PROHIBITIN 3 forms complexes with ISOCHORISMATE …110 ISOCHORISMATE SYNTHASE 1 (ICS1), a plastid-localized enzyme (Strawn et al., 111 2007). The second step is the conversion of IC

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Short title: PROHIBITIN 3 controls stress-induced SA synthesis 1

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TITLE 8

PROHIBITIN 3 forms complexes with ISOCHORISMATE SYNTHASE 9

1 to regulate stress-induced salicylic acid biosynthesis in Arabidopsis 10

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Authors: 15

Aldo Seguel1, Joanna Jelenska2, Ariel Herrera-Vásquez1, Sharon K. Marr3, Michael B. 16

Joyce2, Kelsey R. Gagesch2, Nadia Shakoor2, Shang-Chuan Jiang2, Alejandro 17

Fonseca1, Mary C. Wildermuth3, Jean T. Greenberg2,* and Loreto Holuigue1,*. 18

1Departamento de Genética Molecular y Microbiología, Facultad de Ciencias Biológicas, 19

Pontificia Universidad Católica de Chile. 20

2Department of Molecular Genetics and Cell Biology, The University of Chicago. 21

3Department of Plant and Microbial Pathology, University of California, Berkeley. 22

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* Corresponding authors 24

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26 27

One sentence summary: A PROHIBITIN-family protein promotes salicylic acid 28

production via the isochorismate pathway in response to stress. 29

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FOOTNOTES 31

Plant Physiology Preview. Published on February 1, 2018, as DOI:10.1104/pp.17.00941

Copyright 2018 by the American Society of Plant Biologists

www.plantphysiol.orgon August 23, 2020 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

http://www.plantphysiol.org

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List of author contributions: 33

J.J., J.T.G., A.S., and LH designed the research; J.J., J.T.G. and L.H. supervised the 34

experiments; A.S., J.J, A.H.-V., A.F., M.B.J., K.R.G., N.S. and S.C.J. performed the 35

experiments; A.S. and J.J. analyzed the data; S.K.M. and M.C.W. generated and tested the 36

anti-ICS1 antibody; AS, LH and JTG wrote article with contributions from other authors. 37

38

Funding Information: 39

This work was supported by: the National Commission for Science and Technology 40

CONICYT (FONDECYT grant N° 1141202 to L.H.), the Millennium Science Initiative 41

(Nucleus for Plant Synthetic and Systems Biology, grant NC130030 to Rodrigo Gutiérrez 42

and L.H.), the National Institute of Health (R01 GM54292 to J.T.G), the National Science 43

Foundation (NSF IOS- 1456904 to J.T.G., NSF2010 0822393 to J.T.G. and Richard W. 44

Michelmore, and NSF IOS-1449100 to M.C.W.). A.S. was supported by a PhD fellowship 45

from CONICYT, K.R.G was supported by NSF training grant 1062713 and N.S. by MCB 46

training grant T32 GM 007183. 47

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Corresponding authors emails: 52

[email protected] 53

[email protected] 54

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mailto:[email protected]

mailto:[email protected]


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ABSTRACT 56

Salicylic acid (SA) is a major defense signal in plants. In Arabidopsis (Arabidopsis 57

thaliana), the chloroplast-localized isochorismate pathway is the main source of SA 58

biosynthesis during abiotic stress or pathogen infections. In the first step of the pathway, 59

the enzyme ISOCHORISMATE SYNTHASE 1 (ICS1) converts chorismate to 60

isochorismate. An unknown enzyme subsequently converts isochorismate to SA. Here, we 61

show that ICS1 protein levels increase during UV-C stress. To identify proteins that may 62

play roles in SA production by regulating ICS1, we analyzed proteins that co-63

immunoprecipitated with ICS1 via mass spectrometry. The ICS1 complexes contained a 64

large number of peptides from the PROHIBITIN (PHB) protein family, with PHB3 the 65

most abundant. PHB proteins have diverse biological functions that include acting as 66

scaffolds for protein complex formation and stabilization. PHB3 was previously reported to 67

localize to mitochondria. Using fractionation, protease protection, and live imaging, we 68

show that PHB3 also localizes to chloroplasts, where ICS1 resides. Notably, loss of PHB3 69

function led to decreased ICS1 protein levels in response to UV-C stress. However, ICS1 70

transcript levels remain unchanged, indicating that ICS1 is regulated post-transcriptionally. 71

The phb3 mutant displayed reduced levels of SA, the SA-regulated protein PR1, and 72

hypersensitive cell death in response to UV-C and avirulent strains of Pseudomonas 73

syringae, and correspondingly supported increased growth of P. syringae. Expression of a 74

PHB3 transgene in the phb3 mutant complemented all of these phenotypes. We suggest a 75

model in which the formation of PHB3-ICS1 complexes stabilizes ICS1 to promote SA 76

production in response to stress. 77

78



4

INTRODUCTION 79

The plant hormone salicylic acid (SA) plays diverse roles in development and stress 80

defense responses (Vlot et al., 2009; Dempsey et al., 2011). Its developmental roles include 81

the regulation of flowering time (Martínez et al., 2004), leaf longevity (slow cell death; 82

Morris et al., 2000; Zhang et al., 2013), and biomass (Abreu et al., 2009) in Arabidopsis 83

(Arabidopsis thaliana) as well as thermogenesis in Arum lily inflorescences (Raskin et al., 84

1987). Endogenous SA promotes seed germination under high salinity conditions (Lee et 85

al., 2010), basal thermotolerance (Clarke et al., 2004; Clarke et al., 2009), and growth and 86

development in the presence of the heavy metal cadmium (Guo et al., 2016). During biotic 87

interactions with certain pathogens, SA is needed for the activation of plant defense 88

responses that suppress pathogen growth (Vlot et al., 2009). Such responses can include the 89

transcriptional upregulation of a large number of pathogenesis-related (PR) genes (Uknes et 90

al., 1992; Cao et al., 1997), rapid programmed cell death (the hypersensitive response, Coll 91

et al., 2011; Doorn et al., 2011), defense priming (Beckers et al., 2009; Tateda et al., 2014; 92

Zhang et al., 2014), and systemic immunity to new infections (Fu and Dong, 2013). 93

A major mechanism of SA deployment is through its increased synthesis in 94

response to pathogens and abiotic stresses, such as treatments with UV-C light, high light 95

radiation, and ozone (Yalpani et al., 1994; Nawrath et al., 2002; Ogawa et al., 2005; Mateo 96

et al., 2006; Catinot et al., 2008; Garcion et al., 2008). Interestingly, the Enhanced Disease 97

Susceptibility 5 (EDS5) SA transporter in the chloroplast envelope of Arabidopsis is 98

necessary for stress-induced SA accumulation, possibly due to a regulatory coupling of SA 99

transport and synthesis (Serrano et al., 2013; Yamasaki et al., 2013). Recently, a catabolic 100

enzyme that converts SA to 2,3 dihydroxybenzoic acid in Arabidopsis was described 101

(Zhang et al., 2013). Other enzymes that impact SA levels have been found or inferred from 102



5

the presence of metabolites related to SA (Mauch et al., 2001; Nugroho et al., 2001; Vlot et 103

al., 2009; Simoh et al., 2010; Dempsey et al., 2011; Zhang et al., 2017). 104

In plants, there is evidence for two biosynthetic routes for SA: the isochorismate 105

(IC) and the phenylalanine ammonia-lyase (PAL) pathways. As a precursor, both pathways 106

use chorismate, which is the end product of the shikimate pathway that operates in plastids 107

(Poulsen and Verpoorte, 1991; Schmid and Amrhein, 1995). The IC pathway has two steps: 108

one is the reversible conversion of chorismate to isochorismate catalyzed by 109

ISOCHORISMATE SYNTHASE 1 (ICS1), a plastid-localized enzyme (Strawn et al., 110

2007). The second step is the conversion of IC to SA by a mechanism that is still unknown 111

in plants (Strawn et al., 2007). 112

Regulation of SA production under stress conditions through ICS activity differs in 113

different plant species. In Arabidopsis, most of the basal SA is produced via the PAL 114

pathway (Huang et al., 2010), whereas the IC pathway is responsible for approximately 115

90% of SA production induced by pathogens or UV-C light (Wildermuth et al., 2001; 116

Garcion et al., 2008). However, it has been shown that unlike Arabidopsis, the PAL and IC 117

pathways are equally important for pathogen-induced SA biosynthesis in soybean (Glycine 118

max; Shine et al., 2016). Both Arabidopsis and soybean have two ICS genes. In other land 119

plants, such as poplar (Populus trichocarpa), rice (Oryza sativa), castor bean (Ricinus 120

communis), grapeveine (Vitis vinifera), and alfalfa (Medicago truncatula), alternative 121

splicing of a single ICS gene works as a mechanism to modulate ICS function (Macaulay et 122

al., 2017). Therefore, differential ICS regulation may have evolved to accommodate the 123

chemical defense strategies of different plants (Yuan et al., 2009). 124

The level of SA in different tissues after stress treatment was suggested to be critical 125

for defining the type of defense reaction that is established (Fu et al., 2012). Therefore, 126



6

knowledge of how SA levels are controlled is a central issue for understanding plant 127

defense responses and stress physiology. A number of proteins are needed for normal SA 128

accumulation due to their regulatory and signaling roles in defense (e.g. Cui et al., 2017; 129

Ding et al., 2015; Lu et al., 2003; Nomura et al., 2012; Okrent et al., 2010; Song et al., 130

2004; Wang et al., 2014). Transcriptional regulators of the ICS1 gene have also been 131

studied (Chen et al., 2009; Zhang et al., 2010; Dempsey et al., 2011; van Verk et al., 2011; 132

Zheng et al., 2012; Wang et al., 2015; Zheng et al., 2015). However, proteins implicated in 133

the direct regulation of ICS1 protein and/or activity levels have yet to be documented. In 134

this study, proteins found to co-immunoprecipitate with ICS1 were identified, and the role 135

of one of them, PROHIBITIN 3 (PHB3), is characterized. PHBs play important and diverse 136

biological functions, such as acting as scaffold proteins for complex formation and 137

stabilization (Steglich et al., 1999; Nijtmans et al., 2000; Van Aken et al., 2007). Many 138

molecular studies in diverse organisms such as yeast, mammals, and plants, have focused 139

on the roles of PHBs in mitochondria (Nijtmans et al., 2000; Piechota et al., 2010; Steglich 140

et al., 1999). The current view is that the principal function of PHBs in mitochondria is to 141

support the structural organization of the inner mitochondrial membrane (Piechota et al., 142

2015). In plants, PHBs play a positive role in the development of new tissues and organs, 143

possibly by maintaining optimal mitochondrial activity (Ahn et al., 2006; Van Aken et al., 144

2007). We show here that PHB3 impacts both ICS1 protein and SA accumulation and is 145

found in chloroplasts, making it a potentially direct regulator of this important pathway. 146



7

RESULTS 147

Identification of PROHIBITINS as proteins that form complexes with ICS1 148

We took advantage of previously constructed sid2-2 plants that contain a 149

complementing ICS1-V5 transgene (Strawn et al., 2007) to identify proteins with which 150

ICS1 forms complexes using affinity purification and proteomics. V5 antibody-conjugated 151

beads were used to immunoprecipitate (IP) proteins from extracts of untreated and UV-C-152

treated sid2-2/ICS1-V5 or wild-type (WT) plants. Liquid chromatography-tandem mass 153

spectrometry (LC-MS/MS) analysis showed that together with ICS1 peptides, a large 154

number of peptides from a family of proteins called PROHIBITINs (PHBs, Table 1, 155

Supplemental Table S1) were found in IPs from the ICS1-V5 plant extracts. Supplemental 156

Fig. S1 shows the enrichment of PHBs using spectral counting and Supplemental Table S1 157

shows the top proteins from which peptides were found to be specifically enriched, 158

including PHB3, PHB2, PHB4 and several proteins in the superfamily to which PHBs 159

belong (called Band 7). Immunoblotting using an antibody that recognizes PHB3 and 160

PHB4 (Snedden and Fromm, 1997; Van Aken et al., 2007) confirmed that PHB3/4 proteins 161

were present in the ICS1-containing complexes (Fig. 1A). It was previously shown that the 162

majority of the immunoblot signal found with this antibody comes from PHB3 (Van Aken 163

et al., 2007). The amount of ICS1 and PHB3/4 recovered after IP of ICS1-V5 was 164

unaffected by UV-C light 24 hours post-treatment (Fig. 1B, 1C). These results indicate that 165

the ICS1 protein forms complexes with PHBs. 166

167

ICS1 protein levels are UV-C inducible 168

ICS1 transcript and SA levels are induced by UV-C stress in Arabidopsis (Garcion 169

et al., 2008; Martínez et al., 2004; Nawrath et al., 2002; Serrano et al., 2013; Shapiro and 170



8

Zhang, 2001). As expected, under our conditions, UV-C induced ICS1 transcript levels in 171

WT plants (Fig. 2A, left panel). Immunoblot analysis using an antibody that specifically 172

recognizes ICS1 showed that UV-C also induced ICS1 protein accumulation in WT, but not 173

in the negative control (sid2-2 mutant plants; Fig. 2B). 174

These results contrasted with what was observed in sid2-2/ICS1-V5 plants. In 175

particular, sid2-2/ICS1-V5 plants had high levels of both ICS1-V5 transcript and protein 176

even without stress (Fig. 2A, C, D, see also Fig. 1). ICS1 protein levels were so high in the 177

ICS1-V5 plants that the immunoblots were completely overexposed under conditions 178

where ICS1 protein could be detected with the ICS1 antibody in WT (Fig. 2C). Therefore, 179

the blot in Fig. 2C was stripped and re-probed with V5 antibody. In sid2-2/ICS1-V5 plants, 180

basal levels of PR1 and SA were elevated (Fig. 2D, E). Although significant differences in 181

ICS1-V5 transcript or protein levels in response to UV-C were not detected at the time 182

points tested (Fig. 2A, D), SA and PR1 were elevated (Fig 2D, F). Basal levels of SA in 183

sid2-2/ICS1-V5 were affected by the growth conditions; soil-grown plants (Fig. 2E) showed 184

higher levels of SA than in vitro-grown plants (Fig. 2F). These results indicate that the 185

ICS1 protein accumulates upon UV-C stress exposure in WT plants. 186

187

PHB3 localizes to chloroplasts and mitochondria 188

Since ICS1 forms complexes with PHB3/4 and other PHBs, a pool of PHBs may be 189

present in chloroplasts where ICS1 localizes (Strawn et al., 2007). Previously, PHB3 was 190

described as a mitochondrial protein (Ahn et al., 2006; Van Aken et al., 2007). To evaluate 191

the subcellular localization of PHB3, we used confocal microscopy for live imaging of 192

PHB3-GFP and organelle markers transiently expressed in N. benthamiana, and PHB3-193

GFP constitutively expressed in Arabidopsis. The PHB3-GFP fusion was functional, as it 194



9

could rescue the known small plant phenotype of an Arabidopsis phb3-3 loss-of-function 195

mutant (Wang et al., 2010) (Fig. 3A). This mutant was confirmed to have reduced levels of 196

PHB3 (Supplemental Fig. S2). The control, untransformed N. benthamiana leaves show 197

very little background signal under our imaging conditions (Fig. 3B; Supplemental Fig. S3). 198

PHB3-GFP localized in chloroplasts and small structures resembling mitochondria in both 199

species (Fig. 3C-E). A portion of the PHB3-GFP signal colocalized with chlorophyll 200

autofluorescence (Fig. 3C; Supplemental Fig. S3; Supplemental Video S1). Additionally, 201

PHB3-GFP colocalized with OEP7-RFP, a marker for the envelope membrane of 202

chloroplasts, around N. benthamiana chloroplasts (Lee et al., 2011; Fig. 3C and 203

Supplemental Fig. S3). Stable Arabidopsis transformants also showed colocalization of a 204

portion of the PHB3-GFP signal with chlorophyll autofluorescence in epidermal 205

chloroplasts (Fig. 3D and Supplemental Fig. S3). 206

A portion of the PHB3-GFP signal outside chloroplasts colocalized in small 207

structures with the mitochondrial markers COX4-mCherry (Nelson et al., 2007) and COX4-208

dsRed (Li et al., 2017) in N. benthamiana (Fig. 3E and Supplemental Fig. S3). PHB3-GFP 209

was also visible in similar structures in Arabidopsis (Fig. 3D). Videos of transiently-210

transformed N. benthamiana show characteristic mobility of the mitochondria labeled with 211

PHB3-GFP and COX4-mCherry (Supplemental Videos S1 and S2). 212

To confirm the chloroplast localization of PHB3 and co-fractionation with ICS1, we 213

isolated chloroplasts from sid2-2/ICS1-V5 plants treated or not with UV-C and performed 214

immunoblot analysis. Chloroplasts from non-treated WT plants were also assessed for 215

PHB3/4 localization. PHB3/4 was detected in chloroplast fractions of untreated WT plants, 216

as well as in untreated and UV-C-treated sid2-2/ICS1-V5 plants (Fig. 4A). As expected, 217

ICS1-V5 was detected in the chloroplasts of untreated and treated sid2-2/ICS1-V5 plants. 218



10

We did not observe changes of PHB3/4 or ICS1 localization upon UV treatment. The 219

immunodetection of protein markers for different subcellular fractions confirmed the purity 220

of the chloroplast fractions. Importantly, chloroplasts were not contaminated with the 221

mitochondrial marker Prx IIF (Fig. 4A). 222

PHB is associated with membranes in mitochondria (Piechota et al., 2010; Tatsuta 223

et al., 2005). To test the localization of PHB in chloroplasts, we partitioned isolated 224

chloroplasts into membrane and soluble fractions (Fig. 4B). PHB was detected with the 225

PHB3/4 antibody in the membrane, but not in the soluble fractions of Arabidopsis, 226

spinach and N. benthamiana chloroplasts. The purity of the fractions was confirmed by 227

immunodetection of inner envelope Tic110 and stromal cpHsp70 proteins (Fig. 4B). 228

To test if PHB is a peripheral or internal chloroplast protein, we treated isolated N. 229

benthamiana and Arabidopsis chloroplasts with thermolysin to remove surface proteins 230

(Fig. 4C,D). Transiently produced AtPHB3-GFP in N. benthamiana as well as the native 231

PHBs in N. benthamiana (Fig. 4C) and Arabidopsis (Fig. 4D) chloroplasts were mostly 232

protected from thermolysin. We observed partial proteolysis of the chloroplast inner 233

envelope protein Tic110 (Jackson et al., 1998; Inaba et al., 2003) in both species (Fig. 4C-234

D), as previously reported (Hardré et al., 2014). The outer envelope protein SFR2 from 235

Arabidopsis, detected with an antibody that did not recognize the N. benthamiana protein 236

(Roston et al., 2014), was digested by thermolysin (Fig. 4D). In contrast, the thylakoid 237

membrane-associated proteins AtpB and LHCII, as well as the stromal cpHSP70, were 238

fully protected from proteolysis (Fig. 4C-D). Together, these data demonstrate that a pool 239

of PHB3 localizes to chloroplasts, most likely to the inner envelope. This result is 240

consistent with the finding that this protein forms complexes with ICS1. 241

242



11

SA and PR1 levels in response to UV-C treatment and bacterial infections are reduced 243

in the phb3-3 mutant 244

Since ICS1 forms complexes with PHB3, we evaluated whether the phb3-3 mutant 245

is compromised for SA biosynthesis and/or SA-dependent responses after UV-C stress. 246

After UV-C treatment for 24 h, phb3-3 mutant plants showed reduced SA levels compared 247

to WT. However, SA levels in phb3-3 were not as low as those in the SA biosynthesis 248

mutant sid2-2 (Fig. 5A). The SA response marker PR1 also showed lower levels in phb3-3 249

than in WT (Fig. 5B). UV-C failed to induce PR1 in sid2-2 (Fig. 5C), confirming that this 250

marker is SA-dependent under these conditions. Importantly, PR1 was induced in the phb3-251

3 mutant upon SA treatment, indicating that this mutant still responds to SA (Fig. 5D). 252

We also evaluated whether the phb3-3 mutant was compromised for SA 253

accumulation and responses after infection with a pathogen that induces SA. For this 254

purpose, WT and phb3-3 plants were inoculated by flooding (Ishiga et al., 2011) with an 255

avirulent strain of Pseudomonas syringae pv. tomato DC3000 carrying AvrRpm1 256

(Pst/AvrRpm1). Compared to WT, phb3-3 plants showed lower free SA levels 12 h after 257

infection (Fig. 6A), a phenotype that we previously found strongly correlates with 258

hypersusceptibility (e.g. see (Lu et al., 2003; Song et al., 2004; Lee et al., 2007)). 259

Additionally, glycosylated SA levels were lower in phb3-3 mutant plants compared to WT 260

throughout the time course (Fig. 6A). We also detected a lower accumulation of PR1 261

protein in phb3-3 mutant plants compared to WT plants after infection (Fig. 6B). 262

As predicted by the reduced SA accumulation, phb3-3 mutant plants showed greater 263

growth of Pst/AvrRpm1 compared to WT, similar to the sid2-2 mutant phenotype (Fig. 7A). 264

The phb3-3 mutant was also more susceptible to the avirulent strain Pst/AvrRpt2, and 265

showed similar levels of bacterial growth as sid2-2 (Fig. 7B). This result was expected, 266



12

since Pst/AvrRpt2 normally triggers SA-dependent disease resistance (Nawrath and 267

Métraux, 1999). In WT plants, these two pathogen isolates induce hypersensitive cell death 268

that can be detected at the individual cell level (Kim et al., 2005). To monitor this, we 269

performed light microscopy of leaves stained with trypan blue within 10 h of infection. 270

Both phb3-3 and sid2-2 showed reduced trypan blue staining relative to WT after 271

inoculation with Pst/AvrRpm1 and Pst/AvrRpt2 strains (Fig. 7C-D). Similar phenotypic 272

effects of sid2 mutations on single cell death events were reported previously (Brodersen et 273

al., 2005; Ichimura et al., 2006; Yao and Greenberg, 2006; Lu, 2009). 274

These experiments show that PHB3 promotes SA production during stress and 275

infection and is needed for SA-dependent processes such as suppression of pathogen 276

growth and the hypersensitive response at the single cell level. 277

278

Expression of PHB3 complements phb3-3 mutant plants in abiotic and biotic stress 279

responses 280

To determine whether the main phenotypes observed in phb3-3 mutant plants were 281

due to the lack of PHB3 function, we transformed the mutant with a pUBQ10:PHB3-V5 282

rescue construct. The small plant phenotype of phb3-3 was complemented in transgenic 283

lines PHB3-V5 #15 and PHB3-V5 #17 (Fig. 8A). The production of PHB3-V5 protein in 284

both lines was verified by immunodetection of the V5 epitope (Fig. 8B). We noticed that in 285

phb3-3 leaf cross sections the tissue morphology appeared less organized than in WT, a 286

phenotype that was also complemented by the PHB3 transgene (Fig. 8C). Importantly, the 287

complemented lines were restored for the UV-C-induced SA and PR1 as well as pathogen 288

resistance phenotypes (Fig. 8D-F). These results confirm that the phenotypes we observed 289

are due to the phb3-3 mutation. 290



13

291

PHB3 regulates ICS1 protein levels 292

Since SA levels were decreased in UV-C-stressed phb3-3 plants, we evaluated the 293

effect of the phb3-3 mutation on ICS1 levels. ICS1 transcript levels in WT, phb3-3 and 294

phb3-3/PHB3-V5 complemented plants treated with UV-C light similarly increased with a 295

peak at 2 h after irradiation (Fig. 9A). These data suggest that the regulation of ICS1 by 296

PHB3 may occur at a post-transcriptional level. A decrease in the ICS1 protein levels was 297

detected in phb3-3 plants after the UV-C treatment compared to WT (Fig. 9B). Furthermore, 298

we detected an increase in ICS1 protein levels in the PHB3-V5 complemented lines (Fig. 299

9B) relative to WT levels, in agreement with the increase in SA levels detected in these 300

lines (Fig. 8D). 301

In contrast to ICS1, the levels of chloroplast proteins Tic110, NOA1, AtpB, and 302

LOX2 were not significantly altered in the phb3-3 mutant compared to WT (Fig. 9C). 303

Although phb3-3 affects stressed-induced nitric oxide accumulation in roots (Wang et al., 304

2010), we did not observe differences in the levels of NOA1, a chloroplast protein involved 305

in nitric oxide regulation (Mandal et al., 2012), between phb3-3 and WT leaves (Fig. 9C). 306

These data indicate that phb3-3 does not have a general effect on chloroplast proteins. 307

These results strongly suggest that PHB3 regulates SA accumulation through the 308

formation of complexes and stabilization of ICS1 protein under stress conditions. 309

310

311

DISCUSSION 312

Several lines of evidence from this work suggest that increased SA production 313

during UV-C stress involves the induction of active ICS1-containing multiprotein 314



14

complexes. First, in WT Arabidopsis ICS1 protein levels increase upon UV-C stress. 315

Second, ICS1 forms complexes with PHB3/4 and other PHBs. Third, during stress, ICS1 316

protein (but not RNA) levels and the downstream accumulation of SA show alterations that 317

are correlated with the amount of functional PHB3 in plants. Our findings support the view 318

that PHB3-ICS1 complexes are needed for the full production of SA during stress caused 319

by UV-C. 320

The role of PHB3 in promoting SA production extends beyond the response to UV-321

C stress to the biotic interaction of Arabidopsis with the strongly SA-inducing (avirulent) 322

bacterial strain Pst/AvrRpm1. The phb3-3 mutant is hypersusceptible to this strain as well 323

as the avirulent strain Pst/AvrRpt2. Thus, it is possible that PHB3 is necessary to promote 324

maximal SA production when the need for this defense signal is high, such as during stress 325

and other biotic interactions. 326

It is interesting that even though there is residual SA accumulation in the phb3-3 327

plants after infection, the mutant is as susceptible to two avirulent Pst strains and shows 328

similar hypersensitive cell death suppression as sid2-2 (an SA biosynthesis mutant). One 329

possible explanation for the strong phenotypes of phb3-3 plants is that this mutant fails to 330

sense SA adequately, therefore a normal defense response is not activated. However, the 331

phb3-3 plants respond normally to exogenous SA treatment, indicating that SA signaling is 332

not altered. Instead, the strong phenotype of phb3-3 might be the result of a delay in these 333

plants to fully induce SA. We speculate that there is a threshold level of SA that is needed 334

early after infection to promote the induction of defenses that suppress the growth of P. 335

syringae. Alternatively, SA-independent signal(s) that are affected in the phb3-3 plants 336

under some conditions, such as nitric oxide (Wang et al., 2010) or ethylene (Christians and 337

Larsen, 2007), may also contribute to plant defense. However, other Arabidopsis plants 338



15

with reduced SA production, generated by altered expression/mutation of genes that impact 339

SA biosynthesis, exhibit enhanced susceptibility to virulent and avirulent pathogens, 340

similar to the phenotype of phb3-3 (Delaney et al., 1994; Nawrath and Métraux, 1999; 341

Dewdney et al., 2000; Lu et al., 2003; Song et al., 2004; Lee et al., 2007). 342

In addition to identifying the localization of PHB3 in mitochondria (Van Aken et al., 343

2007; Piechota et al., 2010), this work established that there is a pool of PHB3 that resides 344

in chloroplasts, the organelle where SA is made and where ICS1 is targeted (Fragnire et al., 345

2011; Strawn et al., 2007). PHB3 has a hydrophobic region at the N-terminus that likely 346

serves to anchor it to membranes. In agreement with this, PHB3 fractionated with 347

chloroplast membranes and was mostly protected from thermolysin proteolysis, while 348

PHB3-GFP fluorescence was detected at the periphery of chloroplasts, similar to an 349

envelope marker. This study thus establishes that PHB3 is targeted to chloroplasts, similar 350

to PHB2 and PHB4, which were previously reported to be in the envelope fraction of 351

chloroplasts in a proteomics study (Kleffmann et al., 2004). 352

PHB3 was previously found to co-purify with PHB1, PHB2, PHB4, and PHB6 (Van 353

Aken et al., 2007). It was also described as residing in two very large (1-2 MDa) 354

mitochondrial inner membrane complexes with this same group of PHBs (Piechota et al., 355

2010). These five PHBs all co-immunoprecipitate with ICS1. The mitochondrial matrix 356

AAA protease FTSH10 immunoprecipitates four of the five PHBs (except PHB4) that we 357

identified in ICS1 complexes as well as FTSH3 (Piechota et al., 2010). This result suggests 358

that at least four PHBs may form complexes together in more than one subcellular 359

compartment along with one or more non-PHB protein (FTSH10 and FTSH3 in 360

mitochondria and ICS1 in chloroplasts). PHBs form ring-like structures in the inner 361

mitochondrial membrane (Tatsuta et al., 2005; Piechota et al., 2010). If PHBs are capable 362



16

of forming similar structures/complexes in the chloroplast envelope, they may facilitate the 363

import of ICS1 to this organelle or affect its stability after import. Future work will focus 364

on whether PHBs act as chaperones and whether they form large complexes within 365

chloroplasts. 366

How might PHBs regulate ICS1 levels and/or activity? Using an assay in which 367

radiolabeled ICS1 was imported into isolated pea chloroplasts and then fractionated, Strawn 368

et al. (2007) showed that the majority of ICS1 partitioned with the soluble stroma. However, 369

a fraction of the imported ICS1 protein also partitioned with chloroplast membranes, 370

indicating that ICS1 activity or stability might involve its association with the chloroplast 371

envelope where PHBs most likely reside. ICS1-GFP signals were also visible in the 372

peripheries of chloroplasts, including in stromules (Garcion et al., 2008). In some systems, 373

PHBs play a role in the stabilization of protein complexes. Disruption of mitochondrial 374

PHBs usually destabilizes their interactors and leads to various mitochondrial malfunctions 375

(Van Aken et al., 2007). In yeast, the PHB complex binds to two newly synthesized 376

subunits of respiratory complex IV and protects them against degradation (Steglich et al., 377

1999; Nijtmans et al., 2000). In Arabidopsis, we demonstrate that disruption of PHB3 378

function affects ICS1 protein levels without affecting ICS1 RNA accumulation. Therefore, 379

PHB3 may mainly act by stabilizing the ICS1 protein, although it may also affect ICS1 380

activity. Given the large number of PHBs found in ICS1 complexes, it is possible that 381

several PHBs affect ICS1 and SA production. 382

We focused here on how PHB3 affects ICS1, and downstream production of SA and 383

defense-related signaling outputs such as PR1 and cell death induction. Plants with the 384

phb3-3 mutation show phenotypes that are distinct from those caused by reduced ICS1/SA 385

levels. In particular, the small plant phenotype characteristic of phb3 mutants was not 386



17

observed in sid2 plants. The product of ICS1, isochorismate, is also a precursor for 387

phylloquinone, which is barely detectable in the Arabidopsis sid2ics2 double mutant; this 388

mutant displays a dwarf phenotype similar to phb3-3, although the cause of the dwarfism is 389

not known (Garcion et al., 2008). Disruption in the penultimate step in phylloquinone 390

synthesis also results in a modest reduction in plant size (Lohmann et al., 2006). Future 391

work will determine whether PHB3 is required for phylloquinone biosynthesis. It seems 392

possible that the different phb3-3 mutant phenotypes (reduced size, stress-induced SA and 393

NO) are due to reduced levels of different specific complexes that contain PHB3 in 394

chloroplasts and mitochondria, respectively. 395

An unanticipated finding resulting from this study is the phenotype of the ICS1-V5-396

expressing plants, which have very high levels of ICS1 relative to WT. These plants have 397

only moderately elevated basal SA levels that are further increased in response to UV-C. 398

Why are the SA levels in ICS1-V5 plants low without stress? One possibility is that the 399

upstream chorismate precursor is limiting under basal conditions. This seems unlikely 400

given that basal chorismate production from the shikimate pathway is usually high 401

(Herrmann and Weaver, 1999). Another possibility is that ICS1 needs activation (for 402

example, by posttranslational modification(s) or conformational change), or another step 403

required for SA production is limiting. 404

In conclusion, this work demonstrated that ICS1 is regulated post-transcriptionally 405

by PHB3. During stress or infection, highly increased SA production in Arabidopsis likely 406

requires an increase in ICS1 protein levels. Upon stress, this increase in ICS1 protein levels 407

is mainly produced by transcriptional activation of the ICS1 gene (Wildermuth et al., 2001; 408

Martínez et al., 2004; Garcion et al., 2008). PHB3 seems to contribute to this process 409



18

through stabilization of the protein. Whether PHB3 is involved in SA production beyond 410

stabilizing ICS1 will be an interesting topic for future studies. 411

412

413

MATERIALS AND METHODS 414

Plant growth conditions and UV-C treatments 415

Arabidopsis (Arabidopsis thaliana) wild type (WT), phb3-3 (Wang et al., 2010), 416

sid2-2 (Wildermuth et al., 2001), sid2-2/ICS1-V5 (transgenic complementation line SM156 417

in (Strawn et al., 2007)), phb3-3/pUBQ:PHB3-V5 and phb3-3/p35S:PHB3-GFP lines (this 418

report) were in the Columbia (Col-0) background. For plants grown in vitro, growth 419

medium contained 0.5X MS supplemented with 10 g/l sucrose and 2.6 g/l Phytagel (Sigma) 420

and plants were incubated in a growth chamber (16 h light, 100 μmoles m-2 s-1, 22 ± 2ºC). 421

Nicotiana benthamiana plants were grown in soil at 24°C with 16 h light/8 h dark cycle. 422

Fresh spinach was purchased from a store. 423

For fractionation and immunoprecipitation experiments, plants were grown in soil in 424

conditions described in (Pattanayak et al., 2012). Briefly, plants were grown in 50:50 425

Fafard C2/Metro-Mix soil, 16 h light/8 h dark cycle at 20°C. Otherwise, plants were grown 426

in turba soil mixed with vermiculite 1:1 in a growth room under controlled conditions (16 h 427

light/8 h dark cycle, 100 μmoles m-2 s-1, 22 ± 2ºC). 428

UV-C treatments for immunoprecipitation of ICS1-V5 complexes and fractionation 429

experiments were performed with 21-day-old WT and sid2-2/ICS1-V5 plants grown in soil, 430

by exposing them to 254 nm light from an 18.4 W UVP Mineralight UVGL-55 multiband 431

lamp for 45 minutes at a distance of 30 cm in a growth chamber. Leaves were collected 432

from untreated plants and from plants 8, 24 and 32 h after UV-C exposure. For UV-C 433



19

irradiation of in vitro-grown plants (Nawrath and Métraux, 1999), 14-day-old plants were 434

exposed for 20 min in a chamber equipped with two UV-C fluorescent tubes of 8 Watts 435

each one (λ= 254 nm) at a distance of 30 cm above the plates. UV-treated plants were 436

subsequently placed in a growth chamber under controlled conditions for the indicated 437

periods of time. 438

For SA treatments, 15-day-old seedlings were floated in a solution of 0.5 mM SA in 439

0.5X MS medium (treatment), or 0.5X MS medium as a control, and incubated for the 440

indicated periods of time under continuous light (80 μmoles m-2 s-1). For immunoblot 441

analysis, whole seedlings were immediately frozen in liquid nitrogen and stored at -80ºC 442

until total protein extraction. 443

444

Bacterial strains, plant inoculation conditions, bacterial proliferation and cell death 445

assays 446

Pseudomonas syringae pv. tomato DC3000 virulent strain (Pst), and its isogenic 447

avirulent strains expressing the AvrRpm1 (Pst/AvrRpm1) or AvrRpt2 (Pst/AvrRpt2) 448

effectors (Mackey et al., 2002) were used. Bacterial strains were grown at 28°C on King’s 449

B medium supplemented with kanamycin at 50 μg/ml, sedimented by centrifugation and 450

then resuspended in 10 mM MgCl2. Bacterial inoculation was performed by the flooding of 451

14-days-old plants (Ishiga et al., 2011) using a suspension of 1 x 106 CFU/ml (to evaluate 452

SA and PR-1 levels) or 1 x 105 CFU/ml (for bacterial proliferation assays). Alternatively, 453

bacteria were inoculated by syringe infiltration on the abaxial side of the leaves of 4-week-454

old soil-grown plants (Greenberg et al., 2000), using a suspension of 1 x 105 CFU/ml (for 455

bacterial proliferation assays) or 1 x 108 CFU/ml (for cell death assays). 456



20

For bacterial proliferation assays, leaf discs from 12 independent inoculated plants 457

were taken at 0, 2 and/or 3 days post-inoculation (dpi), ground in 10 mM MgCl2, serially 458

diluted 1:10, and plated onto LB agar plates supplemented with 50 μg/ml kanamycin and 459

50 μg/ml rifampicin. Plates were incubated at 28°C for 2 days and the colony forming units 460

(CFUs) were manually counted. Each bacterial proliferation assay was repeated 3 times. 461

Cell death was visualized in leaves of 4-week-old soil-grown plants 10 h after 462

bacterial or mock (control) infiltration, using trypan blue staining (Pavet et al., 2005). 463

Leaves immersed in freshly prepared lactophenol solution (water, basic phenol, lactic acid, 464

and glycerol in a 1:1:1:1 ratio) containing trypan blue at 250 μg/ml were placed in boiling 465

water for 3 min, cleared in lactophenol without trypan blue at room temperature for 16 h, 466

mounted in 50% glycerol and observed using a compound microscope (Nikon Eclipse 80i 467

microscope) at ×100 magnification. This experiment was repeated 3 times. In each 468

experiment, leaves from 4 independent plants per genotype were analyzed. 469

470

471

Light microscopy of leaf sections 472

Small slices of the sixth leaf of 3-week-old plants were prepared as described in 473

(Leon et al., 2007). Briefly, samples were fixed overnight in 2.5% (v/v) glutaraldehyde in 474

0.1 M sodium cacodylate buffer, pH 7.0, and postfixed in 1% osmium tetroxide for 2 h. 475

Then samples were stained with 1% (w/v) uranyl acetate for 90 min, dehydrated with 476

acetone solutions (50, 70, 95 and 100%) and embedded in Epon resin. Polymerization was 477

performed in a heater at 60ºC for 48 h. Fine cuts (80 nm) obtained with a Sorvall MT5000 478

ultramicrotome were stained with 4% (w/v) uranyl acetate and lead citrate in methanol. 479

Images were taken with a Nikon Eclipse 80i microscope at 40X magnification. 480



21

481

Genetic constructs and stable plant transformation 482

To obtain phb3-3 mutant plants complemented with PHB3, pUBQ10:PHB3-V5 and 483

p35S:PHB3-GFP constructs were generated using the Gateway technology following the 484

manufacturer’s instructions (Invitrogen, Carlsbad, CA, USA). The PHB3 coding region was 485

obtained by amplification of cDNA, using the primers described in Supplemental Table S2. 486

The PCR fragment was cloned into the pENTR/SD/D-TOPO vector (Invitrogen, Carlsbad, 487

CA, USA) and then recombined into the pB7m34gW vector (Karimi et al., 2005) to express 488

the PHB3 protein fused to a V5 tag controlled by the ubiquitin 10 promoter (pUBQ10). For 489

live imaging experiments of PHB3 fused to the eGFP reporter protein, the amplified PHB3 490

coding sequence cloned into the pENTR/SD/D-TOPO vector was recombined into the 491

pKGWG2 vector (Karimi et al., 2002). 492

Final constructs were verified by sequencing and introduced into the Agrobacterium 493

tumefaciens C58 strain. Stable Arabidopsis phb3-3 transformants were obtained using the 494

floral dip method (Zhang et al., 2006). Transgenic seeds were selected in 0.5X MS solid 495

medium supplemented with 50 μg/ml kanamycin for the GFP reporter lines or with 15 496

μg/ml glufosinate-ammonium for the PHB3-V5-expressing lines. Homozygous transgenic 497

lines were selected and used for further analyses. 498

499

500

Protein extracts, immunoblot and immunoprecipitation. 501

Total protein extracts were obtained from WT and transgenic lines by homogenizing 502

0.5 g tissue (each sample was composed of 12-15 seedlings grown on plates, or several 503

mature leaves of plants grown in soil) per 1 ml extraction buffer (50 mM sodium phosphate 504



22

buffer pH 8.0, 150 mM NaCl, 0.2% Igepal, 5 mM EDTA, 1X complete Protease Inhibitor 505

Cocktail solution (Roche Diagnostics Corporation, Indianapolis, IN, USA)). After 506

centrifugation at 2,350 g for 10 min, supernatants were transferred to clean tubes and stored 507

at –80°C. Protein concentration was determined by the Bradford method, using the BioRad 508

Protein Assay (Bio-Rad Laboratories, Inc., CA, USA). 509

For immunoblot analysis, total or chloroplast (see below) protein extracts (30 µg of 510

protein per lane) were separated in 12% SDS–polyacrylamide gels (PAGE) and transferred 511

to ImmobilonTM PDVF membranes (Millipore Co., Bedford, MA, USA) by semi-dry 512

electroblotting. The membranes were blocked for 1 h in phosphate-buffered saline solution 513

(PBS-T: 137 mM NaCl, 2.7 mM KCl, 10 mM Na2HPO4, 2 mM KH2PO4 and 0,1% Tween-514

20) with 5% non-fat dried milk at room temperature. To detect the ICS1-V5 and PHB3-V5 515

fusion proteins, the mouse monoclonal V5 antibody (Invitrogen, Carlsbad, CA, USA, 516

#R96025) was used at a 1:5,000 dilution. To detect PR1, the rabbit polyclonal PR1 517

antibody (Agrisera, Vännäs, Sweden, #AS10 687) was used at a 1:2,500 dilution. PHBs 518

were detected with the PHB3/4 rabbit polyclonal antibody described in (Snedden and 519

Fromm, 1997; Van Aken et al., 2007) at a 1:10,000 dilution. 520

ICS1 was detected with the rabbit polyclonal ICS1 antibody UCB68 at a 1:10,000 521

dilution. This antibody was made by immunizing rabbits with purified recombinant mature 522

ICS1 protein (described in Strawn et al., 2007). The titer and specificity of the antibody 523

were tested by immunoblot analysis. The antibody can detect as low as 31 pg of 524

recombinant ICS1 protein, with ready detection of ICS1 protein in UV-C-induced leaf 525

extracts using a 1:10,000 dilution. 526

Proteins used as markers for subcellular localization were detected using rabbit 527

polyclonal antibodies against: ATP synthase β (AtpB, chloroplast, 1:10,000, a gift from Dr. 528



23

Dominique Drapier, CNRS/UPMC, Paris, France (Drapier et al., 2007)), peroxiredoxin II F 529

(Prx II F, mitochondria, 1:3,000; a gift from Dr. Karl-Josef Dietz, Bielefeld University, 530

Germany (Finkemeier et al., 2005)), cytosolic fructose-1,6.bisphosphatase (cFBPase, 531

cytoplasm, 1:25,000, Agrisera, Vännäs, Sweden, #AS04043), H+ATPase (plasma 532

membrane, 1:2,000, Agrisera, Vännäs, Sweden, #AS07260), Tic110 (chloroplast inner 533

envelope, 1:3000, a gift from Masato Nakai, Osaka University, Japan (Kikuchi et al., 534

2006)), NOA1 (1:10000, a gift from Pradeep Kachroo, University of Kentucky, USA 535

(Mandal et al., 2012)), chloroplast lipooxygenase 2 (LOX-C, 1:30,000, Agrisera, Vännäs, 536

Sweden, #AS07258), light harvesting complex II (LHCII, thylakoid, 1:5000, a gift from 537

Roberto Bassi, Università di Verona, Italy (Di Paolo et al., 1990)), SFR2 N and C 538

(chloroplast outer envelope, 1:1000, a gift from Christoph Benning, Michigan State 539

University, USA (Roston et al., 2014)) and a guinea pig antibody against chloroplast Hsp70 540

(1:12000, a gift from Thomas Leustek, Rutgers University, USA (Wang et al., 1993)). 541

After washing in PBS-T (three times), the membranes were incubated with the anti-542

mouse horseradish peroxidase-conjugated secondary antibody (KPL, Gaithersburg, MD, 543

USA. #074-1806, 1:10,000 and Thermo Fisher, Waltham, MA, USA, #31440, 1:1,000), 544

anti-guinea pig-peroxidase antibody (Sigma, St. Louis, MO, USA, #A5545, 1:100,000) or 545

the anti-rabbit horseradish antibody (Invitrogen, Carlsbad, CA, USA. #65-6120, 1:10,000 546

and Thermo Fisher, Waltham, MA, USA, #32460, 1:1,000). After washing in PBS-T (15 547

min three times), proteins immunodetected were visualized using chemiluminescence kits 548

(Thermo Fisher Scientific, Waltham, MA, USA, #34087 and #34095) according to the 549

manufacturer’s instructions. 550

All immunoblots were repeated 2 or 3 times with new samples, as indicated in the 551

corresponding figure legends. 552



24

For immunoprecipitation of ICS1-V5-containing complexes, total protein extracts of 553

untreated and UV-C treated WT and sid2-2/ICS1-V5 plants (see above) were prepared as 554

described (Jelenska et al., 2010). Immunoprecipitation was performed using anti-V5 555

agarose (Sigma, St. Louis, MO, USA, #A7345). After immunoprecipitation, proteins were 556

separated by SDS/PAGE and analyzed either by Coomassie blue staining and LC-MS/MS 557

or by immunoblotting. This experiment was repeated 3 times with different protein extract 558

samples. 559

560

Database searching of peptides identified by LC-MS/MS. 561

LC-MS/MS protein identification was performed at the Stanford University Mass 562

Spectrometry Facility. Protein bands in ICS1-V5 immunoprecipitations and the 563

corresponding regions of WT samples were cut from the gel; UV-C treated and untreated 564

samples were combined for further analysis. Proteins in gel bands were digested with 565

trypsin, extracted, and peptides were identified as described (Jelenska et al., 2010). MS/MS 566

samples were analyzed using Sequest (Thermo Fisher Scientific, San Jose, CA, USA; 567

version v.27, rev. 11) set up to search the NCBI_Arabidopsis_thaliana database (222041 568

entries) assuming the digestion enzyme stricttrypsin. Scaffold (version Scaffold_3.1.4.1, 569

Proteome Software Inc., Portland, OR, USA) was used to validate MS/MS-based 570

identifications of peptides (at greater than 95.0% probability) and proteins (at greater than 571

95.0% probability and contained at least one identified peptide). 572

573

Chloroplast isolation, fractionation and thermolysin treatment 574

Three-week-old WT and sid2-2/ICS1-V5 plants grown in soil were treated with UV-575

C and chloroplasts were isolated in a percoll gradient as described (Kubis and Lilley, 2008). 576



25

Purity of the chloroplast fractions was evaluated by immunoblot analysis as described 577

above. N. benthamiana chloroplasts were isolated and treated with thermolysin (Sigma, St. 578

Louis, MO, USA) according to (Lamppa, 1995). Arabidopsis chloroplasts for thermolysin 579

treatment experiment were isolated as described (Aronsson and Jarvis, 2002). For 580

membrane association, spinach, N. benthamiana and Arabidopsis chloroplasts were isolated 581

as described in (Kieselbach et al., 1998) and partitioned to membrane and soluble fractions 582

according to (Lamppa, 1995). 583

584

Confocal microscopy 585

Leaves and cotyledons of ~10-day-old seedlings of phb3-3/PHB3-GFP (line #6.5) 586

Arabidopsis were used for imaging. Nicotiana benthamiana plants grown in soil were 587

transiently transformed with Agrobacteria harboring the constructs p35S:PHB3-GFP (see 588

above), pdex:OEP7-RFP (Cecchini et al., 2015), pd35S:COX4-mCherry (mt-rb, (Nelson et 589

al., 2007)) and p35S:COX4-dsRed (from Dr. Guo-Liang Wang, Ohio State University, USA 590

(Li et al., 2017)) as described in (Cecchini et al., 2015; Jelenska et al., 2017). Agrobacteria 591

with different constructs were infiltrated together and N. benthamiana leaves were imaged 592

2 days later. Leaves transformed with pdex:OEP7-RFP construct were sprayed with 3 µM 593

dexamethasone 1 day after agroinfiltration. Three-week-old N. benthamiana plants were 594

used for images with mitochondrial markers and 5–6-week-old plants for other images. 595

Confocal images were obtained using a Zeiss LSM710 laser-scanning confocal 596

microscope (Zeiss, Germany) as described in (Kang et al., 2014; Cecchini et al., 2015; 597

Jelenska et al., 2017). Fluorescence was visualized as follows: GFP excitation 488 598

nm/emission 496-557 nm; RFP ex 561/em 570-619, mCherry/dsRed ex 561/em 580-629, 599

chlorophyll autofluorescence ex 633/em 655-747. Fluorescence in different channels was 600



26

acquired for the same field using a sequential acquisition mode for PHB3 + OEP7 and 601

simultaneously for PHB3 + COX4 to allow imaging of moving mitochondria. Z series 602

images (14-18 µm for N. benthamiana and 21 µm for Arabidopsis) and time series videos 603

(60 image series) were processed with ImageJ (https://imagej.nih.gov/ij). 604

605

Quantitation of SA 606

Free and glycosylated SA (SAG) extracted from leaf tissues were quantified by 607

HPLC using an Atlantis T3 column, as described previously (Verberne et al., 2002). 608

Results show data from 3 independent experiments. Each sample consisted of 0.5 g of 609

tissue collected from a pool of 12-15 seedlings grown on plates or mature leaves from three 610

plants grown in soil. 611

612

RT-qPCR analysis 613

Whole UV-C-treated plants (4 seedlings per genotype) grown in vitro were frozen 614

in liquid nitrogen and stored at -80ºC until RNA isolation. Total RNA was obtained from 615

frozen samples using the TRIzol® Reagent (Invitrogen) according to the manufacturer’s 616

instructions. cDNA was synthesized from each sample (2 μg of total RNA) with an ImProm 617

II Kit (Promega). qPCR was performed using the Brilliant III Ultra-Fast SYBR® Green 618

QPCR Master mix (Agilent Technologies) reagents on a AriaMx real-time PCR system 619

equipment. The expression levels of the ICS1 gene were calculated relative to the YLS8 620

endogenous control. Primers used for each gene are listed in Supplemental Table S2. Data 621

represent results from 3 biological replicates (independent experiments). In each 622

experiment, 3 technical replicates from the same cDNA sample were used. 623

624



27

Accession numbers 625

Sequence data from this article are found in the GenBank/EMBL data libraries under the 626

following accession numbers: 627

-Arabidopsis thaliana: AT1G74710 (ICS1/SID2), AT5G40770 (PHB3), AT1G03860 628

(PHB2), AT3G27280 (PHB4), AT2G20530 (PHB6), AT4G28510 (PHB1), AT2G14610 629

(PR-1), AT5G08290 (YLS8), AT3G52420 (OEP7), AT3G06050 (PRX IIF), AT1G43670 630

(cFBPase), AT4G30190 (H+-ATPase), AT1G06950 (TIC110), AT4G24280 (cpHSP70-1), 631

AT5G49910 (cpHSP70-2), AT3G06510 (SFR2), ATCG00480 (AtpB), AT3G47450 632

(NOA1), AT3G45140 (LOX2). 633

-Saccharomyces cerevisiae: YGL187C (ScCOX4). 634

-Nicotiana benthamiana: DQ121387 (NbPHB1) and DQ121388 (NbPHB2). 635

-Spinacia oleracea: AF035456, AF039083, M99565 (So-cpHSP70s), 2715576 (SoAtpB). 636

637



28

SUPPLEMENTAL MATERIAL 638

The following supplemental materials are available: 639

Supplemental Figure S1. Spectrum count of peptides detected by LC-MS/MS in WT and 640

sid2-2/ICS1-V5 samples. 641

Supplemental Figure S2. PHB3/4 protein levels in UV-C treated WT, phb3-3 and phb3-642

3/PHB3-V5 plants. 643

Supplemental Figure S3. PHB3 colocalizes with chloroplasts and mitochondria markers. 644

Supplemental Video S1. Video of N. benthamiana leaves expressing PHB3-GFP. 645

Supplemental Video S2. Video of N. benthamiana leaves expressing PHB3-GFP and 646

mitochondrial marker COX4-mCherry. 647

Supplemental Table S1. List of peptides matching PHB protein family members and ICS1 648

and the number of spectra of peptides found from the top enriched proteins identified in 649

ICS1-V5 complexes by LC-MS/MS analysis 650

Supplemental Table S2. List of primers 651

652

ACKNOWLEDGMENTS 653

We thank Hillel Fromm (Department of Plant Sciences, Tel Aviv University, Israel) for 654

providing the PHB3/4 antibody, Dominique Drapier (CNRS/UPMC, Paris, France) for the 655

AtpB antibody, Karl-Josef Dietz (Bielefeld University, Germany) for the Prx II F antibody, 656

Pradeep Kachroo (University of Kentucky, USA) for the NOA1 antibody, Gopal 657

Pattanayak (University of Chicago, USA) for antibodies against Tic110 (from Masato 658

Nakai, Osaka University, Japan) and LHCII (from Roberto Bassi, Università di Verona, 659

Italy), Thomas Leustek, (Rutgers University, USA) for the cpHSP70 antibody, Christoph 660

Benning (Michigan State University, USA) for the SFR2 antibody, Andreas Nebenführ 661



29

(University of Tennessee, Knoxville, USA) for the COX4-mCherry marker, and Guo-Liang 662

Wang (Ohio State University, USA) for the COX4-dsRed marker. We also thank Jacquelyn 663

Freeman for help with IP experiments and Michael Allara for help with western blots. 664

665



30

Table 1. Prohibitins found in ICS1-V5 complexes purified from sid2-2/ICS1-V5 plants. 666

Peptides were identified by LC-MS/MS analysis. (*) Number of different peptides that 667

match the indicated protein and may also match one or more other isoforms. (†) Number of 668

peptides specific to the protein isoform indicated. The column % Coverage shows the 669

percentage of the protein sequence represented by the peptides found in the LC-MS/MS 670

analysis. 671

672

673

Proteins AGI Unique peptides*

Specific peptides† % Coverage

ICS1 AT1G74710 16 13 42 PHB3 AT5G40770 19 11 69 PHB2 AT1G03860 16 9 64 PHB4 AT3G27280 12 4 53 PHB6 AT2G20530 9 4 37 PHB1 AT4G28510 8 4 39

674 675



31

FIGURE LEGENDS 676 677

Figure 1. PHB3/4 form complexes with ICS1-V5 under normal and stress conditions. 678

A, Plants grown in soil were treated with UV-C light for 45 min and assayed 24 h later (+). 679

Untreated plants were used as controls (-). Total proteins were extracted and ICS1-680

containing complexes were immunoprecipitated with V5 antibody. The presence of ICS1-681

V5 and PHB3/4 proteins in the total protein extracts (input, left panel) and in the 682

immunoprecipitated ICS1-containing complexes (IP αV5, right panel) was confirmed by 683

immunoblotting using V5 and PHB3/4 antibodies. Coomassie-stained membranes (bottom) 684

show similar loading. Panel A shows a representative blot from three independent 685

experiments (two from total extracts and one from chloroplast extracts). B and C, 686

Quantitation of ICS1-V5 (B) and PHB3/4 (C) protein levels from three IP experiments as 687

in (A), using densitometry with the Image J program. RU, relative units with respect to an 688

average signal of untreated samples for each antibody. Error bars are SEM. Statistical 689

analyses using t-tests showed that no significant differences were detected (p=0.78 for B 690

and; p=0.97 for C). 691

692

Figure 2. ICS1 protein levels are induced by UV-C treatment and constitutively 693

elevated in sid2-2/ICS1-V5 plants. Plants were grown on plates (A, B, C, F) or soil (D), 694

treated with UV-C for 20 min (A, B, C, F) or 45 min (D), and assayed 0, 8 and 24 h post-695

treatment (hpt). Untreated plants were used as controls (–). A, ICS1 transcript levels were 696

measured by RT-qPCR in WT (black bars) and sid2-2/ICS1-V5 (gray bars) plants. 697

Expression is relative (R.) to YLS8 gene (n=3 biological replicates). B, Immunoblot 698

analysis showing that ICS1 is induced by UV-C treatment in WT and is not detectable in 699



32

sid2-2 plants. C, ICS1 protein levels detected by immunoblot in WT and sid2-2/ICS1-V5 700

plants using ICS1 or V5 antibodies. D, PR1 and ICS1-V5 protein levels in WT and sid2-701

2/ICS1-V5 plants. In sid2-2/ICS1-V5 plants, basal PR1 is elevated and UV-C further 702

induces the PR1 level. B-D, Panels show representative results from three (B, C) or two (D) 703

independent experiments. Coomassie stained membranes (bottom) show similar loading. E, 704

F, Free SA (gray bars) and glycosylated SA (SAG, white bars) levels in the indicated plants. 705

E, untreated plants grown in soil, showing higher SA levels in the sid2-2/ICS1-V5 plants 706

than WT (n=5). Similar results were found in an independent trial. F, Free SA and SAG 707

levels are induced by UV-C in plants with constitutive ICS1 levels (n=3). Statistical 708

analyses in A, E and F were performed using ANOVA/Fisher’s LSD test. Each letter group 709

differs from other letter groups at p<0.05. Error bars show SEM. 710

711

Figure 3. PHB3-GFP localizes to chloroplasts and mitochondria. A, Morphological 712

phenotype of the phb3-3 mutant is complemented by the PHB3-GFP transgene. Images 713

show 3-week-old WT, phb3-3 and phb3-3/PHB3-GFP #6.5 plants grown in soil. B-E, 714

Untransformed (B) and transiently transformed (C, E) N. benthamiana leaves, and stably 715

transformed Arabidopsis cotyledons (D), were imaged by confocal microscopy in green 716

(PHB3-GFP), red (OEP7-RFP and COX4-mCherry), chl (chlorophyll auto-fluorescence, 717

blue), and DIC (bright field) channels. Maximum intensity projections of Z series images 718

are shown. Scale bar = 20 µm. C, Co-expression of PHB3-GFP and OEP7-RFP 719

(chloroplast outer envelope marker). D, Expression of PHB3-GFP in Arabidopsis (phb3-720

3/PHB3-GFP #6.5 plants). E, Co-expression of PHB3-GFP and COX4-mCherry 721

(mitochondrial marker). Insert shows higher magnification. Co-localization with COX4-722

dsRed was also performed with similar results. White arrowheads show examples of PHB3-723



33

GFP localization in chloroplasts (C-E). Experiments were done two (D) or three times (B, 724

C and E) with similar results. 725

726

Figure 4. PHB3 is a chloroplast membrane protein. A, Immunodetection of PHB3/4 in 727

total and chloroplast protein extracts obtained from WT and sid2/ICS1-V5 plants, grown in 728

soil, treated (+) or not (–) with UV-C as described in Figure 1. ICS1-V5 was detected with 729

V5 antibody and PHBs were detected with a PHB3/4 antibody (n=2). The purity of the 730

chloroplast fraction was evaluated by immunodetection of markers for specific subcellular 731

localizations (AtpB for chloroplast; Prx II F for mitochondria; cFBPase for cytoplasm; 732

H+ATPase for plasma membrane). B, PHB3 localizes to chloroplast membranes. Spinach 733

(So), Arabidopsis (At) and N. benthamiana (Nb) chloroplasts were partitioned into 734

membrane and soluble fractions. PHB was detected with a PHB3/4 antibody and fractions 735

were confirmed with antibodies against pea Tic110 (membrane) and spinach cpHsp70 736

(soluble). Coomassie blue (A) and Ponceau S (B) staining of proteins show similar loading. 737

C-D, PHB is mostly protected from thermolysin digestion in N. benthamiana (C) and 738

Arabidopsis (D) chloroplasts. Chloroplasts isolated from N. benthamiana transiently 739

expressing AtPHB3-GFP (C, upper 4 panels), control N. benthamiana (C, lower 2 panels) 740

or from Arabidopsis leaves (D) were incubated without (-) or with (+) thermolysin (Therm). 741

Sensitivity to digestion was evaluated for PHB (PHB3/4 antibody), AtPHB3-GFP (GFP 742

antibody and PHB3/4 antibody, C) and for the inner envelope Tic110, the outer envelope 743

SFR2 (D), the thylakoid-associated AtpB, and LHCII and the stromal cpHsp70 (C). Black 744

arrowheads indicate AtPHB3-GFP and white arrowhead shows NbPHB (C). Similar results 745

were obtained for 2-4 chloroplast preparations. 746

747



34

Figure 5. phb3-3 mutant plants have lower SA levels and PR1 accumulation after UV-748

C treatment. A-C, Leaf tissue from plants grown on plates treated with UV-C light for 20 749

min and harvested at 2, 8, and 24 hpt. Untreated plants were used as controls (–). A, Levels 750

of free SA (gray bars) and glycosylated SA (SAG, white bars). FW indicates fresh weight; 751

n/d indicates not detected. Each bar represents the mean of three independent experiments; 752

error bars indicate SEM. Statistical analysis was performed using ANOVA/Fisher’s test. 753

Different letters denote statistically significant differences at p<0.05. B-C, PR1 protein was 754

detected by immunoblot analysis using a PR1 antibody. A non-specific band in the 755

immunoblot shows similar loading in each lane. Panels show representative results from 756

three independent experiments. D, Two-week-old WT, phb3-3, and sid2-2 plants grown on 757

plates were treated with liquid MS growth medium alone (Control) or MS medium 758

supplemented with 0.5 mM SA for 2, 8, and 24 hours. (–) indicates untreated plants. PR1 759

protein was detected by immunoblot analysis as in (B-C). An independent trial of this 760

experiment showed similar results. 761

762

Figure 6. phb3-3 mutant plants have reduced SA accumulation and PR1 protein levels 763

after infection with Pseudomonas syringae pv tomato DC3000/AvrRpm1. Two-week-764

old plants grown on plates were flooded with Pst/AvrRpm1 bacteria at a concentration of 765

1x106 CFU/mL. Samples were taken at 0, 12, 24, 48, and 72 hours post-infection (hpi). A, 766

The levels of free SA (gray bars) and glycosylated SA (SAG, white bars) are shown; each 767

bar represents the average of three independent experiments. Error bars indicate SEM. 768

Statistical analysis was performed using ANOVA/Fisher’s test. Different letters denote 769

statistically significant differences at p<0.05 for free SA and p<0.001 for SAG. B, The 770

levels of PR1 protein were detected by immunoblot analysis using a PR1 antibody. The 771



35

membrane was stained with Coomassie blue to show similar protein loading. Similar results 772

were seen in two additional experiments. 773

774

Figure 7. phb3-3 mutant plants are more susceptible to infection by Pseudomonas 775

syringae pv. tomato strains DC3000/AvrRpm1 and DC3000/AvrRpt2. A, Two-week-old 776

plate-grown plants were inoculated by flooding the plants with Pst/AvrRpm1 at a 777

concentration of 1x105 CFU/ml. Bacteria were enumerated at 0, 2, and 3 days post-778

inoculation (dpi). B, Three-week-old plants grown in soil were inoculated with Pst/AvrRpt2 779

by infiltration using a concentration of 1x105 CFU/mL. Bacteria were counted at 0 and 3 780

dpi. For A and B, bars represent average values of twelve replicates; error bars indicate 781

SEM. Statistical analysis was performed using ANOVA/Fisher’s test. Different letters 782

denote statistically significant differences at p values as follows: A, 2 dpi (p<0.0001), 3 dpi 783

(p≤0.0005); B, 3 dpi (p<0.0001). C-D, Cell death was evaluated using trypan blue staining 784

in leaf tissue of four-week-old plants grown in soil, 10 h after infiltration with Pst/AvrRpm1 785

or Pst/AvrRpt2 (1x108 CFU/mL). Cell death was scored as occurring if at least 6 blue 786

stained cells were visible in the area of tissue shown and if similar staining occurred 787

throughout the inoculated leaf. Numbers indicate the total number of leaves showing cell 788

death out of the total number scored in three independent experiments. Arrowheads indicate 789

examples of the collapsed, trypan blue-stained cells. Scale bar = 200 μm. These 790

experiments were repeated 3 times with similar results. 791

792

Figure 8. Expression of PHB3 complements phb3-3 mutant phenotypes. A, Phenotype 793

of 3-week-old plants grown in soil. B, Immunodetection of the PHB3-V5 protein using V5 794

antibody, in extracts from phb3-3 and complemented phb3-3/PHB3-V5 #15 and #17 two-795



36

week-old plants grown in soil. C, Leaf cross sections of WT, phb3-3, and complemented 796

phb3-3/PHB3-V5 #15 plants. Scale bar = 100 µm. D, Levels of free SA (gray bars) and 797

glycosylated SA (SAG, white bars) in plants grown in plates, treated with UV-C light for 798

20 min and harvested at 24 hpt (+). Untreated plants were used as controls (–). SA levels 799

are expressed as micrograms per gram of fresh weight (FW). Each bar represents the mean 800

value of three independent experiments; error bars indicate SEM. Statistical analysis was 801

performed using ANOVA/Fisher’s test. Different letters denote statistically significant 802

differences at p<0.02 for free SA and p<0.04 for SAG. E, PR1 protein was detected by 803

immunoblot using PR1 antibody in WT, phb3-3, and phb3-3/PHB3-V5 complemented lines, 804

grown on plates, treated with UV-C light for 20 min, then harvested at 8 and 24 hpt. The 805

panel shows a representative result from three independent experiments. F, Bacterial 806

proliferation was quantified in 3-week-old plants grown in soil at 0 and 3 dpi with 1x105 807

CFU/ml Pst/AvrRpt2. Each bar represents the average of 12 replicates; error bars indicate 808

SEM. Statistical analysis was performed using ANOVA/Fisher’s test. Different letters 809

denote statistically significant differences at p<0.05. This experiment was repeated 3 times 810

with similar results. In B and E, membranes were stained with Coomassie blue to show 811

similar protein loading. 812

813

Figure 9. PHB3 regulates ICS1 protein levels. A, ICS1 transcript levels measured by RT-814

qPCR in two-week-old plants grown in plates and treated with UV-C light for 20 min. 815

Whole seedlings were harvested at 2, 8, and 24 hpt. (–) indicates untreated plants. ICS1 816

transcript levels are relative (R.) to YLS8, which was used as endogenous control. Bars 817

show the mean of 3 biological replicates. Error bars show SEM. Statistical analysis was 818

performed using ANOVA/Fisher’s test. Different letters denote statistically significant 819



37

differences at p<0.05. B, ICS1 was detected by immunoblot analysis with ICS1 antibody in 820

extracts of plants treated as in (A). C, PHB3 does not affect other chloroplast protein levels. 821

The chloroplast proteins Tic110, NOA1, AtpB and LOX2 were detected by immunoblot 822

analysis with specific antibodies. Representative data from three (B) or two (C) 823

independent experiments are shown. Coomassie blue (B) and Ponceau S (C) staining of 824

proteins in the membranes show similar loading. LOX2 immunoblot shows the same 825

membrane as ICS1 blot in B (lower panel). 826

827

828

829

830

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Brodersen P, Malinovsky FG, Hématy K, Newman M-A, Mundy J (2005) The role of Salicylic acid in the induction of cell death inArabidopsis acd11. Plant Physiol 138: 1037–1045


Cao H, Glazebrook J, Clarke JD, Volko S, Dong X (1997) The Arabidopsis NPR1 gene that controls systemic acquired resistanceencodes a novel protein containing ankyrin repeats. Cell 88: 57–63


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Cecchini NM, Steffes K, Schläppi MR, Gifford AN, Greenberg JT (2015) Arabidopsis AZI1 family proteins mediate signal mobilization forsystemic defence priming. Nat Commun 6: 7658


Chen H, Xue L, Chintamanani S, Germain H, Lin H, Cui H, Cai R, Zuo J, Tang X, Li X, Guo H, Zhou JM (2009) ETHYLENE INSENSITIVE3and ETHYLENE INSENSITIVE3-LIKE1 repress SALICYLIC ACID INDUCTION DEFICIENT2 expression to negatively regulate plantinnate immunity in Arabidopsis. Plant Cell 21: 2527–2540


Christians MJ, Larsen PB (2007) Mutational loss of the prohibitin AtPHB3 results in an extreme constitutive ethylene responsephenotype coupled with partial loss of ethylene-inducible gene expression in Arabidopsis seedlings. J Exp Bot 58: 2237–2248


Clarke SM, Cristescu SM, Miersch O, Harren FJM, Wasternack C, Mur LAJ (2009) Jasmonates act with salicylic acid to confer basalthermotolerance in Arabidopsis thaliana. New Phytol 182: 175–187


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http://www.ncbi.nlm.nih.gov/pubmed?term=Abreu ME%2C Munné%2DBosch S%2C Munne S %282009%29 Salicylic acid deficiency in NahG transgenic lines and sid2 mutants increases seed yield in the annual plant Arabidopsis thaliana%2E J Exp Bot 60%3A 1261�??1271&dopt=abstract

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http://scholar.google.com/scholar?as_q=Prohibitin is involved in mitochondrial biogenesis in plants.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ahn&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Aronsson H%2C Jarvis P %282002%29 A simple method for isolating import%2Dcompetent Arabidopsis chloroplasts%2E FEBS Lett 529%3A 215�??220&dopt=abstract

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http://scholar.google.com/scholar?as_q=A simple method for isolating import-competent Arabidopsis chloroplasts.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Aronsson&as_ylo=2002&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Beckers GJM%2C Jaskiewicz M%2C Liu Y%2C Underwood WR%2C He SY%2C Zhang S%2C Conrath U %282009%29 Mitogen%2Dactivated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana%2E Plant Cell 21%3A 944�??953&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Beckers GJM, Jaskiewicz M, Liu Y, Underwood WR, He SY, Zhang S, Conrath U (2009) Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana. Plant Cell 21: 944?953

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http://scholar.google.com/scholar?as_q=Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana.&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=Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Beckers&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

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http://scholar.google.com/scholar?as_q=The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Cao&as_ylo=1997&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Catinot J%2C Buchala A%2C Abou%2DMansour E%2C Métraux JP %282008%29 Salicylic acid production in response to biotic and abiotic stress depends on isochorismate in Nicotiana benthamiana%2E FEBS Lett 582%3A 473�??478&dopt=abstract

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http://scholar.google.com/scholar?as_q=Arabidopsis AZI1 family proteins mediate signal mobilization for systemic defence priming.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Cecchini&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Chen H%2C Xue L%2C Chintamanani S%2C Germain H%2C Lin H%2C Cui H%2C Cai R%2C Zuo J%2C Tang X%2C Li X%2C Guo H%2C Zhou JM %282009%29 ETHYLENE INSENSITIVE3 and ETHYLENE INSENSITIVE3%2DLIKE1 repress SALICYLIC ACID INDUCTION DEFICIENT2 expression to negatively regulate plant innate immunity in Arabidopsis%2E Plant Cell 21%3A 2527�??2540&dopt=abstract

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http://scholar.google.com/scholar?as_q=ETHYLENE INSENSITIVE3 and ETHYLENE INSENSITIVE3-LIKE1 repress SALICYLIC ACID INDUCTION DEFICIENT2 expression to negatively regulate plant innate immunity in Arabidopsis.&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=ETHYLENE INSENSITIVE3 and ETHYLENE INSENSITIVE3-LIKE1 repress SALICYLIC ACID INDUCTION DEFICIENT2 expression to negatively regulate plant innate immunity in Arabidopsis.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Chen&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Christians MJ%2C Larsen PB %282007%29 Mutational loss of the prohibitin AtPHB3 results in an extreme constitutive ethylene response phenotype coupled with partial loss of ethylene%2Dinducible gene expression in Arabidopsis seedlings%2E J Exp Bot 58%3A 2237�??2248&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Mutational loss of the prohibitin AtPHB3 results in an extreme constitutive ethylene response phenotype coupled with partial loss of ethylene-inducible gene expression 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=Mutational loss of the prohibitin AtPHB3 results in an extreme constitutive ethylene response phenotype coupled with partial loss of ethylene-inducible gene expression in Arabidopsis seedlings.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Christians&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Clarke SM%2C Cristescu SM%2C Miersch O%2C Harren FJM%2C Wasternack C%2C Mur LAJ %282009%29 Jasmonates act with salicylic acid to confer basal thermotolerance in Arabidopsis thaliana%2E New Phytol 182%3A 175�??187&dopt=abstract

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Kikuchi S, Hirohashi T, Nakai M (2006) Characterization of the preprotein translocon at the outer envelope membrane of chloroplastsby blue native PAGE. Plant Cell Physiol 47: 363–371


Kim H-S, Desveaux D, Singer AU, Patel P, Sondek J, Dangl JL (2005) The Pseudomonas syringae effector AvrRpt2 cleaves its C-terminally acylated target, RIN4, from Arabidopsis membranes to block RPM1 activation. Proc Natl Acad Sci U S A 102: 6496–6501


Kleffmann T, Russenberger D, Zychlinski A Von, Christopher W, Gruissem W, Baginsky S (2004) The Arabidopsis thaliana chloroplastproteome reveals pathway abundance and novel protein functions. Current Biol 14: 354–362


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http://search.crossref.org/?page=1&rows=2&q=Kang Y, Jelenska J, Cecchini NM, Li Y, Lee MW, Kovar DR, Greenberg JT (2014) HopW1 from Pseudomonas syringae disrupts the actin cytoskeleton to promote virulence in Arabidopsis. PLoS Pathog 10: e1004232

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

http://scholar.google.com/scholar?as_q=HopW1 from Pseudomonas syringae disrupts the actin cytoskeleton to promote virulence in Arabidopsis.&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=HopW1 from Pseudomonas syringae disrupts the actin cytoskeleton to promote virulence in Arabidopsis.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kang&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Karimi M%2C Inzé D%2C Depicker A %282002%29 GATEWAYTM vectors for Agrobacterium%2Dmediated plant transformation%2E Trends Plant Sci 7%3A 193�??195&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Karimi M, Inz� D, Depicker A (2002) GATEWAYTM vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7: 193?195

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

http://scholar.google.com/scholar?as_q=GATEWAYTM vectors for Agrobacterium-mediated plant transformation.&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=Karimi M%2C De Meyer B%2C Hilson P %282005%29 Modular cloning in plant cells%2E Trends Plant Sci 10%3A 103�??105&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Karimi M, De Meyer B, Hilson P (2005) Modular cloning in plant cells. Trends Plant Sci 10: 103?105

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

http://scholar.google.com/scholar?as_q=Modular cloning in plant cells.&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=Modular cloning in plant cells.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Karimi&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Kieselbach T%2C Hagman%2C Andersson B%2C Schröder WP %281998%29 The thylakoid lumen of chloroplasts%2E Isolation and characterization%2E J Biol Chem 273%3A 6710�??6716&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kieselbach T, Hagman, Andersson B, Schr�der WP (1998) The thylakoid lumen of chloroplasts. Isolation and characterization. J Biol Chem 273: 6710?6716

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

http://scholar.google.com/scholar?as_q=The thylakoid lumen of chloroplasts.&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 thylakoid lumen of chloroplasts.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kieselbach&as_ylo=1998&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Kikuchi S%2C Hirohashi T%2C Nakai M %282006%29 Characterization of the preprotein translocon at the outer envelope membrane of chloroplasts by blue native PAGE%2E Plant Cell Physiol 47%3A 363�??371&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kikuchi S, Hirohashi T, Nakai M (2006) Characterization of the preprotein translocon at the outer envelope membrane of chloroplasts by blue native PAGE. Plant Cell Physiol 47: 363?371

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

http://scholar.google.com/scholar?as_q=Characterization of the preprotein translocon at the outer envelope membrane of chloroplasts by blue native PAGE.&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=Characterization of the preprotein translocon at the outer envelope membrane of chloroplasts by blue native PAGE.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kikuchi&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Kim H%2DS%2C Desveaux D%2C Singer AU%2C Patel P%2C Sondek J%2C Dangl JL %282005%29 The Pseudomonas syringae effector AvrRpt2 cleaves its C%2Dterminally acylated target%2C RIN4%2C from Arabidopsis membranes to block RPM1 activation%2E Proc Natl Acad Sci U S A 102%3A 6496�??6501&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kim H-S, Desveaux D, Singer AU, Patel P, Sondek J, Dangl JL (2005) The Pseudomonas syringae effector AvrRpt2 cleaves its C-terminally acylated target, RIN4, from Arabidopsis membranes to block RPM1 activation. Proc Natl Acad Sci U S A 102: 6496?6501

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

http://scholar.google.com/scholar?as_q=The Pseudomonas syringae effector AvrRpt2 cleaves its C-terminally acylated target, RIN4, from Arabidopsis membranes to block RPM1 activation.&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 Pseudomonas syringae effector AvrRpt2 cleaves its C-terminally acylated target, RIN4, from Arabidopsis membranes to block RPM1 activation.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kim&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Kleffmann T%2C Russenberger D%2C Zychlinski A Von%2C Christopher W%2C Gruissem W%2C Baginsky S %282004%29 The Arabidopsis thaliana chloroplast proteome reveals pathway abundance and novel protein functions%2E Current Biol 14%3A 354�??362&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kleffmann T, Russenberger D, Zychlinski A Von, Christopher W, Gruissem W, Baginsky S (2004) The Arabidopsis thaliana chloroplast proteome reveals pathway abundance and novel protein functions. Current Biol 14: 354?362

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

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http://www.ncbi.nlm.nih.gov/pubmed?term=Kubis SE%2C Lilley KS JP %282008%29 Isolation and preparation of chloroplasts from Arabidopsis thaliana plants%2E Methods Mol Biol 245%3A 171�??186&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kubis SE, Lilley KS JP (2008) Isolation and preparation of chloroplasts from Arabidopsis thaliana plants. Methods Mol Biol 245: 171?186

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

http://scholar.google.com/scholar?as_q=Isolation and preparation of chloroplasts from Arabidopsis thaliana plants.&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=Isolation and preparation of chloroplasts from Arabidopsis thaliana plants.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kubis&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Lamppa GK %281995%29%2E In vitro import of proteins into chloroplasts%2E In%3A Maliga P%2C Klessig DF%2C Cashmore AR%2C Gruissem W%2C Varner JE%2C editors%2E Methods in Plant Molecular Biology%2E New York%3A Cold Spring Harbor Laboratory Press%2C pp%2E 141�??171%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Lamppa GK (1995). In vitro import of proteins into chloroplasts. In: Maliga P, Klessig DF, Cashmore AR, Gruissem W, Varner JE, editors. Methods in Plant Molecular Biology. New York: Cold Spring Harbor Laboratory Press, pp. 141?171.

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http://scholar.google.com/scholar?as_q=In vitro import of proteins into chloroplasts.&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=In vitro import of proteins into chloroplasts.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Lamppa&as_ylo=1995&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Lee J%2C Lee H%2C Kim J%2C Lee S%2C Kim H%2C Kim S%2C Hwang I %282011%29 Both the hydrophobicity and a positively charged region flanking the C%2Dterminal region of the transmembrane domain of signal%2Danchored proteins play critical roles in determining their targeting specificity to the endoplasmic reticulum or endosymbiotic organelles in Arabidopsis cells%2E Plant Cell 23%3A 1588�??1607&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Lee MW%2C Lu H%2C Jung HW%2C Greenberg JT %282007%29 A Key Role for the Arabidopsis WIN3 Protein in Disease Resistance Triggered by Pseudomonas syringae that Secrete AvrRpt2%2E Mol Plant%2DMicrobe Interact 20%3A 1192�??1200&dopt=abstract

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Lohmann A, Schöttler MA, Bréhélin C, Kessler F, Bock R, Cahoon EB, Dörmann P (2006) Deficiency in phylloquinone (vitamin K1)methylation affects prenyl quinone distribution, photosystem I abundance, and anthocyanin accumulation in the Arabidopsis AtmenGmutant. J Biol Chem 281: 40461–40472


Lu H (2009) Dissection of salicylic acid-mediated defense signaling networks. Plant Signal Behav 4: 713–717Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Lu H, Rate DN, Song JT, Greenberg JT (2003) ACD6, a novel ankyrin protein, is a regulator and an effector of salicylic acid signaling inthe Arabidopsis defense response. Plant Cell 15: 2408–2420


Macaulay KM, Heath GA, Ciulli A, Murphy AM, Abell C, Carr JP, Smith AG (2017) The biochemical properties of the two Arabidopsisthaliana isochorismate synthases. Biochem J 474: 1579–1590


Mackey D, Iii BFH, Wiig A, Dangl JL, Hill C, Carolina N (2002) RIN4 interacts with Pseudomonas syringae type III effector molecules andis required for RPM1-mediated resistance in Arabidopsis. Cell 108: 743–754


Mandal MK, Chandra-Shekara AC, Jeong R-D, Yu K, Zhu S, Chanda B, Navarre D, Kachroo A, Kachroo P (2012) Oleic acid-dependentmodulation of NITRIC OXIDE ASSOCIATED1 protein levels regulates nitric oxide-mediated defense signaling in Arabidopsis. Plant Cell24: 1654–74


Martínez C, Pons E, Prats G, León J (2004) Salicylic acid regulates flowering time and links defence responses and reproductivedevelopment. Plant J 37: 209–217


Mateo A, Funck D, Mühlenbock P, Kular B, Mullineaux PM, Karpinski S (2006) Controlled levels of salicylic acid are required for optimalphotosynthesis and redox homeostasis. J Exp Bot 57: 1795–1807


Mauch F, Mauch-Mani B, Gaille C, Kull B, Haas D, Reimmann C (2001) Manipulation of salicylate content in Arabidopsis thaliana by theexpression of an engineered bacterial salicylate synthase. Plant J 25: 67–77


Morris K, MacKerness SA, Page T, John CF, Murphy AM, Carr JP, Buchanan-Wollaston V (2000) Salicylic acid has a role in regulatinggene expression during leaf senescence. Plant J 23: 677–685


Nawrath C, Heck S, Parinthawong N, Métraux JP (2002) EDS5, an essential component of salicylic acid–dependent signaling fordisease resistance in Arabidopsis, is a member of the MATE transporter family. Plant Cell 14: 275–286


Nawrath C, Métraux JP (1999) Salicylic acid induction–deficient mutants of arabidopsis express PR-2 and PR-5 and accumulate highlevels of camalexin after pathogen inoculation. Plant Cell 11: 1393–1404

Pubmed: Author and TitleCrossRef: Author and Title


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http://search.crossref.org/?page=1&rows=2&q=Lohmann A, Sch�ttler MA, Br�h�lin C, Kessler F, Bock R, Cahoon EB, D�rmann P (2006) Deficiency in phylloquinone (vitamin K1) methylation affects prenyl quinone distribution, photosystem I abundance, and anthocyanin accumulation in the Arabidopsis AtmenG mutant. J Biol Chem 281: 40461?40472

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http://www.ncbi.nlm.nih.gov/pubmed?term=Lu H%2C Rate DN%2C Song JT%2C Greenberg JT %282003%29 ACD6%2C a novel ankyrin protein%2C is a regulator and an effector of salicylic acid signaling in the Arabidopsis defense response%2E Plant Cell 15%3A 2408�??2420&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Nawrath C%2C Heck S%2C Parinthawong N%2C Métraux JP %282002%29 EDS5%2C an essential component of salicylic acid�??dependent signaling for disease resistance in Arabidopsis%2C is a member of the MATE transporter family%2E Plant Cell 14%3A 275�??286&dopt=abstract

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http://scholar.google.com/scholar?as_q=EDS5, an essential component of salicylic acidâ�?�?dependent signaling for disease resistance in Arabidopsis, is a member of the MATE transporter family.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Nawrath&as_ylo=2002&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Nawrath C%2C Métraux JP %281999%29 Salicylic acid induction�??deficient mutants of arabidopsis express PR%2D2 and PR%2D5 and accumulate high levels of camalexin after pathogen inoculation%2E Plant Cell 11%3A 1393�??1404&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Nawrath C, M�traux JP (1999) Salicylic acid induction?deficient mutants of arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. Plant Cell 11: 1393?1404


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Piechota J, Bereza M, Sokołowska A, Suszyn K, Lech K, Jan H (2015) Unraveling the functions of type II prohibitins in Arabidopsismitochondria. 1: 249–267


Piechota J, Kolodziejczak M, Juszczak I, Sakamoto W, Janska H (2010) Identification and characterization of high molecular weightcomplexes formed by matrix AAA proteases and prohibitins in mitochondria of Arabidopsis thaliana. J Biol Chem 285: 12512–12521


Poulsen C, Verpoorte R (1991) Roles of chorismate mutase, isochorismate synthase and anthranilate synthase in plants.Phytochemistry 30: 377–386


Raskin I, Ehmann A, Melander WR, Meeuse BJ (1987) Salicylic Acid: a natural inducer of heat production in Arum lilies. Science 237:1601–1602



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http://www.ncbi.nlm.nih.gov/pubmed?term=Ogawa D%2C Nakajima N%2C Sano T%2C Tamaoki M%2C Aono M%2C Kubo A%2C Kanna M%2C Ioki M%2C Kamada H%2C Saji H %282005%29 Salicylic acid accumulation under O3 exposure is regulated by ethylene in Tobacco plants%2E Plant Cell Physiol 46%3A 1062�??1072&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Okrent RA%2C Brooks MD%2C Wildermuth MC %282010%29 Arabidopsis GH3%2E12 %28PBS3%29 conjugates amino acids to 4%2Dsubstituted benzoates and is inhibited by salicylate%2E J Biol Chem 284%3A 9742�??9754&dopt=abstract

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http://scholar.google.com/scholar?as_q=Arabidopsis GH3.12 (PBS3) conjugates amino acids to 4-substituted benzoates and is inhibited by salicylate.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Okrent&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Pattanayak GK%2C Venkataramani S%2C Hortensteiner S%2C Kunz L%2C Christ B%2C Moulin M%2C Smith AG%2C Okamoto Y%2C Tamiaki H%2C Sugishima M%2C Greenberg JT %282012%29 ACCELERATED CELL DEATH 2 suppresses mitochondrial oxidative bursts and modulates cell death in Arabidopsis%2E Plant J 69%3A 589�??600&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Pattanayak GK, Venkataramani S, Hortensteiner S, Kunz L, Christ B, Moulin M, Smith AG, Okamoto Y, Tamiaki H, Sugishima M, Greenberg JT (2012) ACCELERATED CELL DEATH 2 suppresses mitochondrial oxidative bursts and modulates cell death in Arabidopsis. Plant J 69: 589?600

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http://scholar.google.com/scholar?as_q=ACCELERATED CELL DEATH 2 suppresses mitochondrial oxidative bursts and modulates cell death in Arabidopsis.&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=ACCELERATED CELL DEATH 2 suppresses mitochondrial oxidative bursts and modulates cell death in Arabidopsis.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Pattanayak&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Pavet V%2C Olmos E%2C Kiddle G%2C Mowla S%2C Kumar S%2C Antoniw J%2C Alvarez E%2C Foyer CH %282005%29 Ascorbic acid deficiency activates cell death and disease resistance responses in Arabidopsis%2E Plant Physiol 139%3A 1291�??1303&dopt=abstract

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http://scholar.google.com/scholar?as_q=Ascorbic acid deficiency activates cell death and disease resistance responses in Arabidopsis.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Pavet&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Piechota J%2C Bereza M%2C Soko�?owska A%2C Suszyn K%2C Lech K%2C Jan H %282015%29 Unraveling the functions of type II �?? prohibitins in Arabidopsis mitochondria%2E 1%3A 249�??267&dopt=abstract

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http://scholar.google.com/scholar?as_q=Unraveling the functions of type II â�?�? prohibitins in Arabidopsis mitochondria.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Piechota&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Piechota J%2C Kolodziejczak M%2C Juszczak I%2C Sakamoto W%2C Janska H %282010%29 Identification and characterization of high molecular weight complexes formed by matrix AAA proteases and prohibitins in mitochondria of Arabidopsis thaliana%2E J Biol Chem 285%3A 12512�??12521&dopt=abstract

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http://scholar.google.com/scholar?as_q=Identification and characterization of high molecular weight complexes formed by matrix AAA proteases and prohibitins in mitochondria of Arabidopsis thaliana.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Piechota&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Poulsen C%2C Verpoorte R %281991%29 Roles of chorismate mutase%2C isochorismate synthase and anthranilate synthase in plants%2E Phytochemistry 30%3A 377�??386&dopt=abstract

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http://scholar.google.com/scholar?as_q=Roles of chorismate mutase, isochorismate synthase and anthranilate synthase in plants.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Poulsen&as_ylo=1991&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Raskin I%2C Ehmann A%2C Melander WR%2C Meeuse BJ %281987%29 Salicylic Acid%3A a natural inducer of heat production in Arum lilies%2E Science 237%3A 1601�??1602&dopt=abstract

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Roston RL, Wang K, Kuhn LA, Benning C (2014) Structural determinants allowing transferase activity in SENSITIVE TO FREEZING 2,classified as a family I glycosyl hydrolase. J Biol Chem 289: 26089–26106


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Shapiro AD, Zhang C (2001) The role of NDR1 in avirulence gene-directed signaling and control of programmed cell death inArabidopsis. Plant Physiol 127: 1089–1101


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http://www.ncbi.nlm.nih.gov/pubmed?term=Roston RL%2C Wang K%2C Kuhn LA%2C Benning C %282014%29 Structural determinants allowing transferase activity in SENSITIVE TO FREEZING 2%2C classified as a family I glycosyl hydrolase%2E J Biol Chem 289%3A 26089�??26106&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Roston RL, Wang K, Kuhn LA, Benning C (2014) Structural determinants allowing transferase activity in SENSITIVE TO FREEZING 2, classified as a family I glycosyl hydrolase. J Biol Chem 289: 26089?26106

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

http://scholar.google.com/scholar?as_q=Structural determinants allowing transferase activity in SENSITIVE TO FREEZING 2, classified as a family I glycosyl hydrolase.&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=Structural determinants allowing transferase activity in SENSITIVE TO FREEZING 2, classified as a family I glycosyl hydrolase.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Roston&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Schmid J%2C Amrhein N %281995%29 Molecular organization of the shikimate pathway in higher plants%2E Phytochemistry 39%3A 737�??749&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Schmid J, Amrhein N (1995) Molecular organization of the shikimate pathway in higher plants. Phytochemistry 39: 737?749

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

http://scholar.google.com/scholar?as_q=Molecular organization of the shikimate pathway in higher plants.&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=Molecular organization of the shikimate pathway in higher plants.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Schmid&as_ylo=1995&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Serrano M%2C Wang B%2C Aryal B%2C Garcion C%2C Abou%2Dmansour E%2C Heck S%2C Mauch F%2C Nawrath C%2C Métraux JP %282013%29 Export of salicylic acid from the chloroplast requires the multidrug and toxin extrusion%2Dlike transporter EDS5%2E Plant Physiol 162%3A 1815�??1821&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Serrano M, Wang B, Aryal B, Garcion C, Abou-mansour E, Heck S, Mauch F, Nawrath C, M�traux JP (2013) Export of salicylic acid from the chloroplast requires the multidrug and toxin extrusion-like transporter EDS5. Plant Physiol 162: 1815?1821

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

http://scholar.google.com/scholar?as_q=Export of salicylic acid from the chloroplast requires the multidrug and toxin extrusion-like transporter EDS5.&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=Export of salicylic acid from the chloroplast requires the multidrug and toxin extrusion-like transporter EDS5.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Serrano&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Shapiro AD%2C Zhang C %282001%29 The role of NDR1 in avirulence gene%2Ddirected signaling and control of programmed cell death in Arabidopsis%2E Plant Physiol 127%3A 1089�??1101&dopt=abstract

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http://scholar.google.com/scholar?as_q=Chloroplast envelope localization of EDS5, an essential factor for salicylic acid biosynthesis in Arabidopsis thaliana.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yamasaki&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

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differentially shaped the regulation of isochorismate synthase in Populus and Arabidopsis. Proc Natl Acad Sci U S A 106: 22020–22025Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Zhang K, Halitschke R, Yin C, Liu C, Gan S (2013) Salicylic acid 3-hydroxylase regulates Arabidopsis leaf longevity by mediating salicylicacid catabolism. Proc Natl Acad Sci U S A 36: 14807–14812


Zhang X, Henriques R, Lin S-S, Niu Q-W, Chua N-H (2006) Agrobacterium-mediated transformation of Arabidopsis thaliana using thefloral dip method. Nat Protoc 1: 641–646


Zhang Y, Xu S, Ding P, Wang D, Cheng YT, He J, Gao M, Xu F, Li Y, Zhu Z, et al (2010) Control of salicylic acid synthesis and systemicacquired resistance by two members of a plant-specific family of transcription factors. Proc Natl Acad Sci U S A 107: 18220–18225


Zhang Y, Zhao L, Zhao J, Li Y, Wang J, Guo R, Gan S, Liu C-J, Zhang K (2017) S5H/DMR6 encodes a salicylic acid 5-hydroxylase thatfine-tunes salicylic acid homeostasis. Plant Physiol 175: 1082–1093


Zhang Z, Shrestha J, Tateda C, Greenberg JT (2014) Salicylic acid signaling controls the maturation and localization of the arabidopsisdefense protein ACCELERATED CELL DEATH6. Mol Plant 7: 1365–1383


Zheng X-Y, Spivey NW, Zeng W, Liu P-P, Fu ZQ, Klessig DF, He SY, Dong X (2012) Coronatine promotes Pseudomonas syringaevirulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation. Cell Host Microbe 11: 587–596


Zheng X-Y, Zhou M, Yoo H, Pruneda-Paz JL, Spivey NW, Kay SA, Dong X (2015) Spatial and temporal regulation of biosynthesis of theplant immune signal salicylic acid. Proc Natl Acad Sci U S A 112: 9166–9173



http://www.ncbi.nlm.nih.gov/pubmed?term=Yuan Y%2C Chung J%2DD%2C Fu X%2C Johnson VE%2C Ranjan P%2C Booth SL%2C Harding SA%2C Tsai C%2DJ %282009%29 Alternative splicing and gene duplication differentially shaped the regulation of isochorismate synthase in Populus and Arabidopsis%2E Proc Natl Acad Sci U S A 106%3A 22020�??22025&dopt=abstract

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

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http://scholar.google.com/scholar?as_q=Alternative splicing and gene duplication differentially shaped the regulation of isochorismate synthase in Populus and Arabidopsis.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yuan&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhang K%2C Halitschke R%2C Yin C%2C Liu C%2C Gan S %282013%29 Salicylic acid 3%2Dhydroxylase regulates Arabidopsis leaf longevity by mediating salicylic acid catabolism%2E Proc Natl Acad Sci U S A 36%3A 14807�??14812&dopt=abstract

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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=Salicylic acid 3-hydroxylase regulates Arabidopsis leaf longevity by mediating salicylic acid catabolism.&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=Salicylic acid 3-hydroxylase regulates Arabidopsis leaf longevity by mediating salicylic acid catabolism.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhang X%2C Henriques R%2C Lin S%2DS%2C Niu Q%2DW%2C Chua N%2DH %282006%29 Agrobacterium%2Dmediated transformation of Arabidopsis thaliana using the floral dip method%2E Nat Protoc 1%3A 641�??646&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhang X, Henriques R, Lin S-S, Niu Q-W, Chua N-H (2006) Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nat Protoc 1: 641?646


http://scholar.google.com/scholar?as_q=Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method.&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=Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhang Y%2C Xu S%2C Ding P%2C Wang D%2C Cheng YT%2C He J%2C Gao M%2C Xu F%2C Li Y%2C Zhu Z%2C et al %282010%29 Control of salicylic acid synthesis and systemic acquired resistance by two members of a plant%2Dspecific family of transcription factors%2E Proc Natl Acad Sci U S A 107%3A 18220�??18225&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhang Y, Xu S, Ding P, Wang D, Cheng YT, He J, Gao M, Xu F, Li Y, Zhu Z, et al (2010) Control of salicylic acid synthesis and systemic acquired resistance by two members of a plant-specific family of transcription factors. Proc Natl Acad Sci U S A 107: 18220?18225


http://scholar.google.com/scholar?as_q=Control of salicylic acid synthesis and systemic acquired resistance by two members of a plant-specific family of transcription factors.&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=Control of salicylic acid synthesis and systemic acquired resistance by two members of a plant-specific family of transcription factors.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhang Y%2C Zhao L%2C Zhao J%2C Li Y%2C Wang J%2C Guo R%2C Gan S%2C Liu C%2DJ%2C Zhang K %282017%29 S5H%2FDMR6 encodes a salicylic acid 5%2Dhydroxylase that fine%2Dtunes salicylic acid homeostasis%2E Plant Physiol 175%3A 1082�??1093&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhang Y, Zhao L, Zhao J, Li Y, Wang J, Guo R, Gan S, Liu C-J, Zhang K (2017) S5H/DMR6 encodes a salicylic acid 5-hydroxylase that fine-tunes salicylic acid homeostasis. Plant Physiol 175: 1082?1093


http://scholar.google.com/scholar?as_q=S5H/DMR6 encodes a salicylic acid 5-hydroxylase that fine-tunes salicylic acid homeostasis.&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=S5H/DMR6 encodes a salicylic acid 5-hydroxylase that fine-tunes salicylic acid homeostasis.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhang Z%2C Shrestha J%2C Tateda C%2C Greenberg JT %282014%29 Salicylic acid signaling controls the maturation and localization of the arabidopsis defense protein ACCELERATED CELL DEATH6%2E Mol Plant 7%3A 1365�??1383&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhang Z, Shrestha J, Tateda C, Greenberg JT (2014) Salicylic acid signaling controls the maturation and localization of the arabidopsis defense protein ACCELERATED CELL DEATH6. Mol Plant 7: 1365?1383


http://scholar.google.com/scholar?as_q=Salicylic acid signaling controls the maturation and localization of the arabidopsis defense protein ACCELERATED CELL DEATH6.&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=Salicylic acid signaling controls the maturation and localization of the arabidopsis defense protein ACCELERATED CELL DEATH6.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zheng X%2DY%2C Spivey NW%2C Zeng W%2C Liu P%2DP%2C Fu ZQ%2C Klessig DF%2C He SY%2C Dong X %282012%29 Coronatine promotes Pseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation%2E Cell Host Microbe 11%3A 587�??596&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zheng X-Y, Spivey NW, Zeng W, Liu P-P, Fu ZQ, Klessig DF, He SY, Dong X (2012) Coronatine promotes Pseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation. Cell Host Microbe 11: 587?596

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=Coronatine promotes Pseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation.&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=Coronatine promotes Pseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zheng&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zheng X%2DY%2C Zhou M%2C Yoo H%2C Pruneda%2DPaz JL%2C Spivey NW%2C Kay SA%2C Dong X %282015%29 Spatial and temporal regulation of biosynthesis of the plant immune signal salicylic acid%2E Proc Natl Acad Sci U S A 112%3A 9166�??9173&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zheng X-Y, Zhou M, Yoo H, Pruneda-Paz JL, Spivey NW, Kay SA, Dong X (2015) Spatial and temporal regulation of biosynthesis of the plant immune signal salicylic acid. Proc Natl Acad Sci U S A 112: 9166?9173

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=Spatial and temporal regulation of biosynthesis of the plant immune signal salicylic acid.&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=Spatial and temporal regulation of biosynthesis of the plant immune signal salicylic acid.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zheng&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1


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PROHIBITIN 3 forms complexes with ISOCHORISMATE …110 ISOCHORISMATE SYNTHASE 1 (ICS1), a plastid-localized enzyme (Strawn et al., 111 2007). The second step is the conversion of IC