bes/bzr transcription factor tabzr2 positively regulates … · 3 60 61 62 abstract 63 bri1-ems...

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BES/BZR Transcription Factor TaBZR2 Positively 1

Regulates Drought Responses by Activation of TaGST11 2

Xiao-Yu Cuia,d,2, Yuan Gaoa,2, Jun Guob, Tai-Fei Yua, Wei-Jun Zhengb, Yong-Wei Liuc, 3

Jun Chena, Zhao-Shi Xua,3 and You-Zhi Maa,3 4

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Running title: Functional analysis of TaBZR2 in wheat 6

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1 This research was financially supported by the National Key Research and 8

Development Program of China (2016YFD0100600), the National Transgenic Key 9

Project of the Ministry of Agriculture of China (2018ZX0800909B), the National 10

Natural Science Foundation of China (31871624), and the Technological Innovation 11

Projects of Modern Agriculture of Hebei Province. 12

2 These authors contributed equally to the article. 13

3 Address correspondence to [email protected] or [email protected]. 14

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The authors responsible for distribution of materials integral to the findings 16

presented in this article in accordance with the policy described in the instructions for 17

authors (www.plantphysiol.org) are: Zhao-Shi Xu ([email protected]) and You-Zhi 18

Ma ([email protected]). 19

Z.S.X. coordinated the project, conceived and designed experiments, and edited the 20

manuscript; X.Y.C. performed experiments and wrote the first draft of the manuscript; 21

Y.G. conducted the bioinformatic work and performed experiments; J.G., T.F.Y., 22

W.J.Z., and Y.W.L. generated and analyzed data; J.C. provided analytical tools and 23

managed reagents; Y.Z.M. coordinated the project. 24

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a Institute of Crop Science, Chinese Academy of Agricultural Sciences 26

(CAAS)/National Key Facility for Crop Gene Resources and Genetic Improvement, 27

Key Laboratory of Biology and Genetic Improvement of Triticeae Crops, Ministry of 28

Agriculture, Beijing 100081, China 29

Plant Physiology Preview. Published on March 6, 2019, as DOI:10.1104/pp.19.00100

Copyright 2019 by the American Society of Plant Biologists

www.plantphysiol.orgon February 19, 2020 - Published by Downloaded from Copyright © 2019 American Society of Plant Biologists. All rights reserved.

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b College of Plant Protection/College of Agronomy, Northwest A&F University, 30

Yangling, Shaanxi 712100, China 31

c Institute of Genetics and Physiology, Hebei Academy of Agriculture and Forestry 32

Sciences/Plant Genetic Engineering Center of Hebei Province, Shijiazhuang, Hebei 33

050051, China 34

d Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao, 35

266101, China. 36

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Corresponding author： 38

39

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Zhao-Shi Xu 41

Institute of Crop Science, Chinese Academy of Agricultural Sciences (CAAS)/National 42

Key Facility for Crop Gene Resources and Genetic Improvement, Key Laboratory of 43

Biology and Genetic Improvement of Triticeae Crops, Ministry of Agriculture, Beijing 44

100081, China 45

Telephone: +86-10-82106773 46

E-mail: [email protected] 47

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You-Zhi Ma 49

Institute of Crop Science, Chinese Academy of Agricultural Sciences (CAAS)/National 50

Key Facility for Crop Gene Resources and Genetic Improvement, Key Laboratory of 51

Biology and Genetic Improvement of Triticeae Crops, Ministry of Agriculture, Beijing 52

100081, China 53

Telephone: +86-10-82109718 54

E-mail: [email protected] 55

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One-sentence summary: A BES/BZR-type transcription factor, TaBZR2, activates 57

TaGST1 to scavenge reactive oxygen species and mediates crosstalk between 58

brassinosteroids and drought signaling pathways. 59



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ABSTRACT 62

BRI1-EMS suppressor (BES)/brassinazole-resistant (BZR) family transcription 63

factors are involved in a variety of physiological processes, but the biological 64

functions of some BES/BZR transcription factors remain unknown; moreover, it is not 65

clear if any of these proteins function in the regulation of plant stress responses. Here, 66

TaBZR2-overexpressing plants exhibited drought tolerant phenotypes, whereas 67

down-regulation of TaBZR2 in wheat (Triticum aestivum) by RNA interference 68

resulted in elevated drought sensitivity. Electrophoretic mobility shift assay and 69

luciferase reporter analysis illustrate that TaBZR2 directly interacts with the gene 70

promoter to activate the expression of TaGST1, which functions positively in 71

scavenging drought-induced superoxide anions (O2-). Moreover, TaBZR2 acts as a 72

positive regulator in brassinosteroid (BR) signaling. Exogenous BR treatment 73

enhanced TaBZR2-mediated O2- scavenging and anti-oxidant enzyme gene expression. 74

Taken together, we demonstrate that a BES/BZR family transcription factor, TaBZR2, 75

functions positively in drought responses by activating TaGST1 and mediates the 76

crosstalk between BR and drought signaling pathways. Our results thus provide new 77

insights into the mechanisms underlying how BES/BZR family transcription factors 78

contribute to drought tolerance in wheat. 79

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INTRODUCTION 81

As sessile organisms, plants encounter various environmental stresses, such as 82

drought and salt stresses, that severely affect growth and productivity (Jeong et al., 83

2010; Takasaki et al., 2010; Yu et al., 2013; Zhang et al., 2017; Qi et al., 2018). Plants 84

have developed elaborate mechanisms to cope with such challenges via changes at the 85

physiological and biochemical levels as well as at the cellular and molecular levels 86

(Yamaguchi-Shinozaki and Shinozaki, 2006; Zhang et al., 2012; Yu et al., 2013; Liu et 87

al., 2018; Qi et al., 2018). These adaptive strategies are highly sophisticated processes 88



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regulated by an intricate signaling network and by orchestrating expression of 89

stress-responsive genes (Ramegowda et al., 2015; Liu et al., 2018; Wu et al., 2018). 90

Stress-responsive genes can be classified into two groups: effector genes and 91

regulatory genes (Huang et al., 2013; Liu et al., 2014; Kidokoro et al., 2015). 92

Effector genes encode enzymes required for osmoprotectants, late embryogenesis 93

abundant (LEA) proteins, aquaporin proteins, chaperones, and detoxification enzymes, 94

which protect cell membrane integrity, control ion balances, and scavenge reactive 95

oxygen species (ROS) (Huang et al., 2013; Liu et al., 2014). Regulatory genes encode 96

protein kinases and transcription factors, which function in signal perception, signal 97

transduction, and transcriptional regulation of gene expression (Huang et al., 2013; 98

Liu et al., 2014). Transcription factors, such as the dehydration responsive 99

element-binding (DREB)/C-repeat binding factor (CBF) family (Liu et al., 2013; 100

Kidokoro et al., 2015; Liu et al., 2018), APETALA2 (AP2)/ethylene responsive factor 101

(ERF) family (Seo et al., 2010; Rong et al., 2014), myeloblastosis (MYB) family (Li 102

et al., 2009; Seo et al., 2009; Seo et al., 2011), NAM, ATAF, and CUC (NAC) family 103

(Hao et al., 2011; Mao et al., 2015; Wang et al., 2018), WRKY family (Zhou et al., 104

2008; Wang et al., 2015), and basic leucine zipper (bZIP) family (Tang et al., 2012; 105

Song et al., 2013; Ma et al., 2018), can bind to cis-regulatory elements to modulate 106

the expression of various downstream genes, ultimately regulating adaptive responses 107

to unfavorable environmental conditions. 108

BRI1-EMS suppressor (BES)/brassinazole-resistant (BZR) transcription factors 109

form a small plant-specific gene family (Wang et al., 2002; Yin et al., 2005; Bai et al., 110

2007). Members of the BES/BZR family of transcription factors, which function 111

redundantly in BR response, are key components of the BR signaling pathway (Wang 112

et al., 2002; Yin et al., 2002; Yin et al., 2005; Li et al., 2010). BES1 and BZR1 are two 113

well-known BES/BZR family members that function as positive regulators in 114

Arabidopsis (Arabidopsis thaliana) BR signaling. Gain-of-function mutants bes1-D 115

and bzr1-1D can partially suppress the dwarf phenotypes of brassinosteroid 116

insensitive1 (bri1) and are resistant to the BR biosynthesis inhibitor brassinazole 117

(BRZ) (Wang et al., 2002; Yin et al., 2002). OsBZR1 functions as a positive regulator 118



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in the rice (Oryza sativa) BR signaling pathway, and 14-3-3 proteins inhibit OsBZR1 119

nuclear accumulation to negatively regulate BR signaling (Bai et al., 2007). 120

GmBEHL1 mediates the crosstalk between BR signaling and nodulation signaling 121

pathways that negatively regulates symbiotic nodulation in soybean (Glycine max) 122

(Yan et al., 2018). 123

In addition to their essential roles in BR signaling, BES/BZR family members 124

have been shown to function in Arabidopsis responses to drought and to stress from 125

both high and low temperatures (Oh et al., 2012; Li et al., 2017; Ye et al., 2017). The 126

drought-induced transcription factor RD26 mediates crosstalk between BR and 127

drought pathways via reciprocal inhibition between RD26 and BES1 transcriptional 128

activities (Ye et al., 2017). BZR1-PIF4 interaction integrates BR signaling and 129

environmental signals (Oh et al., 2012). BZR1 positively regulates Arabidopsis 130

freezing tolerance via DREB/CBF-dependent and DREB/CBF-independent pathways 131

(Li et al., 2017). 132

Bread wheat (Triticum aestivum L.) is a cereal crop that is widely grown throughout 133

the world. Drought profoundly affects wheat growth and productivity worldwide. 134

Although a few BES/BZR family members have been characterized in model plants, 135

the biological functions of wheat BES/BZR family transcription factors remain 136

largely unknown. In the present study, both drought and exogenous BR treatments 137

induced expression of a BES/BZR family transcription factor gene, TaBZR2. We then 138

analyzed the function of TaBZR2 through generating overexpression and RNA 139

interference (RNAi) transgenic wheat plants. Moreover, electrophoretic mobility shift 140

assay (EMSA) and luciferase reporter analysis illustrated that TaBZR2 functions 141

positively in drought tolerance by directly up-regulating the transcriptional activity of 142

wheat glutathione S-transferase 1 (TaGST1). Furthermore, TaBZR2 acts as a link 143

between BR and drought signaling pathways. 144

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RESULTS 147

Identification of Stress-Responsive BES/BZR Transcription Factors in Wheat 148

In previous whole-transcriptome analyses of drought and BR on wheat, the transcript 149

of TraesCS3D02G139300.1 was induced by both drought and exogenous BR 150

treatments and exhibited the greatest stress-inducible gene response (Supplemental 151

Table S1). Sequence alignment analysis revealed that this transcript encodes a protein 152

that shows high sequence similarity with rice BES/BZR transcription factor OsBZR2 153

(~ 87%) (https://blast.ncbi.nlm.nih.gov/Blast.cgi). We thus named this transcript 154

TaBZR2 and selected it for further analysis of its role in drought responses. 155

Protein structure analysis illustrated that the TaBZR2 amino acid sequence 156

contained an N-terminal DNA binding domain and 29 putative GSK3-like kinase 157

phosphorylation sites (S/TXXXS/T) but no putative PEST domain (a region rich in 158

proline, glutamate, serine, and threonine) 159

(http://emboss.bioinformatics.nl/cgi-bin/emboss/epestfind) or potential 14-3-3 binding 160

site (RXXXpSXP, where X is any amino acid, R is arginine, pS is phosphoserine, and P 161

is proline) was identified (Rechsteiner and Rogers, 1996; Wang et al., 2002; Yin et al., 162

2002; Bai et al., 2007) (Supplemental Fig. S1A). To explore the relationships among 163

wheat BZRs and their orthologs from other plant species, a phylogenetic tree was 164

constructed by amino acid sequence alignment. TaBZR2 was classified into subgroup 165

V, and the BES/BZRs derived from monocots clustered separately from those of 166

dicots, suggesting a potential functional diversity between dicot and monocot plants 167

(Supplemental Fig. S1B). 168

169

Drought and Exogenous BR Induced TaBZR2 Expression and the Nuclear 170

Accumulation of TaBZR2 Protein 171

We confirmed the expression patterns of TaBZR2 in drought and BR responses by 172

reverse transcription quantitative PCR (RT-qPCR) and immunoblot assays. Drought 173

induced TaBZR2 expression in both shoots and roots , reaching a peak at 2 h (Fig. 1, A 174

and B). TaBZR2 expression increased after treatment with exogenous BR and peaked 175



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at 4 h in BR-treated leaves and roots (Fig. 1, A and B). Furthermore, drought and 176

exogenous BR treatments increased the abundance of TaBZR2 protein (Fig. 1, C and 177

D). To better understand the biological functions of TaBZR2, we investigated the 178

subcellular localization of TaBZR2 protein in response to drought and exogenous BR 179

treatments. The TaBZR2-GFP fluorescence signal was observed in both the cytoplasm 180

and nucleus under unstressed conditions (Fig. 1E). Upon drought and exogenous BR 181

treatments, TaBZR2 proteins translocated from the cytoplasm to the nucleus as shown 182

by the nuclear/cytoplasmic signal ratio (Fig. 1E). 183

184

Overexpression of TaBZR2 Significantly Improves Drought Tolerance in 185

Transgenic Wheat 186

To investigate the drought tolerance associated with TaBZR2, we generated 187

transgenic bread wheat plants on the Fielder background in which TaBZR2, driven by 188

the maize (Zea mays) Ubiquitin promoter, was overexpressed. Three independent 189

transgenic lines that exhibited high TaBZR2 expression level based on RT-qPCR 190



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assays were chosen for further analysis (Fig. 2B). No differences were observed 191

between the TaBZR2-overexpressing (OE5, OE9, and OE11) and wild-type (WT) 192

plants under normal growth conditions (Fig. 2A). Drought treatment caused obvious 193

differences in growth and physiology of both TaBZR2-overexpressing and WT plants. 194

Upon drought treatment, compared with control plants, TaBZR2-overexpressing plants 195

had significantly delayed leaf rolling and higher survival rates (Fig. 2, A and C). 196

Moreover, the proline contents were significantly higher in TaBZR2-overexpressing 197

plants than in WT plants under drought conditions (Fig. 2D). The 198

TaBZR2-overexpressing plants had significantly lower electrolyte leakage levels and 199

malondialdehyde (MDA) contents compared to WT plants under drought conditions 200

(Fig. 2, E and F). Thus, TaBZR2 regulated physiological processes that improve the 201

drought tolerance of transgenic wheat plants. 202

203

Suppression of TaBZR2 Enhances Drought Sensitivity in Wheat 204

To further explore the function of TaBZR2 in drought responses, we produced two 205

independent TaBZR2-RNAi lines (Ri3 and Ri7) and determined the expression of 206

TaBZR2 using RT-qPCR assays. The expression levelof TaBZR2 decreased in the two 207



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lines (Fig. 3B and Supplemental Fig. S2), implying that TaBZR2 was successfully 208

suppressed. There were no obvious differences in the growth performance and 209

physiology between TaBZR2-RNAi and WT plants under normal growth conditions 210

(Fig. 3A). However, upon drought treatment, the survival rates were significantly 211

lower in TaBZR2-RNAi plants than in WT plants under drought conditions (Fig. 3C). 212

Moreover, drought-treated TaBZR2-RNAi lines had significantly lower proline 213

contents, higher electrolyte leakage levels, and higher MDA contents compared to WT 214

plants under drought conditions (Fig. 3, D–F). 215

216

TaBZR2 Positively Regulates the Expression of Multiple Stress-Related Genes 217

To explore how TaBZR2 contributes to drought tolerance, we performed RNA-Seq 218

assays to evaluate the differential gene expression between TaBZR2-overexpressing 219

and WT wheat plants under both normal and drought conditions. As shown in Figure 220

4A, using a threshold of a 2-fold change and a Student's t-test significance cut-off of P 221

<0.05, a comparison of the RNA-Seq data from TaBZR2-overexpressing and WT 222

plants under normal conditions identified 1,399 up-regulated and 1,064 223

down-regulated genes in TaBZR2-overexpressing plants (TaBZR2-OEN) compared 224

with those in WT plants (WTN). Upon drought treatment, the expression of 728 and 225

1,496 genes in the TaBZR2-overexpressing plants (TaBZR2-OED) was up- or 226



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down-regulated, respectively, compared with that in WT plants (WTD). In total, 227

20,224 differentially expressed genes (DEGs) were identified between drought-treated 228

and normal growth WT plants (WTD/WTN). Cluster and Venn diagram analyses 229

revealed that the expression patterns of all DEGs in TaBZR2-OED compared with that 230

in WTD (TaBZR2-OED/WTD) did not significantly overlap with TaBZR2-OEN 231

compared with WTN (TaBZR2-OEN/WTN), or WTD compared with WTN 232

(WTD/WTN). These results demonstrated that TaBZR2 significantly affects the 233

global gene expression profile in wheat, indicating that unknown mechanisms may 234

underlie the drought tolerance of transgenic wheat. 235

Gene Ontology (GO) analysis revealed that the DEGs between the drought-treated 236

TaBZR2-overexpressing and WT plants were significantly enriched in biological 237

process categories including "response to abiotic stimulus", "response to water stress", 238

and "regulation of metabolic and biosynthetic processes" (Fig. 4B). Interestingly, we 239

found that the expression of a range of well-known stress-related genes were among 240

the up-regulated DEGs for the drought-treated TaBZR2-overexpressing plants 241

(Supplemental Table S2). Note that we also used RT-qPCR assays to successfully 242

verify the up-regulated expression trends for the genes identified from the RNA-Seq 243



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data, including TaGST1, TaLEA3, TaDHN3, TaP5CS, TaPOD21, and TaSAPK3 (Fig. 244

4C). Consistent with a direct functional impact of TaBZR2 on the expression of these 245

known stress-related genes, we also used RT-qPCR to examine the expression of 246

these genes in the aforementioned drought-treated TaBZR2-RNAi plants and found 247

that their expression was significantly reduced compared to both drought-treated 248

TaBZR2-RNAi and WT plants (Fig. 4C). GST genes, encoding ROS-scavenging 249

enzymes, function in protecting plants against oxidative damage under stress 250

conditions (Jha et al., 2011; Rong et al., 2014). P5CS is the key enzyme for proline 251

synthesis (Yoshiba et al., 1995; Zhuo et al., 2017). Dehydrins are responsive to 252

various environmental stresses and exhibit multiple biochemical activities, such as 253

buffering water, sequestering ions, stabilizing membranes, or acting as chaperones 254

(Kovacs et al., 2008; Tang et al., 2012; Rong et al., 2014; Zhuo et al., 2017). Sucrose 255

non-fermenting-1-related protein kinase 2 (SnRK2) is implicated in stress signaling 256

transduction via abscisic acid (ABA)-dependent and -independent pathways (Yoshida 257

et al., 2002; Zhang et al., 2011), TaBZR2 could modulate the expression of numerous 258

stress-responsive genes under drought conditions, contributing to the drought 259

tolerance of the transgenic wheat. 260

261

TaBZR2 Functions Positively in Scavenging Drought-Induced Superoxide Anions 262

(O2-) 263

Environmental stimuli, including drought, salt, and high and low temperatures, 264

induce the accumulation of toxic ROS, including H2O2 and O2-, which if not 265

controlled, can eventually lead to oxidative damage (Dat et al., 2000; Wang et al., 266

2017). TaBZR2 has a role in activating antioxidant enzyme gene expression. To 267

investigate whether TaBZR2 participates in scavenging ROS, we analyzed the ROS 268

contents between TaBZR2-RNAi and WT wheat lines under normal and drought 269

conditions. There was no significant difference in H2O2 accumulation between 270

TaBZR2-RNAi and WT wheat lines under unstressed and drought conditions 271

(Supplemental Fig. S3). The O2- contents of TaBZR2-RNAi and WT wheat lines were 272

similar under unstressed conditions (Fig. 5, A and B). Nevertheless, the O2- contents 273



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were significantly higher in the TaBZR2-RNAi plants than in the WT plants under 274

drought conditions (Fig. 5, A and B). DMTU acts as a O2- scavenging reagent (Lv et 275

al., 2018). When DMTU was added to the growth medium to reduce O2-, the O2- 276

contents of TaBZR2-RNAi wheat lines recovered to a level similar to that of the WT 277

plants (Fig. 5, A and B). 278

To investigate whether the TaBZR2-mediated O2- scavenging was associated with 279

the positive role of TaBZR2 in drought responses, we compared the biomass of 280

TaBZR2-RNAi wheat plants with that of the WT wheat plants grown on 1/2-strength 281

Hoagland’s nutrient solution supplemented with different concentrations of PEG 6000 282

and DMTU (0, 15% PEG 6000, 1 mM DMTU, and 15% PEG 6000 + 1 mM DMTU). 283

Biomass was similar for the WT and TaBZR2-RNAi plants grown on 1/2-strength 284

Hoagland’s nutrient solution containing 0 and 1 mM DMTU (Fig. 5, C and D). 285

However, biomass was significantly larger in the WT plants than in the 286

TaBZR2-RNAi plants under drought conditions (Fig. 5, C and D). DMTU treatment 287



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can partially suppress drought (15% PEG 6000)-induced biomass reduction. 288

Importantly, the biomass of TaBZR2-RNAi plants was comparable with that of the 289

WT plants grown on 1/2-strength Hoagland’s nutrient solution containing 15% PEG 290

6000 and 1 mM DMTU (Fig. 5, C and D). These results indicate that TaBZR2 has a 291

role in scavenging O2- to alleviate drought stress. 292

293

TaBZR2 Functions as a Positive Regulator of TaGST1 Expression by Binding to 294

Its Promoter and Activating Transcription 295

RNA-Seq and RT-qPCR analyses both indicated that the expression of TaGST1 is 296

up-regulated by TaBZR2 overexpression, so the transcription of this gene may be 297

activated by TaBZR2. Previous studies have revealed that BES/BZR family 298

transcription factors can bind to E-box (5’-CANNTG-3’) cis-elements to regulate the 299

expression of target genes; we detected ten E-box cis-elements in the TaGST1 300

promoter. We thus used EMSAs to investigate whether TaBZR2 can directly bind to 301

the TaGST1 promoter in vitro. The EMSAs showed that the TaBZR2-GST fusion 302

protein was able to bind to the TaGST1 promoter; no such binding was observed for 303

the control GST protein (Fig. 6, A and B). Further, the observed binding to the 304

biotin-labeled target sequences was dramatically reduced when unlabeled competitor 305

target DNA sequences were added, and no binding was detected when adding the 306

mutated biotin-labeled TaGST1 probes (Fig. 6, A and B). Having determined that 307

TaBZR2 can bind the TaGST1 promoter in vitro, we next used a wheat protoplast 308

transient expression system to assess whether this binding can drive TaGST1 gene 309

expression in vivo. A pGreen II 0800 vector harboring a LUC reporter gene driven by 310

the TaGST1 promoter (~2000-bp) was co-transformed into wheat protoplasts 311

transfected with an empty pJIT16318 vector or a pJIT16318-TaBZR2 vector. 312

Compared with the empty-vector control samples, the protoplasts expressing TaBZR2 313

exhibited significantly increased expression of the reporter (Fig. 6C). To further test if 314

the activation effect of TaBZR2 on the TaGST1 was through binding to the E-box 315

(CACGTG, -1475 to -1481), the TaGST1 promoter containing the mutated E-box was 316

inserted into the pGreen II 0800 vector and coexpressed with the pJIT16318-TaBZR2 317



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vector in wheat protoplasts. The results demonstrated that the E-box mutation 318

(AAAAAA, -1475 to -1481) disrupted TaBZR2-mediated activation of the TaGST1 319

promoter (Fig. 6C), indicating that the TaBZR2 transcription factor is a positive 320

regulator of TaGST1 expression. 321

322

Overexpression of TaGST1 Significantly Improved Drought Tolerance in 323

Transgenic Wheat by Reducing O2- Contents 324

To investigate the function of TaGST1 in the drought response, we generated 325

transgenic wheat plants that overexpressed TaGST1 under the control of the maize 326

Ubiquitin promoter. Three independent homozygous T3 transgenic lines with 327

relatively high expression of TaGST1 were selected for additional phenotypic analyses 328

(Fig. 7E). Under normal growth conditions, there were no notable differences in plant 329

growth or physiology between TaGST1-overexpressing (OE1, OE4, and OE9) and 330

WT plants. However, upon drought treatment, the survival rate of 331

TaGST1-overexpressing plants was significantly higher than that of WT plants (Fig. 7, 332

A and B). Moreover, the drought-treated TaGST1-overexpressing plants had 333

significantly lower O2- content compared to WT plants (Fig. 7, C and D). 334

335

TaBZR2 is a Positive Regulator in the BR Signaling Pathway 336

To obtain more detailed evidence for the role of TaBZR2 in BR responses, we 337



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transformed the BR-insensitive mutant bri1-5 with a TaBZR2 overexpression 338

construct under the control of the CaMV 35S promoter. Two independent homozygous 339

T3 transgenic lines (35S:TaBZR2/bri1-5-B3 and -B7) that strongly expressed TaBZR2 340

were selected for further phenotypic analysis. Overexpression of TaBZR2 partially 341

suppressed the dwarf phenotypes of bri1-5 mutant plants (Supplemental Fig. S4, A 342

and B). Compared with bri1-5 mutant plants, 35S:TaBZR2/bri1-5 transgenic plants 343

had enhanced tolerance to the BR biosynthetic inhibitor BRZ (Supplemental Fig. 344

S4B). In addition, compared with bri1-5 mutant plants, 35S:TaBZR2/bri1-5 transgenic 345

plants showed reduced expression of the BR biosynthesis genes CPD and DWF4 and 346

increased expression of the BR signaling gene SAUR-AC (Supplemental Fig. S4C). 347

To obtain further insights into the role of TaBZR2 in the wheat BR signaling 348

pathway, we investigated the BR sensitivity of TaBZR2 transgenic wheat plants. 349

TaBZR2-overexpressing and TaBZR2-RNAi wheat plants exhibited altered BR 350

sensitivity as indicated by their root length in the absence or presence of BR. In the 351

absence of BR, there was no significant difference in root lengths between 352

TaBZR2-overexpressing, TaBZR2-RNAi, and WT wheat plants (Fig. 8A). However, in 353

the presence of BR, the root lengths of TaBZR2-overexpressing lines were shorter than 354

that of WT plants. Moreover, compared with WT plants, TaBZR2-RNAi plants 355

exhibited BR-insensitive phenotypes with longer roots (Fig. 8A). Previous studies 356

have shown that BES/BZR family transcription factors can bind to the BR-response 357



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element (BRRE) in the promoters of feedback-regulated BR biosynthetic genes to 358

repress their expression (He et al., 2005). EMSAs demonstrated that TaBZR2 can bind 359

to the BRRE cis-regulatory elements in the promoter of the BR biosynthentic gene 360

TaD2 (Fig. 8B). Furthermore, RT-qPCR assays revealed that, compared with WT 361

plants, TaBZR2-overexpressing plants showed reduced expression of the BR 362

biosynthetic genes TaD2 and TaDWARF, whereas TaBZR2-RNAi plants showed 363

enhanced expression of the BR biosynthetic genes TaD2 and TaDWARF in the 364

absence and presence of BR (Fig. 8C). The TaBZR2-modulated inhibition of TaD2 365

and TaDWARF expressions were larger in the presence of BR than in the absence of 366

BR (Fig. 8C). Our data suggest that TaBZR2 functions as a positive regulator in BR 367

signaling. 368

369

TaBZR2 is Involved in BR-mediated Drought Responses 370

To investigate whether TaBZR2 has a role in BR-mediated drought responses, we 371

investigated the expression of stress responsive genes encoding antioxidant enzymes, 372

including TaGST1, TaPOD21, and TaDHN3, in response to BR treatment by RT-qPCR 373

analyses. Upon exogenous BR treatment, the expression of these genes in 374

TaBZR2-overexpression plants was enhanced compared to WT plants, whereas their 375

expression in TaBZR2-RNAi plants was reduced under normal and drought conditions 376

(Fig. 9A). In addition, drought and BR treatments enhanced the abundance of 377

dephosphorylated TaBZR2 proteins in the TaBZR2-overexpressing, TaBZR2-RNAi, 378

and WT plants (Fig. 9B). The amounts of dephosphorylated TaBZR2 proteins were 379



17

larger in TaBZR2-overexpression plants than in WT plants. Nevertheless, compared to 380

WT plants, the amount of dephosphorylated TaBZR2 proteins in TaBZR2-RNAi plants 381

was smaller upon drought and BR treatments (Fig. 9B). The phosphorylation status of 382

the BES/BZR family transcription factors is usually used as the biochemical maker 383

for BR signaling outputs (Zhang et al., 2009). Treatment of immunoprecipitated 384

protein with protein phosphatase eliminated the slowly migrating band (Supplemental 385

Fig. S5), strongly suggesting that the fast band is unphosphorylated and the slow band 386

is phosphorylated TaBZR2. In addition, the O2- accumulation of 387

TaBZR2-overexpressing, TaBZR2-RNAi, and WT plants was similar under normal 388

conditions. When exposed to induced drought conditions, O2- accumulation increased 389

in the roots of TaBZR2-overexpressing, TaBZR2-RNAi, and WT plants. The O2- 390

contents of TaBZR2-overexpressing plants under drought conditions was significantly 391

lower than that of WT plants, whereas the O2- accumulation was significantly higher in 392

TaBZR2-RNAi plants than in WT plants (Fig. 9, C and D). Exogenous BR treatment 393

repressed the O2- accumulation in wheat plants under normal and drought conditions. 394

Compared to WT plants, the BR-mediated O2- scavenging was enhanced in 395

TaBZR2-overexpressing plants, whereas BR-mediated O2- scavenging was reduced in 396

TaBZR2-RNAi plants under drought conditions (Fig. 9, C and D). These results 397

indicated that TaBZR2 participates in BR-mediated O2- scavenging. 398



18

399

400



19

DISCUSSION 401

Plant genomes have many kinds of transcription factors that function importantly in 402

plant adaption to extreme environmental conditions (Zhang et al., 2017; Liu et al., 403

2018; Ma et al., 2018). BES/BZR proteins constitute another important family of 404

plant-specific transcription factors (Wang et al., 2002; Yin et al., 2002; Yin et al., 405

2005), but comparatively little is known about their biological functions in drought 406

responses. In the present study, a drought-inducible BES/BZR-type transcription 407

factor gene TaBZR2 was identified from wheat drought transcriptome data, and 408

follow-up work illustrated that overexpression of TaBZR2 enhanced drought tolerance 409

in transgenic wheat plants with larger accumulation of osmoprotectant metabolites, 410

higher membrane stability, and lower ROS contents compared with the control plants 411

under drought conditions, whereas TaBZR2-RNAi wheat lines exhibited the opposite 412

trend. These results suggest that TaBZR2 functions positively in regulating drought 413

responses in wheat. 414

BES/BZR family members regulate the expression of target genes by interacting 415

with BRRE and/or or E-box cis-elements in their promoters (Goda et al., 2004; 416

Nemhauser et al., 2004; He et al., 2005; Wang et al., 2006; Walcher and Nemhauser, 417

2012; Li et al., 2017). For example, BZR1 binds to BRRE and/or E-box elements in 418

the promoters of the genes encoding CBF1/DREB1A, CBF2/DREB1B, and WRKY6 419

to modulate their expression, contributing to freezing tolerance in Arabidopsis (Li et 420

al., 2017), and BES1 directly binds to the E-box element of the SAUR-AC15 promoter 421

to enhance auxin signaling in Arabidopsis (Goda et al., 2004; Walcher and Nemhauser, 422

2012). Our EMSA and luciferase reporter analyses demonstrated that TaBZR2 directly 423

binds to the promoter of TaGST1 to activate its transcription. GST genes encode 424

detoxification enzymes that function in maintaining cell redox homeostasis and 425

protecting organisms against oxidative stress under stress conditions (Jha et al., 2011; 426

Rong et al., 2014; Qi et al., 2018). Our data illustrated that, compared with the WT 427

plants, the TaGST1-overexpressing wheat lines exhibited drought tolerance 428

phenotypes with lower O2- contents under drought conditions, which was consistent 429



20

with the positive role of TaBZR2 in scavenging drought-induced O2-. These results 430

indicate that TaBZR2 has a role in activating TaGST1 for scavenging O2-, and 431

consequently alleviate drought stress. 432

Genetic and molecular studies have greatly increased our understanding of the BR 433

signaling pathway in model plants (Bai et al., 2007; Yu et al., 2008; Ye et al., 2011; 434

Chen et al., 2017). BRs are perceived by a leucine-rich repeat (LRR)-receptor kinase, 435

BRI1, and transduces the signal to activate the BES/BZR family transcription factor, 436

which regulates the expression of a large number of genes (Wang et al., 2002; Yin et 437

al., 2002; Yin et al., 2005; Bai et al., 2007; Oh et al., 2012; Jiang et al., 2013; Shimada 438

et al., 2015; Yan et al., 2018). Consistent with the positive role of BES/BZR family 439

members in the BR signaling pathway (Wang et al., 2002; Yin et al., 2002; Yan et al., 440

2018), TaBZR2 positively regulates BR signaling in wheat. Exogenous application of 441

BR protects plants from drought stress (Kagale et al., 2007; Xia et al., 2009; Divi et 442

al., 2010, 2016; Nawaz et al., 2017). Previous studies have shown that some 443

components of the BR signaling pathway are involved in drought responses (Koh et 444

al., 2007; Sahni et al., 2016). Overexpression of the Arabidopsis BR biosynthetic gene 445

DWARF4 confers drought tolerance in Brassica napus (Sahni et al., 2016). OsGSK1 is 446

a negative regulator of rice BR signaling: its T-DNA knockout mutants display 447

enhanced tolerance to drought and other abiotic stresses (Koh et al., 2007). 448

Considering that TaBZR2 functions as a positive regulator in drought responses, it is 449

possible that TaBZR2 has a role in mediating the crosstalk between BR and drought 450

responses. A recent study has shown that BR is involved in regulation of the 451

accumulation of O2- (Lv et al., 2018). For example, the BR-deficient mutant det2-9 452

accumulates more O2- in roots (Lv et al., 2018). Our data demonstrated that the 453

expression of some TaBZR2 target genes encoding antioxidant enzymes, including 454

TaGST1, TaPOD21, and TaDHN3, was up-regulated upon exogenous BR treatment. 455

Furthermore, exogenous application of BR can enhance TaBZR2-mediated activation 456

of antioxidant enzymes and scavenging of O2- under drought conditions. Our data 457

indicated that TaBZR2 participates in BR-mediated drought response partially by 458

reducing the accumulation of O2-. 459



21

It is worth noting that recent studies also illustrated several components of the BR 460

signaling pathway negatively regulate drought responses (Chen et al., 2017; Ye et al., 461

2017). For example, in contrast to a positive role of TaBZR2 in drought responses, 462

AtBES1 negatively regulates plant drought tolerance (Ye et al., 2017). BES/BZR 463

family transcription factor genes derived from monocots clustered separately from 464

those of dicots by phylogenetic analysis. Protein structure analyses illustrated that the 465

amino acid sequence of TaBZR2 has an N-terminal binding domain and GSK3-like 466

kinase phosphorylation sites, but no 14-3-3 binding domain and PEST motif were 467

identified, which was different from the well-known BES/BZR family members like 468

AtBES1, AtBZR1, and OsBZR1 (Wang et al., 2002; Yin et al., 2002; Bai et al., 2007). 469

Furthermore, TaBZR2 exhibited a different BR regulated mobility shift pattern with 470

AtBZR1 and AtBES1. Previously, studies revealed that all of phosphorylated AtBZR1 471

and AtBES1 were dephosphorylated upon BR treatment (He et al., 2002; Yin et al., 472

2002), whereas BR treatment caused partially phosphorylated TaBZR2 to convert to 473

the dephosphorylated form. These results indicate that although BES/BZR family 474

members function positively in BR signaling, protein structural differences and the 475

different mechanisms of action may lead to functional differences in environmental 476

stress responses. Our study expands the known functional scope of the BES/BZR 477

family members, and its basic insights should inform the work of both plant abiotic 478

stress researchers and wheat breeders and biotechnologists. 479

480

MATERIALS AND METHODS 481

Plant Materials and Growth Conditions 482

Wheat (Triticum aestivum) plants used for molecular analysis were grown in a 483

greenhouse at 70% relative humidity, 25/23°C day/night temperatures, and long-day 484

conditions (16 h light/8 h dark photoperiod) with a light intensity of approximately 485

300 μmol m-2 s-1. The wheat cultivar KeNong 199 was used to amplify cDNA 486

sequences of TaBZR2 and TaGST1. The wheat cultivar Fielder was used as the 487

receptor material to generate transgenic plants. To analyze the expression of TaBZR2 488



22

under abiotic stress conditions, wheat cultivar KeNong 199 seedlings were grown in 489

1/2-strength Hoagland’s liquid medium in a greenhouse with 70% relative humidity, 490

25/23°C day/night temperatures, long-day conditions (16 h light/8 h dark photoperiod), 491

with a light intensity of approximately 400 μmol m-2 s-1 for 2 weeks. For BR and 492

drought stress treatments, the roots of wheat seedlings were immersed in 1/2-strength 493

Hoagland’s solution containing 1 μM EBL solution (Sigma-Aldrich, USA) and 15% 494

(w/v) PEG 6000. Leaves and roots were sampled at 0, 1, 2, 4, 8, 12, and 24 h, and then 495

immediately frozen in liquid nitrogen and stored at -80°C prior to RNA extraction. The 496

Arabidopsis (Arabidopsis thaliana) plants were subsequently grown in a greenhouse 497

at 23°C under long-day conditions (16 h light/8 h dark photoperiod) and a light 498

intensity of approximately 100 μmol m-2 s-1. For Arabidopsis, the seeds were 499

germinated on 1/2-strength Murashige and Skoog (MS) (Caisson Labs, USA) media 500

supplemented with 2% (w/v) sucrose and grown for a week, after which the seedlings 501

were transplanted into soil. The plants were subsequently grown in a greenhouse with 502

70% relative humidity, 23°C, and long-day conditions (16 h light/8 h dark 503

photoperiod) with a light intensity of approximately 100 μmol m-2 s-1 for 3 weeks. The 504

Arabidopsis BR-insensitive mutant bri1-5 was used for transformation. 505

506

Generation of Transgenic Arabidopsis and Wheat 507

To generate TaBZR2 transgenic wheat plants, the coding region( CDS) of TaBZR2D 508

were cloned into the plant transformation vector pWMB110 driven by the maize (Zea 509

mays) Ubiquitin promoter. The 198-bp TaBZR2 specific fragment was synthesized by 510

Beijing AuGCT Company, which was then fused in both sense and antisense 511

orientations to flank the 508-bp rice (Oryza sativa) zinc finger type family protein gene 512

intron 6. This recombinant DNA was then inserted into the pWMB110 vector to 513

generate the pWMB110-TaBZR2-RNAi construct. To generate TaGST1-overexpression 514

wheat plants, the TaGST1 CDS were also inserted into the pMWB110 vector, driven by 515

the maize Ubiquitin promoter. Genetic transformations were performed using an 516

Agrobacterium tumefaciens-mediated transformation system. To isolate positive 517

transgenic wheat lines, leaves of 10-day-old transgenic wheat seedlings grown in 518



23

1/2-strength Hoagland’s nutrient solution were used for RNA isolation, and then RT- 519

and RT-qPCR analyzes were performed. For Arabidopsis, the CDS of TaBZR2 was 520

introduced into the plant transformation vector pBI121 under the control of the CaMV 521

35S promoter. The resultant constructs were confirmed by sequencing and then 522

transformed into BR-insensitive mutant bri1-5 plants via the vacuum infiltration 523

method (Bechtold and Pelletier, 1998). Homozygous T3 seeds of the transgenic lines 524

were used for phenotypic analyses. Primers used in these studies are in Supplemental 525

Table S3. 526

527

Drought Stress Treatment 528

For drought tolerance assays, TaBZR2 transgenic and WT wheat seedlings were 529

planted in pots containing mixed soil (1:1 vermiculite:humus) and cultured normally in 530

the greenhouse for 3 weeks (until seedlings were at the 3-leaf stage), after which these 531

seedlings were deprived of water until significant differences in wilting were observed 532

between transgenic and WT wheat plants. Three independent experiments were 533

performed. TaGST1 transgenic and WT wheat seedlings were planted in pots 534

containing mixed soil (1:1 vermiculite:humus) and cultured normally in the greenhouse 535

for 3 weeks (until seedlings were at the 3-leaf stage), after which 15% (w/v) PEG 6000 536

solution was applied to the bottom of the plates for ~14 days until significant 537

differences in wilting were observed between transgenic and WT wheat plants. Three 538

independent experiments were performed. 539

540

BR Sensitivity Assays 541

For BR sensitivity assays, sterilized seeds of TaBZR2-overexpressing, 542

TaBZR2-RNAi, and WT wheat plants were maintained at 4°C for 1 week, after which 543

the germinated seeds were transplanted into 1/2-strength Hoagland’s solution 544

containing different concentrations of EBL (0, 0.25, and 1 μM). After 7 days of growth 545

at 23°C under long-day conditions (16-h light/8-h dark photoperiod), images were 546

taken, and the primary root length for each seedling was evaluated using an Epson 547



24

Expression 11000XL root system scanning analyzer (Epson, Japan). For hypocotyl 548

elongation assays, the sterilized seeds of WT plants, 35S:TaBZR2/bri1-5 transgenic 549

Arabidopsis plants, and bri1-5 plants were sown on 1/2-strength MS growth media 550

supplemented with various concentrations (0, 0.25, and 0.5 μM) of BRZ and then kept 551

at 4°C in the dark for 3 days. After 7 days of growth at 22°C under dark conditions, 552

images were taken, and the lengths of hypocotyls were measured. 553

554

RNA Extraction and RT-qPCR Assays 555

The total RNA from Arabidopsis and wheat seedlings was extracted using Trizol 556

reagent (TaKaRa, Japan), and their DNA was digested using RNase-free DNaseI 557

(TaKaRa, Japan). First-strand cDNA was synthesized using a PrimeScript First-Strand 558

cDNA Synthesis Kit (TaKaRa, Japan). RT-qPCR was performed with an ABI 7500 559

real-time PCR system (ThermoFisher Scientific, USA) in conjunction with SYBR to 560

monitor double-stranded DNA products. The reaction was conducted at 95°C for 5 561

min, then 42 cycles of 95°C for 15 s, 58°C to 60°C for 25 s, and 72°C for 30 s. A 562

quantitative analysis using the 2-ΔΔCT method was subsequently performed (Le et al., 563

2011). Each experiment was performed with at least three independent biological 564

replicates. For each primer pair, the amplification efficiency was checked using a 565

melting-curve analysis. For wheat, β-actin was used as the internal control and actin 566

was used an internal control for Arabidopsis (Liu et al., 2013). The specific primers 567

used for RT-qPCR are listed in Supplemental Table S3. 568

569

Immunoblot Assay 570

Wheat cultivar KeNong 199 seedlings were grown in 1/2-strength Hoagland’s liquid 571

medium in a greenhouse with 70% relative humidity, 25/23°C day/night temperatures, 572

and long-day conditions (16 h light/8 h dark photoperiod) with a light intensity of 573

approximately 400 μmol m-2 s-1 for 2 weeks. For BR and drought stress treatments, the 574

roots of wheat seedlings were immersed in 1/2-strength Hoagland’s solution containing 575

1 μM EBL solution and 15% (w/v) PEG 6000. Leaves were sampled at 0, 2, 4, 8, and 576

12 h and then used to extract total protein. Plant protein was isolated with lysis buffer 577



25

(50 m M Tris [pH 7.5], 1 mM EDTA, 150 mM NaCl, 10 m M MgCl2, 10% [v/v] 578

glycerol, 1 mM PMSF, 5 mM DTT, protease inhibitor cocktail Complete Minitablets 579

[Roche], and 0.2% [v/v] Nonidet P-40). For phosphatase treatment, the extracted plant 580

proteins were treated with the Lambda protein phosphatase (NEB, P0753S, USA) 581

according to the manufacturer’s instructions. The dephosphorylation reaction took 582

place at 30°C for 30 min in a thermal cycler (Bio-Rad, USA). TaBZR2 proteins were 583

subsequently detected by immunoblotting using Anti-TaBZR2 antibodies at a 1:1000 584

dilution. IRDye 800CW anti-rabbit IG (H + L) at a 1:10000 dilution (LI-COR, USA) 585

was used as a second antibody. The immunoblots were developed via an Odyssey 586

CLx Infrared Imaging System (LI-COR, USA). 587

588

Subcellular Localization 589

Transient expression assays were conducted as described previously (Liu et al., 590

2013). TaBZR2 was inserted into the subcellular localization vector pJIT16318, which 591

contains a CaMV 35S promoter and a C-terminal GFP. Approximately 4 × 104 592

mesophyll protoplasts were isolated from 10-day-old wheat seedlings and then 593

transfected with pJIT16318-TaBZR2 plasmids by PEG-mediated transformation. The 594

transfected protoplasts were then incubated at 23°C for 12 h. GFP fluorescence in the 595

transformed protoplasts was imaged using a confocal laser-scanning microscope (LSM 596

700, Germany). 597

598

Measurements of Proline Content, Electrolyte Leakage Level, and MDA Content 599

For assays of physiological traits, 3-week-old wheat seedlings at the 3 leaf stage 600

were treated with drought conditions for ~ 12 d. About 0.2 g of wheat leaf leaves were 601

harvested for measurements of physiological parameters. Absorbance values were 602

measured with a Varioskan LUX Multimode Microplate Reader (ThermoFisher 603

Scientific, USA). The proline concentration was determined as described previously 604

(Zhang et al., 2012). The electrolyte leakage was examined in accordance with 605

previously described methods (Cao et al., 2007), and the MDA content was assayed as 606

described previously (Zhang et al., 2012). All of the measurements were repeated three 607



26

times. 608

609

Measurements of O2- Content and H2O2 Content 610

To investigate the contents of O2- and H2O2, 2-week-old wheat seedlings grown on 611

1/2-strength Hoagland’s nutrient solution supplemented with different concentrations 612

of PEG 6000 and BR (0, 15% (w/v) PEG 6000, 10 nM BR, 15% (w/v) PEG 6000 + 613

10 nM BR, 1 mM DMTU, and 15% (w/v) PEG 6000 + 1 mM DMTU) for 72 h. The 614

O2- contents were measured following the protocol of the Superoxide anion content 615

detection kit (Solarbio, USA, BC1295). The H2O2 contents were measured following 616

the protocol of the H2O2 content detection kit (Solarbio, BC3595, USA). For 617

Nitro-blue tetrazolium (NBT) staining, the wheat roots were immersed in NBT stain 618

solution for 30 min and the dark blue color appeared following the protocol of the 619

Alkaline Phosphatase Activity Detection Kit (Amersco, USA). The staining reaction 620

was stopped by the addition of an excess of 95% ethanol. Images were observed and 621

photographed under a stereomicroscope (Leica, Germany). 622

623

RNA-Seq Assays 624

TaBZR2-overexpressing (OE9) and WT (Fielder) plants were grown in 1/2-strength 625

Hoagland’s liquid medium in a greenhouse with 70% relative humidity, 25/23°C 626

day/night temperatures, and long-day conditions (16 h light/8 h dark photoperiod) with 627

a light intensity of approximately 400 μmol m-2 s-1 for 2 weeks. Then, the wheat 628

seedlings were transferred to fresh 1/2-strength Hoagland’s solution that contained 15% 629

(w/v) PEG 6000. Leaves were sampled at 0 and 6 h for transcriptome sequencing 630

experiments, and three biological replicates were used. The RNA-Seq analysis was 631

performed by the Allwegene Company (Beijing). Total RNA was extracted from the 632

samples using TRIzol reagent (Invitrogen, USA) according to the manufacturer’s 633

instructions, and RNA sequencing was conducted on an Illumina HiSeq platform. 634

RNA sequencing data were analyzed as previously described (Mortazavi et al., 2008). 635

DEGs were selected using DESeq (1.10.1) with a relative change threshold of 2-fold 636

(P < 0.05, false discovery rate < 0.01) (Anders and Huber, 2010). GO categories were 637



27

identifined using the GOseq R package (Young et al., 2010). The genome annotation 638

and functional categorization are based on the National Center for Biotechnology 639

Information non-redundant protein sequences 640

(https://ftp.ncbi.nlm.nih.gov/blast/db/FASTA/). 641

642

EMSA Assay 643

The CDS of TaBZR2 was inserted into the pGEX-4T-1 vector. The GST and GST- 644

TaBZR2 fusion proteins were expressed in Escherichia coli (BL21) and purified by 645

glutathione-Sepharose TM 4B (GE Healthcare, Sweden) according to the 646

manufacturer’s protocol. The biotin-labeled probes used in this assay were 647

synthesized (AuGCT, china), and the sequences are listed in Supplemental Table S3. 648

Double-stranded DNA was obtained by heating oligonucleotides at 95 °C for 10 min 649

and annealing at room temperature. The EMSA assay was performed using the 650

LightShift Chemiluminescent EMSA Kit (Thermo, USA) according to the 651

manufacturer’s instructions. In brief, 2 mg of purified fusion protein GST-TaBZR2 or 652

GST protein was added to the binding reaction. The binding reaction took place at 653

25°C for 30 min in a thermal cycler (Bio-Rad, USA). The mixture was separated on a 654

6% polyacrylamide mini gel, and then the DNA was transferred to nylon membrane 655

(Millipore, USA). The signal was visualized with an EasySee Western Blot Kit 656

(TransGen, china). 657

658

Transcriptional Activation Assays in Wheat Protoplasts 659

For the transcriptional activation assay, the promoter fragment of TaGST1 was 660

inserted into LUC reporter plasmid pGreen II 0800, which contained a Renilla 661

luciferase (REN) gene under the control of the CaMV 35S promoter used as an 662

internal control. The effector plasmids and the reporter plasmids were co-transformed 663

into protoplasts by PEG-mediated transformation. After culturing for 16 h at 23°C, the 664

activities of LUC and REN were separately determined using a Dual-Luciferase 665

Reporter Assay System (Promega, E1910, USA). 666

667



28

Antibody Preparation 668

Anti-TaBZR2 was generated by Wuhan Abclonal Biotechnology Cooperation. 669

TaBZR2 CDs (453–999 bp) were inserted into the pET32a vector. Purified 670

His-TaBZR2 (151–333 amino acids) fusion protein was injected into rabbits to 671

produce TaBZR2 polyclonal antibodies. Immunoblots were performed using 672

antiserum against TaBZR2 and visualized with an EasySee Western Blot Kit 673

(TransGen). 674

675

Accession Numbers 676

RNA sequencing data described in this study can be found in the National Center 677

for Biotechnology Information Sequence Read Archive 678

(http://www.ncbi.nlm.nih.gov/sra) under accession number SRP071191. 679

680

Supplemental Data 681

The following supplemental materials are available. 682

Supplemental Figure S1. Sequence and phylogenetic analyses of TaBZR2. 683

684

Supplemental Figure S2. The expression level of BES/BZR family transcription 685

factor genes in TaBZR2-RNAi and WT wheat plants. 686

687

Supplemental Figure S3. Measurements of H2O2 contents in TaBZR2-overexpressing, 688

TaBZR2-RNAi, and WT wheat plants under normal and drought conditions. 689

690

Supplemental Figure S4. TaBZR2 overexpression partially rescued the dwarf 691

phenotypes of bri1-5 plants. 692

693

Supplemental Figure S5. Immunoblot analysis of TaBZR2 protein. 694

695

Supplemental Table S1. Wheat BZRs responsive to drought and BR treatments. 696



29

697

Supplemental Table S2. Analysis of stress-related genes in 698

TaBZR2-overexpressing and WT wheat plants under drought conditions. 699

700

Supplemental Table S3. Primers and probes used in this study. 701

702

ACKNOWLEDGEMENTS 703

We are grateful to Drs. Rui-Lian Jing and Yong-Fu Fu (Institute of Crop Science, 704

Chinese Academy of Agricultural Sciences) for providing wheat seeds and for the 705

BiFC system, respectively. We also thank Dr. Dongying Gao (Department of Plant 706

Sciences, University of Georgia, USA) for suggestions on the manuscript. 707

708



30

FIGURE LEGENDS 709

Figure 1 Expression and localization of TaBZR2 in wheat under BR and drought 710

conditions. (A) and (B) The expression profile of TaBZR2 in 2-week-old wheat 711

seedling leaf and root tissue under drought and BR treatments for the indicated time. 712

Transcript levels were quantified by RT-qPCR assays. The expression of β-actin was 713

analyzed as internal control. Each data point is the mean (± SE) of three experiments. 714

(C) and (D) Protein level of TaBZR2 in 2-week-old wheat seedlings after drought and 715

BR treatments for the indicated time. Total proteins were extracted and subjected to 716

immunoblot analysis with anti-TaBZR2 antibodies. Rubisco was used as a loading 717

control. (E) Localization of TaBZR2 protein under drought and BR conditions. The 718

nuclear/cytoplasmic signal ratio represents nuclear-accumulated TaBZR2 versus 719

cytoplasmic-accumulated TaBZR2. Images were observed under a laser scanning 720

confocal microscope. Scale bar = 12 μm. Each data point is the mean (± SE) of ten 721

biological replicates (**P < 0.01; Student’s t-test). 722

723

Figure 2 TaBZR2-overexpressing wheat plants exhibit improved drought tolerance. 724

(A) Phenotypes of TaBZR2-overexpressing (OE5, OE9, and OE11) and wild-type 725

(WT) wheat plants under well-watered and drought conditions. (B) RT-qPCR analysis 726

of TaBZR2 gene expression in TaBZR2-overexpressing and WT plants. The expression 727

of β-actin was analyzed as an internal control. Each data point is the mean (± SE) of 728

three experiments. (C) Survival rate of the control and water-stressed plants (without 729

irrigation for 21 d). (D) Proline content in seedlings under normal and drought 730

conditions. (E) Electrolyte leakage in seedlings under normal and drought conditions. 731

(F) MDA content in seedlings under normal and drought conditions. Each data point 732

is the mean (± SE) of three experiments (10 seedlings per experiment). The asterisks 733

indicate significant differences between TaBZR2-overexpressing and WT wheat plants 734

(Student’s t-test, *P < 0.05 and **P < 0.01). 735

736

Figure 3 TaBZR2-RNAi wheat plants show enhanced drought sensitivity. (A) 737



31

Phenotypes of TaBZR2-RNAi (Ri3 and Ri7) and WT wheat plants under well-watered 738

and drought conditions. (B) RT-qPCR analysis of TaBZR2 gene expression in 739

TaBZR2-RNAi and WT plants. The expression of β-actin was analyzed as an internal 740

control. Each data point is the mean (± SE) of three experiments. (C) Survival rate of 741

the control and water-stressed plants (without irrigation for 18 d). (D) Proline content 742

in seedlings under normal and drought conditions. (E) Electrolyte leakage in seedlings 743

under normal and drought conditions. (F) MDA content in seedlings under normal and 744

drought conditions. Each data point is the mean (± SE) of three experiments (10 745

seedlings per experiment). The asterisks indicate significant differences between 746

TaBZR2-RNAi and WT wheat plants (Student’s t-test, *P < 0.05 and **P < 0.01). 747

748

Figure 4 Analysis of the expression levels of TaBZR2 downstream genes. (A) Venn 749

diagrams comparing the up- and down-regulated genes between WT plants under 750

normal and drought conditions (WTN and WTD), and TaBZR2-overexpressing and 751

WT plants under normal (TaBZR2-OEN/WTN) and drought conditions 752

(TaBZR2-OED/WTD). (B) Functional categorization analysis of candidate TaBZR2 753

target genes in biological process under drought conditions. (C) The expression levels 754

of drought-responsive genes in TaBZR2-overexpressing, TaBZR2-RNAi, and WT 755

wheat plants. Two-week-old wheat seedlings treated with 15% PEG 6000 for 6 h were 756

used for RNA isolation. Transcript levels were quantified by RT-qPCR assays, and the 757

expression of β-actin was used as an internal control. Each data point is the mean (± 758

SE) of three experiments (10 seedlings per experiment). 759

760

Figure 5 TaBZR2 functions positively in savenging drought-induced O2-. (A) NBT 761

staining in primary root tips of TaBZR2-RNAi and WT wheat plants grown in 762

1/2-strength Hoagland’s liquid medium, medium containing 15% PEG 6000, medium 763

containing 1 mM DMTU, or medium containing 15% PEG 6000 + 1 mM DMTU for 72 764

h. The strength of color shows the concentration of O2- in the root tips. Scale bar = 1 765

mm (B) Measurements of the O2- contents of TaBZR2-RNAi and WT wheat plants 766

grown in 1/2-strength Hoagland’s liquid medium, medium containing 15% PEG 6000, 767



32

medium containing 1 mM DMTU, or medium containing 15% PEG 6000 + 1 mM 768

DMTU for 72 h. Each data point is the mean (± SE) of six biological replicates. The 769

asterisks indicate significant differences between TaBZR2-RNAi and WT wheat plants 770

(Student’s t-test, **P < 0.01) (C) Phentypes of TaBZR2-RNAi and WT wheat plants 771

grown in 1/2-strength Hoagland’s liquid medium, medium containing 15% PEG 6000, 772

medium containing 1 mM DMTU, or medium containing 15% PEG 6000 + 1 mM 773

DMTU. Scale bar = 2 cm. (D) Measurement of the total fresh weight of TaBZR2-RNAi 774

and WT wheat plants grown in 1/2-strength Hoagland’s liquid medium, medium 775

containing 15% PEG 6000, medium containing 1 mM DMTU, or medium containing 776

15% PEG 6000 + 1 mM DMTU. Each data point is the mean (± SE) of six biological 777

replicates. The asterisks indicate significant differences between TaBZR2-RNAi and 778

WT wheat plants (Student’s t-test, *P < 0.05). 779

780

Figure 6 TaBZR2 directly regulates the expression of TaGST1. (A) The diagram 781

shows the structure of the TaGST1 promoter. The sequences represent TaGST1 probe 782

sequences. The underlined sequences indicated the core elements or mutated core 783

elements in the TaGST1 probe. (B) EMSA assay of TaBZR2 binding to the promoter 784

of TaGST1. Biotin-labeled TaGST1 probes (normal and mutated) were incubated with 785

GST or GST-TaBZR2 protein. 100× competitor fragments were added to analyze the 786

specificity of binding. (C) TaBZR2 increases TaGST1 promoter activity in wheat 787

protoplasts. TaBZR2 was co-transfected with either TaGST1 promoter or mutated 788

TaGST1 promoter. The LUC to REN ratio is shown and indicates the activity of the 789

transcription factors on the expression level of the promoters. Each data point is the 790

mean (± SE) of ten biological replicates (**P < 0.01; Student’s t-test). 791

792

Figure 7 TaGST1 overexpression promotes drought tolerance in transgenic wheat. (A) 793

Phenotypes of TaGST1-overexpressing and WT plants under normal and drought 794

conditions. (B) Survival rate of control and water-stressed plants (15% PEG 6000 795

treatment for 14 d). Each data point is the mean (± SE) of three experiments (10 796

seedlings per experiment). (C) NBT staining in primary root tip of 797



33

TaGST1-overexpressing and WT seedlings with 0 or 15% PEG 6000 treatment for 72 798

h. The strength of color shows the concentration of O2- in the root tips. Scale bar =1 799

mm (D) Measurements of the O2- contents of TaGST1-overexpressing and WT plants 800

under normal and drought conditions. Each data point is the mean (± SE) of six 801

biological replicates. (E) RT-qPCR analysis of TaGST1 gene expression in 802

TaGST1-overexpressing and WT wheat seedlings. The expression of β-actin was used 803

as an internal control. Each data point is the mean (± SE) of three experiments (10 804

seedlings per experiment). The asterisks indicate significant differences between 805

TaGST1-overexpressing and WT plants (Student’s t-test, **P < 0.01). 806

807

Figure 8 TaBZR2 is a positive regulator in the BR signaling pathway. (A) Phenotypes 808

of TaBZR2-overexpressing (OE5, OE9, and OE11), TaBZR2-RNAi (Ri3 and Ri7), and 809

WT wheat plants grown in 1/2-strength Hoagland’s liquid medium or medium 810

containing 1 μM BR. Bar = 2 cm. Root length of TaBZR2-overexpressing, 811

TaBZR2-RNAi, and WT wheat plants grown on 1/2-strength Hoagland’s medium that 812

contained different concentrations of BR (0, 0.25, or 1 μM) in the light for 7 d. Each 813

data point is the mean (± SE) of three experiments (20 seedlings per experiment). The 814

asterisks indicate significant differences between TaBZR2 transgenic 815

(TaBZR2-overexpressing lines and TaBZR2-RNAi lines) and WT plants (Student’s 816

t-test, *P < 0.05). (B) EMSA assay of TaBZR2 binding to the BR-response elements 817

(BRRE) in the promoter of TaD2. Biotin-labeled BRRE probes (normal and mutated) 818

were incubated with GST or GST-TaBZR2 protein. 100× competitor fragments were 819

added to analyze the specificity of binding. (C) The expression levels of BR 820

biosynthetic genes in TaBZR2 transgenic (TaBZR2-overexpressing lines and 821

TaBZR2-RNAi lines) and WT plants. The expression of β-actin was used as an internal 822

control. Each data point is the mean (± SE) of three experiments (10 seedlings per 823

experiment). 824

825

Figure 9 TaBZR2 regulates wheat drought tolerance through the BR-dependent 826

pathway. (A) The expression levels of stress-responsive genes in TaBZR2 transgenic 827



34

(TaBZR2-overexpressing lines and TaBZR2-RNAi lines) and WT plants grown in 828

1/2-strength Hoagland’s liquid medium, medium containing 15% PEG 6000, medium 829

containing 10 nM BR, or medium containing 15% PEG 6000 + 10 nM BR for 6 h. Each 830

data point is the mean (± SE) of three experiments (10 seedlings per experiment). (B) 831

Protein level of TaBZR2 in TaBZR2-overexpressing, TaBZR2-RNAi, and WT wheat 832

plants upon drought and BR treatments for 6 h. Total proteins were extracted and 833

subjected to immunoblot analysis with anti-TaBZR2 antibodies. Rubisco was used as 834

a loading control. (C) NBT staining in primary root tip of TaBZR2-overexpressing, 835

TaBZR2-RNAi, and WT wheat plants grown in 1/2-strength Hoagland’s liquid 836

medium, medium containing 15% PEG 6000, medium containing 10 nM BR, or 837

medium containing 15% PEG 6000 + 10 nM BR for 72 h. The strength of color shows 838

the concentration of O2- in the root tips. Scale bar = 1 mm (D) Measurements of the 839

O2- contents of TaBZR2-overexpressing, TaBZR2-RNAi, and WT wheat plants grown 840

in 1/2-strength Hoagland’s liquid medium, medium containing 15% PEG 6000, 841

medium containing 10 nM BR, or medium containing 15% PEG 6000 + 10 nM BR for 842

72 h. Each data point is the mean (± SE) of six biological replicates. The asterisks 843

indicate significant differences between TaBZR2 transgenic (TaBZR2-overexpressing 844

lines and TaBZR2-RNAi lines) and WT plants (Student’s t-test, **P <0.01). 845

846

847



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Jeong JS, Kim YS, Baek KH, Jung H, Ha SH, Do Choi Y, Kim M, Reuzeau C, Kim JK (2010) Root-specific expression of OsNAC10improves drought tolerance and grain yield in rice under field drought conditions. Plant Physiol 153: 185–197


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https://scholar.google.com/scholar?as_q=T-DNA tagged knockout mutation of rice OsGSK1, an orthologue of Arabidopsis BIN2, with enhanced tolerance to various abiotic stresses.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Koh&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

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https://scholar.google.com/scholar?as_q=Genome-wide expression profiling of soybean two-component system genes in soybean root and shoot tissues under dehydration stress.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Le&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

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https://scholar.google.com/scholar?as_q=BZR1 positively regulates freezing tolerance via CBF-dependent and CBF-independent pathways in Arabidopsis.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Li&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

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https://scholar.google.com/scholar?as_q=Arabidopsis IWS1 interacts with transcription factor BES1 and is involved in plant steroid hormone brassinosteroid regulated gene expression.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Li&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

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https://scholar.google.com/scholar?as_q=Arabidopsis MYB30 is a direct target of BES1 and cooperates with BES1 to regulate brassinosteroid-induced gene expression.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Li&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

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https://scholar.google.com/scholar?as_q=Genome-wide analysis of ZmDREB genes and their association with natural variation in drought tolerance at seedling stage of Zea mays L.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Liu&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

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https://www.ncbi.nlm.nih.gov/pubmed?term=Ma H%2C Liu C%2C Li Z%2C Ran Q%2C Xie G%2C Wang B%2C Fang S%2C Chu J%2C Zhang J %282018%29 ZmbZIP4 contributes to stress resistance in maize by regulating ABA synthesis and root development%2E Plant Physiol 178%3A 753%26%23x&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Mortazavi A%2C Williams BA%2C McCue K%2C Schaeffer L%2C Wold B %282008%29 Mapping and quantifying mammalian transcriptomes by RNA%2DSeq%2E Nat Methods 5%3A 621%26%23x&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Nawaz F%2C Naeem M%2C Zulfiqar B%2C Akram A%2C Ashraf MY%2C Raheel M%2C Shabbir RN%2C Hussain RA%2C Anwar I%2C Aurangzaib M %282017%29 Understanding brassinosteroid%2Dregulated mechanisms to improve stress tolerance in plants%3A a critical review%2E Environ Sci Pollut Res Int 24%3A 15959%26%23x&dopt=abstract

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https://scholar.google.com/scholar?as_q=Understanding brassinosteroid-regulated mechanisms to improve stress tolerance in plants: a critical review.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Nawaz&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

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https://scholar.google.com/scholar?as_q=Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Oh&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

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https://scholar.google.com/scholar?as_q=Regulation of grain yield in rice under well-watered and drought stress conditions by GUDK.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ramegowda&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Rechsteiner M%2C Rogers SW %281996%29 PEST sequences and regulation by proteolysis%2E Trends Biochem Sci 21%3A 267%26%23x&dopt=abstract

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https://scholar.google.com/scholar?as_q=PEST sequences and regulation by proteolysis.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Rechsteiner&as_ylo=1996&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Rong W%2C Qi L%2C Wang A%2C Ye X%2C Du L%2C Liang H%2C Xin Z%2C Zhang Z %282014%29 The ERF transcription factor TaERF3 promotes tolerance to salt and drought stresses in wheat%2E Plant Biotechnol J 12%3A 468%26%23x&dopt=abstract

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https://scholar.google.com/scholar?as_q=The ERF transcription factor TaERF3 promotes tolerance to salt and drought stresses in wheat.&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

https://scholar.google.com/scholar?as_q=The ERF transcription factor TaERF3 promotes tolerance to salt and drought stresses in wheat.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Rong&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Sahni S%2C Prasad BD%2C Liu Q%2C Grbic V%2C Sharpe A%2C Singh SP%2C Krishna P %282016%29 Overexpression of the brassinosteroid biosynthetic gene DWF4 in Brassica napus simultaneously increases seed yield and stress tolerance%2E Sci Rep%2DUK&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Seo PJ%2C Lee SB%2C Suh MC%2C Park MJ%2C Go YS%2C Park CM %282011%29 The MYB96 transcription factor regulates cuticular wax biosynthesis under drought conditions in Arabidopsis%2E Plant Cell 23%3A 1138%26%23x&dopt=abstract

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https://scholar.google.com/scholar?as_q=The MYB96 transcription factor regulates cuticular wax biosynthesis under drought conditions in Arabidopsis.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=The MYB96 transcription factor regulates cuticular wax biosynthesis under drought conditions in Arabidopsis.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Seo&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Seo PJ%2C Xiang FN%2C Qiao M%2C Park JY%2C Lee YN%2C Kim SG%2C Lee YH%2C Park WJ%2C Park CM %282009%29 The MYB96 transcription factor mediates abscisic acid signaling during drought stress response in Arabidopsis%2E Plant Physiol 151%3A 275%26%23x&dopt=abstract


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https://www.ncbi.nlm.nih.gov/pubmed?term=Seo YJ%2C Park JB%2C Cho YJ%2C Jung C%2C Seo HS%2C Park SK%2C Nahm BH%2C Song JT %282010%29 Overexpression of the ethylene%2Dresponsive factor gene BrERF4 from Brassica rapa increases tolerance to salt and drought in Arabidopsis plants%2E Mol Cells 30%3A 271%26%23x&dopt=abstract


https://scholar.google.com/scholar?as_q=Overexpression of the ethylene-responsive factor gene BrERF4 from Brassica rapa increases tolerance to salt and drought in Arabidopsis plants.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Overexpression of the ethylene-responsive factor gene BrERF4 from Brassica rapa increases tolerance to salt and drought in Arabidopsis plants.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Seo&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Shimada S%2C Komatsu T%2C Yamagami A%2C Nakazawa M%2C Matsui M%2C Kawaide H%2C Natsume M%2C Osada H%2C Asami T%2C Nakano T %282015%29 Formation and dissociation of the BSS1 protein complex regulates plant development via brassinosteroid signaling%2E Plant Cell 27%3A 375%26%23x&dopt=abstract

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https://scholar.google.com/scholar?as_q=Formation and dissociation of the BSS1 protein complex regulates plant development via brassinosteroid signaling.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Shimada&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1



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Tang N, Zhang H, Li X, Xiao J, Xiong L (2012) Constitutive activation of transcription factor OsbZIP46 improves drought tolerance inrice. Plant Physiol 158: 1755–1768


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Wu Q, Wang M, Shen J, Chen D, Zheng Y, Zhang W (2018) ZmOST1 mediates abscisic acid regulation of guard cell ion channels anddrought stress responses. J Integr Plant Biol


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https://www.ncbi.nlm.nih.gov/pubmed?term=Song QX%2C Li QT%2C Liu YF%2C Zhang FX%2C Ma B%2C Zhang WK%2C Man WQ%2C Du WG%2C Wang GD%2C Chen SY%2C Zhang JS %282013%29 Soybean GmbZIP123 gene enhances lipid content in the seeds of transgenic Arabidopsis plants%2E J Exp Bot 64%3A 4329%26%23x&dopt=abstract

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https://scholar.google.com/scholar?as_q=Soybean GmbZIP123 gene enhances lipid content in the seeds of transgenic Arabidopsis plants.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

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https://www.ncbi.nlm.nih.gov/pubmed?term=Takasaki H%2C Maruyama K%2C Kidokoro S%2C Ito Y%2C Fujita Y%2C Shinozaki K%2C Yamaguchi%2DShinozaki K%2C Nakashima K %282010%29 The abiotic stress%2Dresponsive NAC%2Dtype transcription factor OsNAC5 regulates stress%2Dinducible genes and stress tolerance in rice%2E Mol Genet Genomics 284%3A 173%26%23x&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Tang N%2C Zhang H%2C Li X%2C Xiao J%2C Xiong L %282012%29 Constitutive activation of transcription factor OsbZIP46 improves drought tolerance in rice%2E Plant Physiol 158%3A 1755%26%23x&dopt=abstract

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https://scholar.google.com/scholar?as_q=Constitutive activation of transcription factor OsbZIP46 improves drought tolerance in rice.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Tang&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Walcher CL%2C Nemhauser JL %282012%29 Bipartite promoter element required for auxin response%2E Plant Physiol 158%3A 273%26%23x&dopt=abstract

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

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https://scholar.google.com/scholar?as_q=Bipartite promoter element required for auxin response.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Walcher&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Wang B%2C Wei J%2C Song N%2C Wang N%2C Zhao J%2C Kang Z %282018%29 A novel wheat NAC transcription factor%2C TaNAC30%2C negatively regulates resistance of wheat to stripe rust%2E J Integr Plant Biol 60%3A 432%26%23x&dopt=abstract

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https://scholar.google.com/scholar?as_q=A novel wheat NAC transcription factor, TaNAC30, negatively regulates resistance of wheat to stripe rust.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wang&as_ylo=2018&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Wang F%2C Chen HW%2C Li QT%2C Wei W%2C Li W%2C Zhang WK%2C Ma B%2C Bi YD%2C Lai YC%2C Liu XL%2C Man WQ%2C Zhang JS%2C Chen SY %282015%29 GmWRKY27 interacts with GmMYB174 to reduce expression of GmNAC29 for stress tolerance in soybean plants%2E Plant J 83%3A 224%26%23x&dopt=abstract


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https://www.ncbi.nlm.nih.gov/pubmed?term=Wang N%2C Zhang W%2C Qin M%2C Li S%2C Qiao M%2C Liu Z%2C Xiang F %282017%29 Drought tolerance conferred in soybean %28Glycine max%2E L%29 by GmMYB84%2C a novel R2R3%2DMYB transcription factor%2E Plant Cell Physiol 58%3A 1764%26%23x&dopt=abstract


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https://www.ncbi.nlm.nih.gov/pubmed?term=Wang ZY%2C Nakano T%2C Gendron J%2C He J%2C Chen M%2C Vafeados D%2C Yang Y%2C Fujioka S%2C Yoshida S%2C Asami T%2C Chory J %282002%29 Nuclear%2Dlocalized BZR1 mediates brassinosteroid%2Dinduced growth and feedback suppression of brassinosteroid biosynthesis%2E Dev Cell 2%3A 505%26%23x&dopt=abstract


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https://www.ncbi.nlm.nih.gov/pubmed?term=Wang ZY%2C Wang QM%2C Chong K%2C Wang FR%2C Wang L%2C Bai MY%2C Jia CG %282006%29 The brassinosteroid signal transduction pathway%2E Cell Res 16%3A 427%26%23x&dopt=abstract


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https://www.ncbi.nlm.nih.gov/pubmed?term=Wu Q%2C Wang M%2C Shen J%2C Chen D%2C Zheng Y%2C Zhang W %282018%29 ZmOST1 mediates abscisic acid regulation of guard cell ion channels and drought stress responses%2E J Integr Plant Biol&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Xia XJ%2C Wang YJ%2C Zhou YH%2C Tao Y%2C Mao WH%2C Shi K%2C Asami T%2C Chen ZX%2C Yu JQ %282009%29 Reactive oxygen species are involved in brassinosteroid%2Dinduced stress tolerance in cucumber%2E Plant Physiol 150%3A 801%26%23x&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Yamaguchi%2DShinozaki K%2C Shinozaki K %282006%29 Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses%2E Annu Rev Plant Biol 57%3A 781%26%23x&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Yan QQ%2C Wang LX%2C Li X %282018%29 GmBEHL1%2C a BES1%2FBZR1 family protein%2C negatively regulates soybean nodulation%2E Sci Rep%2DUK&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Ye HX%2C Li L%2C Yin YH %282011%29 Recent advances in the regulation of brassinosteroid signaling and biosynthesis pathways%2E J Integr Plant Biol 53%3A 455%26%23x&dopt=abstract

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

https://scholar.google.com/scholar?as_q=Recent advances in the regulation of brassinosteroid signaling and biosynthesis pathways.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Recent advances in the regulation of brassinosteroid signaling and biosynthesis pathways.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ye&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Ye HX%2C Liu SZ%2C Tang BY%2C Chen JN%2C Xie ZL%2C Nolan TM%2C Jiang H%2C Guo HQ%2C Lin HY%2C Li L%2C Wang YQ%2C Tong HN%2C Zhang MC%2C Chu CC%2C Li ZH%2C Aluru M%2C Aluru S%2C Schnable PS%2C Yin YH %282017%29 RD26 mediates crosstalk between drought and brassinosteroid signalling pathways%2E Nat Commun&dopt=abstract

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

https://scholar.google.com/scholar?as_q=RD26 mediates crosstalk between drought and brassinosteroid signalling pathways.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=RD26 mediates crosstalk between drought and brassinosteroid signalling pathways.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ye&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1



Yin Y, Wang ZY, Mora-Garcia S, Li J, Yoshida S, Asami T, Chory J (2002) BES1 accumulates in the nucleus in response tobrassinosteroids to regulate gene expression and promote stem elongation. Cell 109: 181–191


Yoshiba Y, Kiyosue T, Katagiri T, Ueda H, Mizoguchi T, Yamaguchishinozaki K, Wada K, Harada Y, Shinozaki K (1995) Correlationbetween the induction of a gene for delta(1)-pyrroline-5-carboxylate synthetase and the accumulation of proline in Arabidopsis thalianaunder osmotic-stress. Plant J 7: 751–760


Yoshida R, Hobo T, Ichimura K, Mizoguchi T, Takahashi F, Aronso J, Ecker JR, Shinozaki K (2002) ABA-activated SnRK2 protein kinaseis required for dehydration stress signaling in Arabidopsis. Plant Cell Physiol 43: 1473–1483


Young MD, Wakefield MJ, Smyth GK, Oshlack A (2010) Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol11: R14


Yu L, Chen X, Wang Z, Wang S, Wang Y, Zhu Q, Li S, Xiang C (2013) Arabidopsis enhanced drought tolerance1/HOMEODOMAINGLABROUS11 confers drought tolerance in transgenic rice without yield penalty. Plant Physiol 162: 1378–1391


Yu X, Li L, Li L, Guo M, Chory J, Yin Y (2008) Modulation of brassinosteroid-regulated gene expression by Jumonji domain-containingproteins ELF6 and REF6 in Arabidopsis. Proc Natl Acad Sci USA 105: 7618–7623


Zhang H, Mao X, Jing R, Chang X, Xie H (2011) Characterization of a common wheat (Triticum aestivum L.) TaSnRK2.7 gene involved inabiotic stress responses. J Exp Bot 62: 975–988


Zhang L, Zhao G, Xia C, Jia J, Liu X, Kong X (2012) A wheat R2R3-MYB gene, TaMYB30-B, improves drought stress tolerance intransgenic Arabidopsis. J Exp Bot 63: 5873–5885


Zhang N, Yin Y, Liu X, Tong S, Xing J, Zhang Y, Pudake RN, Izquierdo EM, Peng H, Xin M, Hu Z, Ni Z, Sun Q, Yao Y (2017) The E3 ligaseTaSAP5 alters drought stress responses by promoting the degradation of DRIP proteins. Plant Physiol 175: 1878–1892


Zhang SS, Cai ZY, Wang XL (2009) The primary signaling outputs of brassinosteroids are regulated by abscisic acid signaling. Proc NatlAcad Sci USA 106: 4543–4548


Zhang ZY, Liu X, Wang XD, Zhou MP, Zhou XY, Ye XG, Wei XN (2012) An R2R3 MYB transcription factor in wheat, TaPIMP1, mediateshost resistance to Bipolaris sorokiniana and drought stresses through regulation of defense- and stress-related genes. New Phytol196: 1155-1170


Zhou QY, Tian AG, Zou HF, Xie ZM, Lei G, Huang J, Wang CM, Wang HW, Zhang JS, Chen SY (2008) Soybean WRKY-type transcriptionfactor genes, GmWRKY13, GmWRKY21, and GmWRKY54, confer differential tolerance to abiotic stresses in transgenic Arabidopsisplants. Plant Biotechnol J 6: 486–503


Zhuo C, Liang L, Zhao Y, Guo Z, Lu S (2017) A cold responsive ethylene responsive factor from Medicago falcata confers coldtolerance by up-regulation of polyamine turnover, antioxidant protection, and proline accumulation. Plant Cell Environ 41: 2021–2032.



https://www.ncbi.nlm.nih.gov/pubmed?term=Yin Y%2C Vafeados D%2C Tao Y%2C Yoshida S%2C Asami T%2C Chory J %282005%29 A new class of transcription factors mediates brassinosteroid%2Dregulated gene expression in Arabidopsis%2E Cell 120%3A 249%26%23x&dopt=abstract

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

https://scholar.google.com/scholar?as_q=A new class of transcription factors mediates brassinosteroid-regulated gene expression in Arabidopsis.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=A new class of transcription factors mediates brassinosteroid-regulated gene expression in Arabidopsis.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yin&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Yin Y%2C Wang ZY%2C Mora%2DGarcia S%2C Li J%2C Yoshida S%2C Asami T%2C Chory J %282002%29 BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation%2E Cell 109%3A 181%26%23x&dopt=abstract

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

https://scholar.google.com/scholar?as_q=BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation.&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

https://scholar.google.com/scholar?as_q=BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yin&as_ylo=2002&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Yoshiba Y%2C Kiyosue T%2C Katagiri T%2C Ueda H%2C Mizoguchi T%2C Yamaguchishinozaki K%2C Wada K%2C Harada Y%2C Shinozaki K %281995%29 Correlation between the induction of a gene for delta%281%29%2Dpyrroline%2D5%2Dcarboxylate synthetase and the accumulation of proline in Arabidopsis thaliana under osmotic%2Dstress%2E Plant J 7%3A 751%26%23x&dopt=abstract

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

https://scholar.google.com/scholar?as_q=Correlation between the induction of a gene for delta(1)-pyrroline-5-carboxylate synthetase and the accumulation of proline in Arabidopsis thaliana under osmotic-stress.&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

https://scholar.google.com/scholar?as_q=Correlation between the induction of a gene for delta(1)-pyrroline-5-carboxylate synthetase and the accumulation of proline in Arabidopsis thaliana under osmotic-stress.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yoshiba&as_ylo=1995&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Yoshida R%2C Hobo T%2C Ichimura K%2C Mizoguchi T%2C Takahashi F%2C Aronso J%2C Ecker JR%2C Shinozaki K %282002%29 ABA%2Dactivated SnRK2 protein kinase is required for dehydration stress signaling in Arabidopsis%2E Plant Cell Physiol 43%3A 1473%26%23x&dopt=abstract

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

https://scholar.google.com/scholar?as_q=ABA-activated SnRK2 protein kinase is required for dehydration stress signaling in Arabidopsis.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=ABA-activated SnRK2 protein kinase is required for dehydration stress signaling in Arabidopsis.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yoshida&as_ylo=2002&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Young MD%2C Wakefield MJ%2C Smyth GK%2C Oshlack A %282010%29 Gene ontology analysis for RNA%2Dseq%3A accounting for selection bias%2E Genome Biol 11%3A R&dopt=abstract

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

https://scholar.google.com/scholar?as_q=Gene ontology analysis for RNA-seq: accounting for selection bias.&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

https://scholar.google.com/scholar?as_q=Gene ontology analysis for RNA-seq: accounting for selection bias.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Young&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Yu L%2C Chen X%2C Wang Z%2C Wang S%2C Wang Y%2C Zhu Q%2C Li S%2C Xiang C %282013%29 Arabidopsis enhanced drought tolerance1%2FHOMEODOMAIN GLABROUS11 confers drought tolerance in transgenic rice without yield penalty%2E Plant Physiol 162%3A 1378%26%23x&dopt=abstract

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

https://scholar.google.com/scholar?as_q=Arabidopsis enhanced drought tolerance1/HOMEODOMAIN GLABROUS11 confers drought tolerance in transgenic rice without yield penalty.&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

https://scholar.google.com/scholar?as_q=Arabidopsis enhanced drought tolerance1/HOMEODOMAIN GLABROUS11 confers drought tolerance in transgenic rice without yield penalty.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yu&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Yu X%2C Li L%2C Li L%2C Guo M%2C Chory J%2C Yin Y %282008%29 Modulation of brassinosteroid%2Dregulated gene expression by Jumonji domain%2Dcontaining proteins ELF6 and REF6 in Arabidopsis%2E Proc Natl Acad Sci USA 105%3A 7618%26%23x&dopt=abstract

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

https://scholar.google.com/scholar?as_q=Modulation of brassinosteroid-regulated gene expression by Jumonji domain-containing proteins ELF6 and REF6 in Arabidopsis.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Modulation of brassinosteroid-regulated gene expression by Jumonji domain-containing proteins ELF6 and REF6 in Arabidopsis.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yu&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Zhang H%2C Mao X%2C Jing R%2C Chang X%2C Xie H %282011%29 Characterization of a common wheat %28Triticum aestivum L%2E%29 TaSnRK2%2E7 gene involved in abiotic stress responses%2E J Exp Bot 62%3A 975%26%23x&dopt=abstract

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

https://scholar.google.com/scholar?as_q=Characterization of a common wheat (Triticum aestivum L.) TaSnRK2.7 gene involved in abiotic stress responses.&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

https://scholar.google.com/scholar?as_q=Characterization of a common wheat (Triticum aestivum L.) TaSnRK2.7 gene involved in abiotic stress responses.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Zhang L%2C Zhao G%2C Xia C%2C Jia J%2C Liu X%2C Kong X %282012%29 A wheat R2R3%2DMYB gene%2C TaMYB30%2DB%2C improves drought stress tolerance in transgenic Arabidopsis%2E J Exp Bot 63%3A 5873%26%23x&dopt=abstract


https://scholar.google.com/scholar?as_q=A wheat R2R3-MYB gene, TaMYB30-B, improves drought stress tolerance in transgenic Arabidopsis.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=A wheat R2R3-MYB gene, TaMYB30-B, improves drought stress tolerance in transgenic Arabidopsis.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Zhang N%2C Yin Y%2C Liu X%2C Tong S%2C Xing J%2C Zhang Y%2C Pudake RN%2C Izquierdo EM%2C Peng H%2C Xin M%2C Hu Z%2C Ni Z%2C Sun Q%2C Yao Y %282017%29 The E3 ligase TaSAP5 alters drought stress responses by promoting the degradation of DRIP proteins%2E Plant Physiol 175%3A 1878%26%23x&dopt=abstract


https://scholar.google.com/scholar?as_q=The E3 ligase TaSAP5 alters drought stress responses by promoting the degradation of DRIP proteins.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=The E3 ligase TaSAP5 alters drought stress responses by promoting the degradation of DRIP proteins.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Zhang SS%2C Cai ZY%2C Wang XL %282009%29 The primary signaling outputs of brassinosteroids are regulated by abscisic acid signaling%2E Proc Natl Acad Sci USA 106%3A 4543%26%23x&dopt=abstract


https://scholar.google.com/scholar?as_q=The primary signaling outputs of brassinosteroids are regulated by abscisic acid signaling.&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

https://scholar.google.com/scholar?as_q=The primary signaling outputs of brassinosteroids are regulated by abscisic acid signaling.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Zhang ZY%2C Liu X%2C Wang XD%2C Zhou MP%2C Zhou XY%2C Ye XG%2C Wei XN %282012%29 An R2R3 MYB transcription factor in wheat%2C TaPIMP1%2C mediates host resistance to Bipolaris sorokiniana and drought stresses through regulation of defense%2D and stress%2Drelated genes%2E New Phytol&dopt=abstract



https://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Zhou QY%2C Tian AG%2C Zou HF%2C Xie ZM%2C Lei G%2C Huang J%2C Wang CM%2C Wang HW%2C Zhang JS%2C Chen SY %282008%29 Soybean WRKY%2Dtype transcription factor genes%2C GmWRKY13%2C GmWRKY21%2C and GmWRKY54%2C confer differential tolerance to abiotic stresses in transgenic Arabidopsis plants%2E Plant Biotechnol J 6%3A 486%26%23x&dopt=abstract

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

https://scholar.google.com/scholar?as_q=Soybean WRKY-type transcription factor genes, GmWRKY13, GmWRKY21, and GmWRKY54, confer differential tolerance to abiotic stresses in transgenic Arabidopsis plants.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Soybean WRKY-type transcription factor genes, GmWRKY13, GmWRKY21, and GmWRKY54, confer differential tolerance to abiotic stresses in transgenic Arabidopsis plants.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhou&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Zhuo C%2C Liang L%2C Zhao Y%2C Guo Z%2C Lu S %282017%29 A cold responsive ethylene responsive factor from Medicago falcata confers cold tolerance by up%2Dregulation of polyamine turnover%2C antioxidant protection%2C and proline accumulation%2E Plant Cell Environ 41%3A 2021%26%23x&dopt=abstract

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

https://scholar.google.com/scholar?as_q=A cold responsive ethylene responsive factor from Medicago falcata confers cold tolerance by up-regulation of polyamine turnover, antioxidant protection, and proline accumulation&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=A cold responsive ethylene responsive factor from Medicago falcata confers cold tolerance by up-regulation of polyamine turnover, antioxidant protection, and proline accumulation&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhuo&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1


bes/bzr transcription factor tabzr2 positively regulates … · 3 60 61 62 abstract 63 bri1-ems...

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