Modulation of plant salicylic acid-associated immune ... · 2 39. Abstract. 40. S. alicylic acid (SA) plays a crucial role in plant i. nnate immun. ity. The . deployment of . 41

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Short title: UGT76D1 modulates immune response by DHBA glycosylation 1

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Corresponding author details: Dr. Bing-kai Hou 3

School of Life Sciences, Shandong University, China 4

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Article title: 6

Modulation of plant salicylic acid-associated immune responses 7

via glycosylation of dihydroxybenzoic acids 8

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Xu-xu Huang, Guo-qing Zhu, Qian Liu, Lu Chen, Yan-jie Li, Bing-kai Hou 12

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The Key Laboratory of Plant Development and Environment Adaptation Biology, 14

Ministry of Education; School of Life Science, Shandong University, Jinan 250100, 15

China. 16

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One sentence summary: The glycosyltransferase UGT76D1 catalyzes the 19

glycosylation of dihydroxybenzoic acids and modulates plant salicylic acid 20

homeostasis and immune responses. 21

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List of author contributions: B.K.H conceived the original research plans; X.X.H 26

performed the majority of the experiments; G.Q.Z, Q.L and L.C provided assistance 27

for some experiments; Y.J.L contributed to data analyses and interpretation; B.K.H. 28

and X.X.H wrote the article with input from all the authors. 29

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Funding information：This research was supported by the National Natural Science 33

Foundation of China (no. 91217301, 31570299, 31770313 to B.K.H) 34

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Corresponding author email：[email protected] 38

Plant Physiology Preview. Published on February 26, 2018, as DOI:10.1104/pp.17.01530

Copyright 2018 by the American Society of Plant Biologists

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Abstract 39

Salicylic acid (SA) plays a crucial role in plant innate immunity. The deployment of 40

SA-associated immune responses is primarily affected by SA concentration, which is 41

determined by a balance between SA biosynthesis and catabolism. However, the 42

mechanisms regulating SA homeostasis are poorly understood. In this study, we 43

characterized a unique UDP-glycosyltransferase, UGT76D1, which plays an 44

important role in SA homeostasis and associated immune responses in Arabidopsis 45

thaliana. Expression of UGT76D1 was induced by treatment with both the pathogen 46

Pseudomonas syringae pv. tomato (Pst) DC3000 and SA. Overexpression of 47

UGT76D1 resulted in high SA accumulation, significant up-regulation of 48

pathogen-related genes, and a hypersensitive response (HR)-like lesion mimic 49

phenotype. This HR-like phenotype was not observed following UGT76D1 50

overexpression in SA-deficient NahG transgenic or sid2 plants, suggesting that the 51

phenotype is SA dependent. Biochemical assays showed that UGT76D1 glycosylated 52

2,3-dihydroxybenzoic acid (2,3-DHBA) and 2,5-dihydroxybenzoic acid (2,5-DHBA), 53

the major catabolic forms of SA, to their glucose and xylose conjugates in vitro and in 54

vivo. Moreover, in a mutant background blocked in the formation of 2,3-DHBA and 55

2,5-DHBA, UGT76D1 overexpression did not cause a HR-like lesion mimic 56

phenotype. Following infection with Pst DC3000, UGT76D1 knockout mutants 57

displayed a delayed immune response, with reduced levels of DHBA glycosides and 58

SA, and down-regulated SA synthase expression. By contrast, UGT76D1 59

overexpression lines showed an enhanced immune response and increased SA 60

biosynthesis before and after pathogen infection. Thus, we propose that UGT76D1 61

plays an important role in SA homeostasis and plant immune responses by facilitating 62

glycosylation of dihydroxybenzoic acids. 63

64

Key words: Arabidopsis, Glycosyltransferase, Salicylic acid, Dihydroxybenzoic acid, 65

Immune response 66

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3

INTRODUCTION 68

Plants can initiate the specific hypersensitive response (HR), a localized 69

programmed cell death (PCD) response, at infection sites following challenge by 70

biotrophic pathogens (Heath, 2000; Van Doorn, 2011). This response is likely to be a 71

consequence of the progress of pathogen growth restriction (Coll et al., 2010; Coll et 72

al., 2011). The expression and regulation of HR relies on many components, such as 73

salicylic acid (SA), reactive oxygen species (ROS), jasmonic acid (JA), and ethylene 74

(ETH) (Coll et al., 2011). However, we currently have only a fragmented 75

understanding of the roles of the components leading to HR. 76

The identification of a number of lesion mimic mutants (LMMs), which display 77

spontaneous HR-like cell death, has increased our understanding of plant HR (Walbot 78

et al., 1983; Lorrain et al., 2003; Bruggeman et al., 2015). For instance, the LMM ssi4 79

from Arabidopsis, with a gain-of-function mutation of R-protein SSI4, constitutively 80

activates the ENHANCED DISEASE SUSCEPTIBILITY 1 (EDS1)-dependent SA 81

signaling pathways, and displays a conditional spontaneous lesion formation, 82

demonstrating the function of the R-protein in triggering HR (Shirano et al., 2002; 83

Zhou et al., 2004). One of the constitutive expresser of pathogenesis-related proteins 84

(cpr) mutants, cpr22, accumulates high levels of SA and displays a spontaneous lesion 85

phenotype (Yoshioka et al., 2001). Reducing the SA level in the accelerated cell death 86

(acd6) mutant or blocking SA signaling in the acd5 mutant attenuates the cell death 87

phenotype (Rate et al., 1999; Greenberg et al., 2000). Transgenic plants expressing 88

NahG (bacterial salicylate hydroxylase), which confers low SA concentration, are also 89

capable of inhibiting lesion formation, providing evidence that SA participates in the 90

regulation of cell death (Rate et al., 1999; Shah et al., 2001; Yoshioka et al., 2001). SA 91

can induce the expression of some pathogenesis-related (PR) genes, and promote the 92

production of ROS, and together they regulate cell death (Jabs, 1999; Alvarez, 2000; 93

Straus et al., 2010). In addition to disease resistance, SA also participates in multiple 94

processes in plants including senescence, which is a further kind of PCD. It has been 95

reported that leaf senescence and disease resistance use the same SA signaling 96



4

pathway (Vlot et al., 2009). 97

The biosynthesis of SA in plants has been proposed to occur through two 98

alternative pathways, namely the phenylalanine ammonia-lyase (PAL) and the 99

isochorismatesynthase (ICS) pathways. In the PAL pathway, benzoic acid and 100

ortho-coumaric acid are likely to be the two intermediates for SA biosynthesis 101

(Yalpani et al., 1993; Ryals et al., 1994; Chong et al., 2001). It is believed that the ICS 102

pathway produces most of the SA generated in plants (Wildermuth et al., 2001; 103

Dempsey et al., 2011). A past study showed that the SA level in sid2 (an ICS mutant) 104

was reduced to only 5–10% of the wild-type (WT) level after pathogen infection 105

(Wildermuth et al., 2001). 106

SA biosynthesis is regulated by multiple and complex factors. For instance, 107

ENHANCED DISEASE SUSCEPTIBILITY 1 (EDS1) and NON-RACE-SPECIFIC 108

DISEASE RESISTANCE 1 (NDR1) have been identified as upstream regulators of 109

SA biosynthesis in the effector-triggered immune response (ETI) (Aarts et al., 1998). 110

PHYTOALEXIN DEFICIENT 4 (PAD4) and SENESCENCE-ASSOCIATED 111

CARBOXYLESTERASE 101 (SAG101) are two components of EDS1-mediated 112

immunity (Feys et al., 2001; Feys et al., 2005). In addition, SYSTEMIC ACQUIRED 113

RESISTANCE DEFICIENT1 (SARD1) and its homolog CALMODULIN-BINDING 114

PROTEIN 60g (CBP60g) have been shown to be transcription activators of ICS1 115

expression (Zhang et al., 2010). 116

In addition to upstream regulation, active SA level is also modulated by 117

downstream metabolic modifications, including glycosylation, methylation, amino 118

acid conjugation, and hydroxylation. Different modifications of SA are likely to have 119

different functions in plant defense. Two main glycosyltransferases, UDP-dependent 120

glycosyltransferase 74F1 (UGT74F1) and UGT74F2, can transform SA into its 121

glucoside (SAG) or its glucose ester (SGE) (Lim et al., 2002; Dean and Delaney, 122

2008). SAG and SGE are the inactive forms of SA, and can be transformed back into 123

active SA when plants are challenged by pathogens (Dean and Delaney, 2008). Amino 124

acid-conjugated SA has been reported to be a potential activator of plant immunity 125

(Chen et al., 2013). Hydroxylated SA, including 2,3-dihydroxybenzoic acid 126



5

(2,3-DHBA) and 2,5-dihydroxybenzoic acid (2,5-DHBA), is the major metabolic 127

form of SA. Recently, the enzymes catalyzing SA to 2,3-DHBA (S3H) and to 128

2,5-DHBA (S5H) have been identified, and SA was found to accumulate in s3h or 129

s5h mutants (Zhang et al., 2013; Zhang et al., 2017). 130

The roles of 2,3-DHBA and 2,5-DHBA in Arabidopsis are not known; however, 131

2,5-DHBA in tomato is thought to play a signaling role in the activation of inducible 132

defenses. The signaling role of 2,5-DHBA is thought to be complementary to SA 133

because 2,5-DHBA induces the formation of a different set of pathogenesis-related 134

(PR) proteins that are not induced by SA (Bellés et al. 1999). Because of the 135

cytotoxicity of DHBA, 2,3-DHBA and 2,5-DHBA always exist as sugar conjugates in 136

plants (Bartsch et al., 2010). However, it appears that sugar conjugation of DHBA has 137

other physiological significance besides detoxification. 2,5-DHBA 138

5-O-β-D-xylopyranoside has been found to accumulate to high levels in cucumber 139

and tomato after inoculation with different pathogens (Fayos et al., 2006). It was also 140

reported that the sugar conjugates of 2,3-DHBA and 2,5-DHBA increased in 141

Arabidopsis during expression of pathogen resistance (Bartsch et al., 2010). Research 142

suggested that glycosylation of DHBA may be involved in plant immunity. Some 143

glycosyltransferases have been identified to be capable of catalyzing the 144

transformation of 2,3-DHBA and 2,5-DHBA in vitro to form their glucosyl or xylosyl 145

conjugates, although very little has been carried out towards understanding the 146

physiological relevance of these conjugates (Lim et al., 2001; Lim et al., 2002; Chen 147

and Li, 2017). As a consequence, it is still unclear whether DHBA glycosylation 148

functions in plant defense response and, if so, what its molecular mechanism entails. 149

Here, we identified and characterized the pathogen-induced glycosyltransferase 150

UGT76D1. We found that UGT76D1 was involved in the lesion mimic HR, including 151

the formation of natural necrotic spots, ROS accumulation, SA homeostasis, and PR 152

gene expression in rosette leaves of Arabidopsis. Furthermore, our experiments 153

revealed that UGT76D1 can catalyze the formation of 2,3-DHBA and 2,5-DHBA 154

glycosides in vitro and in vivo. We found that blocking DHBA glycosylation 155

abolished the UGT76D1-induced HR. Together, our data suggest that the 156



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glycosylation of DHBA plays a previously unrecognized role in the plant innate 157

immune response through modulating SA homeostasis. 158

RESULTS 159

UGT76D1 expression is induced by the plant pathogen Pst DC3000 160

Through searching the publicly available microarray data for UDP-dependent 161

glycosyltransferase (UGT) genes associated with plant secondary metabolism, we 162

found that several Arabidopsis UGT genes were induced by Pseudomonas syringae pv. 163

tomato DC3000 (Pst DC3000). UGT76D1 is one of the most highly 164

pathogen-responsive UGT genes. Since the UGT76D subfamily contains only this 165

unique member, UGT76D1 may have an important and specific role in plant immune 166

responses. To examine the reliability of microarray data, RT-qPCR was used to 167

analyze the expression of UGT76D1 at different time points after treatment with Pst 168

DC3000 or SA. The results showed that expression of UGT76D1 was strongly 169

induced by either Pst DC3000 or SA (Figs.1A and 1B). UGT76D1Pro::GUS 170

transgenic plants were constructed and GUS staining also demonstrated the high 171

induction of UGT76D1 expression by pathogen infection (Fig.1C), but not by MgCl2 172

treatment used as a negative control (Fig.1D). Thus, UGT76D1 is a 173

pathogen-responsive gene, and may be involved in plant defense responses. 174

UGT76D1 is involved in the spontaneous HR-like lesion mimic 175

response 176

To study the function of UGT76D1 in plants, we constructed UGT76D1 177

knockout mutants and transgenic lines overexpressing UGT76D1. Through the 178

CRISPR/Cas9 system, two independent mutant lines of UGT76D1 (ko-33, ko-36) 179

were isolated, each with a nucleotide deletion in the target site of the 5′ coding region 180

(Fig.S1, A–D), which causes a frameshift mutation. Nineteen independent UGT76D1 181

overexpression lines were obtained, and two lines (OE-17, OE-32) with a high 182



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expression of UGT76D1 were used in this study (Fig.S1, E). Under long-day 183

conditions, mutant lines exhibited a phenotype comparable to that of WT plants. On 184

the other hand, UGT76D1 overexpression lines showed obvious spontaneous necrotic 185

lesions, a phenotype that mimics hypersensitive cell death (Fig.2A). In the T2 186

generation of OE-17 and OE-32 lines, the lesion phenotype co-segregated with the 187

antibiotic resistance marker (Table S1). The lesions became more severe under 188

short-day conditions (Fig.S2). In addition to the spontaneous necrotic lesions, leaf 189

senescence in UGT76D1 overexpression lines also occurred earlier than in WT plants 190

(Fig.S3). 191

LMMs are mutants with spontaneous HR-like cell death without pathogen 192

infection (Lorrain et al., 2003; Bruggeman et al., 2015). The phenotype of UGT76D1 193

overexpression lines was similar to that of LMM mutants, suggesting a constitutively 194

activated hypersensitive response and localized cell death in the UGT76D1 195

overexpression lines. Trypan blue staining further confirmed cell death in UGT76D1 196

overexpression lines (Fig.2B). Reactive oxygen species (ROS) overproduction can 197

lead to cell death and is a family of crucial signal molecules in the activation of PCD 198

during HR (Malik et al., 2014). DAB staining showed that UGT76D1 overexpression 199

lines accumulated considerable amounts of hydrogen peroxide, whereas UGT76D1 200

knockout mutant lines exhibited hydrogen peroxide levels comparable to those in the 201

WT plants (Fig.2C), a phenomenon which correlated with the HR-like phenotypes of 202

these lines. We next examined the expression of the 203

SA-regulated PR1 and PR2 defense genes. PR1 and PR2 were drastically up-regulated 204

in UGT76D1 overexpression lines, whereas they were downregulated in the 205

UGT76D1 knockout mutant lines (Figs.2D, 2E), suggesting the involvement of 206

UGT76D1 in the SA-associated innate immune response. 207

The difference in changes of PR1 and PR2 expression between UGT76D1 208

overexpression and knockout mutant lines, as well as the spontaneous HR-like lesion 209

mimic phenotype occurring in the UGT76D1 overexpression lines, but not in the 210

mutant lines, prompted us to investigate SA levels in these lines. Our analysis showed 211

that free and total SA levels were considerably higher in UGT76D1 overexpression 212



8

lines than that in WT plants, but were moderately reduced in the mutant lines 213

compared to the WT (Figs.2F, 2G). These data suggest that UGT76D1 may be 214

involved in the plant innate immune response through modulating SA homeostasis. To 215

further explore whether UGT76D1 was involved in pathogen-induced HR, we tested 216

the ability of UGT76D1 mutants to trigger the HR against Pst DC3000 carrying 217

avrRpt2. We found that UGT76D1 knockout mutants suppressed the HR induced by 218

Pst DC3000 carrying avrRpt2 and the disease symptoms occurring at 48 h after 219

inoculation (Fig.3A). Cell death in each line was visualized with trypan blue staining 220

(Fig.3B). These results suggested that UGT76D1 may be a positive activator in at 221

least the Pst DC3000 (avrRpt2)-induced HR. 222

SA is required for the UGT76D1-activated lesion mimic phenotype 223

To determine whether the UGT76D1-activated lesion mimic phenotype is SA 224

dependent, UGT76D1 overexpression lines were crossed transgenic plants expressing 225

NahG, a SA hydroxylase that degrades SA (Delaney et al., 1994). Hybrids with high 226

expression of both UGT76D1 and NahG were selected, and named OE-17 NahG and 227

OE-32 NahG. It was shown that NahG can restore a WT phenotype (Fig. 4A) and 228

prevent a spontaneous lesion mimic phenotype despite UGT76D1 overexpression in 229

hybrid lines (Fig. 4B). Corresponding with the rescued leaf phenotype, cell death 230

(indicated by Trypan blue staining), the H2O2 content (indicated by DAB staining), 231

and the expression of PR1 and PR2 were restored to the levels of WT plants following 232

NahG expression in UGT76D1 overexpression lines (Figs. 4C, 4D and 4E). Most 233

importantly, the contents of free and total SA were reduced to undetectable levels in 234

the UGT76D1 overexpression NahG hybrids (Figs. 4F and 4G). Thus, we propose that 235

SA accumulation is the main factor triggering the UGT76D1-activated lesion mimic 236

phenotype. 237

UGT76D1 possesses biochemical activity towards DHBA 238

glycosylation in vitro 239



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To investigate the mechanism by which UGT76D1 was involved in maintaining 240

SA homeostasis, we next carried out in vitro screening of substrates catalyzed by this 241

glycosyltransferase. Fusion proteins of UGT76D1 with the GST-tag 242

were heterologously expressed in E.coli and then purified (Fig. 5A). When SA was 243

tested as a candidate substrate for UGT76D1, UGT76D1 exhibited no detectable 244

enzymatic activity towards SA, suggesting that SA was not the natural substrate (Fig. 245

5B). We further extended the candidate substrates to SA metabolites, phenolic 246

compounds, plant hormones, and flavonoids (Supplemental Table 2). UGT76D1 had 247

high enzymatic activities towards only the hydroxylated products of SA, namely 248

2,3-DHBA and 2,5-DHBA (Figs. 5C and 5D). No activity or only trace activity was 249

observed towards other compounds in our analyses (Table S2). It was previously 250

reported that 2,3-DHBA and 2,5-DHBA mainly form both glucosides and xylosides in 251

planta, although the physiological roles of these glycosides were unknown (Dempsey 252

et al., 2011). Thus, both UDP-glucose and UDP-xylose were used as the sugar donors 253

in our biochemical assays. We found that UGT76D1 can catalyze 2,3-DHBA and 254

2,5-DHBA to form their corresponding glucosides and xylosides (Figs. 5C and 5D). 255

LC-MS analysis confirmed the identity of the glucosides and xylosides produced from 256

2,3-DHBA and 2, 5-DHBA (Fig. S4). A previous study had found that 2,3-DHBA and 257

2,5-DHBA can be conjugated by UGT89A2 to form 2,3-DHBA or 2,5-DHBA 258

xylosides (Li et al., 2014). To determine the DHBA and sugar donor preferences of 259

UGT76D1 and UGT89A2, specific enzyme activity was tested in vitro. UGT89A2 260

exhibited a strong preference toward UDP-xylose over UDP-glucose. In contrast, 261

UGT76D1 preferred UDP-glucose to UDP-xylose (Table S3). 262

UGT76D1 functions in DHBA glycosylation in vivo 263

To further investigate the biochemical function of UGT76D1 in vivo, glycosides 264

of 2,3-DHBA and 2,5-DHBA were extracted and measured from UGT76D1 265

overexpression and knockout mutant lines. The high performance liquid 266

chromatography (HPLC) profiling of the DHBA sugar conjugates showed that 267

UGT76D1 overexpression lines accumulated much more 2,3-DHBA and 2,5-DHBA 268



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glycosides than that in WT under non-challenged conditions. However, in 269

non-challenged UGT76D1 mutant lines, only 2,3-DHBA xyloside was significantly 270

affected, accumulating at levels lower than that in WT (Figure 6A and 6B). The 271

relative level of DHBA glucosides in the UGT76D1 knockout mutants was very low 272

and comparable to that in WT. 273

The very low base levels of DHBA glucosides made them difficult to measure 274

accurately. To overcome this difficulty, we applied 100 μm 2,3-DHBA and 2,5-DHBA 275

to plants and re-measured the DHBA glucoside concentrations. Although the level of 276

2,5-DHBA glucosides was comparable between UGT76D1 knockout mutants and WT, 277

2,3-DHBA glucoside level in the mutants was much lower than that in WT (Figs. S5A 278

and S5B). Meanwhile, it was observed that UGT76D1 overexpression lines 279

accumulated much higher concentrations of both 2,3-DHBA and 2,5-DHBA 280

glucosides than that in WT upon application of DHBA; a similar result occurred with 281

UGT76D1 overexpression lines without DHBA application. Because expression of 282

UGT76D1 is Pst DC3000 inducible, the concentrations of 2,3-DHBA glycoside and 283

2,5-DHBA glycoside in UGT76D1 mutants and WT were re-measured 48 h after 284

infiltration with Pst DC3000 or with MgCl2 as the negative control. Our analysis 285

revealed that the accumulation of both 2,3-DHBA and 2,5-DHBA glucosides was 286

significantly reduced in Pst DC3000-inoculated UGT76D1 mutant plants compared to 287

that in WT (Figs. 6C and 6D). The concentrations of both 2,3-DHBA and 2,5-DHBA 288

xylosides were only slightly reduced in Pst DC3000-inoculated UGT76D1 mutants. 289

These data suggested that UGT76D1 functions in DHBA glycosylation in vivo and 290

may be the main enzyme responsible for the glucosylation of 2,3-DHBA and 291

2,5-DHBA. 292

We also attempted to determine the concentrations of the free forms of 2,3-DHBA 293

and 2,5-DHBA in the UGT76D1 overexpression and knockout mutant lines. We found 294

that the 2,3-DHBA level was too low to be detectable with or without pathogen 295

inoculation, a result which is consistent with those from previous studies (Bartsch et 296

al., 2010; Zhang et al., 2013). For free 2,5-DHBA, however, an interesting and 297

unexpected change was observed. After Pst DC3000 inoculation, UGT76D1 298



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overexpression lines accumulated much more of the free form of 2,5-DHBA than was 299

determined in the WT, whereas mutant lines had greatly reduced levels of the free 300

form of 2,5-DHBA compared to that in WT (Fig. S6). There are several hypotheses to 301

explain this unexpected change. Firstly, overexpression or mutation of UGT76D1 302

could alter metabolic flux towards the conjugated DHBA form, resulting in feedback 303

activation or inhibition of upstream enzymes of DHBA biosynthesis. Similar 304

situations have been found in previous studies (Chong et al., 2002; Tognetti et al., 305

2010). Secondly, one part of the DHBA pool may arise from cleavage of the 306

glucosylated form by glucosidases. Thirdly, because of the cytotoxicity of DHBAs, an 307

overcompensated degradation of DHBAs may occur in UGT76D1 mutants. 308

Immune response activated by UGT76D1 depends on the formation 309

of 2,3-DHBA and 2,5-DHBA glycosides 310

Previous research indicated that SA 3-hydroxylase (S3H) can convert SA to 311

2,3-DHBA, whereas the formation of 2,3-DHBA is blocked in the mutant s3h (Zhang 312

et al., 2013). To investigate the effects of UGT76D1 on the immune response in the 313

absence of 2,3-DHBA, the preferred substrate of UGT76D1, we produced hybrids 314

between UGT76D1 overexpression lines and s3h mutants. It was found that the s3h 315

background inhibited the spontaneous lesion mimic phenotype caused by UGT76D1 316

overexpression (Fig. 7A). DAB and Trypan blue staining also showed reduced levels 317

of H2O2 and cell death in the UGT76D1 overexpression s3h hybrid lines (Fig. 7B). 318

RT-qPCR analysis revealed that, although the expression of UGT76D1 remained at 319

high levels in the UGT76D1 overexpression s3h hybrids (Figs. 7C), the expression of 320

both PR1 and PR2 was significantly reduced (Figure 7D). We also measured the SA 321

levels in UGT76D1 overexpression s3h hybrid plants and found that the 322

concentrations of both free SA and total SA were markedly reduced (Fig. 7E). These 323

data indicated that the formation of 2,3-DHBA glycosides under the presence of 324

substrate 2,3-DHBA would be important for UGT76D1-activated immune response. 325

Recently, SA 5-hydroxylase (S5H) has also been described (Zhang et al., 2017). 326



12

It was reported that the concentrations of 2,3-DHBA and 2,5-DHBA were reduced in 327

the s3h s5h double mutant, which exhibited a dwarf and early-senescence phenotype 328

(Zhang et al., 2017). Here, we further examined the effect of increased UGT76D1 329

expression on the defense response in the s3h s5h double mutant background. We 330

found that UGT76D1 overexpression in s3h s5h double mutants did not cause the 331

HR-like lesion mimic phenotype seen in the WT background (Fig. 7F), further 332

demonstrating that the function of UGT76D1 in activating the immune response is 333

dependent on DHBA glycosylation. 334

DHBA glycosylation catalyzed by UGT76D1 modulates SA 335

biosynthesis during pathogen infection 336

SA is believed to be the crucial signaling molecule in SA-dependent plant 337

defense responses, where PR1 and PR2 are known to be important marker genes, the 338

expression of which is regulated by SA. It appears that the levels of SA and the 339

expression of PR1/PR2 always correlate with the lesion mimic phenotype of the 340

UGT76D1 overexpression and mutant lines, suggesting an important relationship 341

between UGT76D1-catalyzed DHBA glycosylation and SA synthesis. To further 342

investigate the physiological effects of UGT76D1 on SA synthesis in the plant 343

defense response, we analyzed the changes in SA concentration and PR expression in 344

UGT76D1 overexpression and mutant lines challenged by Pst DC3000 or the MgCl2 345

control. The expression of PR1 and PR2 was detected at different time points after 346

plants were inoculated with Pst DC3000 or the control buffer. It was found that PR1 347

and PR2 had high expression levels in the overexpression lines even at the beginning 348

of the treatment. As the time after pathogen challenge increased, the expression of 349

PR1 and PR2 increased rapidly in UGT76D1 overexpression lines. However, the 350

expression of PR1 and PR2 increased only slowly in the WT. In the UGT76D1 mutant 351

lines, the expression levels of PR1 and PR2 were even lower than that in WT at every 352

time point of pathogen treatment (Figs. 8A and 8B), suggesting that the defense 353

response was retarded by the loss of function of UGT76D1. We analyzed the free and 354



13

total SA concentrations in the UGT76D1 overexpression and mutant lines after 355

exposure to Pst DC3000 or MgCl2 for 48 h. Although SA concentrations in UGT76D1 356

overexpression lines were little more than that in WT 48 h after inoculation, the SA 357

concentrations in the knockout mutant lines were much lower than that in WT (Figs. 358

8C and 8D). These data suggested that the physiological role of UGT76D1 in the 359

SA-dependent defense response was a consequence of modulating SA levels. 360

The mechanism by which SA concentration is modulated by UGT76D1 was also 361

investigated. We analyzed the expression of SA synthesis-related genes in UGT76D1 362

overexpression and mutant lines with or without challenge by Pst DC3000. Without 363

Pst DC3000 treatment, the expression of several key SA-related genes, namely the 364

SA biosynthesis gene ICS1 and the SA biosynthesis regulatory genes EDS1 and PAD4, 365

were substantially increased in the UGT76D1 overexpression lines, whereas they 366

were only slightly decreased in the mutant lines (Fig. 8E). After challenge by Pst 367

DC3000 for 24 h or 48 h, the expression of the key SA biosynthetic gene ICS1 was 368

dramatically decreased in the UGT76D1 mutant lines (Fig. 8F), although the 369

expression levels of EDS1 and PAD4 were still only slightly decreased. It is likely that 370

UGT76D1 was involved in the positive feedback regulation of SA biosynthesis, 371

particularly via the regulation of the ICS1 gene. 372

To verify the role of ICS1 in the UGT76D1-mediated innate immune response, 373

we generated hybrids between UGT76D1 overexpression lines with sid2, an ICS1 374

mutant. Although expression of UGT76D1 remained at a high level in the hybrid lines, 375

the UGT76D1-activated lesion mimic phenotype was totally suppressed (Figs. 9A and 376

9B). We also measured the SA concentrations in the hybrid lines. It was found that 377

both the free SA and total SA were reduced to levels lower than that in WT plants (Fig. 378

9C). These data indicated that the pathogen-induced glycosyltransferase UGT76D1 379

functions in the defense response through modulating salicylic acid biosynthesis. The 380

glycosylation of DHBA by UGT76D1 may be involved in a positive feedback loop of 381

SA biosynthesis, accelerating SA accumulation in the process of plant defense 382

response. 383

384



14

DISCUSSION 385

UGT76D1 is a novel DHBA glycosyltransferase 386

Previous experiments had shown that SA is the main precursor of 2,3-DHBA and 387

2,5-DHBA (Ibrahim and Towers, 1959). The two DHBAs usually exist in a 388

glycosylated form (glucoside or xyloside), and were considered to be among the 389

major inactive forms of SA (Bartsch et al., 2010). However, the enzyme responsible 390

for the formation of those DHBA glycosides had previously been unknown. Recent 391

studies indicated that UGT89A2 is a 2,5-DHBA xylosyltransferase in Arabidopsis (Li 392

et al., 2014). However, overexpression of the UGT89A2 gene did not result in any 393

overt phenotype (Chen and Li, 2017). In this study, UGT76D1 was identified as a 394

novel DHBA glycosyltransferase in Arabidopsis. UGT76D1 can glycosylate both 395

2,3-DHBA and 2,5-DHBA, using either UDP-glucose or UDP-xylose as sugar donors. 396

Our analyses indicated that lines overexpressing UGT76D1 accumulated much higher 397

concentrations of DHBA glycosides, particularly the DHBA glucosides, than did the 398

WT. However, knockout mutant lines of UGT76D1 contained much lower 399

concentrations of DHBA glucosides following pathogen challenge. These data suggest 400

that the role of UGT76D1 in the defense response is mainly with respect to the 401

glucosylation of DHBAs. This hypothesis received support from our enzyme activity 402

analyses. Our results indicated that UGT76D1 prefers UDP-glucose to UDP-xylose as 403

the sugar donor for DHBA glycosylation. By contrast, although UGT89A2 exhibited 404

enzyme activity towards the DHBAs, it exhibited a strong preference toward 405

UDP-xylose over UDP-glucose. UGT76D1 and UGT89A2 seem to be too distant on 406

the phylogenetic tree, whereas they can act on the same substrate, DHBA. Actually, 407

this is a common phenomenon. For example, UGT73C6 and UGT78D1, two UGTs 408

belonging to different groups in the GT1 family, can act on the same flavonol 409

molecules (Jones et al., 2003). Another example involves auxin glycosylation. Both 410

UGT74E2 and UGT75D1 can catalyze the glycosylation of the auxin indole-3-butyric 411

acid (IBA) (Tognetti et al., 2010; Zhang et al., 2016), whereas UGT84B1 is reported 412



15

to act on the auxin indole-3-acetic acid (IAA) (Jackson et al., 2002). What is the 413

biological significance for plants to have several different UGTs acting on the same 414

substrate? It is speculated that plant evolution has involved the formation of 415

functionally redundant multiple glycosyltransferases active towards the same type of 416

substrates. A synergistic or coordinated interaction between different 417

glycosyltransferase members may be meaningful for the fine tuning of metabolic 418

homeostasis. On the other hand, the activities of these enzymes will depend on cell 419

specificity of enzyme expression, relative availability of substrates and sugar donors, 420

and relative compartmentalization of the enzyme and substrates, which may have the 421

potential to enhance the plant’s flexibility in development or in adaptation to diverse 422

environments. 423

Pathogen-induced UGT76D1 may act as a positive component to promote 424

hypersensitive response 425

In plants, the innate immune system has evolved to protect them from the 426

pathogens which attack them, but the mechanisms involved in mediating this defense 427

are poorly understood. Plant cells are usually capable of perceiving signals from 428

pathogens and inducing resistance to the challenge, which is achieved sometimes by 429

launching a cell-suicide mechanism to produce a localized PCD, known as HR, at the 430

infection site (Heath, 2000). The fates of cells at the infection site and in adjacent 431

positions are different due to the SA concentration gradient. In the infection site, high 432

levels of SA induced the degradation of NPR1 (an inhibitor of PCD in ETI), and then 433

cell death. By contrast, in cells adjacent to the infection site, the SA level is not high 434

enough to lead to cell death, so the cells survive and enhance resistance (Fu and Dong, 435

2013). UGT76D1 is a glycosyltranferase gene induced by pathogens. Transgenic 436

plants with high levels of expression of UGT76D1 displayed spontaneous local cell 437

death, a lesion mimic and HR-like phenotype. This finding suggested that UG76D1 438

may be a positive component in the regulation of the HR-related immune response. 439

When the SA hydroxylase gene NahG was transferred into UGT76D1 overexpression 440

lines, the lesion mimic phenotype, the high levels of H2O2 and the upregulated PR 441



16

expression disappeared. Thus, high levels of SA are required for lesion formation in 442

UGT76D1 overexpression lines. Under normal conditions, the basal expression of 443

UGT76D1 is very low. When plants were challenged by pathogens such as Pst 444

DC3000, UGT76D1 expression was induced. Based on these findings, we proposed 445

that UGT76D1 acts as a positive component, playing an important role in the 446

SA-activated hypersensitive response. 447

The glycosylation of DHBAs may be an important process responsible for the 448

UGT76D1-mediated innate immune response 449

2,5-DHBA glucosides accumulated in tomato and cucumber plants after infection 450

by different pathogens (Bellés et al., 1999; Fayos et al., 2006), while 2,3-DHBA 451

xylosides increased in Arabidopsis after induction by Pst DC3000 (avrRpm1) 452

(Bartsch et al., 2010). It is likely that DHBA glycosides have important roles in the 453

plant defense response. In this study, UGT76D1 overexpression lines can accumulate 454

much higher concentrations of 2,3- and 2,5-DHBA glycosides (glucosides and 455

xylosides) than that in WT. By contrast, the UGT76D1 mutants produced less 2,3- and 456

2,5-DHBA glucosides than that in WT after inoculation with Pst DC3000, suggesting 457

the greater role of 2,3-DHBA and 2,5-DHBA glucosylation in the 458

UGT76D1-activated immune response. S3H and S5H are enzymes responsible for the 459

conversion of SA to 2,3-DHBA and 2,5-DHBA, and the s3h s5h double mutants 460

abolished the production of 2,3-DHBA and 2,5-DHBA (Zhang et al., 2013; Zhang et 461

al., 2017). In our experiments, when UGT76D1 was overexpressed in s3h mutant or 462

s3h s5h double mutant backgrounds, we found that the HR-like lesion mimic 463

phenotype caused by UGT76D1 overexpression was totally suppressed. These results 464

suggested that the lack of glycosylation of 2,3-DHBA on its own or of both 465

2,3-DHBA and 2,5-DHBA abolished the UGT76D1-activated immune response. How 466

does the s3h single mutant suppress the lesion mimic phenotype caused by UGT76D1? 467

We proposed several possible reasons. Firstly, it was reported that S3H can convert 468

SA to both 2,3-DHBA and 2,5-DHBA in vitro (Zhang et al., 2013), therefore, s3h 469

mutation may be efficient for blocking the formation of 2,3-DHBA and 2,5DHBA. In 470



17

addition, s3h mutant nearly abolished the formation of 2,3-DHBA, while s5h mutant 471

still maintain the formation of 2,5-DHBA to a greater extent (Zhang et al., 2017), 472

Which may be due to the enzyme activity of S3H in s5h mutant and also suggest a 473

more crucial role for S3H in the metabolic flux from SA to DHBAs. Consistent with 474

this hypothesis, our results indicated that SA level was restored to the s3h level in the 475

UGT76D1OE s3h hybrid plants. Secondly, because of the difference in molecular 476

structures, 2,3-DHBA glucoside may have different roles from 2,5-DHBA glucoside 477

in the defense responses, thus resulting in the elimination of the lesion phenotype 478

when UGT76D1 was overexpressed in a s3h background. Thirdly, 479

UGT76D1-activated immune response is likely to depend on a threshold of 480

2,3-DHBA and 2,5-DHBA concentrations. 481

It was reported that SA accumulated in the s3h s5h double mutant or the s3h 482

single mutant. However, the s3h and s3h s5h mutants did not show the HR-like lesion 483

phenotype as was exhibited in the UGT76D1 overexpression lines, but only showed 484

dwarf or earlier leaf senescence traits when compared to the WT (Zhang et al., 2013; 485

Zhang et al., 2017). Previous studies had indicated that leaf senescence and HR are 486

both examples of PCD, triggered by different stimuli (Love et al., 2008; Rivas-San 487

Vicente and Plasencia, 2011). Here, UGT76D1 was demonstrated to be involved in 488

the HR-like immune response, which was different from the involvement of S3H or 489

S5H in senescence, suggesting that UGT76D1 may respond to the different stimuli 490

from S3H and S5H. In the past, DHBA glycosides were viewed simply as the storage 491

forms of DHBA. In this study, however, we revealed that the sugar conjugates of 492

DHBA, or the process towards their formation, are likely to be an important trigger to 493

initiate PCD in the plant HR response. 494

In this study, we also found that UGT76D1 has trace activity toward coumarins 495

and some other compounds in vitro. Previous studies indicated that scopoletin, a 496

coumarin compound, may be a reactive oxygen intermediate (ROI) scavenger, and 497

play a role in redox homeostasis during the HR of tobacco to TMV (Chong, 2002). 498

Here, because UGT76D1 has only a trace activity toward coumarins in vitro, we 499



18

propose that the glycosylation of coumarins may not be the major stimulus to HR 500

phenotype mediated by UGT76D1. 501

The glycosylation of DHBA may be involved in the positive feedback regulation 502

of SA synthesis 503

SA is a crucial signal for plant defense responses. Its levels and dynamic changes 504

in tissues will directly influence the SA-dependent defense responses of plants. Thus, 505

SA concentrations in plant defense responses must be precisely controlled (Shah, 506

2003; Fu and Dong, 2013). When challenged by a pathogen, plants need to rapidly 507

synthesize more SA at the challenge sites to promote cell death. An amplification loop 508

of immune response may exist. For example, SA itself can activate the expression of 509

R genes and further promote downstream signals to synthesize more SA (Yang and 510

Hua, 2004). Previous studies have usually focused their attentions on the upstream 511

regulation of SA, but with very little attention being paid to downstream regulation of 512

SA. Whether or not the downstream events of SA biosynthesis pathway have an 513

important role in modulating SA concentration is largely unknown. Recently, it was 514

reported that the concentrations of DHBA glycosides increased after plants were 515

inoculated with Pst DC3000 (Bartsch et al., 2010). It was also noticed that expression 516

of both S3H and S5H were induced by plant pathogens, affecting the SA level (Zhang 517

et al., 2013; Zhang et al., 2017). These findings suggested the importance in SA 518

signaling of downstream metabolic processes of SA. In a previous study, 519

glycosyltransferase UGT76B1 was found to be involved in the modulation of SA 520

levels and defense responses (von Saint Paul et al., 2011). Isoleucic acid 521

(2-hydroxy-3-methyl-pentanoic acid) was identified to be a substrate for UGT76B1, 522

and UGT76B1 is known to function as a novel player in SA-JA signaling crosstalk 523

(von Saint Paul et al., 2011). However, the step at which isoleucic acid influences SA 524

level or its action mechanism is currently not clear. In another report, UGT76B1 was 525

found to have SA glycosyltransferase (SAGT) activity, and some immune-priming 526

compounds can repress the activities of SAGTs including UGT74F1and UGT76B1 527

(Noutoshi et al., 2012). These examples suggest the complexity of regulation 528



19

mechanisms in SA levels and defense response. 529

In this study, our focus was on the glycosylation of 2,3- and 2,5-DHBA, the two 530

main forms of hydroxylated SA. UGT76D1 was found to encode DHBA 531

glycosyltransferase, which can convert both 2,3-DHBA and 2,5-DHBA to their 532

glycosides, particularly the glucosides. More importantly, we found that the levels of 533

SA can be changed after disturbing the expression of UGT76D1 in the pathogen 534

infection process. Our analyses indicated that the key SA synthase gene, ICS1, was 535

significantly upregulated in UGT76D1 overexpression lines, but downregulated in 536

UGT76D1 knockout mutants. The findings presented here suggested that the 537

glucosylation of DHBA catalyzed by UGT76D1 may be involved in the positive 538

feedback regulation of SA synthesis. Therefore, this study revealed that the 539

glucosylation of DHBA plays a previously unrecognized role in modulating SA 540

homeostasis and plant immune response. 541

In conclusion, we propose a putative working model for UGT76D1 (Figure 10). 542

When plants are challenged by pathogens, expression of UGT76D1 is induced to a 543

high level, and the formation of DHBA glycosides is accelerated. At the same time, 544

DHBA glycosylation may activate SA synthase and then increase SA synthesis 545

through an unknown positive feedback loop, possibly through increasing the 546

metabolic flux towards SA and the DHBAs. High levels of SA accumulation lead to 547

oxidative burst and PR gene expression, and ultimately lead to PCD and increased 548

plant resistance to pathogens. Considering the xylosyltransferase activity of 549

UGT89A2 towards DHBAs, we cannot exclude the role of UGT89A2 in this 550

immune-priming process. However, the detailed mechanism by which DHBA 551

glycosylation regulates SA biosynthesis requires further investigation. 552

553

554

555

556

557



20

MATERIALS AND METHODS 558

Plant materials and growth conditions 559

Arabidopsis ecotype Columbia-0 (Col-0) was used in this study. For selection of 560

transgenic plants, SA treatment, and GUS staining, seeds were sterilized and imbibed 561

for 3 d at 4°C in the dark and sown on plates with Murashige and Skoog medium and 562

1% (w/v) Suc, solidified with 0.8% (w/v) phytoagar. The plates were transferred to a 563

growth room with a temperature at 22°C in a long day (16 h light/8 h dark). For all 564

other analyses, plants were grown for 1 week as described above and transferred to 565

soil under a long day condition (16 h light/8 h dark, approximately 100 µmol photons 566

m−2

s−1

) for the indicated times. A short day condition (8 h light/16 h dark) was used 567

to determine whether the lesion phenotype of UGT76D1 overexpression lines is 568

influenced by light cycle. 569

GUS staining 570

Sequences about 1500 bp upstream of the UGT76D1 transcription start were 571

amplified from the Arabidopsis genome by PCR using UGT76D1 promoter specific 572

primers (Table S4). The amplified sequences were inserted into the pBI121 plasmid to 573

replace the CaMV35S promoter. Arabidopsis was transformed with the 574

UGT76D1pro:GUS vector to generate UGT76D1pro:GUS transgenic plants through 575

the floral dip method (Clough and Bent, 1998). 576

For GUS staining assays, leaves of two-week-old transgenic seedlings of 577

UGT76D1pro:GUS were soaked in 10 mM MgCl2 (control) or Pst DC3000 (OD600 = 578

0.01). Seedlings were then collected in different time points for GUS staining. At each 579

time point, GUS activity was measured in at least twelve individual plants, most of 580

them with similar results were used to take photos. 581

GUS staining was performed as described by Wang et al. (2012). Briefly, two 582

independent lines of the UGT76D1pro:GUS transgenic plants were first fixed with 583

90% acetone on ice for 20 min, and then washed with staining buffer (50 mM sodium 584



21

phosphate, pH 7.2, 0.2 mM K 3 Fe(CN) 6 , 0.2 mM K 4 Fe(CN) 6, and 0.2% Triton 585

X-100) without X-Gluc (5-bromo-4-chloro-3-indolyl-β-D-galactopyr-anoside) twice 586

before adding staining buffer with X-Gluc (final concentration of 2 mM) and 587

incubation overnight at 37°C. Two independent transgenic lines showing similar 588

results were used as sources for the photos. 589

Plasmid construction and creation of transgenic Arabidopsis lines 590

Full-length cDNA of UGT76D1 was obtained from total RNA of Arabidopsis 591

Col-0 by reverse transcription PCR using specific primers (Table S4). The cDNA was 592

inserted into plasmid pBluescript SK, and then transferred to the plant expression 593

vector pBI121 to replace the GUS gene. The constructed plant expression plasmids 594

were used to transform Arabidopsis, using the floral dip method (Clough and Bent, 595

1998). The transgenic plants were selected for kanamycin resistance. After selection 596

for three generations, the homozygous UGT76D1 overexpression lines were obtained. 597

Two independent overexpression lines (OE-17 and OE-32), with high expression 598

levels of UGT76D1 and similar phenotypes, were selected for further study. 599

UGT76D1 mutant lines were obtained, using the CRISPR/Cas9 system (Feng et al., 600

2013; Li et al., 2013). The 19-bp sequence (5′-GCGTCCTACCTTTCTTCCC-3′), 601

with high specificity to the UGT76D1 gene, was selected as the targeting sequence for 602

UGT76D1. Two knockout mutant lines (ko-33 and ko-36) with different deletions in 603

the 5′ coding region of UGT76D1 were selected for further study. 604

DAB and trypan blue staining 605

Approximately four-week-old plants were used in these staining experiments. 606

For detecting H2O2, DAB staining was performed as described by 607

Thordal-Christensen et al. (1997). Whole rosette leaves were immersed in a 1% 608

solution of 3,3'-diaminobenzidine (DAB) in Tris-HCl buffer (pH 6.5) for 16 h at 25°C 609

under dark conditions, and then cleared by boiling destaining solution (ethanol:acetic 610

acid:glycerol = 3:1:1) for 10 min. H2O2 accumulation was visualized by the 611

yellow-brown color. 612



22

For detecting cell death, trypan blue staining was carried out according to the 613

method described previously (Yang et al., 2015). Plant leaves were boiled 1 min in 614

Trypan Blue solution (10 mL of lactic acid, 10 mL of glycerol, 10 g of phenol, and 10 615

mg of Trypan Blue, dissolved in 10 mL of distilled water) diluted in 1 volume of 616

100% ethanol. Leaves were then bleached in choral hydrate (2.5 g mL−1

) overnight 617

and conserved in 50% glycerol. 618

Protein purification and enzyme assays 619

Full-length cDNA of UGT76D1 was inserted into plasmid pBluescript SK, and 620

then transferred to the prokaryotic expression vector pGEX-2T. The UGT76D1-GST 621

fusion protein was expressed in E. coli XL1-Blue and then purified using the method 622

described previously (Hou et al., 2004). The enzyme assays were performed at 30°C 623

using methods described previously (Lim et al., 2001) with modifications. About 2μg 624

of UGT76D1 fusion protein were added to 200 μL enzyme reaction mixture. The 625

reaction mixture contained 100 mM Tris-HCl (pH 7.6), 14 mM 2-mercaptoethanol, 5 626

mM UDP-glucose or UDP-xylose, 2.5 mM MgSO4, 10 mM KCl and 1mM substrate. 627

The tested substrates in this study are listed in Table S2. The reaction products were 628

analyzed by HPLC, and confirmed by LC-MS. 629

Measurements of SA, DHBA, and DHBA glycosides 630

Four-week-old plants were harvested for the analysis of SA and DHBA glycoside 631

concentrations. Free SA and total SA were extracted and measured by the methods 632

described previously (Nawrath and Metraux, 1999). The internal reference, 633

2,6-dichloroisonicotinic acid (INA), was used to estimate the loss ratesduring 634

extraction. SA was detected with a 295-nm excitation wavelength and a 405-nm 635

emission wavelength, using a fluorescence detector. DHBA glycosides were extracted 636

and measured by the protocol described previously (Zhang et al., 2012; Zhang et al., 637

2013), with modifications. Briefly, DHBA glycosides were extracted from leaves 638

homogenized in 80% (v/v) methanol overnight at 4°C. Caffeic acid and ferulic acid 639

were used as the internal references to estimate the loss rates during extraction. Target 640



23

compounds were analyzed by HPLC (Shimadzu, Kyoto, Japan) on a C18 columnat a 641

flow rate of 0.7 ml min-1

. The mobile phases were composed of sodium acetate (50 642

mM, pH 5.5) and MeOH. DHBA glycosides were detected using a UV detector at 310 643

nm wavelength. The identity of these compounds following HPLC profiling by 644

retention time were confirmed by liquid chromatography-mass spectrometer (LC-MS) 645

(Thermo Scientific, Waltham, MA, USA), and UV absorbance. 2,3-DHBA and 646

2,5-DHBA were extracted and measured as previously described (Zhang et al., 2017). 647

To quantify SA concentration, a SA standard curve was constructed. The peak 648

area of SA showed a close linear relationship with concentration in the standard curve. 649

Because the DHBA glycosides are not commercially available, the relative 650

concentrations of DHBA glycosides were analyzed in this study. The peak areas of 651

DHBA glycosides from the overexpression lines and knockout mutant lines were 652

determined and compared to the corresponding values from the WT. 653

RNA extraction and gene expression analysis 654

For analysis of gene expression, the rosette leaves from four-week-old plants (6 655

plants grown in different pots at the same time for each technical replicates) were 656

collected for RNA extraction. Total RNA was extracted using the Trizol reagent 657

(TaKaRa, Tokyo, Japan). Reverse transcription was performed using Prime Script RT 658

reagent kit (TaKaRa, Tokyo, Japan). RT-qPCR were performed with a Bio-Rad 659

thermal-cycling system (CFX Connect, Hercules, CA, USA), using a SYBR Green 660

PCR Master Mix kit (TaKaRa, Tokyo, Japan). ACTIN2 was used as the internal 661

control. Results were normalized to the reference gene ACTIN2 using the ΔΔCt 662

method. Primers used in RT-qPCR are listed in Supplemental Table S4. 663

Pst DC3000 cultivation and challenge assays 664

Pst DC3000 was used for most of the pathogen assays, while Pst DC3000 665

(avrRpt2) were used for HR assays. Both bacterial strains were cultured in King’s B 666

liquid medium (King et al., 1954) at 30°C, washed twice in 10 mM MgCl2, and 667

resuspended at OD600 = 0.001 (for Pst DC3000) or 0.02 [for Pst DC3000 (avrRpt2)]. 668



24

The resulting suspension solution was injected into the leaves of four-week-old plants; 669

MgCl2 (10 mM) was used as the negative control. Inoculated leaves were collected at 670

different time points to determine the expression of SA-related genes in response to 671

pathogen challenge. SA levels were determined at 48h after injection. 672

Statistical analysis 673

All experiments were carried out with at least three independent biological 674

replicates, with each measurement also being carried out in triplicate. Data are 675

presented as the mean ± SD. Data were statistically analyzed using Student’s t-test. 676

Asterisks indicate significant differences relative to the wild type or control (*P < 677

0.05, **P < 0.01). 678

679

ACCESSION NUMBERS 680

Sequence data from this article can be found in the GenBank/EMBL data libraries 681

under accession numbers UGT76D1 (At2g26480), PR1 (At2g14610), PR2 682

(At3g57260), EDS1 (At3g48090), PAD4 (At3g52430), ICS1 (At1g74710). 683

684

Supplemental Data 685

Supplemental Figure S1. Generation and identification of UGT76D1 mutants 686

and overexpression lines. 687

688

Supplemental Figure S2. Exaggerated necrotic lesion phenotype of 689

UGT76D1 overexpression lines under short day conditions (8 h light/16 h 690

dark). 691

Supplemental Figure S3. The leaf senescence phenotype of UGT76D1 692

overexpression and mutant lines. 693

694

Supplemental Figure S4. LC-MS analyses confirmed the glycoside formation 695

from UGT76D1 catalyzed 2,3-DHBA and 2,5-DHBA under positive ion mode. 696



25

697

Supplemental Figure S5. Analyses of DHBA glucoside in UGT76D1 698

overexpression and mutant lines after application of DHBA. 699

700

Supplemental Figure S6. LC-MS analyses of free forms of 2,3-DHBA and 701

2,5-DHBA in UGT76D1 overexpression and mutant lines with or without 702

inoculation of Pst DC3000. 703

704

Supplemental Table S1. Co-segregation data of LMM phenotype and 705

kanamycin resistance marker in T2 generation 706

707

Supplemental Table S2. Candidate substrates detected for UGT76D1 708

enzymatic activity 709

710

Supplemental Table S3. Glucosyltransferase activity of UGT76D1 and 711

UGT89A2 towards 2,3-DHBA and 2,5-DHBA with different sugar donors 712

713

Supplemental Table S4. Primers used in this study. 714

715

ACKNOWLEDGMENTS 716

We thank Dr. Shuhua Yang (China Agricultural University) for providing the 717

bacteria strains Pst DC3000, Pst DC3000 (avrRpt2) and the sid2 mutant seeds. We 718

also thank Dr. Kewei Zhang (Zhejiang Normal University, China) for providing the 719

s3h mutant and s3h s5h double mutant seeds, Dr. Jia Li (Lanzhou University, China) 720

for providing the NahG transgenic seeds. This research was supported by National 721

Natural Science Foundation of China (no. 91217301, 31570299, 31770313 to B.K.H). 722

723

724

725



26

FIGURE LEGENDS 726

Figure 1. Expression of UGT76D1 is induced by SA and Pst DC3000. A and B, 727

RT-qPCR analysis of UGT76D1 expression induction by SA and Pst DC3000 728

treatment. Mock treatment in A is DMSO solvent. Mock treatment in B is 10 729

mM MgCl2 suspension buffer. The value of WT with mock treatment for 0 h 730

was set at 1. Data are means ± SD of three biological replicates (**P < 0.01, *P 731

< 0.05, Student’s t-test). C and D, GUS staining of UGT76D1Pro:GUS 732

expression following Pst DC3000 (C) and MgCl2 (mock, D) inoculation. Bars = 733

1 mm (upper panels) and 200 μm (lower panels). 734

735

Figure 2. Analysis of UGT76D1 mutant and overexpression lines. A, 736

Phenotype of four-week-old wild-type (WT), UGT76D1 overexpression lines 737

(OE-17 and OE-32) and UGT76D1 mutant lines (ko-33 and ko-36) grown 738

under 22°C and long day conditions (16 h light/8 h dark). Right panel is a 739

magnified photograph showing the spontaneous lesion mimic phenotype in 740

rosette leaves of overexpression lines (Bar = 1cm for both panels). B, Trypan 741

blue staining showing cell death in UGT76D1 overexpression and mutant lines. 742

Four-week-old plants grown under long-day condition were used for the 743

staining assay. The bottom panels are the magnified photographs of top panels. 744

Bars = 1 cm (top panels) and 100 μm (bottom panels). C, DAB staining 745

showing the H2O2 content of UGT76D1 overexpression and mutant lines. 746

Four-week-old plants grown under long-day condition were used for the 747

staining assay. The bottom panels are magnified photographs of top panels. 748

Bars = 1 cm (top panels) and 100 μm (bottom panels). D and E, RT-qPCR 749

analysis of the expression of defense response genes PR1 and PR2 in 750

four-week-old UGT76D1 overexpression lines and mutant lines. The value of 751

WT plants was set at 1.0. Data are means ± SD of three biological replicates 752

(**P < 0.01, *P < 0.05, Student’s t-test). F and G, Quantification of free SA and 753

total SA levels in UGT76D1 overexpression and mutant lines. Leaves of 754



27

four-week-old plants grown under long day conditions at 22°C were collected 755

and used for the measurements. Data are means ± SD of three biological 756

replicates (**P < 0.01, *P < 0.05, Student’s t-test). 757

758

Figure 3. Hypersensitive response phenotype of UGT76D1 mutant lines 759

following avirulent pathogen induction. A and B, HR phenotypes (A) and 760

Trypan Blue staining showing cell death (B) of wild-type (WT) and UGT76D1 761

mutant (ko-33 and ko-36) leaves following inoculation with Pst DC3000 762

(avrRpt2) (OD600 = 0.02). MgCl2 treatment was used as mock control. At least 763

36 leaves were assessed for each genotype during each experiment, with a 764

similar phenotype displayed in most. Representative leaves are shown at 24 h 765

and 48 h post inoculation. Bars = 1cm. 766

767

Figure 4. SA is required for UGT76D1-activated lesion mimic phenotype. A, 768

Phenotypes of four-week-old wild-type (WT), UGT76D1 overexpression 769

(OE-17 and OE-32), NahG-expressing (NahG), and UGT76D1 770

overexpression/NahG hybrid (OE-17 NahG and OE-32 NahG) plants. Bar = 1 771

cm. B, RT-PCR analysis of the expression of UGT76D1 in UGT76D1 772

overexpression/NahG hybrid lines alongside control lines described in A. 773

ACTIN2 was used as the internal control. C, Trypan blue staining (top panel) 774

showing the cell death level and DAB staining (bottom panel) showing the 775

H2O2 contents in leaves from four-week-old plants of UGT76D1 776

overexpression/NahG hybrid lines alongside control lines described in A. Bars 777

= 1 cm. D and E, RT-qPCR analysis of PR1 and PR2 expression in UGT76D1 778

overexpression/NahG hybrid lines alongside control lines described in A. The 779

value of WT plants was set at 1. Data represent mean ± SD of three biological 780

replicates (**P < 0.01, *P < 0.05, Student’s t-test). F and G, Free and total SA 781

contents in UGT76D1 overexpression/NahG hybrid lines alongside control 782

lines described in A. Data are means ± SD of three biological replicates. 783

(*P<0.05, Student’s t-test). ND: not detectable. 784



28

785

Figure 5. UGT76D1 catalyzes the in vitro glycosylation of 2,3-DHBA and 786

2,5-DHBA, but not SA. A, SDS-PAGE detection of the purified recombinant 787

UGT76D1-GST fusion protein. Proteins were visualized by Coomassie Blue 788

staining. GST: glutathione-s-transferase; UGT76D1: UGT76D1 fusion protein. 789

B, HPLC analysis of SA glycosylation by UGT76D1. C and D, HPLC analysis 790

of 2,3-DHBA and 2,5DHBA glycosylation by UGT76D1 G: UDP-glucose; X: 791

UDP-xylose. GST protein was used as the negative control. 792

793

Figure 6. The relative levels of sugar conjugates of 2,3-DHBA and 2,5-DHBA 794

in UGT76D1 overexpression and mutant lines. A and B, HPLC profiling (A) and 795

the quantitation (B) of DHBA sugar conjugates in wild type (WT), UGT76D1 796

overexpression lines (OE-17 and OE-32), and UGT76D1 mutant lines (ko-33 797

and ko-36) in the absence of pathogen exposure. Data were normalized to the 798

corresponding DHBA glycoside in WT to account for the changes in UGT76D1 799

overexpression and mutant lines. C and D, HPLC profiling and the quantitation 800

of DHBA sugar conjugates in wild type and UGT76D1 mutant lines following 801

Pst DC3000 (DC) or 10 mM MgCl2 (Mock) treatment for 48 h. Data were 802

normalized to the corresponding DHBA glycoside in WT treated with Pst 803

DC3000 to account for the changes in UGT76D1 mutant lines. The DHBA 804

sugar conjugates formed by UGT76D1 catalysis in vitro were used as the 805

glycoside standards. Peak1: 2,5-DHBA glucosides; Peak2: 2,3-DHBA 806

glucosides; Peak3: 2,5-DHBA xlyoside; Peak4: 2,3-DHBA xylosides; Peak5: 807

internal reference (caffeic acid). 2,3DHBA-G: 2,3-DHBA glucosides; 808

2,3DHBA-X: 2,3DHBA xyloside; 2,5DHBA-G: 2,5-DHBA glucosides; 809

2,5DHBA-X: 2,5-DHBA xlyoside. Data are means ± SD of three biological 810

replicates (**P < 0.01, *P < 0.05, Student’s t-test). 811

812

Figure 7. UGT76D1-activated immune response depends on DHBA 813

glycosylation. A, Phenotypes of four-week-old wild-type (WT), UGT76D1 814



29

overexpression (OE-17 and OE-32), s3h mutant (s3h), and UGT76D1 815

overexpression/s3h hybrid (OE-17 s3h and OE-32 s3h) plants grown under 816

long day conditions at 22°C. Bar = 1 cm. B, DAB (top row panels) and Trypan 817

blue (bottom row panels) staining showing levels of H2O2 and cell death, 818

respectively, in leaves from four-week-old plants of UGT76D1 819

overexpression/s3h hybrid lines alongside control lines described in A. Bars = 820

100 μm. C, RT-PCR analysis of UGT76D1 expression in UGT76D1 821

overexpression/s3h hybrid lines alongside control lines described in A. 822

ACTIN2 was used as the internal control. D, RT-qPCR analysis of relative PR1 823

and PR2 expression in UGT76D1 overexpression/s3h hybrid lines alongside 824

control lines described in A. The value of WT plants was set at 1. Data are 825

means ± SD of three biological replicates (**P < 0.01, *P < 0.05, Student’s 826

t-test). E, The free and total SA levels in UGT76D1 overexpression/s3h hybrid 827

lines alongside control lines described in A. Data are means ± SD of three 828

biological replicates (**P < 0.01, *P < 0.05, Student’s t-test). F, Phenotypes of 829

transgenic plants overexpressing UGT76D1 in a WT or s3h s5h double mutant 830

background. The right panel shows the enlarged leaf phenotype. Leaf lesions 831

are indicated with red arrowheads. Bars = 1 cm (left panel) and 0.5 cm (right 832

panel). 833

834

Figure 8. The immune response and SA biosynthesis in UGT76D1 835

overexpression and mutant lines following treatment with Pst DC3000. A and B, 836

Relative PR1 and PR2 expression in three-week-old wild-type (WT) and 837

UGT76D1 overexpression (OE) and mutant (ko) plants following Pst DC3000 838

(DC) or MgCl2 (Mock) treatment. For either treatment, expression levels in WT 839

at 0 h were set at 1. C and D, Free and total SA levels in three-week-old 840

UGT76D1 overexpression (OE-17 and OE-32) and mutant (ko-33 and ko-36) 841

lines following treatment with Pst DC3000 or MgCl2 (Mock) for 48 h. E, 842

RT-qPCR analysis of EDS1, PAD4, and ICS1 expression in UGT76D1 843

overexpression and mutant lines without any experimental treatment. Gene 844



30

expression levels in WT were set at 1.0. F, RT-qPCR analysis of EDS1, PAD4, 845

and ICS1 expression in UGT76D1 mutant lines following treatment with Pst 846

DC3000 for 24 h and 48 h. Gene expression levels in WT following 24 h Pst 847

DC3000 treatment were set at 1.0. A to F, Data are means ± SD of three 848

biological replicates (**P < 0.01, *P < 0.05, Student’s t-test). 849

850

Figure 9. UGT76D1-activated immune response depends on SA biosynthesis. 851

A, Phenotypes of four-week-old wild-type (WT), UGT76D1 overexpression 852

(OE-17 and OE-32), sid2 mutant (sid2-1), and UGT76D1 overexpression/sid2 853

hybrid (OE-17 sid2-1 and OE-32 sid2-1) plants. Bar = 1 cm. B, RT-PCR 854

analysis of UGT76D1 expression in UGT76D1 overexpression/sid2 hybrid 855

lines alongside control lines described in A. ACTIN2 was used as the internal 856

control. C, Quantification of free SA and total SA levels in UGT76D1 857

overexpression/sid2 hybrid lines alongside control lines described in A. Leaves 858

of four-week-old plants grown under long day conditions at 22°C were 859

collected and used for the measurements. Data are means ± SD of three 860

biological replicates (Student’s t-test, *P<0.05, * * P <0.01). 861

862

Figure 10. Proposed scheme for the regulation of SA homeostasis and plant 863

defense responses by UGT76D1. When plants are challenged by pathogens, 864

expression of UGT76D1 is induced to a high level, and the formation of DHBA 865

glycosides is accelerated. At the same time, DHBA glycosylation may activate 866

SA synthase and then increase SA biosynthesis through an unknown positive 867

feedback loop, possibly by increasing the metabolic flux towards SA and the 868

DHBAs. High levels of SA accumulation lead to an oxidative burst and PR 869

gene expression, and ultimately lead to PCD and increased plant resistance to 870

pathogens. Considering the xylosyltransferase activity of UGT89A2 towards 871

DHBAs, we cannot exclude the role of UGT89A2 in this immune-priming 872

process. 873



31

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1

Figure 1. Expression of UGT76D1 is induced by SA and Pst DC3000. A and B,

RT-qPCR analysis of UGT76D1 expression induction by SA and Pst DC3000

treatment. Mock treatment in A is DMSO solvent. Mock treatment in B is 10

mM MgCl2 suspension buffer. The value of WT with mock treatment for 0 h

was set at 1. Data are means ± SD of three biological replicates (**P < 0.01, *P

< 0.05, Student’s t-test). C and D, GUS staining of UGT76D1Pro:GUS

expression following Pst DC3000 (C) and MgCl2 (mock, D) inoculation. Bars =

1 mm (upper panels) and 200 μm (lower panels).



1

Figure 2. Analysis of UGT76D1 mutant and overexpression lines. A,

Phenotype of four-week-old wild-type (WT), UGT76D1 overexpression lines



2

(OE-17 and OE-32) and UGT76D1 mutant lines (ko-33 and ko-36) grown

under 22°C and long day conditions (16 h light/8 h dark). Right panel is a

magnified photograph showing the spontaneous lesion mimic phenotype in

rosette leaves of overexpression lines (Bar = 1cm for both panels). B, Trypan

blue staining showing cell death in UGT76D1 overexpression and mutant lines.

Four-week-old plants grown under long-day condition were used for the

staining assay. The bottom panels are the magnified photographs of top panels.

Bars = 1 cm (top panels) and 100 μm (bottom panels). C, DAB staining

showing the H2O2 content of UGT76D1 overexpression and mutant lines.

Four-week-old plants grown under long-day condition were used for the

staining assay. The bottom panels are magnified photographs of top panels.

Bars = 1 cm (top panels) and 100 μm (bottom panels). D and E, RT-qPCR

analysis of the expression of defense response genes PR1 and PR2 in

four-week-old UGT76D1 overexpression lines and mutant lines. The value of

WT plants was set at 1.0. Data are means ± SD of three biological replicates

(**P < 0.01, *P < 0.05, Student’s t-test). F and G, Quantification of free SA and

total SA levels in UGT76D1 overexpression and mutant lines. Leaves of

four-week-old plants grown under long day conditions at 22°C were collected

and used for the measurements. Data are means ± SD of three biological

replicates (**P < 0.01, *P < 0.05, Student’s t-test).



1

Figure 3. Hypersensitive response phenotype of UGT76D1 mutant lines

following avirulent pathogen induction. A and B, HR phenotypes (A) and

Trypan Blue staining showing cell death (B) of wild-type (WT) and UGT76D1

mutant (ko-33 and ko-36) leaves following inoculation with Pst DC3000

(avrRpt2) (OD600 = 0.02). MgCl2 treatment was used as mock control. At least

36 leaves were assessed for each genotype during each experiment, with a

similar phenotype displayed in most. Representative leaves are shown at 24 h

and 48 h post inoculation. Bars = 1cm.



1

Figure 4. SA is required for UGT76D1-activated lesion mimic phenotype. A,

Phenotypes of four-week-old wild-type (WT), UGT76D1 overexpression

(OE-17 and OE-32), NahG-expressing (NahG), and UGT76D1

overexpression/NahG hybrid (OE-17 NahG and OE-32 NahG) plants. Bar = 1

cm. B, RT-PCR analysis of the expression of UGT76D1 in UGT76D1

overexpression/NahG hybrid lines alongside control lines described in A.

ACTIN2 was used as the internal control. C, Trypan blue staining (top panel)



2

showing the cell death level and DAB staining (bottom panel) showing the

H2O2 contents in leaves from four-week-old plants of UGT76D1

overexpression/NahG hybrid lines alongside control lines described in A. Bars

= 1 cm. D and E, RT-qPCR analysis of PR1 and PR2 expression in UGT76D1

overexpression/NahG hybrid lines alongside control lines described in A. The

value of WT plants was set at 1. Data represent mean ± SD of three biological

replicates (**P < 0.01, *P < 0.05, Student’s t-test). F and G, Free and total SA

contents in UGT76D1 overexpression/NahG hybrid lines alongside control

lines described in A. Data are means ± SD of three biological replicates.

(*P<0.05, Student’s t-test). ND: not detectable.



1

Figure 5. UGT76D1 catalyzes the in vitro glycosylation of 2,3-DHBA and

2,5-DHBA, but not SA. A, SDS-PAGE detection of the purified recombinant

UGT76D1-GST fusion protein. Proteins were visualized by Coomassie Blue

staining. GST: glutathione-s-transferase; UGT76D1: UGT76D1 fusion protein.

B, HPLC analysis of SA glycosylation by UGT76D1. C and D, HPLC analysis

of 2,3-DHBA and 2,5DHBA glycosylation by UGT76D1 G: UDP-glucose; X:

UDP-xylose. GST protein was used as the negative control.



1

Figure 6. The relative levels of sugar conjugates of 2,3-DHBA and 2,5-DHBA

in UGT76D1 overexpression and mutant lines. A and B, HPLC profiling (A) and

the quantitation (B) of DHBA sugar conjugates in wild type (WT), UGT76D1

overexpression lines (OE-17 and OE-32), and UGT76D1 mutant lines (ko-33

and ko-36) in the absence of pathogen exposure. Data were normalized to the

corresponding DHBA glycoside in WT to account for the changes in UGT76D1

overexpression and mutant lines. C and D, HPLC profiling and the quantitation

of DHBA sugar conjugates in wild type and UGT76D1 mutant lines following

Pst DC3000 (DC) or 10 mM MgCl2 (Mock) treatment for 48 h. Data were

normalized to the corresponding DHBA glycoside in WT treated with Pst

DC3000 to account for the changes in UGT76D1 mutant lines. The DHBA



2

sugar conjugates formed by UGT76D1 catalysis in vitro were used as the

glycoside standards. Peak1: 2,5-DHBA glucosides; Peak2: 2,3-DHBA

glucosides; Peak3: 2,5-DHBA xlyoside; Peak4: 2,3-DHBA xylosides; Peak5:

internal reference (caffeic acid). 2,3DHBA-G: 2,3-DHBA glucosides;

2,3DHBA-X: 2,3DHBA xyloside; 2,5DHBA-G: 2,5-DHBA glucosides;

2,5DHBA-X: 2,5-DHBA xlyoside. Data are means ± SD of three biological

replicates (**P < 0.01, *P < 0.05, Student’s t-test).



1



2

Figure 7. UGT76D1-activated immune response depends on DHBA

glycosylation. A, Phenotypes of four-week-old wild-type (WT), UGT76D1

overexpression (OE-17 and OE-32), s3h mutant (s3h), and UGT76D1

overexpression/s3h hybrid (OE-17 s3h and OE-32 s3h) plants grown under

long day conditions at 22°C. Bar = 1 cm. B, DAB (top row panels) and Trypan

blue (bottom row panels) staining showing levels of H2O2 and cell death,

respectively, in leaves from four-week-old plants of UGT76D1

overexpression/s3h hybrid lines alongside control lines described in A. Bars =

100 μm. C, RT-PCR analysis of UGT76D1 expression in UGT76D1

overexpression/s3h hybrid lines alongside control lines described in A.

ACTIN2 was used as the internal control. D, RT-qPCR analysis of relative PR1

and PR2 expression in UGT76D1 overexpression/s3h hybrid lines alongside

control lines described in A. The value of WT plants was set at 1. Data are

means ± SD of three biological replicates (**P < 0.01, *P < 0.05, Student’s

t-test). E, The free and total SA levels in UGT76D1 overexpression/s3h hybrid

lines alongside control lines described in A. Data are means ± SD of three

biological replicates (**P < 0.01, *P < 0.05, Student’s t-test). F, Phenotypes of

transgenic plants overexpressing UGT76D1 in a WT or s3h s5h double mutant

background. The right panel shows the enlarged leaf phenotype. Leaf lesions

are indicated with red arrowheads. Bars = 1 cm (left panel) and 0.5 cm (right

panel).



1

Figure 8. The immune response and SA biosynthesis in UGT76D1

overexpression and mutant lines following treatment with Pst DC3000. A and B,



2

Relative PR1 and PR2 expression in three-week-old wild-type (WT) and

UGT76D1 overexpression (OE) and mutant (ko) plants following Pst DC3000

(DC) or MgCl2 (Mock) treatment. For either treatment, expression levels in WT

at 0 h were set at 1. C and D, Free and total SA levels in three-week-old

UGT76D1 overexpression (OE-17 and OE-32) and mutant (ko-33 and ko-36)

lines following treatment with Pst DC3000 or MgCl2 (Mock) for 48 h. E,

RT-qPCR analysis of EDS1, PAD4, and ICS1 expression in UGT76D1

overexpression and mutant lines without any experimental treatment. Gene

expression levels in WT were set at 1.0. F, RT-qPCR analysis of EDS1, PAD4,

and ICS1 expression in UGT76D1 mutant lines following treatment with Pst

DC3000 for 24 h and 48 h. Gene expression levels in WT following 24 h Pst

DC3000 treatment were set at 1.0. A to F, Data are means ± SD of three

biological replicates (**P < 0.01, *P < 0.05, Student’s t-test).



1

Figure 9. UGT76D1-activated immune response depends on SA biosynthesis.

A, Phenotypes of four-week-old wild-type (WT), UGT76D1 overexpression

(OE-17 and OE-32), sid2 mutant (sid2-1), and UGT76D1 overexpression/sid2

hybrid (OE-17 sid2-1 and OE-32 sid2-1) plants. Bar = 1 cm. B, RT-PCR

analysis of UGT76D1 expression in UGT76D1 overexpression/sid2 hybrid

lines alongside control lines described in A. ACTIN2 was used as the internal

control. C, Quantification of free SA and total SA levels in UGT76D1

overexpression/sid2 hybrid lines alongside control lines described in A. Leaves

of four-week-old plants grown under long day conditions at 22°C were

collected and used for the measurements. Data are means ± SD of three

biological replicates (Student’s t-test, *P<0.05, * * P <0.01).



1

Figure 10. Proposed scheme for the regulation of SA homeostasis and plant

defense responses by UGT76D1. When plants are challenged by pathogens,

expression of UGT76D1 is induced to a high level, and the formation of DHBA

glycosides is accelerated. At the same time, DHBA glycosylation may activate

SA synthase and then increase SA biosynthesis through an unknown positive

feedback loop, possibly by increasing the metabolic flux towards SA and the



2

DHBAs. High levels of SA accumulation lead to an oxidative burst and PR

gene expression, and ultimately lead to PCD and increased plant resistance to

pathogens. Considering the xylosyltransferase activity of UGT89A2 towards

DHBAs, we cannot exclude the role of UGT89A2 in this immune-priming

process.



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Li J-F, Norville JE, Aach J, McCormack M, Zhang D, Bush J, Church GM, Sheen J (2013) Multiplex and homologous recombination-mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nature biotechnology 31: 688-691


Li X, Svedin E, Mo H, Atwell S, Dilkes BP, Chapple C (2014) Exploiting natural variation of secondary metabolism identifies a genecontrolling the glycosylation diversity of dihydroxybenzoic acids in Arabidopsis thaliana. Genetics 198: 1267-1276


Lim EK, Doucet CJ, Li Y, Elias L, Worrall D, Spencer SP, Ross J, Bowles DJ (2002) The activity of Arabidopsis glycosyltransferasestoward salicylic acid, 4-hydroxybenzoic acid, and other benzoates. J Biol Chem 277: 586-592


Lim EK, Li Y, Parr A, Jackson R, Ashford DA, Bowles DJ (2001) Identification of glucosyltransferase genes involved in sinapatemetabolism and lignin synthesis in Arabidopsis. J Biol Chem 276: 4344-4349


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http://www.ncbi.nlm.nih.gov/pubmed?term=Noutoshi Y%2C Okazaki M%2C Kida T%2C Nishina Y%2C Morishita Y%2C Ogawa T%2C Suzuki H%2C Shibata D%2C Jikumaru Y%2C Hanada A%2C Kamiya Y%2C Shirasu K %282012%29 Novel plant immune%2Dpriming compounds identified via high%2Dthroughput chemical screening target salicylic acid glucosyltransferases in Arabidopsis%2E Plant Cell 24%3A 3795%2D3804&dopt=abstract

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Rate DN, Cuenca JV, Bowman GR, Guttman DS, Greenberg JT (1999) The gain-of-function Arabidopsis acd6 mutant reveals novelregulation and function of the salicylic acid signaling pathway in controlling cell death, defenses, and cell growth. The Plant Cell 11:1695-1708


Rivas-San Vicente M, Plasencia J (2011) Salicylic acid beyond defence: its role in plant growth and development. Journal ofexperimental botany 62: 3321-3338


Ryals J, Uknes S, Ward E (1994) Systemic acquired resistance. Plant Physiology 104: 1109Shah J (2003) The salicylic acid loop in plantdefense. Current opinion in plant biology 6: 365-371


Shah J (2003) The salicylic acid loop in plant defense. Current opinion in plant biology 6: 365-371Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Shah J, Kachroo P, Nandi A, Klessig DF (2001) A recessive mutation in the Arabidopsis SSI2 gene confers SA-and NPR1-independentexpression of PR genes and resistance against bacterial and oomycete pathogens. The Plant Journal 25: 563-574


Shirano Y, Kachroo P, Shah J, Klessig DF (2002) A gain-of-function mutation in an Arabidopsis Toll Interleukin1 Receptor–NucleotideBinding Site–Leucine-Rich Repeat type R gene triggers defense responses and results in enhanced disease resistance. The PlantCell 14: 3149-3162


Straus MR, Rietz S, Ver Loren van Themaat E, Bartsch M, Parker JE (2010) Salicylic acid antagonism of EDS1-driven cell death isimportant for immune and oxidative stress responses in Arabidopsis. The Plant Journal 62: 628-640


Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillaeand hypersensitive response during the barley—powdery mildew interaction. The Plant Journal 11: 1187-1194


Tognetti VB, Van Aken O, Morreel K, Vandenbroucke K, van de Cotte B, De Clercq I, Chiwocha S, Fenske R, Prinsen E, Boerjan W,Genty B, Stubbs KA, Inze D, Van Breusegem F (2010) Perturbation of indole-3-butyric acid homeostasis by the UDP-glucosyltransferase UGT74E2 modulates Arabidopsis architecture and water stress tolerance. Plant Cell 22: 2660-2679


Van Doorn WG (2011) Classes of programmed cell death in plants, compared to those in animals. Journal of Experimental Botany 62:4749-4761Vlot AC, Dempsey DMA, Klessig DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Annual review ofphytopathology 47: 177-206


Vlot AC, Dempsey DMA, Klessig DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Annual review of phytopathology47: 177-206


von Saint Paul V, Zhang W, Kanawati B, Geist B, Faus-Kessler T, Schmitt-Kopplin P, Schaffner AR (2011) The Arabidopsisglucosyltransferase UGT76B1 conjugates isoleucic acid and modulates plant defense and senescence. Plant Cell 23: 4124-4145



http://www.ncbi.nlm.nih.gov/pubmed?term=Rate DN%2C Cuenca JV%2C Bowman GR%2C Guttman DS%2C Greenberg JT %281999%29 The gain%2Dof%2Dfunction Arabidopsis acd6 mutant reveals novel regulation and function of the salicylic acid signaling pathway in controlling cell death%2C defenses%2C and cell growth%2E The Plant Cell 11%3A 1695%2D1708&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Rate DN, Cuenca JV, Bowman GR, Guttman DS, Greenberg JT (1999) The gain-of-function Arabidopsis acd6 mutant reveals novel regulation and function of the salicylic acid signaling pathway in controlling cell death, defenses, and cell growth. The Plant Cell 11: 1695-1708

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http://www.ncbi.nlm.nih.gov/pubmed?term=Ryals J%2C Uknes S%2C Ward E %281994%29 Systemic acquired resistance%2E Plant Physiology 104%3A 1109Shah J %282003%29 The salicylic acid loop in plant defense%2E Current opinion in plant biology 6%3A 365%2D371&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Ryals J, Uknes S, Ward E (1994) Systemic acquired resistance. Plant Physiology 104: 1109Shah J (2003) The salicylic acid loop in plant defense. Current opinion in plant biology 6: 365-371

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http://www.ncbi.nlm.nih.gov/pubmed?term=Shah J %282003%29 The salicylic acid loop in plant defense%2E Current opinion in plant biology 6%3A 365%2D371&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Shah J (2003) The salicylic acid loop in plant defense. Current opinion in plant biology 6: 365-371

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http://www.ncbi.nlm.nih.gov/pubmed?term=Shah J%2C Kachroo P%2C Nandi A%2C Klessig DF %282001%29 A recessive mutation in the Arabidopsis SSI2 gene confers SA%2Dand NPR1%2Dindependent expression of PR genes and resistance against bacterial and oomycete pathogens%2E The Plant Journal 25%3A 563%2D574&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Shah J, Kachroo P, Nandi A, Klessig DF (2001) A recessive mutation in the Arabidopsis SSI2 gene confers SA-and NPR1-independent expression of PR genes and resistance against bacterial and oomycete pathogens. The Plant Journal 25: 563-574

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http://search.crossref.org/?page=1&rows=2&q=Shirano Y, Kachroo P, Shah J, Klessig DF (2002) A gain-of-function mutation in an Arabidopsis Toll Interleukin1 Receptor?Nucleotide Binding Site?Leucine-Rich Repeat type R gene triggers defense responses and results in enhanced disease resistance. The Plant Cell 14: 3149-3162

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http://search.crossref.org/?page=1&rows=2&q=Straus MR, Rietz S, Ver Loren van Themaat E, Bartsch M, Parker JE (2010) Salicylic acid antagonism of EDS1-driven cell death is important for immune and oxidative stress responses in Arabidopsis. The Plant Journal 62: 628-640

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http://www.ncbi.nlm.nih.gov/pubmed?term=Thordal%2DChristensen H%2C Zhang Z%2C Wei Y%2C Collinge DB %281997%29 Subcellular localization of H2O2 in plants%2E H2O2 accumulation in papillae and hypersensitive response during the barley�??powdery mildew interaction%2E The Plant Journal 11%3A 1187%2D1194&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Tognetti VB%2C Van Aken O%2C Morreel K%2C Vandenbroucke K%2C van de Cotte B%2C De Clercq I%2C Chiwocha S%2C Fenske R%2C Prinsen E%2C Boerjan W%2C Genty B%2C Stubbs KA%2C Inze D%2C Van Breusegem F %282010%29 Perturbation of indole%2D3%2Dbutyric acid homeostasis by the UDP%2Dglucosyltransferase UGT74E2 modulates Arabidopsis architecture and water stress tolerance%2E Plant Cell 22%3A 2660%2D2679&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=von Saint Paul V%2C Zhang W%2C Kanawati B%2C Geist B%2C Faus%2DKessler T%2C Schmitt%2DKopplin P%2C Schaffner AR %282011%29 The Arabidopsis glucosyltransferase UGT76B1 conjugates isoleucic acid and modulates plant defense and senescence%2E Plant Cell 23%3A 4124%2D4145&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=von Saint Paul V, Zhang W, Kanawati B, Geist B, Faus-Kessler T, Schmitt-Kopplin P, Schaffner AR (2011) The Arabidopsis glucosyltransferase UGT76B1 conjugates isoleucic acid and modulates plant defense and senescence. Plant Cell 23: 4124-4145

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

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http://scholar.google.com/scholar?as_q=The Arabidopsis glucosyltransferase UGT76B1 conjugates isoleucic acid and modulates plant defense and senescence&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=von&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1


Walbot V, Hoisington DA, Neuffer M (1983) Disease lesion mimic mutations. In Genetic engineering of plants. Springer, pp 431-442Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Wang B, Jin SH, Hu HQ, Sun YG, Wang YW, Han P, Hou BK (2012) UGT87A2, an Arabidopsis glycosyltransferase, regulates floweringtime via FLOWERING LOCUS C. New Phytologist 194: 666-675


Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence.Nature 414: 562-565


Yalpani N, León J, Lawton MA, Raskin I (1993) Pathway of salicylic acid biosynthesis in healthy and virus-inoculated tobacco. Plantphysiology 103: 315-321


Yang L, Li B, Zheng X-y, Li J, Yang M, Dong X, He G, An C, Deng XW (2015) Salicylic acid biosynthesis is enhanced and contributes toincreased biotrophic pathogen resistance in Arabidopsis hybrids. Nature communications 6: 7309


Yang S, Hua J (2004) A haplotype-specific Resistance gene regulated by BONZAI1 mediates temperature-dependent growth control inArabidopsis. The Plant Cell 16: 1060-1071


Yoshioka K, Kachroo P, Tsui F, Sharma SB, Shah J, Klessig DF (2001) Environmentally sensitive, SA-dependent defense responses inthe cpr22 mutant of Arabidopsis. The Plant Journal 26: 447-459


Zhang GZ, Jin SH, Jiang XY, Dong RR, Li P, Li YJ, Hou BK (2016) Ectopic expression of UGT75D1, a glycosyltransferase preferringindole-3-butyric acid, modulates cotyledon development and stress tolerance in seed germination of Arabidopsis thaliana. Plant MolBiol 90: 77-93


Zhang K, Bhuiya M-W, Pazo JR, Miao Y, Kim H, Ralph J, Liu C-J (2012) An engineered monolignol 4-O-methyltransferase depresseslignin biosynthesis and confers novel metabolic capability in Arabidopsis. The Plant Cell 24: 3135-3152


Zhang K, Halitschke R, Yin C, Liu CJ, Gan SS (2013) Salicylic acid 3-hydroxylase regulates Arabidopsis leaf longevity by mediatingsalicylic acid catabolism. Proc Natl Acad Sci U S A 110: 14807-14812


Zhang Y, Xu S, Ding P, Wang D, Cheng YT, He J, Gao M, Xu F, Li Y, Zhu Z (2010) Control of salicylic acid synthesis and systemicacquired resistance by two members of a plant-specific family of transcription factors. Proceedings of the National Academy ofSciences 107: 18220-18225


Zhang Y, Zhao L, Zhao J, Li Y, Wang J, Guo R, Gan S-S, Liu C-J, Zhang K (2017) S5H/DMR6 Encodes a Salicylic Acid 5-Hydroxylase ThatFine-Tunes Salicylic Acid Homeostasis. Plant physiology 175: 1082–1093


Zhou F, Menke FL, Yoshioka K, Moder W, Shirano Y, Klessig DF (2004) High humidity suppresses ssi4-mediated cell death and diseaseresistance upstream of MAP kinase activation, H2O2 production and defense gene expression. The Plant Journal 39: 920-932


http://www.ncbi.nlm.nih.gov/pubmed?term=Walbot V%2C Hoisington DA%2C Neuffer M %281983%29 Disease lesion mimic mutations%2E In Genetic engineering of plants%2E Springer%2C pp 431%2D442&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Walbot V, Hoisington DA, Neuffer M (1983) Disease lesion mimic mutations. In Genetic engineering of plants. Springer, pp 431-442

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

http://scholar.google.com/scholar?as_q=Disease lesion mimic mutations.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Disease lesion mimic mutations.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Walbot&as_ylo=1983&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Wang B%2C Jin SH%2C Hu HQ%2C Sun YG%2C Wang YW%2C Han P%2C Hou BK %282012%29 UGT87A2%2C an Arabidopsis glycosyltransferase%2C regulates flowering time via FLOWERING LOCUS C%2E New Phytologist 194%3A 666%2D675&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Wang B, Jin SH, Hu HQ, Sun YG, Wang YW, Han P, Hou BK (2012) UGT87A2, an Arabidopsis glycosyltransferase, regulates flowering time via FLOWERING LOCUS C. New Phytologist 194: 666-675

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


http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wang&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Wildermuth MC%2C Dewdney J%2C Wu G%2C Ausubel FM %282001%29 Isochorismate synthase is required to synthesize salicylic acid for plant defence%2E Nature 414%3A 562%2D565&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414: 562-565

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

http://scholar.google.com/scholar?as_q=Isochorismate synthase is required to synthesize salicylic acid for plant defence&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Isochorismate synthase is required to synthesize salicylic acid for plant defence&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wildermuth&as_ylo=2001&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Yalpani N%2C Le�n J%2C Lawton MA%2C Raskin I %281993%29 Pathway of salicylic acid biosynthesis in healthy and virus%2Dinoculated tobacco%2E Plant physiology 103%3A 315%2D321&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yalpani N, Le�n J, Lawton MA, Raskin I (1993) Pathway of salicylic acid biosynthesis in healthy and virus-inoculated tobacco. Plant physiology 103: 315-321

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

http://scholar.google.com/scholar?as_q=Pathway of salicylic acid biosynthesis in healthy and virus-inoculated tobacco&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Pathway of salicylic acid biosynthesis in healthy and virus-inoculated tobacco&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yalpani&as_ylo=1993&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Yang L%2C Li B%2C Zheng X%2Dy%2C Li J%2C Yang M%2C Dong X%2C He G%2C An C%2C Deng XW %282015%29 Salicylic acid biosynthesis is enhanced and contributes to increased biotrophic pathogen resistance in Arabidopsis hybrids%2E Nature communications 6%3A 7309&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yang L, Li B, Zheng X-y, Li J, Yang M, Dong X, He G, An C, Deng XW (2015) Salicylic acid biosynthesis is enhanced and contributes to increased biotrophic pathogen resistance in Arabidopsis hybrids. Nature communications 6: 7309

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http://scholar.google.com/scholar?as_q=Salicylic acid biosynthesis is enhanced and contributes to increased biotrophic pathogen resistance in Arabidopsis hybrids.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yang&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Yang S%2C Hua J %282004%29 A haplotype%2Dspecific Resistance gene regulated by BONZAI1 mediates temperature%2Ddependent growth control in Arabidopsis%2E The Plant Cell 16%3A 1060%2D1071&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yang S, Hua J (2004) A haplotype-specific Resistance gene regulated by BONZAI1 mediates temperature-dependent growth control in Arabidopsis. The Plant Cell 16: 1060-1071

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

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http://scholar.google.com/scholar?as_q=A haplotype-specific Resistance gene regulated by BONZAI1 mediates temperature-dependent growth control in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yang&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Yoshioka K%2C Kachroo P%2C Tsui F%2C Sharma SB%2C Shah J%2C Klessig DF %282001%29 Environmentally sensitive%2C SA%2Ddependent defense responses in the cpr22 mutant of Arabidopsis%2E The Plant Journal 26%3A 447%2D459&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yoshioka K, Kachroo P, Tsui F, Sharma SB, Shah J, Klessig DF (2001) Environmentally sensitive, SA-dependent defense responses in the cpr22 mutant of Arabidopsis. The Plant Journal 26: 447-459

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http://www.ncbi.nlm.nih.gov/pubmed?term=Zhang GZ%2C Jin SH%2C Jiang XY%2C Dong RR%2C Li P%2C Li YJ%2C Hou BK %282016%29 Ectopic expression of UGT75D1%2C a glycosyltransferase preferring indole%2D3%2Dbutyric acid%2C modulates cotyledon development and stress tolerance in seed germination of Arabidopsis thaliana%2E Plant Mol Biol 90%3A 77%2D93&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhang GZ, Jin SH, Jiang XY, Dong RR, Li P, Li YJ, Hou BK (2016) Ectopic expression of UGT75D1, a glycosyltransferase preferring indole-3-butyric acid, modulates cotyledon development and stress tolerance in seed germination of Arabidopsis thaliana. Plant Mol Biol 90: 77-93

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http://www.ncbi.nlm.nih.gov/pubmed?term=Zhang K%2C Bhuiya M%2DW%2C Pazo JR%2C Miao Y%2C Kim H%2C Ralph J%2C Liu C%2DJ %282012%29 An engineered monolignol 4%2DO%2Dmethyltransferase depresses lignin biosynthesis and confers novel metabolic capability in Arabidopsis%2E The Plant Cell 24%3A 3135%2D3152&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhang K, Bhuiya M-W, Pazo JR, Miao Y, Kim H, Ralph J, Liu C-J (2012) An engineered monolignol 4-O-methyltransferase depresses lignin biosynthesis and confers novel metabolic capability in Arabidopsis. The Plant Cell 24: 3135-3152


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http://www.ncbi.nlm.nih.gov/pubmed?term=Zhang K%2C Halitschke R%2C Yin C%2C Liu CJ%2C Gan SS %282013%29 Salicylic acid 3%2Dhydroxylase regulates Arabidopsis leaf longevity by mediating salicylic acid catabolism%2E Proc Natl Acad Sci U S A 110%3A 14807%2D14812&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Zhang Y%2C Xu S%2C Ding P%2C Wang D%2C Cheng YT%2C He J%2C Gao M%2C Xu F%2C Li Y%2C Zhu Z %282010%29 Control of salicylic acid synthesis and systemic acquired resistance by two members of a plant%2Dspecific family of transcription factors%2E Proceedings of the National Academy of Sciences 107%3A 18220%2D18225&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhang Y, Xu S, Ding P, Wang D, Cheng YT, He J, Gao M, Xu F, Li Y, Zhu Z (2010) Control of salicylic acid synthesis and systemic acquired resistance by two members of a plant-specific family of transcription factors. Proceedings of the National Academy of Sciences 107: 18220-18225


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http://www.ncbi.nlm.nih.gov/pubmed?term=Zhang Y%2C Zhao L%2C Zhao J%2C Li Y%2C Wang J%2C Guo R%2C Gan S%2DS%2C Liu C%2DJ%2C Zhang K %282017%29 S5H%2FDMR6 Encodes a Salicylic Acid 5%2DHydroxylase That Fine%2DTunes Salicylic Acid Homeostasis%2E Plant physiology 175%3A 1082�??1093&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhang Y, Zhao L, Zhao J, Li Y, Wang J, Guo R, Gan S-S, Liu C-J, Zhang K (2017) S5H/DMR6 Encodes a Salicylic Acid 5-Hydroxylase That Fine-Tunes Salicylic Acid Homeostasis. Plant physiology 175: 1082?1093


http://scholar.google.com/scholar?as_q=S5H/DMR6 Encodes a Salicylic Acid 5-Hydroxylase That Fine-Tunes Salicylic Acid Homeostasis.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=Zhou F%2C Menke FL%2C Yoshioka K%2C Moder W%2C Shirano Y%2C Klessig DF %282004%29 High humidity suppresses ssi4%2Dmediated cell death and disease resistance upstream of MAP kinase activation%2C H2O2 production and defense gene expression%2E The Plant Journal 39%3A 920%2D932&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhou F, Menke FL, Yoshioka K, Moder W, Shirano Y, Klessig DF (2004) High humidity suppresses ssi4-mediated cell death and disease resistance upstream of MAP kinase activation, H2O2 production and defense gene expression. The Plant Journal 39: 920-932

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

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http://scholar.google.com/scholar?as_q=High humidity suppresses ssi4-mediated cell death and disease resistance upstream of MAP kinase activation, H2O2 production and defense gene expression&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhou&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1


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