Dynamic cytology and transcriptional regulation of rice ...€¦ · 2017-05-12 · 21 One-sentence summary: A systemic study of dynamic morphology, cytology and 22 transcriptome

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Dynamic cytology and transcriptional regulation of rice lamina joint development 1

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Li-Juan Zhou1,2, Lang-Tao Xiao3, and Hong-Wei Xue1,* 3

4 1National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in 5

Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Shanghai Institutes for 6

Biological Sciences, Chinese academy of Sciences, 200032 Shanghai, China 7 2University of the Chinese Academy of Sciences 8 3Hunan Provincial Key Laboratory of Phytohormones and Growth Development, Southern 9

Regional Collaborative Innovation Center for Grain and Oil Crops in China, Hunan 10

Agricultural University, 410128 Changsha, China 11

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Author contributions 13

L.J.Z. performed acquisition of data as well as analysis and interpretation of data and 14

drafted the article. L.T.X provided technical assistance and helps to revise draft. H.W.X. was 15

responsible for conception and design, as well as analysis and interpretation of data and 16

revised the article. 17

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Short title: Transcriptional regulation of rice lamina joint 19

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One-sentence summary: A systemic study of dynamic morphology, cytology and 21

transcriptome reveals the cytological basis and fine-regulation by multiple factors, especially 22

phytohormones, of rice lamina joint. 23

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*Corresponding author: 25

300 Fenglin Road, Shanghai, China 200032 26

Phone: 86-21-54924330 Fax: 86-21-54924331 27

Email: [email protected] 28

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Funding information 30

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This study was supported by NSFC (91535201, 31570372) and MOST grants (No. 32

2012CB944804, 2013CBA01402). 33

Plant Physiology Preview. Published on May 12, 2017, as DOI:10.1104/pp.17.00413

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ABSTRACT 34

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Rice leaf angle is determined by lamina joint and an important agricultural trait determining 36

leaf erectness and hence the photosynthesis efficiency and grain yield. Genetic studies reveal 37

a complex regulatory network of lamina joint development; however, the morphological 38

changes, cytological transitions, and underlying transcriptional programming remain to be 39

elucidated. A systemic morphological and cytological study reveals a dynamic 40

developmental process and suggests a common but distinct regulation of lamina joint. 41

Successive and sequential cell division and expansion, cell wall thickening and programmed 42

cell death at the adaxial or abaxial sides conduct the cytological basis of lamina joint, and the 43

increased leaf angle results from the asymmetric cell proliferation and elongation. Analysis 44

of the gene expression profiles at four distinct developmental stages ranging from initiation 45

to senescence showed that genes related to cell division and growth, hormone synthesis and 46

signaling, transcription (transcription factors) and protein phosphorylation (protein kinases) 47

exhibit distinct spatial-temporal patterns, during lamina joint development. Phytohormones 48

play crucial roles by promoting cell differentiation and growth at early stages or regulating 49

the maturation and senescence at later stages, which is consistent with the quantitative 50

analysis of hormones at different stages. Further comparison with the gene expression profile 51

of leaf inclination1 (lc1-D), a mutant with decreased auxin and increased leaf angle, 52

indicates the synergistic effects of hormones in regulating lamina joint. These results reveal a 53

dynamic cytology of rice lamina joint that is fine-regulated by multiple factors, providing 54

informative clues for illustrating the regulatory mechanisms of leaf angle and plant 55

architecture. 56



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INTRODUCTION 57

58

As an important agronomic trait demerminated by multiple factors, architecture is crucial 59

for crop growth and yields. Leaf erectness, one of the key traits of rice architecture and 60

“ideotype” (Donald, 1968), will help dense planting, enhance light capture and improve 61

photosynthesis (Sakamoto et al., 2006; Sinclair et al., 1999). Leaf angle is determained by 62

the shape of lamina joint, the portion connecting leaf blade and sheath (Hoshikawa, 1989). 63

Lamina joint provides a unique path for transportation between leaf blade and sheath, and 64

addtionally, a supporting foundation for leaf erectness and expanding as a mechanical tissue. 65

The well-ordered cell organizations provide structural basis of lamina joint and abnormal 66

cell constitutions, division and elongation lead to the altered leaf inclination. Deficiency of 67

lamina joint structure (Lee et al., 2007), suppressed longitudinal elongation of adaxial 68

parenchyma cells and increased division of abaxial sclerenchyma cells of lamina joint (Sun 69

et al., 2015; Zhang et al., 2009a) result in the leaf erectness. Conversely, increased expansion 70

or proliferation of adaxial parenchyma cells leads to increased leaf inclination (Zhang et al., 71

2015; Zhao et al., 2010; Zhao et al., 2013). Abnormal vascular bundle formation and cell 72

wall composition also result in changed leaf angle (Ning et al., 2011). 73

Genetic and functional studies indicate the involvement of various factors in regulation 74

of lamina joint development and leaf inclination, especially phytohormones. Mutants 75

deficiency of BR biosynthetic genes, dwarf4-1 (Sakamoto et al., 2006), ebisu dwarf (d2) 76

(Hong et al., 2003) and chromosome segment deleted dwarf 1 (csdd1) (Li et al., 2013), show 77

reduced leaf inclination, which is also observed in BR signaling defective mutant d61 78

(Yamamuro et al., 2000) or transgenic rice plants with suppressed expression of OsBAK1 (Li 79

et al., 2009) and OsBZR1 (Bai et al., 2007). On the other hand, transgenic rice plants 80

overexpressing sterol C-22 hydroxylase (an important enzyme of BR biosynthesis, Wu et al., 81

2008), OsDim/dwf1 (participates in late steps of the sterol biosynthesis, Hong et al., 2005) 82

and OsBAK1 (Li et al., 2009) present increased leaf inclination, which is consistent with that 83

BR promotes cell elongation at adaxial side of lamina joint (Cao and Chen, 1995). A recent 84

study showed that BR signaling inhibits the proliferation of sclerenchyma cells at abaxial 85

side of lamina joint by coordinately regulating an U-type cyclin CYC U4;1 (Sun et al., 86

2015). 87

Auxin homeostasis and signaling regulate leaf inclination and gain-of-function mutants or 88

transgenic plants overexpressing GH3 family members including OsGH3-1, OsGH3-2, 89



4

OsGH3-5, OsGH3-13 present reduced auxin level and enlarged leaf angles (Du et al., 2012; 90

Zhang et al., 2015; Zhang et al., 2009b; Zhao et al., 2013). Overexpression of miR393a/b, 91

which suppresses the expression of OsAFB2 or OsTIR1, leads to the enlarged inclination of 92

flag leaf (Bian et al., 2012). Transgenic rice overexpressing OsARF19 shows enlarged leaf 93

inclination due to the increased expression level of GH3s and decreased free IAA content 94

(Zhang et al., 2015), and overexpression of OsIAA1 results in the increased leaf angle (Song 95

et al., 2009), suggesting the negative effects of auxin in leaf inclination. Interestingly, most 96

auxin-related mutants present changed BR sensitivity (Song et al., 2009; Zhang et al., 2015; 97

Zhao et al., 2013) and the inclination by treatment with brassinolide alone is suppressed by 98

inhibitor of IAA transport (Cao and Chen, 1995), or promoted by additional IAA (Han et al., 99

1997), suggesting a complex regulation of phytohormones in lamina joint development. In 100

addition, BR-induced leaf inclination is accompanied by ethylene production and inhibited 101

by inhibitor of ACC oxidase (Cao and Chen, 1995), or suppressed by treatment with ABA 102

and GA (Han et al., 1997; Tong et al., 2014), further indicating that phytohormones 103

synergistically and antagonistically regulate lamina joint development and leaf inclination. 104

Transcriptional regulation by transcription factors (TFs) and protein modification by 105

protein kinases are involved in leaf inclination regulation. OsLIGULELESS1 (OsLG1) 106

encodes a SBP domain-containing TF and mutant oslg1 abolishes the ligule, auricle, and 107

lamina joint (Lee et al., 2007). LAX PANICLE (LAX) encodes a bHLH TF and ectopic 108

expression of which caused excessive bending of rice lamina joint (Komatsu et al., 2003). 109

INCREASED LEAF ANGLE 1 (ILA1) encodes a Raf-like MAPKKK of Group C and ila1 110

mutant presents increased leaf angle by abnormal vascular bundle formation and cell wall 111

composition in lamina joint (Ning et al., 2011). In addition, LEAF INCLINATION 2 (LC2), a 112

VIN3-like protein, controls leaf inclination by inhibiting the adaxial cell division (Zhao et al., 113

2010). Suppression of small RNA producing genes including OsRDR2 (RNA-dependent RNA 114

polymerase 2), OsDCL3a (RNase III-class Dicer-like 3), OsAGO4a, OsAGO4b (members of 115

Argonaute family) results in the increased bending of lamina joint (Wei et al., 2014), while 116

increased expression of OsAGO7 leads to the leaf erectness (Shi et al., 2007). 117

Although studies demonstrated the involvement of multiple factors in lamina joint 118

development, the underlying cellular and molecular mechanisms are rarely studied. Previous 119

reports showed that when the leaf blade differentiates from the leaf primordium and grows to 120

less than 1 cm, a hollow space appears at the base of leaf blade and differentiation and 121

development of lamina joint initiate (Hoshikawa, 1989). Lamina joint develops along with 122



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leaf blade and sheath, and fully developed lamina joint supports leaf with an appropriate 123

inclination for light capture and high-efficient photosynthesis. To illustrate the relevant 124

regulatory mechanisms, a systematic study of lamina joint development including the 125

morphology, cytology and global transcriptome analyses were performed and results indicate 126

that lamina joint development is well-ordered and progressive, with distinct cytological basis 127

and dynamic processes. Genes associated with transcriptional regulation, signal transduction 128

and metabolic pathways, especially biosynthesis and signaling of hormones, are involved in 129

lamina joint development through regulating multiple biological processes including 130

elongation/division of parenchyma cells, sclerenchyma cell differentiation, vascular 131

development and programmed cell death. These results will provide informative clues on 132

illustrating the regulatory mechanism of rice lamina joint development and hence the plant 133

architecture formation. 134



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RESULTS 136

137

Cytological Observation Reveals the Distinct Characters and Dynamic Development of 138

Rice Lamina Joint 139

Leaf angle varies among different rice cultivars and Zhonghua11 (ZH11) with intermediate 140

leaf inclination was selected for studies. Leaf angle increases after the lamina joint emerges 141

from the prior leaf sheath and daily observation of the dynamic growth shows the six distinct 142

development stages of lamina joint from initiation to senescence that encompass complex 143

developmental and morphological changes (Table 1, Figure 1A). Interestingly, recording the 144

angles of all 13 full leaves showed that although the final inclination degrees, increasing 145

periods and maximum slops of curves vary with each other, a similar and common “S” 146

pattern with the maximum increasing rates at stage 5 is observed (Figure 1B), suggesting the 147

uniformity and distinctness of lamina joint development of different leaves. 148

Observation of the cytology compositions and structures of lamina joint by cross sections 149

showed that the parenchyma cells constitute the basic structure and abundant sclerenchyma 150

tissues provide the mechanical support of lamina joint. The ordered vascular bundles, 151

together with large aerenchymas, provide channels for water/nutrients transport and air 152

circulation (Figure 1C). Structurally, vascular bundles are regularly spaced at both adaxial 153

and abaxial sides and sclerenchyma cells are located at the fringe of vascular bundles. There 154

are several aeration cavities (aerenchymas) inside the lamina joint and the rest is filled with 155

the parenchyma cells which connect the abaxial large vascular bundles with adaxial side. 156

Observation of the longitudinal sections shows the oppressed cells at abaxial side and 157

sclerenchyma cells form the fibers up to bottom (Figure 1D). 158

Lamina joint connects the leaf blade and sheath, and presents a similar anatomic 159

structure but significantly different cell compositions with leaf midrib. Comparison reveals 160

that there is no mesophyll cells but numerous layers of large parenchyma cells instead, and 161

more sclerenchyma cells at both abaxial and adaxial sides of lamina joint (Figure 1C), 162

indicating a distinct cell composition may result in the leaf inclination at lamina joint. 163

Systemic observation of lamina joint at different developmental stages using paraffin 164

sections reveals a similar progressive and distinct cytological changes according to the 165

morphological classification (stages 1-6, cross section of the 8th leaf was shown as 166

representative in Figure 2A; longitudinal section of flag leaf was shown as representative in 167

Figure S1). As described in Table 1, the fine controlled division and expansion of 168



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parenchyma cells, differentiation of sclerenchyma cells, cell wall thickening, and 169

programmed cell death (PCD) are crucial for lamina joint development and final leaf 170

inclination. The PCD proceeds continuously in formation of aerenchyma and vascular 171

bundles, and the development of sclerenchyma tissues. 172



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Detailed calculation reveals an active proliferation and expansion of cells at the horizontal 173

direction. Different with the “S” curves of leaf inclination, the size of lamina joint, adaxial 174

sclerenchyma cluster and parenchyma cell present an increase-decrease tendency (Figure 175

2B). Sclerenchyma cells differentiate and develop synchronously at both adaxial and abaxial 176



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sides. At stage 5, the abaxial cells stop growing, while the remaining parenchyma cells at 177

adaxial side undergo vertical elongation (Figure S1), resulting in the asymmetric growth 178

between adaxial and abaxial sides and hence the increased leaf angle. 179

180

Global Transcriptomes Analysis Reveals the Involvement of Multiple Biological 181

Processes during Lamina Joint Development 182

The lamina joints of last three leaves develop across the vegetative and reproductive 183

growth and show typical leaf angle curves (Figure 1B), and global transcriptome profiles 184

were studied to investigate the underlying molecular mechanisms regulating lamina joint 185

development and leaf inclination. Stages 2, 4, 5, 6 representing distinct developmental 186

phases including the early initiation, mature, inclination-increasing, and senescence of 187

lamina joint (Figure S2A), were analyzed and compared to the adjacent leaf parts of the last 188

third lamina joint at stage 4 (defined as “leaf”) when the lamina joint is fully developed 189

(Figure S2B). Pairwise Pearson correlation coefficient (PCC) analysis reveals the high 190

correlation of gene expression profiles of different lamina joints at same developmental stage 191

(Figure S2C). The contiguous leaves and developmental stages tend to be more correlated. 192

Stages 4-6 are highly correlated (PCCs > 0.96), while stage 2 is distinct with others, which is 193

consistent with the cytological changes during lamina joint development. As expected, there 194

is low correlation between lamina joint and the adjacent parts (0.88 < PCCs < 0.96). 195

Based on the first two principal components (98% of variation captured), the principal 196

component analysis (PCA) additionally showed that expression profiles of the different 197

developmental stages are well-ordered and separated by the principal component 1 (PC1) 198

(temporal factor) (Figure 3A), suggesting the similar transcriptional regulations of different 199

lamina joints at same developmental stages. In addition, the adjacent leaf parts was separated 200

with lamina joint by the principal component 2 (spatial factor), which may be due to the 201

tissue specificity. 202

Identification of organ developmental status could be featured and defined by gene 203

expression profiles, the differentially expressed genes (DEGs) were identified by pairwisely 204

comparing the analyzed stages using Limma packages (Wettenhall and Smyth, 2004). The 205

DEG numbers increase along with the lamina joint development (Figure 3B), and those at 206

stages 2-4 are much more than those between other contiguous stages, suggesting the 207

complex regulation at stage 2, which is consistent with the cytological characteristics. DEG 208

numbers at stages 4-5 or 5-6 are considerably few, indicating the similar gene expression 209



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profile at these 3 stages and stage 5 is a transition period during lamina joint development. In 210

sum, 5,842 (stage 2-4), 161 (stage 4-5), 420 (stage 5-6) and 2,180 (stage 4-6) DEGs of three 211

lamina joints (based on the similar gene expression profiles at same developmental stage) 212

were identified (Figure 3C). 213



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Preferential expression of previous reported genes regulating leaf angle including LG1 214

(Lee et al., 2007), BU1 (Tanaka et al., 2009), LPA1 (Wu et al., 2013) and CYC U4:1 (Sun et 215

al., 2015) at lamina joint (Figure S2D) confirms the accuracy of transcriptome analysis. 216

Genes GRAS19 (Chen et al., 2013), LAZY1 (Li et al., 2007), CYP51G3 (Xia et al., 2015), and 217

GSR1 (Wang et al., 2009) present high expression levels at lamina joint, validating their 218

roles in lamina joint development. In addition, genes involving in biosynthesis and signaling 219

of brassinosteroid (BR) and auxin, which have been implicated the important roles in leaf 220

angle, present diverse expression patterns, including the decreased expressions (CYP51G3, 221

CYC U4:1), increased expressions (DLT, Tong et al, 2009; Tong et al, 2012; GRAS19, 222

GH3-2), constant high expression levels (LIC, Wang et al., 2008; Zhang et al., 2012; LAZY1) 223

and constant low expression levels (ILI1, Zhang et al., 2009a; REL1, Chen et al., 2015), 224

suggesting the complex regulation of leaf angles via different pathways. 225

Analysis of DEGs identifies six clusters with specific expression patterns, i.e. highest 226

expression at stage 2 and reduced from stage 4 to 6 (C1), keep reducing from stage 2 to 6 227

(C2), a relatively high expression at middle stages (C3); while cluster C4, C5, C6 showed 228

opposite expression patterns to C2, C1 and C3 (Figure 3D). Further Enriched Gene Ontology 229

(GO) analysis identifies the stage-specific biological processes that are well consistent with 230

the cytological and functional features of each stage (Figure 3E). Genes preferentially 231

expressed at stage 2 (C1) participate in metabolism, cell cycle, signal transduction and cell 232

wall organization, which is consistent with that cells at stage 2 are active and have partial 233

primordium activity enabling cells to divide and differentiate. Signal transduction and 234

metabolism at all analyzed stages may play roles in determining the cell fate. Genes that are 235

gradually reduced (C2) involve in microtubule-based process in addition to primary 236

metabolism, suggesting the suppressed cell growth along with lamina joint development, 237

which is consistent with the continuous and decreased cell expansion. Genes related to 238

protein phosphorylation, programmed cell death and transport are enriched in C4 and C5, 239

which are closely related to the cytological changes (the vascular development, 240

sclerenchyma fiber formation and aerenchyma enlargement) at later stages and functions of 241

mature lamina joint (mechanical support and transportation). 242

Lamina joint connects leaf blade and whose structure shares similarities with nearby leaf 243

midrib, however, the cell compositions and functions of them significantly 244

differ. Considering that the developmental processes of examined three lamina joints are 245

similar (Figure 3A, 3B, S2C), adjacent part (0.5 cm) of lamina joint of the last third leaf at 246



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stage 4 was collected and used as a representative to study the difference between lamina 247

joint and adjacent parts. The last third leaf presents typical structure of leaf blade and lamina 248

joint, and leaf is fully developed (with mature structures) at stage 4. Comparison of the 249

transcriptomes between lamina joint and adjacent part reveals ~1000 up-regulated and 1500 250

down-regulated genes in lamina joint (FC>2, FDR<0.05; Figure S3A, S3B). GO analysis 251

showed that cell wall organization and cell growth-related progresses are enriched among 252

up-regulated genes, which is consistent with the structural difference (more sclerenchyma 253

cells featured by thickened cell wall and much more large parenchyma cells owing to 254

additional cell division and growth) between lamina joint and adjacent leaf part (Figure S3C, 255

Figure 1C). The photosynthesis-related processes are enriched in the down-regulated genes, 256

which is consistent with the deficiency of chloroplast in lamina joint (due to the lack of 257

mesophyll cells, Figure 1C). The difference of biological processes lays the foundation of 258

leaf angle formation at lamina joint rather than the leaf blade. 259

260

Expression Profile of Transcription Factors and Protein Kinases in Lamina Joint 261

With the focus to identify the candidate regulators of lamina joint development, 262

expression profile of transcription factors (TFs) was analyzed in detail. 373 TFs belonging to 263

45 families and 37 transcription regulators (TRs) belonging to 13 families are differentially 264

expressed with distinct patterns (Figure 4A), suggesting their functions at specific 265

developmental stages of lamina joint. 266

Four C2C2-YABBY genes, DROOPING LEAF (DL) (Os03g11600), OsYABBY3 267

(Os04g45330), OsYABBY4 (Os02g42950) and OsYABBY1 (Os07g06620), which are reported 268

to regulate the midrib formation, lateral organ development, vascular development, and leaf 269

angle (Dai et al., 2007; Liu et al., 2007; Tanaka et al., 2012; Yamaguchi et al., 2004), display 270

rapid down-regulation from stage 2 to 4 (C1 and C2 patterns) and may regulate the early 271

lamina joint development and organogenesis. MYB members show dramatic changes from 272

stage 2 to stage 4 (17 genes with C1 patter, 8 genes with C5 pattern), suggesting their 273

potential roles in secondary cell wall synthesis in early lamina joint development and stress 274

tolerance at later stages (Yang et al., 2014; Zhu et al., 2015). Most of the differentially 275

expressed IAA genes are with C1 and C2 patterns, suggesting the suppressed auxin signaling 276

during lamina joint development (see below). WRKY genes exhibit an opposite pattern to 277

IAAs and are enriched in C4 and C5 patterns, suggesting their roles at later stages of lamina 278

joint by regulating cell wall composition and hormonal signals (salicylic acid and abscisic 279



14

acid) (Wang et al., 2007a; Zhang et al., 2009c). In addition, differentially expressed OFP, 280

SBP, TCP and Trihelix members mainly exhibit C1 and C2 patterns and AP2-EREBP, 281

C2C2-CO-like, G2-like, NAC and Orphans members are enriched in C4 and C5 patterns. 282

Analysis of the differentially expressed TFs between lamina joint and adjacent leaf parts 283



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showed that 58 and 44 TFs are higher or lower expressed in lamina joint respectively (Figure 284

S4A, S4B). Genes belonging to growth regulating factor (GRF), homeobox 285

domain-containing (HB), HRT domain-containing (HRT) and lateral organ boundaries (LOB) 286

family, which are involved in the regulation of cell expansion or differentiation, 287

hormone-response, organ development (Kim et al., 2003; Kappen, 2000; Raventos et 288

al., 1998; Husbands et al., 2007), are consistently enriched in higher expressed TFs, as well 289

as LG1, which present specific expression in lamina joint (Figure S4B). Further analysis of 290

the cis-elements regulated by lamina joint preferential TFs reveal the enrichment of ABA, 291

auxin and MYB-related elements, coinciding with that ARF and MYB members are involved 292

in lamina joint identification (Figure S4C). Unexpectedly, GA-related elements are enriched 293

in down-regulated TF genes. 294

Protein modifications including phosphorylation, glycosylation and ubiquitination are 295

important in regulating various biological processes and protein phosphorylation is highly 296

enriched with C4 and C5 patterns (Figure 3E), indicating the significance of protein kinase 297

during lamina joint development. 423 kinases belonging to 54 subfamilies are differentially 298

expressed and many of them present specific expression patterns (Figure 4B). PVPK_like, 299

Extensin, LRR-III/V/VI/VII/XI/XIII, and RLCK-V/VI subfamilies are enriched with C1 and 300

C2 patterns, while MEKK, CrRLK1L, DUF26, L-LEC, LRR-VIII/X/XII/XV, RLCK-IV/VII, 301

SD-1/2, WAK and Raf subfamilies are enriched with C4 and C5 patterns. L-LEC and MEK 302

kinases, the key regulators in biotic and abiotic stresses, are enriched in C5 pattern, which is 303

consistent with the senescence and enhanced stress tolerance at later stages. In addition, 304

similar expression pattern of same family members suggests the functional redundancy, 305

which may be the reason why few kinase genes were reported by genetic studies. There is 306

very few reports on the roles of protein kinase in lamina joint and these results may provide 307

clues for further studies, especially the functions of protein kinases in organ development. 308

309

Drastic Changes of Cell Division/Expansion-Related Genes at Early Stages 310

Cell division is a predominant process when lamina joint initially develops, and along 311

with cell division, cell expansion starts and lasts longer at adaxial side, leading to the 312

asymmetric growth and hence leaf inclination (cell wall thickening provides mechanical 313

support). Analysis of the expression profile of genes involving in cell cycle and expansion 314

showed that cyclins, cyclin-dependent kinases (CDKs), and other core cell cycle regulators 315

including CDKs inhibitors (CKIs; KRPs), retinoblastoma (Rb/E2F/DP/DP-LIKE) pathway 316



16

members, CDK subunit (CKS) and wee1-like protein kinases (Inze and De Veylder, 2006), 317

display a distinct stage- or tissue-specific expression (Figure 5A). Consistent with that 318

OsCycU4;1 is involved in cell division at abaxial side during lamina joint development (Sun 319

et al., 2015), OsCycU2;1 and OsCycU4;1 are highly expressed in lamina joint with C1 and 320



17

C2 patterns, while OsCycD5;2 is lowly expressed, indicating a distinct regulatory 321

mechanism. Interactions with cyclins and protein phosphorylation are important for CDKs 322

activity. Most cyclins (mainly in class A to D) are highly expressed at early stages (especially 323

stage 2) with C1 or C2 patterns, while majority of CDK members are constantly highly 324

expressed, indicating the significance of transcriptional regulation of cyclins in cell cycle 325

determination. 326

Cell-wall loosening and cell wall synthesis are involved in cell expansion (Shi et al., 2014) 327

and analysis showed that highly expressed expansins (EXPB3, EXP7 and EXPL2) display C1 328

and C2 patterns as well (Figure 5B). Further analysis of the cell wall synthases CESAs 329

(which are responsible for cellulose synthesis, Wang et al., 2010) showed that unlike 330

expansins, lamina joint-preferential CESAs (CESA1, CESA5, CSLA6, CSLC7) display 331

constant expressions during lamina joint development (Figure 5C). However, most of the 332

differentially expressed expansins and CESAs are with C1 and C2 patterns, similar as cell 333

cycle related genes. High expressions of cyclins, expansins and CESAs lead to an enhanced 334

cell proliferation, expansion, elongation and cell wall thickening, and are consistent with the 335

intensive cell division and growth at early stages of lamina joint. 336

337

Vital Roles of Phytohormones in Lamina Joint Development 338

Detailed analysis of hormone biosynthesis- and signaling-related genes according to 339

previous definition (Figure S5, Chen et al., 2015) showed that BR biosynthesis- and 340

signaling-related genes display non-uniform expression patterns (Figure 6A). Genes related 341

to BR biosynthesis (D11, D2) and signaling (BRI1, BAK1, BU1) present a decreased 342

tendency (Figure S2D), suggesting the decreased BR biosynthesis and signaling during 343

lamina joint development, which is consistent that enhanced BR signaling results in the 344

enlarged leaf inclination. 345

Rate-limiting enzyme of GA biosynthesis, GA20ox1, shows decreased expression, while 346

GA metabolic genes (GA2ox:1, GA2ox:2, EUIL3) display opposite tendency, which results 347

in a decreased GA level at later stages. The expression synchronicity of GA and BR-related 348

genes may be due to that they both promote cell elongation, and the complicated crosstalk 349

between them in rice (Tong et al., 2014). Similar to GA, decreased expression of ABA 350

biosynthesis gene (ABA4) and increased metabolic gene (ABA8OX1) may lead to decreased 351

active ABA level at later stages. In contrast to BR and GA, expression of most ethylene 352

biosynthesis and signaling, JA biosynthesis and SA signaling-related genes increase along 353



18

with lamina joint development (Figure 6A). In addition, compared to adjacent leaf parts, 354

expression of genes involving in auxin biosynthesis, signaling and transport, BR signaling, 355

ethylene biosynthesis and signaling are much higher in lamina joint (Figure S6). 356

Due to the complexity of hormone biosynthesis and signaling, especially the feedback and 357



19

post-transcriptional regulation of hormone-related genes, it will be hard to predict the exact 358

hormone biosynthesis and signaling based on the non-uniform gene expression. The exact 359

levels of various hormones were thus quantified at different stages (Figure 6B, BR content is 360

not measured due to the lack of assay system). Being consistent with the transcriptome 361

analysis, levels of active auxin (IAA) and cytokinin (zeatin) decrease from stage 2 to 6, 362

further confirming the roles of them in stimulating cell division at early stage. Content of 363

free JA increases from S2 to S4, which is consistent with the elevated OsLOXs and OsAOS1 364

expressions (Figure S6), while decreases from S4 to S5, which may be due to the massive 365

transformation from JA to the bioactive derivative JA-Ile (modified by OsJAR1) (Fonseca et 366

al., 2009; Sheard et al., 2010; Yan et al., 2016), suggesting the increased amount of bioactive 367

JA on the whole. In addition, amounts of SA increase along with the lamina joint 368

development, which is in accordance with their possible roles in improving biotic and abiotic 369

stress tolerance and enriched cell death, protein phosphorylation and defense responses at 370

later stages (patterns C4 and C5, Figure 3E). ABA amounts show an increase-decrease 371

tendency with maximal at stage 5, suggesting a complex regulation and function of ABA 372

during lamina joint development, especially the senescence process at late stages. 373

Interestingly, amounts of auxin, cytokinin and ABA in lamina joint are higher, while SA is 374

relatively lower, than those of adjacent leaf parts, suggesting that auxin, cytokinin and BR 375

are the possible regulators in promoting lamina joint organogenesis and development. 376

377

Auxin Regulates Lamina Joint Development through Distinct Processes 378

Based on the crucial roles of auxin in lamina joint development, auxin-related genes were 379

particularly analyzed. Expressions of auxin biosynthesis, transport and signaling related 380

genes change dynamically during lamina joint development (Figure 7A). Auxin signaling 381

and transport present a gradually decreasing tendency. Although auxin synthesis-related 382

genes show unobvious changes, TAA1s (key gene involving in auxin biosynthesis) decrease 383

and metabolic genes (GH3 family GH3-2, GH3-6, GH3-8) increase, suggesting a decreased 384

auxin level during lamina joint development especially at early stage, which is consistent 385

with the measurement of free IAA content (Figure 6B). In addition, auxin efflux (OsPIN1C, 386

OsPIN5a, OsPIN5b, OsPIN8) and influx carriers (OsLAX:2, OsLAX:3, OsLAX:4, OsLAX:5) 387

exhibit obvious stage specificity, which may cause the asymmetrical auxin distribution to 388

control the cell division and elongation at adaxial or abaxial side. 389

Most differentially expressed IAA genes (except IAA6 and IAA19) show decreased 390



20

expression tendency. Considering that IAA functions by suppressing ARFs through complex 391

interaction networks of IAAs-ARFs, clustering analysis of all 31 IAAs (Jain et al., 2006) and 392

25 ARFs (Wang et al., 2007b) based on the expression patterns provide further clues of the 393

IAAs-ARFs interactions in regulating lamina joint development. IAA6/IAA25-ARF19, 394



21

IAA12/18/31-ARF1/2/7, IAA21-ARF17 may cooperatively regulate lamina joint 395

development at different stages (Figure 7B). Interestingly, many ARFs and IAAs are 396

constitutively expressed in lamina joint (ARF3/4/6/9/12/15/18/22/23/24/25; 397

IAA1/2/3/5/10/17/24), and further analysis by combining with the interaction analysis will 398

help to illustrate the distinct function of IAA-ARF in lamina joint development. 399

To further study the mechanism of auxin effects in regulating lamina joint development, a 400

gain-of-function mutant lc1-D (Leaf Inclination 1 encodes OsGH3-1, an IAA amino 401

synthetase) which is identified from the Shanghai T-DNA Insertion Population (SHIP) (Fu et 402

al., 2009) and presents reduced auxin level and enlarged leaf angles due to the increased cell 403

elongation in adaxial surface of lamina joint (Zhao et al., 2013) was used. Comparison of 404

transcriptomes of lamina joint of lc1-D and its corresponding original cultivar control ZH11 405

identified 319 up-regulated and 254 down-regulated genes in lc1-D. Interestingly, 55% of the 406

up-regulated genes (175) and 34% of the down-regulated genes (86) in lc1-D are detected in 407

DEGs along with lamina joint development (Figure 7C, S7). Further GO analysis reveal the 408

enrichment of cell division and elongation, stress, defense and lignin metabolic-related 409

processes (Figure 7D), which is consistent with the cytological change and reduced level of 410

auxin at later stages, in lamina joint development. 411

In addition, JA and SA signaling related genes are up-regulated and BR related genes 412

(mainly BR biosynthesis genes) are enriched in down-regulated genes, of lc1-D (Figure 7D, 413

S7), suggesting that auxin may suppress JA and SA signaling, or stimulate BR biosynthesis, 414

to coordinately regulate the lamina joint development. 415

416

Identification of lc3 Mutant with Enlarged Leaf Angle 417

The cytology and transcriptome analysis provide informative clues to identify novel 418

genes regulating leaf angles. By analyzing the DEGs and screening the mutants with altered 419

leaf angles from SHIP, a mutant, designated as leaf inclination 3 (lc3), was identified. LC3 420

(Os06g39480) encodes a novel SPOC-domain containing protein and presents a 421

down-regulated expression from S2 to S6 (Figure 8A). T-DNA locates at the 3’UTR and 422

results in a significantly reduced expression of LC3 (Figure 8B). Detailed observation and 423

measurement showed that lc3 presents much enlarged leaf angles at heading stage (Figure 424

8C), indicating LC3 a novel regulator of leaf inclination and confirming the valuableness of 425

the transcriptome studies. Detailed mechanisms will be further investigated. 426



22

427



23

DISCUSSION 428

429

Appropriate leaf inclination determines the leaf erectness and photosynthesis efficiency, 430

and hence crop yields. Considering the complex regulation and cytological changes (cell 431

division and elongation, cell wall thickening and PCD), and tissue development (vascular 432

bundles, sclerenchyma, parenchyma, aerenchyma are common in various organs), lamina 433

joint is also an ideal model to study the regulatory mechanism of cytology and tissue 434

development, as well as the cross-talk of phytohormones. Through systemic cytology and 435

transcriptome studies, it is shown that cell differentiation, cell division and elongation, cell 436

wall thickening, PCD and senescence are predominantly processes during lamina joint 437

development. Consistently, most of the Cyclin-CDKs (the master factor controlling cell 438

division), expansin genes and CESAs (the factors regulating cell expansion and cell wall 439

thickening) are preferentially expressed at early stages and then declined, which may be 440

regulated by upstream phytohormones signals (auxin, BR, GA). Our studies reveal the 441

distinct characters and cellular processes of rice lamina joint development, which is fine 442

controlled and synergistically regulated by multiple factors, especially hormones (Figure 8D), 443

providing informative clues for understanding the regulatory network of lamina joint 444

development and contributing to genetic breeding for ideal architecture of crops. 445

446

Cytology during Lamina Joint Development 447

Cytological studies reveal that regularly occurred cell activities are closely related to the 448

specific processes at distinct stages during lamina joint development. At early/initiation stage 449

(S2) when the organ pattern is formed, cell division and expansion, cell wall thickening and 450

vascular development occur. Longitudinal elongation of adaxial parenchyma cells at 451

maturation stage (S4) leads to the leaf inclination and degree of leaf angle is mainly 452

determined at stage 4. The most significant change at senescence stage (S5-S6) is the 453

distortion of lamina joint. Interestingly, programmed cell death (PCD) happens throughout 454

the whole process of lamina joint development (Figure 8D). 455

In addition to cell proliferation and elongation, sclerenchyma cell properties and 456

parenchyma cell numbers or size regulate the leaf inclination as well. The parenchyma cells 457

are living cells with plasticity and the number of which at adaxial side is the main factor 458

determining leaf inclination. Indeed, altered parenchyma cell numbers or size lead to the 459

altered leaf angle (Zhang et al., 2015; Zhao et al., 2013). 460



24

Sclerenchyma clusters are mechanical tissues to support lamina joint, and change of 461

whose size and cell wall thickness results in the altered mechanical strength and hence leaf 462

angle, although there are only a few relevant reports (Ning et al., 2011; Sun et al., 2015). 463

Although PCD is a significant process throughout the lamina joint development, there is 464

no report on the effects of PCD-related genes in regulation of leaf angle, which may be due 465

to the fact that PCD happens not exclusively in lamina joint but also in leaf blade and sheath. 466

Consistently, the PCD-related GO term is not enriched in lamina joint when compared to 467

adjacent leaf parts. In addition, simultaneous occurrence of PCD at both adaxial and abaxial 468

sides indicates that PCD may not directly regulate the leaf inclination. 469

470

Multilevel Regulation of Lamina Joint Development 471

Although lamina joint start to bend at stage 4 and constantly enlarge, molecular and 472

cytological changes during the period from stages 2 (initiation) to stage 4 (maturation) are 473

crucial and provide the foundation for leaf angle formation, which is consistent with the 474

transcriptome analysis showing the significant changes of gene expressions at early stages 475

and moderate but considerable changes at later stages. 476

Many TFs and kinases present the distinct expression patterns, resulting in the specifically 477

enriched biological processes. At early/initiation stage, primary metabolisms, cell cycle, cell 478

wall organization and microtubule based-movement are enriched, which may be regulated by 479

organogenesis related TFs (GATAs, YABBYs, OFPs, IAAs). While at maturation and 480

following senescence stage, NACs, WRKYs may regulate the cell death, protein 481

phosphorylation and transport to achieve the enhanced stress tolerance, function of mature 482

lamina joint and on-going PCD processes. In addition to transcriptional regulation, 483

post-translational modification such as phosphorylation regulates lamina joint development 484

by modulating the downstream signaling pathways, including the cell expansion or stress 485

responses by extensins/WAKs, cell death or defense response by RLKs/MAPKs. 486

Although inclination angle of each leaf differs from one another, lamina joints of all 487

leaves display consistent developmental process: the changing trajectories of leaf angles tend 488

to display a similar “S” curve with varied maximum angles resulting from the differential 489

cell properties, layers and expansion, suggesting the existence of an intrinsic mechanism to 490

determine the consistence and divergence of lamina joints. The intrinsic factors including 491

spatial (leaf order from bottom to up) or temporal effect (leaf order from front to behind), 492

and external factors such as light, temperature, gravity, nutrition and planting density, may 493



25

synergistically regulate the cytology and final determination of leaf inclination by 494

coordinating the gene expressions. 495

496

Crucial Roles of Phytohormones in Lamina Joint Development 497

Measurement and transcriptome analysis suggest that at early stages, high amounts of 498

auxin, BR, GA, and CK promote the cell division and expansion, while at later stages, 499

ethylene, SA and JA, may regulate the senescence and stress-response, of lamina joint 500

(Figure 8D). BR deficient or insensitive mutants display erect leaves, and increased BR 501

biosynthesis or signaling results in enlarged leaf angles. Endogenous BR regulates leaf angle 502

either by enhancing the parenchyma cell elongation at adaxial side (similar to that caused by 503

BR treatment) or by inhibiting the proliferation of sclerenchyma cells at abaxial side. The 504

cytological and transcriptome analysis confirm the importance of these two cell types in 505

lamina joint development and leaf inclination. 506

Reduced free auxin level causes enhanced leaf angle bending due to the stimulated cell 507

elongation of parenchyma cells at adaxial side (Zhao et al., 2013), suggesting the 508

suppression effect of auxin on leaf inclination. Indeed, high auxin level is detected at early 509

stages and reduces along with the developmental progress, which is consistent with the 510

increased expression of GH3s. Combined with the cytological observations, it is suggested 511

that when the lamina joint initiates at early stage, auxin is synthesized and polarly 512

transported, resulting in the high local auxin concentration and stimulated cell division but 513

suppressed elongation; while along with the lamina joint development, auxin level decreases 514

and results in the promoted elongation of parenchyma cells. However, increased auxin level 515

does not lead to smaller leaf angles, implying the presence of a compensatory pathway in 516

these cells that stimulates the cell elongation. The fact that expression levels of BR 517

biosynthesis genes are increased in lc1-D mutant suggests the possibly compensatory effects 518

of BR and that auxin and BR cooperatively regulate the lamina joint development. 519

In addition, various hormones may regulate the lamina joint development synergistically 520

and antagonistically. Auxin may function with BR to promote cell growth at early stages and 521

decreased auxin not only stimulates the cell elongation, but also relieves the suppression of 522

JA and SA signals to regulate the stress response or senescence at later stages (Figure 8E). 523

524



26

Materials and methods 525

526

Plant Materials and Growth Conditions 527

Rice plants ZH11 (Oryza sativa, japonica cultivar Zhonghua11) and lc3 mutant for leaf angle 528

recording and paraffin section were grown in the paddy field in Shanghai. For microarray 529

analysis, ZH11 was cultivated in a greenhouse with a 12 h-light (28°C) / 12 h-dark (22°C) 530

cycle. The lamina joints were collected (those of the last third leaf at 50, 55, 60 and 70 days 531

after sowing, DAS; those of the last second leaf at 55, 60, 65 and 75 DAS; those of the last 532

leaf at 60, 65, 70 and 80 DAS). 533

Adjacent part (0.5 cm) of lamina joint of the last third leaf at stage 4 (55 DAS) was 534

collected (defined as “leaf”) and used as a representative to study the difference between 535

lamina joint and adjacent part. Thirteen samples in total were collected and each sample has 536

two biological replicates. 537

538

Leaf Angle Measurement 539

Leaf lamina joint with 1 cm section of leaf and sheath on the main tiller were cut and 540

photographed. Leaf angle was calculated by 180 degrees minus angle between sheath and 541

leaf, which was measured with the aid of the ImageJ program (http://rsb.info.nih.gov/ij/). At 542

least 10 leaf angles of individual plants were measured at each time point. 543

544

Paraffin Sections and Cytological Analysis 545

Rice lamina joints and leaves were fixed in FAA solution (50% ethanol, 5% acetic acid and 546

10% formaldehyde in water), dehydrated in a graded ethanol series, and embedded in 547

paraffin (Sigma). Microtome sections (8 mm) were applied onto microscope slides. The 548

sections were de-paraffinized in xylene, dehydrated through a graded ethanol series, and 549

stained with toluidine blue. Sections were observed and photographed to measure the size of 550

lamina joint or calculate the cell number and length using ImageJ software. 551

552

RNA Extraction, Microarray Hybridization and Data Normalization 553

Total RNA from lamina joints and adjacent leaf parts was extracted using TRIZOL Reagent 554

(Cat#15596-018, Life technologies) and purified by RNeasy micro kit (QIAGEN) and 555

RNase-Free DNase Set (QIAGEN). Resultant total RNA was amplified, labeled and purified 556

by using GeneChip 3’IVT Express Kit (Cat#901229, Affymetrix, Sata Clara, CA, US) 557



27

following the manufacturer’s instructions to obtain the biotin-labeled cRNA. Array 558

hybridization and wash were performed using GeneChip Hybridization, Wash and Stain Kit 559

(Cat#900720, Affymetrix) in Hybridization Oven 645 and Fluidics Station 450 (Affymetrix) 560

following the manufacturer’s instructions. GeneChips were scanned using a GeneChip 561

Scanner 3000 (Affymetrix). The obtained data of this study can be accessed at GEO under 562

number GSE92895. 563

Analyses were performed using the R software package (http://www.r-project.org) and 564

packages by Bioconductor (Gentleman et al., 2004, http://www.bioconductor.org) if not 565

specified. The raw data were evaluated (Gentleman et al., 2006; Wilson et al., 2010) to 566

generate the QC reports. After comparing the performances of popular methods on our data, 567

the RMA (Irizarry et al., 2003) method was used to obtain summary expression values for 568

each probe set. Gene expression intensities were analyzed on a logarithmic scale. The data 569

were separately normalized using MAS 5.0 algorithm to generate Present/Absent calls. 570

Probesets showing “A” or “M” in all samples were excluded for further analysis. Pearson 571

correlation coefficients (PCCs) were calculated from RMA generated logarithmic scale 572

expression values by Microsoft Excel 2010 to compare the relationships between samples. 573

PCA analyses were performed in the R environment. 574

575

Identification of Differentially Expressed Genes (DEGs) and Clustering Analysis 576

The linear statistical model in Limma package (Wettenhall and Smyth, 2004) from 577

Bioconductor was used to identify the DEGs between two groups (lamina joint sample 578

pairwise comparisons or comparison between lamina joint and adjacent leaf parts) by 579

calculating fold change (FC) and applying an false discovery rate (FDR) correction based on 580

Benjamini and Hochberg method (Benjamini and Hochberg, 1995). Only genes expressed at 581

least in one sample were used for DE analysis (MAS 5.0 normalization). For pairwise 582

comparison among lamina joint samples of three leaves (Figure 4A), analyses were based on 583

the two replicates, the threshold was set as FDR adjusted p value < 0.05 and FC > 2.0. For 584

comparison between developmental stages of lamina joint (Figure 4B), samples at same 585

stage of three leaves were used as replicates. For comparison between lamina joint and 586

adjacent leaf parts (Figure S3A), all lamina joint samples were used as replicates and two 587

samples of adjacent leaf parts were used as leaf replicates. Different criteria were tested to 588

identify DEGs and adjusted p value < 0.05, FC > 2.0 was finally used for analysis. For 589



28

comparison between lc1-D mutant and the corresponding control ZH11 lamina joint (Figure 590

7C), p value < 0.05, FC > 2.0 was used. 591

Identified DEGs were gathered after discarding the duplicate ones. The remaining genes 592

average expression values of the replicates were normalized across all developmental stages 593

using the MultiExperiment Viewer 4.9 (MeV4.9; Saeed et al., 2003; 594

http://www.tm4.org/mev.html). K-means clustering with Euclidean distance was used to 595

group genes based on merit analysis. Heat map of gene expression values were generated in 596

MeV4.8 or Microsoft Excel. The hierarchical clustering were used average linkage 597

clustering and Pearson correlation within MeV4.8. 598

599

Gene Ontology Analysis 600

To annotate functions of identified gene sets, the gene ontology information from AgriGO 601

(Du et al., 2010; http://bioinfo.cau.edu.cn/agriGO/analysis.php), Rice Genome Annotation 602

(Kawahara et al., 2013; http://rice.plantbiology.msu.edu/) and Arabidopsis annotation 603

(ftp://ftp.arabidopsis.org/home/tair/Ontologies/Gene_Ontology/) were used. Gene Ontology 604

analysis was performed using BiNGO software (Maere et al., 2005), which works as a 605

Cytoscape plugin (Shannon et al., 2003). GO enrichment was derived with Fisher’s exact test 606

and a cutoff of FDR < 0.05. Only biological process GO terms were summarized using 607

REVIGO (Supek et al., 2011) and shown. 608

609

Gene Family Enrichment Analysis 610

Rice transcription factors (TFs) and other transcriptional regulators (OTRs) were referred to 611

plant transcription factor databases PlnTFDB (Perez-Rodriguez et al., 2010; 612

http://plntfdb.bio.uni-potsdam.de/v3.0/) and PlantTFDB (Jin et al., 2014; 613

http://planttfdb.cbi.pku.edu.cn/). TFs and OTRs were gathered from the two websites after 614

discarding the duplicates. Kinase genes were referred to Rice Kinase Database (RKD) (Jung 615

et al., 2010; http://ricephylogenomics.ucdavis.edu/kinase/). Differentially expressed TFs or 616

kinases were extracted from figure 4C. Hypergeometric distribution analysis was performed 617

to identify transcription factor or kinase families enriched in cluster-grouped data sets. 618

619

Cis-elements Enrichment Analysis 620

Upstream sequence of each gene (up to 1000 nt from ATG) was extracted from the genome 621

and known cis-elements were mapped onto the promoters using Plant Cis-acting Regulatory 622



29

DNA Elements (PLACE) (Higo et al., 1999; http://www.dna.affrc.go.jp/htdocs/PLACE/). 623

The ratio of each cis-element in a particular group was compared with that in the whole 624

genome followed by performing Hypergeometric distribution analysis. Raw p values were 625

adjusted for multiple comparisons by the Benjamini-Hochberg procedure, which controls the 626

false discovery rate. If a known cis-element was enriched with a low adjusted p value < 0.05, 627

which will be annotated as enrichment in the promoters in a certain group. 628

629

Quantification of Various Hormones 630

The lamina joints of ZH11 last leaf at 60, 65, 70 and 80 DAS (corresponding to stages S2, S4, 631

S5 and S6) and 0.5-cm adjacent part of lamina joint of last leaf blade at 60 and 65 DAS 632

(corresponding to stages S2 and S4, as leaf samples) were collected for quantification assays 633

of various hormones (Liu et al., 2010). 634

Auxin (IAA), abscisic acid (ABA), salicylic acid (SA), jasmonic acid (JA) and zeatin 635

(cytokinin) contents were measured by liquid chromatography-tandem mass spectrometry 636

(LC-MS/MS 8030 plus, Shimadzu, Japan) as follows. 200 mg fresh sample was frozen by 637

liquid nitrogen and well homogenized using a TissueLyser homogenizer (QIAGEN, 638

Germany). Following the addition of 1.0 mL of 80% methanol, homogenates were well 639

mixed in an ultrasonic bath and kept overnight (4°C). After centrifugation at 15200 g for 10 640

min, the supernatant was collected and vacuumed to dryness in a Jouan RCT-60 concentrator. 641

Dried extract was dissolved in 200 µL of sodium phosphate solution (0.1 mol/L, pH 7.8) and 642

later passed through a Sep-Pak C18 cartridge (Waters, USA) eluted with 1.5 mL of 80% 643

methanol. The eluate was vacuumed to dryness again and dissolved in 10 mL of 10% 644

methanol, 5 µL solution was then injected into the LC-MS/MS system. 645

Liquid chromatography was performed using a 2.0 mm I.D. X 75 mm Shim-pack XR 646

ODS I column (2.2 μm, Shimadzu, Japan) under a column temperature of 40°C. The mobile 647

phase comprised of solvent A (0.02%, v/v, aqueous acetic acid) and solvent B (100%, v/v, 648

methanol) was employed in a gradient mode [time / A concentration / B concentration (min / % 649

/ %) for 0 / 90 / 10; 5 / 10 / 90; 6 / 10 /90; 6.1 / 80 / 20] at an eluant flow rate of 0.3 mL/min. 650

The mass system was set to multiple reaction monitoring (MRM) mode using electrospray 651

ionization (ESI) for different hormones. For IAA, ABA, JA and SA, negative ion mode was 652

used. For zeatin, positive ion mode was used. Operation conditions including nebulizing gas 653

flow, drying gas flow, desolvation temperature, heat block temperature were respectively 654

optimized for different hormones using standards. Deuteriums labeled hormones (Olchemim, 655



30

Czech Republic) were used as internal standards. Collision energy of -16 eV and 656

mass-to-charge ratio (m/z) of 174.2 for IAA, collision energy of 11 eV and m/z of 263.2 for 657

ABA, collision energy of 15 eV and m/z of 209.2 for JA, collision energy of 28 eV and m/z 658

of 137 for SA, collision energy of 32 eV and m/z of 218 for zeatin, were respectively 659

employed. 660

661

Identification of lc3 Mutant and Quantitative Real-Time-PCR (qRT-PCR) Analysis 662

T-DNA insertion was confirmed by PCR using primers LP 663

(5'-GCAAACTCTTCCTCTTTCCGAC-3') and LB-3 (5'-CCTAAAACCAAAATCCAG-3'), 664

LB-2 (5'-GTGTTGAGCATATAAGAAACCCTTAG-3'), or LB-1 665

(5'-TAGGGTTCCTATAGGGTTTCGCTCA-3'). Identified homozygous lines were used for 666

analysis. 667

qRT-PCR analysis was performed to examine the expression level of LC3 in WT and lc3 668

mutant. Total RNAs were extracted from flag leaf (10 days after heading) with Trizol 669

solution and reverse-transcribed. qRT-PCR analyses were carried out on the BIO-RAD CFX 670

CONNECTTM Real-Time PCR Detection Systems with a SYBR green probe (SYBR 671

Premix Ex Taq System, TaKaRa) using primers 672

(5'-GGTGAAAAGACATCCACAAACGA-3' and 673

5'-TATGAGTCAATGGTCCGCAAGA-3'). Rice Actin gene (03g50890) was amplified 674

(primers 5'-CCTTCAACACCCCTGCTATG-3' and 5'-TGAGTAACCACGCTCCGTCA-3') 675

and used as internal reference control. 676



31

Acknowledgements 677

678

We thank Ms. Jian-Hua Tong at Hunan Agricultural University for measurement of various 679

phytohormones. 680

681

Supplemental Data 682

Supplemental Figure 1. Cytological dynamics of lamina joint of rice flag leaf by longitudinal 683

section analysis. 684

Supplemental Figure 2. Expression patterns of previous reported genes regulating lamina 685

joint development. 686

Supplemental Figure 3. Differentially expressed genes between lamina joint and adjacent 687

leaf parts. 688

Supplemental Figure 4. Transcription factors showing differential expressions between 689

lamina joint and adjacent leaf parts. 690

Supplemental Figure 5. Schematic diagram of hormonal biosynthesis and signaling 691

pathways. 692

Supplemental Figure 6. Differentially expressed hormone-related genes between lamina joint 693

and adjacent leaf parts. 694

Supplemental Figure 7. Auxin-regulated genes involved in lamina joint development. 695



32

Table 1. Developmental and Cytological Changes during Lamina Joint (LJ) Growth. 696

697

Stages Morphology Cytology S1 (Initiation ) A ligule and a pair of auricles

differentiate at the LJ initiation site.

LJ is hollow and transparent.

No aerenchyma in LJ, which is full with parenchyma cells except vascular bundles arranged at the abaxial side.

Small parenchyma cell clusters at adaxial side and abaxial region between developing vascular bundles.

The periphery of abaxial vascular bundles protrude to form ridges.

S2 (Young) LJ, leaf blade and sheath are white or creamy yellow.

LJ protrudes and becomes larger.

LJ size increases mainly due to the extensive expansion of parenchyma cells.

Programmed cell death (PCD) of mature large parenchyma cells occurs to form small holes.

Longitudinal holes connect and fuse to form intact aerenchyma.

S3 (Young) Leaf continues to elongate and leaf blade expands.

LJ is still enclosed by the prior leaf sheath.

Leaf blade and sheath become green, while LJ is white (distinguishable with each other).

A pair of horn-shaped auricles and a tongue-like ligule can be observed.

Rapid cell division between the vascular bundles and epidermis cells at abaxial domain.

Small parenchyma cell clusters are formed at adaxial side.

Parenchyma cells continue expanding. Large and small vascular bundles

locating at abaxial side develop continuously.

S4 (Maturation) Leaf blade and sheath fully develop.

LJ emerges from prior leaf sheath and is exposed in the air.

LJ is firm and plump. LJ starts to bend.

Thickenness of cell walls of small-cell-clusters results in the formation of sclerenchyma cell clusters.

Newly formed sclerenchyma cells at both sides perforate through longitudinally to form sclerenchyma fibers.

Vascular bundles and nearby wall-thickened small-cell-clusters at adaxial side form ridges along the longitudinal direction.

Parenchyma cells stop proliferation. The periphery of whole LJ become

smooth and transverse size of LJ achieve the maximum.

S5 (Post-maturation)

LJ adaxial side elongates and bends to the abaxial side to form a curvature, resulting in the increasing leaf angle.

Ongoing thickenness of cell walls of small-cell-clusters at both sides.

Parenchyma cells at adaxial side undergo longitudinal elongation.

Asymmetric cell growth between adaxial and abaxial sides leads to the increased leaf inclination.

S6 (Senescence) LJ approaches the maximum angle and begins to wither due to the loss of water.

Large aerenchyma and fewer layers of parenchyma cells.

LJ is dehydrated and distorted.



33

Figure legends 698

699

Figure 1. Morphological and cytological observation of rice lamina joint. 700

A. Morphologies of lamina joint of rice flag leaf at 2, 3, 5, 8, 13 or 23 days (corresponding 701

to stages 1-6) after lamina joint initiation (DAI). Representative images are shown. 702

Bar=1 cm. 703

B. Statistics of lamina joint inclination of rice leaves. Angles (0) of each lamina joint at 704

different days after sowing were measured and statistically analyzed. Rice leaves from 705

bottom (13th leaf, the first full leaf) to flag leaf (1st leaf) were analyzed. Experiments 706

were biologically repeated 3 times and data are shown as means ± SD (n > 10). 707

C. Comparison of cytology between lamina joint and midrib of mature leaf (8th leaf was 708

used as representative) by cross section analysis. Highlighted and magnified differences 709

include layer and cell numbers of abaxial sclerenchyma cells (1) and adaxial 710

sclerenchyma cells (2); the mesophyll cells in midrib were replaced by multiple layers of 711

large parenchyma cells in lamina joint (3). aer, aerenchyma; lvb, large vascular bundle; 712

svb, small vascular bundle; ph, phloem; xy, xylem; scc, sclerenchyma cluster; pc, 713

parenchyma cell; mc, mesophyll cell. Bar=200 μm. 714

D. Longitudinal section of lamina joint of mature flag leaf. aer, aerenchyma; vb, vascular 715

bundle; scc, sclerenchyma cluster; pc, parenchyma cell. Bar=200 μm. 716

717

Figure 2. Cytological dynamics of lamina joint development. 718

A. Cytological dynamics of lamina joint from initiation to maturation (left, bar=200 μm), 719

which can be divided as 6 stages (S1-S6). Lamina joint of 8th leaf was observed by cross 720

section and the adaxial (middle, bar=100 μm) and abaxial side (right, bar=100 μm) were 721

enlarged, respectively. 722

B. Statistics of cytological changes of lamina joint at different developmental stages. 723

Lamina joints of 1st - 3rd and 8th - 10th leaf were cross sectioned at different days after 724

sowing and sizes of horizontal area, adaxial sclerenchyma cluster, adaxial parenchyma 725

cells, were measured and statistically analyzed. Data are shown as means ± SD (n = 3). 726

727

Figure 3. Genome-wide gene expression profiles of rice lamina joint. 728

A. Principal component analysis (PCA) reveals the spatial and temporal features of 729

examined samples (with repetition). Samples were named as: 1-S2.1, first repetition of 730



34

lamina joint of 1st leaf at stage 2; 3-S4.2, second repetition of lamina joint of 3rd leaf at 731

stage 4. L, adjacent leaf parts. 732

B. Number of genes showing differential expressions between every two developmental 733

stages (S2-S4, S2-S5, S2-S6, S4-S5, S5-S6, or S4-S6) of lamina joints from flag leaf (1st 734

leaf), last 2nd and 3rd leaves respectively. Numbers of genes encoding transcription 735

factors (TFs), kinases or others are shown. 736

C. Numbers of differentially expressed genes between two continuous stages of lamina 737

joints of last three leaves. 738

D. Heat map of differentially expressed genes (identified in B), which can be classified into 739

six distinct patterns (clusters 1-6) by K-means clustering method. Expression values 740

were scaled per gene across samples and shown as the scaled expression. Diagrams of 741

the expression patterns are shown (right) and gene numbers of each cluster are indicated. 742

E. Enriched GO process terms for clusters 1-6 (from C), which were summarized by using 743

REVIGO. Column length indicates the overrepresentation significance of a group of GO 744

terms. 745

746

Figure 4. Expression profiles of DEGs encoding transcription factors and kinases 747

during lamina joint development. 748

Numbers of differentially expressed genes and enrichment of a given gene family encoding 749

transcription factors (A) or kinases (B) are shown. Gene members presenting expression 750

patterns (C1-C6, as described in 3D) or members of a dedicated gene family are indicated. 751

Enrichment of the gene family is indicated by calculating the p values by Fisher's Exact Test. 752

753

Figure 5. Expression profiles of cell cycle, cell wall synthesis and cell expansion related 754

genes during lamina joint development. 755

Heat map shows the expression profiles of genes related to cell cycle (cyclins, 756

cyclin-dependent-kinases (CDK) and other core cell cycle regulators; A), cell expansion 757

(expansins, EXPs; B), and cell wall synthesis (cellulose synthase genes, CESA; cellulose 758

synthase-like genes, CSL; C) at four developmental stages of lamina joint and adjacent leaf 759

parts, which are shown as the unscaled log2 expression level. Gene expression patterns are 760

indicated (C1-C6, as described in 3D). 761

762

Figure 6. Expression profiles of hormone related genes during lamina joint 763



35

development. 764

A. Expression patterns of differentially expressed hormone-related genes at four 765

developmental stages of lamina joint and adjacent leaf parts, which are shown as the 766

unscaled log2 expression. Processes (types) of genes involving in hormone biosynthesis 767

and signaling are indicated in supplemental figure 5. 768

B. Amounts of various hormones at four developmental stages of lamina joint and adjacent 769

leaf parts (S2 and S4 stages). For each sample, ~ 30 to 80 lamina joints were collected 770

for assay. Measurement was biologically repeated for three times and data are shown as 771

means ± SD (n=3). 772

773

Figure 7. Expression profile of auxin-related genes and altered genes in lc1-D mutant 774

during lamina joint development. 775

A. Heat map shows the expression patterns of differentially expressed auxin-related genes 776

involving in biosynthesis, signaling and transport at four developmental stages of lamina 777

joint and adjacent leaf parts, which are shown as the unscaled log2 expression. Processes 778

(types) of genes involving in auxin biosynthesis are indicated in supplemental figure 5. 779

B. Hierarchical clustering analysis of all AUX/IAA and ARF genes. Genes with similar 780

expression patterns were grouped by horizontal lines. IAAs and ARFs were distinguished 781

by green or yellow backgrounds. 782

C. Venn diagram of overlapping genes between differentially expressed genes in lc1-D 783

lamina joint and during lamina joint development of ZH11. The lc1-D microarray 784

datasets can be accessed at GEO database (GSE16640). 785

D. GO enrichment analysis of auxin-regulating genes during lamina joint development. 786

Genes were obtained from (C) and GO terms of auxin up- or down-regulated genes are 787

shown in blue or red respectively. P values were calculated by Fisher's Exact Test. 788

789

Figure 8. Identification and phenotypic observation of rice lc3 mutant and schematic 790

model of rice lamina joint development. 791

A. Expressions of Os06g39480 (LC3) gene during lamina joint development at four 792

developmental stages analyzed by Affymetrix Chips. Expression levels are shown as the 793

log2 values. 794

B. Schematic and confirmation of the lc3 mutant. T-DNA insertion position is indicated 795

(upper panel, exons, filled boxes; introns, lines; UTR, empty boxes). Primers LP, RP, 796



36

together with LB-1/2/3, were used to confirm the T-DNA insertion in lc3 and to identify 797

the homozygous lines by PCR amplification using genomic DNA as template (left 798

bottom panel). qRT-PCR analysis confirmed the significantly reduced expression of LC3 799

in mutant (right bottom panel). Transcript levels were normalized with Actin and relative 800

expressions were shown by setting the LC3 expression of WT flag leaf as 1.0. 801

Experiments were biologically repeated for three times and data are shown as means ± 802

SE (n=3). 803

C. Phenotypic observation (left, bar=10 cm) and measurement (right) showed the enlarged 804

leaf inclination of lc3 mutant. Flag leaf angles of WT and lc3 were measured at 10 days 805

after flowering and statistically analyzed by student’s T-test. Data are shown as means ± 806

SD (n>20; **, p<0.01). 807

D. Rice lamina joint development contains distinct developmental stages and is fine 808

controlled by multiple factors. At early initiation stage, auxin, BR, GA, and CK stimulate 809

cell division and expansion, while ethylene, JA and SA control programmed cell death 810

and senescence at later stages. Crucial biological processes are enriched (corresponding 811

genes with distinct expression patterns C1, C2, C4, C5, as described in 4C) and specific 812

transcription factor and kinase families present certain expression patterns to modulate 813

the corresponding cellular biological processes, leading to the specific cytological 814

processes and formation of leaf angle. In the cartoons showing lamina joint anatomies, 815

vascular bundles, sclerenchyma cells and parenchyma cells are highlighted with purple, 816

green or blue shade colors, respectively. 817

E. A schematic model shows how phytohormones synergistically regulate the rice lamina 818

joint development. 819



37

820



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Fonseca S, Chini A, Hamberg M, Adie B, Porzel A, Kramell R, Miersch O, Wasternack C, Solano R (2009) (+)-7-iso-Jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate. Nat Chem Bio 5: 344-350


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http://www.ncbi.nlm.nih.gov/pubmed?term=Benjamini Y%2C Hochberg Y%2E %281995%29%2E Controlling the false discovery rate%3A a practical and powerful approach to multiple testing%2E J R Stat Soc B 57%3A 289%2D300&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Cao HP%2C Chen SK %281995%29 Brassinosteroid%2Dinduced rice lamina joint inclination and its relation to indole%2D3%2Dacetic acid and ethylene%2E Plant Growth Regul 16%3A 189%2D196&dopt=abstract

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http://search.crossref.org/?page=1&rows=2&q=Kappen C (2000) The homeodomain: an ancient evolutionary motif in animals and plants. Comput Chem 24: 95-103

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http://www.ncbi.nlm.nih.gov/pubmed?term=Kawahara Y%2C de la Bastide M%2C Hamilton JP%2C Kanamori H%2C McCombie WR%2C Ouyang S%2C Schwartz DC%2C Tanaka T%2C Wu J%2C Zhou S%2C et al %282013%29 Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data%2E Rice 6%3A 4&dopt=abstract

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

http://scholar.google.com/scholar?as_q=The AtGRF family of putative transcription factors is involved in leaf and cotyledon growth 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 AtGRF family of putative transcription factors is involved in leaf and cotyledon growth in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kim&as_ylo=2003&as_allsubj=all&hl=en&c2coff=1

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http://scholar.google.com/scholar?as_q=LAX and SPA: major regulators of shoot branching in rice&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Komatsu&as_ylo=2003&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Lee J%2C Park JJ%2C Kim SL%2C Yim J%2C An G %282007%29 Mutations in the rice liguleless gene result in a complete loss of the auricle%2C ligule%2C and laminar joint%2E Plant Mol Biol 65%3A 487%2D499&dopt=abstract

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http://scholar.google.com/scholar?as_q=Brassinosteroid signaling regulates leaf erectness in Oryza sativa via the control of a specific U-type cyclin and cell proliferation&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Sun&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

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http://scholar.google.com/scholar?as_q=REVIGO summarizes and visualizes long lists of gene ontology terms.&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=REVIGO summarizes and visualizes long lists of gene ontology terms.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Supek&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Tanaka A%2C Nakagawa H%2C Tomita C%2C Shimatani Z%2C Ohtake M%2C Nomura T%2C Jiang CJ%2C Dubouzet JG%2C Kikuchi S%2C Sekimoto H%2C et al %282009%29 BRASSINOSTEROID UPREGULATED1%2C encoding a helix%2Dloop%2Dhelix protein%2C is a novel gene involved in brassinosteroid signaling and controls bending of the lamina joint in rice%2E Plant Physiol 151%3A 669%2D680&dopt=abstract

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http://scholar.google.com/scholar?as_q=The YABBY gene TONGARI-BOUSHI1 is involved in lateral organ development and maintenance of meristem organization in the rice spikelet&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Tanaka&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

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http://scholar.google.com/scholar?as_q=DWARF AND LOW-TILLERING, a new member of the GRAS family, plays positive roles in brassinosteroid signaling in rice&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Tong&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1


Tong H, Liu L, Jin Y, Du L, Yin Y, Qian Q, Zhu L, Chu C (2012). DWARF AND LOW-TILLERING acts as a direct downstream target ofa GSK3/SHAGGY-like kinase to mediate brassinosteroid responses in rice. Plant Cell 24: 2562-2577.


Tong H, Xiao Y, Liu D, Gao S, Liu L, Yin Y, Jin Y, Qian Q, Chu C (2014) Brassinosteroid regulates cell elongation by modulatinggibberellin metabolism in rice. Plant Cell 26: 4376-4393


Wang D, Pei K, Fu Y, Sun Z, Li S, Liu H, Tang K, Han B, Tao Y (2007b) Genome-wide analysis of the auxin response factors (ARF)gene family in rice (Oryza sativa). Gene 394: 13-24


Wang HH, Hao JJ, Chen XJ, Hao ZN, Wang X, Lou YG, Peng YL, Guo ZJ (2007a) Overexpression of rice WRKY89 enhancesultraviolet B tolerance and disease resistance in rice plants. Plant Mol Biol 65: 799-815


Wang L, Guo K, Li Y, Tu Y, Hu H, Wang B, Cui X, Peng L (2010) Expression profiling and integrative analysis of the CESA/CSLsuperfamily in rice. BMC Plant Biol 10: 282


Wang L, Wang Z, Xu Y, Joo SH, Kim SK, Xue Z, Xu Z, Wang Z, Chong K (2009) OsGSR1 is involved in crosstalk between gibberellinsand brassinosteroids in rice. Plant J 57: 498-510


Wang L, Xu Y, Zhang C, Ma Q, Joo SH, Kim SK, Xu Z, Chong K (2008) OsLIC, a novel CCCH-type zinc finger protein withtranscription activation, mediates rice architecture via brassinosteroids signaling. PLoS One 3: e3521


Wei L, Gu L, Song X, Cui X, Lu Z, Zhou M, Wang L, Hu F, Zhai J, Meyers BC, et al (2014) Dicer-like 3 produces transposableelement-associated 24-nt siRNAs that control agricultural traits in rice. Proc Natl Acad Sci USA 111: 3877-3882


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Wu CY, Trieu A, Radhakrishnan P, Kwok SF, Harris S, Zhang K, Wang J, Wan J, Zhai H, Takatsuto S, Matsumoto S, et al (2008)Brassinosteroids regulate grain filling in rice. Plant Cell 20: 2130-2145


Wu X, Tang D, Li M, Wang K, Cheng Z (2013) Loose Plant Architecture1, an INDETERMINATE DOMAIN protein involved in shootgravitropism, regulates plant architecture in rice. Plant Physiol 161: 317-329


Xia K, Ou X, Tang H, Wang R, Wu P, Jia Y, Wei X, Xu X, Kang SH, Kim SK (2015) Rice microRNA osa-miR1848 targets theobtusifoliol 14alpha-demethylase gene OsCYP51G3 and mediates the biosynthesis of phytosterols and brassinosteroids duringdevelopment and in response to stress. New Phytol 208: 790-802


Yamaguchi T, Nagasawa N, Kawasaki S, Matsuoka M, Nagato Y, Hirano HY (2004) The YABBY gene DROOPING LEAF regulatescarpel specification and midrib development in Oryza sativa. Plant Cell 16: 500-509



http://www.ncbi.nlm.nih.gov/pubmed?term=Tong H%2C Liu L%2C Jin Y%2C Du L%2C Yin Y%2C Qian Q%2C Zhu L%2C Chu C %282012%29%2E DWARF AND LOW%2DTILLERING acts as a direct downstream target of a GSK3%2FSHAGGY%2Dlike kinase to mediate brassinosteroid responses in rice%2E Plant Cell 24%3A 2562%2D2577%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Tong H, Liu L, Jin Y, Du L, Yin Y, Qian Q, Zhu L, Chu C (2012). DWARF AND LOW-TILLERING acts as a direct downstream target of a GSK3/SHAGGY-like kinase to mediate brassinosteroid responses in rice. Plant Cell 24: 2562-2577.


http://scholar.google.com/scholar?as_q=DWARF AND LOW-TILLERING acts as a direct downstream target of a GSK3/SHAGGY-like kinase to mediate brassinosteroid responses 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=DWARF AND LOW-TILLERING acts as a direct downstream target of a GSK3/SHAGGY-like kinase to mediate brassinosteroid responses in rice&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Tong&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Tong H%2C Xiao Y%2C Liu D%2C Gao S%2C Liu L%2C Yin Y%2C Jin Y%2C Qian Q%2C Chu C %282014%29 Brassinosteroid regulates cell elongation by modulating gibberellin metabolism in rice%2E Plant Cell 26%3A 4376%2D4393&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Tong H, Xiao Y, Liu D, Gao S, Liu L, Yin Y, Jin Y, Qian Q, Chu C (2014) Brassinosteroid regulates cell elongation by modulating gibberellin metabolism in rice. Plant Cell 26: 4376-4393


http://scholar.google.com/scholar?as_q=Brassinosteroid regulates cell elongation by modulating gibberellin metabolism 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=Brassinosteroid regulates cell elongation by modulating gibberellin metabolism in rice&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Tong&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Wang D%2C Pei K%2C Fu Y%2C Sun Z%2C Li S%2C Liu H%2C Tang K%2C Han B%2C Tao Y %282007b%29 Genome%2Dwide analysis of the auxin response factors %28ARF%29 gene family in rice %28Oryza sativa%29%2E Gene 394%3A 13%2D24&dopt=abstract

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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=Genome-wide analysis of the auxin response factors (ARF) gene family in rice (Oryza sativa)&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=Genome-wide analysis of the auxin response factors (ARF) gene family in rice (Oryza sativa)&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wang&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Wang HH%2C Hao JJ%2C Chen XJ%2C Hao ZN%2C Wang X%2C Lou YG%2C Peng YL%2C Guo ZJ %282007a%29 Overexpression of rice WRKY89 enhances ultraviolet B tolerance and disease resistance in rice plants%2E Plant Mol Biol 65%3A 799%2D815&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Wang HH, Hao JJ, Chen XJ, Hao ZN, Wang X, Lou YG, Peng YL, Guo ZJ (2007a) Overexpression of rice WRKY89 enhances ultraviolet B tolerance and disease resistance in rice plants. Plant Mol Biol 65: 799-815


http://scholar.google.com/scholar?as_q=Overexpression of rice WRKY89 enhances ultraviolet B tolerance and disease resistance in rice plants&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Overexpression of rice WRKY89 enhances ultraviolet B tolerance and disease resistance in rice plants&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wang&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Wang L%2C Guo K%2C Li Y%2C Tu Y%2C Hu H%2C Wang B%2C Cui X%2C Peng L %282010%29 Expression profiling and integrative analysis of the CESA%2FCSL superfamily in rice%2E BMC Plant Biol 10%3A 282&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Wang L, Guo K, Li Y, Tu Y, Hu H, Wang B, Cui X, Peng L (2010) Expression profiling and integrative analysis of the CESA/CSL superfamily in rice. BMC Plant Biol 10: 282


http://scholar.google.com/scholar?as_q=Expression profiling and integrative analysis of the CESA/CSL superfamily 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=Expression profiling and integrative analysis of the CESA/CSL superfamily in rice.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wang&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Wang L%2C Wang Z%2C Xu Y%2C Joo SH%2C Kim SK%2C Xue Z%2C Xu Z%2C Wang Z%2C Chong K %282009%29 OsGSR1 is involved in crosstalk between gibberellins and brassinosteroids in rice%2E Plant J 57%3A 498%2D510&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Wang L, Wang Z, Xu Y, Joo SH, Kim SK, Xue Z, Xu Z, Wang Z, Chong K (2009) OsGSR1 is involved in crosstalk between gibberellins and brassinosteroids in rice. Plant J 57: 498-510


http://scholar.google.com/scholar?as_q=OsGSR1 is involved in crosstalk between gibberellins and brassinosteroids 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=OsGSR1 is involved in crosstalk between gibberellins and brassinosteroids in rice&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wang&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Wang L%2C Xu Y%2C Zhang C%2C Ma Q%2C Joo SH%2C Kim SK%2C Xu Z%2C Chong K %282008%29 OsLIC%2C a novel CCCH%2Dtype zinc finger protein with transcription activation%2C mediates rice architecture via brassinosteroids signaling%2E PLoS One 3%3A e3521&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Wang L, Xu Y, Zhang C, Ma Q, Joo SH, Kim SK, Xu Z, Chong K (2008) OsLIC, a novel CCCH-type zinc finger protein with transcription activation, mediates rice architecture via brassinosteroids signaling. PLoS One 3: e3521


http://scholar.google.com/scholar?as_q=OsLIC, a novel CCCH-type zinc finger protein with transcription activation, mediates rice architecture via brassinosteroids signaling.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=OsLIC, a novel CCCH-type zinc finger protein with transcription activation, mediates rice architecture via brassinosteroids signaling.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wang&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Wei L%2C Gu L%2C Song X%2C Cui X%2C Lu Z%2C Zhou M%2C Wang L%2C Hu F%2C Zhai J%2C Meyers BC%2C et al %282014%29 Dicer%2Dlike 3 produces transposable element%2Dassociated 24%2Dnt siRNAs that control agricultural traits in rice%2E Proc Natl Acad Sci USA 111%3A 3877%2D3882&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Wei L, Gu L, Song X, Cui X, Lu Z, Zhou M, Wang L, Hu F, Zhai J, Meyers BC, et al (2014) Dicer-like 3 produces transposable element-associated 24-nt siRNAs that control agricultural traits in rice. Proc Natl Acad Sci USA 111: 3877-3882

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http://scholar.google.com/scholar?as_q=Dicer-like 3 produces transposable element-associated 24-nt siRNAs that control agricultural traits in rice&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wei&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Wettenhall JM%2C Smyth GK %282004%29 LimmaGUI%3A a graphical user interface for linear modeling of microarray data%2E Bioinformatics 20%3A 3705%2D3706&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Wettenhall JM, Smyth GK (2004) LimmaGUI: a graphical user interface for linear modeling of microarray data. Bioinformatics 20: 3705-3706

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

http://scholar.google.com/scholar?as_q=LimmaGUI: a graphical user interface for linear modeling of microarray data&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=LimmaGUI: a graphical user interface for linear modeling of microarray data&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wettenhall&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Wu CY%2C Trieu A%2C Radhakrishnan P%2C Kwok SF%2C Harris S%2C Zhang K%2C Wang J%2C Wan J%2C Zhai H%2C Takatsuto S%2C Matsumoto S%2C et al %282008%29 Brassinosteroids regulate grain filling in rice%2E Plant Cell 20%3A 2130%2D2145&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Wu CY, Trieu A, Radhakrishnan P, Kwok SF, Harris S, Zhang K, Wang J, Wan J, Zhai H, Takatsuto S, Matsumoto S, et al (2008) Brassinosteroids regulate grain filling in rice. Plant Cell 20: 2130-2145

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

http://scholar.google.com/scholar?as_q=Brassinosteroids regulate grain filling 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=Brassinosteroids regulate grain filling in rice&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wu&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Wu X%2C Tang D%2C Li M%2C Wang K%2C Cheng Z %282013%29 Loose Plant Architecture1%2C an INDETERMINATE DOMAIN protein involved in shoot gravitropism%2C regulates plant architecture in rice%2E Plant Physiol 161%3A 317%2D329&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Wu X, Tang D, Li M, Wang K, Cheng Z (2013) Loose Plant Architecture1, an INDETERMINATE DOMAIN protein involved in shoot gravitropism, regulates plant architecture in rice. Plant Physiol 161: 317-329

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


http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wu&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Xia K%2C Ou X%2C Tang H%2C Wang R%2C Wu P%2C Jia Y%2C Wei X%2C Xu X%2C Kang SH%2C Kim SK %282015%29 Rice microRNA osa%2DmiR1848 targets the obtusifoliol 14alpha%2Ddemethylase gene OsCYP51G3 and mediates the biosynthesis of phytosterols and brassinosteroids during development and in response to stress%2E New Phytol 208%3A 790%2D802&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Xia K, Ou X, Tang H, Wang R, Wu P, Jia Y, Wei X, Xu X, Kang SH, Kim SK (2015) Rice microRNA osa-miR1848 targets the obtusifoliol 14alpha-demethylase gene OsCYP51G3 and mediates the biosynthesis of phytosterols and brassinosteroids during development and in response to stress. New Phytol 208: 790-802

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

http://scholar.google.com/scholar?as_q=Rice microRNA osa-miR1848 targets the obtusifoliol 14alpha-demethylase gene OsCYP51G3 and mediates the biosynthesis of phytosterols and brassinosteroids during development and in response to stress&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Rice microRNA osa-miR1848 targets the obtusifoliol 14alpha-demethylase gene OsCYP51G3 and mediates the biosynthesis of phytosterols and brassinosteroids during development and in response to stress&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Xia&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Yamaguchi T%2C Nagasawa N%2C Kawasaki S%2C Matsuoka M%2C Nagato Y%2C Hirano HY %282004%29 The YABBY gene DROOPING LEAF regulates carpel specification and midrib development in Oryza sativa%2E Plant Cell 16%3A 500%2D509&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yamaguchi T, Nagasawa N, Kawasaki S, Matsuoka M, Nagato Y, Hirano HY (2004) The YABBY gene DROOPING LEAF regulates carpel specification and midrib development in Oryza sativa. Plant Cell 16: 500-509

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

http://scholar.google.com/scholar?as_q=The YABBY gene DROOPING LEAF regulates carpel specification and midrib development in Oryza sativa&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 YABBY gene DROOPING LEAF regulates carpel specification and midrib development in Oryza sativa&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yamaguchi&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1


Yamamuro C, Ihara Y, Wu X, Noguchi T, Fujioka S, Takatsuto S, Ashikari M, Kitano H, Matsuoka M (2000) Loss of function of a ricebrassinosteroid insensitive1 homolog prevents internode elongation and bending of the lamina joint. Plant Cell 12: 1591-1605


Yang C, Li D, Liu X, Ji C, Hao L, Zhao X, Li X, Chen C, Cheng Z, Zhu L (2014) OsMYB103L, an R2R3-MYB transcription factor,influences leaf rolling and mechanical strength in rice (Oryza sativa L). BMC Plant Biol 14: 158


Yan J, Li S, Gu M, Yao R, Li Y, Chen J, Yang M, Tong J, Xiao L, Nan F, et al (2016) Endogenous bioactive jasmonate is composed ofa set of (+)-7-iso-JA-amino acid conjugates. Plant Physiol 172: 2154-2164


Zhang C, Xu Y, Guo S, Zhu J, Huan Q, Liu H, Wang L, Luo G, Wang X, Chong K (2012). Dynamics of brassinosteroid responsemodulated by negative regulator LIC in rice. PLoS Genet. 8: e1002686.


Zhang L, Bai M, Wu J, Zhu J, Wang H, Zhang Z, Wang W, Sun Y, Zhao J, Sun X, et al (2009a) Antagonistic HLH/bHLH transcriptionfactors mediate brassinosteroid regulation of cell elongation and plant development in rice and Arabidopsis. Plant Cell 21: 3767-3780


Zhang S, Wang S, Xu Y, Yu C, Shen C, Qian Q, Geisler M, Jiang de A, Qi Y (2015) The auxin response factor, OsARF19, controlsrice leaf angles through positively regulating OsGH3-5 and OsBRI1. Plant Cell Environ 38: 638-654


Zhang SW, Li CH, Cao J, Zhang YC, Zhang SQ, Xia YF, Sun DY, Sun Y (2009b) Altered architecture and enhanced drought tolerancein rice via the down-regulation of indole-3-acetic acid by TLD1/OsGH313 activation. Plant Physiol 151: 1889-1901


Zhang ZL, Shin M, Zou X, Huang J, Ho TH, Shen QJ (2009c) A negative regulator encoded by a rice WRKY gene represses bothabscisic acid and gibberellins signaling in aleurone cells. Plant Mol Biol 70: 139-151


Zhao SQ, Hu J, Guo LB, Qian Q, Xue HW (2010) Rice leaf inclination 2, a VIN3-like protein, regulates leaf angle through modulatingcell division of the collar. Cell Res 20: 935-947


Zhao SQ, Xiang JJ, Xue HW (2013) Studies on the rice LEAF INCLINATION1 (LC1), an IAA-amido synthetase, reveal the effects ofauxin in leaf inclination control. Mol Plant 6: 174-187


Zhu N, Cheng S, Liu X, Du H, Dai M, Zhou DX, Yang W, Zhao Y (2015) The R2R3-type MYB gene OsMYB91 has a function incoordinating plant growth and salt stress tolerance in rice. Plant Sci 236: 146-156



http://www.ncbi.nlm.nih.gov/pubmed?term=Yamamuro C%2C Ihara Y%2C Wu X%2C Noguchi T%2C Fujioka S%2C Takatsuto S%2C Ashikari M%2C Kitano H%2C Matsuoka M %282000%29 Loss of function of a rice brassinosteroid insensitive1 homolog prevents internode elongation and bending of the lamina joint%2E Plant Cell 12%3A 1591%2D1605&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yamamuro C, Ihara Y, Wu X, Noguchi T, Fujioka S, Takatsuto S, Ashikari M, Kitano H, Matsuoka M (2000) Loss of function of a rice brassinosteroid insensitive1 homolog prevents internode elongation and bending of the lamina joint. Plant Cell 12: 1591-1605

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

http://scholar.google.com/scholar?as_q=Loss of function of a rice brassinosteroid insensitive1 homolog prevents internode elongation and bending of the lamina joint&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=Loss of function of a rice brassinosteroid insensitive1 homolog prevents internode elongation and bending of the lamina joint&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yamamuro&as_ylo=2000&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Yang C%2C Li D%2C Liu X%2C Ji C%2C Hao L%2C Zhao X%2C Li X%2C Chen C%2C Cheng Z%2C Zhu L %282014%29 OsMYB103L%2C an R2R3%2DMYB transcription factor%2C influences leaf rolling and mechanical strength in rice %28Oryza sativa L%29%2E BMC Plant Biol 14%3A 158&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yang C, Li D, Liu X, Ji C, Hao L, Zhao X, Li X, Chen C, Cheng Z, Zhu L (2014) OsMYB103L, an R2R3-MYB transcription factor, influences leaf rolling and mechanical strength in rice (Oryza sativa L). BMC Plant Biol 14: 158

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

http://scholar.google.com/scholar?as_q=OsMYB103L, an R2R3-MYB transcription factor, influences leaf rolling and mechanical strength in 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=OsMYB103L, an R2R3-MYB transcription factor, influences leaf rolling and mechanical strength in rice (Oryza sativa L).&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yang&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Yan J%2C Li S%2C Gu M%2C Yao R%2C Li Y%2C Chen J%2C Yang M%2C Tong J%2C Xiao L%2C Nan F%2C et al %282016%29 Endogenous bioactive jasmonate is composed of a set of %28%2B%29%2D7%2Diso%2DJA%2Damino acid conjugates%2E Plant Physiol 172%3A 2154%2D2164&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yan J, Li S, Gu M, Yao R, Li Y, Chen J, Yang M, Tong J, Xiao L, Nan F, et al (2016) Endogenous bioactive jasmonate is composed of a set of (+)-7-iso-JA-amino acid conjugates. Plant Physiol 172: 2154-2164

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

http://scholar.google.com/scholar?as_q=Endogenous bioactive jasmonate is composed of a set of (+)-7-iso-JA-amino acid conjugates&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=Endogenous bioactive jasmonate is composed of a set of (+)-7-iso-JA-amino acid conjugates&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yan&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhang C%2C Xu Y%2C Guo S%2C Zhu J%2C Huan Q%2C Liu H%2C Wang L%2C Luo G%2C Wang X%2C Chong K %282012%29%2E Dynamics of brassinosteroid response modulated by negative regulator LIC in rice%2E PLoS Genet%2E 8%3A e1002686%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhang C, Xu Y, Guo S, Zhu J, Huan Q, Liu H, Wang L, Luo G, Wang X, Chong K (2012). Dynamics of brassinosteroid response modulated by negative regulator LIC in rice. PLoS Genet. 8: e1002686.

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=Dynamics of brassinosteroid response modulated by negative regulator LIC 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=Dynamics of brassinosteroid response modulated by negative regulator LIC in rice&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=Zhang L%2C Bai M%2C Wu J%2C Zhu J%2C Wang H%2C Zhang Z%2C Wang W%2C Sun Y%2C Zhao J%2C Sun X%2C et al %282009a%29 Antagonistic HLH%2FbHLH transcription factors mediate brassinosteroid regulation of cell elongation and plant development in rice and Arabidopsis%2E Plant Cell 21%3A 3767%2D3780&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhang L, Bai M, Wu J, Zhu J, Wang H, Zhang Z, Wang W, Sun Y, Zhao J, Sun X, et al (2009a) Antagonistic HLH/bHLH transcription factors mediate brassinosteroid regulation of cell elongation and plant development in rice and Arabidopsis. Plant Cell 21: 3767-3780


http://scholar.google.com/scholar?as_q=Antagonistic HLH/bHLH transcription factors mediate brassinosteroid regulation of cell elongation and plant development in rice and 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=Antagonistic HLH/bHLH transcription factors mediate brassinosteroid regulation of cell elongation and plant development in rice and Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhang S%2C Wang S%2C Xu Y%2C Yu C%2C Shen C%2C Qian Q%2C Geisler M%2C Jiang de A%2C Qi Y %282015%29 The auxin response factor%2C OsARF19%2C controls rice leaf angles through positively regulating OsGH3%2D5 and OsBRI1%2E Plant Cell Environ 38%3A 638%2D654&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhang S, Wang S, Xu Y, Yu C, Shen C, Qian Q, Geisler M, Jiang de A, Qi Y (2015) The auxin response factor, OsARF19, controls rice leaf angles through positively regulating OsGH3-5 and OsBRI1. Plant Cell Environ 38: 638-654



http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhang SW%2C Li CH%2C Cao J%2C Zhang YC%2C Zhang SQ%2C Xia YF%2C Sun DY%2C Sun Y %282009b%29 Altered architecture and enhanced drought tolerance in rice via the down%2Dregulation of indole%2D3%2Dacetic acid by TLD1%2FOsGH313 activation%2E Plant Physiol 151%3A 1889%2D1901&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhang SW, Li CH, Cao J, Zhang YC, Zhang SQ, Xia YF, Sun DY, Sun Y (2009b) Altered architecture and enhanced drought tolerance in rice via the down-regulation of indole-3-acetic acid by TLD1/OsGH313 activation. Plant Physiol 151: 1889-1901


http://scholar.google.com/scholar?as_q=Altered architecture and enhanced drought tolerance in rice via the down-regulation of indole-3-acetic acid by TLD1/OsGH313 activation&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=Altered architecture and enhanced drought tolerance in rice via the down-regulation of indole-3-acetic acid by TLD1/OsGH313 activation&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhang ZL%2C Shin M%2C Zou X%2C Huang J%2C Ho TH%2C Shen QJ %282009c%29 A negative regulator encoded by a rice WRKY gene represses both abscisic acid and gibberellins signaling in aleurone cells%2E Plant Mol Biol 70%3A 139%2D151&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhang ZL, Shin M, Zou X, Huang J, Ho TH, Shen QJ (2009c) A negative regulator encoded by a rice WRKY gene represses both abscisic acid and gibberellins signaling in aleurone cells. Plant Mol Biol 70: 139-151


http://scholar.google.com/scholar?as_q=A negative regulator encoded by a rice WRKY gene represses both abscisic acid and gibberellins signaling in aleurone cells&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=A negative regulator encoded by a rice WRKY gene represses both abscisic acid and gibberellins signaling in aleurone cells&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhao SQ%2C Hu J%2C Guo LB%2C Qian Q%2C Xue HW %282010%29 Rice leaf inclination 2%2C a VIN3%2Dlike protein%2C regulates leaf angle through modulating cell division of the collar%2E Cell Res 20%3A 935%2D947&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhao SQ, Hu J, Guo LB, Qian Q, Xue HW (2010) Rice leaf inclination 2, a VIN3-like protein, regulates leaf angle through modulating cell division of the collar. Cell Res 20: 935-947

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


http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhao&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhao SQ%2C Xiang JJ%2C Xue HW %282013%29 Studies on the rice LEAF INCLINATION1 %28LC1%29%2C an IAA%2Damido synthetase%2C reveal the effects of auxin in leaf inclination control%2E Mol Plant 6%3A 174%2D187&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhao SQ, Xiang JJ, Xue HW (2013) Studies on the rice LEAF INCLINATION1 (LC1), an IAA-amido synthetase, reveal the effects of auxin in leaf inclination control. Mol Plant 6: 174-187

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

http://scholar.google.com/scholar?as_q=Studies on the rice LEAF INCLINATION1 (LC1), an IAA-amido synthetase, reveal the effects of auxin in leaf inclination control&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=Studies on the rice LEAF INCLINATION1 (LC1), an IAA-amido synthetase, reveal the effects of auxin in leaf inclination control&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhao&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhu N%2C Cheng S%2C Liu X%2C Du H%2C Dai M%2C Zhou DX%2C Yang W%2C Zhao Y %282015%29 The R2R3%2Dtype MYB gene OsMYB91 has a function in coordinating plant growth and salt stress tolerance in rice%2E Plant Sci 236%3A 146%2D156&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhu N, Cheng S, Liu X, Du H, Dai M, Zhou DX, Yang W, Zhao Y (2015) The R2R3-type MYB gene OsMYB91 has a function in coordinating plant growth and salt stress tolerance in rice. Plant Sci 236: 146-156

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=The R2R3-type MYB gene OsMYB91 has a function in coordinating plant growth and salt stress tolerance 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 R2R3-type MYB gene OsMYB91 has a function in coordinating plant growth and salt stress tolerance in rice&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhu&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1


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Dynamic cytology and transcriptional regulation of rice ...€¦ · 2017-05-12 · 21 One-sentence summary: A systemic study of dynamic morphology, cytology and 22 transcriptome