AVR2 targets BSL family members, which act as ......Feb 19, 2019 · 9 Invergowrie, Dundee DD2 5DA, UK. 10 2Key Laboratory of Horticultural Plant Biology (HZAU), Ministry of Education,

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Short title: PiAVR2 Suppresses Host Immunity 1

AVR2 targets BSL family members, which act as susceptibility 2

factors to suppress host immunity 3

Dionne Turnbull1§, Haixia Wang1,2§, Susan Breen1,3,4, Marek Malec5, Shaista 4

Naqvi1, Lina Yang1,3,6, Lydia Welsh3, Piers Hemsley1,3, Tian Zhendong2, Frederic 5

Brunner5,7, Eleanor M Gilroy3, Paul RJ Birch1,3* 6

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1Division of Plant Science, School of Life Science, University of Dundee (at JHI), 8

Invergowrie, Dundee DD2 5DA, UK. 9

2Key Laboratory of Horticultural Plant Biology (HZAU), Ministry of Education, Key 10

Laboratory of Potato Biology and Biotechnology, Ministry of Agriculture, Huazhong 11

Agricultural University, Wuhan, Hubei, 430070, China. 12

3Cell and Molecular Science, James Hutton Institute, Invergowrie, Dundee DD2 5DA, 13

UK. 14

4Current Address: Life Sciences, University of Warwick, Coventry CV4 7AL, UK 15

5Department of Biochemistry, Centre for Plant Molecular Biology, Eberhard Karls 16

University, Auf der Morgenstelle 32, D-72076 Tübingen, Germany 17

6Fujian Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian 18

Agricultural and Forestry University, Fuzhou, Fujian 350002, China 19

7Current Address: Plant Response Biotech, S.L., Centre for Plant Biotechnology and 20

Genomics (CBGP), Campus de Montegancedo, 28223 Pozuelo de Alarcón, Madrid, 21

Spain. 22

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§These authors contributed equally 25

*To whom correspondence should be addressed: [email protected] 26

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One-sentence summary: Late blight pathogen Phytophthora infestans uses effector 28

Avr2 to target BSL phosphatases to suppress plant immunity. 29

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Author Contributions 31

PRJB, EMG, FB, TZ, and PH designed the research; DT, HW, SB, MM, SN, LY 32

and LW performed the research; DT, HW, SB, MM, SN and LY analysed the 33

data; and DT, HW, EMG and PRJB wrote the paper with input from all co-34

authors. 35

Plant Physiology Preview. Published on February 19, 2019, as DOI:10.1104/pp.18.01143

Copyright 2019 by the American Society of Plant Biologists

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Summary (175 words) 36

To be successful plant pathogens, microbes use “effector proteins” to manipulate 37

host functions to their benefit. Identifying host targets of effector proteins and 38

characterizing their role in the infection process allow us to better understand plant–39

pathogen interactions and the plant immune system. Yeast two-hybrid and 40

coimmunoprecipitation were used to demonstrate that the Phytophthora infestans 41

effector PiAVR2 interacts with all three BSU1-like (BSL) family members from potato 42

(Solanum tuberosum). Transient expression of BSL1, 2, and 3 enhanced P. 43

infestans leaf infection. BSL1 and BSL3 suppressed INF1 elicitin-triggered cell 44

death, showing that they negatively regulate immunity. Virus-induced gene silencing 45

studies revealed that BSL2 and 3 are required for BSL1 stability and show that basal 46

levels of immunity are increased in BSL-silenced plants. Immune suppression by 47

BSL family members is dependent on the brassinosteroid-responsive host 48

transcription factor CHL1. The P. infestans effector PiAVR2 targets all three BSL 49

family members in the crop plant S. tuberosum. These phosphatases, known for 50

their role in growth-promoting brassinosteroid signaling, all support P. infestans 51

virulence and thus can be regarded as susceptibility factors in late blight infection. 52

53

Keywords: Plant immunity; Effector-triggered susceptibility; Plant disease; Late 54

blight; Virulence; Plant pathogens; Pathogenicity 55

Introduction: 1321 words 56

Results: 1702 words 57

Discussion: 977 words 58

Figures: 8 59

Supplementary items: 6 60

61



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INTRODUCTION 62

Plants are constantly challenged by microbes, such as bacteria, fungi, and 63

oomycetes, the majority of which are nonpathogenic by virtue of the highly effective 64

plant immune system. However, those that do cause disease have the potential to 65

devastate crop yields, with pathogens responsible for 10-16 % loss of our global 66

harvest (Chakraborty and Newton, 2011). Faced with the challenge of increasing 67

food production to feed a growing population, our research seeks to understand the 68

complexity of plant-pathogen interactions: How does a pathogen cause disease, and 69

how does the plant recognize and respond to it? The plant immune system can be 70

triggered in two main ways: first, by detection of broadly conserved 71

microbe/pathogen-associated molecular patterns (MAMPs/PAMPs), which may be 72

structural elements, such as bacterial flagellin and fungal chitin, or secreted proteins, 73

such as the oomycete elicitin INF1. MAMPs/PAMPs are recognized by 74

transmembrane proteins called pattern recognition receptors (PRRs) to elicit pattern-75

triggered immunity (PTI) (Jones and Dangl 2006). Second, specific pathogen 76

“effector proteins” can be perceived either directly or indirectly by resistance (R) 77

proteins, activating effector-triggered immunity (ETI). Immune activation can trigger 78

considerable physiological change in the plant, including differential gene 79

transcription, MAPK activation, production of reactive oxygen species, callose 80

deposition, and a form of programmed cell death called the hypersensitive response 81

(HR) (Feechan et al. 2015). ETI is also associated with systemic acquired resistance 82

(SAR), in which pathogen recognition results in systemic signaling to prime the 83

whole plant for defense (Durrant and Dong, 2004). 84

The effector protein repertoire can be viewed as a pathogen “toolkit,” a combination 85

of secreted proteins that facilitate manipulation of the host plant to the advantage of 86

the microbe. Effectors play a variety of roles in pathogenicity, from suppressing the 87

plant immune response, to providing physical and metabolic alterations that support 88

infection. Immune suppression can be broadly achieved in two ways: either by 89

reducing the activity of a positive immune regulator or by enhancing the function of a 90

negative immune regulator. The late blight pathogen Phytophthora infestans has 91

been shown to use both strategies to achieve virulence (Whisson et al 2016). 92

Whereas the RXLR effectors AVR3a, PexRD2, Pi03192, and SFI3 reduce defenses 93

by means of interaction with positive regulators of immunity (Bos et al., 2010; Gilroy 94



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et al., 2011a; King et al., 2014; McLellan et al., 2013; He et al 2018a), recent 95

research has shown that RXLR effectors Pi04089, Pi04314, Pi02860, and Pi17316 96

interact with negative regulators of immunity (Wang et al., 2015; Boevink et al, 97

2016a; Yang et al., 2016; Murphy et al., 2018; He et al. 2018b). These effector 98

targets are capable of attenuating P. infestans infection when silenced, increasing P. 99

infection colonization when overexpressed, or both, classifying them as 100

“susceptibility (S) factors” in late blight infection (Whisson et al., 2016; Boevink et al., 101

2016b; Van Schie and Takken, 2014). 102

Phytohormones, such as salicylic acid, ethylene, and brassinosteroids, are intrinsic 103

to integrating environmental cues. While initially recognized for their effects on plant 104

growth and development, they are also perceived to play important roles in defense 105

and immunity, such as SA-mediated resistance to biotrophic pathogens and 106

ethylene/jasmonic acid signaling associated with resistance to necrotrophs. 107

Hormone signaling pathways do not function in isolation, and both complementary 108

and opposing effects have been described. The negative crosstalk between growth-109

promoting brassinosteroid signaling and the plant immune response is well 110

characterized. Brassinosteroid signaling begins at the plasma membrane with the 111

perception of brassinosteroid hormone (BR) by the receptor-like kinase BR 112

INSENSITIVE1 (BRI1) (Li and Chory, 1997). BR induces BRI1 dimerization, hetero-113

oligomerization, and transphosphorylation of the coreceptor BAK1 (Li et al., 2002; 114

Nam and Li 2002), as well as phosphorylation and subsequent dissociation of the 115

negative regulators BKI1 and BIK1 (Wang and Chory, 2006; Lin et al., 2013). 116

Activated BRI1 phosphorylates the cytoplasmic RLKs CDG1 and the BSK family 117

(Kim et al., 2011; Tang et al., 2008), which proceed to phosphorylate a family of 118

kelch-repeat phosphatase proteins. The best characterized of these is bri1 119

SUPPRESSOR1 (BSU1) in Arabidopsis (Arabidopsis thaliana), with other family 120

members designated BSU1-like 1 (BSL1), BSL2, and BSL3 (Mora-Garcia et al., 121

2004; Kim et al., 2009). The family is collectively referred to as the BSL family 122

throughout this article. In addition to likely unknown substrates, the BSL family 123

dephosphorylates and deactivates the glycogen synthase kinase 124

BRASSINOSTEROID-INSENSITIVE2 (BIN2) (Nam and Li, 2002), allowing 125

PROTEIN PHOSPHATASE 2A (PP2A) to dephosphorylate the homologous 126

transcription factors BRASSINOAZOLE RESISTANT1 (BRZ1) and bri1-EMS 127



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SUPPRESSOR1 (BES1), which can then participate in gene regulation events in the 128

nucleus (Tang et al., 2011). BR-induced transcriptional changes include those linked 129

to cell expansion and growth, light signaling and photomorphogenesis, as well as 130

regulation of other hormone signaling pathways such as auxin and ethylene (Goda et 131

al., 2002; Mussig et al., 2002). 132

The inverse correlation between growth and immune function was initially postulated 133

to be a result of competition for the shared coreceptor BAK1, which, in addition to 134

being required for BR signaling, is also required for immune signaling by PRRs such 135

as FLS2, EFR, and ELR (Chapparo-Garcia et al., 2011, Chinchilla et al., 2007; Du et 136

al., 2015). However, this was not the case, as BAK1 was shown not to be the rate-137

limiting factor between brassinosteroid and immune signaling (Albrecht et al., 2011). 138

More recently, BR immune antagonism has been attributed to transcription factors 139

downstream of BR perception. BZR1 activation has been shown to inhibit PTI 140

responses, with an overrepresentation of defense-related genes under its 141

transcriptional control (Lozano-Duran et al., 2013). BZR1 upregulates several bHLH 142

transcription factors that act as negative regulators of immunity in Arabidopsis, such 143

as CIB1, HBI1, and BEE2. This crosstalk is bidirectional; while these transcription 144

factors are positively regulated by BR signaling, they are down-regulated by PAMP 145

perception (Malinovsky et al., 2014). 146

The large, repeat-rich genome of P. infestans boasts more than 500 RXLR effector 147

gene candidates (Haas et al. 2009; Vleeshouwers et al. 2011), with only a minority of 148

these characterized to date. One of these effectors is PiAVR2, recognized by the 149

potato resistance protein R2 from Solanum demissum (Gilroy et al., 2011b). PiAVR2 150

interacts with the plant phosphatase StBSL1, and this interaction is a prerequisite for 151

R2-mediated HR (Saunders et al., 2012). Our recent work has shown that PiAVR2 152

functions to exploit growth/immune crosstalk by upregulating brassinosteroid 153

pathway signaling to attenuate the immune response (Turnbull and Yang et al., 154

2017). Markers of BR signaling were shown to be increased in PiAVR2-expressing 155

transgenic potato, with one of these, StCHL1, identified as a transcriptional regulator 156

capable of suppressing innate immunity. Notably, silencing of BSL1 has neither a 157

developmental nor a virulence phenotype, with P. infestans able to infect as normal 158

(Saunders et al., 2012). This raised the possibility of StBSL1 acting as a decoy (Van 159



6

der Hoorn and Kamoun, 2008), involved solely in the recognition of PiAVR2 by R2 160

rather than playing a role in plant development. 161

Data presented here show that PiAVR2 interacts not only with StBSL1, but also with 162

the other family members, StBSL2 and StBSL3. This interaction requires a specific 163

C-terminal region of the PiAVR2 protein, without which the effector is stripped of its 164

virulence function and is no longer recognized by the resistance protein R2. 165

Furthermore, all three phosphatases are capable of enhancing P. infestans virulence 166

when overexpressed, identifying the StBSL proteins as susceptibility factors in late 167

blight infection. However, this is not a straightforward case of redundancy; there are 168

functional differences and regulatory interactions between BSL family members at 169

both the gene expression and the protein levels. In addition, INF1 cell death 170

suppression by StBSL1 and StBSL3 is shown to require the bHLH transcription 171

factor StCHL1, recently shown to function downstream of BR signaling as a 172

suppressor of immunity (Turnbull and Yang et al., 2017). This work builds upon 173

previous functional characterization of the P. infestans effector PiAVR2, revealing 174

additional complexity in its host targets, the StBSL phosphatases, and provides 175

insight into how this oomycete effector tips the balance between growth and 176

immunity in favor of disease. 177

178

RESULTS (1702 words) 179

PIAVR2 interacts with the BSL family in Solanum tuberosum 180

The kelch-phosphatase StBSL1 was originally identified as a target of PiAVR2 in 181

both potato and tomato (Saunders et al., 2012). A yeast two-hybrid (Y2H) library of 182

cDNA made from potato infected with P. infestans (Bos et al., 2010) was screened 183

with a GAL4 DNA binding domain-PiAVR2 fusion (“bait”) construct to a depth of 9 x 184

106 yeast cotransformants. Four independent yeast colonies recovered from 185

selection plates that contained GAL4 activation domain (“prey”) fusions yielded 186

sequences encoding StBSL3. In Arabidopsis, this family consists of four members: 187

AtBSL1, 2, and 3, and BSU1. The bulk of research to date has focused on AtBSU1 188

with all four members linked to brassinosteroid pathway signaling (Kim et al., 2009, 189

2011; Mora-Garcia et al., 2004). BLAST analysis of the Solanum tuberosum genome 190

revealed only three family members in potato, with homologs of AtBSL1, 2, and 3 191



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identified but no homolog of AtBSU1, which is regarded as Brassicaceae specific 192

(Maselli et al., 2014) (Supplemental Figure S1). Y2H analysis revealed that not only 193

full-length StBSL1, but also StBSL2 and StBSL3, interacted with the effector PiAVR2 194

while showing no interaction with the control effector Pi08949 (Figure 1A). This was 195

confirmed in planta using coimmunoprecipitation, which again showed all three 196

family members to specifically interact with PiAVR2, but not PiAVR3a (Figure 1B), 197

which was selected as a control as it shares a cytoplasmic localisation with PiAVR2 198

in planta (Bos et al., 2010). 199

Interaction with the BSL family is essential for PIAVR2 virulence function 200

To identify a minimal region of PiAVR2 required for BSL interaction, a series of 201

deletion constructs were generated (Figure S2) and GFP tagged for use in 202

coimmunoprecipitation. Residues 1-65 were shown to be dispensable, with fragment 203

66-116 still able to facilitate interaction between PiAVR2 and all three BSLs (Figure 204

2A). Further deletion of residues 101-116 to give PiAVR2 66-100 abolished PiAVR2-205

BSL interaction (Figure 2A), suggesting that this 16-amino acid region is essential 206

for binding. It may contain the site of binding itself or potentially be a critical region 207

for maintaining the required protein conformation necessary for AVR2-BSL 208

interaction. 209

Many effectors play a role in pathogenicity by means of immune suppression. 210

Recognition of the oomycete elicitin INF1, leading to localized cell death, can be 211

used as a readout for successful immune signaling (Kamoun et al., 1997; Du et al., 212

2015). PiAVR2 has been shown previously to suppress INF1-triggered cell death 213

(ICD) (Turnbull and Yang et al., 2017), as do several other characterized P. infestans 214

effectors, such as PiAVR3a, Pi18215, Pi02860, and Pi17316 (Bos et al. 2010; Zheng 215

et al 2014; Yang et al., 2016; Murphy et al., 2018; He et al. 2018b). Transient 216

coexpression of INF1 with full-length and truncated forms of PiAVR2 was used to 217

assess the extent of immune suppression. PiAVR2 66-116 was shown to suppress 218

ICD to the same extent as the full-length effector (Figure 2B). However, removal of 219

residues 100-116 rendered PiAVR2 unable to suppress ICD (Figure 2B). Crucially, 220

this also translates into pathogenicity, with transient expression of PiAVR2 66-100 221

providing no enhancement of P. infestans colonization on Nicotiana benthamiana 222

(Figure 2C), whereas PiAVR2 66-116 expression facilitated a significant increase in 223

lesion size, comparable to the full-length effector. 224



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StBSL1 has been shown to be required for PiAVR2 recognition by the NB-LRR 225

protein R2, with BSL1 silencing in N. benthamiana resulting in a significant decrease 226

in R2-mediated hypersensitive response (HR) (Saunders et al., 2012). Figure 2D 227

supports a model in which PiAVR2-BSL interaction is required for R2 activation. 228

PiAVR2 66-116, which maintains BSL interaction, is recognized to the same extent 229

as the full-length effector triggering a full HR. In contrast, PiAVR2 66-100 is unable to 230

trigger R2-mediated HR, suggesting that impaired BSL interaction has abolished 231

effector recognition. 232

BSL-silenced plants show enhanced immune responses 233

Virus-induced gene silencing (VIGS) constructs were designed to transiently reduce 234

expression of the BSL genes in N. benthamiana (Saunders et al., 2012; this study). 235

High sequence similarity prevented the design of NbBSL2 and NbBSL3-specific 236

silencing constructs, so dual-silencing constructs were generated to reduce both 237

NbBSL2 and NbBSL3 expression simultaneously. NbBSL1-silenced plants appeared 238

phenotypically normal, whereas NbBSL2/3-silenced plants exhibited severe 239

dwarfism with short petioles and curled, brittle leaves (Figure S3), reminiscent of 240

AtBRI1 knockout mutants in the literature (Clouse et al., 1996; Noguchi et al., 1999). 241

Reverse transcription quantitative PCR (RT-qPCR) confirmed effective silencing of 242

the NbBSLs using these constructs and revealed a striking relationship between 243

expression levels of NbBSL1 and NbBSL2/3. When NbBSL1 expression is silenced, 244

NbBSL2 and NbBSL3 transcripts increase between 1.5- and 2-fold. Similarly, when 245

NbBSL2 and NbBSL3 are simultaneously silenced, NbBSL1 transcripts accumulate 246

almost 3-fold (Figure S3). This may be a compensatory or feedback mechanism to 247

attempt to achieve homeostasis of BR signaling in the absence of one or multiple 248

members. However, immunoblot analysis of all three StBSLs in the NbBSL-silenced 249

plants revealed that an increased accumulation of BSL1 transcripts may not 250

necessarily translate into increased protein level. StBSL2 and StBSL3 are 251

undetectable in BSL2/3-silenced plants but remain detectable in BSL1-silenced 252

plants, as expected. Also as anticipated, StBSL1 is undetectable in BSL1-silenced 253

plants. However, unexpectedly, StBSL1 protein was undetectable in NbBSL2/3-254

silenced plants as well (Figure S4). This suggests a regulatory relationship between 255

the BSLs at the protein level; it may be that BSL2, BSL3, or both are required for 256

BSL1 stability, whether directly or indirectly. The NbBSL2/3 silencing construct 257



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effectively creates a BSL-null plant. VIGS construct sequences can be seen in 258

Figure S5. 259

NbBSL-silenced plants were screened for ICD as a readout for strength of immune 260

response. Silencing NbBSL1 resulted in a trend towards an increase in ICD, 261

although this did not reach statistical significance. However, a pronounced increase 262

in ICD was observed in NbBSL2/3-silenced plants (Figure 3). This suggests that 263

negative regulation of PTI has been removed or reduced, allowing a stronger 264

response to PAMP recognition. This increased immune response might be expected 265

to hinder P. infestans infection. Previous work showed NbBSL1 silencing alone to 266

have no clear effect on pathogen virulence (Saunders et al., 2012). To investigate 267

whether NbBSL2/3 silencing, effectively creating a BSL-null scenario, impacts P. 268

infestans pathogenicity, NbBSL2/3-silenced plants were inoculated with zoospore 269

suspension and a variety of infection parameters measured. Percentage of 270

inoculation sites forming lesions, lesion diameter, and number of sporangia 271

recovered all show a striking decrease in successful infection in the absence of the 272

BSLs (Figure 4). 273

274

BSL1, BSL2, and BSL3 are susceptibility factors 275

Pathogen effectors are often responsible for inhibiting the function of target proteins 276

(e.g. King et al., 2014). Previously, we have shown that silencing NbBSL1 had no 277

discernable effect on P. infestans lesion development (Saunders et al., 2012). Here, 278

we show that silencing NbBSL2 and NbBSL3 in combination (indirectly also reducing 279

BSL1 protein level) significantly reduced infection. This suggests that P. infestans 280

would not benefit from negatively affecting BSL function. On the contrary, the 281

pathogen may benefit from increased BSL levels or activity. To determine whether 282

overexpression of the StBSLs has an effect on the plant immune response, we first 283

examined ICD following coexpression of INF1 with free GFP, with GFP-tagged 284

StBSL1/2/3, or with GFP-tagged PiAVR3a as a known suppressor of ICD. Scoring 285

the percentage of ICD reveals StBSL1 to have a strong suppressive effect, StBSL3 286

to have a moderate effect, and BSL2 to have no effect (Figure 5A). To determine 287

the effect of BSL overexpression on P. infestans infection, StBSL1, StBSL2, or 288

StBSL3 was transiently expressed in one half of an N. benthamiana leaf, with free 289



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GFP expressed in the other half, and the leaf was inoculated 1 day later on both 290

sides with zoospore suspension. In each case, expression of StBSL1, StBSL2, or 291

StBSL3 resulted in a significant increase in P. infestans infection (Figure 5B). 292

Together, the VIGS and overexpression studies demonstrate the status of the BSL 293

family as “S factors,” plant proteins that the pathogen requires to reach full infection 294

potential. 295

The ability of PiAVR2 to suppress ICD was further characterized using VIGS of 296

NbBSL1 or NbBSL2/3. While PiAVR3a remains able to suppress ICD regardless of 297

NbBSL1 or NbBSL2/3 silencing, PiAVR2 could suppress ICD only in the NbBSL1-298

silenced plants and not in the NbBSL2/3-silenced plants, which are effectively BSL 299

null (Figure 6). 300

StBSL immune suppression requires the downstream susceptibility factor 301

CHL1 302

Work in our group previously identified the transcription factor StCHL1 as a negative 303

regulator of immunity in N. benthamiana and potato (Turnbull and Yang et al., 2017). 304

CHL1 was shown to suppress ICD and to increase P. infestans leaf infection. 305

Moreover, the ability of PiAVR2 to suppress ICD was dependent on CHL1. To 306

determine whether ICD suppression by BSL1 and BSL3 is also CHL1 dependent, 307

CHL1 was transiently silenced in N. benthamiana, followed by coexpression of INF1 308

plus StBSL1, StBSL3, PiAVR3a, or free GFP as a control. ICD was suppressed by 309

PiAVR3a independent of NbCHL1 silencing. In contrast, StBSL1 and StBSL3 310

showed a significant decrease in ICD suppression on NbCHL1-silenced plants. 311

While StBSL1 was still able to achieve moderate, albeit significantly reduced, 312

suppression in the CHL1-silenced plants, StBSL3 was unable to suppress ICD at all 313

(Figure 7). 314

315

Discussion 316

In this work we have determined that the P. infestans effector PiAVR2 targets all 317

three members of the BSL family in S. tuberosum: StBSL1, StBSL2, and StBSL3 318

(Figure 1). Transient overexpression of each is able to enhance leaf colonization by 319

P. infestans, identifying these proteins as susceptibility (S) factors in late blight 320

infection (Figure 5b). This family of kelch-repeat phosphatases is homologous to 321



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Arabidopsis BSU1, characterized as a positive regulator in the growth-promoting 322

brassinosteroid signaling pathway. Previous work had established that PiAVR2 323

interacts with StBSL1 (Saunders et al., 2012) and that PiAVR2 upregulates 324

brassinosteroid-induced genes, exploiting the crosstalk that exists between growth 325

and immunity in plants (Turnbull and Yang et al., 2017). The main findings of this 326

work are represented in Figure 8. 327

We identified that interaction between PiAVR2 and the StBSL family requires a 328

specific C-terminal region of the effector (Figure 2a). Crucially, loss of this region, 329

and, thus, loss of BSL interaction, strips PiAVR2 of its virulence function. The 330

truncated effector PiAVR2 66-100 can no longer suppress ICD and can no longer 331

enhance P. infestans leaf colonization (Figure 2b, 2c). This region of interest 332

contains sequence similarity to known phosphatase interaction motifs. KKLV 333

(PiAVR2 102-105) is reminiscent of the KKVI of BSU1, recently shown to be required 334

for oligomerization between BSL family members in Arabidopsis (Kim et al., 2015). 335

Another, LKIKG (PiAVR2 108-112), contains the same residues as the PP1 binding 336

sequence KGILK (also referred to as the GILK, or SILK, motif), essential for potent 337

inhibition of PP1 by the inhibitor I2 (Huang et al., 1999; Connor et al., 2000). 338

Phosphatases, in contrast to kinases, are relatively few in number in the plant 339

proteome. Where kinases have increased specificity by means of gene duplication 340

and specialization, phosphatases have achieved diversity by interacting with a large 341

number of regulatory subunits, forming “holoenzymes” (Hendrickx et al., 2009). 342

These regulatory subunits can specify substrate or localization, act as inhibitors or 343

chaperones, or a combination of these roles (Wakula et al., 2003). This raises the 344

possibility that PiAVR2 acts to modify oligomerization between the BSLs, by 345

occluding an interaction site, or perhaps favoring a particular BSL combination. 346

Alternatively, or as a result of this, it may act to enhance or inhibit BSL activity on a 347

particular substrate. Modification of plant phosphatase function by pathogenic 348

effectors is not unprecedented; the P. infestans effector Pi04314 has recently been 349

shown to interact with three PP1c isoforms in potato, resulting in their relocalization 350

from the nucleolus to the nucleoplasm, with PP1c activity required for successful 351

infection (Boevink et al. 2016a). Detailed examination of BSL oligomerization in S. 352

tuberosum, identification of substrates, and analysis of enzymatic activity in the 353



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presence/absence of PiAVR2 will be an important next step in elucidating effector 354

function. 355

While all three StBSL family members interact with PiAVR2, and all enhance 356

pathogen virulence when overexpressed, this is not a straightforward case of 357

functional redundancy. There are several key differences between the BSL family 358

members, which show functional differences as well as regulatory interactions 359

between family members at both the gene expression and protein levels. Particularly 360

striking is the loss of StBSL1 protein in NbBSL2/3-silenced plants, suggesting that 361

BSL2 or 3 is required to maintain BSL1 stability (Figure S4). StBSL2 also presents 362

an interesting discrepancy, showing no ICD suppression while still able to provide a 363

significant enhancement to P. infestans infection (Figure 5). This implies that BSL2 364

mode of action may be distinct from ICD suppression or that PiAVR2 is not simply 365

increasing the normal activity of StBSL2 but may be modifying it to facilitate ICD 366

suppression. 367

We recently showed that PiAVR2 requires the solanaceous transcription factor CHL1 368

for full virulence function (Turnbull and Yang et al., 2017). CHL1 expression is 369

upregulated by brassinosteroid signaling and functions as a negative regulator of 370

plant innate immunity. We revisited NbCHL1 silencing to determine whether ICD 371

suppression by StBSL1 and StBSL3 also requires this transcription factor; while 372

StBSL1 retained some limited ability to suppress cell death, StBSL3 was rendered 373

unable to do so on NbCHL1 VIGS plants (Figure 7). This again highlights 374

differences between the BSLs and may reflect interdependency between family 375

members. If the BSLs function together, as is suggested by the report of 376

oligomerization (Kim et al., 2016), then one protein may require higher levels of the 377

other family members to take full effect. 378

In conclusion, this work identifies the StBSL family as targets of P. infestans PiAVR2, 379

the first filamentous pathogen effector shown to exploit crosstalk between the 380

brassinosteroid pathway and immune signaling in plants. All three phosphatases act 381

as S factors in P. infestans infection, allowing increased disease potential when 382

overexpressed and decreased disease when silenced in combination. The next step 383

will be to elucidate the biochemical mechanism behind PiAVR2-mediated immune 384

suppression and that of R2 recognition. Is BSL phosphatase activity required for 385

immune suppression or PiAVR2 recognition? How does PiAVR2 affect 386



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oligomerization and downstream activity/substrate specificity of the BSL family? This 387

work also raises interesting areas for enquiry with regard to the BSL family 388

members, which do not act with the functional redundancy once thought. Each 389

member of the brassinosteroid signaling cascade is a member of a multigene family, 390

and while redundancy does exist to an extent, the true picture is likely to be more 391

complex with family members potentially playing distinct roles. 392

S factors such as the BSLs present an interesting avenue to explore in terms of 393

breeding for disease resistance. Whilst R protein-mediated resistance is highly 394

effective, it is also highly specific, with success often short-lived due to rapidly 395

evolving pathogen populations. Subtle manipulation of the balance between growth 396

and immunity may be a more indirect way of providing plant protection. Identification 397

of S factors provides insight not only into disease processes, but also into the 398

fundamentals of healthy plant function, knowledge that can be exploited in our 399

ongoing quest for disease resistance and sustainable food security. 400

401

MATERIALS AND METHODS 402

Plant Material 403

N. benthamiana plants were grown in general purpose compost under long-day 404

glasshouse conditions of 16-h light at 22°C, light intensity of 130 to 150 µE m−2 s−1, 405

and 40% humidity. Plants were used for cell death/P. infestans colonization at 4 to 5 406

weeks old. 407

Constructs and cloning 408

StBSL1, 2, and 3 were amplified from S. tuberosum cDNA using gene-specific 409

primers (Eurofins) modified with attB Gateway recombination sites (Invitrogen), 410

before recombination into pDONR201 to generate entry clones by BP reaction (BP 411

clonase, Invitrogen). LR clonase (Invitrogen) was used to recombine genes of 412

interest into pB7WGF2 (N-terminal GFP tag) or pGWB18 (N-terminal myc tag). 413

Primer sequences can be found in Table S1. 414

INF1, GFP-PiAVR2, and GFP-PiAVR3a constructs were generated as previously 415

described (Gilroy et al., 2011a; Gilroy et al, 2011b; Engelhardt et al., 2012). 416

Agrobacterium-mediated transient expression and cell death assays 417



14

Agrobacterium strain AGL1 VirG pSOUP was transformed with the constructs of 418

interest by electroporation and screened by colony PCR. Liquid YEB medium was 419

inoculated with single colonies from plates containing selective antibiotics and 420

incubated with shaking overnight at 28°C. Bacteria were pelleted by centrifugation at 421

4,000 x g for 10 minutes, with the pellet resuspended in 10 mM MES and 10 mM 422

MgCl. OD600 was adjusted as appropriate, and acetosyringone added to 200 µM. 423

Leaves were infiltrated on the abaxial surface, using a 1-ml syringe after needle 424

wounding. 425

For coimmunoprecipitation, western blotting, and cell death assays, cultures were 426

infiltrated at an OD600 of 0.5, with an OD600 of 0.1 used for P. infestans leaf 427

colonization assays. Agrobacterium with the silencing suppressor construct pJL3-428

P19 was coinfiltrated at an OD600 of 0.05. 429

Hypersensitive response/INF1-triggered cell death assays were performed by 430

coinfiltration of the relevant constructs (infiltration site ~1 cm diameter) and scoring 431

sites positive/negative for cell death after 7 days. A positive score was determined as 432

50% or more of the infiltrated area showing cell death. Independent experimental 433

replicates consisted of 6 or more individual plants (biological replicates), with multiple 434

leaves (technical replicates) infiltrated per plant. Data from each biological replicate 435

were used to perform statistical analysis using one-way ANOVA (Newman-Keuls 436

method) in Sigmaplot (Systat Software Inc.). 437

Virus-induced gene silencing 438

VIGS constructs consisted of approximately 250-bp PCR fragments of the gene 439

targeted for silencing, cloned into pBinary Tobacco Rattle Virus (TRV) vectors (Liu et 440

al., 2002). A TRV construct expressing a fragment of GFP was used as a control 441

(Gilroy et al., 2011), and BSL1 and CHL1 constructs were as previously described 442

(Saunders et al., 2012; Turnbull and Yang et al., 2017). BSL2/3 silencing fragments 443

were amplified from N. benthamiana cDNA using the primers BSL2/3-1 F and 444

BSL2/3-1 R, and BSL2/3-2 F and BSL2/3-2 R (see Table S1). To achieve transient 445

silencing, the two largest leaves of N. benthamiana plants at the four-leaf stage were 446

fully syringe infiltrated with a mixture of Agrobacterium strain LBA4404 containing 447

TRV-RNA1 and the silencing fragment of interest, each at an OD600 of 0.25. Viral 448


https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5411136/#bib45



15

infection was allowed to progress systemically for 2 to 3 weeks before the plants 449

were used in experiments. 450

RT-qPCR 451

RNA was extracted from plant tissue using the Qiagen RNeasy Plant Mini Kit, 452

complete with on-column DNase treatment, and used to synthesise cDNA with 453

SuperScript II reverse transcriptase (Invitrogen) both according to the manufacturers’ 454

instructions. RT-qPCR was performed using Maxima SYBR green qPCR mastermix 455

(Thermo Scientific) with detection using a Chromo4 real-time detector with an MJ 456

Research PTC-200 thermal cycler and Opticon Monitor 3.1.32 software (Bio-RAD 457

Laboratories Inc.) Reactions were incubated at 95°C for 15 minutes, followed by 40 458

cycles (95°C for 15 sec, 60°C for 1 min, plate read, hold 5 sec). Data were analyzed 459

using the ΔΔCt method (Schmittgen and Livak, 2008), with expression normalized to 460

the housekeeping gene NbEF1α. Primers were generated by Eurofins MWG Operon, 461

with primer design facilitated by NetPrimer software (PREMIER Biosoft; 462

http://www.premierbiosoft.com/netprimer/) (Table S1). 463

Y2H Assays 464

Y2H screening was carried out using the ProQuest system (Invitrogen). PiAVR2 and 465

the control effector Pi08949 were ligated into the prey vector pDEST22, with StBSL1, 466

StBSL2, and StBSL3 ligated into the bait vector pDEST32. Pairwise interaction was 467

tested using bait and prey to transform the yeast strain MaV203. Transformants were 468

identified by selection on media lacking leucine and tryptophan. These were 469

screened for HIS3 induction and URA3 induction by plating on the appropriate 470

dropout media and for β-galactosidase induction by X-gal assay according to the 471

manufacturer’s instructions. 472

Western blot 473

To examine protein levels, N. benthamiana was infiltrated with the relevant 474

Agrobacterium transformants, with leaf tissue sampled 48 h post-infiltration and 475

immediately frozen in liquid nitrogen. Protein extraction was performed by heating 476

ground tissue samples at 95°C for 10 minutes in 2x SDS gel-loading buffer (100 nM 477

Tris-HCl, pH 6.8, 0.2% bromophenol blue, 20% glycerol, and 4% SDS), followed by 478

centrifugation at 16,000 x g for 5 minutes. Proteins were separated on 4-12% Bis-479

Tris PAGE gels with MES buffer, using an X-blot Mini Cell (Thermo Fisher Scientific 480



16

Ltd.), followed by transfer to nitrocellulose membrane (GE Healthcare Life Sciences) 481

using an X10 Blot Module (Thermo Fisher Scientific Inc.) according to the 482

manufacturer’s instructions. Membranes were stained with Ponceau solution to 483

confirm transfer and even loading. 484

Membranes were blocked in 4% milk in 1x PBS 0.1% Tween (1xPBS-T) with shaking 485

overnight at 4°C, before incubation with the appropriate antibodies (Santa Cruz sc-486

40 and sc-9996). 487

Signal was visualized by incubation with Amersham ECL Prime, on Amersham ECL 488

Hyperfilm (both GE Healthcare Life Sciences), developed with a Compact X4 489

Automatic Processor (Xograph Healthcare Ltd). 490

491

Coimmunoprecipitation 492

For coimmunoprecipitation, proteins were extracted in GTEN buffer (10% vol/vol 493

glycerol, 25 mM Tris-HCl (pH 7.5), 1 mM EDTA, and 150 mM NaCl) with 10 mM 494

DTT, protease inhibitor cocktail, 1 mM phenylmethylsulfonyl fluoride, and 0.2% 495

Nonidet P-40. To immunoprecipitate GFP-tagged proteins, protein extracts were 496

incubated with GFP-Trap_M beads (Chromotek) for 1 hour at 4°C. Beads were 497

washed three times in GTEN buffer with phenylmethylsulfonyl fluoride and protease 498

inhibitor cocktail as above, before resuspending in 2x SDS gel-loading buffer. 499

Samples were then processed by Western blot as described above. 500

P. infestans colonization assays 501

P. infestans strain 88069 expressing fluorescent protein tdTomato (McLellan et al., 502

2013, Saunders et al., 2012) was grown on rye agar supplemented with 20 µg/mL 503

geneticin. Ten-day-old plates were flooded with sterile distilled water and sporangia 504

harvested using a 70-µm cell strainer. The suspension was centrifuged at 3,000 x g 505

for 10 min, supernatant discarded, and pellet resuspended in sterile distilled water. 506

Sporangia were quantified using a haemocytometer and adjusted to 50,000 per mL-1. 507

Droplets (10 µl) were pipetted onto the abaxial surface of detached leaves, placed in 508

sealed boxes with moist tissue to maintain humidity, and kept in darkness for 24 509

hours to reduce UV degradation of inoculum. Lesions were measured at the widest 510

point 7 days post inoculation. 511






17

If required, leaves were infiltrated with appropriate agrobacterium constructs 24 512

hours pre-sporangia inoculation to achieve transient expression of the gene of 513

interest. 514

Data from infection and cell death assays were subjected to statistical analysis using 515

one-way ANOVA (Newman-Keuls method) in Sigmaplot (Systat Software Inc.) 516

Accession Numbers 517

Sequence data from this article can be found in the GenBank/EMBL data libraries under 518

accession numbers XXX. 519

Supplemental Data 520

Supplemental Figure S1. Phylogenetic tree of BSL family members from potato and 521

Arabidopsis. 522

Supplemental Figure S2. Protein alignment of PiAVR2 full length, PiAVR2 66-116 and 523

PiAVR2 66-100. 524

Supplemental Figure S3. NbBSL expression levels and phenotypes of NbBSL1, NbBSL2 and 525

NbBSL3 silenced N. benthamiana. 526

Supplemental Figure S4. Protein stability of 35S promoter-driven GFP-BSL1, GFP-BSL2 527

and GFP-BSL3 transiently expressed in VIGS N. benthamiana plants expressing TRV:BSL1 528

or TRV:BSL2/3 constructs as indicated. 529

Supplemental Figure S5. Nucleotide alignment of the N. benthamiana BSL sequences 530

cloned in TRV constructs with the same region of potato BSL1, 2 and 3. 531

Supplemental Table S1. Primers used in the study. 532

533

Acknowledgements 534

We are grateful for financial support from the Biotechnology and Biological Sciences 535

Research Council (BBSRC) (grants BB/N009967/1, BB/G015244/1, BB/L026880/1), 536

the Scottish Government Rural and Environment Science and Analytical Services 537

Division (RESAS), the National Natural Science Foundation of China (grants 538

31171603, 31471550), the National High Technology Research and Development 539

Program of China (grants 2013AA102603), Fundamental Research Funds for the 540

Central Universities of China (grants, 2662017PY069), and the German Research 541

Foundation (FDG: BR 3875/3-1). 542

543

544

545



18

546

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718

719



23

Figure Legends 720

Fig. 1: PiAVR2 interacts with StBSL1, StBSL2, and StBSL3. 721

(a) Yeast coexpressing BSL1, BSL2, or BSL3 with PiAVR2 grew on -histidine (LTH) medium 722 and yielded β-galactosidase (LacZ) activity, while those coexpressed with the control 723 effector Pi08949 did not. The +HIS (LT) control shows that all yeast were able to grow in the 724 presence of histidine. 725

(b) Immunoprecipitation (IP) of protein extracts from agroinfiltrated leaves using GFP-Trap 726 confirmed that cMYC-StBSL1, cMYC-StBSL2, and cMYC-StBSL3 associated in N. 727 benthamiana with GFP-tagged PiAVR2, but no association was seen with the GFP-PiAVR3a 728 control. Expression of constructs in the leaves is indicated by +. Protein size markers are 729 indicated in kDa, and protein loading is indicated by Ponceau stain (PS). 730

Fig. 2: Interaction with the BSL family is essential for PiAVR2 virulence function. 731 732 a) IP of protein extracts from agroinfiltrated leaves using GFP-Trap confirmed that cMYC-733 StBSL1, cMYC-StBSL2, and cMYC-StBSL3 associated in N. benthamiana with GFP-tagged 734 PiAVR2 and PiAVR2-66_116, but no association was seen with GFP- PiAVR2-66_100. 735 Expression of constructs in the leaves is indicated by +. Protein size markers are indicated in 736 kDa, and protein loading is indicated by Ponceau stain (PS) 737 b) Transient coexpression of GFP-PiAVR2 or truncated forms of PiAVR2 with INF1 738 indicated that PiAVR2 and PiAVR2-66_116 can suppress ICD in N. benthamiana, similar to 739 the GFP-AVR3a control, whereas PiAVR2-66_100 did not. Cell death sites were counted at 740 4 days post infiltration. Results combine data from three independent experimental 741 replicates, each consisting of 8 individual plants (biological replicates), with 3 leaves 742 (technical replicates) infiltrated per plant. 743 c) P. infestans lesion sizes at 8 days post inoculation of sporangia suspension (diameter in 744 mm) following expression of GFP-tagged PiAVR2, PiAVR2-66_116, PiAVR2-66_100, and 745 control GFP. Data shown combine 4 independent experimental replicates, each consisting of 746 18 leaves taken from 6 individual plants, with 4 inoculations per leaf. 747 d) Transient coexpression of GFP-PiAVR2 or truncated forms of PiAVR2 with R2 indicated 748 that PiAVR2 and PiAVR2-66_116 are recognized by R2 in N. benthamiana, whereas 749 PiAVR2-66_100 is not. Cell death sites accounted at 3 days post infiltration. Results 750 combine data from three independent experimental replicates, each consisting of 8 individual 751 plants, with 3 leaves infiltrated per plant. Error bars indicate SEM. Significant difference in 752 (b), (c), and (d) is denoted by letters (p<0.001 in one-way ANOVA, using the Student-753 Newman-Keuls method). 754 755

Fig. 3 Silencing of the BSL family increases INF1-triggered cell death in Nicotiana 756 benthamiana. 757 758 Silencing BSL1 slightly increases ICD, and BSL2/3 significantly accelerates ICD at 4 days 759 post infiltration of Agrobacterium allowing transient expression of INF1. Silencing was 760 achieved using VIGS. Significant difference is denoted by letters (p<0.001 in one-way 761 ANOVA, using the Student-Newman-Keuls method). Results shown are a combination of 762 data from three independent experimental replicates, each consisting of 7 individual plants, 763 with three leaves infiltrated per plant. Error bars indicate SEM. Representative ICD lesions 764 are shown. 765 766 767



24

Fig. 4 VIGS of BSL2 and BSL3 in Nicotiana benthamiana resulted in decreased 768 susceptibility to P. infestans. 769 770 BSL2/3-silenced plants were inoculated with a P. infestans zoospore suspension and a 771 variety of measurements made at 7 day post inoculation: (a) percentage of inoculation sites 772 forming lesions, (b) lesion diameter, and (c) number of sporangia per ml. Results were 773 combined from four independent experimental replicates, each involving 8 individual plants, 774 with three leaves inoculated per plant. Error bars indicate SEM. Significant difference is 775 represented by stars (p<0.01 in one way ANOVA, using the Student-Newman-Keuls 776 method). 777 778 Fig. 5 The BSL family suppresses immunity and enhances P. infestans leaf 779 colonization 780 781 a) INF1-triggered cell death following coexpression of INF1 with GFP-StBSL1, GFP-StBSL2, 782 and GFP-StBSL3 transiently expressed in N. benthamiana. Data are a combination of 3 783 independent experimental replicates, consisting of 8 individual plants, with three leaves 784 infiltrated per plant. Representative ICD lesions are shown. 785 786 b) P. infestans lesion sizes following transient expression of GFP-StBSL1, GFP-StBSL2, and 787 GFP-StBSL3 in N. benthamiana at 8 days post inoculation of sporangia. Data are a 788 combination of 3 independent experimental replicates, each involving 15 leaves from 7 789 individual plants. Significant differences in (a) and (b) are represented by letters (p<0.05 in 790 one-way ANOVA, using the Student-Newman-Keuls method). Error bars indicate SEM. 791 Representative leaf images show the full extent of the lesion under UV light, converted to 792 grayscale. 793 794 Fig. 6 Silencing of BSL2/3 compromises the suppression of INF1-triggered cell death 795 by PiAVR2 in Nicotiana benthamiana. 796 797 Coinfiltration INF1 with GFP-PiAVR2, GFP-PiAVR3a, and GFP control in TRV:BSL1, 798 TRV:BSL2/3, and TRV:GFP plants. Cell death sites were counted at 5 days post infiltration. 799 Significant difference was represented by letters (p<0.001 in one-way ANOVA, using the 800 Student-Newman-Keuls method). Results are combined data across three independent 801 experimental replicates, consisting of 7 individual plants, with 3 leaves infiltrated per plant. 802 Error bars indicate SEM. 803 804 Fig. 7: Silencing of CHL1 attenuated the suppression of INF1-triggered cell death by 805 GFP-BSL1 and GFP-BSL3 in Nicotiana benthamiana. 806 807 INF1 was coinfiltrated with GFP-StBSL1, GFP-StBSL3, GFP-AVR3a, and GFP control in 808 TRV:CHL1 and TRV:GFP control plants. Cell death sites were counted at 5 days post 809 infiltration. Significant difference is represented by letters (p<0.001 in one-way ANOVA, 810 using the Student-Newman-Keuls method). Results shown are combined data across three 811 independent biological replicates, each consisting of 7 individual plants, with 3 leaves 812 infiltrated per plant. Error bars indicate SEM. 813

814

Fig. 8: Schematic diagram illustrating main findings of this work. 815

AVR2 is an RXLR effector secreted into the plant by P. infestans, where it interacts with the 816 kelch-repeat phosphatases StBSL1, 2, and 3. A 16-amino acid region at the C terminus of 817 the effector is shown to be essential for BSL interaction. All three BSL family members can 818 be considered to be susceptibility S factors, with overexpression increasing P. infestans leaf 819 infection. Overexpression of StBSL1 and BSL3 can suppress INF1-mediated cell death 820



25

(ICD), with no effect seen for StBSL2. Silencing StBSL1 results in no change to P. infestans 821 leaf infection or to ICD. Silencing StBSL2 and 3 in combination significantly reduces P. 822 infestans leaf infection and significantly increases ICD. Notably, silencing StBSL2 and 3 823 reduces protein level of StBSL1, suggesting that one or both of these are required for 824 StBSL1 stability. Finally, suppression of ICD by StBSL1 and StBSL3 has been shown to 825 require the transcription factor StCHL1, a suppressor of immunity in Solanaceous plants. 826



















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https://www.ncbi.nlm.nih.gov/pubmed?term=Albrecht C%2C Boutrot F%2C Segonzac C%2C Schwessinger B%2C Gimenez%2DIbanez S%2C Chinchilla D%2C Rathjen JP%2C de Vries SC%2C Zipfel C%2E 2011%2E Brassinosteroids inhibit pathogen%2Dassociated molecular pattern%26%23x2013%3Btriggered immune signaling independent of the receptor kinase BAK1%2E Proceedings of the National Academy of Sciences %28USA&dopt=abstract

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AVR2 targets BSL family members, which act as ......Feb 19, 2019 · 9 Invergowrie, Dundee DD2 5DA, UK. 10 2Key Laboratory of Horticultural Plant Biology (HZAU), Ministry of Education,