The BABY BOOM transcription factor activates the LEC1-ABI3 ...LEC1 and LEC2 116 directly regulate expression of seed maturation- and auxin response and 117 biosynthesis genes (Lotan

1

Short title: BABY BOOM regulates LAFL gene expression

Corresponding author details: Kim Boutilier ([email protected]); 1

Wageningen University and Research, Bioscience; Droevendaalsesteeg 1, 2

6708 PB Wageningen, Netherlands 3

Article title:

The BABY BOOM transcription factor activates the LEC1-ABI3-FUS3-

LEC2 network to induce somatic embryogenesis

Anneke Horstmana,b, Mengfan Lia,b, Iris Heidmannb,c,1, Mieke

Weemena, Baojian Chena,b, Jose M. Muinod, Gerco C. Angenenta,b and

Kim Boutiliera

4

a Wageningen University and Research, Bioscience, Droevendaalsesteeg 1, 5

6708 PB Wageningen, Netherlands; 6

b Wageningen University and Research, Laboratory of Molecular Biology, 7

Droevendaalsesteeg 1, 6708 PB Wageningen, Netherlands; 8

c Enza Zaden Research and Development B.V, Haling 1-E, 1602 DB 9

Enkhuizen, Netherlands; 10

d Max Planck Institute for Molecular Genetics, Ihnestraße 63-73 11

14195 Berlin, Germany 12

1 Current address: Acepo - Analysis & Advice around Cells & Pollen, 13

Seyndersloot 20, 1602 HA Enkhuizen 14

15

Author contributions: A.H., K.B., G.A. designed research; A.H., M.L., I.H., 16

B.C. and M.W. performed research, J.M. analysed data; and A.H. and K.B. 17

wrote the paper with input from the co-authors. 18

19

Plant Physiology Preview. Published on August 22, 2017, as DOI:10.1104/pp.17.00232

Copyright 2017 by the American Society of Plant Biologists

www.plantphysiol.orgon July 2, 2020 - Published by Downloaded from Copyright © 2017 American Society of Plant Biologists. All rights reserved.

http://www.plantphysiol.org

2

Funding information: This work was funded by grants from the Technology 20

Top Institute-Green Genetics and the Netherlands Organisation for Scientific 21

Research (NWO) program, NWO-Groen (project number 870.15.110). 22

23

One sentence summary: 24

25

BBM and other AIL transcription factors induce somatic embryogenesis in a 26

dose- and context-dependent mechanism and through direct transcriptional 27

regulation of major embryo identity genes. 28

29

30

31



3

Abstract 32

Somatic embryogenesis is an example of induced cellular totipotency, where 33

embryos develop from vegetative cells rather than from gamete fusion. 34

Somatic embryogenesis can be induced in vitro by exposing explants to 35

growth regulator and/or stress treatments. The BABY BOOM (BBM) and 36

LEAFY COTYLEDON1 (LEC1) and LEC2 transcription factors are key regulators 37

of plant cell totipotency, as ectopic overexpression of either transcription 38

factor induces somatic embryo formation from arabidopsis (Arabidopsis 39

thaliana) seedlings without exogenous growth regulators or stress 40

treatments. Although LEC and BBM proteins regulate the same 41

developmental process it is not known whether they function in the same 42

molecular pathway. We show that BBM transcriptionally regulates LEC1 and 43

LEC2, as well as the two other ‘LAFL’ genes, FUSCA3 (FUS3) and ABI 44

INSENSITIVE3 (ABI3). LEC2 and ABI3 quantitatively regulate BBM-mediated 45

somatic embryogenesis, while FUS3 and LEC1 are essential for this process. 46

BBM-mediated somatic embryogenesis is dose- and context-dependent, and 47

the context-dependent phenotypes are associated with differential LAFL 48

expression. We also uncover functional redundancy for somatic 49

embryogenesis among other arabidopsis BBM-like proteins, and show that 50

one of these proteins, PLETHORA2, also regulates LAFL gene expression. 51

Our data places BBM upstream of other major regulators of plant embryo 52

identity and totipotency. 53

54



4

Introduction 55

56

Plant cells show a high degree of developmental plasticity and can be 57

induced readily to regenerate new tissues or organs (pluripotency) and even 58

embryos (totipotency) from in vitro-cultured explants. Somatic 59

embryogenesis is a type of plant totipotency in which embryos are induced to 60

form on vegetative explants, usually in response to exogenous hormones, 61

especially auxins, or stress treatments (Feher, 2014). Somatic 62

embryogenesis is extensively used as a clonal propagation tool in 63

biotechnology applications (Lelu-Walter et al., 2013; Sharma et al., 2013; 64

Park and Paek, 2014), and while the tissue culture requirements for somatic 65

embryo induction are well known (Gaj, 2004), only a few of the molecular 66

components that drive this process have been described (Elhiti et al., 2013). 67

A number of plant transcription factors have been identified that can 68

convert somatic cells into embryogenic, totipotent cells. One of these 69

transcription factors, Brassica napus BABY BOOM, encodes an 70

AINTEGUMENTA-LIKE (AIL) APETALA2/ethylene-responsive element–binding 71

factor (AP2/ERF) (Boutilier et al., 2002). In arabidopsis, AIL genes form a 72

small, eight-member clade within the AP2/ERF transcription factor family, 73

which, in addition to BBM, comprises AINTEGUMENTA (ANT), AIL1, 74

PLETHORA1 (PLT1), PLT2, AIL6/PLT3, CHOTTO1 (CHO1)/EMBRYOMAKER 75

(EMK)/AIL5/PLT5 and PLT7. AIL genes are expressed in dividing tissues, 76

including root, shoot and floral meristems, where they act in a redundant 77

manner to maintain a meristematic state (Horstman et al., 2014). Single AIL 78

knock-out mutants show no or only minor defects, but double or triple 79

mutants have stronger phenotypes related to reduced cell proliferation or 80

altered cell identity, including smaller floral organs with partial loss of 81

identity (Krizek, 2009; Krizek, 2015), embryo arrest (Galinha et al., 2007) 82

and impaired root and shoot meristem maintenance (Aida et al., 2004; 83

Galinha et al., 2007; Mudunkothge and Krizek, 2012). BBM is expressed in 84



5

the embryo and root meristem, where it regulates cell identity and growth 85

together with other AIL proteins (Aida et al., 2004; Galinha et al., 2007). In 86

line with their loss-of-function phenotypes, overexpression of arabidopsis AIL 87

transcription factors induces pluripotency, totipotency and/or cell 88

proliferation, with different functions being assigned to specific AIL proteins 89

(Krizek, 1999; Nole-Wilson et al., 2005; Galinha et al., 2007; Tsuwamoto et 90

al., 2010; Krizek and Eaddy, 2012). However, unlike other AIL genes, the 91

genetic pathways in which BBM functions have not been well characterized 92

(Horstman et al., 2014), and it is not known how this single protein controls 93

both pluripotent and totipotent growth. 94

Overexpression of native or heterologous BBM genes also induces 95

regeneration in other species (Morcillo et al., 2007; Deng et al., 2009; El 96

Ouakfaoui et al., 2010; Heidmann et al., 2011; Lutz et al., 2011; Bandupriya 97

et al., 2014; Yang et al., 2014; Florez et al., 2015; Lowe et al., 2016) and is 98

therefore used as a biotechnology tool to improve plant transformation in 99

model and crop species (Deng et al., 2009; Heidmann et al., 2011; Lutz et 100

al., 2011; Florez et al., 2015; Lowe et al., 2016). 101

Other transcription factors also induce somatic embryogenesis when 102

ectopically expressed in seedlings, including LEAFY COTYLEDON1 (LEC1), 103

which encodes subunit B of a nuclear factor Y protein (NF-YB), and the B3 104

domain protein LEC2 (Lotan et al., 1998; Stone et al., 2001). LEC1 and 105

LEC2, together with LEC1-LIKE (LIL), and the B3 domain proteins ABSCISIC 106

ACID (ABA)-INSENSITIVE3 (ABI3) and FUSCA3 (FUS3) are collectively 107

referred to as the LAFL network (for LEC1/L1L, ABI3, FUS3 and LEC2) (Jia et 108

al., 2014). LAFL proteins function throughout embryogenesis, where they 109

redundantly regulate early developmental processes such as embryo identity 110

and later processes such as embryo maturation (storage product 111

accumulation and desiccation tolerance) and dormancy (Jia et al., 2013). 112

Although FUS3 and ABI3 do not induce somatic embryogenesis when 113

overexpressed, they do activate embryo traits in seedlings (Parcy et al., 114



6

1994; Parcy and Giraudat, 1997; Gazzarrini et al., 2004). LEC1 and LEC2 115

directly regulate expression of seed maturation- and auxin response and 116

biosynthesis genes (Lotan et al., 1998; Braybrook et al., 2006), and both of 117

these functions could play a role in inducing a totipotent state (Braybrook 118

and Harada, 2008). Moreover, LEC2 directly activates the MADS-box 119

transcription factor gene AGAMOUS-LIKE15 (AGL15), which enhances 120

somatic embryogenesis from immature zygotic embryos when overexpressed 121

(Harding et al., 2003; Braybrook et al., 2006). LAFL gene expression is 122

controlled by the chromatin remodeller PICKLE (PKL) and by B3 domain-123

containing VIVIPAROUS1/ABI3-LIKE (VAL)/HIGH-LEVEL EXPRESSION OF 124

SUGAR-INDUCIBLE GENE (HSI) transcription factors. Mutations in PKL or VAL 125

genes lead to increased LAFL gene expression in seedlings and maintain 126

embryo identity (Ogas et al., 1999; Dean Rider et al., 2003; Henderson et 127

al., 2004; Suzuki et al., 2007). 128

While both BBM and LEC promote totipotency, it is not known whether 129

they function in the same developmental pathways. To gain insight into 130

signalling pathways regulated by BBM we performed a global analysis of BBM 131

DNA binding sites in somatic embryo tissue (Horstman et al., 2015). Here we 132

show that BBM induces cell totipotency during seed germination through 133

transcriptional activation of the LAFL network, and that BBM induces somatic 134

embryogenesis in a dose- and context-dependent manner. 135



7

Results 136

137

BBM binds and transcriptionally activates LAFL genes 138

To understand BBM regulatory networks during embryogenesis, we 139

identified genes that were bound by BBM in somatic embryo cultures using 140

chromatin immunoprecipitation of BBM-YFP (BBM:BBM-YFP) and BBM-GFP 141

(35S:BBM-GFP) fusion proteins followed by next-generation sequencing 142

(ChIP-seq) (Horstman et al., 2015). BiNGO analysis (Maere et al., 2005) of 143

the top 1000 potential target genes in these ChIP experiments was 144

performed to identify overrepresented gene ontology (GO) categories 145

(Dataset S1, a selection of which is shown in Table S1). Genes involved in 146

auxin biosynthesis, transport and signalling, as well root development, 147

meristem initiation and maintenance were overrepresented in the ChIP-seq 148

data sets, as expected from BBM’s function in the root, and in line with 149

studies on other AIL proteins (Horstman et al., 2014; Santuari et al., 2016). 150

Genes involved in adaxial/abaxial polarity specification and shoot 151

development were also overrepresented among BBM–bound genes (Dataset 152

S1, Table S1). Notably, BBM bound to the promoter regions of genes with 153

known functions in embryo identity and maturation, including the LAFL genes 154

LEC1, LEC2, ABI3 and FUS3 (but not L1L), the MADS box transcription factor 155

gene AGL15, which enhances somatic embryogenesis and functions in a 156

positive feedback network with LEC2 (Harding et al., 2003; Braybrook et al., 157

2006; Zheng et al., 2009), and NF-YA9, which also induces somatic 158

embryogenesis when overexpressed (Mu et al., 2013) (Dataset S1, Table S1, 159

Figure 1A). Here we focus our efforts on characterization of the interaction 160

between BBM and members of the LAFL/AGL15 network. We confirmed BBM 161

binding to the promoters of LEC1, LEC2, ABI3 and AGL15 by independent 162

ChIP-qPCR experiments in somatic embryos (Figure S1A). We did not 163

observe BBM binding to the FUS3 promoter, which is consistent with its lower 164

and atypically-shaped BBM ChIP-seq peak (Figure S1). 165



8

ANT/AIL DNA binding motifs were previously determined in vitro by 166

SELEX and EMSA (Nole-Wilson and Krizek, 2000; Yano et al., 2009; O'Malley 167

et al., 2016; Santuari et al., 2016). MEME analysis (Bailey and Elkan, 1994) 168

of in vivo BBM-bound regions identified and overrepresented sequence motif 169

that resembles the ANT/AIL DNA binding motif (Figure S1B)(Santuari et al., 170

2016). The BBM-bound region in LEC1, LEC2 and FUS3 contains this BBM 171

binding motif, while the ABI3 bound region contains a slightly degenerated 172

version thereof (Figure S1C). The BBM binding motif was not found in the 173

region bound by BBM in the AGL15 gene, which suggests that BBM binds 174

AGL15 using a different motif or via an intermediate protein. 175

We determined whether BBM regulates LAFL/AGL15 gene expression 176

during somatic embryo induction from imbibed seeds using a steroid 177

(dexamethasone, DEX)-regulated 35S::BBM-GR line in combination with 178

qRT-PCR and reporter gene analysis. qRT-PCR analysis in the presence of 179

DEX and the translational inhibitor cycloheximide (CHX) showed that LEC1, 180

LEC2, FUS3 and ABI3 expression, but not AGL15 expression, was 181

upregulated after BBM-GR activation in imbibed seeds (Figure 1B). 182

LAFL/AGL15 genes were not differentially regulated upon BBM-GR activation 183

in the same material that was used for the ChIP (2,4-D-induced embryo 184

cultures; data not shown). An explanation for this lack of transcriptional 185

response could be the use of different promoters to drive BBM in the two 186

experiments. BBM might only bind and activate LAFL/AGL15 genes during 187

the induction/early stages of somatic embryogenesis (pBBM:BBM-YFP used 188

for ChIP is expressed during early embryogenesis; (Horstman et al., 2015)), 189

but not at later stages of somatic embryogenesis (p35S:BBM-GR used for 190

transcription analysis (qRT-PCR) is expressed during late embryogenesis; 191

(Johnson et al., 2005)). 192

Next, a LEC1:LEC1-GFP reporter (Li et al., 2014) was used to chart the 193

dynamics of LEC1 expression during BBM-induced somatic embryogenesis 194

(Figure 1C). 35S:BBM-GR seedlings initially form somatic embryos on the 195



9

cotyledon tip and later from the SAM and cotyledon margins. LEC1-GFP was 196

observed one day after BBM-GR activation, in small patches of cells on the 197

abaxial side of the cotyledon (Figure 1C, +1) and one day later at the 198

cotyledon tip and in patches of cells on the adaxial cotyledon blade (Figure 199

1C, +2). LEC1-GFP became stronger in the cotyledon tip and margin at the 200

time when the tip began to swell (Figure 1C, +3), and could be found later in 201

the somatic embryos that formed at the cotyledon tip and at the margin 202

(Figure 1C, +6). 203

Our results demonstrate that BBM overexpression can ectopically 204

activate LAFL gene expression during seed germination. 205

206

LAFL proteins modulate BBM-induced embryogenesis 207

We investigated the genetic relationship between BBM and its 208

LAFL/AGL15 gene targets. Since outcrossing BBM overexpression lines 209

silences the BBM phenotype (Figure S2), we introduced the 35S:BBM-GR 210

construct into the lec1-2, lec2-1, fus3-3, agl15-3 and abi3 (three alleles) 211

mutant backgrounds by transformation (Figure 2). The lec1-2 and fus3-3 212

seeds are desiccation intolerant (Meinke et al., 1994), therefore 213

heterozygous mutants (lec1-2/+ and fus3-3/+) were used for 214

transformation. 215

In wild-type arabidopsis, 6-7% of the primary (T1) 35S:BBM-GR 216

transformants were embryogenic when grown on DEX (Figure 2). 217

Transformation of the lec1-2/+, lec2-1, fus3-3/+ and agl15-3 mutants with 218

the 35S:BBM-GR construct resulted in a significantly reduced percentage of 219

embryogenic seedlings compared to transformed wild-type seedlings (Figure 220

2). We determined the genotype of the few embryogenic seedlings that were 221

generated after transformation of 35S:BBM-GR to the lec1-2/+ and fus3-3/+ 222

backgrounds. Only one of the embryogenic lec1-2/+ progeny contained the 223

lec1-2 mutant allele, while none of the embryogenic fus3-3/+ progeny 224

contained the fus3-3 mutant allele (Table S2). To determine whether BBM-225



10

GR activation can induce somatic embryogenesis in a homozygous lec1-2 226

background, we rescued immature zygotic embryos from the single 227

embryogenic lec1-2/+ 35S:BBM-GR line to bypass the lec1-2 desiccation 228

intolerance phenotype and cultured them on DEX-containing medium. 229

Embryos were separated phenotypically into lec1-2 homozygous mutant and 230

combined lec1-2 heterozygous/wild-type classes. Somatic embryos formed in 231

lec1-2 heterozygous/wild-type seedlings, but not in the homozygous lec1-2 232

seedlings (Table S2). 233

These results suggest that LEC1, LEC2 and FUS3 are positive 234

regulators of BBM-mediated somatic embryogenesis, and that LEC1 and 235

FUS3 are essential for this process. Surprisingly, we found that AGL15 is also 236

a positive regulator of BBM-induced somatic embryogenesis, even though it 237

is not transcriptionally regulated by BBM at the start of somatic embryo 238

induction; AGL15 might be transcriptionally regulated by BBM at a later time 239

point. 240

In contrast to the results obtained with the fus3, lec and agl15 mutants, 241

transformation of the 35S:BBM-GR construct to three different abi3 mutants 242

enhanced the number of embryogenic seedlings (Figure 2). abi3 is the only 243

LAFL mutant that is insensitive to ABA and overexpression of ABI3 does not 244

induce somatic embryogenesis (Parcy et al., 1994; Parcy and Giraudat, 245

1997). To separate the effects of ABA-insensitivity and other embryo defects 246

of abi3 mutants on the BBM phenotype, we tested another ABA-insensitive 247

mutant, abi5-7, which does not show mutant embryo phenotypes other than 248

ABA-insensitivity (Nambara et al., 2002). As with the abi3 mutants, the abi5-249

7 mutant also enhanced the frequency of the BBM phenotype (Figure 2), 250

suggesting that BBM-mediated totipotency is suppressed by ABA signalling, 251

rather than by other functions of the ABI3/ABI5 proteins. 252

A number of regulatory proteins repress LAFL gene expression during 253

the transition from seed to post-embryonic growth. Seedlings with loss-of-254

function mutations in these proteins ectopically express LAFL genes and 255



11

retain embryo identity (Jia et al., 2014). We determined whether loss-of-256

function mutants for two of these proteins, the CHD3 chromatin remodeller 257

PKL and the B3 domain protein VAL1/HSI2 influence the penetrance of BBM-258

induced embryogenesis (Figure 2). The pkl-1 and val1-2 (hsi2-5) mutants 259

improved the efficiency of BBM-mediated somatic embryogenesis, as 260

measured by a higher percentage of embryogenic primary transformants. 261

Together, the data show that members of the LAFL network, as well their 262

upstream negative regulators are important direct and indirect components 263

of the BBM signalling pathway. 264

265

AIL/PLT proteins promote totipotency and regulate LAFL gene 266

expression 267

BBM is expressed in the embryo and the root meristem where it 268

regulates cell identity and growth along with other AIL proteins (Aida et al., 269

2004; Galinha et al., 2007). PLT1 and PLT2 induce spontaneous root 270

organogenesis (Aida et al., 2004) and have roles in hormone-mediated 271

regeneration (Kareem et al., 2015), while BBM and CHO1/EMK/AIL5/PLT5 272

(Tsuwamoto et al., 2010) are the only genes reported to induce somatic 273

embryogenesis. We generated 35S:AIL overexpression lines for the six AIL 274

genes that have not been reported to induce somatic embryogenesis when 275

overexpressed, namely ANT, AIL1, PLT1, PLT2, PLT3/AIL6 and PLT7, and 276

found that overexpression of all these genes except the phylogenetically-277

distinct ANT and AIL1 (Kim et al., 2006) induced somatic embryogenesis in 278

the primary transformants (Figure S3, A, B). A PLT2-GR fusion protein 279

directly activated LEC1, LEC2 and FUS3 gene expression, but not ABI3 and 280

AGL15 expression (Figure S3C). Together these data suggest extensive 281

overlap in AIL protein function. 282

283

BBM- and PLT2-mediated somatic embryogenesis is dose-dependent 284



12

Ectopic AIL expression induces spontaneous adventitious growth 285

including somatic embryos, ectopic shoots and roots, and callus formation 286

(Boutilier et al., 2002). These phenotypes are correlated with the amount of 287

nuclear-localized BBM protein in DEX-treated 35S:BBM-(GFP)-GR lines 288

(Figure 3 and Figure 4A). A relatively low BBM dose induced the formation of 289

small seedlings with epinastic cotyledons and leaves (Figure 3B and Figure 290

4B) that showed reduced cell differentiation (Figure 4C and Figure 4D). 291

Intermediate DEX concentrations also induced ectopic trichome-bearing 292

protrusions or ectopic leaves on their cotyledon petioles (Figure 3, C-E and 293

Figure 4B), and ectopic roots appeared after longer exposure to DEX (Figure 294

3, F, G). A low frequency of seedlings with somatic embryos on their 295

cotyledons (Figure 3H) was also observed at intermediate DEX 296

concentrations and this phenotype became highly penetrant at the highest 297

effective DEX concentration (Figure 4B). PLT2 also directs the same dose-298

dependent overexpression phenotypes (Figure S4) as BBM overexpression, 299

although ectopic root formation was evident earlier in the PLT2-GR lines than 300

in the BBM-GR lines. These data suggest that AIL protein dose drives the 301

developmental fate of regenerating tissues. 302

303

BBM promotes context-specific embryogenesis 304

Previously we identified direct BBM target genes in four-day-old 305

35S:BBM-GR seedlings using microarray analysis (Passarinho et al., 2008). 306

LAFL/AGL15 genes were not identified as BBM target genes in this study, and 307

in general there was little overlap between these seedling microarray-derived 308

targets and the top 1000 ChIP-seq-derived targets identified in somatic 309

embryos (Table S3). This discrepancy might be explained by the different 310

tissues that were used in each study. We therefore examined the relationship 311

between the developmental competence for BBM-mediated regeneration and 312

LAFL transcription. 313



13

We activated BBM-GR at different time points before and after 314

germination. When 35S:BBM-GR seeds were placed directly in DEX-315

containing medium before or during germination (d0-d2), 100% of the 316

seedlings formed somatic embryos directly on their cotyledons after circa one 317

week (Figure 5A and Figure S5A). By contrast, post-germination DEX 318

treatment (d3-d4) induced callus formation on the adaxial side of the 319

cotyledons of circa 40% of the seedlings from which somatic embryos 320

eventually developed (Figure 5B and Figure S5A). We obtained similar results 321

when we activated PLT2-GR before and after germination (Figure S5, B, C). 322

Thus, AIL proteins induce somatic embryogenesis in two ways depending on 323

the developmental stage of the explant: directly from cotyledons in a narrow 324

window before germination, and indirectly via a callus phase after 325

germination. In agreement with our previous microarray results, neither 326

LEC1, LEC2, FUS3, nor ABI3 were expressed when BBM-GR (or PLT2-GR) 327

was activated in post-germination seedlings, although AGL15 expression was 328

slightly upregulated under these conditions (Figure S5D). LEC1-GFP was only 329

detected in this indirect pathway 10 days after DEX-induction (Figure 5B), 330

where it was localized to globular-like embryos that emerged from the callus. 331

The dessication intolerance combined with the lack of or weak 332

embryogenesis phenotypes of the lec1/fus3 35S:BBM-GR lines (above) 333

complicated further genetic analysis of the role of LEC1 and FUS3 in this 334

indirect pathway. 335

Our results highlight the existence of a narrow developmental window 336

of competence for direct embryogenesis, and suggest that tissues outside 337

this window require more extensive reprogramming, e.g. callus formation, 338

before embryogenesis can be induced. LAFL genes are transcriptionally 339

silenced after germination (Zhang et al., 2012; Zhou et al., 2013), therefore 340

these loci might only become transcriptionally accessible after 341

redifferentiation of cotyledon cells to callus. 342

343



14

Discussion 344

345

BBM-mediated embryogenesis requires LAFL genes 346

An increasing number of proteins are being identified that regulate cell 347

totipotency in vivo and in vitro, including members of the LAFL network and 348

AIL proteins (Feher, 2014; Horstman et al., 2014). LAFL transcription is 349

regulated at the chromatin level and by extensive transcriptional feedback 350

loops between LAFL proteins. The interactions between LAFL proteins and 351

other regulators of cell totipotency are less well known. Our data now places 352

BBM/AIL proteins directly upstream of the LAFL/AGL15 genes. There is some 353

evidence that LAFL proteins might act upstream of AILs: A Phaseolus vulgaris 354

ABI3-like factor (Pv-ALF) binds and activates arabidopsis 355

CHO1/EMK/AIL5/PLT5 (Sundaram et al., 2013), and arabidopsis FUS was 356

shown to bind BBM, PLT2, AIL6/PLT3 and PLT7, although transcriptional 357

regulation was not investigated (Wang and Perry, 2013). In contrast, the 358

lack of AIL deregulation after inducible overexpression of LEC1, ABI3, FUS3 359

or LEC2 (Braybrook and Harada, 2008; Yamamoto et al., 2010; Junker et al., 360

2012; Monke et al., 2012) suggests that there is no direct feedback of LAFLs 361

on AILs. BBM expression is reduced in lafl mutant seeds (Figure S6), but 362

this genetic interaction could be indirect. Although BBM proteins appear to 363

directly activate LAFL genes, the data is inconclusive as to whether there are 364

additional direct transcriptional feedback loops in the AIL-LAFL cell 365

totipotency network. 366

LAFL/AGL15 proteins are required for BBM function, as BBM 367

overexpression in lec1, lec2, fus3 and agl15 mutants either reduced or 368

eliminated the capacity of seedlings to form somatic embryos. The reduced 369

competence for somatic embryogenesis in these mutants could be explained 370

in two ways: (1) the developmental defects in the mutants change the 371

physiological state of the mature embryo/seedling in such a way that it is no 372

longer responsive for BBM; or (2) BBM-induced embryogenesis relies on 373



15

transcriptional activation of the LEC1, LEC2, FUS3 and AGL15 genes. Several 374

lines of evidence support the latter scenario. First, we observed a reduced 375

responsiveness to BBM in segregating lec1 and fus3 populations, which 376

contained wild-type and heterozygous plants. However, the few embryogenic 377

transformants in these populations were mainly wild-types, suggesting that 378

the lec1 and fus3 mutations affect BBM function in the heterozygote state. 379

Heterozygous lec1 and fus3 mutants do not show obvious growth defects, 380

suggesting that reduced LEC1 or FUS3 levels (dose) in the heterozygous 381

mutants, rather than a change in the physiological state of the tissue, 382

reduces the response to BBM overexpression. Secondly, the abi3 mutant 383

shows overlapping maturation defects with the other LAFL mutants (To et al., 384

2006; Roscoe et al., 2015), yet the abi3 mutations had the opposite effect 385

on BBM-induced embryogenesis. Therefore, we hypothesize that the inability 386

of BBM to induce LEC and FUS gene expression reduces the capacity for 387

embryogenic growth in these mutants. This hypothesis is further 388

strengthened by our observations that mutations in LAFL repressors enhance 389

BBM-mediated embryogenesis, possibly by facilitating elevated LAFL gene 390

expression. 391

392

Embryo induction is a dose-dependent phenotype 393

It was previously suggested that the PLT2 protein regulates root 394

meristem size and maintenance through a protein concentration gradient, 395

with high, intermediate and low AIL concentrations instructing stem cell fate, 396

cell division and differentiation, respectively (Galinha et al., 2007). 397

AIL6/PLT3 overexpression also induces dose-dependent phenotypes in floral 398

organs (Krizek and Eaddy, 2012). We showed that a high BBM/PLT2 dose 399

induces embryogenesis, a lower dose induces organogenesis and the lowest 400

dose inhibits differentiation. Our overexpression data therefore support a 401

general dose-dependent AIL output in plant tissues. This dose-dependency 402

complicates functional complementation studies on AILs, as even 403



16

complementation with endogenous promoters (Galinha et al., 2007; Santuari 404

et al., 2016) can lead to differences in expression levels among 405

transformants and a range of developmental outcomes. 406

How dedifferentiation, organogenesis and somatic embryogenesis are 407

induced at successively higher AIL doses is not clear, but likely reflects the 408

endogenous roles of AIL proteins during embryo, organ and meristem 409

development. Mechanistically, AIL dose-dependent phenotypes could result 410

from dose-dependent expression levels of the same set of target genes 411

and/or from dose-specific activation of specific target genes. A transcription 412

factor gradient can regulate different sets of target genes through differences 413

in binding site number and affinity (Rogers and Schier, 2011). Target genes 414

with many or high-affinity binding sites are activated by low levels of the 415

transcription factor, whereas genes with few or low-affinity binding sites are 416

only activated at high transcription factor levels. Specificity might also be 417

determined at the level of protein-protein interactions (Horstman et al., 418

2015). Defining the overlapping and unique target genes for each AIL 419

transcription factor at different doses and the protein complexes in which 420

they function will shed light on how AIL dose directs specific developmental 421

fates. 422

423

424

425



17

MATERIALS AND METHODS 426

427

Plant material and growth conditions 428

The lec2-1 (CS3868), lec1-2 (CS3867), fus3-3 (CS8014), agl15-3 429

(CS16479), and pkl-1 (CS3840) mutants were obtained from the Nottingham 430

Arabidopsis Stock Centre. The val1-2 (hsi2-5)(Sharma et al., 2013), abi3-8, 431

abi3-9, abi3-10 and abi5-7 (Nambara et al., 2002) mutants and the 432

LEC1:LEC1-GFP marker (Li et al., 2014) were described previously. All 433

mutants are in Col-0 background, except lec1-2 and lec2-1, which are in Ws 434

background. 435

Seeds were sterilized with liquid bleach as described previously 436

(Boutilier et al., 2002; Passarinho et al., 2008) and germinated on half-437

strength MS medium containing 1% sucrose and vitamins (½MS-10). 438

Dexamethasone (DEX) and cycloheximide (CHX) (both Sigma) were added to 439

the medium as described in the text. Solid and liquid (rotary shaker, 60 440

rpm/min) cultures were kept at 21 ˚C and 25 ˚C, respectively (16 hour 441

light/8 hour dark regime). lec1-2 35S:BBM-GR mutant embryos were 442

rescued by excising them from sterilized siliques and allowing them to 443

germinate on solid ½MS-10 with DEX and kanamycin (for selection of the 444

BBM transgene). 445

446

Vector construction and transformation 447

The 35S:BBM-GR construct was described previously (Passarinho et al., 448

2008). The ANT, PLT3/AIL6, PLT7 and PLT1 protein coding regions were 449

amplified from Arabidopsis Col-0 genomic DNA and the PLT2 protein coding 450

region from cDNA, using the primers listed in Table S4. 35S:AIL ectopic 451

overexpression constructs were made using the Gateway (GW) binary vector 452

pGD625 (Chalfun et al., 2005). The 35:BBM-GFP-GR construct was made 453

using the GW-compatible destination vector pARC146 (Danisman et al., 454

2012). BBM-GFP used in the 35:BBM-GFP-GR construct was amplified from a 455



18

BBM:BBM-GFP plasmid (Horstman et al., 2015). Constructs were introduced 456

into wild-type or mutant lines by floral dip transformation (Clough and Bent, 457

1998). 458

459

Confocal microscopy 460

Confocal imaging was performed as previously described (Soriano et al., 461

2014). Propidium iodide (PI, 10 µg/mL) counterstaining (35S:BBM-GFP-GR 462

roots) and autofluorescence (LEC1:LEC1-GFP cotyledons) were used to 463

delineate the tissue. Both fluorophores were excited with a 532 nm laser and 464

detected at 600-800 nm. 465

To quantify the subcellular BBM-GFP-GR localisation in root, confocal 466

images were made of the meristematic region of roots of 35S:BBM-GFP-GR 467

seedlings grown for seven days in medium containing different DEX 468

concentrations. ImageJ was used to calculate the ratio of nuclear to 469

cytoplasmic fluorescence by comparing the average fluorescence intensity in 470

the nucleus with the average fluorescence intensity of an area of equal size 471

in the cytoplasm. 472

473

Leaf imaging and quantification of stomatal development 474

The first leaf pairs of nine day-old seedlings were placed overnight in 475

70% ethanol at 4 ˚C, then transferred to 85% ethanol for 6 hours, and 476

subsequently to 3% bleach overnight or until imaging. Leaves were mounted 477

in HCG solution (80 g chloral hydrate, 10 ml glycerol, 30 ml water) prior to 478

imaging with a Nikon Optiphot microscope. The stomatal, meristemoid and 479

stomatal lineage indices (SI, MI and SLI) were calculated as previously 480

described (Peterson et al., 2013). 481

To calculate stomatal indices, eight images from the abaxial sides of 482

cleared first leaves of nine day-old 35:BBM-GR plants grown with or without 483

DEX were analysed (n= 125 and 350 cells per image). The SI, MI and SLI 484

were calculated as previously described (Peterson et al., 2013). SI = 485



19

(number of stomata/(total number of stomata + non-stomatal epidermal 486

cells)) x 100. For the SI, only mature stomata with a pore were counted. MI 487

= (number of meristemoids/(total number of stomata + non-stomatal 488

epidermal cells)) x 100. SLI = (number of stomata and stomata 489

precursors/(total number of stomata + non-stomatal epidermal cells)) x 100. 490

491

ChIP-seq 492

The previously published ChIP-seq data and data analysis (Horstman et 493

al., 2015) can be downloaded from GEO (GSE52400). The ChIP-seq 494

experimental set-up is described in (Horstman et al., 2015); briefly, the 495

experiments were performed using somatic embryos from either 2,4-496

dichlorophenoxyacetic acid (2,4-D)-induced BBM:BBM-YFP cultures (with 497

BBM:NLS-GFP as a control) or a 35S:BBM-GFP overexpression line (with 498

35S:BBM as a control). Two independent ChIP-qPCR experiments on 2,4-D-499

induced BBM:BBM-YFP cultures were performed to validate the ChIP-seq 500

results, using the same protocol as previously described (Horstman et al., 501

2015). A fold change was calculated by comparison to an unbound genomic 502

control region (ARR6) and statistically significant differences between BBM-503

bound regions and a second unbound genomic control region (HSF1) were 504

determined using Student’s t-test (p<0.05). The DNA primers are shown in 505

Table S4. 506

507

Expression analysis 508

cDNA from Col-0 and 35S:BBM-GR seeds or seedlings (3 biological 509

replicates of each) were treated as described in the text and used for 510

quantitative real-time RT-PCR (qPCR). qPCR was performed using the 511

BioMark HD System (Fluidigm). The data were normalized against the SAND 512

gene (Czechowski et al., 2005) and relative gene expression was calculated 513

by comparison with similarly-treated wild-type Col-0 or untreated 35S::BBM-514

GR (Livak and Schmittgen, 2001). The DNA primers are shown in Table S4. 515



20

516

SUPPLEMENTAL MATERIAL 517

518

Table S1. BBM target genes. 519

Table S2. Effect of the lec1 and fus3 mutant backgrounds on BBM-mediated 520

somatic embryogenesis. 521

Table S3. Overlap between BBM targets obtained using microarray and 522

ChIP-seq analysis. 523

Table S4. Oligonucleotide primers used in this study. 524

Figure S1. BBM binds to an ANT-like DNA binding motif. 525

Figure S2. Outcrossing BBM overexpression lines silences the BBM 526

phenotype 527

Figure S3. Ectopic overexpression of AIL proteins induces somatic 528

embryogenesis and activates LAFL expression. 529

Figure S4. PLT2 ectopic overexpression induces dose-dependent 530

phenotypes. 531

Figure S5. AIL proteins induce context-dependent somatic embryogenesis. 532

Figure S6. BBM expression is reduced in lafl mutant seeds. 533

Dataset S1. BBM target genes. 534

535

536

ACKNOWLEDGMENTS 537

We thank Nirmala Sharma for the val1-2 (hsi2-5) mutant and Bas Dekkers 538

for the abi3-8, abi3-9, abi3-10 and abi5-7 mutants. The authors declare no 539

conflict of interest. 540



21

FIGURE LEGENDS 541

542

Figure 1. BBM binds and transcriptionally regulates LAFL genes. 543

(A) ChIP-seq BBM binding profiles for embryo-expressed genes. 35S:BBM-544

GFP (upper profile) and BBM:BBM-YFP (lower profile). X-axis, nucleotide 545

position (TAIR 10 annotation; black bars indicate exons, lines indicate 546

introns); y-axis, ChIP-seq score (fold-enrichment of the BBM-GFP/YFP ChIP 547

to the control ChIP), as calculated by the CSAR package in Bioconductor; 548

>>, direction of gene transcription; *, peaks with scores that are considered 549

statistically significant (FDR<0.05). (B-C) Transcriptional regulation of LAFL 550

genes. Relative expression was determined by qPCR in 35S:BBM-GR and Col-551

0 seeds one day after seed plating. Samples were treated for three hours 552

with DEX and CHX (both at 10 µM) (B). Error bars indicate standard errors 553

of the three biological replicates. Statistically significant differences (*) 554

between DEX+CHX-treated 35S:BBM-GR and DEX+CHX-treated Col-0 were 555

determined using Student’s t-test (p<0.01). (C) LEC1:LEC1-GFP regulation 556

by BBM. Samples were treated with 10 µM DEX one day after plating and 557

imaged on subsequent days as indicated in the panel. The images show the 558

adaxial sides of cotyledons, unless indicated (ab, abaxial side). The green 559

signal in Col-0 and LEC1:LEC1-GFP cotyledon tips is autofluorescence. Scale 560

bars, 250 µm. 561

562

Figure 2. BBM-induced embryogenesis is modulated by LAFL genes. 563

Percentage of primary embryogenic transformants obtained after 564

transformation of the 35S:BBM-GR construct to wild-type Ws or Col-0 565

backgrounds or the indicated mutant lines. Statistically significant differences 566

(*) in the number of embryogenic transgenic lines between the mutant and 567

the corresponding wild-type line were determined using a Pearson’s chi-568

squared test (p<0.05). The total number of transformants per line is 569

indicated above each bar. Somatic embryo formation was not observed in 570



22

any of the individual mutant backgrounds alone, or mutant + 35S:BBM-GR 571

backgrounds in the absence of BBM-GR activation. 572

573

Figure 3. BBM overexpression phenotypes are dose-dependent. 574

Phenotypes of 35S:BBM-GR seedlings grown for two (A-E, H) or three (F, 575

G) weeks on the DEX concentration (µM) indicated in the panel. (A) A 576

phenotypically normal seedling. (B) A small seedling with epinastic leaves 577

and cotyledons. (C) A small, epinastic seedling with a trichome-bearing 578

ectopic leaf (arrow) on the cotyledon petiole. (D) A seedling with ectopic 579

leaves on the petioles of both cotyledons (arrows). (E) A magnified view of 580

the ectopic leaf in (D). (F) A 35S:BBM-GR seedling with an ectopic root (*). 581

(G) A magnified view of the ectopic root in (F). (H) A seedling with somatic 582

embryos on the cotyledon margins (arrowheads). Scale bars, 2.5 mm. 583

584

Figure 4. Quantification of BBM dose-dependent phenotypes. 585

(A) BBM-GFP-GR nuclear localization increases with increasing 586

dexamethasone concentration. The effect of dexamethasone (DEX) on BBM 587

localization in roots of 35S:BBM-GFP-GR seedlings grown for seven days in 588

medium containing the indicated DEX concentration. Non-DEX treated (Col-589

0) roots are shown as a GFP-negative control. Subcellular BBM-GFP-GR 590

localisation was quantified for each DEX concentration by calculating the 591

average nuclear/cytoplasmic GFP ratio (63-133 cells of 5-8 roots per DEX 592

concentration), which is indicated on the bottom of the images (± standard 593

error). The average ratios are significantly different from each other (p<0.01 594

in Student’s t-test). Green, GFP. Magenta, propidium iodide. (B) Frequency 595

of phenotypes observed in 35S:BBM-GR seedlings from two independent 596

transgenic lines (solid and hatched bars) grown for two weeks on medium 597

containing different DEX concentrations (n= 100 to 350 seedlings). Leaf, 598

ectopic leaves; SE, somatic embryos. Seedlings that showed both ectopic 599

shoots and somatic embryos were scored as ‘SE’. SE refers to both 600



23

embryogenic tissue (smooth, swollen, bright green in colour and lacks 601

trichomes) or cotyledons, as well as histodifferentiated embryos. (C) A 602

relatively low BBM dose induces smaller and less-lobed leaf pavement cells 603

compared to the control. The abaxial sides of cleared first leaves of nine-day-604

old 35:BBM-GR seedlings grown on medium without DEX (left) or with 0.1 605

μM DEX (right). Scale bars, 25 μm. (D) Stomatal differentiation in DEX-606

treated 35:BBM-GR seedlings is reduced compared to untreated seedlings. In 607

DEX-treated 35S::BBM-GR seedlings, fewer cells are commited to stomatal 608

development, as reflected by a lower stomatal lineage index (SLI). Also, 609

fewer mature stomata were found in leaves of DEX-treated seedlings 610

(stomatal index, SI), while the number of stomatal meristemoids was 611

increased (meristemoid index, MI). Error bars indicate standard errors. *, 612

statistically significant difference compared to the non-DEX treated control 613

(p<0.05 in Student’s t-test). 614

615

616

Figure 5. BBM-induced embryogenesis is context-dependent. 617

(A) 35S:BBM-GR plants were cultured with 10 µM DEX starting at the dry 618

seed stage (d0) or after germination (d4). The culture time after DEX 619

application is indicated on the bottom right of each picture. Arrowheads, 620

callus; arrows, somatic embryos/embryogenic tissue; ‘le’, callused leaf 621

tissue. The lower-most image is a magnification of the boxed region in the 622

‘d4 +14’ image. (B) LEC1:LEC1-GFP regulation by BBM. Seedlings were 623

treated with 10 µM DEX after germination (d4) and imaged on subsequent 624

days as indicated in the panel. The images show the adaxial sides of 625

cotyledons. Arrowhead, callus on the distal end of the cotyledon blade; 626

arrows, GFP-positive embryo clusters. The outline of the cotyledon margins is 627

shown with dashed lines. Autofluorescence (magenta) was used to delineate 628

the tissue. Scale bars, 250 M. 629

630



24

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Parsed CitationsAida M, Beis D, Heidstra R, Willemsen V, Blilou I, Galinha C, Nussaume L, Noh YS, Amasino R, Scheres B (2004) The PLETHORA genesmediate patterning of the Arabidopsis root stem cell niche. Cell 119: 109-120

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Bailey TL, Elkan C (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. In Proceedings of theSecond International Conference on Intelligent Systems for Molecular Biology. AAAI Press, California, pp 28-36


Bandupriya HDD, Gibbings JG, Dunwell JM (2014) Overexpression of coconut AINTEGUMENTA-like gene, CnANT, promotes in vitroregeneration in transgenic Arabidopsis. Plant Cell Tiss Org 116: 67-79


Boutilier K, Offringa R, Sharma VK, Kieft H, Ouellet T, Zhang L, Hattori J, Liu CM, van Lammeren AA, Miki BL, Custers JB, vanLookeren Campagne MM (2002) Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. PlantCell 14: 1737-1749


Braybrook SA, Harada JJ (2008) LECs go crazy in embryo development. Trends Plant Sci 13: 624-630Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Braybrook SA, Stone SL, Park S, Bui AQ, Le BH, Fischer RL, Goldberg RB, Harada JJ (2006) Genes directly regulated by LEAFYCOTYLEDON2 provide insight into the control of embryo maturation and somatic embryogenesis. Proc Natl Acad Sci U S A 103: 3468-3473


Chalfun A, Franken J, Mes JJ, Marsch-Martinez N, Pereira A, Angenent GC (2005) ASYMMETRIC LEAVES2-LIKE1 gene, a member ofthe AS2/LOB family, controls proximal-distal patterning in Arabidopsis petals. Plant Mol Biol 57: 559-575


Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J16: 735-743


Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR (2005) Genome-wide identification and testing of superior referencegenes for transcript normalization in Arabidopsis. Plant Physiol 139: 5-17


Danisman S, van der Wal F, Dhondt S, Waites R, de Folter S, Bimbo A, van Dijk AJ, Muino JM, Cutri L, Dornelas MC, Angenent GC,Immink RGH (2012) Arabidopsis Class I and Class II TCP Transcription Factors Regulate Jasmonic Acid Metabolism and LeafDevelopment Antagonistically. Plant Physiol 159: 1511-1523


Dean Rider S, Jr., Henderson JT, Jerome RE, Edenberg HJ, Romero-Severson J, Ogas J (2003) Coordinate repression of regulators ofembryonic identity by PICKLE during germination in Arabidopsis. Plant J 35: 33-43


Deng W, Luo KM, Li ZG, Yang YW (2009) A novel method for induction of plant regeneration via somatic embryogenesis. Plant Science177: 43-48

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http://www.ncbi.nlm.nih.gov/pubmed?term=Aida M%2C Beis D%2C Heidstra R%2C Willemsen V%2C Blilou I%2C Galinha C%2C Nussaume L%2C Noh YS%2C Amasino R%2C Scheres B %282004%29 The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche%2E Cell 119%3A 109%2D120&dopt=abstract

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http://search.crossref.org/?page=1&rows=2&q=Bandupriya HDD, Gibbings JG, Dunwell JM (2014) Overexpression of coconut AINTEGUMENTA-like gene, CnANT, promotes in vitro regeneration in transgenic Arabidopsis. Plant Cell Tiss Org 116: 67-79

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http://search.crossref.org/?page=1&rows=2&q=Braybrook SA, Harada JJ (2008) LECs go crazy in embryo development. Trends Plant Sci 13: 624-630

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Morcillo F, Gallard A, Pillot M, Jouannic S, Aberlenc-Bertossi F, Collin M, Verdeil JL, Tregear JW (2007) EgAP2-1, an AINTEGUMENTA-like (AIL) gene expressed in meristematic and proliferating tissues of embryos in oil palm. Planta 226: 1353-1362


Mu J, Tan H, Hong S, Liang Y, Zuo J (2013) Arabidopsis transcription factor genes NF-YA1, 5, 6, and 9 play redundant roles in malegametogenesis, embryogenesis, and seed development. Mol Plant 6: 188-201


Mudunkothge JS, Krizek BA (2012) Three Arabidopsis AIL/PLT genes act in combination to regulate shoot apical meristem function.Plant J 71: 108-121


Nambara E, Suzuki M, Abrams S, McCarty DR, Kamiya Y, McCourt P (2002) A screen for genes that function in abscisic acid signaling inArabidopsis thaliana. Genetics 161: 1247-1255


Nole-Wilson S, Krizek BA (2000) DNA binding properties of the Arabidopsis floral development protein AINTEGUMENTA. Nucleic AcidsRes 28: 4076-4082


Nole-Wilson S, Tranby TL, Krizek BA (2005) AINTEGUMENTA-like (AIL) genes are expressed in young tissues and may specifymeristematic or division-competent states. Plant Mol Biol 57: 613-628


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http://www.ncbi.nlm.nih.gov/pubmed?term=Lowe K%2C Wu E%2C Wang N%2C Hoerster G%2C Hastings C%2C Cho MJ%2C Scelonge C%2C Lenderts B%2C Chamberlin M%2C Cushatt J%2C Wang L%2C Ryan L%2C Khan T%2C Chow%2DYiu J%2C Hua W%2C Yu M%2C Banh J%2C Bao Z%2C Brink K%2C Igo E%2C Rudrappa B%2C Shamseer PM%2C Bruce W%2C Newman L%2C Shen B%2C Zheng P%2C Bidney D%2C Falco SC%2C Register IJ%2C Zhao ZY%2C Xu D%2C Jones TJ%2C Gordon%2DKamm WJ %282016%29 Morphogenic Regulators Baby boom and Wuschel Improve Monocot Transformation%2E Plant Cell&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Lutz KA%2C Azhagiri A%2C Maliga P %282011%29 Transplastomics in Arabidopsis%3A progress toward developing an efficient method%2E Methods Mol Biol 774%3A 133%2D147&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Maere S%2C Heymans K%2C Kuiper M %282005%29 BiNGO%3A a Cytoscape plugin to assess overrepresentation of Gene Ontology categories in biological networks%2E Bioinformatics 21%3A 3448%2D3449&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Meinke DW%2C Franzmann LH%2C Nickle TC%2C Yeung EC %281994%29 Leafy Cotyledon Mutants of Arabidopsis%2E Plant Cell 6%3A 1049%2D1064&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Monke G%2C Seifert M%2C Keilwagen J%2C Mohr M%2C Grosse I%2C Hahnel U%2C Junker A%2C Weisshaar B%2C Conrad U%2C Baumlein H%2C Altschmied L %282012%29 Toward the identification and regulation of the Arabidopsis thaliana ABI3 regulon%2E Nucleic Acids Res 40%3A 8240%2D8254&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Monke G, Seifert M, Keilwagen J, Mohr M, Grosse I, Hahnel U, Junker A, Weisshaar B, Conrad U, Baumlein H, Altschmied L (2012) Toward the identification and regulation of the Arabidopsis thaliana ABI3 regulon. Nucleic Acids Res 40: 8240-8254

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http://www.ncbi.nlm.nih.gov/pubmed?term=Morcillo F%2C Gallard A%2C Pillot M%2C Jouannic S%2C Aberlenc%2DBertossi F%2C Collin M%2C Verdeil JL%2C Tregear JW %282007%29 EgAP2%2D1%2C an AINTEGUMENTA%2Dlike %28AIL%29 gene expressed in meristematic and proliferating tissues of embryos in oil palm%2E Planta 226%3A 1353%2D1362&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Mu J%2C Tan H%2C Hong S%2C Liang Y%2C Zuo J %282013%29 Arabidopsis transcription factor genes NF%2DYA1%2C 5%2C 6%2C and 9 play redundant roles in male gametogenesis%2C embryogenesis%2C and seed development%2E Mol Plant 6%3A 188%2D201&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Nambara E%2C Suzuki M%2C Abrams S%2C McCarty DR%2C Kamiya Y%2C McCourt P %282002%29 A screen for genes that function in abscisic acid signaling in Arabidopsis thaliana%2E Genetics 161%3A 1247%2D1255&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Nole%2DWilson S%2C Tranby TL%2C Krizek BA %282005%29 AINTEGUMENTA%2Dlike %28AIL%29 genes are expressed in young tissues and may specify meristematic or division%2Dcompetent states%2E Plant Mol Biol 57%3A 613%2D628&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Nole-Wilson S, Tranby TL, Krizek BA (2005) AINTEGUMENTA-like (AIL) genes are expressed in young tissues and may specify meristematic or division-competent states. Plant Mol Biol 57: 613-628

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http://scholar.google.com/scholar?as_q=AINTEGUMENTA-like (AIL) genes are expressed in young tissues and may specify meristematic or division-competent states&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Nole-Wilson&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=O%27Malley RC%2C Huang SC%2C Song L%2C Lewsey MG%2C Bartlett A%2C Nery JR%2C Galli M%2C Gallavotti A%2C Ecker JR %282016%29 Cistrome and Epicistrome Features Shape the Regulatory DNA Landscape%2E Cell 166%3A 1598&dopt=abstract


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Ogas J, Kaufmann S, Henderson J, Somerville C (1999) PICKLE is a CHD3 chromatin-remodeling factor that regulates the transitionfrom embryonic to vegetative development in Arabidopsis. Proc Natl Acad Sci U S A 96: 13839-13844


Parcy F, Giraudat J (1997) Interactions between the ABI1 and the ectopically expressed ABI3 genes in controlling abscisic acidresponses in Arabidopsis vegetative tissues. Plant J 11: 693-702


Parcy F, Valon C, Raynal M, Gaubier-Comella P, Delseny M, Giraudat J (1994) Regulation of gene expression programs duringArabidopsis seed development: roles of the ABI3 locus and of endogenous abscisic acid. Plant Cell 6: 1567-1582


Park SY, Paek KY (2014) Bioreactor culture of shoots and somatic embryos of medicinal plants for production of bioactive compounds.In Production of Biomass and Bioactive Compounds Using Bioreactor Technology, pp 337-368


Passarinho P, Ketelaar T, Xing M, van Arkel J, Maliepaard C, Hendriks MW, Joosen R, Lammers M, Herdies L, den Boer B, van derGeest L, Boutilier K (2008) BABY BOOM target genes provide diverse entry points into cell proliferation and cell growth pathways.Plant Mol Biol 68: 225-237


Peterson KM, Shyu C, Burr CA, Horst RJ, Kanaoka MM, Omae M, Sato Y, Torii KU (2013) Arabidopsis homeodomain-leucine zipper IVproteins promote stomatal development and ectopically induce stomata beyond the epidermis. Development 140: 1924-1935


Rogers KW, Schier AF (2011) Morphogen gradients: from generation to interpretation. Annu Rev Cell Dev Biol 27: 377-407Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Roscoe TT, Guilleminot J, Bessoule JJ, Berger F, Devic M (2015) Complementation of Seed Maturation Phenotypes by EctopicExpression of ABSCISIC ACID INSENSITIVE3, FUSCA3 and LEAFY COTYLEDON2 in Arabidopsis. Plant Cell Physiol 56: 1215-1228


Santuari L, Sanchez-Perez GF, Luijten M, Rutjens B, Terpstra I, Berke L, Gorte M, Prasad K, Bao D, Timmermans-Hereijgers JL, MaeoK, Nakamura K, Shimotohno A, Pencik A, Novak O, Ljung K, van Heesch S, de Bruijn E, Cuppen E, Willemsen V, Mahonen AP, LukowitzW, Snel B, de Ridder D, Scheres B, Heidstra R (2016) The PLETHORA Gene Regulatory Network Guides Growth and CellDifferentiation in Arabidopsis Roots. Plant Cell 28: 2937-2951


Sharma N, Bender Y, Boyle K, Fobert PR (2013) High-level expression of sugar inducible gene2 (HSI2) is a negative regulator ofdrought stress tolerance in Arabidopsis. BMC Plant Biol 13: 170


Sharma S, Shahzad A, Teixeira da Silva JA (2013) Synseed technology-A complete synthesis. Biotechnology Advances 31: 186-207Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Soriano M, Li H, Jacquard C, Angenent GC, Krochko J, Offringa R, Boutilier K (2014) Plasticity in Cell Division Patterns and AuxinTransport Dependency during in Vitro Embryogenesis in Brassica napus. Plant Cell 26: 2568-2581



http://search.crossref.org/?page=1&rows=2&q=O'Malley RC, Huang SC, Song L, Lewsey MG, Bartlett A, Nery JR, Galli M, Gallavotti A, Ecker JR (2016) Cistrome and Epicistrome Features Shape the Regulatory DNA Landscape. Cell 166: 1598

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=O'Malley&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Cistrome and Epicistrome Features Shape the Regulatory DNA Landscape.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=Ogas J%2C Kaufmann S%2C Henderson J%2C Somerville C %281999%29 PICKLE is a CHD3 chromatin%2Dremodeling factor that regulates the transition from embryonic to vegetative development in Arabidopsis%2E Proc Natl Acad Sci U S A 96%3A 13839%2D13844&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Ogas J, Kaufmann S, Henderson J, Somerville C (1999) PICKLE is a CHD3 chromatin-remodeling factor that regulates the transition from embryonic to vegetative development in Arabidopsis. Proc Natl Acad Sci U S A 96: 13839-13844

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Ogas&hl=en&c2coff=1

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http://scholar.google.com/scholar?as_q=PICKLE is a CHD3 chromatin-remodeling factor that regulates the transition from embryonic to vegetative development in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ogas&as_ylo=1999&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Parcy F%2C Giraudat J %281997%29 Interactions between the ABI1 and the ectopically expressed ABI3 genes in controlling abscisic acid responses in Arabidopsis vegetative tissues%2E Plant J 11%3A 693%2D702&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Parcy F, Giraudat J (1997) Interactions between the ABI1 and the ectopically expressed ABI3 genes in controlling abscisic acid responses in Arabidopsis vegetative tissues. Plant J 11: 693-702

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Parcy&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Interactions between the ABI1 and the ectopically expressed ABI3 genes in controlling abscisic acid responses in Arabidopsis vegetative tissues&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Interactions between the ABI1 and the ectopically expressed ABI3 genes in controlling abscisic acid responses in Arabidopsis vegetative tissues&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Parcy&as_ylo=1997&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Parcy F%2C Valon C%2C Raynal M%2C Gaubier%2DComella P%2C Delseny M%2C Giraudat J %281994%29 Regulation of gene expression programs during Arabidopsis seed development%3A roles of the ABI3 locus and of endogenous abscisic acid%2E Plant Cell 6%3A 1567%2D1582&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Parcy F, Valon C, Raynal M, Gaubier-Comella P, Delseny M, Giraudat J (1994) Regulation of gene expression programs during Arabidopsis seed development: roles of the ABI3 locus and of endogenous abscisic acid. Plant Cell 6: 1567-1582

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Parcy&hl=en&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=Park SY%2C Paek KY %282014%29 Bioreactor culture of shoots and somatic embryos of medicinal plants for production of bioactive compounds%2E In Production of Biomass and Bioactive Compounds Using Bioreactor Technology%2C pp 337%2D368&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Park SY, Paek KY (2014) Bioreactor culture of shoots and somatic embryos of medicinal plants for production of bioactive compounds. In Production of Biomass and Bioactive Compounds Using Bioreactor Technology, pp 337-368

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http://www.ncbi.nlm.nih.gov/pubmed?term=Passarinho P%2C Ketelaar T%2C Xing M%2C van Arkel J%2C Maliepaard C%2C Hendriks MW%2C Joosen R%2C Lammers M%2C Herdies L%2C den Boer B%2C van der Geest L%2C Boutilier K %282008%29 BABY BOOM target genes provide diverse entry points into cell proliferation and cell growth pathways%2E Plant Mol Biol 68%3A 225%2D237&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Passarinho P, Ketelaar T, Xing M, van Arkel J, Maliepaard C, Hendriks MW, Joosen R, Lammers M, Herdies L, den Boer B, van der Geest L, Boutilier K (2008) BABY BOOM target genes provide diverse entry points into cell proliferation and cell growth pathways. Plant Mol Biol 68: 225-237

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http://www.ncbi.nlm.nih.gov/pubmed?term=Peterson KM%2C Shyu C%2C Burr CA%2C Horst RJ%2C Kanaoka MM%2C Omae M%2C Sato Y%2C Torii KU %282013%29 Arabidopsis homeodomain%2Dleucine zipper IV proteins promote stomatal development and ectopically induce stomata beyond the epidermis%2E Development 140%3A 1924%2D1935&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Peterson KM, Shyu C, Burr CA, Horst RJ, Kanaoka MM, Omae M, Sato Y, Torii KU (2013) Arabidopsis homeodomain-leucine zipper IV proteins promote stomatal development and ectopically induce stomata beyond the epidermis. Development 140: 1924-1935

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http://www.ncbi.nlm.nih.gov/pubmed?term=Rogers KW%2C Schier AF %282011%29 Morphogen gradients%3A from generation to interpretation%2E Annu Rev Cell Dev Biol 27%3A 377%2D407&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Roscoe TT%2C Guilleminot J%2C Bessoule JJ%2C Berger F%2C Devic M %282015%29 Complementation of Seed Maturation Phenotypes by Ectopic Expression of ABSCISIC ACID INSENSITIVE3%2C FUSCA3 and LEAFY COTYLEDON2 in Arabidopsis%2E Plant Cell Physiol 56%3A 1215%2D1228&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Santuari L%2C Sanchez%2DPerez GF%2C Luijten M%2C Rutjens B%2C Terpstra I%2C Berke L%2C Gorte M%2C Prasad K%2C Bao D%2C Timmermans%2DHereijgers JL%2C Maeo K%2C Nakamura K%2C Shimotohno A%2C Pencik A%2C Novak O%2C Ljung K%2C van Heesch S%2C de Bruijn E%2C Cuppen E%2C Willemsen V%2C Mahonen AP%2C Lukowitz W%2C Snel B%2C de Ridder D%2C Scheres B%2C Heidstra R %282016%29 The PLETHORA Gene Regulatory Network Guides Growth and Cell Differentiation in Arabidopsis Roots%2E Plant Cell 28%3A 2937%2D2951&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Sharma N%2C Bender Y%2C Boyle K%2C Fobert PR %282013%29 High%2Dlevel expression of sugar inducible gene2 %28HSI2%29 is a negative regulator of drought stress tolerance in Arabidopsis%2E BMC Plant Biol 13%3A 170&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Sharma S%2C Shahzad A%2C Teixeira da Silva JA %282013%29 Synseed technology%2DA complete synthesis%2E Biotechnology Advances 31%3A 186%2D207&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Soriano M%2C Li H%2C Jacquard C%2C Angenent GC%2C Krochko J%2C Offringa R%2C Boutilier K %282014%29 Plasticity in Cell Division Patterns and Auxin Transport Dependency during in Vitro Embryogenesis in Brassica napus%2E Plant Cell 26%3A 2568%2D2581&dopt=abstract

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Zhang H, Bishop B, Ringenberg W, Muir WM, Ogas J (2012) The CHD3 remodeler PICKLE associates with genes enriched fortrimethylation of histone H3 lysine 27. Plant Physiol 159: 418-432


Zheng Y, Ren N, Wang H, Stromberg AJ, Perry SE (2009) Global identification of targets of the Arabidopsis MADS domain proteinAGAMOUS-Like15. Plant Cell 21: 2563-2577


Zhou Y, Tan B, Luo M, Li Y, Liu C, Chen C, Yu CW, Yang S, Dong S, Ruan J, Yuan L, Zhang Z, Zhao L, Li C, Chen H, Cui Y, Wu K, HuangS (2013) HISTONE DEACETYLASE19 interacts with HSL1 and participates in the repression of seed maturation genes in Arabidopsisseedlings. Plant Cell 25: 134-148



http://www.ncbi.nlm.nih.gov/pubmed?term=Stone SL%2C Kwong LW%2C Yee KM%2C Pelletier J%2C Lepiniec L%2C Fischer RL%2C Goldberg RB%2C Harada JJ %282001%29 LEAFY COTYLEDON2 encodes a B3 domain transcription factor that induces embryo development%2E Proc Natl Acad Sci U S A 98%3A 11806%2D11811&dopt=abstract

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http://scholar.google.com/scholar?as_q=LEAFY COTYLEDON2 encodes a B3 domain transcription factor that induces embryo development&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Stone&as_ylo=2001&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Sundaram S%2C Kertbundit S%2C Shakirov EV%2C Iyer LM%2C Juricek M%2C Hall TC %282013%29 Gene networks and chromatin and transcriptional regulation of the phaseolin promoter in Arabidopsis%2E Plant Cell 25%3A 2601%2D2617&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Suzuki M%2C Wang HH%2C McCarty DR %282007%29 Repression of the LEAFY COTYLEDON 1%2FB3 regulatory network in plant embryo development by VP1%2FABSCISIC ACID INSENSITIVE 3%2DLIKE B3 genes%2E Plant Physiol 143%3A 902%2D911&dopt=abstract

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http://scholar.google.com/scholar?as_q=Repression of the LEAFY COTYLEDON 1/B3 regulatory network in plant embryo development by VP1/ABSCISIC ACID INSENSITIVE 3-LIKE B3 genes&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Suzuki&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=To A%2C Valon C%2C Savino G%2C Guilleminot J%2C Devic M%2C Giraudat J%2C Parcy F %282006%29 A network of local and redundant gene regulation governs Arabidopsis seed maturation%2E Plant Cell 18%3A 1642%2D1651&dopt=abstract

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http://scholar.google.com/scholar?as_q=A network of local and redundant gene regulation governs Arabidopsis seed maturation&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=To&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Tsuwamoto R%2C Yokoi S%2C Takahata Y %282010%29 Arabidopsis EMBRYOMAKER encoding an AP2 domain transcription factor plays a key role in developmental change from vegetative to embryonic phase%2E Plant Mol Biol 73%3A 481%2D492&dopt=abstract

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http://scholar.google.com/scholar?as_q=Arabidopsis EMBRYOMAKER encoding an AP2 domain transcription factor plays a key role in developmental change from vegetative to embryonic phase&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Tsuwamoto&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Wang F%2C Perry SE %282013%29 Identification of direct targets of FUSCA3%2C a key regulator of Arabidopsis seed development%2E Plant Physiol 161%3A 1251%2D1264&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Yamamoto A%2C Kagaya Y%2C Usui H%2C Hobo T%2C Takeda S%2C Hattori T %282010%29 Diverse roles and mechanisms of gene regulation by the Arabidopsis seed maturation master regulator FUS3 revealed by microarray analysis%2E Plant Cell Physiol 51%3A 2031%2D2046&dopt=abstract

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http://scholar.google.com/scholar?as_q=Diverse roles and mechanisms of gene regulation by the Arabidopsis seed maturation master regulator FUS3 revealed by microarray analysis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yamamoto&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Yang HF%2C Kou YP%2C Gao B%2C Soliman TMA%2C Xu KD%2C Ma N%2C Cao X%2C Zhao LJ %282014%29 Identification and functional analysis of BABY BOOM genes from Rosa canina%2E Biol Plantarum 58%3A 427%2D435&dopt=abstract

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http://scholar.google.com/scholar?as_q=Identification and functional analysis of BABY BOOM genes from Rosa canina&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yang&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Yano R%2C Kanno Y%2C Jikumaru Y%2C Nakabayashi K%2C Kamiya Y%2C Nambara E %282009%29 CHOTTO1%2C a putative double APETALA2 repeat transcription factor%2C is involved in abscisic acid%2Dmediated repression of gibberellin biosynthesis during seed germination in Arabidopsis%2E Plant Physiol 151%3A 641%2D654&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Zhang H%2C Bishop B%2C Ringenberg W%2C Muir WM%2C Ogas J %282012%29 The CHD3 remodeler PICKLE associates with genes enriched for trimethylation of histone H3 lysine 27%2E Plant Physiol 159%3A 418%2D432&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhang H, Bishop B, Ringenberg W, Muir WM, Ogas J (2012) The CHD3 remodeler PICKLE associates with genes enriched for trimethylation of histone H3 lysine 27. Plant Physiol 159: 418-432

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Zhang&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The CHD3 remodeler PICKLE associates with genes enriched for trimethylation of histone H3 lysine 27&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The CHD3 remodeler PICKLE associates with genes enriched for trimethylation of histone H3 lysine 27&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zheng Y%2C Ren N%2C Wang H%2C Stromberg AJ%2C Perry SE %282009%29 Global identification of targets of the Arabidopsis MADS domain protein AGAMOUS%2DLike15%2E Plant Cell 21%3A 2563%2D2577&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zheng Y, Ren N, Wang H, Stromberg AJ, Perry SE (2009) Global identification of targets of the Arabidopsis MADS domain protein AGAMOUS-Like15. Plant Cell 21: 2563-2577

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Zheng&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Global identification of targets of the Arabidopsis MADS domain protein AGAMOUS-Like15&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Global identification of targets of the Arabidopsis MADS domain protein AGAMOUS-Like15&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zheng&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhou Y%2C Tan B%2C Luo M%2C Li Y%2C Liu C%2C Chen C%2C Yu CW%2C Yang S%2C Dong S%2C Ruan J%2C Yuan L%2C Zhang Z%2C Zhao L%2C Li C%2C Chen H%2C Cui Y%2C Wu K%2C Huang S %282013%29 HISTONE DEACETYLASE19 interacts with HSL1 and participates in the repression of seed maturation genes in Arabidopsis seedlings%2E Plant Cell 25%3A 134%2D148&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhou Y, Tan B, Luo M, Li Y, Liu C, Chen C, Yu CW, Yang S, Dong S, Ruan J, Yuan L, Zhang Z, Zhao L, Li C, Chen H, Cui Y, Wu K, Huang S (2013) HISTONE DEACETYLASE19 interacts with HSL1 and participates in the repression of seed maturation genes in Arabidopsis seedlings. Plant Cell 25: 134-148

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Zhou&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=HISTONE DEACETYLASE19 interacts with HSL1 and participates in the repression of seed maturation genes in Arabidopsis seedlings&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=HISTONE DEACETYLASE19 interacts with HSL1 and participates in the repression of seed maturation genes in Arabidopsis seedlings&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhou&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1


Documents

The BABY BOOM transcription factor activates the LEC1-ABI3 ...LEC1 and LEC2 116 directly regulate expression of seed maturation- and auxin response and 117 biosynthesis genes (Lotan