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery 908
of synergid-expressed genes encoding filiform apparatus localized proteins Plant 909
Cell 19 2557-2568 910
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria 911
vesca L compared to those of cultivated berries Fragariatimes ananassa cv Senga 912
Sengana J Agric Food Chem 27 19-22 913
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W 914
Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of the strawberry 915
flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone 916
oxidoreductase Plant Cell 18 1023-1037 917
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L 918
Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim M Broun P Zhang 919
JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription 920
factors genome-wide comparative analysis among eukaryotes Science 290 921
2105-2110 922
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the 923
formation of 25-dimethyl-4-hydroxy-3(2H)-furanone in detached ripening 924
strawberry fruits J Agric Food Chem 46 1488-1493 925
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 926
25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in 927
strawberry fruits Phytochemistry 43 155-159 928
Schwab W (1998) Application of stable isotope ratio analysis explaining the 929
bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone in plants by a biological 930
maillard reaction J Agric Food Chem 46 2266ndash2269 931
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
33
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) 932
Molecules 18 6936-6951 933
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard 934
products Recent Res Dev Phytochem 1 643-673 935
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL 936
Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJ Sims CA 937
Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical 938
compositions a seasonal influence and effects on sensory perception PLoS One 9 939
e88446 940
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) 941
Identification phylogeny and transcript profiling of ERF family genes during 942
development and abiotic stress treatments in tomato Mol Genet Genomics 284 943
455-475 944
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) 945
CitAP210 activation of the terpene synthase CsTPS1 is associated with the 946
synthesis of (+)-valencene in lsquoNewhallrsquo orange J Exp Bot 67 4105-4115 947
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes 948
Dev Genes Evol 214 105-114 949
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K 950
Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the 951
key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151 952
Spitzer-Rimon B Farhi M Albo B Cnarsquoani A Ben Zvi MM Masci T Edelbaum 953
O Yu YX Shklarman E Ovadis M Vainstein A (2012) The R2R3-MYB-like 954
regulatory factor EOBI acting downstream of EOBII regulates scent production 955
by activating ODO1 and structural scent-related genes in petunia Plant Cell 24 956
5089-5105 957
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp 958
Bot 68 4407-4409 959
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla 960
JF Amaya I Giavalisco P Fernie AR Botella MA Valpuesta V (2015) Central 961
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
34
role of FaGAMYB in the transition of the strawberry receptacle from development 962
to ripening New Phytol 208 482-496 963
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 964
regulates fragrance biosynthesis in petunia flowers Plant Cell 17 1612-1624 965
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS 966
(2018) The potassium channel FaTPK1 plays a critical role in fruit quality 967
formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748 968
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) 969
Isolation cloning and expression of a multifunctional O-methyltransferase capable 970
of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma 971
compounds in strawberry fruits Plant J 31 755-765 972
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor 973
types their evolutionary origin and species distribution In A handbook of 974
transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular 975
Biochemistry 52 25-73 976
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of 977
odor (Buettner A Ed) Springer Cham 9-10 978
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS 979
(2014) Isolation classification and transcription profiles of the AP2ERF 980
transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271 981
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in 982
regulation of fruit quality Crit Rev Plant Sci 35 120-130 983
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ 984
Zhang SL Wu J (2017) Map-based cloning of the pear gene MYB114 identifies an 985
interaction with other transcription factors to coordinately regulate fruit 986
anthocyanin biosynthesis Plant J 92 437-451 987
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes 988
involved in regulating fruit ripening Plant Physiol 153 1280-1292 989
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35
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) 990
Expression of ethylene response genes during persimmon fruit astringency removal 991
Planta 235 895-906 992
Zabetakis I Gramshaw JW Robinson DS (1999) 993
25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis and 994
biosynthesis-a review Food Chem 65 139-151 995
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci 996
Food Agric 74 421-434 997
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 998
an AP2ERF gene is a novel regulator of fruit lignification induced by chilling 999
injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1000
1325-1334 1001
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation 1002
classification and transcription profiles of the Ethylene Response Factors (ERFs) in 1003
ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215 1004
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML 1005
(2012) Genome-wide analysis of the AP2ERF superfamily in peach (Prunus 1006
persica) Genet Mol Res 11 4788-4809 1007
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and 1008
expression analysis of a CRTDRE-binding factor gene FaCBF1 from Fragaria times 1009
ananassa Acta Hortic 41 240-248 1010
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The 1011
Arabidopsis AP2ERF transcription factor RAP26 participates in ABA salt and 1012
osmotic stress responses Gene 457 1-12 1013
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B 1014
Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) Genome-wide 1015
analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic 1016
(Amsterdam) 123 73-81 1017
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF 1018
Valpuesta V Botella MA Granell A Amaya I (2012) Genetic analysis of 1019
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
36
strawberry fruit aroma and identification of O-methyltransferase FaOMT as the 1020
locus controlling natural variation in mesifurane content Plant Physiol 159 1021
851-870 1022
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
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Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech JC Ohme-Takagi M Regad F Bouzayen M (2012)Functional analysis and binding affinity of tomato ethylene response factors provide insight on the molecular bases of plant differentialresponses to ethylene BMC Plant Biol 12 190
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) Methylpentoses are possible precursors of furanones in fruits PriklBiokhim Mikrobiol 28 123-127
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery of synergid-expressed genes encoding filiformapparatus localized proteins Plant Cell 19 2557-2568
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria vesca L compared to those of cultivated berriesFragariatimes ananassa cv Senga Sengana J Agric Food Chem 27 19-22
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of thestrawberry flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone oxidoreductase Plant Cell 18 1023-1037
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim MBroun P Zhang JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription factors genome-wide comparative analysisamong eukaryotes Science 290 2105-2110
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the formation of 25-dimethyl-4-hydroxy-3(2H)-furanonein detached ripening strawberry fruits J Agric Food Chem 46 1488-1493
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in strawberry fruits Phytochemistry 43 155-159
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (1998) Application of stable isotope ratio analysis explaining the bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone inplants by a biological maillard reaction J Agric Food Chem 46 2266ndash2269
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) Molecules 18 6936-6951Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard products Recent Res Dev Phytochem 1 643-673Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJSims CA Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical compositions a seasonal influence and effects on sensoryperception PLoS One 9 e88446
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) Identification phylogeny and transcript profiling of ERFfamily genes during development and abiotic stress treatments in tomato Mol Genet Genomics 284 455-475
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) CitAP210 activation of the terpene synthase CsTPS1 isassociated with the synthesis of (+)-valencene in Newhall orange J Exp Bot 67 4105-4115
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes Dev Genes Evol 214 105-114Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Spitzer-Rimon B Farhi M Albo B Cnaani A Ben Zvi MM Masci T Edelbaum O Yu YX Shklarman E Ovadis M Vainstein A (2012) TheR2R3-MYB-like regulatory factor EOBI acting downstream of EOBII regulates scent production by activating ODO1 and structuralscent-related genes in petunia Plant Cell 24 5089-5105
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp Bot 68 4407-4409Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla JF Amaya I Giavalisco P Fernie AR Botella MAValpuesta V (2015) Central role of FaGAMYB in the transition of the strawberry receptacle from development to ripening New Phytol208 482-496
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 regulates fragrance biosynthesis in petunia flowers PlantCell 17 1612-1624
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS (2018) The potassium channel FaTPK1 plays a critical role infruit quality formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) Isolation cloning and expression of a multifunctional O- wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma compounds in strawberry fruitsPlant J 31 755-765
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor types their evolutionary origin and speciesdistribution In A handbook of transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular Biochemistry 52 25-73
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of odor (Buettner A Ed) Springer Cham 9-10Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS (2014) Isolation classification and transcription profiles ofthe AP2ERF transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in regulation of fruit quality Crit Rev Plant Sci 35 120-130
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ Zhang SL Wu J (2017) Map-based cloning of the pear geneMYB114 identifies an interaction with other transcription factors to coordinately regulate fruit anthocyanin biosynthesis Plant J 92437-451
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Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes involved in regulating fruit ripening Plant Physiol 1531280-1292
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Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) Expression of ethylene response genes during persimmonfruit astringency removal Planta 235 895-906
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zabetakis I Gramshaw JW Robinson DS (1999) 25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis andbiosynthesis-a review Food Chem 65 139-151
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Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci Food Agric 74 421-434Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 an AP2ERF gene is a novel regulator of fruit lignificationinduced by chilling injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1325-1334
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Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation classification and transcription profiles of the Ethylene ResponseFactors (ERFs) in ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML (2012) Genome-wide analysis of the AP2ERF superfamily inpeach (Prunus persica) Genet Mol Res 11 4788-4809
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Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and expression analysis of a CRTDRE-binding factor gene FaCBF1from Fragaria times ananassa Acta Hortic 41 240-248
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Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The Arabidopsis AP2ERF transcription factor RAP26 participatesin ABA salt and osmotic stress responses Gene 457 1-12
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Genome-wide analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic (Amsterdam) 123 73-81Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF Valpuesta V Botella MA Granell A Amaya I (2012) Geneticanalysis of strawberry fruit aroma and identification of O-methyltransferase FaOMT as the locus controlling natural variation inmesifurane content Plant Physiol 159 851-870
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33
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) 932
Molecules 18 6936-6951 933
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard 934
products Recent Res Dev Phytochem 1 643-673 935
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL 936
Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJ Sims CA 937
Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical 938
compositions a seasonal influence and effects on sensory perception PLoS One 9 939
e88446 940
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) 941
Identification phylogeny and transcript profiling of ERF family genes during 942
development and abiotic stress treatments in tomato Mol Genet Genomics 284 943
455-475 944
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) 945
CitAP210 activation of the terpene synthase CsTPS1 is associated with the 946
synthesis of (+)-valencene in lsquoNewhallrsquo orange J Exp Bot 67 4105-4115 947
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes 948
Dev Genes Evol 214 105-114 949
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K 950
Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the 951
key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151 952
Spitzer-Rimon B Farhi M Albo B Cnarsquoani A Ben Zvi MM Masci T Edelbaum 953
O Yu YX Shklarman E Ovadis M Vainstein A (2012) The R2R3-MYB-like 954
regulatory factor EOBI acting downstream of EOBII regulates scent production 955
by activating ODO1 and structural scent-related genes in petunia Plant Cell 24 956
5089-5105 957
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp 958
Bot 68 4407-4409 959
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla 960
JF Amaya I Giavalisco P Fernie AR Botella MA Valpuesta V (2015) Central 961
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
34
role of FaGAMYB in the transition of the strawberry receptacle from development 962
to ripening New Phytol 208 482-496 963
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 964
regulates fragrance biosynthesis in petunia flowers Plant Cell 17 1612-1624 965
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS 966
(2018) The potassium channel FaTPK1 plays a critical role in fruit quality 967
formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748 968
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) 969
Isolation cloning and expression of a multifunctional O-methyltransferase capable 970
of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma 971
compounds in strawberry fruits Plant J 31 755-765 972
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor 973
types their evolutionary origin and species distribution In A handbook of 974
transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular 975
Biochemistry 52 25-73 976
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of 977
odor (Buettner A Ed) Springer Cham 9-10 978
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS 979
(2014) Isolation classification and transcription profiles of the AP2ERF 980
transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271 981
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in 982
regulation of fruit quality Crit Rev Plant Sci 35 120-130 983
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ 984
Zhang SL Wu J (2017) Map-based cloning of the pear gene MYB114 identifies an 985
interaction with other transcription factors to coordinately regulate fruit 986
anthocyanin biosynthesis Plant J 92 437-451 987
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes 988
involved in regulating fruit ripening Plant Physiol 153 1280-1292 989
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
35
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) 990
Expression of ethylene response genes during persimmon fruit astringency removal 991
Planta 235 895-906 992
Zabetakis I Gramshaw JW Robinson DS (1999) 993
25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis and 994
biosynthesis-a review Food Chem 65 139-151 995
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci 996
Food Agric 74 421-434 997
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 998
an AP2ERF gene is a novel regulator of fruit lignification induced by chilling 999
injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1000
1325-1334 1001
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation 1002
classification and transcription profiles of the Ethylene Response Factors (ERFs) in 1003
ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215 1004
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML 1005
(2012) Genome-wide analysis of the AP2ERF superfamily in peach (Prunus 1006
persica) Genet Mol Res 11 4788-4809 1007
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and 1008
expression analysis of a CRTDRE-binding factor gene FaCBF1 from Fragaria times 1009
ananassa Acta Hortic 41 240-248 1010
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The 1011
Arabidopsis AP2ERF transcription factor RAP26 participates in ABA salt and 1012
osmotic stress responses Gene 457 1-12 1013
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B 1014
Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) Genome-wide 1015
analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic 1016
(Amsterdam) 123 73-81 1017
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF 1018
Valpuesta V Botella MA Granell A Amaya I (2012) Genetic analysis of 1019
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
36
strawberry fruit aroma and identification of O-methyltransferase FaOMT as the 1020
locus controlling natural variation in mesifurane content Plant Physiol 159 1021
851-870 1022
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
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wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
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Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJSims CA Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical compositions a seasonal influence and effects on sensoryperception PLoS One 9 e88446
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) Identification phylogeny and transcript profiling of ERFfamily genes during development and abiotic stress treatments in tomato Mol Genet Genomics 284 455-475
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) CitAP210 activation of the terpene synthase CsTPS1 isassociated with the synthesis of (+)-valencene in Newhall orange J Exp Bot 67 4105-4115
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes Dev Genes Evol 214 105-114Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Spitzer-Rimon B Farhi M Albo B Cnaani A Ben Zvi MM Masci T Edelbaum O Yu YX Shklarman E Ovadis M Vainstein A (2012) TheR2R3-MYB-like regulatory factor EOBI acting downstream of EOBII regulates scent production by activating ODO1 and structuralscent-related genes in petunia Plant Cell 24 5089-5105
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp Bot 68 4407-4409Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla JF Amaya I Giavalisco P Fernie AR Botella MAValpuesta V (2015) Central role of FaGAMYB in the transition of the strawberry receptacle from development to ripening New Phytol208 482-496
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 regulates fragrance biosynthesis in petunia flowers PlantCell 17 1612-1624
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS (2018) The potassium channel FaTPK1 plays a critical role infruit quality formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) Isolation cloning and expression of a multifunctional O- wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma compounds in strawberry fruitsPlant J 31 755-765
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34
role of FaGAMYB in the transition of the strawberry receptacle from development 962
to ripening New Phytol 208 482-496 963
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 964
regulates fragrance biosynthesis in petunia flowers Plant Cell 17 1612-1624 965
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS 966
(2018) The potassium channel FaTPK1 plays a critical role in fruit quality 967
formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748 968
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) 969
Isolation cloning and expression of a multifunctional O-methyltransferase capable 970
of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma 971
compounds in strawberry fruits Plant J 31 755-765 972
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor 973
types their evolutionary origin and species distribution In A handbook of 974
transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular 975
Biochemistry 52 25-73 976
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of 977
odor (Buettner A Ed) Springer Cham 9-10 978
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS 979
(2014) Isolation classification and transcription profiles of the AP2ERF 980
transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271 981
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in 982
regulation of fruit quality Crit Rev Plant Sci 35 120-130 983
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ 984
Zhang SL Wu J (2017) Map-based cloning of the pear gene MYB114 identifies an 985
interaction with other transcription factors to coordinately regulate fruit 986
anthocyanin biosynthesis Plant J 92 437-451 987
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes 988
involved in regulating fruit ripening Plant Physiol 153 1280-1292 989
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
35
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) 990
Expression of ethylene response genes during persimmon fruit astringency removal 991
Planta 235 895-906 992
Zabetakis I Gramshaw JW Robinson DS (1999) 993
25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis and 994
biosynthesis-a review Food Chem 65 139-151 995
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci 996
Food Agric 74 421-434 997
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 998
an AP2ERF gene is a novel regulator of fruit lignification induced by chilling 999
injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1000
1325-1334 1001
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation 1002
classification and transcription profiles of the Ethylene Response Factors (ERFs) in 1003
ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215 1004
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML 1005
(2012) Genome-wide analysis of the AP2ERF superfamily in peach (Prunus 1006
persica) Genet Mol Res 11 4788-4809 1007
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and 1008
expression analysis of a CRTDRE-binding factor gene FaCBF1 from Fragaria times 1009
ananassa Acta Hortic 41 240-248 1010
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The 1011
Arabidopsis AP2ERF transcription factor RAP26 participates in ABA salt and 1012
osmotic stress responses Gene 457 1-12 1013
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B 1014
Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) Genome-wide 1015
analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic 1016
(Amsterdam) 123 73-81 1017
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF 1018
Valpuesta V Botella MA Granell A Amaya I (2012) Genetic analysis of 1019
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
36
strawberry fruit aroma and identification of O-methyltransferase FaOMT as the 1020
locus controlling natural variation in mesifurane content Plant Physiol 159 1021
851-870 1022
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methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma compounds in strawberry fruitsPlant J 31 755-765
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Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in regulation of fruit quality Crit Rev Plant Sci 35 120-130
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Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ Zhang SL Wu J (2017) Map-based cloning of the pear geneMYB114 identifies an interaction with other transcription factors to coordinately regulate fruit anthocyanin biosynthesis Plant J 92437-451
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes involved in regulating fruit ripening Plant Physiol 1531280-1292
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) Expression of ethylene response genes during persimmonfruit astringency removal Planta 235 895-906
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Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci Food Agric 74 421-434Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
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Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) 990
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Food Agric 74 421-434 997
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expression analysis of a CRTDRE-binding factor gene FaCBF1 from Fragaria times 1009
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Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci Food Agric 74 421-434Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 an AP2ERF gene is a novel regulator of fruit lignificationinduced by chilling injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1325-1334
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Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation classification and transcription profiles of the Ethylene ResponseFactors (ERFs) in ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML (2012) Genome-wide analysis of the AP2ERF superfamily inpeach (Prunus persica) Genet Mol Res 11 4788-4809
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and expression analysis of a CRTDRE-binding factor gene FaCBF1from Fragaria times ananassa Acta Hortic 41 240-248
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The Arabidopsis AP2ERF transcription factor RAP26 participatesin ABA salt and osmotic stress responses Gene 457 1-12
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Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Genome-wide analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic (Amsterdam) 123 73-81Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF Valpuesta V Botella MA Granell A Amaya I (2012) Geneticanalysis of strawberry fruit aroma and identification of O-methyltransferase FaOMT as the locus controlling natural variation inmesifurane content Plant Physiol 159 851-870
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
36
strawberry fruit aroma and identification of O-methyltransferase FaOMT as the 1020
locus controlling natural variation in mesifurane content Plant Physiol 159 1021
851-870 1022
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
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wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Parsed CitationsAgarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression of PgDREB2A transcription factor enhances abioticstress tolerance and activates downstream stress-responsive genes Mol Biol Rep 37 1125-1135
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Araguumlez I Osorio S Hoffmann T Rambla JL Medina-Escobar N Granell A Botella MAacute Schwab W Valpuesta V (2013) Eugenolproduction in achenes and receptacles of strawberry fruits is catalyzed by synthases exhibiting distinct kinetics Plant Physiol 163 946-958
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Carvalho RF Carvalho SD OGrady K Folta KM (2016) Agroinfiltration of strawberry fruit - a powerful transient expression system forgene validation Curr Plant Biol 6 19-37
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic (Amsterdam) 210 34-40Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating RNA from pine trees Plant Mol Biol Rep 11 113-116Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC Clark DG (2011) PhMYB4 fine-tunes the floral volatilesignature of Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143
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wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
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Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You J-S Rohloff J Randall SK Alsheikh M (2012) Proteomicstudy of low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ in cold tolerance Plant Physiol 159 1787-1805
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Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic (Amsterdam) 210 34-40Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating RNA from pine trees Plant Mol Biol Rep 11 113-116Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC Clark DG (2011) PhMYB4 fine-tunes the floral volatilesignature of Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz EA Taylor MG Smits-Kroon MT Schuurink RC HaringMA Giovannoni J Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic pathway by ectopic expression of aMYB transcription factor in tomato fruit Plant Cell 23 2738-2753
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan XW Yang ZY (2017) Differential responses of fourbiosynthetic pathways of aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under interaction of light andtemperature Food Chem 221 356-364
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of differentially-expressed genes during somatic embryogenesis inFragaria times ananassa Duch Benihopp J Hortic Sci Biotechnol 90 671-681
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 transcriptionally regulates chilling-induced lignification ofloquat fruit via physical interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM (2004) Functional interactions between a glutaminesynthetase promoter and MYB proteins Plant J 39 513-526
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) Sucrose nonfermenting1-related protein kinase26 anortholog of open stomata1 is a negative regulator of strawberry fruit development and ripening Plant Physiol 167 915-930
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene expression in strawberry fruit (Fragaria times ananassa) byagroinfiltration a rapid assay for gene function analysis Plant J 48 818-826
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of selected aroma-active compounds in strawberries byheadspace solid-phase microextraction gas chromatography and correlation with sensory descriptive analysis J Food Sci 72 S487-S496
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid plays an important role in the regulation of strawberry fruitripening Plant Physiol 157 188-199
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of NaCl-stressed Arabidopsis roots reveals novel classes ofresponsive genes BMC Plant Biol 6 20
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN (2005) MYB98 is required for pollen tube guidance andsynergid cell differentiation in Arabidopsis Plant Cell 17 2981-2992
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional characterization of enone oxidoreductases from strawberry andtomato fruit J Agric Food Chem 55 6705-6711
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You J-S Rohloff J Randall SK Alsheikh M (2012) Proteomicstudy of low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ in cold tolerance Plant Physiol 159 1787-1805
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional characterization of four APETALA2-family genes (RAP26 RAP26LDREB19 and DREB26) in Arabidopsis Plant Mol Biol 75 107-127
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon J Gupta V (2013) An oxidoreductase from Alphonsomango catalyzing biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in strawberries Z Lebensm-Unters Forsch 195 120-123Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X (2015) Label-free quantitative proteomics to investigatestrawberry fruit proteome changes under controlled atmosphere and low temperature storage J Proteomics 120 44-57
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 cooperates with CitWRKY1 to participate in citric aciddegradation via up-regulation of CitAco3 J Exp Bot 68 3419-3426
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription factor CitERF71 activates the terpene synthase geneCitTPS16 involved in the synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and transcriptomic analysis of the AP2ERF superfamily inVitis vinifera BMC Genomics 11 719
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive Factor (AP2ERF) transcription factors mediators of stressresponses and developmental programs New Phytol 199 639-649
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 interacting with EOBI negatively regulates fragrancebiosynthesis in petunia flowers New Phytol 215 1490-1502
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 inregulating anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) during anthocyanin biosynthesis Plant CellTissue Organ Cult 115 285-298
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title wwwplantphysiolorgon February 25 2020 - Published by Downloaded from
Copyright copy 2018 American Society of Plant Biologists All rights reserved
Google Scholar Author Only Title Only Author and Title
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphatesignaling and homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597
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Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor regulates eugenol production in ripe strawberry fruitreceptacles Plant Physiol 168 598-614
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics and volatile constituents of strawberry (cv Cigaline)during maturation J Agric Food Chem 52 1248-1254
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS (2012) Ethylene-responsive transcription factors interact withpromoters of ADH and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 63 6393-6405
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-FrancoA Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific transcription factor FaDOF2 regulates the production ofeugenol in ripe fruit receptacles J Exp Bot 68 4529-4543
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) Comparison and verification of the genes involved in ethylenebiosynthesis and signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice Plant Physiol140 411-432
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in sour cherry and strawberry and the heterologousexpression of CBF1 in strawberry J Am Soc Hortic Sci 127 489-494
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech JC Ohme-Takagi M Regad F Bouzayen M (2012)Functional analysis and binding affinity of tomato ethylene response factors provide insight on the molecular bases of plant differentialresponses to ethylene BMC Plant Biol 12 190
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) Methylpentoses are possible precursors of furanones in fruits PriklBiokhim Mikrobiol 28 123-127
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery of synergid-expressed genes encoding filiformapparatus localized proteins Plant Cell 19 2557-2568
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria vesca L compared to those of cultivated berriesFragariatimes ananassa cv Senga Sengana J Agric Food Chem 27 19-22
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of thestrawberry flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone oxidoreductase Plant Cell 18 1023-1037
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Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim MBroun P Zhang JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription factors genome-wide comparative analysisamong eukaryotes Science 290 2105-2110
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wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the formation of 25-dimethyl-4-hydroxy-3(2H)-furanonein detached ripening strawberry fruits J Agric Food Chem 46 1488-1493
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Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in strawberry fruits Phytochemistry 43 155-159
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Schwab W (1998) Application of stable isotope ratio analysis explaining the bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone inplants by a biological maillard reaction J Agric Food Chem 46 2266ndash2269
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Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) Molecules 18 6936-6951Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard products Recent Res Dev Phytochem 1 643-673Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJSims CA Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical compositions a seasonal influence and effects on sensoryperception PLoS One 9 e88446
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Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) CitAP210 activation of the terpene synthase CsTPS1 isassociated with the synthesis of (+)-valencene in Newhall orange J Exp Bot 67 4105-4115
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Google Scholar Author Only Title Only Author and Title
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphatesignaling and homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor regulates eugenol production in ripe strawberry fruitreceptacles Plant Physiol 168 598-614
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics and volatile constituents of strawberry (cv Cigaline)during maturation J Agric Food Chem 52 1248-1254
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS (2012) Ethylene-responsive transcription factors interact withpromoters of ADH and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 63 6393-6405
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-FrancoA Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific transcription factor FaDOF2 regulates the production ofeugenol in ripe fruit receptacles J Exp Bot 68 4529-4543
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) Comparison and verification of the genes involved in ethylenebiosynthesis and signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice Plant Physiol140 411-432
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in sour cherry and strawberry and the heterologousexpression of CBF1 in strawberry J Am Soc Hortic Sci 127 489-494
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech JC Ohme-Takagi M Regad F Bouzayen M (2012)Functional analysis and binding affinity of tomato ethylene response factors provide insight on the molecular bases of plant differentialresponses to ethylene BMC Plant Biol 12 190
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) Methylpentoses are possible precursors of furanones in fruits PriklBiokhim Mikrobiol 28 123-127
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery of synergid-expressed genes encoding filiformapparatus localized proteins Plant Cell 19 2557-2568
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria vesca L compared to those of cultivated berriesFragariatimes ananassa cv Senga Sengana J Agric Food Chem 27 19-22
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of thestrawberry flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone oxidoreductase Plant Cell 18 1023-1037
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim MBroun P Zhang JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription factors genome-wide comparative analysisamong eukaryotes Science 290 2105-2110
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the formation of 25-dimethyl-4-hydroxy-3(2H)-furanonein detached ripening strawberry fruits J Agric Food Chem 46 1488-1493
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in strawberry fruits Phytochemistry 43 155-159
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (1998) Application of stable isotope ratio analysis explaining the bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone inplants by a biological maillard reaction J Agric Food Chem 46 2266ndash2269
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) Molecules 18 6936-6951Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard products Recent Res Dev Phytochem 1 643-673Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJSims CA Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical compositions a seasonal influence and effects on sensoryperception PLoS One 9 e88446
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) Identification phylogeny and transcript profiling of ERFfamily genes during development and abiotic stress treatments in tomato Mol Genet Genomics 284 455-475
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) CitAP210 activation of the terpene synthase CsTPS1 isassociated with the synthesis of (+)-valencene in Newhall orange J Exp Bot 67 4105-4115
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes Dev Genes Evol 214 105-114Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Spitzer-Rimon B Farhi M Albo B Cnaani A Ben Zvi MM Masci T Edelbaum O Yu YX Shklarman E Ovadis M Vainstein A (2012) TheR2R3-MYB-like regulatory factor EOBI acting downstream of EOBII regulates scent production by activating ODO1 and structuralscent-related genes in petunia Plant Cell 24 5089-5105
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp Bot 68 4407-4409Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla JF Amaya I Giavalisco P Fernie AR Botella MAValpuesta V (2015) Central role of FaGAMYB in the transition of the strawberry receptacle from development to ripening New Phytol208 482-496
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Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 regulates fragrance biosynthesis in petunia flowers PlantCell 17 1612-1624
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Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS (2018) The potassium channel FaTPK1 plays a critical role infruit quality formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748
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Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) Isolation cloning and expression of a multifunctional O- wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma compounds in strawberry fruitsPlant J 31 755-765
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Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor types their evolutionary origin and speciesdistribution In A handbook of transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular Biochemistry 52 25-73
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of odor (Buettner A Ed) Springer Cham 9-10Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS (2014) Isolation classification and transcription profiles ofthe AP2ERF transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in regulation of fruit quality Crit Rev Plant Sci 35 120-130
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ Zhang SL Wu J (2017) Map-based cloning of the pear geneMYB114 identifies an interaction with other transcription factors to coordinately regulate fruit anthocyanin biosynthesis Plant J 92437-451
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Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes involved in regulating fruit ripening Plant Physiol 1531280-1292
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Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) Expression of ethylene response genes during persimmonfruit astringency removal Planta 235 895-906
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zabetakis I Gramshaw JW Robinson DS (1999) 25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis andbiosynthesis-a review Food Chem 65 139-151
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Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci Food Agric 74 421-434Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 an AP2ERF gene is a novel regulator of fruit lignificationinduced by chilling injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1325-1334
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Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation classification and transcription profiles of the Ethylene ResponseFactors (ERFs) in ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215
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Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML (2012) Genome-wide analysis of the AP2ERF superfamily inpeach (Prunus persica) Genet Mol Res 11 4788-4809
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Genome-wide analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic (Amsterdam) 123 73-81Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF Valpuesta V Botella MA Granell A Amaya I (2012) Geneticanalysis of strawberry fruit aroma and identification of O-methyltransferase FaOMT as the locus controlling natural variation inmesifurane content Plant Physiol 159 851-870
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wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
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wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
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Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp Bot 68 4407-4409Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla JF Amaya I Giavalisco P Fernie AR Botella MAValpuesta V (2015) Central role of FaGAMYB in the transition of the strawberry receptacle from development to ripening New Phytol208 482-496
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 regulates fragrance biosynthesis in petunia flowers PlantCell 17 1612-1624
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS (2018) The potassium channel FaTPK1 plays a critical role infruit quality formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) Isolation cloning and expression of a multifunctional O- wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma compounds in strawberry fruitsPlant J 31 755-765
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor types their evolutionary origin and speciesdistribution In A handbook of transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular Biochemistry 52 25-73
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of odor (Buettner A Ed) Springer Cham 9-10Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS (2014) Isolation classification and transcription profiles ofthe AP2ERF transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in regulation of fruit quality Crit Rev Plant Sci 35 120-130
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ Zhang SL Wu J (2017) Map-based cloning of the pear geneMYB114 identifies an interaction with other transcription factors to coordinately regulate fruit anthocyanin biosynthesis Plant J 92437-451
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes involved in regulating fruit ripening Plant Physiol 1531280-1292
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) Expression of ethylene response genes during persimmonfruit astringency removal Planta 235 895-906
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zabetakis I Gramshaw JW Robinson DS (1999) 25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis andbiosynthesis-a review Food Chem 65 139-151
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci Food Agric 74 421-434Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 an AP2ERF gene is a novel regulator of fruit lignificationinduced by chilling injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1325-1334
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation classification and transcription profiles of the Ethylene ResponseFactors (ERFs) in ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML (2012) Genome-wide analysis of the AP2ERF superfamily inpeach (Prunus persica) Genet Mol Res 11 4788-4809
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and expression analysis of a CRTDRE-binding factor gene FaCBF1from Fragaria times ananassa Acta Hortic 41 240-248
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The Arabidopsis AP2ERF transcription factor RAP26 participatesin ABA salt and osmotic stress responses Gene 457 1-12
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Genome-wide analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic (Amsterdam) 123 73-81Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF Valpuesta V Botella MA Granell A Amaya I (2012) Geneticanalysis of strawberry fruit aroma and identification of O-methyltransferase FaOMT as the locus controlling natural variation inmesifurane content Plant Physiol 159 851-870
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Parsed CitationsAgarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression of PgDREB2A transcription factor enhances abioticstress tolerance and activates downstream stress-responsive genes Mol Biol Rep 37 1125-1135
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Araguumlez I Osorio S Hoffmann T Rambla JL Medina-Escobar N Granell A Botella MAacute Schwab W Valpuesta V (2013) Eugenolproduction in achenes and receptacles of strawberry fruits is catalyzed by synthases exhibiting distinct kinetics Plant Physiol 163 946-958
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Carvalho RF Carvalho SD OGrady K Folta KM (2016) Agroinfiltration of strawberry fruit - a powerful transient expression system forgene validation Curr Plant Biol 6 19-37
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic (Amsterdam) 210 34-40Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating RNA from pine trees Plant Mol Biol Rep 11 113-116Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC Clark DG (2011) PhMYB4 fine-tunes the floral volatilesignature of Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143
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Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 transcriptionally regulates chilling-induced lignification ofloquat fruit via physical interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136
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Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene expression in strawberry fruit (Fragaria times ananassa) byagroinfiltration a rapid assay for gene function analysis Plant J 48 818-826
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Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of selected aroma-active compounds in strawberries byheadspace solid-phase microextraction gas chromatography and correlation with sensory descriptive analysis J Food Sci 72 S487-S496
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wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid plays an important role in the regulation of strawberry fruitripening Plant Physiol 157 188-199
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Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN (2005) MYB98 is required for pollen tube guidance andsynergid cell differentiation in Arabidopsis Plant Cell 17 2981-2992
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Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional characterization of enone oxidoreductases from strawberry andtomato fruit J Agric Food Chem 55 6705-6711
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Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You J-S Rohloff J Randall SK Alsheikh M (2012) Proteomicstudy of low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ in cold tolerance Plant Physiol 159 1787-1805
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wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
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Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic (Amsterdam) 210 34-40Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating RNA from pine trees Plant Mol Biol Rep 11 113-116Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC Clark DG (2011) PhMYB4 fine-tunes the floral volatilesignature of Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz EA Taylor MG Smits-Kroon MT Schuurink RC HaringMA Giovannoni J Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic pathway by ectopic expression of aMYB transcription factor in tomato fruit Plant Cell 23 2738-2753
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan XW Yang ZY (2017) Differential responses of fourbiosynthetic pathways of aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under interaction of light andtemperature Food Chem 221 356-364
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of differentially-expressed genes during somatic embryogenesis inFragaria times ananassa Duch Benihopp J Hortic Sci Biotechnol 90 671-681
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 transcriptionally regulates chilling-induced lignification ofloquat fruit via physical interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM (2004) Functional interactions between a glutaminesynthetase promoter and MYB proteins Plant J 39 513-526
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) Sucrose nonfermenting1-related protein kinase26 anortholog of open stomata1 is a negative regulator of strawberry fruit development and ripening Plant Physiol 167 915-930
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene expression in strawberry fruit (Fragaria times ananassa) byagroinfiltration a rapid assay for gene function analysis Plant J 48 818-826
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of selected aroma-active compounds in strawberries byheadspace solid-phase microextraction gas chromatography and correlation with sensory descriptive analysis J Food Sci 72 S487-S496
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid plays an important role in the regulation of strawberry fruitripening Plant Physiol 157 188-199
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of NaCl-stressed Arabidopsis roots reveals novel classes ofresponsive genes BMC Plant Biol 6 20
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN (2005) MYB98 is required for pollen tube guidance andsynergid cell differentiation in Arabidopsis Plant Cell 17 2981-2992
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional characterization of enone oxidoreductases from strawberry andtomato fruit J Agric Food Chem 55 6705-6711
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You J-S Rohloff J Randall SK Alsheikh M (2012) Proteomicstudy of low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ in cold tolerance Plant Physiol 159 1787-1805
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional characterization of four APETALA2-family genes (RAP26 RAP26LDREB19 and DREB26) in Arabidopsis Plant Mol Biol 75 107-127
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon J Gupta V (2013) An oxidoreductase from Alphonsomango catalyzing biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in strawberries Z Lebensm-Unters Forsch 195 120-123Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X (2015) Label-free quantitative proteomics to investigatestrawberry fruit proteome changes under controlled atmosphere and low temperature storage J Proteomics 120 44-57
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 cooperates with CitWRKY1 to participate in citric aciddegradation via up-regulation of CitAco3 J Exp Bot 68 3419-3426
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription factor CitERF71 activates the terpene synthase geneCitTPS16 involved in the synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and transcriptomic analysis of the AP2ERF superfamily inVitis vinifera BMC Genomics 11 719
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive Factor (AP2ERF) transcription factors mediators of stressresponses and developmental programs New Phytol 199 639-649
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 interacting with EOBI negatively regulates fragrancebiosynthesis in petunia flowers New Phytol 215 1490-1502
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 inregulating anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) during anthocyanin biosynthesis Plant CellTissue Organ Cult 115 285-298
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title wwwplantphysiolorgon February 25 2020 - Published by Downloaded from
Copyright copy 2018 American Society of Plant Biologists All rights reserved
Google Scholar Author Only Title Only Author and Title
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphatesignaling and homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor regulates eugenol production in ripe strawberry fruitreceptacles Plant Physiol 168 598-614
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics and volatile constituents of strawberry (cv Cigaline)during maturation J Agric Food Chem 52 1248-1254
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS (2012) Ethylene-responsive transcription factors interact withpromoters of ADH and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 63 6393-6405
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-FrancoA Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific transcription factor FaDOF2 regulates the production ofeugenol in ripe fruit receptacles J Exp Bot 68 4529-4543
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) Comparison and verification of the genes involved in ethylenebiosynthesis and signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice Plant Physiol140 411-432
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in sour cherry and strawberry and the heterologousexpression of CBF1 in strawberry J Am Soc Hortic Sci 127 489-494
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech JC Ohme-Takagi M Regad F Bouzayen M (2012)Functional analysis and binding affinity of tomato ethylene response factors provide insight on the molecular bases of plant differentialresponses to ethylene BMC Plant Biol 12 190
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) Methylpentoses are possible precursors of furanones in fruits PriklBiokhim Mikrobiol 28 123-127
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery of synergid-expressed genes encoding filiformapparatus localized proteins Plant Cell 19 2557-2568
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria vesca L compared to those of cultivated berriesFragariatimes ananassa cv Senga Sengana J Agric Food Chem 27 19-22
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of thestrawberry flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone oxidoreductase Plant Cell 18 1023-1037
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim MBroun P Zhang JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription factors genome-wide comparative analysisamong eukaryotes Science 290 2105-2110
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the formation of 25-dimethyl-4-hydroxy-3(2H)-furanonein detached ripening strawberry fruits J Agric Food Chem 46 1488-1493
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in strawberry fruits Phytochemistry 43 155-159
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (1998) Application of stable isotope ratio analysis explaining the bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone inplants by a biological maillard reaction J Agric Food Chem 46 2266ndash2269
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) Molecules 18 6936-6951Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard products Recent Res Dev Phytochem 1 643-673Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJSims CA Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical compositions a seasonal influence and effects on sensoryperception PLoS One 9 e88446
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) Identification phylogeny and transcript profiling of ERFfamily genes during development and abiotic stress treatments in tomato Mol Genet Genomics 284 455-475
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) CitAP210 activation of the terpene synthase CsTPS1 isassociated with the synthesis of (+)-valencene in Newhall orange J Exp Bot 67 4105-4115
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes Dev Genes Evol 214 105-114Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151
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Spitzer-Rimon B Farhi M Albo B Cnaani A Ben Zvi MM Masci T Edelbaum O Yu YX Shklarman E Ovadis M Vainstein A (2012) TheR2R3-MYB-like regulatory factor EOBI acting downstream of EOBII regulates scent production by activating ODO1 and structuralscent-related genes in petunia Plant Cell 24 5089-5105
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Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp Bot 68 4407-4409Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla JF Amaya I Giavalisco P Fernie AR Botella MAValpuesta V (2015) Central role of FaGAMYB in the transition of the strawberry receptacle from development to ripening New Phytol208 482-496
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Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) Isolation cloning and expression of a multifunctional O- wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma compounds in strawberry fruitsPlant J 31 755-765
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wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
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Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics and volatile constituents of strawberry (cv Cigaline)during maturation J Agric Food Chem 52 1248-1254
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS (2012) Ethylene-responsive transcription factors interact withpromoters of ADH and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 63 6393-6405
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-FrancoA Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific transcription factor FaDOF2 regulates the production ofeugenol in ripe fruit receptacles J Exp Bot 68 4529-4543
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) Comparison and verification of the genes involved in ethylenebiosynthesis and signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice Plant Physiol140 411-432
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in sour cherry and strawberry and the heterologousexpression of CBF1 in strawberry J Am Soc Hortic Sci 127 489-494
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech JC Ohme-Takagi M Regad F Bouzayen M (2012)Functional analysis and binding affinity of tomato ethylene response factors provide insight on the molecular bases of plant differentialresponses to ethylene BMC Plant Biol 12 190
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) Methylpentoses are possible precursors of furanones in fruits PriklBiokhim Mikrobiol 28 123-127
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery of synergid-expressed genes encoding filiformapparatus localized proteins Plant Cell 19 2557-2568
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria vesca L compared to those of cultivated berriesFragariatimes ananassa cv Senga Sengana J Agric Food Chem 27 19-22
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of thestrawberry flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone oxidoreductase Plant Cell 18 1023-1037
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim MBroun P Zhang JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription factors genome-wide comparative analysisamong eukaryotes Science 290 2105-2110
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the formation of 25-dimethyl-4-hydroxy-3(2H)-furanonein detached ripening strawberry fruits J Agric Food Chem 46 1488-1493
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in strawberry fruits Phytochemistry 43 155-159
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (1998) Application of stable isotope ratio analysis explaining the bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone inplants by a biological maillard reaction J Agric Food Chem 46 2266ndash2269
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) Molecules 18 6936-6951Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard products Recent Res Dev Phytochem 1 643-673Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJSims CA Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical compositions a seasonal influence and effects on sensoryperception PLoS One 9 e88446
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) Identification phylogeny and transcript profiling of ERFfamily genes during development and abiotic stress treatments in tomato Mol Genet Genomics 284 455-475
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) CitAP210 activation of the terpene synthase CsTPS1 isassociated with the synthesis of (+)-valencene in Newhall orange J Exp Bot 67 4105-4115
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes Dev Genes Evol 214 105-114Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Spitzer-Rimon B Farhi M Albo B Cnaani A Ben Zvi MM Masci T Edelbaum O Yu YX Shklarman E Ovadis M Vainstein A (2012) TheR2R3-MYB-like regulatory factor EOBI acting downstream of EOBII regulates scent production by activating ODO1 and structuralscent-related genes in petunia Plant Cell 24 5089-5105
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp Bot 68 4407-4409Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla JF Amaya I Giavalisco P Fernie AR Botella MAValpuesta V (2015) Central role of FaGAMYB in the transition of the strawberry receptacle from development to ripening New Phytol208 482-496
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 regulates fragrance biosynthesis in petunia flowers PlantCell 17 1612-1624
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS (2018) The potassium channel FaTPK1 plays a critical role infruit quality formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) Isolation cloning and expression of a multifunctional O- wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma compounds in strawberry fruitsPlant J 31 755-765
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor types their evolutionary origin and speciesdistribution In A handbook of transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular Biochemistry 52 25-73
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of odor (Buettner A Ed) Springer Cham 9-10Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS (2014) Isolation classification and transcription profiles ofthe AP2ERF transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in regulation of fruit quality Crit Rev Plant Sci 35 120-130
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ Zhang SL Wu J (2017) Map-based cloning of the pear geneMYB114 identifies an interaction with other transcription factors to coordinately regulate fruit anthocyanin biosynthesis Plant J 92437-451
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes involved in regulating fruit ripening Plant Physiol 1531280-1292
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) Expression of ethylene response genes during persimmonfruit astringency removal Planta 235 895-906
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zabetakis I Gramshaw JW Robinson DS (1999) 25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis andbiosynthesis-a review Food Chem 65 139-151
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci Food Agric 74 421-434Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 an AP2ERF gene is a novel regulator of fruit lignificationinduced by chilling injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1325-1334
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation classification and transcription profiles of the Ethylene ResponseFactors (ERFs) in ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML (2012) Genome-wide analysis of the AP2ERF superfamily inpeach (Prunus persica) Genet Mol Res 11 4788-4809
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and expression analysis of a CRTDRE-binding factor gene FaCBF1from Fragaria times ananassa Acta Hortic 41 240-248
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Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The Arabidopsis AP2ERF transcription factor RAP26 participatesin ABA salt and osmotic stress responses Gene 457 1-12
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Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Genome-wide analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic (Amsterdam) 123 73-81Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF Valpuesta V Botella MA Granell A Amaya I (2012) Geneticanalysis of strawberry fruit aroma and identification of O-methyltransferase FaOMT as the locus controlling natural variation inmesifurane content Plant Physiol 159 851-870
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wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Parsed CitationsAgarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression of PgDREB2A transcription factor enhances abioticstress tolerance and activates downstream stress-responsive genes Mol Biol Rep 37 1125-1135
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Araguumlez I Osorio S Hoffmann T Rambla JL Medina-Escobar N Granell A Botella MAacute Schwab W Valpuesta V (2013) Eugenolproduction in achenes and receptacles of strawberry fruits is catalyzed by synthases exhibiting distinct kinetics Plant Physiol 163 946-958
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Carvalho RF Carvalho SD OGrady K Folta KM (2016) Agroinfiltration of strawberry fruit - a powerful transient expression system forgene validation Curr Plant Biol 6 19-37
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Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic (Amsterdam) 210 34-40Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating RNA from pine trees Plant Mol Biol Rep 11 113-116Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC Clark DG (2011) PhMYB4 fine-tunes the floral volatilesignature of Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143
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Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz EA Taylor MG Smits-Kroon MT Schuurink RC HaringMA Giovannoni J Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic pathway by ectopic expression of aMYB transcription factor in tomato fruit Plant Cell 23 2738-2753
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Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 transcriptionally regulates chilling-induced lignification ofloquat fruit via physical interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136
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methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma compounds in strawberry fruitsPlant J 31 755-765
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor types their evolutionary origin and speciesdistribution In A handbook of transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular Biochemistry 52 25-73
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of odor (Buettner A Ed) Springer Cham 9-10Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS (2014) Isolation classification and transcription profiles ofthe AP2ERF transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in regulation of fruit quality Crit Rev Plant Sci 35 120-130
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ Zhang SL Wu J (2017) Map-based cloning of the pear geneMYB114 identifies an interaction with other transcription factors to coordinately regulate fruit anthocyanin biosynthesis Plant J 92437-451
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes involved in regulating fruit ripening Plant Physiol 1531280-1292
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) Expression of ethylene response genes during persimmonfruit astringency removal Planta 235 895-906
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zabetakis I Gramshaw JW Robinson DS (1999) 25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis andbiosynthesis-a review Food Chem 65 139-151
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci Food Agric 74 421-434Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 an AP2ERF gene is a novel regulator of fruit lignificationinduced by chilling injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1325-1334
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation classification and transcription profiles of the Ethylene ResponseFactors (ERFs) in ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML (2012) Genome-wide analysis of the AP2ERF superfamily inpeach (Prunus persica) Genet Mol Res 11 4788-4809
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and expression analysis of a CRTDRE-binding factor gene FaCBF1from Fragaria times ananassa Acta Hortic 41 240-248
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The Arabidopsis AP2ERF transcription factor RAP26 participatesin ABA salt and osmotic stress responses Gene 457 1-12
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Genome-wide analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic (Amsterdam) 123 73-81Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF Valpuesta V Botella MA Granell A Amaya I (2012) Geneticanalysis of strawberry fruit aroma and identification of O-methyltransferase FaOMT as the locus controlling natural variation inmesifurane content Plant Physiol 159 851-870
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Parsed CitationsAgarwal P Agarwal PK Joshi AJ Sopory SK Reddy MK (2010) Overexpression of PgDREB2A transcription factor enhances abioticstress tolerance and activates downstream stress-responsive genes Mol Biol Rep 37 1125-1135
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Araguumlez I Osorio S Hoffmann T Rambla JL Medina-Escobar N Granell A Botella MAacute Schwab W Valpuesta V (2013) Eugenolproduction in achenes and receptacles of strawberry fruits is catalyzed by synthases exhibiting distinct kinetics Plant Physiol 163 946-958
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Carvalho RF Carvalho SD OGrady K Folta KM (2016) Agroinfiltration of strawberry fruit - a powerful transient expression system forgene validation Curr Plant Biol 6 19-37
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Chai L Shen YY (2016) FaABI4 is involved in strawberry fruit ripening Sci Hortic (Amsterdam) 210 34-40Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Chang SJ Puryear J Cairney J (1993) A simple and efficient method for isolating RNA from pine trees Plant Mol Biol Rep 11 113-116Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Colquhoun TA Kim JY Wedde AE Levin LA Schmitt KC Schuurink RC Clark DG (2011) PhMYB4 fine-tunes the floral volatilesignature of Petuniatimeshybrida through PhC4H J Exp Bot 62 1133-1143
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Dal Cin V Tieman DM Tohge T McQuinn R de Vos RCH Osorio S Schmelz EA Taylor MG Smits-Kroon MT Schuurink RC HaringMA Giovannoni J Fernie AR Klee HJ (2011) Identification of genes in the phenylalanine metabolic pathway by ectopic expression of aMYB transcription factor in tomato fruit Plant Cell 23 2738-2753
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Fu XM Cheng SH Zhang YQ Du B Feng C Zhou Y Mei X Jiang YM Duan XW Yang ZY (2017) Differential responses of fourbiosynthetic pathways of aroma compounds in postharvest strawberry ( Fragaria times ananassa Duch) under interaction of light andtemperature Food Chem 221 356-364
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gao LM Zhang J Hou Y Yao YC Ji QL (2015) RNA-Seq screening of differentially-expressed genes during somatic embryogenesis inFragaria times ananassa Duch Benihopp J Hortic Sci Biotechnol 90 671-681
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Ge H Zhang J Zhang YJ Li X Yin XR Grierson D Chen KS (2017) EjNAC3 transcriptionally regulates chilling-induced lignification ofloquat fruit via physical interaction with an atypical CAD-like gene J Exp Bot 68 5129-5136
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Goacutemez-Maldonado J Avila C Torre F Cantildeas R Caacutenovas FM Campbell MM (2004) Functional interactions between a glutaminesynthetase promoter and MYB proteins Plant J 39 513-526
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Han Y Dang R Li J Jiang J Zhang N Jia M Wei L Li Z Li B Jia W (2015) Sucrose nonfermenting1-related protein kinase26 anortholog of open stomata1 is a negative regulator of strawberry fruit development and ripening Plant Physiol 167 915-930
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene expression in strawberry fruit (Fragaria times ananassa) byagroinfiltration a rapid assay for gene function analysis Plant J 48 818-826
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Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of selected aroma-active compounds in strawberries byheadspace solid-phase microextraction gas chromatography and correlation with sensory descriptive analysis J Food Sci 72 S487-S496
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid plays an important role in the regulation of strawberry fruitripening Plant Physiol 157 188-199
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Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of NaCl-stressed Arabidopsis roots reveals novel classes ofresponsive genes BMC Plant Biol 6 20
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN (2005) MYB98 is required for pollen tube guidance andsynergid cell differentiation in Arabidopsis Plant Cell 17 2981-2992
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Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional characterization of enone oxidoreductases from strawberry andtomato fruit J Agric Food Chem 55 6705-6711
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You J-S Rohloff J Randall SK Alsheikh M (2012) Proteomicstudy of low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ in cold tolerance Plant Physiol 159 1787-1805
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Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional characterization of four APETALA2-family genes (RAP26 RAP26LDREB19 and DREB26) in Arabidopsis Plant Mol Biol 75 107-127
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Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon J Gupta V (2013) An oxidoreductase from Alphonsomango catalyzing biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494
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Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in strawberries Z Lebensm-Unters Forsch 195 120-123Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X (2015) Label-free quantitative proteomics to investigatestrawberry fruit proteome changes under controlled atmosphere and low temperature storage J Proteomics 120 44-57
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Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 cooperates with CitWRKY1 to participate in citric aciddegradation via up-regulation of CitAco3 J Exp Bot 68 3419-3426
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Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription factor CitERF71 activates the terpene synthase geneCitTPS16 involved in the synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938
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Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and transcriptomic analysis of the AP2ERF superfamily inVitis vinifera BMC Genomics 11 719
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Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive Factor (AP2ERF) transcription factors mediators of stressresponses and developmental programs New Phytol 199 639-649
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Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 interacting with EOBI negatively regulates fragrancebiosynthesis in petunia flowers New Phytol 215 1490-1502
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Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 inregulating anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) during anthocyanin biosynthesis Plant CellTissue Organ Cult 115 285-298
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Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS (2012) Ethylene-responsive transcription factors interact withpromoters of ADH and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 63 6393-6405
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Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Hoffmann T Kalinowski G Schwab W (2006) RNAi-induced silencing of gene expression in strawberry fruit (Fragaria times ananassa) byagroinfiltration a rapid assay for gene function analysis Plant J 48 818-826
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jetti RR Yang E Kurnianta A Finn C Qian MC (2007) Quantification of selected aroma-active compounds in strawberries byheadspace solid-phase microextraction gas chromatography and correlation with sensory descriptive analysis J Food Sci 72 S487-S496
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Jia HF Chai YM Li CL Lu D Luo JJ Qin L Shen YY (2011) Abscisic acid plays an important role in the regulation of strawberry fruitripening Plant Physiol 157 188-199
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jiang YQ Deyholos MK (2006) Comprehensive transcriptional profiling of NaCl-stressed Arabidopsis roots reveals novel classes ofresponsive genes BMC Plant Biol 6 20
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kasahara RD Portereiko MF Sandaklie-Nikolova L Rabiger DS Drews GN (2005) MYB98 is required for pollen tube guidance andsynergid cell differentiation in Arabidopsis Plant Cell 17 2981-2992
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Klein D Fink B Arold B Eisenreich W Schwab W (2007) Functional characterization of enone oxidoreductases from strawberry andtomato fruit J Agric Food Chem 55 6705-6711
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Koehler G Wilson RC Goodpaster JV Sonsteby A Lai X Witzmann FA You J-S Rohloff J Randall SK Alsheikh M (2012) Proteomicstudy of low-temperature responses in strawberry cultivars (Fragaria x ananassa) that differ in cold tolerance Plant Physiol 159 1787-1805
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Krishnaswamy S Verma S Rahman MH Kav NNV (2011) Functional characterization of four APETALA2-family genes (RAP26 RAP26LDREB19 and DREB26) in Arabidopsis Plant Mol Biol 75 107-127
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon J Gupta V (2013) An oxidoreductase from Alphonsomango catalyzing biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Larsen M Poll L (1992) Odour thresholds of some important aroma compounds in strawberries Z Lebensm-Unters Forsch 195 120-123Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X (2015) Label-free quantitative proteomics to investigatestrawberry fruit proteome changes under controlled atmosphere and low temperature storage J Proteomics 120 44-57
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 cooperates with CitWRKY1 to participate in citric aciddegradation via up-regulation of CitAco3 J Exp Bot 68 3419-3426
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription factor CitERF71 activates the terpene synthase geneCitTPS16 involved in the synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and transcriptomic analysis of the AP2ERF superfamily inVitis vinifera BMC Genomics 11 719
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive Factor (AP2ERF) transcription factors mediators of stressresponses and developmental programs New Phytol 199 639-649
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 interacting with EOBI negatively regulates fragrancebiosynthesis in petunia flowers New Phytol 215 1490-1502
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 inregulating anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) during anthocyanin biosynthesis Plant CellTissue Organ Cult 115 285-298
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title wwwplantphysiolorgon February 25 2020 - Published by Downloaded from
Copyright copy 2018 American Society of Plant Biologists All rights reserved
Google Scholar Author Only Title Only Author and Title
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphatesignaling and homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor regulates eugenol production in ripe strawberry fruitreceptacles Plant Physiol 168 598-614
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics and volatile constituents of strawberry (cv Cigaline)during maturation J Agric Food Chem 52 1248-1254
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS (2012) Ethylene-responsive transcription factors interact withpromoters of ADH and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 63 6393-6405
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-FrancoA Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific transcription factor FaDOF2 regulates the production ofeugenol in ripe fruit receptacles J Exp Bot 68 4529-4543
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) Comparison and verification of the genes involved in ethylenebiosynthesis and signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice Plant Physiol140 411-432
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in sour cherry and strawberry and the heterologousexpression of CBF1 in strawberry J Am Soc Hortic Sci 127 489-494
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech JC Ohme-Takagi M Regad F Bouzayen M (2012)Functional analysis and binding affinity of tomato ethylene response factors provide insight on the molecular bases of plant differentialresponses to ethylene BMC Plant Biol 12 190
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) Methylpentoses are possible precursors of furanones in fruits PriklBiokhim Mikrobiol 28 123-127
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery of synergid-expressed genes encoding filiformapparatus localized proteins Plant Cell 19 2557-2568
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria vesca L compared to those of cultivated berriesFragariatimes ananassa cv Senga Sengana J Agric Food Chem 27 19-22
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of thestrawberry flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone oxidoreductase Plant Cell 18 1023-1037
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Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim MBroun P Zhang JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription factors genome-wide comparative analysisamong eukaryotes Science 290 2105-2110
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the formation of 25-dimethyl-4-hydroxy-3(2H)-furanonein detached ripening strawberry fruits J Agric Food Chem 46 1488-1493
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in strawberry fruits Phytochemistry 43 155-159
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (1998) Application of stable isotope ratio analysis explaining the bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone inplants by a biological maillard reaction J Agric Food Chem 46 2266ndash2269
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) Molecules 18 6936-6951Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard products Recent Res Dev Phytochem 1 643-673Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJSims CA Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical compositions a seasonal influence and effects on sensoryperception PLoS One 9 e88446
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) Identification phylogeny and transcript profiling of ERFfamily genes during development and abiotic stress treatments in tomato Mol Genet Genomics 284 455-475
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) CitAP210 activation of the terpene synthase CsTPS1 isassociated with the synthesis of (+)-valencene in Newhall orange J Exp Bot 67 4105-4115
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Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes Dev Genes Evol 214 105-114Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151
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Spitzer-Rimon B Farhi M Albo B Cnaani A Ben Zvi MM Masci T Edelbaum O Yu YX Shklarman E Ovadis M Vainstein A (2012) TheR2R3-MYB-like regulatory factor EOBI acting downstream of EOBII regulates scent production by activating ODO1 and structuralscent-related genes in petunia Plant Cell 24 5089-5105
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Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp Bot 68 4407-4409Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla JF Amaya I Giavalisco P Fernie AR Botella MAValpuesta V (2015) Central role of FaGAMYB in the transition of the strawberry receptacle from development to ripening New Phytol208 482-496
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Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 regulates fragrance biosynthesis in petunia flowers PlantCell 17 1612-1624
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Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS (2018) The potassium channel FaTPK1 plays a critical role infruit quality formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748
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Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) Isolation cloning and expression of a multifunctional O- wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma compounds in strawberry fruitsPlant J 31 755-765
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Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor types their evolutionary origin and speciesdistribution In A handbook of transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular Biochemistry 52 25-73
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Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS (2014) Isolation classification and transcription profiles ofthe AP2ERF transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271
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Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in regulation of fruit quality Crit Rev Plant Sci 35 120-130
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Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes involved in regulating fruit ripening Plant Physiol 1531280-1292
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Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) Expression of ethylene response genes during persimmonfruit astringency removal Planta 235 895-906
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Zabetakis I Gramshaw JW Robinson DS (1999) 25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis andbiosynthesis-a review Food Chem 65 139-151
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Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci Food Agric 74 421-434Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 an AP2ERF gene is a novel regulator of fruit lignificationinduced by chilling injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1325-1334
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wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
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Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria vesca L compared to those of cultivated berriesFragariatimes ananassa cv Senga Sengana J Agric Food Chem 27 19-22
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of thestrawberry flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone oxidoreductase Plant Cell 18 1023-1037
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim MBroun P Zhang JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription factors genome-wide comparative analysisamong eukaryotes Science 290 2105-2110
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the formation of 25-dimethyl-4-hydroxy-3(2H)-furanonein detached ripening strawberry fruits J Agric Food Chem 46 1488-1493
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in strawberry fruits Phytochemistry 43 155-159
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (1998) Application of stable isotope ratio analysis explaining the bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone inplants by a biological maillard reaction J Agric Food Chem 46 2266ndash2269
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) Molecules 18 6936-6951Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard products Recent Res Dev Phytochem 1 643-673Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJSims CA Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical compositions a seasonal influence and effects on sensoryperception PLoS One 9 e88446
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) Identification phylogeny and transcript profiling of ERFfamily genes during development and abiotic stress treatments in tomato Mol Genet Genomics 284 455-475
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) CitAP210 activation of the terpene synthase CsTPS1 isassociated with the synthesis of (+)-valencene in Newhall orange J Exp Bot 67 4105-4115
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes Dev Genes Evol 214 105-114Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Spitzer-Rimon B Farhi M Albo B Cnaani A Ben Zvi MM Masci T Edelbaum O Yu YX Shklarman E Ovadis M Vainstein A (2012) TheR2R3-MYB-like regulatory factor EOBI acting downstream of EOBII regulates scent production by activating ODO1 and structuralscent-related genes in petunia Plant Cell 24 5089-5105
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp Bot 68 4407-4409Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla JF Amaya I Giavalisco P Fernie AR Botella MAValpuesta V (2015) Central role of FaGAMYB in the transition of the strawberry receptacle from development to ripening New Phytol208 482-496
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 regulates fragrance biosynthesis in petunia flowers PlantCell 17 1612-1624
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS (2018) The potassium channel FaTPK1 plays a critical role infruit quality formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) Isolation cloning and expression of a multifunctional O- wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma compounds in strawberry fruitsPlant J 31 755-765
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor types their evolutionary origin and speciesdistribution In A handbook of transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular Biochemistry 52 25-73
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of odor (Buettner A Ed) Springer Cham 9-10Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS (2014) Isolation classification and transcription profiles ofthe AP2ERF transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in regulation of fruit quality Crit Rev Plant Sci 35 120-130
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ Zhang SL Wu J (2017) Map-based cloning of the pear geneMYB114 identifies an interaction with other transcription factors to coordinately regulate fruit anthocyanin biosynthesis Plant J 92437-451
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes involved in regulating fruit ripening Plant Physiol 1531280-1292
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) Expression of ethylene response genes during persimmonfruit astringency removal Planta 235 895-906
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zabetakis I Gramshaw JW Robinson DS (1999) 25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis andbiosynthesis-a review Food Chem 65 139-151
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci Food Agric 74 421-434Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 an AP2ERF gene is a novel regulator of fruit lignificationinduced by chilling injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1325-1334
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation classification and transcription profiles of the Ethylene ResponseFactors (ERFs) in ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML (2012) Genome-wide analysis of the AP2ERF superfamily inpeach (Prunus persica) Genet Mol Res 11 4788-4809
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Genome-wide analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic (Amsterdam) 123 73-81Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF Valpuesta V Botella MA Granell A Amaya I (2012) Geneticanalysis of strawberry fruit aroma and identification of O-methyltransferase FaOMT as the locus controlling natural variation inmesifurane content Plant Physiol 159 851-870
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wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
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Kulkarni R Chidley H Deshpande A Schmidt A Pujari K Giri A Gershenzon J Gupta V (2013) An oxidoreductase from Alphonsomango catalyzing biosynthesis of furaneol and reduction of reactive carbonyls SpringerPlus 2 494
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Li L Luo ZS Huang XH Zhang L Zhao PY Ma HY Li XH Ban ZJ Liu X (2015) Label-free quantitative proteomics to investigatestrawberry fruit proteome changes under controlled atmosphere and low temperature storage J Proteomics 120 44-57
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Li SJ Yin XR Wang WL Liu XF Zhang B Chen KS (2017) Citrus CitNAC62 cooperates with CitWRKY1 to participate in citric aciddegradation via up-regulation of CitAco3 J Exp Bot 68 3419-3426
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Li X Xu YY Shen SL Yin XR Klee HJ Zhang B Chen KS (2017) Transcription factor CitERF71 activates the terpene synthase geneCitTPS16 involved in the synthesis of E-geraniol in sweet orange fruit J Exp Bot 68 4929-4938
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Licausi F Giorgi FM Zenoni S Osti F Pezzotti M Perata P (2010) Genomic and transcriptomic analysis of the AP2ERF superfamily inVitis vinifera BMC Genomics 11 719
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Licausi F Ohme-Takagi M Perata P (2013) APETALA2Ethylene Responsive Factor (AP2ERF) transcription factors mediators of stressresponses and developmental programs New Phytol 199 639-649
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Liu F Xiao ZN Yang L Chen Q Shao L Liu JX Yu YX (2017) PhERF6 interacting with EOBI negatively regulates fragrancebiosynthesis in petunia flowers New Phytol 215 1490-1502
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Liu XF Yin XR Allan AC Lin Wang K Shi YN Huang YJ Ferguson IB Xu CJ Chen KS (2013) The role of MrbHLH1 and MrMYB1 inregulating anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) during anthocyanin biosynthesis Plant CellTissue Organ Cult 115 285-298
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Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics and volatile constituents of strawberry (cv Cigaline)during maturation J Agric Food Chem 52 1248-1254
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS (2012) Ethylene-responsive transcription factors interact withpromoters of ADH and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 63 6393-6405
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Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-FrancoA Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific transcription factor FaDOF2 regulates the production ofeugenol in ripe fruit receptacles J Exp Bot 68 4529-4543
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Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) Comparison and verification of the genes involved in ethylenebiosynthesis and signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice Plant Physiol140 411-432
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in sour cherry and strawberry and the heterologousexpression of CBF1 in strawberry J Am Soc Hortic Sci 127 489-494
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech JC Ohme-Takagi M Regad F Bouzayen M (2012)Functional analysis and binding affinity of tomato ethylene response factors provide insight on the molecular bases of plant differentialresponses to ethylene BMC Plant Biol 12 190
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) Methylpentoses are possible precursors of furanones in fruits PriklBiokhim Mikrobiol 28 123-127
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery of synergid-expressed genes encoding filiformapparatus localized proteins Plant Cell 19 2557-2568
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria vesca L compared to those of cultivated berriesFragariatimes ananassa cv Senga Sengana J Agric Food Chem 27 19-22
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of thestrawberry flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone oxidoreductase Plant Cell 18 1023-1037
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim MBroun P Zhang JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription factors genome-wide comparative analysisamong eukaryotes Science 290 2105-2110
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the formation of 25-dimethyl-4-hydroxy-3(2H)-furanonein detached ripening strawberry fruits J Agric Food Chem 46 1488-1493
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in strawberry fruits Phytochemistry 43 155-159
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (1998) Application of stable isotope ratio analysis explaining the bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone inplants by a biological maillard reaction J Agric Food Chem 46 2266ndash2269
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) Molecules 18 6936-6951Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard products Recent Res Dev Phytochem 1 643-673Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJSims CA Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical compositions a seasonal influence and effects on sensoryperception PLoS One 9 e88446
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) Identification phylogeny and transcript profiling of ERFfamily genes during development and abiotic stress treatments in tomato Mol Genet Genomics 284 455-475
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) CitAP210 activation of the terpene synthase CsTPS1 isassociated with the synthesis of (+)-valencene in Newhall orange J Exp Bot 67 4105-4115
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes Dev Genes Evol 214 105-114Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Spitzer-Rimon B Farhi M Albo B Cnaani A Ben Zvi MM Masci T Edelbaum O Yu YX Shklarman E Ovadis M Vainstein A (2012) TheR2R3-MYB-like regulatory factor EOBI acting downstream of EOBII regulates scent production by activating ODO1 and structuralscent-related genes in petunia Plant Cell 24 5089-5105
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp Bot 68 4407-4409Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla JF Amaya I Giavalisco P Fernie AR Botella MAValpuesta V (2015) Central role of FaGAMYB in the transition of the strawberry receptacle from development to ripening New Phytol208 482-496
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 regulates fragrance biosynthesis in petunia flowers PlantCell 17 1612-1624
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS (2018) The potassium channel FaTPK1 plays a critical role infruit quality formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) Isolation cloning and expression of a multifunctional O- wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma compounds in strawberry fruitsPlant J 31 755-765
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor types their evolutionary origin and speciesdistribution In A handbook of transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular Biochemistry 52 25-73
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of odor (Buettner A Ed) Springer Cham 9-10Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS (2014) Isolation classification and transcription profiles ofthe AP2ERF transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in regulation of fruit quality Crit Rev Plant Sci 35 120-130
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ Zhang SL Wu J (2017) Map-based cloning of the pear geneMYB114 identifies an interaction with other transcription factors to coordinately regulate fruit anthocyanin biosynthesis Plant J 92437-451
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes involved in regulating fruit ripening Plant Physiol 1531280-1292
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) Expression of ethylene response genes during persimmonfruit astringency removal Planta 235 895-906
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zabetakis I Gramshaw JW Robinson DS (1999) 25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis andbiosynthesis-a review Food Chem 65 139-151
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci Food Agric 74 421-434Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 an AP2ERF gene is a novel regulator of fruit lignificationinduced by chilling injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1325-1334
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation classification and transcription profiles of the Ethylene ResponseFactors (ERFs) in ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML (2012) Genome-wide analysis of the AP2ERF superfamily inpeach (Prunus persica) Genet Mol Res 11 4788-4809
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and expression analysis of a CRTDRE-binding factor gene FaCBF1from Fragaria times ananassa Acta Hortic 41 240-248
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The Arabidopsis AP2ERF transcription factor RAP26 participatesin ABA salt and osmotic stress responses Gene 457 1-12
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Genome-wide analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic (Amsterdam) 123 73-81Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF Valpuesta V Botella MA Granell A Amaya I (2012) Geneticanalysis of strawberry fruit aroma and identification of O-methyltransferase FaOMT as the locus controlling natural variation inmesifurane content Plant Physiol 159 851-870
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Google Scholar Author Only Title Only Author and Title
Lv QD Zhong YJ Wang YG Wang ZY Zhang L Shi J Wu ZC Liu Y Mao CZ Yi KK Wu P (2014) SPX4 negatively regulates phosphatesignaling and homeostasis through its interaction with PHR2 in rice Plant Cell 26 1586-1597
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Medina-Puche L Molina-Hidalgo FJ Boersma M Schuurink RC Loacutepez-Vidriero I Solano R Franco-Zorrilla J-M Caballero JL Blanco-Portales R Muntildeoz-Blanco J (2015) An R2R3-MYB transcription factor regulates eugenol production in ripe strawberry fruitreceptacles Plant Physiol 168 598-614
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Meacutenager I Jost M Aubert C (2004) Changes in physicochemical characteristics and volatile constituents of strawberry (cv Cigaline)during maturation J Agric Food Chem 52 1248-1254
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Min T Yin XR Shi YN Luo ZR Yao Y Grierson D Ferguson IB Chen KS (2012) Ethylene-responsive transcription factors interact withpromoters of ADH and PDC involved in persimmon (Diospyros kaki) fruit de-astringency J Exp Bot 63 6393-6405
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Molina-Hidalgo FJ Medina-Puche L Cantildeete-Goacutemez C Franco-Zorrilla JM Loacutepez-Vidriero I Solano R Caballero JL Rodriacuteguez-FrancoA Blanco-Portales R Muntildeoz-Blanco J Moyano E (2017) The fruit-specific transcription factor FaDOF2 regulates the production ofeugenol in ripe fruit receptacles J Exp Bot 68 4529-4543
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mu Q Wang BJ Leng XP Sun X Shangguan LF Jia HF Fang JG (2016) Comparison and verification of the genes involved in ethylenebiosynthesis and signaling in apple grape peach pear and strawberry Acta Physiol Plant 38 44
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Nakano T Suzuki K Fujimura T Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice Plant Physiol140 411-432
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Owens CL Thomashow MF Hancock JF Iezzoni AF (2002) CBF1 orthologs in sour cherry and strawberry and the heterologousexpression of CBF1 in strawberry J Am Soc Hortic Sci 127 489-494
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pirrello J Prasad BN Zhang WS Chen KS Mila I Zouine M Latcheacute A Pech JC Ohme-Takagi M Regad F Bouzayen M (2012)Functional analysis and binding affinity of tomato ethylene response factors provide insight on the molecular bases of plant differentialresponses to ethylene BMC Plant Biol 12 190
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pisarnitskii AF Demechenko AG Egorov IA Gvelesiani RK (1992) Methylpentoses are possible precursors of furanones in fruits PriklBiokhim Mikrobiol 28 123-127
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Punwani JA Rabiger DS Drews GN (2007) MYB98 positively regulates a battery of synergid-expressed genes encoding filiformapparatus localized proteins Plant Cell 19 2557-2568
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pyysalo T Honkanen E Hirvi T (1979) Volatiles of wild strawberries Fragaria vesca L compared to those of cultivated berriesFragariatimes ananassa cv Senga Sengana J Agric Food Chem 27 19-22
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Raab T Loacutepez-Raacuteez JA Klein D Caballero JL Moyano E Schwab W Muntildeoz-Blanco J (2006) FaQR required for the biosynthesis of thestrawberry flavor compound 4-hydroxy-25-dimethyl-3(2H)-furanone encodes an enone oxidoreductase Plant Cell 18 1023-1037
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Riechmann JL Heard J Martin G Reuber L Jiang CZ Keddie J Adam L Pineda O Ratcliffe OJ Samaha RR Creelman R Pilgrim MBroun P Zhang JZ Ghandehari D Sherman BK Yu GL (2000) Arabidopsis transcription factors genome-wide comparative analysisamong eukaryotes Science 290 2105-2110
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the formation of 25-dimethyl-4-hydroxy-3(2H)-furanonein detached ripening strawberry fruits J Agric Food Chem 46 1488-1493
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in strawberry fruits Phytochemistry 43 155-159
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (1998) Application of stable isotope ratio analysis explaining the bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone inplants by a biological maillard reaction J Agric Food Chem 46 2266ndash2269
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) Molecules 18 6936-6951Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard products Recent Res Dev Phytochem 1 643-673Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJSims CA Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical compositions a seasonal influence and effects on sensoryperception PLoS One 9 e88446
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) Identification phylogeny and transcript profiling of ERFfamily genes during development and abiotic stress treatments in tomato Mol Genet Genomics 284 455-475
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) CitAP210 activation of the terpene synthase CsTPS1 isassociated with the synthesis of (+)-valencene in Newhall orange J Exp Bot 67 4105-4115
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes Dev Genes Evol 214 105-114Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Spitzer-Rimon B Farhi M Albo B Cnaani A Ben Zvi MM Masci T Edelbaum O Yu YX Shklarman E Ovadis M Vainstein A (2012) TheR2R3-MYB-like regulatory factor EOBI acting downstream of EOBII regulates scent production by activating ODO1 and structuralscent-related genes in petunia Plant Cell 24 5089-5105
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp Bot 68 4407-4409Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla JF Amaya I Giavalisco P Fernie AR Botella MAValpuesta V (2015) Central role of FaGAMYB in the transition of the strawberry receptacle from development to ripening New Phytol208 482-496
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 regulates fragrance biosynthesis in petunia flowers PlantCell 17 1612-1624
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS (2018) The potassium channel FaTPK1 plays a critical role infruit quality formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) Isolation cloning and expression of a multifunctional O- wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma compounds in strawberry fruitsPlant J 31 755-765
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor types their evolutionary origin and speciesdistribution In A handbook of transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular Biochemistry 52 25-73
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of odor (Buettner A Ed) Springer Cham 9-10Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS (2014) Isolation classification and transcription profiles ofthe AP2ERF transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in regulation of fruit quality Crit Rev Plant Sci 35 120-130
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ Zhang SL Wu J (2017) Map-based cloning of the pear geneMYB114 identifies an interaction with other transcription factors to coordinately regulate fruit anthocyanin biosynthesis Plant J 92437-451
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes involved in regulating fruit ripening Plant Physiol 1531280-1292
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) Expression of ethylene response genes during persimmonfruit astringency removal Planta 235 895-906
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zabetakis I Gramshaw JW Robinson DS (1999) 25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis andbiosynthesis-a review Food Chem 65 139-151
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci Food Agric 74 421-434Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 an AP2ERF gene is a novel regulator of fruit lignificationinduced by chilling injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1325-1334
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation classification and transcription profiles of the Ethylene ResponseFactors (ERFs) in ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML (2012) Genome-wide analysis of the AP2ERF superfamily inpeach (Prunus persica) Genet Mol Res 11 4788-4809
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and expression analysis of a CRTDRE-binding factor gene FaCBF1from Fragaria times ananassa Acta Hortic 41 240-248
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The Arabidopsis AP2ERF transcription factor RAP26 participatesin ABA salt and osmotic stress responses Gene 457 1-12
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Genome-wide analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic (Amsterdam) 123 73-81Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF Valpuesta V Botella MA Granell A Amaya I (2012) Geneticanalysis of strawberry fruit aroma and identification of O-methyltransferase FaOMT as the locus controlling natural variation inmesifurane content Plant Physiol 159 851-870
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Roscher R Bringmann G Schreier P Schwab W (1998) Radiotracer studies on the formation of 25-dimethyl-4-hydroxy-3(2H)-furanonein detached ripening strawberry fruits J Agric Food Chem 46 1488-1493
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Roscher R Herderich M Steffen JP Schreier P Schwab W (1996) 25-dimethyl-4-hydroxy-3[2H]-furanone 6o-malonyl-β-d-glucopyranoside in strawberry fruits Phytochemistry 43 155-159
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (1998) Application of stable isotope ratio analysis explaining the bioformation of 25-dimethyl-4-hydroxy-3(2H)-furanone inplants by a biological maillard reaction J Agric Food Chem 46 2266ndash2269
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W (2013) Natural 4-hydroxy-25-dimethyl-3(2H)-furanone (Furaneolreg) Molecules 18 6936-6951Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwab W Roscher R (1997) 4-Hydroxy-3(2H)-furanones natural and maillard products Recent Res Dev Phytochem 1 643-673Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schwieterman ML Colquhoun TA Jaworski EA Bartoshuk LM Gilbert JL Tieman DM Odabasi AZ Moskowitz HR Folta KM Klee HJSims CA Whitaker VM Clark DG (2014) Strawberry flavor diverse chemical compositions a seasonal influence and effects on sensoryperception PLoS One 9 e88446
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Sharma MK Kumar R Solanke AU Sharma R Tyagi AK Sharma AK (2010) Identification phylogeny and transcript profiling of ERFfamily genes during development and abiotic stress treatments in tomato Mol Genet Genomics 284 455-475
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shen SL Yin XR Zhang B Xie XL Jiang Q Grierson D Chen KS (2016) CitAP210 activation of the terpene synthase CsTPS1 isassociated with the synthesis of (+)-valencene in Newhall orange J Exp Bot 67 4105-4115
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shigyo M Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes Dev Genes Evol 214 105-114Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Song C Hong X Zhao S Liu J Schulenburg K Huang F-C Franz-Oberdorf K Schwab W (2016) Glucosylation of 4-hydroxy-25-dimethyl-3(2H)-furanone the key strawberry flavor compound in strawberry fruit Plant Physiol 171 139-151
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Spitzer-Rimon B Farhi M Albo B Cnaani A Ben Zvi MM Masci T Edelbaum O Yu YX Shklarman E Ovadis M Vainstein A (2012) TheR2R3-MYB-like regulatory factor EOBI acting downstream of EOBII regulates scent production by activating ODO1 and structuralscent-related genes in petunia Plant Cell 24 5089-5105
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tieman D (2017) Transcriptional control of strawberry ripening ndash two to tango J Exp Bot 68 4407-4409Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vallarino JG Osorio S Bombarely A Casantildeal A Cruz-Rus E Saacutenchez-Sevilla JF Amaya I Giavalisco P Fernie AR Botella MAValpuesta V (2015) Central role of FaGAMYB in the transition of the strawberry receptacle from development to ripening New Phytol208 482-496
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Verdonk JC Haring MA van Tunen AJ Schuurink RC (2005) ODORANT1 regulates fragrance biosynthesis in petunia flowers PlantCell 17 1612-1624
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wang SF Song MY Guo JX Huang Y Zhang F Xu C Xiao YH Zhang LS (2018) The potassium channel FaTPK1 plays a critical role infruit quality formation in strawberry (Fragaria times ananassa) Plant Biotechnol J 16 737-748
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wein M Lavid N Lunkenbein S Lewinsohn E Schwab W Kaldenhoff R (2002) Isolation cloning and expression of a multifunctional O- wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aroma compounds in strawberry fruitsPlant J 31 755-765
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Weirauch MT Hughes TR (2011) A catalogue of eukaryotic transcription factor types their evolutionary origin and speciesdistribution In A handbook of transcription factors (Hughes TR Ed) Springer Dordrecht Subcellular Biochemistry 52 25-73
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Wuumlst M (2017) Biosynthesis of plant-derived odorants In Springer handbook of odor (Buettner A Ed) Springer Cham 9-10Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Shen SL Yin XR Xu Q Sun CD Grierson D Ferguson I Chen KS (2014) Isolation classification and transcription profiles ofthe AP2ERF transcription factor superfamily in citrus Mol Biol Rep 41 4261-4271
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Xie XL Yin XR Chen KS (2016) Roles of APETALA2ethylene-response factors in regulation of fruit quality Crit Rev Plant Sci 35 120-130
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yao GF Ming ML Allan AC Gu C Li LT Wu X Wang RZ Chang YJ Qi KJ Zhang SL Wu J (2017) Map-based cloning of the pear geneMYB114 identifies an interaction with other transcription factors to coordinately regulate fruit anthocyanin biosynthesis Plant J 92437-451
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Allan AC Chen KS Ferguson IB (2010) Kiwifruit EIL and ERF genes involved in regulating fruit ripening Plant Physiol 1531280-1292
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) Expression of ethylene response genes during persimmonfruit astringency removal Planta 235 895-906
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
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Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 an AP2ERF gene is a novel regulator of fruit lignificationinduced by chilling injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1325-1334
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Genome-wide analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic (Amsterdam) 123 73-81Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
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Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yin XR Shi YN Min T Luo ZR Yao YC Xu Q Ferguson I Chen KS (2012) Expression of ethylene response genes during persimmonfruit astringency removal Planta 235 895-906
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zabetakis I Gramshaw JW Robinson DS (1999) 25-dimethyl-4-hydroxy-2H-furan-3-one and its derivatives analysis synthesis andbiosynthesis-a review Food Chem 65 139-151
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zabetakis I Holden MA (1997) Strawberry flavour analysis and biosynthesis J Sci Food Agric 74 421-434Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zeng JK Li X Xu Q Chen JY Yin XR Ferguson IB Chen KS (2015) EjAP2-1 an AP2ERF gene is a novel regulator of fruit lignificationinduced by chilling injury via interaction with EjMYB transcription factors Plant Biotechnol J 13 1325-1334
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang AD Hu X Kuang S Ge H Yin XR Chen KS (2016) Isolation classification and transcription profiles of the Ethylene ResponseFactors (ERFs) in ripening kiwifruit Sci Hortic (Amsterdam) 199 209-215
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang CH Shangguan LF Ma RJ Sun X Tao R Guo L Korir NK Yu ML (2012) Genome-wide analysis of the AP2ERF superfamily inpeach (Prunus persica) Genet Mol Res 11 4788-4809
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhang Y Tang HR Luo Y Wang XR Chen Q Liu ZJ (2014) Isolation and expression analysis of a CRTDRE-binding factor gene FaCBF1from Fragaria times ananassa Acta Hortic 41 240-248
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhu Q Zhang JT Gao XS Tong JH Xiao LT Li WB Zhang HX (2010) The Arabidopsis AP2ERF transcription factor RAP26 participatesin ABA salt and osmotic stress responses Gene 457 1-12
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zhuang J Peng RH Cheng ZM (Max) Zhang J Cai B Zhang Z Gao F Zhu B Fu XY Jin XF Chen JM Qiao YS Xiong AS Yao QH (2009) wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Genome-wide analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic (Amsterdam) 123 73-81Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF Valpuesta V Botella MA Granell A Amaya I (2012) Geneticanalysis of strawberry fruit aroma and identification of O-methyltransferase FaOMT as the locus controlling natural variation inmesifurane content Plant Physiol 159 851-870
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved
Genome-wide analysis of the putative AP2ERF family genes in Vitis vinifera Sci Hortic (Amsterdam) 123 73-81Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
Zorrilla-Fontanesi Y Rambla JL Cabeza A Medina JJ Sanchez-Sevilla JF Valpuesta V Botella MA Granell A Amaya I (2012) Geneticanalysis of strawberry fruit aroma and identification of O-methyltransferase FaOMT as the locus controlling natural variation inmesifurane content Plant Physiol 159 851-870
Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title
wwwplantphysiolorgon February 25 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved