Low temperature enhances plant immunity via salicylic acid ... · 11/6/2019 · SID1/EDS5 encodes a multidrug and toxin extrusion-like transporter and 78 functions in the export

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Short title: Low temperature enhances plant immunity 1

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Low temperature enhances plant immunity via salicylic acid pathway genes that are 4

repressed by ethylene 5

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Zhan Li1,2, Huimin Liu3, Zehong Ding4, Jiapei Yan2, Huiyun Yu2, Ronghui Pan1, Jin Hu1, Yajing 7

Guan1,*, Jian Hua2,3,* 8

9 1Seed Science Center, Institute of Crop Science, College of Agriculture and Biotechnology, Zhejiang 10 University, Hangzhou 310058, P.R. China 11 2School of Integrative Plant Science, Plant Biology Section, Cornell University, Ithaca, NY 14853, USA. 12 3State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, 13 Nanjing, P.R. China 14 4Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and 15 Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou, 571101, China. 16 *Corresponding authors: [email protected] and [email protected] 17

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One-sentence Summary: 19

Disease resistance to the pathogen Pseudomonas syringae in Arabidopsis is enhanced by a lower 20 temperature via upregulating multiple genes in the salicylic acid pathway which are repressed by 21 ethylene. 22

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AUTHOR CONTRIBUTIONS 24

JHua conceived the study. ZL and JHua designed the experiments. JHua, YG and JHu supervised 25

the project. ZL, HL and HY performed the experiments. ZD analyzed the RNA-seq data. ZL and 26

JHua wrote the paper. JY and RP revised the manuscript. All authors read and approved the 27

manuscript. 28

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Plant Physiology Preview. Published on November 6, 2019, as DOI:10.1104/pp.19.01130

Copyright 2019 by the American Society of Plant Biologists

https://plantphysiol.orgDownloaded on March 10, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.

https://plantphysiol.org

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Abstract 30

Temperature has a large impact on plant immune responses. Earlier studies identified 31

intracellular immune receptor nucleotide-binding leucine-rich repeat (NLR) genes and salicylic 32

acid (SA) as targets of high temperature inhibition of plant immunity. Here we report that 33

moderately low temperature enhances immunity to the bacterial pathogen Pseudomonas syringae 34

in Arabidopsis thaliana. This enhancement is dependent on SA signaling and is accompanied by 35

upregulation of multiple SA biosynthesis and signaling genes at lower temperature. SA signaling 36

is repressed by jasmonic acid and ethylene at both normal and low temperatures. The inhibition 37

of SA biosynthesis by ethylene, while mainly through ISOCHORISMATE SYNTHASE 38

1/SALICYLIC ACID-INDUCTION DEFICIENT 2 (ICS1/SID2) at normal temperature, is through 39

ENHANCED DISEASE SUSCEPTIBILITY5 (EDS5)/SID1, ICS2, and ICS1/SID2 at lower 40

temperature. The repression by ethylene is mediated by a direct regulation of the ethylene 41

response transcription factor Ethylene Insensitive 3 (EIN3) on multiple SA biosynthesis and 42

signaling genes. Thus, low temperature enhances the SA pathway to promote immunity and at 43

the same time uses ethylene to repress multiple SA regulators to achieve fine-tuned immune 44

responses. 45

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Key words 48

ethylene, ICS2, immunity, salicylic acid, SID2, temperature 49



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INTRODUCTION 50

Temperature has a large impact on plant growth, development, and defense responses. 51

Temperature sensitivity was reported for plant disease resistance as early as 1969 (Dropkin, 52

1969) and has been observed in various plant-pathogen interactions (Wang et al., 2009). Ambient 53

temperature within the normal range of plant growth influences both pathogen virulence and host 54

immune response (Colhoun, 1973; Browder, 1985; Huot et al., 2017). 55

Plants rely on multi-layered and multi-branched immune systems to fight off pathogens 56

(Chisholm et al., 2006; Jones and Dangl, 2006). The first branch, named pathogen-triggered 57

immunity (PTI), uses pattern recognition receptors (PRRs) to detect microbe- or pathogen-58

associated molecular patterns (MAMPs or PAMPs) to trigger basal resistance (Boller and Felix, 59

2009). The second immunity branch, named effector-triggered immunity (ETI), recognizes 60

effectors by Resistance (R) proteins, mostly nod-like receptor, or nucleotide-binding leucine rich 61

repeat (NLR) proteins and mount a more robust response (Cui et al., 2015). 62

Plant immune responses are regulated by multiple plant hormones such as salicylic acid 63

(SA), jasmonic acid (JA), and ethylene (ET). SA is a major hormone for both ETI and PTI (Vlot 64

et al., 2009). It is synthesized mainly through the isochorismate pathway and partially from 65

phenylalamine through the phenylalanine pathway. ISOCHORISMATE SYNTHASE 1 (ICS1), 66

also known as SALICYLIC ACID-INDUCTION DEFICIENT 2 (SID2), is the key enzyme in 67

the isochorismate pathway and it is thought to play a major role for SA production induced by 68

pathogen infection (Wildermuth et al., 2001). ICS2, with the same biochemical function as ICS1, 69

has a minimal role in SA accumulation (Garcion et al., 2008). The phenylalanine pathway of SA 70

biosynthesis is mediated by PHENYLALANINE AMMONIA LYASE (PAL) that catalyzes 71

phenylalanine to trans-cinnamic acid, a precursor of diverse phenolic compounds (Dempsey et 72

al., 2011). In Arabidopsis thaliana, pathogen-induction of SA biosynthesis occurs predominantly 73

through the isochorismate pathway, which contributes to 90% of the SA content (Rekhter et al., 74

2019). SA accumulation upon pathogen infection is shown to be dependent on SALICYLIC 75

ACID-INDUCTION DEFICIENT (SID1)/ENHANCED DISEASE SUSCEPTIBILITY5 (EDS5) 76

(Nawrath et al., 2002). SID1/EDS5 encodes a multidrug and toxin extrusion-like transporter and 77

functions in the export of isochorismate, the precursor of SA, from the chloroplast to the 78

cytoplasm (Serrano et al., 2013; Rekhter et al., 2019). The blocking of the SA export in the sid1 79

mutant results in low SA, probably through an inhibition of SA biosynthesis from an over 80



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accumulation of SA in the chloroplast. The SA defense signal is potentiated by positive feedback 81

loops involving signaling components of PTI and ETI. In particular, EDS1 and PHYTOALEXIN 82

DEFICIENT 4 (PDA4), as essential components for NLR-mediated ETI, are important for 83

pathogen-induced SA accumulation (Jirage et al., 1999; Feys et al., 2001). Besides SA, plant 84

hormones JA and ET also play critical roles in plant immunity (Shigenaga and Argueso, 2016). 85

These hormones have antagonistic or synergistic interactions among themselves, thus generating 86

complex signaling networks (Tsuda and Katagiri, 2010). This is thought to confer tunable 87

immune regulation to respond to developmental and environmental variations. SA has negative 88

or positive interactions with JA and ET in regulating plant defenses against microbes (Robert-89

Seilaniantz et al., 2011). JA induces the expression of SID1/EDS5 but inhibits the expression of 90

PAD4 which is likely responsible for the mitigation of SA accumulation in plant immunity by JA 91

(Mine et al., 2017). ET in general acts antagonistically to SA signaling. The ET signaling 92

transcription factors EIN3 and EIN3-like1 (EIL1) bind directly to the promoter of SID2 and 93

repress its expression (Chen et al., 2009). The interaction of plant hormones in plant immunity 94

was extensively investigated using combinations of mutants defective in DELAYED-95

DEHISCENCE 2 (DDE2), EIN2, PAD4, and SID2. PTI induced by a peptide from flagellin 96

(flg22) and ETI induced by pathogen effector AvrRpt2 were mostly abolished in the dde2 ein2 97

pad4 sid2 quadruple mutant, but were largely intact in plants with mutations in any one of these 98

genes. This suggests that SA, PAD4, JA, and ET signaling sectors together contribute positively 99

to PTI and ETI (Tsuda et al., 2009). 100

Variations in ambient temperature have a pronounced effect on PTI and ETI in plant 101

immunity. Temperature sensitivity of disease resistance has been found in multiple host-102

pathogen interactions (Hua, 2014). Resistance of Arabidopsis plants to virulent and avirulent 103

Pseudomonas syringae pathovar tomato (Pst) strain DC3000 is reduced at a moderately elevated 104

temperature of 28°C, which is accompanied by a reduced expression of SA signaling molecules 105

PAD4 and EDS1 compared to the normal growth temperature of 22°C (Wang et al., 2009). 106

Temperature modulation of NLR gene activity, exemplified by NLR protein subcellular 107

localization, is one of the key causes for high temperature inhibition of disease resistance (Zhu et 108

al., 2010). Different variants of the NLR gene Suppressor of npr1, constitutive 1 (SNC1) confer 109

immune responses with differential temperature sensitivity, indicating that SNC1 itself is a 110

temperature sensitive component of plant immune responses (Zhu et al., 2010). In addition, SA 111



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biosynthesis is inhibited at 30°C compared to 22°C and application of the SA analog 112

benzothiadiazole (BTH) potentiates disease resistance to virulent pathogens at 30ºC, indicating 113

that inhibition of SA is critical for high temperature inhibition of basal resistance (Huot et al., 114

2017). Studies also suggest that high temperature shifts resistance from ETI to PTI, as 115

expression of PTI induced genes is elevated at moderately high temperatures (Cheng et al., 2013). 116

Here we examined the propagation of the bacterial pathogen Pst DC3000 in Arabidopsis at 117

different ambient temperatures: moderately low (16°C, referred as low), normal (22°C) and 118

moderately high (28°C, referred as high). We found that low temperature enhances plant 119

immunity and does not compromise the virulence of the pathogen. Further, we utilized mutants 120

deficient in single and multiple signaling sectors of SA, JA, ET, and PAD4 to reveal a potential 121

different genetic requirement for resistance at different temperatures. We found that SA 122

signaling is a major sector mediating the enhancement of resistance at low temperature. In 123

addition, ET and SA have different genetic interactions at low and normal temperatures. Further 124

transcriptome analysis revealed that ET antagonizes the SA sector through the SA biosynthesis 125

gene ICS1/SID2 at normal temperature but through multiple SA biosynthesis regulators 126

including ICS1/SID2, EDS5/SID1 and ICS2 at low temperature. Therefore, low temperature 127

potentiates a higher number of SA biosynthesis genes for higher disease resistance which is 128

balanced with direct repression by the EIN3 transcription factor. 129

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RESULTS 132

Lower temperature reduces pathogen propagation in Arabidopsis 133

Prior studies showed that basal resistance to the virulent pathogen Pst DC3000 is 134

inhibited at a moderately high temperature of 28°C compared to the normal growth temperature 135

of 22°C in Arabidopsis. Here we examined resistance to this bacterial pathogen at a moderately 136

low temperature 16°C in comparison to 22°C and 28°C in the reference accession Col-0 of 137

Arabidopsis. 138

Consistent with previous findings, propagation of Pst DC3000 was higher by more than 139

10-fold at 28°C compared to 22°C at 3 days post inoculation (dpi) (Fig. 1A). In contrast, 140

propagation was the lowest at 16°C, with more than 10-fold reduction compared to 22°C at 3 dpi 141

(Fig. 1A). To assess the effect of a lower temperature on bacterial growth in plants, we 142

monitored pathogen propagation at 3, 4 and 5 dpi. No significant difference was found for 143

pathogen growth at 4 dpi compared to 5 dpi or 3 dpi, although there was a slight increase from 3 144

dpi to 4 dpi at 16°C (Fig. 1B). To minimize potential effects of lower temperature on pathogen 145

growth and plant growth, we used 4 dpi at 16°C and 3 dpi at 22°C for further analysis. 146

We next examined the requirement of pathogen virulent factors for the reduced pathogen 147

growth at 16°C compared to 22°C using the Pst DC3000 ΔhrcU strain, which is defective in the 148

type III secretion system (T3SS) (Roine et al., 1997) and the Pst DC3000 ΔCOR strain, which is 149

defective in coronatine production (Ma et al., 1991). Similar to Pst DC3000, Pst DC3000 ΔCOR 150

grew less at 16°C than at 22°C (Fig. 1C, 1D). Multivariate analysis of variance (MANOVA) 151

analysis revealed no significant influence of COR over the temperature effect on pathogen 152

growth (Fig. 1E). In contrast, the Pst DC3000 ΔhrcU strain had no detectable decrease in growth 153

at 16°C compared to 22°C (Fig. 1C). The interaction between temperature and hrcU on pathogen 154

growth is significant (Fig. 1F). This data indicates that a lower growth of Pst DC3000 in plants at 155

16°C is dependent on a functional T3SS but not COR production from the pathogen. 156

Low temperature does not reduce pathogen virulence 157

We next examined whether the reduced pathogen propagation in plants at 16°C compared 158

to 22°C is due to an increase of plant immunity or a reduction of pathogen growth or virulence at 159

lower temperature. Firstly, the growth of Pst DC3000 at 16°C and 22°C was analyzed in liquid 160

rich media where the maximum growth rate could be achieved. From 6 to 30 h post inoculation 161

(hpi), Pst DC3000 became slightly denser at 22°C than at 16°C, but after 30 hpi, they grew to a 162



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similar density (Fig. 2A). We expect that the growth rate of the pathogen in plants is unlikely to 163

exceed that in rich medium, and the difference of growth rates at the two temperatures will likely 164

be reduced in plants. Because pathogen growth in liquid media differed only in the early phase 165

and the maximum difference was 3-fold, the decrease of pathogen propagation in plants by 166



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almost 10 fold at 16°C compared to 22°C could not be explained by a lower intrinsic pathogen 167

growth rate at 16°C. 168

Secondly, translocation of two effector proteins from the pathogen was analyzed by 169

cyclic AMPs (cAMPs) produced by their fusions with the reporter protein adenylate cyclase A 170

(CyaA). CyaA converts ATP into cAMP only when they are present in plant cells but not 171



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bacteria where calmodulin is not available for its activity (Schechter et al., 2004). Arabidopsis 172

plants grown at 16°C and 22°C were inoculated by infiltration with Pst DC3000 strains carrying 173

the fusions between the effectors (AvrPto or HopY1) and the reporter CyaA (named AvrPto-174

CyaA or HopY1-CyaA) (as described in Schechter et al, 2004 and Schechter et al., 2006), and 175

the amount of cAMP produced by CyaA in leaves at 4 hpi was measured. The cAMP amount had 176

an apparent increase of 1–2 folds for both effectors at 22°C compared to that at 16°C (Fig. S1). 177

Early biochemical studies indicate that the enzymatic activity of CyaA is positively correlated 178

with temperature, and its activity at 22°C was found to be 1.8 and 3 folds of that at 16°C in the 179

two studies (Murayama et al., 1994; Raffelberg et al., 2013). To verify this temperature 180

dependence of enzymatic activity from the CyaA reporter protein, we mixed plant extracts with 181

lysate of Pst DC3000 strains carrying HopY1-CyaA or AvrPto-CyaA and incubated the reactions 182

at 16°C, 22°C and 28°C. With the plant extract provided at the protein concentration of 1 μg/μl 183

in the reaction, the CyaA activity was found to increase from 16°C to 22°C by 2.9-2.7 folds and 184

from 22°C to 28°C by 3 fold (Fig. 2B, S1B). With the plant extract provided at a lower protein 185

concentration of 0.5 μg/μl, there was also an increase of cAMP production from 16°C to 22°C 186

and from 22°C to 28°C, but the amount of cAMP was lower probably due to insufficient 187

calmodulin provided from the plant extract (Fig. 2B, S1B). No cAMP, product of CyaA, could 188

be detected from reactions containing only the plant extracts without the lysate from the bacterial 189

strain carrying AvrPto-CyaA (Fig. S1C), indicating that the activity detected came from the 190

bacteria carrying the CyaA reporter protein. We therefore adjusted the measured cAMP amount 191

at 22°C relative to that at 16°C by a factor of 2.4 fold for direct comparison of the amount of the 192

effector-CyaA fusion protein. This factor is the average of those from the two previous 193

biochemical studies, and is close to the 2.7-3.0 fold found in this study and therefore is a 194

conservative factor for decreased activity at 16°C. The normalized cAMP concentration was 195

significantly higher in infected plants at 16°C compared to 22°C for Pst DC3000 strains carrying 196

AvrPto-CyaA or HopY1-CyaA (Fig. 2C). As a control, a Pst DC3000 ΔhrcQ-hrcU mutant strain 197

where T3SS is defective (Cunnac et al., 2011) carrying the same AvrPto-CyaA induced little 198

cAMP production in plants after infection, and there was no difference of the cAMP amount 199

between 16°C and 22°C at 4 hpi (Fig. 2C). Therefore, effector secretion from the pathogen is not 200

reduced at 16°C compared to 22°C. This lack of decrease of virulence at low temperature, 201

combined with no drastic reduction of intrinsic pathogen growth, indicates that the lower 202



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propagation of the pathogen in plants is mainly due to an enhancement of plant immunity at low 203

temperatures. 204

Involvement of the SID2 and PAD4 pathway but not the C-repeat binding factor (CBF) 205

genes in low temperature enhances plant immunity 206

An early study found that a short-term treatment of 4°C enhances plant immunity (Wu et 207

al., 2019) Therefore, we investigated whether or not the C-repeat binding factor (CBF) genes that 208

mediate cold acclimation could be involved in the enhancement of plant immunity by moderately 209

low temperature. The cbf mutants, where all three CBF genes are knocked out (Jia et al., 2016), 210

were analyzed for disease resistance at 16°C and 22°C. Both cbf-1 and cbf-2 mutants supported a 211

similar pathogen growth as the wild type, with a lower pathogen growth at 16°C than 22°C (Fig. 212

2D). This suggests that the CBF pathways does not play a major role in mediating low 213

temperature enhancement of disease resistance to Pst DC3000. 214

Because SA signaling is critical for high temperature conferred inhibition of disease 215

resistance, we asked if it is critical for the effects of both high and low temperatures on plant 216

immunity. To this end, pathogen growth was analyzed in the SA biosynthesis mutant sid2 and 217

SA signaling mutant pad4 at 16°C, 22°C and 28°C. The sid2 and pad4 mutants both exhibited 218

the same susceptibility (slightly more but not significant) at 28°C compared to 22°C in contrast 219

to that in the wild-type Col-0 (Fig. 2E, 2F). The pad4 and sid2 mutants were more susceptible 220

than the wild type at 16ºC, indicating an important role of the SA signaling sector in resistance at 221

16ºC. Most strikingly, pathogen growth in the pad4 and sid2 mutants was similar between 16ºC 222

and 22ºC (Fig. 2E, F), indicating that the loss of the SA sector abolishes the low temperature 223

enhancement of disease resistance. Therefore, PAD4 and SID2 play an important role in 224

enhancing plant immunity at lower temperatures. Further MANOVA revealed a significant 225

interaction between temperature and genotypes on disease resistance (P-value 2.41E-09) (Fig. 226

2G, 2H), indicating a strong influence of PAD4 and SID2 over the temperature effect on basal 227

resistance. 228

ET and JA repress resistance through SA and PAD4 at 22°C 229

Because temperature affects production and signaling of plant hormones (Scott et al., 230

2004), we investigated whether or not varying temperature could alter the contribution from and 231

interaction among hormones in plant immunity. To do this, we conducted pathogen growth 232



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assays at 16ºC, 22ºC and 28ºC on the well-characterized hormone sector mutant set including the 233

single and combined mutants of sid2, dde2, ein2, and pad4. 234

At 22°C, the quadruple mutant dde2 ein2 sid2 pad4 was more susceptible to Pst DC3000 235

than the wild type assayed by either dipping or infiltration inoculation (Fig. 3A and S2). This 236

indicates that these genes collectively make a positive contribution to plant immunity. Among 237

the single mutants, dde2 and ein2 were more resistant than the wild type while sid2 and pad4 238

were more susceptible than the wild type, indicating a positive role of SA and a negative role of 239

JA and ET in resistance to Pst DC3000. The inhibition of resistance by JA and ET is mediated 240

by SID2 and PAD4. The double mutants between the more resistant dde2 or ein2 mutants and the 241

more susceptible sid2 or pad4 mutants (dde2 sid2, dde2 pad4, ein2 sid2, and ein2 pad4) were all 242

more susceptible to Pst DC3000 than the wild type. Furthermore, the dde2 pad4 and ein2 pad4 243

double mutants were as susceptible as the pad4 mutant, while dde2 sid2 was more susceptible 244

than dde2 although more resistant than the sid2 mutant (Fig. 3A and S2). This suggests that the 245

effect of JA and ET is mainly through their inhibition of SID2 and PAD4, although the JA 246

suppression of resistance is not entirely through SID2. 247

PAD4 appears to be the most important player among the four genes in basal resistance to 248

Pst DC3000 at 22°C. No significant difference in susceptibility was observed between the sid2, 249

pad4, and sid2 pad4 mutants (Fig. 3A and S2). All mutants containing pad4, including dde2 ein2 250

pad4, had a similar susceptibility as the pad4 single mutant (Fig. 3A), indicating a dependence of 251

resistance inhibition on PAD4 from the combined action of JA and ET. The dde2 ein2 sid2 pad4 252

mutant, like other combinations containing both sid2 and pad4, was only slightly less susceptible 253

than the sid2 pad4 double mutant (Fig. 3A), and the difference was very small; The dde2 ein2 254

sid2 mutant, although more susceptible than the dde2 ein2 mutant, was more resistant to Pst 255

DC3000 than the sid2 mutant (Fig. 3A). These data indicate that SID2 has a similar but a smaller 256

role compared to PAD4 in resistance to Pst DC3000 and that JA and ET work through 257

PAD4/SID2 in plant immunity at 22°C. 258

The contributions from four signaling sectors to disease resistance are minor at 28°C 259

The growth of Pst DC3000 was measured in the wild type and the sector mutants at 28ºC 260

by dipping inoculation (Fig. 3B) or infiltration inoculation (Fig. S3). The pad4 and sid2 single 261

mutants were as susceptible as the wild type while the ein2 mutant exhibited less susceptibility 262

compared to the wild type. A slight decrease of susceptibility was observed in the dde2 mutant 263



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but it did not appear to be significant. The double mutants, ein2 pad4, ein2 sid2, dde2 pad4 and 264



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dde2 sid2, were as susceptible as the single pad4 and sid2 mutants or the wild type. Therefore, 265

the loss of PAD4 or SID2 function alone does not affect disease susceptibility but their function 266

is revealed in the ein2 and perhaps dde2 mutant. 267

PAD4 and SID2 are critical for disease resistance at 16ºC 268

Growth of Pst DC3000 in the singling sector mutants were analyzed at 16ºC and the 269

patterns of growth were similar between using dipping and infiltration inoculation methods (Fig. 270

3C, S4). The dde2 and ein2 mutants were both more resistant than the wild type at 16ºC, but the 271

dde2 pad4 and the ein2 pad4 double mutants were as susceptible as the pad4 mutant. In addition, 272

the ein2 sid2 pad4 and dde2 sid2 pad4 triple mutants were as susceptible as the sid2 and pad4 273

single mutants, indicating that the repression of resistance by JA and ET is through PAD4 and 274

SID2. Overall, relative pathogen growth in single and combined mutants at 16ºC was also similar 275

to that at 22ºC (Fig. 3C and 3A), suggesting a similar contribution and interaction from the four 276

signaling sectors at these two temperatures. The only exception is the ein2 sid2 mutant, which 277

exhibited an enhanced resistance compared to the sid2 single mutant at 16ºC but had the same 278

resistance as sid2 at 22ºC (Fig. 3C, S4, 3A, S2). This suggests that enhanced resistance in the 279

ein2 mutant is fully dependent on SID2 at 22ºC but not at 16ºC. 280

Transcriptome analysis reveals a module associated with differential contributions of SID2 281

to immunity at 16°C and 22°C 282

To reveal the underlying mechanism of this temperature dependence of the ein2 and sid2 283

interaction, we performed transcriptome analysis using 3’ RNA-seq (Tandonnet and Torres, 284

2017) on seedlings of Col-0, ein2, sid2, and ein2 sid2 grown at 16°C and 22°C. A total of 8400 285

genes were differentially expressed between the mutants and the wild type or between 16°C and 286

22°C (Fig. S5A). Cluster analysis based on these differentially expressed genes (DEGs) revealed 287

that sid2 22°C and ein2 sid2 22°C were closely related while ein2 16°C and ein2 sid2 16°C were 288

closely related (Fig. 4A, S5B). This is in agreement with the pathogen resistance phenotype 289

where the ein2 sid2 double mutant was similar to sid2 at 22°C but was more similar to ein2 at 290

16°C (Fig. 3A, 3C). 291

We carried out Weighted Gene Co-expression Network Analysis (WGCNA) (Stuart et al., 292

2003) on the DEGs to reveal potential gene networks that are differentially associated with ein2 293

sid2 at 22°C and 16°C. Six modules (M1 to M6) were identified for all DEGs (Table S2, Fig. 4A, 294

S5B). Genes in the ein2 sid2 mutant had different relative expression levels at 22°C and 16°C in 295



14

all modules except for M1. Among the modules between M2 to M6, only genes in the M4 296

module had expression in the ein2 sid2 mutant resembling ein2 more at 16°C but resembling 297

sid2 at 22°C. In addition, genes in M4 had higher expression in the ein2 mutant but lower 298

expression in the sid2 mutant. 299

Because the expression pattern of the M4 module is highly correlated with the disease 300

resistance properties of the ein2 sid2 mutant at 16°C and 22°C (Fig. 3A, 3C), we examined the 301

genes in this module in detail. Gene ontology (GO) term analysis of the M4 module revealed an 302

enrichment of defense related genes (Fig. 4B). More specifically, terms related to SA 303

biosynthesis were enriched, including SA biosynthetic processes and signaling pathway (Fig. 304

4B). This indicates that the SA biosynthesis process might be affected by the ein2 sid2 mutations 305

in a temperature dependent manner. Consistent with this hypothesis, multiple SA inducible genes 306

such as PR1 (Pathogenesis Related Protein 1) and PR2 are present in the M4 module. PR2 had a 307

higher expression at 16°C compared to 22°C. PR1 had the same expression at 16°C compared to 308



15

22°C (although there was a slight but not significant increase at 16°C), and both expression 309

levels were very low which is consistent with its induced nature by stress conditions. Their 310

expressions were much higher in the ein2 mutant than in Col-0 at both temperatures and were 311

lower in the sid2 mutant compared to the wild type (Fig. S6A, S6B). Similar to other genes in the 312

M4 module, both had a higher expression in the ein2 sid2 mutant than in the sid2 mutant at 16°C 313

but not at 22°C (Fig. 4A, S5B). 314

EDS1 and PAD4, regulators of SA signaling and biosynthesis, are also found in the M4 315

module. EDS1, but not PAD4, had a slightly higher expression at 16°C than at 22°C (Fig. S6C, 316

S6D). Their expression was not drastically affected by the sid2 mutation but was significantly 317

higher in the ein2 mutant than in the wild type at both 16°C and 22°C (Fig. S6C, S6D). Similar 318

to other genes in the M4 module, their expression in the ein2 sid2 mutant was significantly 319

higher at 16°C than at 22°C (Fig. S6C, S6D). In summary, genes in M4 are involved in both SA 320

biosynthesis and signaling and they likely contribute to the temperature-dependent interaction 321

between ein2 and sid2. 322

SA biosynthesis genes in the ein2 sid2 mutant have a higher expression at 16°C than 22°C 323

The expression pattern of SA-induced defense genes suggests that SA biosynthesis and/or 324

signaling are affected by the ein2 mutation and that the involvement of SID2 in these SA 325

processes is temperature-dependent. To test this hypothesis, we measured SA content in Col-0, 326

ein2, sid2, and ein2 sid2 plants at 22°C and 16°C. The wild-type Col-0 plants accumulated more 327

SA at 16°C than at 22°C (Fig. 5A), which could explain the enhanced disease resistance at 16°C 328

(Fig. 1A). As expected, the sid2 mutant contained less SA than the wild type at both 16°C and 329

22°C. In contrast, the ein2 mutant accumulated more SA than the wild type at both temperatures, 330

which is consistent with a higher disease resistance in the ein2 mutant than in the wild type (Fig. 331

3). Interestingly, the ein2 sid2 double mutant had a reduced SA level compared to the ein2 332

mutant, to a level similar to sid2 at 22ºC, but it had a higher SA level compared to the ein2 sid2 333

mutant to a similar level of the wild type at 16°C. Therefore, the SA content is closely correlated 334

with disease resistance at the two temperatures for the ein2 sid2 mutant. 335

To better understand the molecular basis for a higher SA content in the ein2 sid2 mutant 336

compared to the sid2 mutant at 16 ºC but not 22 ºC, we examined the expression of genes 337

involved in SA biosynthesis. SID2/ICS1 had a higher expression in the ein2 mutant than in the 338

wild type (Fig. 5C), which is associated with a higher SA content in the ein2 mutant than in the 339



16

wild type. Meanwhile, SID1 was also expressed at a higher level in the ein2 mutant than in the 340

wild type and in the ein2 sid2 mutant than in the sid2 mutant at 16°C (Fig. 5B), indicating an 341

inhibition of SID1 expression by EIN2. At 22°C, SID1 was expressed at a slightly higher level in 342

the ein2 mutant than in the wild type, but to a similar level in the ein2 sid2 and sid2 mutants. For 343

the alternative PAL pathway, PAL1 and PAL2, but not PAL3 and PAL4, exhibited a 10-fold 344

increase of expression at 16°C compared to at 22°C, and this increase was observed in the wild 345

type as well as in the ein2 and sid2 mutants (Fig. 5E, 5F, 5G, 5H). However, PAL1, PAL2 and 346

PAL3 did not have a higher expression in the ein2 sid2 mutant compared to the sid2 mutant at 347

16°C (Fig. 5E, 5F, 5G). PAL4 had an increased expression in the ein2 sid2 mutant compared to 348

the sid2 mutant at 16°C (Fig. 5H), but the contribution of this increase to a higher SA level in the 349

ein2 sid2 mutant might be minimal because its expression is extremely low compared to the 350

other three PAL genes. 351

Interestingly, ICS2, the SID2/ICS1 homolog, had a higher expression at 16°C compared 352

to at 22°C in all genotypes tested. It's worth noting that it is more highly expressed in the ein2 353



17

sid2 mutant compared to the sid2 mutant at 16°C (Fig. 5D); the relative expression level of ICS2 354

in the ein2 sid2 and sid2 mutants was correlated with the SA content at 16°C (Fig. 5A). 355

Pst DC3000 induces SID1 and ICS2 expression in ein2sid2 at 16°C 356

Because SID1 and ICS2 expression under non-pathogenic conditions is correlated with 357

SA accumulation in the ein2 sid2 mutant at 16°C (Fig. 5A, 5B), we examined its expression after 358

pathogen infection to determine whether or not its expression level could contribute to disease 359

resistance. Seedlings of the wild type, ein2, sid2, and ein2 sid2 were dipping inoculated by Pst 360

DC3000, and the expression of SID1 and ICS2 was assayed by reverse transcription quantitative 361

PCR (RT-qPCR) (Fig. 6A). In all these wild type and mutant plants, the SID1 gene was 362

expressed at a higher level by 8 to 12 folds at 5 hpi compared to 0 hpi. In addition, it was 363

expressed at a significantly higher level in the ein2 and ein2 sid2 mutants than in the wild type 364

and the sid2 mutant at 5 hpi, and this difference was more drastic at 16°C than at 22°C. 365

Therefore, SID1 expression is higher in plants containing the ein2 mutation compared to EIN2 366

wild-type plants and the higher expression is more pronounced at lower temperature. In contrast 367

to the previous notion, ICS2 expression was induced by the pathogen by 5-7 folds in the wild 368

type and mutant plants at both 16°C and 22°C. In addition, it was expressed at a slightly higher 369

level in the ein2 mutant than in the wild type and in the ein2 sid2 mutant than in the sid2 mutant 370

at 5 hpi (Fig. 6C). These results suggest that ICS2 plays a role in SA induction after pathogen 371

infection. 372

The expression of other SA biosynthesis genes SID2 and PAL1 was also examined in the 373

wild type and mutants after pathogen infection (Fig. 6B, 6D). SID2 was not expressed in the sid2 374

and ein2 sid2 mutant plant, as expected. It was induced by pathogen infection, although the 375

induction fold was smaller than that of SID1. Unlike SID1, SID2, or ICS2, PAL1 was not 376

significantly induced in expression after pathogen infection except in the sid2 mutant at 22°C 377

(Fig. 6D). However, it had a significantly higher expression at 16°C than at 22°C in all 378

genotypes with or without infection (Fig. 5D, 6D). 379



18

We observed an inconsistency on the relative expression levels of SID1 and SID2 at 16°C 380

versus 22°C in RNA-seq data (Fig. 5B, 5C) and in the RT-qPCR data without infection (Fig. 6A 381

and 6B, 0 hpi). It turns out that the expression of SID1 and SID2 is impacted by the circadian 382

clock, and both had a higher expression at 16°C compared to 22°C at the end of the night but 383

similar expression at the two temperatures at the end of the day (Fig. S7). This is consistent with 384

earlier findings that the SA pathway is circadian clock regulated (Zheng et al., 2015). 385

EIN3 directly regulates the expression of SID1 and ICS2 386

The up-regulation of SA biosynthesis and signaling genes, including SID2, SID1, ICS2, 387

PAD4, and EDS1, likely plays an important role in the enhancement of disease resistance by low 388

temperature. Because early studies revealed a direct transcriptional repression of SID2 by EIN3 389

(Chen et al., 2009), we explored the possibility that EIN3 acts as a direct transcription factor of 390



19

these genes. EIN3-binding sites were experimentally identified by DNA affinity purification 391



20

(DAP)-seq and chromatin immunoprecipitation (ChIP)-seq (Fig. S8A, S8B) (Chang et al., 2013; 392

O'Malley et al., 2016) and a consensus sequence of ‘A(C/T)G(A/T)A(C/T)CT’ was reported to 393

be the binding motifs of the EIN3/EIL family protein (Kosugi and Ohashi, 2000; Chang et al., 394

2013). We searched in the promoters of these genes for EIN3 binding consensus motifs and 395

EIN3/EIL binding sites using DAP-seq and ChIP-seq data. EDS1 is a strong candidate for a 396

direct target of EIN3 based on the presence of five perfect binding motifs (Fig. S8A) and EIN3 397

indeed showed binding footprints in its promoter region (Fig. S8C) (O'Malley et al., 2016). SID2 398

was demonstrated to be directly bound by EIN3 via a number of in vivo and in vitro methods 399

(Chen et al., 2009) and five EIN3-binding motifs were also found in its promoter (Fig. 7A). 400

However, SID2 was not considered as a strong target gene of EIN3 based on DAP-seq or ChIP-401

seq (Fig. S8C), suggesting a low sensitivity of –seq detection or a low binding activity of EIN3 402

to the SID2 promoter. For ICS2 and SID1, EIN3-binding motifs were found in their promoter 403

regions (Fig. 7A). EIN3-binding signals were stronger for ICS2 and SID1 than SID2 in the ChIP-404

seq experiment (Fig. S8C), suggesting that ICS2 and SID1 are direct target genes of EIN3/EILs. 405

We next tested the direct association of EIN3 to the predicted binding sites in the promoters 406

of the SID1 and ICS2 genes using ChIP. A green fluorescent protein (GFP) fusion of EIN3 407

(EIN3-GFP) was expressed under the 35S promoter in Arabidopsis protoplasts. Chromatins 408

associated with EIN3-GFP were immuno-precipitated (IPed) with the anti-GFP antibody, and the 409

precipitated chromatins were analyzed by quantitative PCR for enrichment of the chosen 410

promoter regions. The P region of the SID2 promoter ( -115 to -324 bp relative to the 411

transcription start site, Fig. 7A), shown to be bound by EIN3 in an earlier study (Chen et al., 412

2009), was indeed enriched in the EIN3-GFP ChIPed chromatin compared to the no-antibody 413

control. The P2 region of SID1 (-392 to -618 bp), with no predicted binding motifs of EIN3, did 414

not show any enrichment in the ChIP samples (Fig. 7B). In contrast, predicted EIN3 binding sites, 415

including P1 (-128 to -331 bp) and P3 (-574 to -782 bp) of SID1 as well as P1 (-109 to -358 bp), 416

P2 (-358 to -621bp) and P3 (-621 to -818bp) of ICS2, were all found to have a higher ChIP 417

output versus the genomic DNA input in GFP-antibody ChIPed chromatins over no-antibody 418

ChIPed controls (Fig. 7B, 7C). The association of EIN3 with SID1 and ICS2 was observed at 419

both 22°C and 16°C, with no significant difference in output/input percentage. 420

421



21

DISCUSSION 422

Temperature is one of the most important climatic factors that impact the interactions 423

between plants and pathogenic bacteria, fungi, and insects. In the model plant-pathogen 424

interaction system, we found a reduced propagation of Pst DC3000 at a moderately low 425

temperature of 16°C compared to the normal growth temperature of 22°C in Arabidopsis. This is 426

due to an increase of basal resistance and NLR triggered immunity in Arabidopsis at low 427

temperature (Fig.1, 3) while the virulence of Pst DC3000 was not reduced at low temperature 428

(Fig. 2B, 2C). This enhancement of plant immunity is accompanied by a higher SA content at 429

low temperature even without pathogen infection (Fig. 5A). We further demonstrate that the SA 430

pathway is the major contributor to the enhanced resistance at 16°C. Mutants defective in SA 431

biosynthesis and signaling, sid2 and pad4, not only have higher susceptibility compared to the 432

wild type at 16°C, but also exhibit no enhancement of disease resistance at 16°C compared to 433

22°C (Fig. 2E, 2F). Therefore, SA is a key target for temperature regulation of plant immunity 434

with lower temperature increasing SA signaling and enhancing plant immunity. 435

Earlier studies have found that NLR proteins have a higher activity at lower temperatures. 436

Hybrid necrosis mediated by activation of NLR proteins was present at 16°C but was suppressed 437

at 23°C (Bomblies et al., 2007). Chilling sensitive (chs) mutants containing active forms of NLR 438

proteins exhibit low temperature-induced cell death (Wang et al., 2013). Because NLR activation 439

can induce SA biosynthesis and SA can induce the expression of some NLR genes, it is likely 440

that NLR forms an amplification loop with SA to enhance resistance at low temperature (Fig. 441

8A). Similar feedback regulation likely occurs at moderately high temperatures as well. High 442

temperature inhibits plant immune receptor NLR genes and the plant hormone SA (Huot et al., 443

2017). The suppression of one or multiple components in the loop could lead to amplification of 444

the effect of high temperature (Fig. 8A). 445

Low temperature induces a higher production of SA mainly due to an upregulation of SA 446

biosynthesis genes (Fig. 5A, 5C). The increase of expression of SID2, the key gene in the 447

isochorismate pathway, is essential for the increased SA content at 16°C because the loss of 448

SID2 function abolishes an increase of SA at 16°C. The production of SA upon pathogen 449

infection at low temperature is not yet determined. A higher production is expected under 450

pathogen infection conditions compared to no infection because the extent of induction of SID2 451

by infection is much higher at 16°C compared to 22°C (Fig. 6B). 452



22

JA and ET repress plant defenses through SA at a broad temperature range. The loss of 453

their biosynthesis or signaling (in dde2 and ein2 mutants) confers a higher basal resistance at 454

both 22°C and 16°C and to some extent at 28°C (Fig. 3). This negative regulation is through their 455

inhibition of the SA biosynthesis and signaling pathway because the loss of PAD4 abolishes their 456

effects (Fig. 3). At 28°C, the suppression of the SA pathway by high temperature renders almost 457

all the signaling sector mutants as susceptible as the wild type, removing the differences of basal 458

resistance across the genotypes. Despite the overall enhancement of plant immunity at low 459

temperature, the four signaling sectors have similar relative contributions to plant immunity at 460

low and normal temperatures. However, the interaction between ET and SA was different at 461

16°C and 22°C. The repression of immunity by ET is totally dependent on SID2 at 22ºC but was 462

partially dependent on SID2 at 16ºC (Fig. 3A, S2, 3B, S4). Nevertheless, the repression of 463

immunity by ET at 16ºC is through the SA pathway despite a reduced role of SID2 in SA 464

biosynthesis under ET repression. This is supported by the total dependence of PAD4 for ET 465

repression at 16°C (Fig. 3A, 3C). 466



23

The repression of immunity by ET at low temperature is through multiple SA 467

biosynthesis genes including SID1 and ICS2 besides SID2. At normal temperature, the SID2 468

gene is directly regulated by the transcription factor EIN3 (Chen et al., 2009). At low 469

temperature, SID2 is also directly associated with EIN3 and it has a higher expression in the ein2 470

mutant (Fig. 5C, 6B, 7). SID1 is another EIN3 target gene as indicated by its increased 471

expression in the ein2 mutant and an association of the EIN3 protein with its promoter (Fig. 5B, 472

6A, 7). Similarly, the SID2 homologous gene ICS2 is also directly repressed by EIN3, as EIN3 is 473

associated with its promoter and represses its expression. In addition, the SA signaling gene 474

EDS1 is another regulatory target of ET (O'Malley et al., 2016), the upregulation of EDS1 in the 475

ein2 mutant may amplify SA signaling and thus influence SA biosynthesis at low temperature. 476

Thus, ET represses multiple target genes to influence the SA pathway. 477

SID2 is the ET target that is a major player in SA biosynthesis at 22°C, while SID1 and 478

ICS2 are additional targets that contribute to SA biosynthesis at 16°C (Fig. 8). ICS2 has a minor 479

role in SA biosynthesis compared to SID2, but it could replace the role of SID2 at low 480

temperature when its repression by ET is released. Expressing EIN3 (EIN3-GFP) under the 35S 481

promoter did not reveal differences of its association with the promoters of SID1 and ICS2 at 482

16°C and 22°C (Fig. 7B, 7C). It is yet to be determined quantitatively the level of endogenous 483

EIN3 protein and its relative binding to target genes at normal and low temperatures. In addition 484

to the potential differential EIN3 activity at the two temperatures, the differential activities of SA 485

biosynthesis proteins at the two temperatures could also contribute to an increased SA level at 486

low temperature. 487

In sum, ET might exert an effective repression on the SA pathway through repressing 488

multiple genes in SA biosynthesis, transport and signaling. This repression might be more 489

critical for balancing growth and immunity at lower temperature when immunity is enhanced. 490

The temperature-dependent interaction of hormone biosynthesis and signaling might provide 491

versatility to achieve optimal defense responses for a broad range of pathogen interaction and 492

environmental conditions. 493

494

MATERIALS AND METHODS 495

Plants and growth conditions 496



24

The single and combined Arabidopsis thaliana mutants of dde2, ein2, sid2 and pad4 were 497

as previously described (Tsuda et al., 2009). Primers and restriction enzymes used for mutant 498

analyses are listed in Table S1. 499

The Arabidopsis plants were grown in chambers with a light intensity of 100 μmol m-2 sec-1 500

and relative humidity at 50-70%. Plants for the pathogen growth assay were grown under a 12 501

hour light/12 hour dark photoperiod unless specified. 502

RNA expression analysis 503

Total RNAs were extracted from soil-grown 14-day-old plants (22°C) and 21-day-old plants 504

(16°C) with TRIzol reagent (Invitrogen) according to the manufacturer’s protocol. For 505

expression analysis of individual genes, cDNAs were synthesized from total RNAs by using the 506

AffinityScript QPCR cDNA Synthesis Kit (Agilent Technologies). Quantitative PCR (qPCR) 507

was performed on the BIO-RAD PCR System using iQSYBR GREEN SuperMix (BIO-RAD). 508

Primers used in the qPCR are listed in Table S2. ACTIN2 was used as an internal control. 509

For whole transcriptome analysis, total RNAs were processed at the Cornell Genomic 510

Facility for 3’-RNA seq analysis (Tandonnet and Torres, 2017) on Illumina NextSeq500. The 511

read count for each gene was obtained from the mapping results and normalized to CPM (count 512

per million reads). Differentially expressed genes (DEGs) were defined by FDR (false discovery 513

rate) ≤0.001 and absolute value of Log2Ratio≥1. 514

Weighted Gene Co-expression Network Analysis (WGCNA) 515

DEGs were identified by DESeq2 (Moderated estimation of fold change and dispersion for 516

RNA-seq data with DESeq2 based on pairwise comparison between the mutants (ein2, sid2, and 517

ein2 sid2) and the wild type (Col-0), respectively, setting q-value < 0.05 and log2|fold-change|>1. 518

Subsequently, the expression levels of these DEGs were subjected to WGCNA (WGCNA: an R 519

package for weighted correlation network analysis) for gene co-expression analysis. To render 520

the network scale free, a soft thresholding power (softPower = 26) was chosen to transform the 521

Pearson similarity matrix into an adjacency matrix. Modules, in which genes exhibited similar 522

expression patterns, were determined by the dynamic tree cut method, and modules with high 523

correlated genes (e.g., Pearson correlation >= 0.8) were merged. The heatmap of genes assigned 524

into the modules was plot by pheatmap (R package). 525

Chromatin immunoprecipitation (ChIP) analysis 526



25

ChIP analysis was performed in Arabidopsis protoplasts as previously described (He et al., 527

2013; Bao et al., 2014). The coding regions of EIN3 were cloned into destination vector 528

pSATN1-GW (Zhang et al., 2017) using LR clonase (Invitrogen). Protoplasts were collected at 529

16 h after transformation. Immunoprecipitation experiments were carried out with anti-GFP 530

monoclonal antibodies (Life Technologies). 531

Pathogen growth assay 532

Pathogen growth assays were performed by dipping inoculation (Gou et al., 2015) unless 533

otherwise specified. Seedlings used for infection were grown for 21 days at 16°C, 14 days at 534

22°C, or 12 days at 28°C under a 12 hour light/12 hour dark photoperiod so that they reached a 535

similar developmental stage. The amounts of bacteria in plants were analyzed at 1 h (0 dpi), 3 d 536

(3 dpi) or 4 d (4 dpi) after dipping. For infiltration infection (Liu et al., 2015), seedlings were 537

grown for five weeks at 16°C, four weeks at 22°C or 18 days at 28°C before they were leaf-538

infiltrated with a bacterial solution. The amounts of bacteria in plants were analyzed at 1 h (0 539

dpi), 2 d (3 dpi) or 3 d (4 dpi) after infiltration. Pathogen growth was determined by log10-540

transformed bacterial number in infected leaves. 541

SA measurement 542

Total SA contents were assayed as previously described (Lou et al., 2016). Plants were 543

grown for 15 days at 22°C or 21 days at 16°C under a 12 h light/12 h dark photoperiod before 544

analysis. 545

Effector translocation assay 546

To determine the temperature dependence of the CyaA enzymatic activity, Pst DC3000 or 547

the Pst DC3000 ΔhrcQ-hrcU strains carrying the AvrPto-CyaA or HopY1-CyaA (as described in 548

Schechter et al, 2004 and Schechter et al., 2006) were cultured overnight in a KB plate. Bacteria 549

were washed from the KB plate by 10 mM MgCl2 and its concentration was adjusted to an 550

OD600 of 2. The cultures were centrifuged, and the pellets were washed and resuspended in 551

sonication buffer (20 mM Tris-HCl [pH 8.0], 10 mM MgCl2). The bacteria were disrupted by 552

sonication with a microtip for 2 min, and the cellular debris was pelleted by centrifugation and 553

the supernatant was collected as cell lysate. Plant extracts were made by grinding the leaf tissues 554

with liquid nitrogen and resuspending the tissue powder in sonication buffer. The reaction was 555

carried out by mixing 10 µl of lysate with plant extracts at 0.5 or 1.0 µg/µl in a 100 µl volume at 556

the designated temperature. 557



26

For translocation analysis, plants were infiltrated using a needless syringe with an inoculum 558

(OD=0.002) of Pst DC3000 or the Pst DC3000ΔhrcQ-hrcU mutant carrying the AvrPto-CyaA or 559

HopY1-CyaA. Leaf discs were harvested using a biopsy punch for cAMP quantification. 560

The CyaA product cAMP was extracted and quantified using the Direct cAMP ELISA kit 561

(ENZO) according to the manufacturer’s instruction, as previously described (Schechter et al., 562

2004). The measurement was normalized by total plant protein and the relative CyaA enzyme 563

activity at the two temperatures. 564

565

Accession Numbers 566

Accession numbers of the major genes in this research are listed in Table S1. 567

List of Supplemental Data 568

SUPPLEMENTAL DATA 569

Supplemental table S1 Short description of genes used in this study. 570 Supplemental table S2 Primers for genotyping, gene expression analysis and ChIP assays. 571

Supplemental table S3 Expression levels of differentially expressed genes (DEGs) used in 572

WGCNA. 573

Supplemental figure S1 The absolute amount of cAMPs produced by the CyaA reporter protein. 574

Supplemental figure S2 Pathogen growth after infiltration inoculation in hormone sector mutants 575

at 22°C. 576


at 28°C. 578


at 16°C. 580

Supplemental figure S5 Differentially expressed genes (DEGs) and co-expression modules 581

identified by WGCNA. 582

Supplemental figure S6 SA signaling genes have higher expression at lower temperature. 583

Supplemental figure S7 Expression of SID1 and SID2 at different times of the day. 584

Supplemental figure S8 Binding of EIN3 to the promoters of SA related genes. 585

586

587

ACKNOWLEDGEMENTS 588



27

We thank Arabidopsis Resource Center for Arabidopsis mutant seeds. We thank Dr. Allan 589

Collmer for the CyaA reporter strains. This work is supported by grants from NSF of USA (IOS 590

1353738) to J. Hua, the National Natural Science Foundation of China No. 31670269 to J. Hua, 591

the National Natural Science Foundation of China No. 31671774 and 31201279 to J. Hu and Y.J. 592

Guan, Fund of National Key Research and Development Project (No. 2018YFD0100902) to Y.J. 593

Guan, the Fundamental Research Funds for the Central Universities (No. 2019QNA6015) to R.H. 594

Pan, Jiangsu Collaborative Innovation Center for Modern Crop Production to J. Hu and J. Hua, 595

Dabeinong Funds for Discipline Development and Talent Training in Zhejiang University to J. 596

Hu. 597

598

599

Figure Legends 600

FIGURE LEGENDS 601

Figure 1 Lower temperature reduces pathogen propagation in Arabidopsis. 602

(A) Growth of the virulent pathogen Pst DC3000 in wild-type Col-0 plants at 0 and 3 days post 603

inoculation (dpi) for 22°C and 28°C or at 4 dpi for 16°C. 604

(B) Growth of Pst DC3000 in the wild-type Col-0 at 16°C at 3, 4 and 5 dpi. 605

(C) Growth of Pst DC3000, Pst DC3000 ΔCOR (coronatine-deficient) and Pst DC3000 ΔhrcU 606

(T3SS-deficient) in the wild type Col-0 at 4 dpi at 16°C and 3 dpi at 22°C. 607

For A-C, values represent means ± standard deviation (SD) for three biological repeats (n = 3); 608

‘*’ indicates a statistically significant difference between samples determined by Student’s t-test 609

(*: P < 0.05; ***: P<0.001; ns: not significant). Letters indicate statistically significant 610

differences by ANOVA (P < 0.05). Similar results were obtained from three independent 611

experiments (each with three biological repeats). FW, Fresh weight. cfu, colony forming unit. 612

(D) Disease symptoms after infection with Pst DC3000, Pst DC3000 (ΔCOR) or Pst DC3000 613

(ΔhrcU). 614

(E-F) Multivariate analysis of variance (MANOVA) for growth of Pst DC3000 and Pst DC3000 615

(ΔCOR) (E) and Pst DC3000 and Pst DC3000 (ΔhrcU) (F) at different temperatures. SS: square 616

sum; MS: mean square; F: F-text. Temp: temperature. 617

618

Figure 2 SA and PAD4 are critical for low temperature enhancement of plant immunity. 619



28

(A) Growth curve of Pst DC3000 grown in LB liquid medium at 16 °C and 22°C. Shown is the 620

result from one experiment and similar growth curves were observed for each temperature in a 621

second experiment. 622

(B) Effect of temperature on the enzymatic activity of HopY1-CyaA. Shown are means ± SD of 623

the amount of cAMP produced in reactions containing the lysate of Pst DC3000 carrying 624

HopY1-CyaA with plant extracts at 16°C, 22°C and 28°C. The plant extract was provided at a 625

concentration of 0.5 μg/μl or 1 μg/μl. Data are means from seven biological repeats, and the 626

standard deviations are indicated by error bars. 627

(C) Effector translation at different temperatures. Shown is the amount of cyclic AMP (cAMP) in 628

leaves of temperature-acclimated plants syringe-infiltrated with Pst DC3000 with AvrPto-CyaA, 629

Pst DC3000 with HopY1-CyaA, or Pst DC3000 ΔhrcQ-hrcU with AvrPto-CyaA. Values were 630

normalized by the total protein amount and the relative CyaA enzyme activity at the two 631

temperatures. Data are means from seven biological repeats, and the standard deviations are 632

indicated by error bars. Asterisks indicate statistical significance based on Student’s t-test (**: P 633

< 0.01) of pairwise comparisons for each individual effector strain at 16°C vs at 22 °C. 634

(D) Growth of Pst DC3000 in wild type Col-0, and cbfs-1 and cbfs-2 mutants measured at 4 dpi 635

for 16°C and 3 dpi for 22°C. Values represent means ± SD (n = 3). 636

(E, F) Growth of Pst DC3000 in the pad4 (E) and sid2 (F) mutants at 16 °C, 22°C and 28°C. The 637

bacterial growth was measured at 4 dpi, 3 dpi and 3 dpi at 16°C, 22°C and 28°C, respectively. 638

Values represent means ± SD (n = 3). Letters indicate statistically significant differences by 639

ANOVA (P < 0.05). Similar results were obtained in three independent experiments and shown is 640

the result from one experiment with three biological repeats. 641

(G-H) Multivariate analysis of variance (MANOVA) for pathogen growth in the mutant plants 642

pad4 (G) or sid2 (H) compared with the wild-type plants at different temperatures. SS: square 643

sum; MS: mean square; F: F-text. Temp: temperature. 644

Figure 3 ET and JA repress disease resistance through SA and PAD4. 645

Growth of Pst DC3000 in the wild type Col-0 and single and combined mutants of dde2, ein2, 646

sid2, and pad4. The bacterial growth was measured at 3 dpi, 3 dpi and 4 dpi for 22°C (A), 28°C 647

(B) and 16°C (C) respectively. Values represent means ± SD (n = 3); Letters indicate statistically 648

significant differences among different genotypes determined by ANOVA (P < 0.05). Similar 649

results were obtained in three independent experiments, and shown is the result from one 650



29

experiment with three biological repeats. dpi: days post inoculation. FW, Fresh weight. cfu, 651

colony forming unit. 652

Figure 4 Transcriptome analysis reveals differential contributions of SID2 to resistance at 653

low and normal temperature. 654

(A) Heatmap of gene expression in 6 modules defined by WGCNA (Weighted Gene Co-655

expression Network Analysis). Blue color indicates relatively high expression and red color 656

indicates relatively low expression. 657

(B) GO term analysis of genes in module 4. Shown are the results with significance of 658

Bonferroni-corrected (P < 0.05). The green star makers indicate genes involved in SA 659

biosynthesis and signaling. 660

Figure 5 SA biosynthesis genes in the ein2 sid2 mutant have a higher expression at 16°C 661

than at 22°C. 662

(A) Total SA in 3-week-old plants grown at 22°C or 4-week-old plants grown at 16 °C. 663

(B-D) Normalized expression levels as CPM (counts per million) of SID1 (B), SID2 (C), ICS2 664

(D), PAL1 (E), PAL2 (F), PAL3 (G), and PAL4 (H) analyzed by 3’-RNA-seq. 665

Values are means ± SD from three biological replicates. Letters indicate statistically significant 666

differences among different genotypes determined by ANOVA (P < 0.05). 667

Figure 6 Pst DC3000 induces SID1 and ICS2 expression in the ein2 sid2 mutant at low 668

temperature. 669

Relative expression levels of SID1 (A), SID2 (B), ICS2 (C) and PAL1 (D) analyzed by RT–qPCR 670

in leaves dipping-inoculated by Pst DC3000 at 0 hpi and 5 hpi. Expression levels are normalized 671

by gene expression at 22°C in Col-0 at 0 hpi. Values represent means ± SD from two 672

independent experiments. Letters indicate statistically significant differences among different 673

genotypes determined by ANOVA (P < 0.05). 674

Figure 7 EIN3 is associated with the promoter regions of SID1, SID2 and ICS2. 675

(A) Schematic diagram of DNA fragments used for ChIP experiments, and the EIN3 binding 676

motifs found in the promoters of SID1, SID2, EDS1 and ICS2. Triangles indicate the position of 677

the EIN3 binding motifs relative to the translation start site. 678

(B, C) ChIP assays of EIN3 binding to the promoter regions of SID1 (B) and ICS2 (C). Shown is 679

the qPCR results from samples precipitated with antibody (Ab) or without Ab of GFP. SID2 was 680

used as a positive control. Significant difference between samples was determined by Student’s 681



30

test. ‘ns’ meansno significant difference. Values represent means ± SD from two independent 682

experiments. 683

Figure 8 Models of low temperature enhancement of plant immunity. 684

(A) Modulation of plant immunity by temperature. SA and NLR form a positive amplification 685

loop. Low temperature promotes the SA pathway and NLR activities while high temperature 686

inhibits the SA pathway and NLR activities. 687

(B) Interaction of ET with the SA pathway at 22°C and 16°C. SA and EDS1/PAD4 form a 688

positive feedback loop; and upregulation of biosynthesis genes including SID1, ICS2 and SID2 689

contribute to the higher SA level at 16°C. SID2 plays a major role in SA biosynthesis at both 690

temperatures. ET represses multiple target genes to influence the SA pathway. SID2 is the ET 691

target that is a major player in SA biosynthesis at 22°C, while SID1and ICS2 are additional 692

targets that contribute to SA biosynthesis at 16°C. ICS2 has a minor role in SA biosynthesis 693

compared to SID2, but it could replace the role of SID2 at low temperature when its repression 694

by ET is released. 695

696

697



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https://www.ncbi.nlm.nih.gov/pubmed?term=He Y%2C Sidhu G%2C Pawlowski WP %282013%29 Chromatin immunoprecipitation for studying chromosomal localization of meiotic proteins in maize%2E Methods Mol Biol&dopt=abstract

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