short title: medea attenuates pathogen defense in arabidopsis … · 16 jawaharlal nehru university...

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Short title: MEDEA attenuates pathogen defense in Arabidopsis 1

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Corresponding Author: Ashis Kumar Nandi, School of Life Science, Jawaharlal Nehru 3

University, New Delhi -110067, India. E-mail: [email protected], Phone: +91-11-4

26704152 5

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Article Title: 7

The polycomb-group repressor MEDEA attenuates pathogen defense 8

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Authors: 10

Shweta Roy1, Priya Gupta1, Mohit Pradip Rajabhoj2, Ravi Maruthachalam2, and Ashis Kumar 11

Nandi1 12

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Affiliation: 14 1415, School of life Sciences 15

Jawaharlal Nehru University 16

New Delhi -110067, India 17 2Indian Institute of Science Education and Research, Thiruvananthapuram 18

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One sentence summary: 20

Pathogen inoculation in Arabidopsis thaliana activates the expression of the imprinted gene 21

MEDEA, a component of the PRC2 complex, which hinders defense against pathogens. 22

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Author contributions: A.K.N. conceptualized and designed most of the experiments; S.R. 24

and R.M. designed some of the experiments; S.R. performed most of the experiments and 25

analyzed the data; P.G. and M.P.R. performed some of the experiments, S.R. and A.K.N. 26

wrote the manuscript, which has been further modified and approved by all the authors. 27

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Funding Information: This work is supported by the Science & Engineering Research 29

Board project (SERB/SR/SO/PS/150/2012) to A.K.N.; the CSIR fellowship to S.R., and the 30

PG.IISERTVM fellowship (MHRD, Govt. of India) to M.P.R. R.M. acknowledges the 31

funding support from the DBT Ramalingaswami Fellowship, the Dupont Young Professor 32

Grant and IISER-TVM intramural funds. 33

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Plant Physiology Preview. Published on June 28, 2018, as DOI:10.1104/pp.17.01579

Copyright 2018 by the American Society of Plant Biologists

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Corresponding author email: [email protected] 35

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Abstract 37

Plants recruit positive and negative regulators for fine tuning the balance between growth and 38

development. Negative regulators of pathogen defense generally modulate defense hormone 39

biosynthesis and signaling. Here, we report a mechanism for attenuation of the defense 40

response in Arabidopsis thaliana, which is mediated by the polycomb-group repressor 41

MEDEA (MEA). Our results showed that pathogen inoculation or exogenous application of 42

salicylic acid, methyl jasmonate, or the bacterial 22-amino acid-domain of flagellin peptide 43

induces the expression of MEA. MEA expression was higher when plants were inoculated 44

with the avirulent strain of Pseudomonas syringae pv. tomato (Pst) carrying the AvrRpt2 45

effector (Pst-AvrRpt2) compared to the virulent Pst strain. MEA remains suppressed during 46

the vegetative phase via DNA and histone (H3K27) methylation, and only the maternal copy 47

is expressed in the female gametophyte and endosperm via histone and DNA demethylation. 48

In contrast, Pst-AvrRpt2 induces high levels of MEA expression via hyper-accumulation of 49

H3K4me3 at the MEA locus. MEA over-expressing transgenic plants are susceptible to the 50

fungal pathogen Botrytis cinerea and bacterial pathogens Pst and Pst-AvrRpt2, whereas mea 51

mutant plants are more resistant to these pathogens. AvrRpt2-mediated immunity requires the 52

function of RESISTANCE TO P. SYRINGAE 2 (RPS2) in Arabidopsis. Using 53

transcriptional analysis and chromatin immunoprecipitation, we established that MEA 54

directly targets RPS2 and suppresses its transcription. We screened an Arabidopsis cDNA 55

library using MEA as the bait in a yeast2-hybrid assay and identified DROUGHT- 56

INDUCED 19 (DI19), a transcription factor that interacts with MEA and recruits it at the 57

RPS2 promoter. The results identified a previously unknown mechanism of defense response 58

attenuation in plants. 59

60

Introduction 61

Plants are capable of defending themselves from pathogen attack with the help of well 62

elaborated immune machinery. Plants possess both constitutive and inducible immune 63

systems (Spoel and Dong, 2012). By virtue of its cellular content, plants impose a 64

constitutive barrier to many pathogens. The inducible immune system is activated upon the 65

recognition of pathogens. Recognition of conserved pathogen-/microbe-associated molecular 66



3

patterns (PAMPs) activates pattern-triggered immunity (PTI). Pathogen-derived molecules 67

such as bacterial flagellin, elongation factor-TU (EF-TU) lipo-oligosaccharides, fungal cell 68

wall chitin, glucan and glycoproteins of oomycetes are sources of patterns for activating 69

PTI(Zhang and Zhou, 2010). Successful pathogens release effector molecules to suppress 70

PTI. During the co-evolution of plants and microbes, plants often evolved recognition 71

systems for certain effector molecules to activate strong immune response (effector-triggered 72

immunity; ETI) that renders the pathogen incompatible with the host (Jones and Dangl, 2006; 73

Spoel and Dong, 2012). For ETI activation, the effectors (avirulent factors) function in 74

combination with resistance (R) genes of the host. In the absence of cognate R genes, the 75

avirulent factors contribute to effector-triggered susceptibility (Jones and Dangl, 2006; Kim 76

et al., 2009; Deslandes and Rivas, 2012). Both PTI and ETI involve the activation of 77

mitogen-activated protein kinase (MAPK) signaling, the accumulation of reactive oxygen 78

species and hormones, and the biosynthesis of antimicrobial compounds such as phytoalexins 79

and peptides (Zhang and Zhou, 2010). ETI is a magnified form of PTI, which results in the 80

activation of defense responses to a much higher level (Jones and Dangl, 2006). Additionally, 81

ETI is often associated with the hypersensitive response (HR), a rapid programmed cell death 82

at the pathogen invasion site (Morel and Dangl, 1997). HR helps in restricting the growth of 83

pathogens and signaling for systemic acquired resistance. Plant hormones such as salicylic 84

acid (SA), ethylene (ET) and jasmonic acid (JA) play central roles in activating both PTI and 85

ETI (Robert-Seilaniantz et al., 2011; Pieterse et al., 2012). 86

Plants activate defense at the cost of growth and development (Heil and Baldwin, 87

2002; Tian et al., 2003; Huot et al., 2014). With limited resources plants must balance the 88

trade-off between growth and defense. Signaling-crosstalk among plant hormones plays 89

fundamental roles in maintaining this balance. Hormones like auxin, gibberellins, cytokinins, 90

brassinosteroid, and abscisic acid promote growth while limiting the defense output (Denance 91

et al., 2013; Huot et al., 2014). These hormones are implicated in functioning as antagonists 92

to defense signaling activated by SA or ET/JA pathways. In addition, SA- or ET/JA-mediated 93

defense responses are also regulated by proteins that limit the biosynthesis of hormones and 94

signaling pathways (Frye et al., 2001; Jirage et al., 2001; Shah et al., 2001; Journot-Catalino 95

et al., 2006; Zhang et al., 2006b; Swain et al., 2011; Giri et al., 2017). Here we report a 96

mechanism of attenuation of the immune response mediated by a polycomb group (PcG) 97

repressor protein MEDEA (MEA). PcG proteins regulate gene expression by chromatin 98

modification. These modifications lead to stable transcription silencing which can be 99



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inherited through many mitotic cell divisions (Margueron and Reinberg, 2011; Derkacheva 100

and Hennig, 2014; Grossniklaus and Paro, 2014). PcG proteins function as large protein 101

complexes. Plants contain two major PcG protein complexes, Polycomb Repressive Complex 102

1 (PRC1) and PRC2. Both PRC1 and PRC2 complexes work together for stable 103

transcriptional silencing of target genes. PRC2 methylates H3 at lysine 27 to induce 104

epigenetic silencing, whereas PRC1 identifies and binds to these modifications to induce 105

structural changes in chromatin (Kohler and Hennig, 2010; Kalb et al., 2014). MEA belongs 106

to PRC2 and has a SET domain for methyltransferase activity (Grossniklaus et al., 1998).Our 107

results show that pathogen inoculation enhances MEA expression, and enhanced MEA 108

expression limits the growth of pathogens. 109

This observation is important because the expression of MEAis tightly controlled by 110

developmental cues. MEA is an imprinted gene, for which only the maternal copy expresses 111

in the female gametophyte and endosperm (Grossniklaus et al., 1998; Kinoshita et al., 1999). 112

MEA remains repressed throughout the vegetative stage and in floral buds; its mRNA starts 113

appearing in unpollinated siliques having female gametophytes and continues to express until 114

seed maturation. Our results identified a mechanism of MEA activation during pathogenesis, 115

i.e. accumulation of H3K4me3 at the MEA locus, which is distinct from its developmental 116

activation. 117

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5

Results 119

MEA expression is derepressed upon activation of the defense response 120

Though MEA is epigenetically silenced throughout the vegetative phase, we observed its 121

transcript abundance while analysing pathogen-induced transcriptome profiles generated in 122

our laboratory and by others (Lewis et al., 2015). To experimentally validate this observation, 123

we treated wild-type (WT) Arabidopsis (Col-0) leaves with the virulent pathogen P. Syringae 124

pv.tomato DC3000 (Pst) and an avirulent strain of Pst that carried the AvrRpt2 effector (Pst-125

AvrRpt2) and monitored MEA transcript accumulation by reverse transcription quantitative 126

PCR (RT-qPCR). We detected a high level of MEA transcripts within 6 hours of Pst-AvrRpt2 127

inoculation, which further increased until 12-24 hours post-inoculation (hpi; Figure1A). The 128

virulent pathogen also enhanced MEA expression but to a lower level than the avirulent 129

pathogen in the early hours (Figure 1A). However, MEA expression induced by the virulent 130

pathogen was enhanced in the late hours. The results suggested an association of MEA 131

expression with defense response activation. The observation was further validated by the 132

MEA promoter activity and by analysing MEA expression after induction of the defense 133

response by chemicals. MEA promoter-driven β-glucuronidase (GUS) reporter expression 134

(MEA:GUS), which was barely detectable in mock-inoculated leaves of Arabidopsis, was 135

significantly enhanced after inoculating with Pst-AvrRpt2 (Figure 1B). Induction of defense 136

by salicylic acid (Figure 1C), flg22 (Supplemental Figure S1) or methyl jasmonate (MeJA) 137

(Figure 1D) also induced MEA expression in Arabidopsis leaves. The other members of the 138

transcriptional repressor complex in which MEA belongs, include MULTICOPY 139

SUPPRESSOR OF IRA 1 (MSI1) and FERTILIZATION-INDEPENDENT ENDOSPERM 140

(FIE) (Kohler et al., 2003). However, pathogen (Pst-AvrRpt2) inoculation failed to induce 141

MSI1 or FIE significantly (Supplemental Figure S2A and B). Thus, defense activation 142

specifically induced MEA of the PcG core complex. These results demonstrated that 143

activation of the defense response overrides silencing of MEA in the vegetative tissue. 144

Homozygous mea-6 mutant plants are resistant to virulent and avirulent bacterial 145 pathogens 146

Loss-of-function mutants of MEA are embryonic lethal (Grossniklaus et al., 1998) and thus, it 147

is difficult to obtain homozygous mea mutants by conventional diploid genetic methods. 148

However, the female gameotphyte lethal mea mutant allele can normally be transmitted 149

through the male gamete/gametophyte (pollen). Therefore, by exploiting a haploid genetics 150



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approach it is possible to obtain mea haploid progeny by producing paternal haploids (Ravi et 151

al., 2014). To generate the mea-6 homozygous mutant (C24 ecotype), we crossed 152

heterozygous MEA/mea-6 plants that harbor a point mutation at the MEA locus (Guitton et 153

al., 2004) to the haploid inducer GFP-tailswap line as the female parent (Ravi et al., 2014). 154

MEA functions in seed development by regulating endosperm development. In the case of 155

seeds with a haploid embryo carrying the mutant allele of MEA, the endosperm receives two 156

functional copies of MEA via the haploid inducer female parent. A fraction of the resultant F1 157



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seeds are viable and develop into haploid plants and subsequently into homozygous mea-6 158

diploids (doubled haploids). A majority of seeds from the doubled haploid mea-6/mea-6 159

plants were dead but a fraction (213/676) were viable and among the viable seeds around 160

30% (78/213 seeds) were late germinating (upto a week delay) in contrast to WT seedlings 161

(Supplemental Figure S3A, B). These late germinating seedlings show aberrant phenotypes 162

during early vegetative growth until 2-3 weeks post-germination as shown in Supplemental 163

Figure S3C and D. However, these plants recover later and regain normal morphology prior 164



8

to bolting. Only WT looking mea-6/mea-6 plants as shown in Supplemental Figure S3E were 165

used for pathogen inoculation experiments. To investigate the possible role of MEA in disease 166

defense we studied pathogen growth and defense responses in the mea-6 homozygous mutant 167

and wild type (WT) C24 plants. Compared to WT plants, mea-6 mutants showed a higher 168

level of resistance against the virulent strain of Pst (Figure 2A) and the avirulent strain of Pst 169

carrying the AvrRpt2 effector (Pst-AvrRpt2) (Figure 2B). Lower bacterial loads in the mea-6 170

mutant also resulted in a reduced level of disease symptoms in these plants. Hyper-resistance 171



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of the mea-6 mutant was supported by enhanced expression of PATHOGENESIS-RELATED 172

GENE 1 (PR1) in these plants compared to the corresponding WT plants (Figure 2C and D). 173

We also observed higher SA accumulation in both Pst and Pst-AvrRpt2 inoculated leaves of 174

the mea-6 mutant than in WT plants (Figure 2E). Also, mea-6 mutants showed enhanced HR-175

associated cell death (Figure 2F) and H2O2 accumulation (Figure 2G) after Pst-AvrRpt2 176

inoculation. The HR as measured by ion-leakage was significantly more in mea-6 mutants 177

compared to WT plants upon Pst-AvrRpt2 inoculation (Figure 2H). The results suggested that 178

MEA function may be associated with the susceptibility towards pathogens. 179

180

Enhanced MEA expression supports growth of pathogens 181

To further investigate the consequence of enhanced MEA expression upon pathogenesis 182

(Figure 1), we generated multiple independent transgenic Arabidopsis lines (in the Col-0 183

background) constitutively expressing MEA (Supplemental Figure S4), under the Cauliflower 184

mosaic virus 35S promoter (35S:MEA). The 35S:MEA transgenic plants were 185

morphologically normal like WT plants (Supplemental Figure S4C). To examine whether 186

constitutive MEA expression affects embryo development we observed the developing 187

35S:MEA embryos. We did not find any defective embryos in 40 siliques randomly taken 188

from three different 35S:MEA lines (Supplemental Figure S5). We used MEA/mea 189

(CS876294; ABRC) plants as a control for this experiment, and as expected (Grossniklaus et 190

al., 1998) found half of the embryos were aborted in these plants (Supplemental Figure S5). 191

Regarding defense against pathogens, we observed enhanced bacterial and fungal growth in 192

MEA over-expression plants. The MEA over-expression plants supported higher Pst growth 193

than WT plants (Figure 3A), suggesting reduced immunity in these plants. This observation 194

was further supported by the reduced pathogen-induced PR1 expression (Figure 3B) and SA 195

accumulation (Figure 3C, D) in the 35S:MEA plants compared to WT plants. To investigate 196

the possible consequence of elevated MEA expression on ETI, we monitored the growth of 197

Pst-AvrRpt2 in 35S:MEA and WT plants. As a control we used non-expresser of PR genes1 198

(npr1-1), a susceptible mutant of Arabidopsis (Cao et al., 1994). We observed higher 199

bacterial load in npr1-1 and 35S:MEA plants than WT plants (Figure 3E and Supplemental 200

Figure S6). The reduced resistance in 35S:MEA plants was also associated with reduced PR1 201

transcript accumulation (Figure 3F). Similarly, the HR as measured by ion-leakage was 202

significantly reduced in the 35S:MEA plants compared to WT plants upon Pst-AvrRpt2 203

inoculation (Figure 3G). The reduced level of HR in the MEA over-expressing plants was in 204



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agreement with the reduced resistance against Pst-AvrRpt2. In addition, the MEA over-205

expression plants showed a much higher level of disease symptoms than WT plants when 206



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inoculated with the necrotrophic pathogen Botrytis cinerea (Figure 3H). Resistance to 207

necrotrophic pathogens is associated with ET/JA signaling. In agreement with the loss-of-208

resistance phenotype, the MEA over-expression plants also showed reduced PLANT 209

DEFENSIN 1.2 (PDF1.2) expression compared to WT plants upon exogenous application of 210

MeJA (Figure 3I). 211

The results described above showed that activation of the defense response enhances 212

MEA expression and enhanced MEA expression attenuates the defense response. Thus, MEA 213

may function as a negative feedback regulator of defense in Arabidopsis. Since MEA 214

expression was induced to a very high level upon Pst-AvrRpt2 inoculation (Figure 1A), we 215

investigated the mechanism and consequence of MEA expression using this pathogen. 216

217

Pathogenesis-induced MEA expression is associated with altered methylated histone 218 occupancy at the MEA locus 219

Silencing of MEA is mediated by methylation of DNA and di- and tri-methylation of histone 220

3 at lysine 27 (H3K27me2/H3K27me3) (Baubec and Mittelsten Scheid, 2006; Gehring et al., 221

2006; Jullien et al., 2006). Two distinct mechanisms are in place for activation of the 222

maternal MEA allele in the female gametophyte and endosperm, and repression of the 223

paternal allele in the sperm cell and endosperm (Baubec and Mittelsten Scheid, 2006; 224

Gehring et al., 2006). The PcG repressor complex, involving MEA, is responsible for H3K27 225

methylation and suppression of MEA in vegetative tissue and suppression of the paternal 226

allele in endosperm (Gehring et al., 2006). Activation of the maternal MEA allele in the 227

endosperm is mediated by DEMETER (DME) that removes cytosine (C) methylation 228

(Gehring et al., 2006). HpaII cleaves at unmethylated CCGG contexts in DNA but not when 229

the central C is methylated (Yaish et al., 2014). We designed a pair of primers for amplifying 230

260 bp of the MEA promoter that covers the potential methylation sites (Figure 4A). An 231

HpaII-digested genomic DNA template would amplify that 260 bp region only when not 232

cleaved (i.e, methylated). Contrary to our expectation, we did not observe any reduction in 233

the level of methylation at the MEA locus upon pathogen inoculation (Figure 4B). We used 234

another restriction enzyme, McrBc for which methylation at any two C residues preceded by 235

a purine (A or G; PumC) within 40 to 3000 bp of the recognition site generates a restriction 236

site (Gast et al., 1997; Stewart et al., 2000). Thus, the McrBc enzyme can detect methylation 237

over a larger region of the DNA. We also did not observe any significant difference in the 238



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level of PCR amplicons between pathogen- and mock-inoculated samples (Figure 4C), 239



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suggesting no change in DNA methylation at theMEA promoter after Pst-AvrRpt2 240

inoculation. The results ruled out the possibility of MEA activation through DNA 241

demethylation. 242

To investigate the possible change in the occupancy of methylated H3K27 at theMEA 243

locus, we performed a chromatin immuno-precipitation (ChIP) assay by using chromatins 244

from mock, Pst and Pst-AvrRpt2 inoculated samples with an anti-H3K27me3 antibody. We 245

found a significant reduction in H3K27me3 occupancy at three different regions of theMEA 246

locus (Figure 4A) upon Pst or Pst-AvrRpt2 inoculation (Figure 4D-F). In addition to removal 247

of H3K27 methylation, enrichment of H3K4me3 also activates transcription. Thus, we also 248

performed a ChIP assay by using the anti-H3K4me3 antibody. In agreement with the 249

increased expression of MEA, we observed enhanced occupancy of H3K4me3 in regions of 250

the MEA locus, especially after Pst-AvrRpt2 inoculation (Figure 4G-J). Compared to mock-251

treated samples, Pst-inoculated samples showed enhanced occupancy of H3K4me3 in area 3, 252

which is about 1kb downstream of the transcription start site (Figure 4I). However, Pst-253

AvrRpt2 inoculation resulted in enhanced occupancy of H3K4me3 in all the regions tested. 254

As positive controls of our ChIP experiment we monitored the occupancy of H3K27me3 and 255

H3K4me3 in FLOWERING LOCUS T (FT) and ACTIN2 (ACT2) loci respectively, which 256

were known to accumulate these modified histones (Saleh et al., 2008). Both FT and ACT2 257

loci showed predicted enrichment of modified histones (Supplemental Figure S7). The results 258

suggested that pathogen-induced MEA expression is associated with the decrease of 259

H3K27me3 and increase of H3K4me3 at the MEA locus, especially after inoculation with the 260

avirulent pathogen Pst-AvrRpt2. 261

262

High-level MEA induction by Pst-AvrRpt2 requires RPS2 function 263

The results described above (Figure 1A) showed that inoculation with Pst-AvrRpt2 results in 264

high-level expression of MEA, compared to inoculation with the virulent pathogen. Pst-265

AvrRpt2 inoculation activates ETI in aRPS2-dependent manner (Kunkel et al., 1993; Bent et 266

al., 1994; Guttman and Greenberg, 2001; Mackey et al., 2003; Belkhadir et al., 2004; Lim 267

and Kunkel, 2004, 2005; Chen et al., 2007). To investigate whether RPS2 function is required 268

for MEA activation we inoculated WT and rps2 mutants with Pst-AvrRpt2 and monitored 269

MEA transcript accumulation. We observed Pst-AvrRpt2-induced high-level MEA expression 270

in the WT background but not in rps2 mutant plants (Figure 5). The level of MEA induction 271



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in the rps2 mutant was comparable to that of Pst-induced expression in WT plants. Thus, 272

RPS2 function, which is required for AvrRpt2 effector-mediated ETI, is also required for Pst-273

AvrRpt2-mediated induction of MEA expression. 274

275

RPS2 is a target of MEA for transcriptional suppression 276

Our result showed that Pst-AvrRpt2 inoculation enhances MEA expression in a RPS2-277

dependenet manner (Figure 5) and MEA expression suppressed RPS2-medited ETI (Figure 278

3E-G). Thus, there is a feedback inhibition of the defense response mediated by MEA. To 279

investigate whether MEA expression modulates RPS2 expression, we monitored its mRNA 280

accumulation in WT and 35S:MEA plants. Basal, as well as Pst-AvrRpt2-induced RPS2 281

expression was suppressed in 35S:MEA plants (Figure 6A, 6B), suggesting that MEA 282

negatively regulates RPS2 expression. This was further validated in mea-6 mutants, in which 283

both constitutive and pathogen-induced RPS2 expression was higher than in WT plants 284

(Figure 6C). We further demonstrated that co-expression of MEA suppressed RPS2:GUS but 285

not 35S:GUS expression (Figure 6D) in Nicotiana benthamiana leaves in a transient 286

expression system.Thus, RPS2 appeared to be a transcriptional target of MEA-mediated 287

suppression. 288

The PRC2 repressor complex physically associates with the target loci. The transgenic 289

35S:MEA plants contained a hemagglutinin (HA) tag as translational fusion with MEA. We 290

examined the physical association of MEA-HA with the RPS2 locus by ChIP using an anti-291



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HA tag antibody. As a negative control, we used ACTIN2 (ACT2), the expression of which 292



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was not affected by MEA over-expression. And as positive control, we used PHERES1 293

(PHE1), a known target of MEA. MEA is recruited at the PHE1promoter, which results in 294

enrichment of nucleosomes with H3K27me3 and thereby suppresses its expression 295

(Makarevich et al., 2006). As expected, we found a MEA-HA association with the PHE1 296

promoter but not with the ACT2 promoter (Supplemental Figure S8). Three different regions 297

of the RPS2 locus were used for the ChIP study, one at the promoter and two in the coding 298

areas (Figure 6E). We observed constitutive MEA-HA accumulation throughout the RPS2 299

locus in - 35S:MEA plants (Figure 6F). Upon pathogen inoculation, MEA-HA occupancy 300

further increases at areas 1 and 3 of the RPS2 locus (Figure 6F). Interestingly, MEA 301

accumulation at area 2 of RPS2 reduces after Pst-AvrRpt2 inoculation (Figure 6F). It is 302

possible that the other transcription factors that are involved for RPS2 expression partly 303

displaced MEA-HA during pathogenesis. Being a part of a polycomb group repressor, MEA 304

contributes to transcriptional suppression of target loci by histone methylation (Makarevich et 305

al., 2006). Since MEA physically associates with the RPS2 locus, we speculated a similar 306

mechanism for AvrRpt2-mediated suppression of RPS2. To test this hypothesis, we monitored 307

H3K27me3 occupancy at the RPS2 locus by ChIP. WT and 35S:MEA plants were inoculated 308

with Pst-AvrRpt2 and chromatin fragments were precipitated by anti-H3K27me3 antibody. 309

Relative abundance of hitone methylation at the RPS2 locus was determined by qPCR. We 310

observed significantly high levels of H3K27me3 occupancy in 35S:MEA plants compared to 311

the WT at the RPS2 locus (Figure 6G). In agreement with this observation we found reduced 312

enrichment of H3K27me3 in mea-6mutants than in WT plants at all tested regions (Figure 313

6H).The FLOWERING LOCUS T (FT) that accumulates highlevels of H3K27me3 served as 314

the required control (Saleh et al., 2008) (Supplemental Figures S9 and S10). The results 315

demonstrated that RPS2 is a direct target for MEA-mediated transcriptional repression. 316

317

Di19 interacts with and recruits MEA at the RPS2 promoter 318

The interaction of SET domain-containing proteins of the PRC-2 complex with target DNA is 319

indirect, mediated by other DNA binding proteins (Margueron and Reinberg, 2011). We 320

could not detect any direct association of MEA with the RPS2 promoter in agel-shift assay. 321

By screening an Arabidopsis cDNA library, using MEA as bait, we identified DROUGHT-322

INDUCED 19 (Di19/AtDi19-1) as an interacting factor involved in RPS2 suppression and 323

promotion of bacterial growth. Di19 is a member of the AtDi19 gene family which has seven 324



17

members (AtDi19-1 to AtDi19-7) each containing two hydrophilic Cys2/His2 (C2H2) zinc-325



18

finger-like domains (Milla et al., 2006). These C2H2 zinc finger motifs are evolutionarily 326

conserved among monocots and dicots suggesting a conserved biological function. Most of 327

the family members express ubiquitously in all organs and have similar sub-cellular 328

localization, i.e. the nucleus (Milla et al., 2006), indicating possible functional redundancy 329

among family members. To identify the essential domains of Di19 and MEA for their 330

physical interaction, we performed a yeast two-hybrid assay with full length and deletion 331

proteins. MEA contains an acidic region and a cysteine-rich domain in the N-terminal half, 332

and a nuclear localization signal (NLS), a CXC domain and the SET domain in the C-333

terminal half (Yadegari et al., 2000) (Figure 7A). Di19 contains two zinc-finger domains and 334

one NLS (Milla et al., 2006; Liu et al., 2013) (Figure 7A). Interaction studies in yeast with 335

deleted domains of MEA and Di19 suggested that the N-terminal part containing the acidic 336

region of MEA was sufficient, whereas the zinc-finger domains and the C-terminal region 337

including the NLS of Di19 were required for the interaction (Figure 7B). An In planta 338

interaction of MEA with Di19 was confirmed in onion (Allium cepa) epidermal cells by a 339

bimolecular fluorescence complementation assay (Figure 7C). Di19 codes for a DNA-binding 340

transcription factor-like protein. The RPS2 promoter contains one predicted Di19 binding 341

sequence (DiBS; TACA(A/G)T; Liu et al., 2013) at -422 bp from the transcription start site. 342

A gel-electrophoresis mobility shift assay (EMSA) revealed that Di19 binds with the RPS2 343

promoter (Figure 7D).To further establish the possible role of Di19 in defense, we used the 344

di19 mutant (Salk_088814, Supplemental Figure S11A and B) and the Di19 over-expressing 345

line (Supplemental Figure S11B; Liu et al., 2013). In agreement with the predicted function 346

of the repressor complex, the di19 mutant showed enhanced RPS2 expression (Figure 7E). 347

Moreover, similar toMEA over-expression, Di19 over-expression supported higher Pst-348

AvrRpt2 growth (Figure 7F), whereas its mutant showed resistance (Figure 7G). A modest 349

difference in bacterial growth between WT and Di19 over-expression or mutant plants 350

indicates that MEA-mediated susceptibility may involve other proteins in addition to Di19. 351

Functional redundancy among Di19 family members may also be the possible reason for the 352

difference. Nevertheless, our results suggest that MEA and Di19 forms a functional PRC-2-353

like complex, which associates at the RPS2 promoter and suppresses it expression. 354

355

356



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Discussion 357

358

MEA functions as a feedback inhibitor of defense 359

Activation of the immune response takes place at the cost of metabolic energy. Thus, plants 360

possessfactors that do not allow spontaneous activation of the immune response and checks 361

that limit the defense responses once activated to an optimal level. Genetic screens identified 362

many negative regulators, mutations in which activate spontaneous defense. For example, 363

mutants of CONSTITUTIVE FOR PR1(CPR1), CPR5, SUPPRESSOR OF SA INSENSITIVE 1 364

(SSI1), SSI2, CONSTITUTIVE EXPRESSION OF VSP1 (CEV1), and SUPPRESSOR OF 365

NPR1-1 CONSTITUTIVE 1 (SNC1) activate constitutive defense, suggesting a negative 366

regulatory role of these genes in defense (Bowling et al., 1994; Bowling et al., 1997; Shah et 367

al., 1999; Ellis and Turner, 2001; Jirage et al., 2001; Li et al., 2001; Shah et al., 2001). The 368

mutants of these genes spontaneously activate SA or ET/JA signaling and thereby activate 369

cell death and other defense responses. In addition, plants also recruit factors such as LESION 370

SIMULATING DISEASE 1 (LSD1) that regulate excessive cell death upon pathogen 371

inoculation (Dietrich et al., 1994). LSD1 negatively regulates basal defense independent of 372

SA, but regulates cell death downstream of SA accumulation in a NPR1-dependent manner 373

(Aviv et al., 2002). Our results identified a very different mechanism of defense response 374

regulation mediated by MEA, a known epigenetic modulator and transcriptional repressor. 375

MEA expression, which remains suppressed in the vegetative tissue, is induced upon 376

pathogenesis (Figure 1) and artificial expression of MEA negatively regulates defense (Figure 377

3). The results prompted us to hypothesize that MEA functions as a feedback inhibitor of 378

defense (Figure 8A). SinceMEA is induced by both SA and JA-pathway activation, and MEA 379

expression negatively regulates both biotrophic and necrotrophic pathogens, MEA is likely to 380

control multiple aspects of plant immune response. Via the Arabidopsis and Pst-AvrRpt2 381

interaction, we showed that MEA suppresses RPS2 expression (Figure 6).RPS2 is the R gene 382

that functions in combination with the AvrRpt2 effector for activating ETI(Kunkel et al., 383

1993; Bent et al., 1994; Guttman and Greenberg, 2001; Mackey et al., 2003; Belkhadir et al., 384

2004; Lim and Kunkel, 2004, 2005; Chen et al., 2007). Interestingly, only partial suppression 385

of RPS2 expression in MEA-overexpressing plants was sufficient to significantly suppress 386

Pst-AvrRpt2-mediated ETI. However, the results are in agreement with earlier observations in 387

CPR1 over-expressing plants, which showed partial accumulation of RPS2 with a 388



20

dramaticreduction in the resistance against Pst-AvrRpt2 (Cheng et al., 2011). Interestingly, 389

RPS2 function is also required for Pst-AvrRpt2-induced high-level expression of MEA 390

(Figure 5). This result further supports the feedback inhibitory role of MEA in defense 391

(Figure 8A). However, target genes of the MEA-PRC2 complex involved in basal defense 392

remain unidentified. 393

Mechanism of MEA activation and RPS2 suppression 394

395

Chromatin modification by the PcG repressor complex (PRC) is a common strategy of gene 396

silencing in higher eukaryotes (Simon and Kingston, 2013). Two groups of PRCs exist. PRC-397

2 contributes to methylation at H3K27, whereas PRC-1 recognizes such modification and 398

brings structural changes in chromatin (Kohler and Hennig, 2010; Kalb et al., 2014). MEA, 399

which belongs to the PRC-2 group, contributes to its own suppression in vegetative tissues 400

(Baubec and Mittelsten Scheid, 2006; Jullien et al., 2006). Suppression of MEA in vegetative 401

tissues and the paternal allele in the embryo is associated with H3K27 methylation (Jullien et 402

al., 2006). In the female gametophyte, embryonic tissues and central cells, demethylation of 403



21

H3K27me3 takes place through a yet unidentified histone demethylase, which allows its 404

expression. In addition to H3K27 methylation, MEA is also suppressed by DNA methylation 405

in vegetative tissues and in the paternal allele in endosperm (Gehring et al., 2006). Our results 406

demonstrated that, contrary to the pathogen-induced expression, the epigenetic repressor 407

marks (DNA methylation) are not removed from the MEA locus (Figure 4B and 408

4C).However, pathogenesis overrides the suppression through a different epigenetic 409

mechanism, which is indicated by the enhancement of H3K4me3 with reduction of 410

H3K27me3 marks at the MEA locus. Though the role of histone methylations in gene 411

expression is not fully established (Henikoff and Shilatifard, 2011), H3K4me3 is often 412

associated with actively transcribing genes, whereas H3K27me3 is associated with the 413

transcriptionally silenced genes (Schones and Zhao, 2008). Chromatin modification at the 414

MEA locus is in agreement with the pathogenesis-induced transcript accumulation of MEA. 415

Our results clearly showed that MEA and its interactor Di19 negatively regulate RPS2 416

expression (Figure 6A-C, 7E). PcG repressors associate physically with the target loci and 417

induce chromatin modification (Simon and Kingston, 2013; Entrevan et al., 2016). Through 418

ChIP and EMSA, we showed that MEA and Di19 associate with the RPS2 locus (Figure 6F, 419

7D). The most important function of PRC2 is to methylate H3 at K27. Similar to the reported 420

MEA target PHE1, the RPS2 locus also accumulates H3K27me3 in MEA expressing plants 421

(Figure 6G),whereas the mea-6 mutant has lower occupancy of H3K27me3 (Figure 422

6H).Altogether, ourresults demonstrated that RPS2 is a direct target of MEA for 423

transcriptional suppression, and Di19 takes part in recruiting MEA at the RSP2 promoter 424

(Figure 8B). 425

In summary, the imprinted PcG suppressor MEA remains transcriptionally silent in 426

vegetative tissues. Pathogen inoculation activates MEA transcription, which in turn limits the 427

induction of excessive immune response. Thus, MEA functions as a feedback inhibitor of 428

defense and plays roles in the growth-defense tradeoff. 429

430

Experimental Procedures: 431

432

Plant growth conditions and pathogen inoculation 433

Arabidopsis plants were grown as described previously (Swain et al., 2011; Singh et al., 434

2013), in a growth room at 21⁰C and 65% relative humidity with an alternate light (80 µE m–435



22

1s–1)/dark period of 12 hours each. Bacterial cultures were grown overnight and harvested and 436

resuspended in 10mM MgCl2 and diluted as required before infiltrating abaxial sides of 437

leaves with a needleless syringe. Bacterial loads in the leaves were determined as described 438

previously (Singh et al., 2013). In brief, we inoculated about 12-16 plants per line and 1-2 439

leaves per plant with the bacteria suspended in 10mM MgCl2. While collecting samples, we 440

randomly selected 20 leaves. Leaves were pooled into groups of four each having five leaves. 441

Using a cork-borer, a disc of 5mm diameter was taken from each leaf, homogenized and 442

serially diluted in 10 mM MgCl2 before plating for counting colony forming units (CFUs). 443

For Botrytis cinerea inoculation, spores were suspended in potato dextrose broth 444

(5x105spores/ml) and sprayed on plants. Inoculated plants were covered with a transparent 445

plastic dome and kept in low light for four days. Symptoms were observed after 4 days of 446

inoculation. 447

448

Generation of mea-6 homozygous lines 449

450

Heterozygous MEA/mea-6 (CS6996) plants were obtained from the Arabidopsis stock center. 451

To generate mea-6 homozygous mutants, MEA/mea-6 plants were crossed as the male parent 452

to haploid inducer GFP-tailswap plants as the female parent (Ravi et al., 2014). The resultant 453

F1 seeds were germinated on Murashige and Skoog agar plates and later transferred to soil 454

for further growth. Haploids were identified both phenotypically and cytologically as 455

described earlier (Ravi and Bondada, 2016). All the haploids were PCR genotyped using a 456

derived Cleaved Amplified Polymorphic Sequence (dCAPS) analysis. Both MEA and mea-6 457

alleles generate a 152 bpamplicon with MR260 and MR261 primers (Supplemental Table 458

S1). The PCR product from themea-6 allele cleaved into two fragments of 128 bp and 24 bp 459

upon digestion with XbaI enzyme, whereas the WT MEA allele remains uncut (Supplemental 460

Figure S12). The mea-6 haploid plants were grown to full maturity and spontaneous seeds 461

arising either due to mitotic and/or meiotic chromosome doubling were collected and viable 462

seeds were sown further to generate doubled haploid (mea-6/mea-6) plants which were again 463

confirmed by dCAPs genotyping for homozygosity (Supplemental Figure S12). The seeds 464

obtained from the doubled haploid mea-6/mea-6 plants were used for the experiments 465

described here. 466

467

468



23

Chemical treatment 469

For expression analysis, SA (500 µM in water) was thoroughly sprayed on plants, whereas 470

flg22 (1µM in water) was pressure infiltrated through the abaxial leaf surface (Swain et al., 471

2015). After the treatment, plants were transferred to a growth chamber and covered with a 472

plastic dome overnight for maintaining humidity. Detached leaves of five-week-old plants 473

were floated in 5 µM MeJA dissolved in 0.1% ethanol. Control samples were floated in 0.1% 474

ethanol. Samples were collected at the indicated time intervals. Expression was determined 475

by RT-qPCR. 476

477

Salicylic acid estimation 478

Estimation of SA was done by high-performance liquid chromatography (HPLC) (Agilent 479

1220 LC) exactly as described previously (Singh et al., 2013). 480

481

RNA isolation, cDNA synthesis and expression analysis 482

RNA wasisolated from leaf samples. Total RNA was extracted by the 483

guanidiniumthiocyanate–phenol–chloroform method (Chomczynski and Sacchi, 1987). For 484

reverse-transcription PCR (RT-PCR), 1.0 µg of RNA was treated with DNase I (Thermo 485

Scientific, USA) for 30 min at 37°C, and was used for first strand cDNA synthesis using a kit 486

(iscriptcDNA synthesis kit, Bio-Rad, USA Cat# 170-8891). Semi-quantitative RT-PCR and 487

RT-qPCR) was carried out by gene specific primers listed in SupplementalTable 1. 488

Quantitative PCR was carried out by a 7500 Fast Real-Time PCR machine (Applied 489

Biosystems, U.S.A.) using 2X Power SYBR Green master mix (Applied Biosystems Cat # 490

4367659). Typically, each experiment contained 3 biological samples with 2 technical 491

replicates. The average of the two technical replicates was taken as the reading for that 492

biological sample.ACTIN2 (ACT2, At3g18780) and TUBULIN2 (TUB2; At5g62690) 493

wereused for normalization. The data represented here are normalised with ACT2 only.Non-494

template controls were included in each RT-qPCR reaction. The melting curve generated by 495

the software was usedto ensure the presence of a single PCR product in each lane, which was 496

verified by agarose gel electrophoresis. Further, we sequenced the PCR products from each 497

set of primers to confirm the specific product. 498

Ion leakage experiment 499



24

Leaves of five-week-old plants were infiltrated through the abaxial surface with a suspension 500

of Pst-AvrRpt2 at 1x107 CFU/ml in 10mM MgCl2. Only 10mM MgCl2 was used as the mock 501

treatment. Infiltrated plants were covered with a plastic dome and dark incubated for 7 hours 502

in a growth room. After that leaf discs (0.7 cm diameter) were punched out with a cork borer 503

and washed for 45 minutes in distilled water with gentle shaking. Then the leaf discs were 504

floated in distilled water in a 6 well plate. Usually, every sample contained 8 leaf discs in 8 505

ml of water and each experimental set contained three biological replicates. The conductivity 506

of water in terms of µS/cm2/s using a conductivity meter (HI2300, Hanna, USA) was 507

measured from 8 to 22 hours afterinoculation. At the end, the leaf discs along with water 508

were autoclaved to achieve a maximum release of ionic content. Ion leakage was plotted as a 509

percentage of maximum conductivity. 510

Generation of MEA over-expression and GFP tagged lines 511

The full lengthMEA coding sequence (CDS) was amplified from an Arabidopsis cDNA pool 512

prepared from a pathogen-inoculated leaf sample, using a proofreading capable DNA 513

polymerase Pfu (NEB, USA). For the 35S:MEA construct, the MEACDS was amplified using 514

Pfu DNA polymerase with end primers and an A-overhang was generated by Taq DNA 515

polymerase. The pCXSN vector (Chen et al., 2009) was digested with XcmIto generatea T-516

overhang and ligated with the PCR amplified MEA CDS. For expression as a GFP tagged 517

protein (MEA-GFP), the MEA CDS was cloned into thepCXDG vector (Chen et al., 2009) as 518

described for 35S:MEA. For generation of transgenic plants, WT Arabidopsis (Col-0) was 519

transformed by the Agrobacterium mediated floral dip transformation method (Zhang et al., 520

2006a). Transformed seeds were screened on MS media supplemented with hygromycin (25 521

mg/L). Antibiotic resistant plants were later confirmed for the presence of the antibiotic 522

resistance gene by PCR and expression analysis. 523

MEA:GUS vector construction and transient assay 524

The DNA fragment spanning the 1085 bp upstream region from the transcription start site of 525

MEA was amplified using specific primers (Supplemental Table S1). The 35SCaMV 526

promoter of thepBI121 vector was excised by HindIII and BamHI and the MEA promoter was 527

ligated to generate the MEA:GUS construct. Agrobacterium tumefaciens strain C58 was 528

transformed with either 35S:GUS (pBI121) or MEA:GUS. Transient GUS activity in 529

Arabidopsis leaves was observed as described in (Lee and Yang, 2006). Briefly, 4 week old 530

Arabidopsis leaves were infiltrated with A. tumefacienscontainingeither 35S:GUS or 531



25

MEA:GUS(0.4 OD). After 48 hours leaves were infiltrated with Pst-AvrRpt2 (106CFU/ml 532

suspended in 10 mM MgCl2), or only 10 mM MgCl2 as the mock. At 12 hours after pathogen 533

inoculation, leaves were stained overnight at 37⁰C in GUS staining solution (1 mM EDTA 534

(pH 8), 5 mM potassium ferricyanide, 5 mM potassium ferrocyanide, 100 mM sodium 535

phosphate (pH 7.0), 1% Triton-X-100, and 1 mg/ml X-Gluc). Stained leaves were kept in 536

ethanol for removal of chlorophyll. 537

538

RPS2:GUS vector construction and transient expression in Nicotianabenthamiana 539

The DNA fragment of 995 bp upstream of RPS2was amplified and cloned in the binary 540

vector pBI121 between PstI and XbaI after replacing the 35SCaMV promoter. 541

Nicotianabenthamianaleaves were co-infiltrated with Agrobacterium tumefaciens carrying 542

binary vectors expressing RPS2:GUS with either MEA under the CaMV35S promoter in the 543

pCXDG vector or the empty vector (0.4:0.4 OD). After 2 days the leaves were either 544

infiltrated with Pst-AvrRpt2 (106CFU/ml suspended in 10 mM MgCl2), or only 10 mM 545

MgCl2 as the mock. At 12 hours afterpathogen inoculation, leaves were stained for GUS 546

expression as described above. 547

548

Chromatin Immunoprecipitation 549

Chromatin immunoprecipitation (ChIP) was performed as described previously (Saleh et al., 550

2008; Singh et al., 2014). Briefly, Arabidopsis leaves were inoculated with the bacterial 551

pathogen (1x106CFU/ml) suspended in 10mM MgCl2 or only 10mM MgCl2 as the mock 552

treatment. Each sample consisted of 4.0 g of freshly harvested leaves.Immunoprecipitation 553

was done with either anti-H3K4me3, anti-HA (Abcam, USA) or anti-H3K27me3 (Millipore, 554

USA) antibody. Fold enrichment of immunoprecipitated chromatin for each target gene was 555

plotted according to the ΔΔCTmethod by RT-qPCR. The CT value for the antibody sample 556

(+AB) and for no antibody control (-AB) was independently subtracted from the CT value of 557

the corresponding input to find ΔCT. Then ΔCT–AB was subtracted from ΔCT+AB to get the 558

ΔΔCT for each sample and 2-ΔΔCT was plotted (Mukhopadhyay et al., 2008; Han et al., 2016). 559

Primers used in this study are mentioned in Supplemental TableS1. 560

561

Embryo microscopy 562



26

Siliques of different maturity levels were taken for the study. Developing embryos were taken 563

out and cleared in Hoyer’s solution overnight to remove chlorophyll. The morphology of 564

developing embryos was observed under microscope. 565

566

DNA methylation analysis 567

Five-week old WT Arabidopsis leaves were inoculated with either P. syringaepv.tomato 568

carrying AvrRpt2 (107CFU/ml) suspended in 10mM MgCl2 or only 10mM MgCl2 as mock 569

treatment. Leaf samples were harvested at 24 hpi and genomic DNA was extracted using 570

plant DNA extraction Kit (Thermoscientific, USA). To 1µg of gDNA, methylation sensitive 571

enzymes HpaII 2.0U (Thermoscientific) or McrBc2.0U (NEB) was added in a 50µl reaction 572

and incubated for 8 hrs. Relative content of digested DNA was determined by qPCR. 573

574

Bimolecular Flourescence Complementation (BiFC) 575

BiFC constructs were generated by cloning thedesired gene CDS in either pSPYNE(R)173 or 576

pSPYCE(M) as described previously (Waadt et al., 2008). Clones were transformed in 577

Agrobacterium C58 strain. Fleshy onion scales were fully immersed in transformed C58 578

strain of Agrobacterium suspension (0.8 OD) and kept at 28⁰C for 12-24 hrs. Scales were 579

then transferred on half strength MS media and incubated for 2-3 days. Co-cultivated scales 580

were thoroughly washed with sterile water and the epidermal layer was peeled off and 581

mounted on a slide for observation. Samples were observed under a confocal microscope and 582

analysed with the OLYMPUS FV1000 viewer software. 583

Electrophoretic-mobility shift assay (EMSA) 584

For construction ofthe MBP-Di19 recombinant fusion protein, Di19 sequences were cloned in 585

the pMAL-p2X vector (NEB) at the C-terminal end of MBP between EcoRI and BamHI 586

restriction sites. MBP and MBP-Di19 were expressed in the Escherichia coli BL21 (DE3) 587

strain and purified using amylose resin (NEB). For the binding assay, 400ng, 1µg, 1.6µg and 588

2µg of MBP or MBP Di19 was used. Oligonucleotides (40bp) surrounding DiBs were used 589

and radiolabeled with γP32 ATP at the 5´ endby T4 polynucleotide kinase (NEB). For 590

competitive binding, 50X and 100X non-radiolabeledRPS2 DNA was used along with 1 µg 591

of MBP or MBP-Di19. EMSA was performed as described previously (Hellman and Fried, 592

2007) using a 10% polyacrylamide gel. 593

Yeast Two-Hybrid library Screening 594



27

The MEDEA CDSwas cloned into the pBGKT7 vector between EcoRI and BamHI restriction 595

sites to fuse with the GAL4 transcription factor DNA binding domain. The Di19 CDS was 596

cloned into the pGADT7 vector between NdeI and EcoRI, to fuse with the activation domain. 597

Confirmation of interactors was done by activation of reporter genes and survival on 598

quadruple drop out (-leu, -trp, -his, -ade) media. Yeast growth, transformation and depleted 599

synthetic media preparation was done according to the manufacturer’s protocol (Clontech, 600

USA). 601

Accession Numbers 602

The gene accession numbers that were used in this study are as follows: At1g02580 603

(MEDEA), At1g56280 (AtDi19), At3g18780 (ACTIN2), At4g26090 (RPS2), At5g62690 604

(TUBULIN2), At1g65480 (FT), At5g44420 (PDF1.2), At2g14610 (PR1), At1g65330 605

(PHE1), At5g58230 (MSI1), At3g20740 (FIE). 606

607

608

609

Acknowledgements 610

We acknowledge Yi-Fang Chen, China Agricultural University for the Di19 over-expression 611

plants, and ABRC, Ohio State University, for the mutant seeds; Utpal Nath for critical 612

reading and comments on the manuscript. 613

614

Short legends for supporting information: 615

616

Supplemental Figure S1. MEA transcript accumulation in WT plants after flg22treatment. 617

Supplemental Figure S2.FIE and MSI1 expression in WT plants after pathogen inoculation. 618

Supplemental Figure S3. Morphological phenotype of WT (C24) and mea-6 plants. 619

Supplemental Figure S4. 35S:MEA transgenic plants. 620

Supplemental Figure S5. Morphology of developing embryo of WT, 35S:MEA and mea/+ 621 plants. 622

Supplemental Figure S6. Defense against the bacterial pathogen in 35S:MEA plants. 623



28

Supplemental Figure S7. H3K27me3 and H3K4me3 occupancy on FT and ACT2. 624

Supplemental Figure S8. Fold enrichment of MEA-HA at PHE and ACT2 loci. 625

Supplemental Figure S9. H3K27me3 occupancy on the FT locus in Col-0 plants. 626

Supplemental Figure S10. H3H27me3 occupancy on the FT locus in C24 WT plants 627

Supplemental Figure S11. Confirmation of the di19 mutant and over-expression lines 628

Supplemental Figure S12. Genotyping of plants for mea-6 and MEA alleles. 629 630 631 Supplemental Table S1: Primer sequences 632 633

634

Figure Legends 635

Figure 1.MEA expression after pathogen, SA and MeJA treatment. (A) Relative abundance of MEA 636

mRNA in WT (Col-0) plants after mock, Pst and Pst-AvrRpt2 (1x106 CFU/ml) inoculation. (B) 637

35S:GUS or MEA:GUS activity in Arabidopsis leaves after Pst-AvrRpt2 (1x106 CFU/ml) or MgCl2 638

infiltration. (C) MEA mRNA accumulation after SA treatment (0.5 mM spray). (D) MEA expression 639

after 5µM MeJA treatment. Each bars represent mean ± S.D. (n=3). * (P<0.05) and ** (P<0.001) 640

indicate the mean values that are significantly different from 0 hours samples or respective mock 641

samples as determined by Student’s t-test. Experiments were repeated at least two times with similar 642

results. 643

644

Figure 2. Bacterial numbers and defense responses in mea-6 and C24 (WT) plants. (A) Pst numbers 645

and disease symptom at 3 days post-inoculation (dpi). (B) Pst-AvrRpt2 numbers and disease symptom 646

at 3 dpi. (C) PR1 expression in WT and mea-6 plants after Pst inoculation.(D) PR1 expression in WT 647

and mea-6 plants after Pst-AvrRpt2 inoculation. (E) Total SA (free SA+SA-glucoside) content in 648

leaves of WT and mea-6 plants after 36 hours of mock, Pst or Pst-AvrRpt2 inoculation. (F) HR-649

induced cell death after Pst-AvrRpt2 inoculation. Samples were harvested 15 hours post-inoculation 650

(hpi) for staining with trypan blue. (G) DAB staining for H2O2 accumulation at 15 hpi with Pst-651

AvrRpt2.(H) HR-induced ion-leakage in WT and mea-6 plants after Pst-AvrRpt2 inoculation (107 652

CFU/ml). Pathogens were inoculated at 5 x 105CFU/ml. Each bars represent mean ± S.D. (n=3). * 653

(P<0.05) and ** (P<0.001) indicate the mean values of mea-6 plants that are significantly different 654

from respective WT samples as determined by Student’s t-test. Experiments were repeated at least 655

two times with similar results. 656

657



29

Figure 3. Defense response in MEA over-expression and WT (Col-0) plants. (A) Numbers of Pst in 658

WTand 35S:MEA plants at 3 days post-inoculation (5 x 105CFU/ml). (B) PR1 expression in WT and 659

35S:MEA plants after Pst inoculation. (C) Total SA (free SA+SA-glucoside) content in leaves of WT 660

and 35S:MEA plants after 36 hours of Pst or mock inoculation. (D) Free SA content in leaves of WT 661

and 35S:MEA plants after 36 hours of Pst inoculation. (E) Numbers of Pst-AvrRpt2 in WT and 662

35S:MEA plants at 3 days post-inoculation (5x105 CFU/ml). (F) PR1 expression in WT and 35S:MEA 663

plants after Pst-AvrRpt2 inoculation. (G) HR-induced ion-leakage in WT and 35S:MEA plants after 664

Pst-AvrRpt2 inoculation (107CFU/ml). (H) Disease symptoms in WT and 35S:MEA plants after 4 665

days of Botrytis cinerea inoculation (5 X 105spores/ml). (I) Expression of PDF1.2 in WT and 666

35S:MEA plants after MeJA treatment (5 µM). Inset shows PDF1.2 expression after water treatment 667

only. In (A) and (E), error bars represent mean ± S.D. (n=5). Different letters above the bars indicate 668

mean values that are significantly different (P<0.05) as analyzed by one-way ANOVA (post-hoc 669

Holm-Sidak method). In (B), (F) and (I), relative abundance of transcripts was determined by RT-670

qPCR. Error bars represent mean ± S.D. (n=3). In C and D, error bars represent mean ± S.D. (n=5). In 671

G, each point represents mean ± S.D. (n=3), and each sample contained 8 leaf-disc of 7 mm diameter. 672

* (P<0.05) and ** (P<0.001) indicate the mean values that are significantly different from mock-673

treated or respective WT samples as determined by Student’s t-test. Experiments were repeated at 674

least two times with similar results. 675

676

Figure 4. DNA and histone methylation at the MEA locus. (A) Schematic diagram of the MEA locus. 677

Black bars -coding sequences, grey bars – UTR, line - intron/promoter, thick lines above the 678

structure- region used for histone modification study, blue line below promoter – region used for 679

DNA methylation study. Numbers indicate nucleotide position with respect to the transcription start 680

site (TSS). (B) Relative amount of HpaII digested DNA in mock or Pst-AvrRpt2 treated leaves of WT 681

(Col-0) plants. (C) Relative amount of McrBc digested DNA in mock or Pst-AvrRpt2 treated leaves of 682

WT (Col-0) plants. In (B) and (C) samples were collected at 24 hpiwith Pst-AvrRpt2 (1 x 683

106CFU/ml). Error bars represent mean ± S.D. (n=3). D-F, Fold enrichment of H3K27me3 containing 684

nucleosomes at the MEA locus. G-J, Fold enrichment of H3K4me3 containing nucleosomes at the 685

MEA locus. In (D-J) samples were collected at 24 hpi of Pst-AvrRpt2 (1 x 106CFU/ml). In (D-J) grey 686

and black bars indicate specific antibody and no antibody control, respectively. Error bars represent 687

mean ± S.D. (n=3). * (P<0.05) and ** (P<0.001) indicate the mean values of pathogen inoculated 688

antibody precipitated sample that are significantly different from mock inoculated antibody 689

precipitated sample as determined by Student’s t-test. Experiments were repeated at least two times 690

with similar results. 691

692

Figure 5. Relative abundance of MEA mRNA in WT (Col-0) and rps2 mutant after Pst-AvrRpt2 693

inoculation. Five-week-old plants were inoculated with Pst-AvrRpt2 (1x106 CFU/ml) and leaf samples 694



30

were harvested at the indicated time. Inset shows MEA expression in the rps2 mutant background. 695

Relative abundance was measured by RT-qPCR. Error bars represent mean ± S.D. (n=3). * (P<0.05) 696

and ** (P<0.001) indicate the mean values that are significantly different from respective 0 hr 697

samples as determined by Student’s t-test. Experiments were repeated at least two times with similar 698

results. 699

700

Figure 6. Influence of MEA on RPS2 expression. (A) Relative abundance of RPS2 mRNA in WT and 701

35S:MEA plants without pathogen inoculation. (B) Relative abundance of RPS2 mRNA in WT and 702

35S:MEA plants after 10 hours of Pst-AvrRpt2 inoculation. (C) Relative abundance of RPS2 mRNA in 703

WT and mea-6 plants after 10 hours of mock or Pst-AvrRpt2 inoculation. In (A), (B) and (C), error 704

bars represent mean ± S.D. (n=3). * (P<0.05) and ** (P<0.001) indicate the mean values that are 705

significantly different from respective WT samples as determined by Student’s t-test. (D) RPS2:GUS 706

expression in N. benthamiana with or without co-expression of MEA. (E), Schematic diagram of the 707

RPS2 locus showing the transcriptionstart site (TSS) and the areas used for the ChIP experiment. (F) 708

Fold enrichment of MEA-HA at the RPS2 locus. Error bars represent mean ± S.D. (n=3). * (P<0.05) 709

and ** (P<0.001) indicate the mean values of anti-HA antibody precipitate that are significantly 710

different from respective no antibody treated samples as determined by Student’s t-test. (G) Fold 711

enrichmentof H3K27me3 containing nucleosomes at the RPS2 locus in WT and 35S:MEAplants. (H) 712

Fold enrichment of H3K27me3 containing nucleosomes at the RPS2 locus in WT and mea-6 plants. 713

Samples were harvested at 12 hours post-inoculation withPst-AvrRpt2 (1 x 106 CFU/ml). In (F-H) 714

error bars represent mean ± S.D. (n=3). * (P<0.05) and ** (P<0.001) indicate the mean values of 715

antibody precipitated sample that are significantly different from WT antibody-precipitated samples 716

as determined by Student’s t-test. Experiments were repeated at least two times with similar results. 717

718

719

Figure 7. Di19 interacts with MEA and influences disease resistance. (A) Schematic diagram of MEA 720

and Di19, full and truncated proteins used in the interaction study. (B) Yeast2-hybrid interaction. 721

Transformed yeast cells were grown on Leu-, Trp-, His- and Ade- (-LTHA) medium, which allows 722

only interacting clones to grow. p53 and T-antigen were used as positive controls, and empty vectors 723

were used as negative controls. (C) BiFC in transiently expressed onion epidermal cells. (D). 724

Electrophoretic mobility shift assay (EMSA) for confirmation of Di19 with theRPS2 promoter. Each 725

reaction contained 50ng of radiolabeled oligonucleotides containing DiBS from the RPS2 promoter 726

and either MBP or MBP-Di19 (0.4 to 2 µg). For the competitive binding assay, 50X and 100X of non-727

radiolabeled oligonucleotide was used with 1µg of protein. * indicates non-specific bindings. (E) 728

Relative abundance of RPS2 mRNA in WT and di19 mutant plants after Pst-AvrRpt2 inoculation. 729

Error bars represent mean ± S.D. (n=3). * (P<0.05) and ** (P<0.001) indicate the mean values that 730

are significantly different from respective time point WT samples as determined by Student’s t-test. 731



31

(F) Numbers of Pst-AvrRpt2 in WT and Di19 over-expressionplants at 3 days postPst-AvrRpt2 732

inoculation. (G) Numbers of Pst-AvrRpt2 in WT and di19 mutant plants at 3 days postPst-AvrRpt2 733

inoculation. In (F) and (G), error bars represent mean ± S.D. (n=5). Experiments were repeated atleast 734

two times with similar results. * (P<0.05) indicate the mean values that are significantly different 735

from WT samples as determined by Student’s t-test. 736

737

Figure 8. Models depicting the involvement of MEA in defense. (A) General role of MEA in 738

defense attenuation. Pathogen infection leads to induction of defense responses and also activates 739

MEA expression. MEA negatively regulates the defense output. (B) Involvement of MEA in 740

attenuating AvrRpt2-induced ETI. Under normal conditions, MEA expression is suppressed by 741

histone and DNA methylation. AvrRpt2 activates RPS2-mediated ETI and MEA expression. Pst-742

AvrRpt2-induced high-level accumulation of H3K4me3 overrides MEA suppression. MEA along 743

with Di19 binds to the promoter of RPS2 to suppress its expression and thereby to attenuate RPS2-744

mediated ETI. 745

746

747



Parsed CitationsAviv, D.H., Rusterucci, C., Holt, B.F., 3rd, Dietrich, R.A., Parker, J.E., and Dangl, J.L. (2002). Runaway cell death, but not basal diseaseresistance, in lsd1 is SA- and NIM1/NPR1-dependent. Plant J 29, 381-391.

Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Baubec, T., and Mittelsten Scheid, O. (2006). Medea in full self-control. Trends Plant Sci 11, 469-471.Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Belkhadir, Y., Nimchuk, Z., Hubert, D.A., Mackey, D., and Dangl, J.L. (2004). Arabidopsis RIN4 negatively regulates disease resistancemediated by RPS2 and RPM1 downstream or independent of the NDR1 signal modulator and is not required for the virulence functionsof bacterial type III effectors AvrRpt2 or AvrRpm1. Plant Cell 16, 2822-2835.


Bent, A.F., Kunkel, B.N., Dahlbeck, D., Brown, K.L., Schmidt, R., Giraudat, J., Leung, J., and Staskawicz, B.J. (1994). RPS2 ofArabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes. Science 265, 1856-1860.


Bowling, S.A., Clarke, J.D., Liu, Y., Klessig, D.F., and Dong, X. (1997). The cpr5 mutant of Arabidopsis expresses both NPR1-dependentand NPR1-independent resistance. Plant Cell 9, 1573-1584.


Bowling, S.A., Guo, A., Cao, H., Gordon, A.S., Klessig, D.F., and Dong, X. (1994). A mutation in Arabidopsis that leads to constitutiveexpression of systemic acquired resistance. Plant Cell 6, 1845-1857.


Cao, H., Bowling, S.A., Gordon, A.S., and Dong, X. (1994). Characterization of an Arabidopsis Mutant That Is Nonresponsive to Inducersof Systemic Acquired Resistance. Plant Cell 6, 1583-1592.


Chen, S., Songkumarn, P., Liu, J., and Wang, G.L. (2009). A versatile zero background T-vector system for gene cloning and functionalgenomics. Plant Physiol 150, 1111-1121.


Chen, Z., Agnew, J.L., Cohen, J.D., He, P., Shan, L., Sheen, J., and Kunkel, B.N. (2007). Pseudomonas syringae type III effector AvrRpt2alters Arabidopsis thaliana auxin physiology. Proc Natl Acad Sci U S A 104, 20131-20136.


Cheng, Y.T., Li, Y., Huang, S., Huang, Y., Dong, X., Zhang, Y., and Li, X. (2011). Stability of plant immune-receptor resistance proteins iscontrolled by SKP1-CULLIN1-F-box (SCF)-mediated protein degradation. Proc Natl Acad Sci U S A 108, 14694-14699.


Chomczynski, P., and Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroformextraction. Anal Biochem 162, 156-159.


Denance, N., Sanchez-Vallet, A., Goffner, D., and Molina, A. (2013). Disease resistance or growth: the role of plant hormones inbalancing immune responses and fitness costs. Frontiers in plant science 4, 155.


Derkacheva, M., and Hennig, L. (2014). Variations on a theme: Polycomb group proteins in plants. Journal of experimental botany 65,2769-2784.


Deslandes, L., and Rivas, S. (2012). Catch me if you can: bacterial effectors and plant targets. Trends Plant Sci 17, 644-655.Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Dietrich, R.A., Delaney, T.P., Uknes, S.J., Ward, E.R., Ryals, J.A., and Dangl, J.L. (1994). Arabidopsis mutants simulating diseaseresistance response. Cell 77, 565-577.

Pubmed: Author and Title www.plantphysiol.orgon March 19, 2020 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

http://www.ncbi.nlm.nih.gov/pubmed?term=Aviv%2C D%2EH%2E%2C Rusterucci%2C C%2E%2C Holt%2C B%2EF%2E%2C 3rd%2C Dietrich%2C R%2EA%2E%2C Parker%2C J%2EE%2E%2C and Dangl%2C J%2EL%2E %282002%29%2E Runaway cell death%2C but not basal disease resistance%2C in lsd1 is SA%2D and NIM1%2FNPR1%2Ddependent%2E Plant J 29%2C 381%2D391%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Runaway cell death, but not basal disease resistance, in lsd1 is SA- and NIM1/NPR1-dependent&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=Baubec%2C T%2E%2C and Mittelsten Scheid%2C O%2E %282006%29%2E Medea in full self%2Dcontrol%2E Trends Plant Sci 11%2C 469%2D471%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Medea in full self-control&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=Medea in full self-control&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Baubec,&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Belkhadir%2C Y%2E%2C Nimchuk%2C Z%2E%2C Hubert%2C D%2EA%2E%2C Mackey%2C D%2E%2C and Dangl%2C J%2EL%2E %282004%29%2E Arabidopsis RIN4 negatively regulates disease resistance mediated by RPS2 and RPM1 downstream or independent of the NDR1 signal modulator and is not required for the virulence functions of bacterial type III effectors AvrRpt2 or AvrRpm1%2E Plant Cell 16%2C 2822%2D2835%2E&dopt=abstract

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

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http://www.ncbi.nlm.nih.gov/pubmed?term=Bowling%2C S%2EA%2E%2C Clarke%2C J%2ED%2E%2C Liu%2C Y%2E%2C Klessig%2C D%2EF%2E%2C and Dong%2C X%2E %281997%29%2E The cpr5 mutant of Arabidopsis expresses both NPR1%2Ddependent and NPR1%2Dindependent resistance%2E Plant Cell 9%2C 1573%2D1584%2E&dopt=abstract

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

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http://www.ncbi.nlm.nih.gov/pubmed?term=Bowling%2C S%2EA%2E%2C Guo%2C A%2E%2C Cao%2C H%2E%2C Gordon%2C A%2ES%2E%2C Klessig%2C D%2EF%2E%2C and Dong%2C X%2E %281994%29%2E A mutation in Arabidopsis that leads to constitutive expression of systemic acquired resistance%2E Plant Cell 6%2C 1845%2D1857%2E&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Cao%2C H%2E%2C Bowling%2C S%2EA%2E%2C Gordon%2C A%2ES%2E%2C and Dong%2C X%2E %281994%29%2E Characterization of an Arabidopsis Mutant That Is Nonresponsive to Inducers of Systemic Acquired Resistance%2E Plant Cell 6%2C 1583%2D1592%2E&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Chen%2C S%2E%2C Songkumarn%2C P%2E%2C Liu%2C J%2E%2C and Wang%2C G%2EL%2E %282009%29%2E A versatile zero background T%2Dvector system for gene cloning and functional genomics%2E Plant Physiol 150%2C 1111%2D1121%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=A versatile zero background T-vector system for gene cloning and functional genomics&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://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Chen,&hl=en&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=Chomczynski%2C P%2E%2C and Sacchi%2C N%2E %281987%29%2E Single%2Dstep method of RNA isolation by acid guanidinium thiocyanate%2Dphenol%2Dchloroform extraction%2E Anal Biochem 162%2C 156%2D159%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction&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=Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Chomczynski,&as_ylo=1987&as_allsubj=all&hl=en&c2coff=1

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

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

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

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http://www.ncbi.nlm.nih.gov/pubmed?term=Dietrich%2C R%2EA%2E%2C Delaney%2C T%2EP%2E%2C Uknes%2C S%2EJ%2E%2C Ward%2C E%2ER%2E%2C Ryals%2C J%2EA%2E%2C and Dangl%2C J%2EL%2E %281994%29%2E Arabidopsis mutants simulating disease resistance response%2E Cell 77%2C 565%2D577%2E&dopt=abstract


Google Scholar: Author Only Title Only Author and Title

Ellis, C., and Turner, J.G. (2001). The Arabidopsis mutant cev1 has constitutively active jasmonate and ethylene signal pathways andenhanced resistance to pathogens. Plant Cell 13, 1025-1033.


Entrevan, M., Schuettengruber, B., and Cavalli, G. (2016). Regulation of Genome Architecture and Function by Polycomb Proteins.Trends in cell biology 26, 511-525.


Frye, C.A., Tang, D., and Innes, R.W. (2001). Negative regulation of defense responses in plants by a conserved MAPKK kinase. ProcNatl Acad Sci U S A 98, 373-378.


Gast, F.U., Brinkmann, T., Pieper, U., Kruger, T., Noyer-Weidner, M., and Pingoud, A. (1997). The recognition of methylated DNA by theGTP-dependent restriction endonuclease McrBC resides in the N-terminal domain of McrB. Biological chemistry 378, 975-982.


Gehring, M., Huh, J.H., Hsieh, T.F., Penterman, J., Choi, Y., Harada, J.J., Goldberg, R.B., and Fischer, R.L. (2006). DEMETER DNAglycosylase establishes MEDEA polycomb gene self-imprinting by allele-specific demethylation. Cell 124, 495-506.


Giri, M.K., Singh, N., Banday, Z.Z., Singh, V., Ram, H., Singh, D., Chattopadhyay, S., and Nandi, A.K. (2017). GBF1 differentially regulatesCAT2 and PAD4 transcription to promote pathogen defense in Arabidopsis thaliana. Plant J 91, 802-815.


Grossniklaus, U., and Paro, R. (2014). Transcriptional silencing by polycomb-group proteins. Cold Spring Harbor perspectives inbiology 6, a019331.


Grossniklaus, U., Vielle-Calzada, J.P., Hoeppner, M.A., and Gagliano, W.B. (1998). Maternal control of embryogenesis by MEDEA, apolycomb group gene in Arabidopsis. Science 280, 446-450.


Guitton, A.E., Page, D.R., Chambrier, P., Lionnet, C., Faure, J.E., Grossniklaus, U., and Berger, F. (2004). Identification of new membersof Fertilisation Independent Seed Polycomb Group pathway involved in the control of seed development in Arabidopsis thaliana.Development 131, 2971-2981.


Guttman, D.S., and Greenberg, J.T. (2001). Functional analysis of the type III effectors AvrRpt2 and AvrRpm1 of Pseudomonas syringaewith the use of a single-copy genomic integration system. Mol Plant Microbe Interact 14, 145-155.


Han, Y.C., Kuang, J.F., Chen, J.Y., Liu, X.C., Xiao, Y.Y., Fu, C.C., Wang, J.N., Wu, K.Q., and Lu, W.J. (2016). Banana Transcription FactorMaERF11 Recruits Histone Deacetylase MaHDA1 and Represses the Expression of MaACO1 and Expansins during Fruit Ripening.Plant Physiol 171, 1070-1084.


Heil, M., and Baldwin, I.T. (2002). Fitness costs of induced resistance: emerging experimental support for a slippery concept. TrendsPlant Sci 7, 61-67.


Hellman, L.M., and Fried, M.G. (2007). Electrophoretic mobility shift assay (EMSA) for detecting protein-nucleic acid interactions. NatProtoc 2, 1849-1861.


Henikoff, S., and Shilatifard, A. (2011). Histone modification: cause or cog? Trends in genetics : TIG 27, 389-396.Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Huot, B., Yao, J., Montgomery, B.L., and He, S.Y. (2014). Growth-defense tradeoffs in plants: a balancing act to optimize fitness. MolPlant 7, 1267-1287. www.plantphysiol.orgon March 19, 2020 - Published by Downloaded from

Copyright © 2018 American Society of Plant Biologists. All rights reserved.

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

http://scholar.google.com/scholar?as_q=Arabidopsis mutants simulating disease resistance response&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=Arabidopsis mutants simulating disease resistance response&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Dietrich,&as_ylo=1994&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Ellis%2C C%2E%2C and Turner%2C J%2EG%2E %282001%29%2E The Arabidopsis mutant cev1 has constitutively active jasmonate and ethylene signal pathways and enhanced resistance to pathogens%2E Plant Cell 13%2C 1025%2D1033%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=The Arabidopsis mutant cev1 has constitutively active jasmonate and ethylene signal pathways and enhanced resistance to pathogens&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 Arabidopsis mutant cev1 has constitutively active jasmonate and ethylene signal pathways and enhanced resistance to pathogens&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ellis,&as_ylo=2001&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Entrevan%2C M%2E%2C Schuettengruber%2C B%2E%2C and Cavalli%2C G%2E %282016%29%2E Regulation of Genome Architecture and Function by Polycomb Proteins%2E Trends in cell biology 26%2C 511%2D525%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Regulation of Genome Architecture and Function by Polycomb Proteins&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=Regulation of Genome Architecture and Function by Polycomb Proteins&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Entrevan,&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Frye%2C C%2EA%2E%2C Tang%2C D%2E%2C and Innes%2C R%2EW%2E %282001%29%2E Negative regulation of defense responses in plants by a conserved MAPKK kinase%2E Proc Natl Acad Sci U S A 98%2C 373%2D378%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Negative regulation of defense responses in plants by a conserved MAPKK kinase&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=Negative regulation of defense responses in plants by a conserved MAPKK kinase&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Frye,&as_ylo=2001&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Gast%2C F%2EU%2E%2C Brinkmann%2C T%2E%2C Pieper%2C U%2E%2C Kruger%2C T%2E%2C Noyer%2DWeidner%2C M%2E%2C and Pingoud%2C A%2E %281997%29%2E The recognition of methylated DNA by the GTP%2Ddependent restriction endonuclease McrBC resides in the N%2Dterminal domain of McrB%2E Biological chemistry 378%2C 975%2D982%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=The recognition of methylated DNA by the GTP-dependent restriction endonuclease McrBC resides in the N-terminal domain of McrB&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 recognition of methylated DNA by the GTP-dependent restriction endonuclease McrBC resides in the N-terminal domain of McrB&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Gast,&as_ylo=1997&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Gehring%2C M%2E%2C Huh%2C J%2EH%2E%2C Hsieh%2C T%2EF%2E%2C Penterman%2C J%2E%2C Choi%2C Y%2E%2C Harada%2C J%2EJ%2E%2C Goldberg%2C R%2EB%2E%2C and Fischer%2C R%2EL%2E %282006%29%2E DEMETER DNA glycosylase establishes MEDEA polycomb gene self%2Dimprinting by allele%2Dspecific demethylation%2E Cell 124%2C 495%2D506%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=DEMETER DNA glycosylase establishes MEDEA polycomb gene self-imprinting by allele-specific demethylation&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=DEMETER DNA glycosylase establishes MEDEA polycomb gene self-imprinting by allele-specific demethylation&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Gehring,&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Giri%2C M%2EK%2E%2C Singh%2C N%2E%2C Banday%2C Z%2EZ%2E%2C Singh%2C V%2E%2C Ram%2C H%2E%2C Singh%2C D%2E%2C Chattopadhyay%2C S%2E%2C and Nandi%2C A%2EK%2E %282017%29%2E GBF1 differentially regulates CAT2 and PAD4 transcription to promote pathogen defense in Arabidopsis thaliana%2E Plant J 91%2C 802%2D815%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=GBF1 differentially regulates CAT2 and PAD4 transcription to promote pathogen defense 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=GBF1 differentially regulates CAT2 and PAD4 transcription to promote pathogen defense in Arabidopsis thaliana&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Giri,&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Grossniklaus%2C U%2E%2C and Paro%2C R%2E %282014%29%2E Transcriptional silencing by polycomb%2Dgroup proteins%2E Cold Spring Harbor perspectives in biology 6%2C a019331%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Transcriptional silencing by polycomb-group proteins&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=Transcriptional silencing by polycomb-group proteins&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Grossniklaus,&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Grossniklaus%2C U%2E%2C Vielle%2DCalzada%2C J%2EP%2E%2C Hoeppner%2C M%2EA%2E%2C and Gagliano%2C W%2EB%2E %281998%29%2E Maternal control of embryogenesis by MEDEA%2C a polycomb group gene in Arabidopsis%2E Science 280%2C 446%2D450%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Maternal control of embryogenesis by MEDEA, a polycomb group gene 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=Maternal control of embryogenesis by MEDEA, a polycomb group gene in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Grossniklaus,&as_ylo=1998&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Guitton%2C A%2EE%2E%2C Page%2C D%2ER%2E%2C Chambrier%2C P%2E%2C Lionnet%2C C%2E%2C Faure%2C J%2EE%2E%2C Grossniklaus%2C U%2E%2C and Berger%2C F%2E %282004%29%2E Identification of new members of Fertilisation Independent Seed Polycomb Group pathway involved in the control of seed development in Arabidopsis thaliana%2E Development 131%2C 2971%2D2981%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Identification of new members of Fertilisation Independent Seed Polycomb Group pathway involved in the control of seed development 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=Identification of new members of Fertilisation Independent Seed Polycomb Group pathway involved in the control of seed development in Arabidopsis thaliana&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Guitton,&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Guttman%2C D%2ES%2E%2C and Greenberg%2C J%2ET%2E %282001%29%2E Functional analysis of the type III effectors AvrRpt2 and AvrRpm1 of Pseudomonas syringae with the use of a single%2Dcopy genomic integration system%2E Mol Plant Microbe Interact 14%2C 145%2D155%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Functional analysis of the type III effectors AvrRpt2 and AvrRpm1 of Pseudomonas syringae with the use of a single-copy genomic integration system&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=Functional analysis of the type III effectors AvrRpt2 and AvrRpm1 of Pseudomonas syringae with the use of a single-copy genomic integration system&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Guttman,&as_ylo=2001&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Han%2C Y%2EC%2E%2C Kuang%2C J%2EF%2E%2C Chen%2C J%2EY%2E%2C Liu%2C X%2EC%2E%2C Xiao%2C Y%2EY%2E%2C Fu%2C C%2EC%2E%2C Wang%2C J%2EN%2E%2C Wu%2C K%2EQ%2E%2C and Lu%2C W%2EJ%2E %282016%29%2E Banana Transcription Factor MaERF11 Recruits Histone Deacetylase MaHDA1 and Represses the Expression of MaACO1 and Expansins during Fruit Ripening%2E Plant Physiol 171%2C 1070%2D1084%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Banana Transcription Factor MaERF11 Recruits Histone Deacetylase MaHDA1 and Represses the Expression of MaACO1 and Expansins during Fruit Ripening&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=Banana Transcription Factor MaERF11 Recruits Histone Deacetylase MaHDA1 and Represses the Expression of MaACO1 and Expansins during Fruit Ripening&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Han,&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Heil%2C M%2E%2C and Baldwin%2C I%2ET%2E %282002%29%2E Fitness costs of induced resistance%3A emerging experimental support for a slippery concept%2E Trends Plant Sci 7%2C 61%2D67%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Fitness costs of induced resistance: emerging experimental support for a slippery concept&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=Fitness costs of induced resistance: emerging experimental support for a slippery concept&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Heil,&as_ylo=2002&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Hellman%2C L%2EM%2E%2C and Fried%2C M%2EG%2E %282007%29%2E Electrophoretic mobility shift assay %28EMSA%29 for detecting protein%2Dnucleic acid interactions%2E Nat Protoc 2%2C 1849%2D1861%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Electrophoretic mobility shift assay (EMSA) for detecting protein-nucleic acid interactions&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=Electrophoretic mobility shift assay (EMSA) for detecting protein-nucleic acid interactions&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Hellman,&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Henikoff%2C S%2E%2C and Shilatifard%2C A%2E %282011%29%2E Histone modification%3A cause or cog%3F Trends in genetics %3A TIG 27%2C 389%2D396%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Histone modification: cause or cog&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Histone modification: cause or cog&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Henikoff,&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1



Jirage, D., Zhou, N., Cooper, B., Clarke, J.D., Dong, X., and Glazebrook, J. (2001). Constitutive salicylic acid-dependent signaling incpr1 and cpr6 mutants requires PAD4. Plant J 26, 395-407.


Jones, J.D., and Dangl, J.L. (2006). The plant immune system. Nature 444, 323-329.Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Journot-Catalino, N., Somssich, I.E., Roby, D., and Kroj, T. (2006). The transcription factors WRKY11 and WRKY17 act as negativeregulators of basal resistance in Arabidopsis thaliana. Plant Cell 18, 3289-3302.


Jullien, P.E., Katz, A., Oliva, M., Ohad, N., and Berger, F. (2006). Polycomb group complexes self-regulate imprinting of the Polycombgroup gene MEDEA in Arabidopsis. Curr Biol 16, 486-492.


Kalb, R., Latwiel, S., Baymaz, H.I., Jansen, P.W., Muller, C.W., Vermeulen, M., and Muller, J. (2014). Histone H2A monoubiquitinationpromotes histone H3 methylation in Polycomb repression. Nat Struct Mol Biol 21, 569-571.


Kim, M.G., Geng, X., Lee, S.Y., and Mackey, D. (2009). The Pseudomonas syringae type III effector AvrRpm1 induces significantdefenses by activating the Arabidopsis nucleotide-binding leucine-rich repeat protein RPS2. Plant J 57, 645-653.


Kinoshita, T., Yadegari, R., Harada, J.J., Goldberg, R.B., and Fischer, R.L. (1999). Imprinting of the MEDEA polycomb gene in theArabidopsis endosperm. Plant Cell 11, 1945-1952.


Kohler, C., and Hennig, L. (2010). Regulation of cell identity by plant Polycomb and trithorax group proteins. Curr Opin Genet Dev 20,541-547.


Kohler, C., Hennig, L., Bouveret, R., Gheyselinck, J., Grossniklaus, U., and Gruissem, W. (2003). Arabidopsis MSI1 is a component ofthe MEA/FIE Polycomb group complex and required for seed development. EMBO J 22, 4804-4814.


Kunkel, B.N., Bent, A.F., Dahlbeck, D., Innes, R.W., and Staskawicz, B.J. (1993). RPS2, an Arabidopsis disease resistance locusspecifying recognition of Pseudomonas syringae strains expressing the avirulence gene avrRpt2. Plant Cell 5, 865-875.


Lee, M.W., and Yang, Y. (2006). Transient expression assay by agroinfiltration of leaves. Methods Mol Biol 323, 225-229.Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Lewis, L.A., Polanski, K., de Torres-Zabala, M., Jayaraman, S., Bowden, L., Moore, J., Penfold, C.A., Jenkins, D.J., Hill, C., Baxter, L.,Kulasekaran, S., Truman, W., Littlejohn, G., Prusinska, J., Mead, A., Steinbrenner, J., Hickman, R., Rand, D., Wild, D.L., Ott, S.,Buchanan-Wollaston, V., Smirnoff, N., Beynon, J., Denby, K., and Grant, M. (2015). Transcriptional Dynamics Driving MAMP-TriggeredImmunity and Pathogen Effector-Mediated Immunosuppression in Arabidopsis Leaves Following Infection with Pseudomonas syringaepv tomato DC3000. Plant Cell 27, 3038-3064.


Li, X., Clarke, J.D., Zhang, Y., and Dong, X. (2001). Activation of an EDS1-mediated R-gene pathway in the snc1 mutant leads toconstitutive, NPR1-independent pathogen resistance. Mol Plant Microbe Interact 14, 1131-1139.


Lim, M.T., and Kunkel, B.N. (2004). The Pseudomonas syringae type III effector AvrRpt2 promotes virulence independently of RIN4, apredicted virulence target in Arabidopsis thaliana. Plant J 40, 790-798.


Lim, M.T., and Kunkel, B.N. (2005). The Pseudomonas syringae avrRpt2 gene contributes to virulence on tomato. Mol Plant Microbe www.plantphysiol.orgon March 19, 2020 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

http://www.ncbi.nlm.nih.gov/pubmed?term=Huot%2C B%2E%2C Yao%2C J%2E%2C Montgomery%2C B%2EL%2E%2C and He%2C S%2EY%2E %282014%29%2E Growth%2Ddefense tradeoffs in plants%3A a balancing act to optimize fitness%2E Mol Plant 7%2C 1267%2D1287%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Growth-defense tradeoffs in plants: a balancing act to optimize fitness&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=Growth-defense tradeoffs in plants: a balancing act to optimize fitness&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Huot,&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Jirage%2C D%2E%2C Zhou%2C N%2E%2C Cooper%2C B%2E%2C Clarke%2C J%2ED%2E%2C Dong%2C X%2E%2C and Glazebrook%2C J%2E %282001%29%2E Constitutive salicylic acid%2Ddependent signaling in cpr1 and cpr6 mutants requires PAD4%2E Plant J 26%2C 395%2D407%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Constitutive salicylic acid-dependent signaling in cpr1 and cpr6 mutants requires PAD4&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=Constitutive salicylic acid-dependent signaling in cpr1 and cpr6 mutants requires PAD4&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Jirage,&as_ylo=2001&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Jones%2C J%2ED%2E%2C and Dangl%2C J%2EL%2E %282006%29%2E The plant immune system%2E Nature 444%2C 323%2D329%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=The plant immune system&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 plant immune system&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Jones,&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Journot%2DCatalino%2C N%2E%2C Somssich%2C I%2EE%2E%2C Roby%2C D%2E%2C and Kroj%2C T%2E %282006%29%2E The transcription factors WRKY11 and WRKY17 act as negative regulators of basal resistance in Arabidopsis thaliana%2E Plant Cell 18%2C 3289%2D3302%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=The transcription factors WRKY11 and WRKY17 act as negative regulators of basal resistance 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=The transcription factors WRKY11 and WRKY17 act as negative regulators of basal resistance in Arabidopsis thaliana&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Journot-Catalino,&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Jullien%2C P%2EE%2E%2C Katz%2C A%2E%2C Oliva%2C M%2E%2C Ohad%2C N%2E%2C and Berger%2C F%2E %282006%29%2E Polycomb group complexes self%2Dregulate imprinting of the Polycomb group gene MEDEA in Arabidopsis%2E Curr Biol 16%2C 486%2D492%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Polycomb group complexes self-regulate imprinting of the Polycomb group gene MEDEA 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=Polycomb group complexes self-regulate imprinting of the Polycomb group gene MEDEA in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Jullien,&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Kalb%2C R%2E%2C Latwiel%2C S%2E%2C Baymaz%2C H%2EI%2E%2C Jansen%2C P%2EW%2E%2C Muller%2C C%2EW%2E%2C Vermeulen%2C M%2E%2C and Muller%2C J%2E %282014%29%2E Histone H2A monoubiquitination promotes histone H3 methylation in Polycomb repression%2E Nat Struct Mol Biol 21%2C 569%2D571%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Histone H2A monoubiquitination promotes histone H3 methylation in Polycomb repression&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Histone H2A monoubiquitination promotes histone H3 methylation in Polycomb repression&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kalb,&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Kim%2C M%2EG%2E%2C Geng%2C X%2E%2C Lee%2C S%2EY%2E%2C and Mackey%2C D%2E %282009%29%2E The Pseudomonas syringae type III effector AvrRpm1 induces significant defenses by activating the Arabidopsis nucleotide%2Dbinding leucine%2Drich repeat protein RPS2%2E Plant J 57%2C 645%2D653%2E&dopt=abstract

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 type III effector AvrRpm1 induces significant defenses by activating the Arabidopsis nucleotide-binding leucine-rich repeat protein RPS2&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 type III effector AvrRpm1 induces significant defenses by activating the Arabidopsis nucleotide-binding leucine-rich repeat protein RPS2&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kim,&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Kinoshita%2C T%2E%2C Yadegari%2C R%2E%2C Harada%2C J%2EJ%2E%2C Goldberg%2C R%2EB%2E%2C and Fischer%2C R%2EL%2E %281999%29%2E Imprinting of the MEDEA polycomb gene in the Arabidopsis endosperm%2E Plant Cell 11%2C 1945%2D1952%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Imprinting of the MEDEA polycomb gene in the Arabidopsis endosperm&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=Imprinting of the MEDEA polycomb gene in the Arabidopsis endosperm&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kinoshita,&as_ylo=1999&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Kohler%2C C%2E%2C and Hennig%2C L%2E %282010%29%2E Regulation of cell identity by plant Polycomb and trithorax group proteins%2E Curr Opin Genet Dev 20%2C 541%2D547%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Regulation of cell identity by plant Polycomb and trithorax group proteins&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=Regulation of cell identity by plant Polycomb and trithorax group proteins&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kohler,&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Kohler%2C C%2E%2C Hennig%2C L%2E%2C Bouveret%2C R%2E%2C Gheyselinck%2C J%2E%2C Grossniklaus%2C U%2E%2C and Gruissem%2C W%2E %282003%29%2E Arabidopsis MSI1 is a component of the MEA%2FFIE Polycomb group complex and required for seed development%2E EMBO J 22%2C 4804%2D4814%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Arabidopsis MSI1 is a component of the MEA/FIE Polycomb group complex and required for seed development&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=Arabidopsis MSI1 is a component of the MEA/FIE Polycomb group complex and required for seed development&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kohler,&as_ylo=2003&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Kunkel%2C B%2EN%2E%2C Bent%2C A%2EF%2E%2C Dahlbeck%2C D%2E%2C Innes%2C R%2EW%2E%2C and Staskawicz%2C B%2EJ%2E %281993%29%2E RPS2%2C an Arabidopsis disease resistance locus specifying recognition of Pseudomonas syringae strains expressing the avirulence gene avrRpt2%2E Plant Cell 5%2C 865%2D875%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=&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=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kunkel,&as_ylo=1993&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Lee%2C M%2EW%2E%2C and Yang%2C Y%2E %282006%29%2E Transient expression assay by agroinfiltration of leaves%2E Methods Mol Biol 323%2C 225%2D229%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Transient expression assay by agroinfiltration of leaves&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=Transient expression assay by agroinfiltration of leaves&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Lee,&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Lewis%2C L%2EA%2E%2C Polanski%2C K%2E%2C de Torres%2DZabala%2C M%2E%2C Jayaraman%2C S%2E%2C Bowden%2C L%2E%2C Moore%2C J%2E%2C Penfold%2C C%2EA%2E%2C Jenkins%2C D%2EJ%2E%2C Hill%2C C%2E%2C Baxter%2C L%2E%2C Kulasekaran%2C S%2E%2C Truman%2C W%2E%2C Littlejohn%2C G%2E%2C Prusinska%2C J%2E%2C Mead%2C A%2E%2C Steinbrenner%2C J%2E%2C Hickman%2C R%2E%2C Rand%2C D%2E%2C Wild%2C D%2EL%2E%2C Ott%2C S%2E%2C Buchanan%2DWollaston%2C V%2E%2C Smirnoff%2C N%2E%2C Beynon%2C J%2E%2C Denby%2C K%2E%2C and Grant%2C M%2E %282015%29%2E Transcriptional Dynamics Driving MAMP%2DTriggered Immunity and Pathogen Effector%2DMediated Immunosuppression in Arabidopsis Leaves Following Infection with Pseudomonas syringae pv tomato DC3000%2E Plant Cell 27%2C 3038%2D3064%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Transcriptional Dynamics Driving MAMP-Triggered Immunity and Pathogen Effector-Mediated Immunosuppression in Arabidopsis Leaves Following Infection with Pseudomonas syringae pv tomato DC3000&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=Transcriptional Dynamics Driving MAMP-Triggered Immunity and Pathogen Effector-Mediated Immunosuppression in Arabidopsis Leaves Following Infection with Pseudomonas syringae pv tomato DC3000&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Lewis,&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Li%2C X%2E%2C Clarke%2C J%2ED%2E%2C Zhang%2C Y%2E%2C and Dong%2C X%2E %282001%29%2E Activation of an EDS1%2Dmediated R%2Dgene pathway in the snc1 mutant leads to constitutive%2C NPR1%2Dindependent pathogen resistance%2E Mol Plant Microbe Interact 14%2C 1131%2D1139%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Activation of an EDS1-mediated R-gene pathway in the snc1 mutant leads to constitutive, NPR1-independent pathogen resistance&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=Activation of an EDS1-mediated R-gene pathway in the snc1 mutant leads to constitutive, NPR1-independent pathogen resistance&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Li,&as_ylo=2001&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Lim%2C M%2ET%2E%2C and Kunkel%2C B%2EN%2E %282004%29%2E The Pseudomonas syringae type III effector AvrRpt2 promotes virulence independently of RIN4%2C a predicted virulence target in Arabidopsis thaliana%2E Plant J 40%2C 790%2D798%2E&dopt=abstract

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


http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Lim,&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1


Interact 18, 626-633.Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Liu, W.X., Zhang, F.C., Zhang, W.Z., Song, L.F., Wu, W.H., and Chen, Y.F. (2013). Arabidopsis Di19 functions as a transcription factor andmodulates PR1, PR2, and PR5 expression in response to drought stress. Mol Plant 6, 1487-1502.


Mackey, D., Belkhadir, Y., Alonso, J.M., Ecker, J.R., and Dangl, J.L. (2003). Arabidopsis RIN4 is a target of the type III virulence effectorAvrRpt2 and modulates RPS2-mediated resistance. Cell 112, 379-389.


Makarevich, G., Leroy, O., Akinci, U., Schubert, D., Clarenz, O., Goodrich, J., Grossniklaus, U., and Kohler, C. (2006). DifferentPolycomb group complexes regulate common target genes in Arabidopsis. EMBO Rep 7, 947-952.


Margueron, R., and Reinberg, D. (2011). The Polycomb complex PRC2 and its mark in life. Nature 469, 343-349.Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Milla, M.A., Townsend, J., Chang, I.F., and Cushman, J.C. (2006). The Arabidopsis AtDi19 gene family encodes a novel type of Cys2/His2zinc-finger protein implicated in ABA-independent dehydration, high-salinity stress and light signaling pathways. Plant molecularbiology 61, 13-30.


Morel, J.B., and Dangl, J.L. (1997). The hypersensitive response and the induction of cell death in plants. Cell Death Differ 4, 671-683.Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Mukhopadhyay, A., Deplancke, B., Walhout, A.J., and Tissenbaum, H.A. (2008). Chromatin immunoprecipitation (ChIP) coupled todetection by quantitative real-time PCR to study transcription factor binding to DNA in Caenorhabditis elegans. Nat Protoc 3, 698-709.


Pieterse, C.M., Van der Does, D., Zamioudis, C., Leon-Reyes, A., and Van Wees, S.C. (2012). Hormonal modulation of plant immunity.Annual review of cell and developmental biology 28, 489-521.


Ravi, M., and Bondada, R. (2016). Genome Elimination by Tailswap CenH3: In Vivo Haploid Production in Arabidopsis thaliana. MethodsMol Biol 1469, 77-99.


Ravi, M., Marimuthu, M.P., Tan, E.H., Maheshwari, S., Henry, I.M., Marin-Rodriguez, B., Urtecho, G., Tan, J., Thornhill, K., Zhu, F.,Panoli, A., Sundaresan, V., Britt, A.B., Comai, L., and Chan, S.W. (2014). A haploid genetics toolbox for Arabidopsis thaliana. NatCommun 5, 5334.


Robert-Seilaniantz, A., Grant, M., and Jones, J.D. (2011). Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu Rev Phytopathol 49, 317-343.


Saleh, A., Alvarez-Venegas, R., and Avramova, Z. (2008). An efficient chromatin immunoprecipitation (ChIP) protocol for studyinghistone modifications in Arabidopsis plants. Nat Protoc 3, 1018-1025.


Schones, D.E., and Zhao, K. (2008). Genome-wide approaches to studying chromatin modifications. Nature reviews. Genetics 9, 179-191.


Shah, J., Kachroo, P., and Klessig, D.F. (1999). The Arabidopsis ssi1 mutation restores pathogenesis-related gene expression in npr1plants and renders defensin gene expression salicylic acid dependent. Plant Cell 11, 191-206.


Shah, J., Kachroo, P., Nandi, A., and Klessig, D.F. (2001). A recessive mutation in the Arabidopsis SSI2 gene confers SA- and NPR1- www.plantphysiol.orgon March 19, 2020 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

http://www.ncbi.nlm.nih.gov/pubmed?term=Lim%2C M%2ET%2E%2C and Kunkel%2C B%2EN%2E %282005%29%2E The Pseudomonas syringae avrRpt2 gene contributes to virulence on tomato%2E Mol Plant Microbe Interact 18%2C 626%2D633%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=The Pseudomonas syringae avrRpt2 gene contributes to virulence on tomato&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 avrRpt2 gene contributes to virulence on tomato&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Lim,&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Liu%2C W%2EX%2E%2C Zhang%2C F%2EC%2E%2C Zhang%2C W%2EZ%2E%2C Song%2C L%2EF%2E%2C Wu%2C W%2EH%2E%2C and Chen%2C Y%2EF%2E %282013%29%2E Arabidopsis Di19 functions as a transcription factor and modulates PR1%2C PR2%2C and PR5 expression in response to drought stress%2E Mol Plant 6%2C 1487%2D1502%2E&dopt=abstract

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


http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Liu,&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Mackey%2C D%2E%2C Belkhadir%2C Y%2E%2C Alonso%2C J%2EM%2E%2C Ecker%2C J%2ER%2E%2C and Dangl%2C J%2EL%2E %282003%29%2E Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2%2Dmediated resistance%2E Cell 112%2C 379%2D389%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance&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=Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Mackey,&as_ylo=2003&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Makarevich%2C G%2E%2C Leroy%2C O%2E%2C Akinci%2C U%2E%2C Schubert%2C D%2E%2C Clarenz%2C O%2E%2C Goodrich%2C J%2E%2C Grossniklaus%2C U%2E%2C and Kohler%2C C%2E %282006%29%2E Different Polycomb group complexes regulate common target genes in Arabidopsis%2E EMBO Rep 7%2C 947%2D952%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Different Polycomb group complexes regulate common target genes 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=Different Polycomb group complexes regulate common target genes in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Makarevich,&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Margueron%2C R%2E%2C and Reinberg%2C D%2E %282011%29%2E The Polycomb complex PRC2 and its mark in life%2E Nature 469%2C 343%2D349%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=The Polycomb complex PRC2 and its mark in life&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 Polycomb complex PRC2 and its mark in life&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Margueron,&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Milla%2C M%2EA%2E%2C Townsend%2C J%2E%2C Chang%2C I%2EF%2E%2C and Cushman%2C J%2EC%2E %282006%29%2E The Arabidopsis AtDi19 gene family encodes a novel type of Cys2%2FHis2 zinc%2Dfinger protein implicated in ABA%2Dindependent dehydration%2C high%2Dsalinity stress and light signaling pathways%2E Plant molecular biology 61%2C 13%2D30%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=The Arabidopsis AtDi19 gene family encodes a novel type of Cys2/His2 zinc-finger protein implicated in ABA-independent dehydration, high-salinity stress and light signaling pathways&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 Arabidopsis AtDi19 gene family encodes a novel type of Cys2/His2 zinc-finger protein implicated in ABA-independent dehydration, high-salinity stress and light signaling pathways&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Milla,&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Morel%2C J%2EB%2E%2C and Dangl%2C J%2EL%2E %281997%29%2E The hypersensitive response and the induction of cell death in plants%2E Cell Death Differ 4%2C 671%2D683%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=The hypersensitive response and the induction of cell death in 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=The hypersensitive response and the induction of cell death in plants&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Morel,&as_ylo=1997&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Mukhopadhyay%2C A%2E%2C Deplancke%2C B%2E%2C Walhout%2C A%2EJ%2E%2C and Tissenbaum%2C H%2EA%2E %282008%29%2E Chromatin immunoprecipitation %28ChIP%29 coupled to detection by quantitative real%2Dtime PCR to study transcription factor binding to DNA in Caenorhabditis elegans%2E Nat Protoc 3%2C 698%2D709%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Chromatin immunoprecipitation (ChIP) coupled to detection by quantitative real-time PCR to study transcription factor binding to DNA in Caenorhabditis elegans&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=Chromatin immunoprecipitation (ChIP) coupled to detection by quantitative real-time PCR to study transcription factor binding to DNA in Caenorhabditis elegans&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Mukhopadhyay,&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Pieterse%2C C%2EM%2E%2C Van der Does%2C D%2E%2C Zamioudis%2C C%2E%2C Leon%2DReyes%2C A%2E%2C and Van Wees%2C S%2EC%2E %282012%29%2E Hormonal modulation of plant immunity%2E Annual review of cell and developmental biology 28%2C 489%2D521%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Hormonal modulation of plant immunity&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=Hormonal modulation of plant immunity&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Pieterse,&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Ravi%2C M%2E%2C and Bondada%2C R%2E %282016%29%2E Genome Elimination by Tailswap CenH3%3A In Vivo Haploid Production in Arabidopsis thaliana%2E Methods Mol Biol 1469%2C 77%2D99%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Genome Elimination by Tailswap CenH3: In Vivo Haploid Production 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=Genome Elimination by Tailswap CenH3: In Vivo Haploid Production in Arabidopsis thaliana&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ravi,&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Ravi%2C M%2E%2C Marimuthu%2C M%2EP%2E%2C Tan%2C E%2EH%2E%2C Maheshwari%2C S%2E%2C Henry%2C I%2EM%2E%2C Marin%2DRodriguez%2C B%2E%2C Urtecho%2C G%2E%2C Tan%2C J%2E%2C Thornhill%2C K%2E%2C Zhu%2C F%2E%2C Panoli%2C A%2E%2C Sundaresan%2C V%2E%2C Britt%2C A%2EB%2E%2C Comai%2C L%2E%2C and Chan%2C S%2EW%2E %282014%29%2E A haploid genetics toolbox for Arabidopsis thaliana%2E Nat Commun 5%2C 5334%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=A haploid genetics toolbox for 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=A haploid genetics toolbox for Arabidopsis thaliana&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ravi,&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Robert%2DSeilaniantz%2C A%2E%2C Grant%2C M%2E%2C and Jones%2C J%2ED%2E %282011%29%2E Hormone crosstalk in plant disease and defense%3A more than just jasmonate%2Dsalicylate antagonism%2E Annu Rev Phytopathol 49%2C 317%2D343%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism&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=Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Robert-Seilaniantz,&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Saleh%2C A%2E%2C Alvarez%2DVenegas%2C R%2E%2C and Avramova%2C Z%2E %282008%29%2E An efficient chromatin immunoprecipitation %28ChIP%29 protocol for studying histone modifications in Arabidopsis plants%2E Nat Protoc 3%2C 1018%2D1025%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=An efficient chromatin immunoprecipitation (ChIP) protocol for studying histone modifications in Arabidopsis 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=An efficient chromatin immunoprecipitation (ChIP) protocol for studying histone modifications in Arabidopsis plants&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Saleh,&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Schones%2C D%2EE%2E%2C and Zhao%2C K%2E %282008%29%2E Genome%2Dwide approaches to studying chromatin modifications%2E Nature reviews%2E Genetics 9%2C 179%2D191%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Genome-wide approaches to studying chromatin modifications&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=Genome-wide approaches to studying chromatin modifications&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Schones,&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Shah%2C J%2E%2C Kachroo%2C P%2E%2C and Klessig%2C D%2EF%2E %281999%29%2E The Arabidopsis ssi1 mutation restores pathogenesis%2Drelated gene expression in npr1 plants and renders defensin gene expression salicylic acid dependent%2E Plant Cell 11%2C 191%2D206%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=The Arabidopsis ssi1 mutation restores pathogenesis-related gene expression in npr1 plants and renders defensin gene expression salicylic acid dependent&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 Arabidopsis ssi1 mutation restores pathogenesis-related gene expression in npr1 plants and renders defensin gene expression salicylic acid dependent&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Shah,&as_ylo=1999&as_allsubj=all&hl=en&c2coff=1


independent expression of PR genes and resistance against bacterial and oomycete pathogens. Plant J 25, 563-574.Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Simon, J.A., and Kingston, R.E. (2013). Occupying chromatin: Polycomb mechanisms for getting to genomic targets, stoppingtranscriptional traffic, and staying put. Mol Cell 49, 808-824.


Singh, V., Roy, S., Singh, D., and Nandi, A.K. (2014). Arabidopsis flowering locus D influences systemic-acquired-resistance- inducedexpression and histone modifications of WRKY genes. J Biosci 39, 119-126.


Singh, V., Roy, S., Giri, M.K., Chaturvedi, R., Chowdhury, Z., Shah, J., and Nandi, A.K. (2013). Arabidopsis thaliana FLOWERING LOCUSD is required for systemic acquired resistance. Mol Plant Microbe Interact 26, 1079-1088.


Spoel, S.H., and Dong, X. (2012). How do plants achieve immunity? Defence without specialized immune cells. Nat Rev Immunol 12, 89-100.


Stewart, F.J., Panne, D., Bickle, T.A., and Raleigh, E.A. (2000). Methyl-specific DNA binding by McrBC, a modification-dependentrestriction enzyme. Journal of molecular biology 298, 611-622.


Swain, S., Singh, N., and Nandi, A.K. (2015). Identification of plant defence regulators through transcriptional profiling of Arabidopsisthaliana cdd1 mutant. J Biosci 40, 137-146.


Swain, S., Roy, S., Shah, J., Van Wees, S., Pieterse, C.M., and Nandi, A.K. (2011). Arabidopsis thaliana cdd1 mutant uncouples theconstitutive activation of salicylic acid signalling from growth defects. Mol Plant Pathol 12, 855-865.


Tian, D., Traw, M.B., Chen, J.Q., Kreitman, M., and Bergelson, J. (2003). Fitness costs of R-gene-mediated resistance in Arabidopsisthaliana. Nature 423, 74-77.


Waadt, R., Schmidt, L.K., Lohse, M., Hashimoto, K., Bock, R., and Kudla, J. (2008). Multicolor bimolecular fluorescencecomplementation reveals simultaneous formation of alternative CBL/CIPK complexes in planta. Plant J 56, 505-516.


Yadegari, R., Kinoshita, T., Lotan, O., Cohen, G., Katz, A., Choi, Y., Nakashima, K., Harada, J.J., Goldberg, R.B., Fischer, R.L., and Ohad,N. (2000). Mutations in the FIE and MEA genes that encode interacting polycomb proteins cause parent-of-origin effects on seeddevelopment by distinct mechanisms. Plant Cell 12, 2367-2382.


Yaish, M.W., Peng, M., and Rothstein, S.J. (2014). Global DNA methylation analysis using methyl-sensitive amplification polymorphism(MSAP). Methods Mol Biol 1062, 285-298.


Zhang, J., and Zhou, J.M. (2010). Plant immunity triggered by microbial molecular signatures. Mol Plant 3, 783-793.Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Zhang, X., Henriques, R., Lin, S.S., Niu, Q.W., and Chua, N.H. (2006a). Agrobacterium-mediated transformation of Arabidopsis thalianausing the floral dip method. Nat Protoc 1, 641-646.


Zhang, Y., Cheng, Y.T., Qu, N., Zhao, Q., Bi, D., and Li, X. (2006b). Negative regulation of defense responses in Arabidopsis by twoNPR1 paralogs. Plant J 48, 647-656.



http://www.ncbi.nlm.nih.gov/pubmed?term=Shah%2C J%2E%2C Kachroo%2C P%2E%2C Nandi%2C A%2E%2C and Klessig%2C D%2EF%2E %282001%29%2E A recessive mutation in the Arabidopsis SSI2 gene confers SA%2D and NPR1%2Dindependent expression of PR genes and resistance against bacterial and oomycete pathogens%2E Plant J 25%2C 563%2D574%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=A recessive mutation in the Arabidopsis SSI2 gene confers SA- and NPR1-independent expression of PR genes and resistance against bacterial and oomycete pathogens&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=A recessive mutation in the Arabidopsis SSI2 gene confers SA- and NPR1-independent expression of PR genes and resistance against bacterial and oomycete pathogens&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Shah,&as_ylo=2001&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Simon%2C J%2EA%2E%2C and Kingston%2C R%2EE%2E %282013%29%2E Occupying chromatin%3A Polycomb mechanisms for getting to genomic targets%2C stopping transcriptional traffic%2C and staying put%2E Mol Cell 49%2C 808%2D824%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Occupying chromatin: Polycomb mechanisms for getting to genomic targets, stopping transcriptional traffic, and staying put&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=Occupying chromatin: Polycomb mechanisms for getting to genomic targets, stopping transcriptional traffic, and staying put&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Simon,&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Singh%2C V%2E%2C Roy%2C S%2E%2C Singh%2C D%2E%2C and Nandi%2C A%2EK%2E %282014%29%2E Arabidopsis flowering locus D influences systemic%2Dacquired%2Dresistance%2D induced expression and histone modifications of WRKY genes%2E J Biosci 39%2C 119%2D126%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Arabidopsis flowering locus D influences systemic-acquired-resistance- induced expression and histone modifications of WRKY genes&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=Arabidopsis flowering locus D influences systemic-acquired-resistance- induced expression and histone modifications of WRKY genes&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Singh,&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Singh%2C V%2E%2C Roy%2C S%2E%2C Giri%2C M%2EK%2E%2C Chaturvedi%2C R%2E%2C Chowdhury%2C Z%2E%2C Shah%2C J%2E%2C and Nandi%2C A%2EK%2E %282013%29%2E Arabidopsis thaliana FLOWERING LOCUS D is required for systemic acquired resistance%2E Mol Plant Microbe Interact 26%2C 1079%2D1088%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Arabidopsis thaliana FLOWERING LOCUS D is required for systemic acquired resistance&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=Arabidopsis thaliana FLOWERING LOCUS D is required for systemic acquired resistance&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Singh,&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Spoel%2C S%2EH%2E%2C and Dong%2C X%2E %282012%29%2E How do plants achieve immunity%3F Defence without specialized immune cells%2E Nat Rev Immunol 12%2C 89%2D100%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=How do plants achieve immunity&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=How do plants achieve immunity&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Spoel,&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Stewart%2C F%2EJ%2E%2C Panne%2C D%2E%2C Bickle%2C T%2EA%2E%2C and Raleigh%2C E%2EA%2E %282000%29%2E Methyl%2Dspecific DNA binding by McrBC%2C a modification%2Ddependent restriction enzyme%2E Journal of molecular biology 298%2C 611%2D622%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Methyl-specific DNA binding by McrBC, a modification-dependent restriction enzyme&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=Methyl-specific DNA binding by McrBC, a modification-dependent restriction enzyme&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Stewart,&as_ylo=2000&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Swain%2C S%2E%2C Singh%2C N%2E%2C and Nandi%2C A%2EK%2E %282015%29%2E Identification of plant defence regulators through transcriptional profiling of Arabidopsis thaliana cdd1 mutant%2E J Biosci 40%2C 137%2D146%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Identification of plant defence regulators through transcriptional profiling of Arabidopsis thaliana cdd1 mutant&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=Identification of plant defence regulators through transcriptional profiling of Arabidopsis thaliana cdd1 mutant&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Swain,&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Swain%2C S%2E%2C Roy%2C S%2E%2C Shah%2C J%2E%2C Van Wees%2C S%2E%2C Pieterse%2C C%2EM%2E%2C and Nandi%2C A%2EK%2E %282011%29%2E Arabidopsis thaliana cdd1 mutant uncouples the constitutive activation of salicylic acid signalling from growth defects%2E Mol Plant Pathol 12%2C 855%2D865%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Arabidopsis thaliana cdd1 mutant uncouples the constitutive activation of salicylic acid signalling from growth defects&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=Arabidopsis thaliana cdd1 mutant uncouples the constitutive activation of salicylic acid signalling from growth defects&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Swain,&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Tian%2C D%2E%2C Traw%2C M%2EB%2E%2C Chen%2C J%2EQ%2E%2C Kreitman%2C M%2E%2C and Bergelson%2C J%2E %282003%29%2E Fitness costs of R%2Dgene%2Dmediated resistance in Arabidopsis thaliana%2E Nature 423%2C 74%2D77%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Fitness costs of R-gene-mediated resistance 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=Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Tian,&as_ylo=2003&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Waadt%2C R%2E%2C Schmidt%2C L%2EK%2E%2C Lohse%2C M%2E%2C Hashimoto%2C K%2E%2C Bock%2C R%2E%2C and Kudla%2C J%2E %282008%29%2E Multicolor bimolecular fluorescence complementation reveals simultaneous formation of alternative CBL%2FCIPK complexes in planta%2E Plant J 56%2C 505%2D516%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Multicolor bimolecular fluorescence complementation reveals simultaneous formation of alternative CBL/CIPK complexes in planta&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=Multicolor bimolecular fluorescence complementation reveals simultaneous formation of alternative CBL/CIPK complexes in planta&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Waadt,&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Yadegari%2C R%2E%2C Kinoshita%2C T%2E%2C Lotan%2C O%2E%2C Cohen%2C G%2E%2C Katz%2C A%2E%2C Choi%2C Y%2E%2C Nakashima%2C K%2E%2C Harada%2C J%2EJ%2E%2C Goldberg%2C R%2EB%2E%2C Fischer%2C R%2EL%2E%2C and Ohad%2C N%2E %282000%29%2E Mutations in the FIE and MEA genes that encode interacting polycomb proteins cause parent%2Dof%2Dorigin effects on seed development by distinct mechanisms%2E Plant Cell 12%2C 2367%2D2382%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Mutations in the FIE and MEA genes that encode interacting polycomb proteins cause parent-of-origin effects on seed development by distinct mechanisms&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=Mutations in the FIE and MEA genes that encode interacting polycomb proteins cause parent-of-origin effects on seed development by distinct mechanisms&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yadegari,&as_ylo=2000&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Yaish%2C M%2EW%2E%2C Peng%2C M%2E%2C and Rothstein%2C S%2EJ%2E %282014%29%2E Global DNA methylation analysis using methyl%2Dsensitive amplification polymorphism %28MSAP%29%2E Methods Mol Biol 1062%2C 285%2D298%2E&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Global DNA methylation analysis using methyl-sensitive amplification polymorphism (MSAP)&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Global DNA methylation analysis using methyl-sensitive amplification polymorphism (MSAP)&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yaish,&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhang%2C J%2E%2C and Zhou%2C J%2EM%2E %282010%29%2E Plant immunity triggered by microbial molecular signatures%2E Mol Plant 3%2C 783%2D793%2E&dopt=abstract

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

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http://www.ncbi.nlm.nih.gov/pubmed?term=Zhang%2C X%2E%2C Henriques%2C R%2E%2C Lin%2C S%2ES%2E%2C Niu%2C Q%2EW%2E%2C and Chua%2C N%2EH%2E %282006a%29%2E Agrobacterium%2Dmediated transformation of Arabidopsis thaliana using the floral dip method%2E Nat Protoc 1%2C 641%2D646%2E&dopt=abstract



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http://www.ncbi.nlm.nih.gov/pubmed?term=Zhang%2C Y%2E%2C Cheng%2C Y%2ET%2E%2C Qu%2C N%2E%2C Zhao%2C Q%2E%2C Bi%2C D%2E%2C and Li%2C X%2E %282006b%29%2E Negative regulation of defense responses in Arabidopsis by two NPR1 paralogs%2E Plant J 48%2C 647%2D656%2E&dopt=abstract



http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang,&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1


short title: medea attenuates pathogen defense in arabidopsis … · 16 jawaharlal nehru university...

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