1 running head: es1 affects water loss 2 corresponding authors: … · 156 senescence marker genes,...

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Running Head: ES1 affects water loss 1

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Corresponding authors: 3

Dali Zeng 4

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State Key Laboratory of Rice Biology, China National Rice Research Institute, Hangzhou 6

310006, China 7

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Tel: (+0571)6337 0537 9

Fax: (+0571)6337 0389 10

E-mail: [email protected] 11

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Research Area: Genes, Development and Evolution13

Plant Physiology Preview. Published on August 4, 2015, as DOI:10.1104/pp.15.00991

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EARLY SENESCENCE 1 Encodes a SCAR-like Protein2 that Affects Water 15

Loss in Rice 16

Yuchun Rao†, Yaolong Yang†, Jie Xu†, Xiaojing Li, Yujia Leng, Liping Dai, Lichao Huang, 17

Guosheng Shao, Deyong Ren, Jiang Hu, Longbiao Guo, Jianwei Pan, Dali Zeng* 18

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State Key Laboratory of Rice Biology, China National Rice Research Institute, Hangzhou 20

310006, China (Y.R., Y.Y., J.X., Y.L., L.D., L.H., G.S., D.R., J.H., L.G. and D.Z.); College of 21

Chemistry and Life Sciences, Zhejiang Normal University, Jinhua 321004, China (Y.R., X.L 22

and J.P.); Key Laboratory of Crop Physiology, Ecology and Genetic Breeding, Ministry of 23

Education, Jiangxi Agricultural University, Nanchang 330045, China (Y.Y. and J.X.) 24

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One sentence summary: 27

The SCAR/WAVE-like protein2 affects water loss by regulating stomatal density in rice 28

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Total word count: 10652 30

Total characters (including space): 67804 31

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Footnotes 35

36 1This work was supported by grants from the National Natural Science Foundation of China 37

(31201183, 31221004, 31171531, 31171520, and 91435105), the State Key Basic Research 38

Program (2013CBA01403), the Ministry of Agriculture of China for transgenic research 39

(No.2013ZX08009003-001), and the China Postdoctoral Science Foundation 40

(2014M561108). 41

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*Corresponding author e-mail: [email protected] 44

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47 1 The author responsible for the distribution of materials integral to the findings presented in 48

this article in accordance with the policy described in the Instructions for Authors 49

(www.plantphysiol.org) is: Dali Zeng ([email protected]). 50

† These authors contributed equally to this work. 51

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Abstract 62

The global problem of drought threatens agricultural production and constrains the 63

development of sustainable agricultural practices. In plants, excessive water loss causes 64

drought stress and induces early senescence. In this study, we isolated a rice (Oryza sativa) 65

mutant, designated as early senescence 1 (es1), which exhibits early leaf senescence. The 66

es1-1 leaves undergo water loss at the seedling stage (as reflected by whitening of the leaf 67

margin and wilting) and display early senescence at the three-leaf stage. We used map-based 68

cloning to identify ES1, which encodes a SCAR-like protein 2, a component of the 69

SCAR/WAVE complex involved in actin polymerization and function. The es1-1 mutants 70

exhibited significantly higher stomatal density. This resulted in excessive water loss and 71

accelerated water flow in es1-1, also enhancing the water absorption capacity of the roots and 72

water transport capacity of the stems, as well as promoting in vivo enrichment of metal ions 73

co-transported with water. Expression of ES1 is higher in the leaves and leaf sheaths than in 74

other tissues, consistent with its role in controlling water loss from leaves. GFP-ES1 fusion 75

proteins were ubiquitously distributed in the cytoplasm of plant cells. Collectively, our data 76

suggest that ES1 is important for regulating water loss in rice. 77

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Key words: ES1; water loss; SCAR; stomatal density 79

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INTRODUCTION 81

Rice is a major world-wide food crop, but it consumes more water than most crops 82

(Bruce et al., 2015), with water consumption for rice cultivation accounting for 83

approximately 65% of agricultural water usage. Rice provides a staple food for about 3 84

billion people, while using an estimated 24–30% of the world's developed freshwater 85

resources (Bouman et al., 2007). Severe water shortages restrict the expansion of rice 86

production and hinder the irrigation of existing paddy fields (Zhu et al., 2013). One effective 87

way to overcome water shortages is to reduce water loss in rice plants, thus allowing 88

cultivation of this key crop in environments with less water (Nguyen et al., 1997). 89

In plants, the stomata on the leaf surface work as the main channels for discharge of 90



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water and entry of carbon dioxide, and thus strongly affect physiological processes such as 91

transpiration and photosynthesis. Previous studies showed that mutations in some genes 92

could affect stomatal density or differentiation, such as AtTMM (Yang et al., 1995), 93

AtSCRM2 (Kanaoka et al., 2008), AtSDD1(Von Groll et al., 2002), AtYODA2(Bergmann et 94

al.,2004). Stomata show a regular distribution on rice leaves (Huang et al., 2009) during plant 95

growth and development, various environmental factors affect the density and size of 96

stomata, as well as the chlorophyll contents of rice leaves. For example, rice leaves that 97

develop under water stress show substantial fewer stomata compared with leaves that develop 98

under well-watered conditions (Huang et al., 2009). Changes in stomatal density and 99

morphology affect water loss (Boonrueng et al., 2013). In rice, OsSRO1 (Similar to RCD-100

One) enhances drought tolerance by regulating stomatal closure (You et al., 2013) while the 101

zinc finger protein DST (Drought and Salt Tolerance) functions in drought and salt tolerance 102

by adjusting stomatal aperture (Huang et al., 2009). In Arabidopsis thaliana, overexpression 103

of the Mg-chelatase H subunit in guard cells confers drought tolerance by promoting stomatal 104

closure (Tsuzuki et al., 2013). Thus, stomatal closure and low stomatal density enhance 105

drought tolerance by reducing water loss in plants. 106

The epicuticular wax layer in plants acts as the first barrier to environmental conditions 107

by reducing water loss due to transpiration and preventing plant damage due to excessively 108

strong sunlight (Riederer et al., 2001). Leaf transpiration involves both stomatal and cuticular 109

transpiration. Stomatal conductance controls stomatal transpiration, but the physicochemical 110

properties of the leaf surface mainly control cuticular transpiration. For example, the 111

composition, thickness, and microstructure of the cuticular wax affect water permeability and 112

transport (Buschhaus et al., 2012; Svenningsson, 1988; Xu et al., 1995). OsDWA1 (rice 113

Drought-induced Wax Accumulation 1), OsGL1 (GLOSSY1), and OsWR1 (rice Wax 114

synthesis Regulatory gene 1) affect drought tolerance by regulating deposition or 115

biosynthesis of cuticular wax (Islam et al., 2009; Wang et al., 2012; Zhou et al., 2013; Zhu et 116

al., 2013). 117

Besides, leaf trichomes can also affect water loss (Konrad et al., 2015), and leaf 118

trichomes closely linked with actin cytoskeleton. The involvement of the actin cytoskeleton 119

in controlling directional cell expansion in trichomes has received much attention (Zhang et 120

al., 2005). Generally, genes that affect cytoplasmic organization can be studied by screening 121

leaf trichome mutants (Qiu et al., 2002). In Arabidopsis, a reproducible morphogenetic 122

program directs the polarized development of trichome branches (Le et al., 2006; Mathur et 123

al., 1999; Syzmanski et al., 1999). Some of these genes affect the cytoskeleton and also affect 124



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the morphology of normal plant cells, especially epidermal cells. For example, mutation of 125

SPIKE1 in Arabidopsis causes epidermal cells to show simple arrangement and 126

morphologies, i.e., all cells dividing along a single axis (Qiu et al., 2002). 127

To study the molecular mechanisms underlying water loss in rice, we isolated and 128

characterized the es1-1 (early senescence 1-1) rice mutant, which showed excessive water 129

loss and early senescence phenotypes. Map-based cloning data showed that ES1 encodes a 130

SCAR-like protein 2, and its Arabidopsis thaliana homolog affects the polymerization of 131

actin. The es1-1 mutants showed obvious changes in leaf trichomes, similar to Arabidopsis. 132

However, few studies have reported a connection between the actin cytoskeleton and water 133

loss in Arabidopsis. Our results demonstrated a critical role of the actin cytoskeleton in 134

regulating water loss in rice. 135

RESULTS 136

Identification and Characterization of Early Senescence Mutants 137

To study the mechanisms of senescence in rice, we screened a large pool of mutants 138

generated in the japonica rice cultivar Nipponbare (NPB) background by mutagenesis using 139

ethyl methanesulfonate (EMS). From this pool, we identified two mutants with an early 140

senescence phenotype. The two mutants showed similar phenotypes under the same growth 141

conditions and F1 hybrid individuals produced by the two parental mutants exhibited 142

phenotypes like the parental line with the weaker phenotype (subsequently named es1-1, see 143

below), indicating that the two mutants are allelic (Supplemental Table 1); therefore, we 144

termed these mutants early senescence 1 (es1-1 and es1-2). Under normal growth conditions, 145

es1-1 plants showed severely retarded development. At the seedling stage, the es1-1 mutants 146

displayed whitish and yellowish leaf tips (Figure 1A), a hallmark of early senescence (Li et 147

al., 2014); this phenotype increased with increasing leaf age, becoming more severe at the 148

heading stage (Figure 1B). Newly developed leaves showed yellowing margins that rolled 149

inwards or formed a spiral and old leaves showed spots with a rusty color and water 150

deficiency phenotypes, including wilting (Figures 1A and 1B). Histochemical analysis 151

showed that concentrations of senescence-related substances, including hydrogen peroxide 152

(H2O2), superoxide radical (O2•-), and malondialdehyde (MDA), were higher in es1-1 leaves 153

than in the wild-type leaves (Figures 1C and 1D), indicating that the mutant does show 154

senescence phenotypes (Moradi et al., 2007). Moreover, we measured the expression of two 155



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senescence marker genes, Staygreen (Sgr) and Os185, in NPB and es1-1 (Supplemental 156

Figures 1F and 1G). We found that the transcript levels of these two genes were substantially 157

higher in es1-1 than in NPB, suggesting that es1-1 caused senescence (Park et al., 2007; Lee 158

et al., 2001). We also measured plant height, finding that es1-1 plants were much shorter than 159

the wild-type plants from the seedling to the mature stages (Figures 1A and 1B, Supplemental 160

Table2). At the mature stage, es1-1 mutants showed degraded or white panicles with a low 161

seed setting rate (only 2.4%; Figure 1E, Supplemental Table 2), short internodes (Figure 1F, 162

Supplemental Table2), and brown, open glumes (Figure 1G). Scanning transmission electron 163

microscopy showed that es1-1 mutants had disordered thylakoids, compared with the neat 164

and well-ordered thylakoids observed in wild-type plants; moreover, es1-1 mutants had lower 165

chlorophyll contents than wild type NPB. 166

Compared with es1-1, the es1-2 plants had more tillers (Supplemental Figures 1A and 167

1C), higher plants (Supplemental Figures 1A and 1D), and showed a stronger early 168

senescence phenotype in the leaves (Supplemental Figure 1B). In this study, we mainly 169

focused on es1-1 mutants, unless otherwise specified. 170

Map-Based Cloning of ES1 171

To clarify whether es1-1 phenotypes were caused by a single or multiple gene(s) and 172

dominant or recessive genes, we crossed the mutant plants directly and reciprocally with 173

three wild-type cultivars. All the F1 plants showed no symptoms of early senescence. In the 174

F2 segregating populations of these three crosses, normal and early senescent plants showed a 175

typical segregation ratio of 3:1 (Supplemental Table 3). This result suggested that a single 176

recessive nuclear gene controls the early senescence phenotype of es1-1. 177

For cloning ES1, we crossed the mutant es1-1 (japonica) with a typical indica cultivar 178

(NJ6). Plants with the es1-1 phenotype were identified from the F2 generation and used as the 179

initial mapping population. For primary chromosome mapping, we used 164 pairs of simple 180

sequence repeat (SSR) primers distributed on the 12 chromosomes of rice at a distance of 10–181

30 cM from each other to detect differences between es1-1 and NJ6. A significant 182

amplification difference was detected on chromosome 1 using the SSR marker M1, showing 183

linkage with a small population in the F2. The M1 marker was further used to analyze 320 184

mutants in the F2 population, which detected 15 recombinants. Genetic linkage analysis 185

mapped the M1 marker to a distance of 2.3 cM from ES1 (Figure 2A). 186



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For fine mapping of ES1, the mutation in ES1 must be flanked by two molecular 187

markers. Thus, we designed multiple pairs of primers at positions relatively far from M1 188

(Supplemental Table 4). The marker M6 also showed polymorphisms between es1-1 and NJ6. 189

Screening of the primary mapping population (320 mutants) identified 11 recombinants that 190

differed from those identified using M1 (Figure 2A). Linkage analysis mapped the M6 191

marker to a distance of 1.8 cM from ES1. Next, we used M1 and M6 to screen the entire 192

population (2850 plants), which identified 50 and 39 recombinants, respectively (Figure 2A). 193

To further narrow the ES1 region, we developed a large number of sequence-tagged site 194

(STS) and cleaved amplified polymorphic sequence (CAPS) markers between M3 and M4. 195

Primers C1–C9 showed good polymorphisms between es1-1 and TN1. Thus, we used these 196

primers to analyze the recombinants obtained by preliminary screening and to construct fine 197

genetic and physical maps of ES1 (Figure 2B; Supplemental Table 4). The number of 198

recombinants detected by C1 and C10 decreased to 28 and 35, respectively. Similarly, the 199

number of recombinants screened by C2 and C9 decreased to 10 and 12, respectively, and 200

those detected by C3 and C8 further decreased to three and four, respectively. The 201

recombinants detected by C3 and C8 corresponded to different individual plants. 202

We also designed primers for the region between C3 and C8 to further screen the 203

recombinants. Finally, these new primers detected only one recombinant and thus these 204

markers tightly co-segregate with ES1 (Figure 2B). The physical distance between the end 205

markers C5 and C6 was 13.1 kb, which included two predicted open reading frames. 206

Sequencing analysis detected a unique mutation in LOC-Os01g11040 within the 13.1 kb 207

region in es1-1 compared with the wild-type sequence. This single-base mutation replaced G 208

with A in the first nucleotide of the third intron (nucleotide 2275; Figure 2C). To test whether 209

this mutation alters the normal splicing of the third intron, we generated es1-1 and wild-type 210

genomic cDNAs using reverse transcription. Sequencing showed that the es1-1 cDNA was 62 211

bases longer than the wild-type cDNA (Figure 2D). This increase in length coincided with the 212

length of the third intron, which contains a stop codon that results in the premature 213

termination of protein translation (Figure 2E). Similarly, sequencing analysis showed that the 214

mutation in es1-2 was a single-base substitution (G to A) at nucleotide 4660. This mutation 215

changed the tryptophan (Trp) codon into a stop codon, thus resulting in the premature 216

termination of protein translation (Figures 2E). 217

We then used genetic complementation to verify the identity of ES1. A 10.6-kb fragment 218

containing ES1 (including the upstream 2-kb and downstream 1-kb sequences) was 219



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introduced into es1-1 and es1-2 mutants, and 52 and 36 transgenic plants, respectively, were 220

recovered. Exogenous ES1 rescued the phenotypes of es1-1 and es1-2 (Figure 2F), and the 221

complementation reversed the mutant phenotype of es1-1. Taken together, these data 222

demonstrate that LOC-Os01g11040 (Os01g0208600) is ES1. 223

ES1 Encodes a SCAR-Like Protein of the Arp2/3-SCAR Pathway 224

We performed a BLAST search to identify ES1 homologs in more than 20 different 225

plant species. ES1 showed high amino acid sequence similarity to proteins in other species 226

such as Oryza brachyantha (85%), Brachypodium distachyon (68%), maize (60%), and 227

Setaria italica (64%) (Figure 3E). ES1 also shares high amino acid sequence similarity to 228

proteins in both monocots and dicots, suggesting that ES1 and its homologs may perform 229

similar functions. Examination of ES1 homologs in Arabidopsis showed that ES1 230

(Os01g0208600) encodes a SCAR-like protein 2; its closest homolog in Arabidopsis forms 231

part of the actin-related 2/3 (ARP2/3) complex, which functions in regulating actin filament 232

polymerization and has been examined in detail in Arabidopsis. ARP2/3 alone is inactive in 233

Arabidopsis. A domain formed by the SCAR-like family proteins, and members of other 234

protein families (e.g., SPA1 and ABI families) are responsible for binding to and activation of 235

the Arp2/3 complex (Zhang et al., 2005). In Arabidopsis, mutation of the gene encoding 236

SCAR-like protein 2 leads to changes in leaf trichomes and stomata (Basu et al., 2005). In 237

our study, we observed substantial changes in leaf trichomes of es1-1, mainly reflected by the 238

serious degradation of the trichome tip (Figures 3A and 3B). The leaves of es1-1 had smooth 239

leaf margins without a jagged pattern (Figure 3A). 240

To examine the possible role of ES1 in regulating actin filaments, we examined the 241

organization of F-actin in the roots of wild type and es1-1 mutants by Alexa Fluor 488-242

phalloidin staining. The actin filaments were well organized in wild type (Figure 3C). The 243

actin filaments in wild-type were complete, orderly arranged, while es1-1 showed irregular 244

arrangement. Moreover, the actin filaments in es1-1 were shorter than that in wild type, as 245

indicated by arrows (Figure 3D), which indicated that ES1 likely functions in the Arp2/3-246

SCAR pathway in rice and that a mutation in ES1 affects the actin cytoskeleton in rice cells 247

(Dyachok et al., 2011). 248



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Expression of ES1 and Subcellular Localization of ES1 249

To monitor the tissue-specific expression of ES1, we generated an ES1:GUS (β-250

glucuronidase) reporter construct containing the 2.0-kb genomic region upstream of the start 251

codon of ES1. We detected high GUS activity in leaves, leaf sheaths, and root tips, and also 252

detected lower GUS activity in stamens and vascular bundles (Figures 4A–4E). Reverse-253

transcription quantitative polymerase chain reaction (RT-qPCR) assays showed that ES1 was 254

ubiquitously expressed in various tissues at the tillering and heading stages, including the 255

roots, culms, leaves, sheaths, and spikelets. We observed the highest levels of ES1 expression 256

in the leaf and leaf sheath (Figure 4F). Consistent with the RT-qPCR data, ES1:GUS 257

expression was higher in rice leaves and leaf sheaths than in other plant tissues. 258

To investigate the subcellular localization of ES1, we constructed a construct to express 259

eGFP-ES1 (35S::eGFP-ES1 DNA) and introduced it into onion and tobacco epidermal cells. 260

Fluorescence signals were detected in both cell types, and the signals surrounded the 261

cytoplasm, nucleus, and cell membrane (Figures 4G, 4H, 4I, and 4J). Consistent results were 262

obtained by examining protoplasts extracted from tobacco leaves after the expression of the 263

fusion protein (Figures 4K and 4L). These results indicated that ES1 was ubiquitously 264

distributed in the cytoplasm of plant cells. 265

ES1 Affects the Density of Leaf Stomata in Rice 266

Scanning electron microscopy of es1-1 leaves showed that these leaves had smoother 267

surfaces than the leaves of wild-type plants. In addition, these leaves showed substantial 268

smaller siliceous protrusions at the seedling stage and substantially more stomata per unit leaf 269

area compared with wild-type leaves. The number of semi-open stomata in es1-1 was also 270

larger than that in wild-type (Figures 5A and 5B). Moreover, the tips of trichomes and the 271

waxy layer were severely degraded on the leaf surface of es1-1 mutants (Figure 5A). 272

Statistical data showed that, regardless of the position, stomatal density was significantly 273

higher in es1-1 than that in the wild-type. While both stomatal conductance and transpiration 274

rate were also detected, they were also significantly higher in es1-1, these data indirectly 275

suggested stomatal density in es1-1 was higher (Figure 5B). The maximum and minimum 276

stomatal apertures were greater in the wild-type compared with es1-1(Figure 5C). At the 277

seedling stage, the transcriptional level of several genes which could affect the increase of 278



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stomatal density were analyzed by the real-time PCR, including OsTMM, OsSCRM, 279

OsSDD1, OsYODA2 (Du et al., 2014). The expression level of OsTMM, OsSCRM and 280

OsSDD1 were significantly higher in es1-1 than that in the wild-type, and ES1 gene also 281

showed higher expression level in es1-1(Figure 5E). 282

Leaves of wild-type and es1-1 at seedling stage were sprayed with 300 umol / L ABA, 283

after 3 hours, quantitative analysis of OsTMM, OsSCRM, OsSDD1, OsYODA2 was taken. In 284

the wild-type, the expression level of these genes almost didn’t change; but in es1-1, the 285

majority of these genes had shown a significantly declined expression level, this indicated in 286

es1-1 those genes which could affect the increase of stomatal density were sensitive to ABA. 287

We also detected the rate of vitro water loss (RWL) of seedling leaves from the same position 288

of the wild-type and es1-1 before and after ABA treatment. The results showed that, no 289

matter with or without ABA treatment, the vitro RWL value was always higher in es1-1 than 290

that in the wild-type. The vitro RWL value in the wild-type was reduced after ABA 291

treatment, and the value in es1-1 was also reduced after ABA treatment, but it was not so 292

obvious compared with the wild-type (Figure 5D). SEM assay on the leaves of wild-type and 293

es1-1 with ABA treatment showed that nearly all stomata of both wild-type and es1-1 were 294

closed. Moreover, we also examined the expression level of multiple ABA response-related 295

genes (ABA signaling genes) in wild-type and es1-1 before and after ABA treatment (Shang 296

et al., 2010), and discovered that after ABA treatment, OsDREB2A gene was up-regulated, 297

while OsABI4 gene was down-regulated. These results suggest that both wild-type and es1-1 298

were sensitive to ABA (Figure 5E). 299

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The es1-1 Plants Showed Higher Water Loss Rates than Wild Type 301

In vitro, the rate of water loss of es1-1 was higher than that of NPB at the seedling 302

stage (Figure 6A), as the detached leaves of es1-1 shrunk into a line at 30 min, but the NPB 303

leaves remained nearly normal in width (Figure 6A). To confirm this phenomenon, we also 304

measured water loss per unit of time (g cm-2.10-3) at the tillering stage in vivo and in vitro 305

(Figures 6B and 6C), which gave similar results: the water loss per unit of time in vitro 306

(detached leaves) in different periods was uniformly higher in es1-1 than in NPB (Figure 6B). 307

The water loss per unit of time in vivo was also uniformly higher in es1-1 than in NPB at 4, 8, 308

and 14 days after tillering (Figure 6C). 309

To verify excessive water loss in es1-1, we performed a guttation experiment, where we 310



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looked for the exudation of drops of xylem sap on the leaf periphery in plants grown at 311

different humidities. Hydroponic seedlings were cultured in light, in an incubator at different 312

humidities, from 30% and 90%, and the es1-1 and wild-type plants were examined for 313

guttation. At the seedling stage (two-leaf), both the wild-type plants and es1-1 were capable 314

of guttation at 30% humidity. However, higher humidity was required for guttation with plant 315

growth. Until the strong seedling stage (two-tiller), guttation was observed in wild-type 316

plants but not in es1-1 (Supplemental Figure 2). This result indicated that water loss occurred 317

more rapidly in es1-1 mutants than in the wild-type plants. 318

319

Water Absorption and Transport Capacity was Increased in es1-1 320

Mutants 321

It is unknown whether excessive water loss through leaves affects water absorption in 322

the root. To address this, we measured root traits in es1-1 and wild-type plants (Figures 7A, 323

7B, 7C, and 7D). The es1-1 plants had smaller primary and total root lengths (Figures 7E and 324

7F) but higher average root diameters, total root volumes, and total numbers of fibrous roots, 325

compared with the wild-type plants (Figures 7G, 7H, 7I, and 7J). As fibrous roots are a major 326

tissue for water adsorption in rice (Smith et al., 2012), an increase in fibrous root number 327

indicated an increase in the water absorption capacity of the roots in es1-1 mutants. 328

329

Examination of cross sections of the culm and primary root from es1-1 and NPB showed 330

that the es1-1 stems had 3–4 additional vascular bundles (Figures 8A, 8B, and 8C) and the 331

es1-1 primary roots had 2 to 3 additional conduits, compared with NPB (Figures 8D, 8E, and 332

8F). Vascular bundles and conduits are necessary for water transport (Kim et al., 2014). 333

Moreover, the water potential values were all higher in es1-1 than that in wild-type in various 334

tissues, including roots, stems, leaves, and sheath, which indicated that the ability to transport 335

water was stronger in es1-1 than in WT (Figure 8G) (Silva et al., 2011). Therefore, our results 336

indicate that es1-1 mutants have an enhanced ability to transport water. 337

338

Excessive Water Loss Causes in Situ Enrichment of Minerals in es1-1 339

In es1-1 mutants, excessive water loss through the leaves enhances the water absorption 340



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capacity of the roots and the water transportation capacity of the roots and culms. This in turn 341

accelerates water circulation in the plant, thus leading to predicted in situ enrichment of metal 342

ions cotransported with water (Kim et al., 2014). To test this hypothesis in this mutant, we 343

determined the mineral concentrations of different tissues of es1-1 and wild-type plants at the 344

mature stage. Consistent with the hypothesis, the concentrations of all four minerals tested 345

(Cu, Fe, Mn, and Zn) in the examined tissues were much higher in es1-1, especially in the 346

roots and new leaves, than in wild-type plants (Table 1). The manganese (Mn) concentration 347

in es1-1 leaves (719 mg kg-1) was seven times higher than that in wild-type plants (100 mg 348

kg-1). The concentrations of the four minerals were also higher in es1-1 seeds than in NPB 349

(Table 1). These results suggested that mutation in ES1 promoted the accumulation of 350

minerals in plants. The substantial accumulation of metal ions in es1-1 plants was likely due 351

to excessive water loss and higher transpiration pull in the upper part of the plant. 352

DISCUSSION 353

In this study, we characterized es1-1, an early senescence mutant that experienced 354

excessive water loss. Map-based cloning showed that ES1 encodes a SCAR-like protein 2, a 355

component of the SCAR/WAVE complex that is involved in actin polymerization. This 356

suggests that a mutation in ES1 affects polymerization of actin and causes an abnormality in 357

the cytoskeleton that promotes a higher stomatal density (Huang et al., 2000; Xiao et al., 358

2003; Yu et al., 2001; Zhang et al., 2012), thus leading to excessive water loss. 359

Under stress conditions, plants develop a wax layer on the leaf surface or moderately roll 360

their leaves to reduce transpiration, thereby protecting themselves from excessive water loss 361

(Hu et al., 2012; Jäger et al., 2014). Although stomata account for only 1–2% of the leaf area, 362

approximately 90% of water loss occurs through stomata (Buckley et al., 2005). Under 363

drought conditions, rice cultivars that can maintain relatively high water potential and low 364

transpiration rate in their leaves have strong drought resistance (Luo et al., 2001). These 365

drought-resistant cultivars commonly retain water in the plant body by closing their stomata. 366

Small stomatal aperture and large diffusion resistance can jointly reduce water loss due to 367

transpiration, thus avoiding the adverse effects of drought. Grill and Ziegler (1998) proposed 368

that controlling the stomata is the most important way to improve the efficiency of water use 369

in plants. In the present study, scanning electron microscopy showed that the es1-1 mutants 370

had substantially more stomata than wild-type plants. The expression level of OsTMM, 371

OsSCRM and OsSDD1 were significantly higher in es1-1 than that in the wild-type (Figure 372



14

5E), which was closely related to stomatal density. Stomatal density was significantly higher 373

in es1-1 than that in the wild-type. While both stomatal conductance and transpiration were 374

also significantly higher in es1-1 than that in the wild-type (Figure 5B), these data suggested 375

that es1-1 definitely lose water more quickly than wild-type. Nearly all stomata of both wild-376

type and es1-1 were closed after ABA treatment, and the vitro RWL value in the wild-type 377

was reduced after ABA treatment, the value in es1-1 was also reduced after ABA treatment, 378

but it was not so obvious compared with the wild-type (Figure 5D). Moreover, the wax layer 379

on the leaf surface of es1-1 mutants was considerably degraded. So, we thought the excessive 380

water loss in es1-1 mainly due to increased stomatal density, meanwhile the degradation of 381

waxy layer and leaves hair may aggravate the rate of water loss. 382

Excessive water loss in the leaves inevitably depletes water from the body of es1-1 383

plants. Thus, more water needs to be absorbed through the roots to meet the metabolic 384

requirements of es1-1 plants. In this study, we analyzed the roots of es1-1 and found that the 385

total volume of root and the number of fibrous roots increased compared to wild type 386

(Figures 7I and 7J), indicating that the water absorption capacity of the roots was enhanced in 387

es1-1. Cross-sections of the primary root and stems also showed that the number of vascular 388

bundles in the stems increased by four (Figure 8C) and those in the roots increased by two to 389

three in es1-1 compared to the wild-type plants (Figure 8F). Moreover, the water potential 390

values were all higher in es1-1 than in wild-type in various tissues (Figure 8G). These 391

observations confirmed that the water transport capacity of the roots was enhanced in es1-1. 392

All the above changes inevitably accelerate water circulation and cause minerals 393

commonly cotransported with water to accumulate in the various tissues of es1-1 plants. 394

Indeed, in different tissues, the concentrations of four minerals were higher in es1-1 than in 395

NPB (Table 1). For example, the Cu concentration in es1-1 (446.3 mg kg-1) was 18-times 396

higher than in wild-type plants (23.5 mg kg-1), which could cause Cu overload in es1-1 397

plants. Enrichment of low-mobility metal elements (e.g., Cu, Fe, Mn, and Zn) in various 398

tissues of es1-1 may in turn accelerate the onset of senescence. Moreover, the higher 399

concentrations of mineral nutrients in seeds from the es1-1 mutants might produce more-400

nutritious food; however, the accumulation of toxic elements such as arsenic might produce 401

food that could adversely affect human health. 402

In our study, we found that actin filaments were shorter in es1-1, and the continuity was 403

poor compared with wild-type (Figures 3C and 3D). Actin filaments function in many 404

endomembrane processes, such as endocytosis of plasma membrane, vacuole formation, 405

plasma membrane protrusion in crawling cells, and vesicle transport from the Golgi complex 406



15

(Svitkina et al., 1999; Eitzen et al., 2002; Kaksonen et al., 2003; Mathur et al., 2003; Chen et 407

al., 2004). The ARP2/3 complex functions as a key regulator of actin filament nucleation in 408

plants (Zhang et al., 2008). The ARP2/3 is inactive by itself, as actin polymerization requires 409

activation by the SCAR/WAVE complex, formed by proteins of the SCAR family. The 410

SCAR/WAVE complex is highly conserved in plants. A deficiency of the SCAR/WAVE 411

complex often leads to morphological changes in leaf trichomes and epidermal cells. This 412

phenomenon has been reported in several studies in Arabidopsis (Li et al., 2003; Mathur et 413

al., 2003; Saedler et al., 2004) but not in rice. In our study, es1-1 showed evident 414

morphological changes in leaf trichomes (Figures 3A, 3B, and 5C), confirming that the 415

function of the SCAR/WAVE complex is conserved in different species. Additional 416

components of the SCAR/WAVE complex can be identified by screening for mutants that 417

affect the leaf trichomes of the es1-1 mutant. 418

Actin polymerization occurs in the cytoplasm. In the present study, the fluorescent 419

signal of eGFP-ES1 was detected in the cytoplasm and plasma membrane of tobacco and 420

onion epidermal cells, a localization consistent with the predicted function of ES1 in affecting 421

the actin cytoskeleton. After fusing the ES1 promoter with the GUS reporter gene, GUS 422

staining was observed in various tissues, including the roots, root hairs, stems, leaves, leaf 423

sheath, and vascular bundles, which are associated with water absorption, transportation, and 424

loss. The ES1 expression level was relatively high in the leaves and leaf sheaths—the two 425

major tissues involved in water loss. All these results are consistent with the proposed 426

function of ES1. 427

The increased number of stomata would increase water loss and induce drought stress 428

in es1-1 plants. Drought stress affects photosynthetic capacity, respiration, membrane 429

permeability, osmotic adjustment, enzyme activity, and hormone levels in rice leaves, thus 430

reducing leaf area, leaf area index, and dry weight. Drought stress also prevents the 431

accumulation of dry matter and accelerates senescence (Hu et al., 2010; Ding et al., 2014; 432

Sellammal et al., 2014). In the present study, es1-1 plants showed early senescence 433

characterized by yellowish leaf color and wilting of leaf margins at the seedling stage. 434

Transmission electron microscopy showed that the volume percentage of chloroplasts in the 435

es1-1 cells was lower than that in wild-type cells; however, the number of chloroplasts 436

(irregular and fine prolate) was higher in es1-1 cells than in wild-type cells (Figure 1H). This 437

might have caused the decline in chlorophyll content in es1-1, causing the leaves to turn 438

yellowish. In es1-1, the chloroplasts contained disorganized thylakoids (Figure 1H) as 439



16

opposed to the well-organized thylakoids in wild-type plants. The disordered thylakoids may 440

have reduced the capacity to absorb light energy, which in turn would decrease the 441

photosynthetic rate, thus causing early senescence in plant leaves. 442

Early senescence in rice (especially in functional leaves) is extremely unfavorable for 443

rice growth and production because of its serious effects on yield and quality (Zhu et al., 444

2012). Therefore, rice breeders generally avoid lines showing early senescence. Similarly, the 445

stay-green trait in rice also does not improve yield; although the stay-green trait promotes the 446

ability of source tissues to fix carbon, it does not necessarily enhance the contents of sink 447

tissues in plants. For example, a study on a stay-green mutant of rice (sgr[t]) reported that 448

late photosynthesis and yield traits (seed-setting rate and thousand-grain weight) were not 449

enhanced in sgr[t] mutants (Cha et al., 2002). In the present study, the early senescing mutant 450

es1-1 showed other phenotypes such as decreased number of tillers and substantially reduced 451

seed-setting rate. Our data provide new insights into the molecular mechanisms underlying 452

early senescence in plants, which will help genetically improve rice yield. 453

MATERIALS AND METHODS 454

Plant Growth and Sampling 455

The es1-1 and es1-2 mutants were isolated from the japonica variety Nipponbare that 456

was subjected to EMS treatment. After multiple generations of inbreeding, the phenotypes of 457

these two mutants were stably inherited, and homozygous mutant strains were obtained. The 458

homozygous mutant es1-1 was directly and reciprocally crossed with two typical japonica 459

cultivars (Zhonghua 11 and Chunjiang 06) and one typical indica rice cultivar (Nanjing 6) 460

providing a relatively clear genetic background to construct the genetic population. The 461

obtained seeds of the F1 generation were sown and transplanted as individual plants to 462

generate the F2 generation by inbreeding. The numbers of individuals showing wild-type and 463

early senescence phenotypes were counted at the seedling stage. The segregation ratio was 464

calculated using statistical methods. Genetic analysis was performed on es1-1, and recessive 465

individuals were retrieved for preliminary mapping of the mutation. Plant materials were bred 466

in experimental field of the China National Rice Research Institute, Hangzhou, China. 467



17

Detection of Reactive Oxygen Species and Malondialdehyde 468

H2O2 and O2•- were detected using nitroblue tetrazolium (NBT) and diaminobenzidine 469

(DAB), respectively, according to (Li et al., 2010; Wi et al., 2010) with some modifications. 470

Leaves of 3-week-old plants that were grown in growth chambers were incubated in 0.05% 471

NBT (Duchefa) or 0.1% DAB (Sigma) at room temperature in darkness with gentle shaking 472

for 12 hrs. Chlorophyll was cleared by treating with 90% ethanol at 80°C. The concentration 473

of malondialdehyde (MDA) was measured according to the method described by Moradi and 474

Ismail (2007) with minor modifications (Moradi et al., 2007). 475

Determination of Water Potential 476

Ten seeds of NPB and es1-1 were selected, germinated for 3 days, then cultured in an 477

incubator at 28°C for 60 days. The WP4-T Dewpoint PotentiaMeter was preheated for 30 478

min until the temperature remained stable. Various tissues such as leaf, sheath, culm, and root 479

of NPB and es1-1 were harvested from the same position on each plant and cut into short 480

pieces. After making sure the sample temperature was lower than room temperature, the 481

samples were put in the measuring apparatus, which showed the water potential value of the 482

sample. Every sample measurement had six independent repeats, and the weight of the 483

samples was equal. 484

Map-Based Cloning of ES1 485

The mutation in es1-1 was mapped in the F2 population of a cross between es1-1 and the 486

indica variety NJ6. To finely map the ES1 locus, new molecular markers were developed 487

using public databases (Supplemental Table 4). Further, ES1 was sequenced using specific 488

primers (Supplemental Table 4). 489

490

Fluorescence Microscopy of Actin Filaments 491

For F-actin observation, plants were grown in a culture chamber with 16/8 hrs 492

photoperiod at 30°C. Seedling roots were used to observe actin organization. F-actin was 493

stained using the previously described method (Olyslaegers and Verbelen, 1998; Zhang et al., 494



18

2011). Seven-day-old roots were fixed in PEM buffer (100 mM PIPES, 10 mM EGTA, 0.3 M 495

mannitol, 5 mM MgSO4, pH 6.9) with 3% paraformaldehyde for 30 min and washed 3 times 496

with PEM. After washing, roots were incubated in PEM buffer with 0.66 mM Alexa Fluor 497

488-phalloidin (Life Technologies). After overnight incubation at 4°C, samples were washed 498

three times with PEM buffer and then observed in 50% glycerol with a confocal microscope 499

(Olympus FLUOVIEW FV1000). 500

501

Phylogenetic Analyses 502

A BLAST search of the SCAR-like 2 amino acid sequence was performed 503

against the database (http://www.ebi.ac.uk/Tools/sss/ncbiblast/). The phylogenetic tree was 504

constructed based on the amino acid sequences. Maximum likelihood (ML) phylogenetic 505

analysis was performed by MEGA6.0 (Tamura et al., 2013). ML analysis of the SCAR-like 2 506

family was based on the amino acid sequences using the Jones-Taylor-Thornton model, 507

which was chosen after model testing. Support for the ML trees was evaluated by 1000 508

bootstrap replicates. 509

510

Plasmid Construction and Plant Transformation 511

The cDNA sequence of ES1 was amplified using the primers cES1-F and cES1-R (Table 512

S3). This cDNA was fused in frame with eGFP in pCambia1300 (http://www.cambia.org) 513

with minor modifications to generate the transient expression vector 35S::eGFP:cES1. The 514

35S::eGFP-cES1 plasmids were transferred into Agrobacterium tumefaciens strain EHA105 515

by electroporation; the cells of rice ES1, Nicotiana tabacum, and onion were transformed 516

according to a previously described method (Hiei et al., 1994; Lv, 2010). 517

For the molecular complementation assay, a 10.6-kb genomic fragment comprising the 518

ES1 promoter region, coding sequence, and 3′ untranslated region was PCR amplified from 519

the genomic DNA of wild-type plants using pES-F and pES-R primers (Table S3). The PCR 520

amplification product was cloned into pCAMBIA1300 to generate the ES1:ES1 construct. 521

Briefly, the pCambia1300::ES1 vector was first digested with the restriction enzymes PstI 522

and XbaI. Next, the fragment containing ES1 was digested with restriction enzymes Sse83871 523



19

and NheI. All the restriction enzymes used above are isocaudomers. The pCambia1300::ES1 524

plasmids were transformed into A. tumefaciens strain EHA105 by electroporation. The es1-1 525

and es1-2 plants were transformed according to a published method (Hiei et al., 1994). 526

To generate the ES1:GUS fusion construct, a 2.0-kb upstream genomic region of the 527

ES1 start codon was amplified with the primers ES1-gus-F and ES1-gus-R (Table S3). The 528

amplified fragment was linked with the reporter GUS gene and together inserted in the 529

pCambia1305 vector (http://www.cambia.org). 530

GUS Staining 531

Samples (proES1::GUS) were stained with a solution containing 50 mM NaPO4 buffer, 1 532

mM 5-bromo-4-chloro-3-indolyl-β-d-glucuronic acid, 0.4 mM K3Fe(CN)6 , 0.4 mM 533

K4Fe(CN)6, and 0.1% (v/v) Triton X-100. The samples were then incubated at 37°C in the 534

dark for 10 hrs. Chlorophyll was removed with 70% ethanol for observation. 535

RNA Extraction and RT-qPCR 536

Total RNA was extracted from the roots, culms, leaves, sheaths, and spikelets of wild-537

type and es1-1 plants at the seedling, tillering and heading stages using an RNeasy Plant Mini 538

Kit (Qiagen). Reverse transcription was handled with the ReverTra Ace qPCR-RT Kit 539

(TOYOBO), the primers are described in Supplemental Table 4. RT-qPCR analysis was 540

conducted with the StepOnePlus System (ABI) using THUNDERBIRD qPCR Mix 541

(TOYOBO), reaction procedure was 95°C 30 s; 95°C 5 s, 55°C 10 s, 72°C 15s for 40 cycles. 542

OsActin was used as a control. The 2-ΔΔCt method was used for quantification (Livak et al., 543

2001). 544

Microscopy 545

In different periods, especially at the noon when the sunlight was the strongest (and thus 546

the stomata are likely to be closed), fresh leaf specimens were collected from the same 547

position ( 1/4, 1/2 and 3/4 of leaf blade ) in the mutant es1-1 and the control Nipponbare, 548

from plants that showed consistent growth. The specimens were cut into approximately 1 × 2 549



20

mm pieces and processed as follows for microscopic examination. 550

Dual fixation: The specimens were fixed in 2.5% glutaraldehyde solution, vacuumed in a 551

vacuum apparatus for approximately 20–30 min (which allowed the specimens to be 552

immersed in the fixative as completely as possible), and kept at 4°C overnight. Thereafter, 553

the fixative was discarded, and the specimens were rinsed with 0.1 M phosphate-buffered 554

saline (PBS), pH 7.0. The specimens were rinsed 3–4 times (15 min each). The specimens 555

were then fixed in 1% osmium tetroxide for at least 1 h. The fixative was discarded, and the 556

specimens were rinsed with 0.1 M PBS three times (15 min each) as described above. 557

Dehydration: The specimens were first dehydrated with a gradient of ethanol (50%, 70%, 558

80%, 90%, and 95%; 15 min to 20 min at each gradient), processed in anhydrous ethanol for 559

20 min, and treated in pure acetone for 20 min. 560

After dehydration, the specimens were immersed in a mixture of ethanol and isoamyl 561

acetate esters (volume ratio 1:1) for 30 min and were then treated with pure isoamyl acetate 562

for 1-2 h. The specimens were dried, coated, and examined using a Hitachi TM-1000 563

scanning electron microscope. 564

For transmission electron microscopy of the leaves and cross-sectional examination of 565

the leaves and roots, the specimens were pretreated as described above. After dehydration, 566

the specimens were treated with a mixture of embedding agent and pure acetone at a volume 567

ratio of 1:1 for 1 h, followed by treatment with a mixture of embedding agent and pure 568

acetone at a volume ratio of 3:1 for 3 h and pure embedding agent overnight. The specimens 569

were then embedded in small boxes and heated at 70°C for approximately 9 h. The obtained 570

embedded samples were sliced into 70-90 nm sections using a Reichert ultramicrotome and 571

stained with lead citrate solution and saturated uranyl acetate solution in 50% ethanol for 15 572

min each. The sections were examined and photographed using a Hitachi H-7650 type 573

transmission electron microscope. 574

Determination of Minerals 575

Wild-type and es1-1 plants were cultured in complete hydroponic nutrient solution up 576

to the heading stage. Tissue specimens were taken from the roots, stems, old leaves, leaf 577

sheaths, and new leaves. The weight of fresh specimens was more than 10 g for the different 578



21

tissues. The specimens were oven dried at 80°C for 3 days to achieve a constant weight. After 579

grinding, the dry samples (0.25 g for es1-1 and NPB, respectively) were digested with a 580

mixture of concentrated nitric acid and perchloric acid (volume ratio 1:3). The volume of the 581

digestion solution was adjusted to 25 ml with single-distilled water. The treated samples were 582

then used for elemental analysis. Concentrations of elements were determined using a full-583

spectrum direct reading inductively coupled plasma-atomic emission spectroscopy (IRIS 584

Intrepid II XSP ICP-OES PE-2100; Thermo Electron Co., Ltd, USA; Shao et al., 2008). 585

Detection of the Rate of Water Loss 586

In vitro detection: The same leaf parts were selected from NPB and es1-1 plants at the 587

seedling stage. These leaf parts were left at room temperature and observed and photographed 588

every 10 min to examine their dehydration. At the tillering stage, the same leaf parts of NPB 589

and es1-1 were quickly weighed (W1), and the total area (S) was measured. Moreover, the 590

weights of the leaf blade (W2, W3, and W4) were also measured every 1 h. The formula 591

(W1-W2) S-1 was used to calculate the rate of water loss. Accordingly, the rate of water loss 592

at different time points was obtained. 593

In vivo detection: After accelerating germination, the wild-type and es1-1 seeds were 594

cultured in fine sand and watered twice a day (in the morning and evening). At the 1–2-leaf 595

stage, rice seedlings were washed off and wrapped in a long sponge, then placed in a closed 596

bottle with clean water. At the 3-leaf stage, clean water was replaced by complete nutrient 597

solution. After the seedlings developed new roots, all the bottles were filled with a sufficient 598

volume of nutrient solution, and the level was marked for subsequent measurement. The 599

leaves were weighed on days 1 (W1), 4 (W2), 8 (W3), and 14 (W4). The corresponding leaf 600

areas were also measured (S2, S3, and S4). Water loss per unit of time in 4 days was 601

calculated as (W1 − W2) S2-1. Six plants were used for every time interval measurement (the 602

results are presented as mean values). Analogously, (W1 − W3) S3-1 was the amount of water 603

loss per unit of time in 8 days, and (W1 − W4) S4-1 was the amount of water loss per unit of 604

time in 14 days. 605



22

Measurement of Root Traits 606

Hydroponic experiments were conducted using the wild-type and es1-1 plants. The seeds 607

were soaked for two days, during which time the water was changed once. Next, the seeds 608

were transferred into a germination box to accelerate germination. Three days later, seeds 609

with radicals breaking through the testa were transferred into fine sand for cultivation. After 610

incubation for 7 days, the seedlings were washed carefully to avoid damage to the roots. The 611

plants were transferred into a black bucket containing tap water. After the transition, the 612

plants were supplied with complete nutrient solution. The seedlings entered the two-leaf stage 613

after three days. At the 5-leaf stage, seedlings of the mutant and wild-type plants (10 each) 614

were taken out for root measurements. The hydroponic seedlings were rinsed and placed in a 615

transparent rectangular box containing single-distilled water and loaded onto a scanner 616

(ScanWizard Pro: ScanMarker 1000XL) for transparent scanning. The obtained images were 617

loaded into Win-RHIZO. Pro. V. 2002c for data analysis, and the results were exported to 618

MS Excel 2011 (Microsoft, USA) for analysis. 619

620



23

621 Accession Numbers 622

Sequence data from this article are available at the NBCI website 623

(http:www.ncbi.nlm.nih.gov) with the accession numbers: LOC_Os01g11040 624

(NP_001172227.1), OB01G1689 (XP_006643892.1), Bradi2g06610(XP_003565325.1), 625

Oryza_sativa_indica (OsI_00845), Setaria italica (Si000056m.g), Hordeum vulgare var. 626

distichum (M0XEC2), Aegilops tauschii (F775_07293), Triticum aestivum (W5CZS7), Zea 627

mays (ZEAMMB73_679274), Triticum urartu (TRIUR3_31093), Musa acuminata subsp. 628

Malaccensis (M0UB73), Medicago truncatula (MTR_8g086300), Theobroma cacao 629

(TCM_029698), Phaseolus vulgaris (PHAVU_002G238500g), Jatropha curcas 630

(JCGZ_21566), Glycine max (I1K3Z5), Populus trichocarpa (POPTR_0004s05600g), 631

Prunus persica (PRUPE_ppa000443mg), Citrus sinensis (CISIN_1g001053mg), Citrus 632

clementina (CICLE_v10014081mg), Eucalyptus grandis (EUGRSUZ_D00489), Solanum 633

lycopersicum (Solyc02g076840.2), Erythranthe guttata (MIMGU_mgv1a000504mg), Vitis 634

vinifera (VIT_10s0003g01270), Ricinus communis (RCOM_0850090), Amborella trichopoda 635

(AMTR_s00021p00061660), Morus notabilis (L484_002198), Arabidopsis lyrata 636

subsp.(Lyrata ARALYDRAFT_903078). 637

638

Supplemental Data 639

Supplemental Table 1. Allelic analysis of es1-1 and es1-2. 640

Supplemental Table 2: Phenotypic data of NPB and es1-1. 641

Supplemental Table 3. Reciprocal cross experiments between es1-1 and three crop strains 642

(ZH11, CJ06, and NJ6). 643

Supplemental Table 4. Primers used for PCR in this study. 644

Supplemental Figure 1. Phenotype of allelic mutants. 645

A, wild-type; bar = 10 cm. B, allelic mutants; bar = 10 cm (left, es1-1; right, es1-2). C, 646

Leaves of allelic mutants; bar = 5 cm (left, es1-1; right, es1-2). D, Difference in tiller number 647

between es1-1 and es1-2. E, Difference of plant height between es1-1 and es1-2. F-G, 648

Expression level of SGR and esl85 between NPB and es1-1. The results are given as means of 649

three independent assays, and error bars indicate SD. *, ** significant at the level of 5% and 650

1%, respectively. 651

Supplemental Figure 2. Comparison of guttation between wild-type and es1-1 plants. NPB 652

leaf showing guttation drops at the point of emergence (adaxial side). 653



24

654

ACKNOWLEDGEMENTS 655

We sincerely thank Prof.Jianru Zuo (Institute of Genetics and Developmental Biology, 656

Chinese Academy of Sciences) for sharing unpublished data. This work was supported by 657

grants from the National Natural Science Foundation of China (31201183, 31221004, 658

31171531, 31171520, 91435105) and the State Key Basic Research Program 659

(2013CBA01403), the Ministry of Agriculture of China for transgenic research 660

(No.2013ZX08009003-001), China Postdoctoral Science Foundation (2014M561108). 661

662

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growth stage and grain yield of rice. Rice Sci 19(1): 44-48. 826

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resistance by regulating stress-induced wax deposition in rice. Proc Natl Acad Sci USA 828

110: 17790-17795 829

830

831

832



30

833

Table 1. Comparison of mineral contents between wild-type and es1-1 plants. 834

Cu(mg kg-1) Fe(mg kg-1) Mn(mg kg-1) Zn(mg kg-1)

root NPB 23.5±3.83 3757.7±122.55 17.75±1.75 28.49±1.12 es1-1 446.3±18.52** 18155.3±326.27** 58.97±3.88** 91.26±5.88**

culm NPB 8.61±1.21 35.52±3.7 32.19±1.3 28.75±1.81 es1-1 20.18±4.7** 46.05±3.54** 147.99±10.06** 85.83±6.35**

shealth NPB 6.59±1.15 136.2±8.59 92.331±5.9 42.52±3.4 es1-1 16.88±2.43** 240.2±14.65** 582.2±13.22** 65.36±7.92**

old leaf

NPB 9.32±2.1 228.8±15.1 100.01±7.1 29.89±2.56 es1-1 18.27±3.88** 358.3±21.94** 719.05±34.8** 64.04±7.5**

young leaf

NPB 8.02±1.16 102.1±6.78 27.51±3.32 30.48±3.44 es1-1 17.07±2.91** 223.1±11.4** 175.81±12.24** 62.22±4.28**

seed NPB 4.26±0.64 4.05±0.35 31.62±2.86 24.23±2.6 es1-1 5.91±0.72** 6.98±1.06** 50.36±4.1** 53.13±8.12**

The results are given as mean ± SD of three independent assays. 835

*, ** significant at the level of 5% and 1%, respectively 836

837

Figures and Legends 838

Table 1. Comparison of mineral contents between wild-type and es1-1 plants. 839

Figure 1. Phenotypes of wild-type and es1-1 plants. 840

A, Plants in the seedling stage. Wild-type (NPB, left) and es1-1 (right) plants; bar = 3 cm. B, 841

Plants at the heading stage. Wild-type (NPB, left) and es1-1 (right) plants; bar = 10 cm. C, 842

Nitroblue tetrazolium (NBT) staining (up: NPB, left; es1-1, right); Diaminobenzidine (DAB) 843

staining (down: NPB, left; es1-1, right). D, Malondialdehyde (MDA) contents at the seedling 844

stage. (NPB, left; es1-1, right). E, Panicle rachis (NPB, left; es1-1, right); bar = 5 cm. F, Leaf 845

at different parts (NPB, left; es1-1, right); from left to right, internode length of the first to 846

top, internode length of the second to top, internode length of third to top, and internode 847

length of fourth to top; bar = 3 cm. G, Grain size (NPB, up; es1-1, down); bar = 1 mm. H, 848

Chloroplasts, observed by transmission electron microscopy; (NPB, up; es1-1, down); bar = 849

0.5 μm. 850

851

Figure 2. Map-based cloning of ES1, and phenotype of es1-1 complementation transgenic 852

line. 853



31

A, Location of es1-1 on rice chromosome 1. B, Coarse linkage map of es1-1. C, es1-1 gene 854

structure. D, Reverse transcription of es1-1. E, Schematic diagram of es1-1 and mutated 855

proteins encoded by es1-1 and es1-2. F, Phenotype of complementation transgenic lines; es1-856

1 plant (left), Wild-type (NPB, middle) and transgenic line (right), bar = 10 cm. 857

858

Figure 3. ES1 is a SCAR homolog. 859

A, Leaf margin (left, NPB; right, es1-1). B, Trichome phenotype (macro hairs; upper, NPB; 860

down, es1-1). C, D, F-actin organization was visualized with Alexa Fluor 488-phalloidin in 861

root cells of wild type and es1. Over 40 roots were used in this analysis. Bar =5 μm (C, NPB; 862

D, es1-1). Arrows indicate the continuity of F-actin. E, Phylogenetic tree of SCAR-like 2 863

protein in several species. 864

865

Figure 4. Expression of ES1 and subcellular localization of ES1. 866

A–E, GUS staining of leaf (A), leaf sheath (B), fibrous root (C), stamen (D), and culm 867

vascular bundles (E). F, Quantitative real-time PCR analysis of ES1 expression in different 868

tissues at the tillering stage (T) and heading (H) stage. The results are given as means of three 869

independent assays, and each error bar represents the percent standard deviation of the mean. 870

G–L, GFP fluorescence visualized by confocal microscopy. Transient expression of eGFP 871

(G) and eGFP–ES1 cDNA (H) in epidermal cells of onion. 35S::eGFP::ES1 cDNA and 872

35S::GFP were transiently expressed in onion epidermal cells. Transient expression of eGFP 873

in epidermal cells (I) and protoplasts (K) and expression of eGFP–ES1 in epidermal cells (J) 874

and protoplasts (L) of Nicotiana benthamiana leaves. 35S::eGFP::ES1 and 35S::GFP were 875

transiently expressed in N. benthamiana leaves. 876

877

Figure 5. Observation of stomata between NPB and es1-1. 878

A, Stomata density of the wild-type (left) and es1-1 (right) leaves. Bar = 30 µm. the red 879

triangle indicate the position of stomata. B, Statistical analysis of stomatal parameters, such 880

as stomata density, partially-open stomata, stomatal conductance, transpiration rate. C, 881

Morphological characteristics (left) and maximum opening size (right) of stomata between 882

wild-type (up) and es1-1 (down) plants. Bar = 5 µm D, Comparison of water loss rate 883

between wild-type and es1-1 plants with and without 300um ABA treatment at the 3-leaf-884

stage. E, qRT-PCR analysis of stomata density related genes (OsTMM, OsSCRM, OsSDD1, 885

OsYODA2), ES1, and some ABA response-related genes (OsDREB1A, OsDREB2A, 886

OsMYB2,OsABI4, OsABI5, OsABF4) in WT and es1-1 leaves before and after 300um ABA 887



32

treatment at the 3-leaf-stage. The values were normalized to the Actin1 gene. ** indicates 888

significance (t-test) at the P<0.01. Different letters indicate significant difference at the 1% 889

level (Duncan multiple range test) 890

891

892

Figure 6. Observation of water loss rate between wild-type and es1-1 plants. 893

A, Water loss rate of detached leaves at the seedling stage (left, NPB; right, es1-1). B, Water 894

loss rate of detached leaves at the tillering stage. C, Water loss per unit of time of living 895

leaves between NPB and es1-1 plants at the tillering stage. Error bars indicate SD (n = 15). 896

Asterisks indicate the significance of differences between NPB and es1-1 plants, as 897

determined by t-test. *0.01 ≤ P < 0.05, **P < 0.01. 898

899

Figure 7. Phenotype comparison of the roots between NPB and es1-1 plants. 900

A, Root scanning of NPB plants; bar = 5 cm. B, Root scanning of es1-1 plants; bar = 5 cm. 901

C, Enlarged figure of roots in NPB plants; bar = 5 cm. D, Enlarged figure of root in es1-1 902

plants; bar = 5 cm. E–J, Statistical analysis of the main root length (E), total root length (F), 903

total area of the root (G), average diameter of the root (H), total volume of the root (I), total 904

number of fibrous roots (J) of NPB and es1-1 plants. The results are given as means of three 905

independent assays, and error bars indicate SD. Asterisks indicate the significance of 906

differences between NPB and es1-1 plants, as determined by t-test. *0.01 ≤ P < 0.05, **P < 907

0.01. 908

909

Figure 8. Number of vascular bundles and conduits in wild-type and es1-1 plants. 910

A, Number of vascular bundles in NPB plants. B, Number of vascular bundles in es1-1 911

plants. C, Comparison of the number of vascular bundles between NPB and es1-1 plants. D, 912

Number of conduits in NPB plants. E, Number of conduits in es1-1 plants. F, Comparison of 913

the number of conduits between NPB and es1-1 plants. G, Detection of the water potential 914

value in WT and es1-1. Relative water potential value in different tissues at seedling stage of 915

WT and es1-1 analyzed by WP4-T Dewpoint PotentiaMeter. The results are given as means 916

of three independent assays, and error bars indicate SD. *, ** significant at the level of 5% 917

and 1%, respectively. 918 919



1

Figure 1. Phenotypes of wild-type and es1-1 plants.

A, Plants in the seedling stage. Wild-type (NPB, left) and es1-1 (right) plants; bar = 3 cm. B,

Plants at the heading stage. Wild-type (NPB, left) and es1-1 (right) plants; bar = 10 cm. C,

Nitroblue tetrazolium (NBT) staining (up: NPB, left; es1-1, right); Diaminobenzidine (DAB)

staining (down: NPB, left; es1-1, right). D, Malondialdehyde (MDA) contents at the seedling

stage. (NPB, left; es1-1, right). E, Panicle rachis (NPB, left; es1-1, right); bar = 5 cm. F, Leaf

at different parts (NPB, left; es1-1, right); from left to right, internode length of the first to top,

internode length of the second to top, internode length of third to top, and internode length of

fourth to top; bar = 3 cm. G, Grain size (NPB, up; es1-1, down); bar = 1 mm. H, Chloroplasts,

observed by transmission electron microscopy; (NPB, up; es1-1, down); bar = 0.5 μm.



1

Figure 2. Map-based cloning of ES1, and phenotype of es1-1 complementation transgenic

line.

A, Location of es1-1 on rice chromosome 1. B, Coarse linkage map of es1-1. C, es1-1 gene

structure. D, Reverse transcription of es1-1. E, Schematic diagram of es1-1 and mutated

proteins encoded by es1-1 and es1-2. F, Phenotype of complementation transgenic lines;

es1-1 plant (left), Wild-type (NPB, middle) and transgenic line (right), bar = 10 cm.



1

Figure 3. ES1 is a SCAR homolog.

A, Leaf margin (left, NPB; right, es1-1). B, Trichome phenotype (macro hairs; upper, NPB;

down, es1-1). C, D, F-actin organization was visualized with Alexa Fluor 488-phalloidin in

root cells of wild type and es1. Over 40 roots were used in this analysis. Bar =5 μm (C, NPB;

D, es1-1). Arrows indicate the continuity of F-actin. E, Phylogenetic tree of SCAR-like 2

protein in several species.



1

Figure 4. Expression of ES1 and subcellular localization of ES1.

A–E, GUS staining of leaf (A), leaf sheath (B), fibrous root (C), stamen (D), and culm

vascular bundles (E). F, Quantitative real-time PCR analysis of ES1 expression in different

tissues at the tillering stage (T) and heading stage (H). The results are given as means of three

independent assays, and each error bar represents the percent standard deviation of the mean.

G–L, GFP fluorescence visualized by confocal microscopy. Transient expression of eGFP (G)

and eGFP–ES1 cDNA (H) in epidermal cells of onion. 35S::eGFP::ES1 cDNA and

35S::GFP were transiently expressed in onion epidermal cells. Transient expression of eGFP

in epidermal cells (I) and protoplasts (K) and expression of eGFP–ES1 in epidermal cells (J)

and protoplasts (L) of Nicotiana benthamiana leaves. 35S::eGFP::ES1 and 35S::GFP were



2

transiently expressed in N. benthamiana leaves.



1

Figure 5. Observation of stomata between NPB and es1-1.

A, Stomata density of the wild-type (left) and es1-1 (right) leaves. Bar = 30 µm. the red

triangle indicate the position of stomata. B, Statistical analysis of stomatal parameters, such

as stomata density, partially-open stomata, stomatal conductance, transpiration rate. C,

Morphological characteristics (left) and maximum opening size (right) of stomata between

wild-type (up) and es1-1 (down) plants. Bar = 5 µm D, Comparison of water loss rate

between wild-type and es1-1 plants with and without 300um ABA treatment at the

3-leaf-stage. E, qRT-PCR analysis of stomata density related genes (OsTMM, OsSCRM,

OsSDD1, OsYODA2) and ES1, and some ABA response-related genes (OsDREB1A,

OsDREB2A, OsMYB2,OsABI4, OsABI5, OsABF4) in WT and es1-1 leaves before and after

300um ABA treatment at the 3-leaf-stage. The values were normalized to the Actin1 gene. **



2

indicates significance (t-test) at the P<0.01. Different letters indicate significant difference at

the 1% level (Duncan multiple range test)



1

Figure 6. Observation of water loss rate between wild-type and es1-1 plants.

A, Water loss rate of detached leaves at the seedling stage (left, NPB; right, es1-1). B, Water

loss rate of detached leaves at the tillering stage. C, Water loss per unit of time of living

leaves between NPB and es1-1 plants at the tillering stage. Error bars indicate SD (n = 15).

Asterisks indicate the significance of differences between NPB and es1-1 plants, as

determined by t-test. *0.01 ≤ P < 0.05, **P < 0.01.



1

Figure 7. Phenotype comparison of the roots between NPB and es1-1 plants.

A, Root scanning of NPB plants; bar = 5 cm. B, Root scanning of es1-1 plants; bar = 5 cm.

C, Enlarged figure of roots in NPB plants; bar = 5 cm. D, Enlarged figure of root in es1-1

plants; bar = 5 cm. E–J, Statistical analysis of the main root length (E), total root length (F),

total area of the root (G), average diameter of the root (H), total volume of the root (I), total

number of fibrous roots (J) of NPB and es1-1 plants. The results are given as means of three

independent assays, and error bars indicate SD. Asterisks indicate the significance of

differences between NPB and es1-1 plants, as determined by t-test. *0.01 ≤ P < 0.05, **P <

0.01.



1

Figure 8. Number of vascular bundles and conduits in wild-type and es1-1 plants.

A, Number of vascular bundles in NPB plants. B, Number of vascular bundles in es1-1 plants.

C, Comparison of the number of vascular bundles between NPB and es1-1 plants. D, Number

of conduits in NPB plants. E, Number of conduits in es1-1 plants. F, Comparison of the

number of conduits between NPB and es1-1 plants. G, Detection of the water potential value

in WT and es1-1. Relative water potential value in different tissues at seedling stage of WT

and es1-1 analyzed by WP4-T Dewpoint PotentiaMeter. The results are given as means of

three independent assays, and error bars indicate SD. *, ** significant at the level of 5% and

1%, respectively.



1

Table 1. Comparison of mineral contents between wild-type and es1-1 plants. Cu(mg kg-1) Fe(mg kg-1) Mn(mg kg-1) Zn(mg kg-1)

root NPB 23.5±3.83 3757.7±122.55 17.75±1.75 28.49±1.12 es1-1 446.3±18.52** 18155.3±326.27** 58.97±3.88** 91.26±5.88**

culm NPB 8.61±1.21 35.52±3.7 32.19±1.3 28.75±1.81 es1-1 20.18±4.7** 46.05±3.54** 147.99±10.06** 85.83±6.35**

shealth NPB 6.59±1.15 136.2±8.59 92.331±5.9 42.52±3.4 es1-1 16.88±2.43** 240.2±14.65** 582.2±13.22** 65.36±7.92**

old leaf

NPB 9.32±2.1 228.8±15.1 100.01±7.1 29.89±2.56 es1-1 18.27±3.88** 358.3±21.94** 719.05±34.8** 64.04±7.5**

young leaf

NPB 8.02±1.16 102.1±6.78 27.51±3.32 30.48±3.44 es1-1 17.07±2.91** 223.1±11.4** 175.81±12.24** 62.22±4.28**

seed NPB 4.26±0.64 4.05±0.35 31.62±2.86 24.23±2.6 es1-1 5.91±0.72** 6.98±1.06** 50.36±4.1** 53.13±8.12**

The results are given as mean ± SD of three independent assays.

*, ** significant at the level of 5% and 1%, respectively



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Jäger K, Fábián A, Eitel G, Szabó L, Deák C, Barnabás B, Papp I (2014) A morpho-physiological approach differentiates breadwheat cultivars of contrasting tolerance under cyclic water stress. Plant Physiol 171: 1256-1266


Grill E, Ziegler H (1998) A plant's dilemma. Science 282, 252 -253. www.plantphysiol.orgon September 4, 2020 - Published by Downloaded from Copyright © 2015 American Society of Plant Biologists. All rights reserved.

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http://scholar.google.com/scholar?as_q=DISTORTED3/SCAR2 is a putative Arabidopsis WAVE complex subunit that activates the Arp2/3 complex and is required for epidermal morphogenesis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Basu&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28spp%2E indica and its mutants induced by low%2Denergy ion beam%2E Rice Sci%5BTitle%5D%29 AND 20%5BVolume%5D AND 213%5BPagination%5D AND Boonrueng N%2C Anuntalabhochai S%2C Jampeetong A%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=Leaf pubescence as a possibility to increase water use efficiency by promoting condensation&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Konrad&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

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http://scholar.google.com/scholar?as_q=Arabidopsis BRICK1/HSPC300 is an essential WAVE-Complex subunit that selectively stabilizes the Arp2/3 activator SCAR2&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Le&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

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

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http://scholar.google.com/scholar?as_q=ZEBRA-NECROSIS, a thylakoid-bound protein, is critical for the photoprotection of developing chloroplasts during early leaf development&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Li&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Physiol%5BTitle%5D%29 AND 132%5BVolume%5D AND 2034%5BPagination%5D AND Li S%2C Blanchoin L%2C Yang Z%2C Lord EM%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=The putative Arabidopsis Arp2/3 complex controls leaf cell morphogenesis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Li&as_ylo=2003&as_allsubj=all&hl=en&c2coff=1


Li Z, Zhang Y, Liu L, Liu Q, Bi Z, Yu N, Cheng S, Cao L (2014) Fine mapping of the lesion mimic and early senescence 1(lmes1) inrice (Oryza sativa). Plant Physiol Biochem 80: 300-307


Livak K, Schmittgen T (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-??Ct method.Methods 25: 402-408.


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Lv F (2010) Optimization for Agrobacterium Tumefaciens-mediated transformation system for exogenous genes of tobacco. JAnhui Agri Sci 38: 10065-10066 (in Chinese with English abstract)


Mathur J, Spielhofer P, Kost B, Chua N-H (1999) The actin cytoskeleton is required to elaborate and maintain spatial patterningduring trichome cell morphogenesis in Arabidopsis thaliana. Development 126: 5559-5568


Mathur J, Mathur N, Kernebeck B, Hülskamp M (2003) Mutations in actin-related proteins 2 and 3 affect cell shape development inArabidopsis. Plant Cell 15: 1632-1645


Moradi F, Iamail A.(2007)Responses of photosynthesis, chlorophyII fluorescence and ROS-scavenging systems to salt stressduring seedling and reproductive stages in rice. Ann Bot 99:1161-1173


Nguyen HT, Babu RC, Blum A (1997) Breeding for drought resistance in rice: physiology and molecular genetics considerations.Crop Sci 37: 1426-1434


Park S, Yu J, Park J, Li J, Yoo S, Lee N, Lee S, Jeong S, Seo H, Koh H, Jeon J, Park Y, Paek N (2007) The senescence-inducedstaygreen protein regulates chlorophyII degradation. Plant Cell 19: 1649-1664


Qiu J-L, Jilk R, Marks MD, Szymanski DB (2002) The Arabidopsis SPIKE1 gene is required for normal cell shape control and tissuedevelopment. Plant Cell 14: 101-118


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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Ct method%2E Methods%5BTitle%5D%29 AND 25%5BVolume%5D AND 402%5BPagination%5D AND Livak K%2C Schmittgen T%5BAuthor%5D&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28 Chin J Rice Sci%5BTitle%5D%29 AND 15%5BVolume%5D AND 209%5BPagination%5D AND Luo L%2C Zhang Q%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Luo L, Zhang Q (2001) The status and strategy on drought resistance of rice (Oryza sativa L.) Chin J Rice Sci 15: 209-214 (in Chinese with English abstract)

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

http://scholar.google.com/scholar?as_q=The status and strategy on drought resistance of rice (Oryza sativa L&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The status and strategy on drought resistance of rice (Oryza sativa L&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Luo&as_ylo=2001&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28J Anhui Agri Sci%5BTitle%5D%29 AND 38%5BVolume%5D AND 10065%5BPagination%5D AND Lv F%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Lv F (2010) Optimization for Agrobacterium Tumefaciens-mediated transformation system for exogenous genes of tobacco. J Anhui Agri Sci 38: 10065-10066 (in Chinese with English abstract)

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

http://scholar.google.com/scholar?as_q=Optimization for Agrobacterium Tumefaciens-mediated transformation system for exogenous genes of tobacco&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Optimization for Agrobacterium Tumefaciens-mediated transformation system for exogenous genes of tobacco&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Lv&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Development%5BTitle%5D%29 AND 126%5BVolume%5D AND 5559%5BPagination%5D AND Mathur J%2C Spielhofer P%2C Kost B%2C Chua N%2DH%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Mathur J, Spielhofer P, Kost B, Chua N-H (1999) The actin cytoskeleton is required to elaborate and maintain spatial patterning during trichome cell morphogenesis in Arabidopsis thaliana. Development 126: 5559-5568

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

http://scholar.google.com/scholar?as_q=The actin cytoskeleton is required to elaborate and maintain spatial patterning during trichome cell morphogenesis in Arabidopsis thaliana&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The actin cytoskeleton is required to elaborate and maintain spatial patterning during trichome cell morphogenesis in Arabidopsis thaliana&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Mathur&as_ylo=1999&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell%5BTitle%5D%29 AND 15%5BVolume%5D AND 1632%5BPagination%5D AND Mathur J%2C Mathur N%2C Kernebeck B%2C H�lskamp M%5BAuthor%5D&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Mutations in actin-related proteins 2 and 3 affect cell shape development 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

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Ann Bot%5BTitle%5D%29 AND 99%5BVolume%5D AND 1161%5BPagination%5D AND Moradi F%2C Iamail A%2E%5BAuthor%5D&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Responses of photosynthesis, chlorophyII fluorescence and ROS-scavenging systems to salt stress during seedling and reproductive stages in rice&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Responses of photosynthesis, chlorophyII fluorescence and ROS-scavenging systems to salt stress during seedling and reproductive stages in rice&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Moradi&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Crop Sci%5BTitle%5D%29 AND 37%5BVolume%5D AND 1426%5BPagination%5D AND Nguyen HT%2C Babu RC%2C Blum A%5BAuthor%5D&dopt=abstract

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

http://scholar.google.com/scholar?as_q=Breeding for drought resistance in rice: physiology and molecular genetics considerations&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Breeding for drought resistance in rice: physiology and molecular genetics considerations&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Nguyen&as_ylo=1997&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell%5BTitle%5D%29 AND 19%5BVolume%5D AND 1649%5BPagination%5D AND Park S%2C Yu J%2C Park J%2C Li J%2C Yoo S%2C Lee N%2C Lee S%2C Jeong S%2C Seo H%2C Koh H%2C Jeon J%2C Park Y%2C Paek N%5BAuthor%5D&dopt=abstract

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

http://scholar.google.com/scholar?as_q=The senescence-induced staygreen protein regulates chlorophyII degradation&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The senescence-induced staygreen protein regulates chlorophyII degradation&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Park&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell%5BTitle%5D%29 AND 14%5BVolume%5D AND 101%5BPagination%5D AND Qiu J%2DL%2C Jilk R%2C Marks MD%2C Szymanski DB%5BAuthor%5D&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28J Exp Bot%5BTitle%5D%29 AND 52%5BVolume%5D AND 2023%5BPagination%5D AND Riederer M%2C Schreiber%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=Protecting against water loss: analysis of the barrier properties of plant cuticles&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Riederer&as_ylo=2001&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell Physiol%5BTitle%5D%29 AND 45%5BVolume%5D AND 813%5BPagination%5D AND Saedler R%2C Mathur N%2C Srinivas BP%2C Kernebeck B%2C H�lskamp M%2C Mathur J%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Saedler R, Mathur N, Srinivas BP, Kernebeck B, H�lskamp M, Mathur J (2004) Actin control over microtubules suggested by DISTORTED2 encoding the Arabidopsis ARPC2 subunit homolog. Plant Cell Physiol 45: 813-822

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

http://scholar.google.com/scholar?as_q=Actin control over microtubules suggested by DISTORTED2 encoding the Arabidopsis ARPC2 subunit homolog&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Actin control over microtubules suggested by DISTORTED2 encoding the Arabidopsis ARPC2 subunit homolog&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Saedler&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

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Shao G, Chen M, Wang D, Xu C, Mou R, Cao Z, Zhang X (2008) Iron manure regulation of cadmium accumulation in rice. Chin SciBull (C): Life Sci 38: 180-187


Silva D, Favreau R, Auzmendi I, Dejong T(2011) Linking water stress effects on carbon partitioning by introducing a xylem circuitinto L-PEACH. Ann Bot 108:1135-1145


Smith S, Smet I (2012) Root system architecture: insights from Arabidopsis and cereal crops. Phil.Trans.R.Soc.B 367:1441-1452Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Svenningsson M (1988) Epi- and intracuticular lipids and cuticular transpiration rates of primary leaves of eight barley (Hordeumvulgare) cultivars. Plant Physiol 73: 512-517


Svitkina TM, Borisy GG (1999) Arp2/3 complex and actin depolymerizing factor/cofilin in dendritic organization and treadmilling ofactin filament array in lamellipodia. J Cell Biol 145: 1009-1026


Szymanski DB, Marks MD, Wick SM (1999) Organized F-Actin is essential for normal trichome morphogenesis in Arabidopsis. PlantCell 11: 2331-2347


Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6:Molecular evolutionary genetics analysis version6.0. Mol BioEvol 30:2725-2729


Tsuzuki T, Takahashi K, Tomiyama M, Inoue S, Kinoshita T (2013) Overexpression of the Mg-chelatase H subunit in guard cellsconfers drought tolerance via promotion of stomatal closure in Arabidopsis thaliana. Front Plant Sci 4: 440


Von G, Berger D, Altmann T (2002) The subtilisin-like serine protease SDD1 mediates cell-to-cell signaling during Arabidopsisstomatal development. Plant Cell 14: 1527-1539


Wang Y, Wan L, Zhang L, Zhang Z, Zhang H, Quan R, Zhou S, Huang R (2012) An ethylene response factor OsWR1 responsive todrought stress transcriptionally activates wax synthesis related genes and increases wax production in rice. Plant Mol Biol 78:275-288


Wi SJ, Jang SJ, Park KY (2010) Inhibition of biphasic ethylene production enhances tolerance to abiotic stress by reducing theaccumulation of reactive oxygen species in Nicotiana tabacum. Mol Cells 30: 37-49


Xiao Y, Chen Y, Wang X (2003) Filaments skeleton in guard cell. Chin Bull Bot 20: 489-494Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Xu H, Gauthier L, Gossenlin A (1995) Stomatal and cuticular transpiration of greenhouse tomato plants in response to highsolution electrical conductivity and low soil water content. J Amer Soc Hort Sci 120: 417-422

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http://search.crossref.org/?page=1&rows=2&q=Shang Y, Yan L, Liu Z, Cao Z, Mei C, Xin Q, Wu F, Wang X, Du S, Jiang T, Zhang X, Zhao R, Sun H, Liu R, Yu Y, Zhang D (2010) The Mg-chelatase H subunit of Arabidopsis antagonizes a group of WRKY transcription repressors to relieve ABA-responsive genes of inhibition. Plant Cell 22: 1909-1935

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

http://scholar.google.com/scholar?as_q=The Mg-chelatase H subunit of Arabidopsis antagonizes a group of WRKY transcription repressors to relieve ABA-responsive genes of inhibition&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The Mg-chelatase H subunit of Arabidopsis antagonizes a group of WRKY transcription repressors to relieve ABA-responsive genes of inhibition&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Shang&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Chin Sci Bull C%3A Life Sci%5BTitle%5D%29 AND 38%5BVolume%5D AND 180%5BPagination%5D AND Shao G%2C Chen M%2C Wang D%2C Xu C%2C Mou R%2C Cao Z%2C Zhang X%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Shao G, Chen M, Wang D, Xu C, Mou R, Cao Z, Zhang X (2008) Iron manure regulation of cadmium accumulation in rice. Chin Sci Bull (C): Life Sci 38: 180-187

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

http://scholar.google.com/scholar?as_q=Iron manure regulation of cadmium accumulation in rice&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Iron manure regulation of cadmium accumulation in rice&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Shao&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Ann Bot%5BTitle%5D%29 AND 108%5BVolume%5D AND 1135%5BPagination%5D AND Silva D%2C Favreau R%2C Auzmendi I%2C Dejong T%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Silva D, Favreau R, Auzmendi I, Dejong T(2011) Linking water stress effects on carbon partitioning by introducing a xylem circuit into L-PEACH. Ann Bot 108:1135-1145

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

http://scholar.google.com/scholar?as_q=Linking water stress effects on carbon partitioning by introducing a xylem circuit into L-PEACH&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Linking water stress effects on carbon partitioning by introducing a xylem circuit into L-PEACH&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Silva&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Phil%2ETrans%2ER%2ESoc%2EB%5BTitle%5D%29 AND 367%5BVolume%5D AND 1441%5BPagination%5D AND Smith S%2C Smet I%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Smith S, Smet I (2012) Root system architecture: insights from Arabidopsis and cereal crops. Phil.Trans.R.Soc.B 367:1441-1452

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

http://scholar.google.com/scholar?as_q=Root system architecture: insights from Arabidopsis and cereal crops&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Root system architecture: insights from Arabidopsis and cereal crops&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Smith&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Physiol%5BTitle%5D%29 AND 73%5BVolume%5D AND 512%5BPagination%5D AND Svenningsson M%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Svenningsson M (1988) Epi- and intracuticular lipids and cuticular transpiration rates of primary leaves of eight barley (Hordeum vulgare) cultivars. Plant Physiol 73: 512-517

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

http://scholar.google.com/scholar?as_q=Epi- and intracuticular lipids and cuticular transpiration rates of primary leaves of eight barley (Hordeum vulgare) cultivars&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Epi- and intracuticular lipids and cuticular transpiration rates of primary leaves of eight barley (Hordeum vulgare) cultivars&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Svenningsson&as_ylo=1988&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28J Cell Biol%5BTitle%5D%29 AND 145%5BVolume%5D AND 1009%5BPagination%5D AND Svitkina TM%2C Borisy GG%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Svitkina TM, Borisy GG (1999) Arp2/3 complex and actin depolymerizing factor/cofilin in dendritic organization and treadmilling of actin filament array in lamellipodia. J Cell Biol 145: 1009-1026

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

http://scholar.google.com/scholar?as_q=Arp2/3 complex and actin depolymerizing factor/cofilin in dendritic organization and treadmilling of actin filament array in lamellipodia&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell%5BTitle%5D%29 AND 11%5BVolume%5D AND 2331%5BPagination%5D AND Szymanski DB%2C Marks MD%2C Wick SM%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Szymanski DB, Marks MD, Wick SM (1999) Organized F-Actin is essential for normal trichome morphogenesis in Arabidopsis. Plant Cell 11: 2331-2347

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

http://scholar.google.com/scholar?as_q=Organized F-Actin is essential for normal trichome morphogenesis in Arabidopsis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Organized F-Actin is essential for normal trichome morphogenesis in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Szymanski&as_ylo=1999&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28MEGA%5BTitle%5D%29 AND 6%5BVolume%5D AND Molecular evolutionary genetics analysis version6%2E0%2E Mol Bio Evol 30%3A2725%5BPagination%5D AND Tamura K%2C Stecher G%2C Peterson D%2C Filipski A%2C Kumar S%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6:Molecular evolutionary genetics analysis version6.0. Mol Bio Evol 30:2725-2729

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

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

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Overexpression of the Mg%2Dchelatase H subunit in guard cells confers drought tolerance via promotion of stomatal closure in Arabidopsis thaliana%2E%5BTitle%5D%29 AND Tsuzuki T%2C Takahashi K%2C Tomiyama M%2C Inoue S%2C Kinoshita T%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Tsuzuki T, Takahashi K, Tomiyama M, Inoue S, Kinoshita T (2013) Overexpression of the Mg-chelatase H subunit in guard cells confers drought tolerance via promotion of stomatal closure in Arabidopsis thaliana. Front Plant Sci 4: 440

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

http://scholar.google.com/scholar?as_q=Overexpression of the Mg-chelatase H subunit in guard cells confers drought tolerance via promotion of stomatal closure in Arabidopsis thaliana.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Overexpression of the Mg-chelatase H subunit in guard cells confers drought tolerance via promotion of stomatal closure in Arabidopsis thaliana.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Tsuzuki&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell%5BTitle%5D%29 AND 14%5BVolume%5D AND 1527%5BPagination%5D AND Von G%2C Berger D%2C Altmann T%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Von G, Berger D, Altmann T (2002) The subtilisin-like serine protease SDD1 mediates cell-to-cell signaling during Arabidopsis stomatal development. Plant Cell 14: 1527-1539

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

http://scholar.google.com/scholar?as_q=The subtilisin-like serine protease SDD1 mediates cell-to-cell signaling during Arabidopsis stomatal development&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The subtilisin-like serine protease SDD1 mediates cell-to-cell signaling during Arabidopsis stomatal development&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Von&as_ylo=2002&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Mol Biol%5BTitle%5D%29 AND 78%5BVolume%5D AND 275%5BPagination%5D AND Wang Y%2C Wan L%2C Zhang L%2C Zhang Z%2C Zhang H%2C Quan R%2C Zhou S%2C Huang R%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Wang Y, Wan L, Zhang L, Zhang Z, Zhang H, Quan R, Zhou S, Huang R (2012) An ethylene response factor OsWR1 responsive to drought stress transcriptionally activates wax synthesis related genes and increases wax production in rice. Plant Mol Biol 78: 275-288

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

http://scholar.google.com/scholar?as_q=An ethylene response factor OsWR1 responsive to drought stress transcriptionally activates wax synthesis related genes and increases wax production in rice&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=An ethylene response factor OsWR1 responsive to drought stress transcriptionally activates wax synthesis related genes and increases wax production in rice&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wang&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Mol Cells%5BTitle%5D%29 AND 30%5BVolume%5D AND 37%5BPagination%5D AND Wi SJ%2C Jang SJ%2C Park KY%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Wi SJ, Jang SJ, Park KY (2010) Inhibition of biphasic ethylene production enhances tolerance to abiotic stress by reducing the accumulation of reactive oxygen species in Nicotiana tabacum. Mol Cells 30: 37-49

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

http://scholar.google.com/scholar?as_q=Inhibition of biphasic ethylene production enhances tolerance to abiotic stress by reducing the accumulation of reactive oxygen species in Nicotiana tabacum&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Inhibition of biphasic ethylene production enhances tolerance to abiotic stress by reducing the accumulation of reactive oxygen species in Nicotiana tabacum&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wi&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Chin Bull Bot%5BTitle%5D%29 AND 20%5BVolume%5D AND 489%5BPagination%5D AND Xiao Y%2C Chen Y%2C Wang X%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Xiao Y, Chen Y, Wang X (2003) Filaments skeleton in guard cell. Chin Bull Bot 20: 489-494

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

http://scholar.google.com/scholar?as_q=Filaments skeleton in guard cell&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Filaments skeleton in guard cell&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Xiao&as_ylo=2003&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28J Amer Soc Hort Sci%5BTitle%5D%29 AND 120%5BVolume%5D AND 417%5BPagination%5D AND Xu H%2C Gauthier L%2C Gossenlin A%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Xu H, Gauthier L, Gossenlin A (1995) Stomatal and cuticular transpiration of greenhouse tomato plants in response to high solution electrical conductivity and low soil water content. J Amer Soc Hort Sci 120: 417-422

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

http://scholar.google.com/scholar?as_q=Stomatal and cuticular transpiration of greenhouse tomato plants in response to high solution electrical conductivity and low soil water content&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Stomatal and cuticular transpiration of greenhouse tomato plants in response to high solution electrical conductivity and low soil water content&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Xu&as_ylo=1995&as_allsubj=all&hl=en&c2coff=1


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Zhang C, Mallery EL, Schlueter J, Huang S, Fan Y, Brankle S, Staiger CJ, Szymanski DB (2008) Arabidopsis SCARs functioninterchangeably to meet actin-related protein 2/3 activation thresholds during morphogenesis. Plant Cell 20: 995-1011


Zhang Q, Lin F, Mao T, Nie J, Yan M, Yuan M, Zhang W (2012) Phosphatidic Acid Regulates Microtubule Organization by Interactingwith MAP65-1 in Response to Salt Stress in Arabidopsis. Plant Cell 24:4555-4576


Zhang X, Dyachok J, Krishnakumar S, Smith LG, Oppenheimer DG (2005) IRREGULAR TRICHOME BRANCH1 in Arabidopsisencodes a plant homolog of the actin-related protein2/3 complex activator Scar/WAVE that regulates actin and microtubuleorganization. Plant Cell 17: 2314-2326


Zhou L, Ni E, Yang J, Zhou H, Liang H, Li J, Jiang D, Wang Z, Liu Z, Zhuang C (2013) Rice OsGL1-6 is involved in leaf cuticular waxaccumulation and drought resistance. PLoS One 8: e65139 1-12


Zhu LF, Yu SM, Jin QY (2012) Effects of aerated irrigation on leaf senescence at late growth stage and grain yield of rice. Rice Sci19(1): 44-48.


Zhu X, Xiong L (2013) Putative megaenzyme DWA1 plays essential roles in drought resistance by regulating stress-induced waxdeposition in rice. Proc Natl Acad Sci USA 110: 17790-17795



http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell%5BTitle%5D%29 AND 7%5BVolume%5D AND 2227%5BPagination%5D AND Yang M%2C Sack F%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yang M, Sack F (1995) The too many mouths and four lips mutations affect stomatal production in Arabidopsis. Plant Cell 7: 2227-2239

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http://scholar.google.com/scholar?as_q=The too many mouths and four lips mutations affect stomatal production in Arabidopsis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The too many mouths and four lips mutations affect stomatal production in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yang&as_ylo=1995&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28J Exp Bot%5BTitle%5D%29 AND 64%5BVolume%5D AND 569%5BPagination%5D AND You J%2C Zong W%2C Li X%2C Ning J%2C Hu H%2C Li X%2C Xiao J%2C Xiong L%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=You J, Zong W, Li X, Ning J, Hu H, Li X, Xiao J, Xiong L (2013) The SNAC1-targeted gene OsSRO1c modulates stomatal closure and oxidative stress tolerance by regulating hydrogen peroxide in rice. J Exp Bot 64: 569-583

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

http://scholar.google.com/scholar?as_q=The SNAC1-targeted gene OsSRO1c modulates stomatal closure and oxidative stress tolerance by regulating hydrogen peroxide in rice&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The SNAC1-targeted gene OsSRO1c modulates stomatal closure and oxidative stress tolerance by regulating hydrogen peroxide in rice&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=You&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Protoplasma%5BTitle%5D%29 AND 216%5BVolume%5D AND 113%5BPagination%5D AND Yu R%2C Huang R%2C Wang X%2C Yuan M%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yu R, Huang R, Wang X, Yuan M (2001) Microtubule dynamics are involved in stomatal movement of Vicia faba L. Protoplasma 216:113-118

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

http://scholar.google.com/scholar?as_q=Microtubule dynamics are involved in stomatal movement of Vicia faba L&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Microtubule dynamics are involved in stomatal movement of Vicia faba L&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yu&as_ylo=2001&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell%5BTitle%5D%29 AND 20%5BVolume%5D AND 995%5BPagination%5D AND Zhang C%2C Mallery EL%2C Schlueter J%2C Huang S%2C Fan Y%2C Brankle S%2C Staiger CJ%2C Szymanski DB%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhang C, Mallery EL, Schlueter J, Huang S, Fan Y, Brankle S, Staiger CJ, Szymanski DB (2008) Arabidopsis SCARs function interchangeably to meet actin-related protein 2/3 activation thresholds during morphogenesis. Plant Cell 20: 995-1011

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

http://scholar.google.com/scholar?as_q=Arabidopsis SCARs function interchangeably to meet actin-related protein 2/3 activation thresholds during morphogenesis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Arabidopsis SCARs function interchangeably to meet actin-related protein 2/3 activation thresholds during morphogenesis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell%5BTitle%5D%29 AND 24%5BVolume%5D AND 4555%5BPagination%5D AND Zhang Q%2C Lin F%2C Mao T%2C Nie J%2C Yan M%2C Yuan M%2C Zhang W%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhang Q, Lin F, Mao T, Nie J, Yan M, Yuan M, Zhang W (2012) Phosphatidic Acid Regulates Microtubule Organization by Interacting with MAP65-1 in Response to Salt Stress in Arabidopsis. Plant Cell 24:4555-4576


http://scholar.google.com/scholar?as_q=Phosphatidic Acid Regulates Microtubule Organization by Interacting with MAP65-1 in Response to Salt Stress in Arabidopsis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Phosphatidic Acid Regulates Microtubule Organization by Interacting with MAP65-1 in Response to Salt Stress in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell%5BTitle%5D%29 AND 17%5BVolume%5D AND 2314%5BPagination%5D AND Zhang X%2C Dyachok J%2C Krishnakumar S%2C Smith LG%2C Oppenheimer DG%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhang X, Dyachok J, Krishnakumar S, Smith LG, Oppenheimer DG (2005) IRREGULAR TRICHOME BRANCH1 in Arabidopsis encodes a plant homolog of the actin-related protein2/3 complex activator Scar/WAVE that regulates actin and microtubule organization. Plant Cell 17: 2314-2326


http://scholar.google.com/scholar?as_q=IRREGULAR TRICHOME BRANCH1 in Arabidopsis encodes a plant homolog of the actin-related protein2/3 complex activator Scar/WAVE that regulates actin and microtubule organization&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=IRREGULAR TRICHOME BRANCH1 in Arabidopsis encodes a plant homolog of the actin-related protein2/3 complex activator Scar/WAVE that regulates actin and microtubule organization&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28PLoS One%5BTitle%5D%29 AND 8%5BVolume%5D AND e65139 1%5BPagination%5D AND Zhou L%2C Ni E%2C Yang J%2C Zhou H%2C Liang H%2C Li J%2C Jiang D%2C Wang Z%2C Liu Z%2C Zhuang C%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhou L, Ni E, Yang J, Zhou H, Liang H, Li J, Jiang D, Wang Z, Liu Z, Zhuang C (2013) Rice OsGL1-6 is involved in leaf cuticular wax accumulation and drought resistance. PLoS One 8: e65139 1-12

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

http://scholar.google.com/scholar?as_q=Rice OsGL1-6 is involved in leaf cuticular wax accumulation and drought resistance&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Rice OsGL1-6 is involved in leaf cuticular wax accumulation and drought resistance&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhou&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Rice Sci%5BTitle%5D%29 AND 19%5BVolume%5D AND 44%5BPagination%5D AND Zhu LF%2C Yu SM%2C Jin QY%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhu LF, Yu SM, Jin QY (2012) Effects of aerated irrigation on leaf senescence at late growth stage and grain yield of rice. Rice Sci 19(1): 44-48.

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

http://scholar.google.com/scholar?as_q=Effects of aerated irrigation on leaf senescence at late growth stage and grain yield of rice&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Effects of aerated irrigation on leaf senescence at late growth stage and grain yield of rice&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhu&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Proc Natl Acad Sci USA%5BTitle%5D%29 AND 110%5BVolume%5D AND 17790%5BPagination%5D AND Zhu X%2C Xiong L%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhu X, Xiong L (2013) Putative megaenzyme DWA1 plays essential roles in drought resistance by regulating stress-induced wax deposition in rice. Proc Natl Acad Sci USA 110: 17790-17795

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

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http://scholar.google.com/scholar?as_q=Putative megaenzyme DWA1 plays essential roles in drought resistance by regulating stress-induced wax deposition in rice&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhu&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1


1 running head: es1 affects water loss 2 corresponding authors: … · 156 senescence marker genes,...

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