OsSHI1 Regulates Plant Architecture Through Modulating the … · 2019-03-25 · 1 1 RESEARCH...

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RESEARCH ARTICLE 1

OsSHI1 Regulates Plant Architecture Through Modulating the 2

Transcriptional Activity of IPA1 in Rice 3

Erchao Duana,1, Yihua Wanga,1, Xiaohui Lia, Qibing Linb, Ting Zhangc, Yupeng 4

Wangb, Chunlei Zhoua, Huan Zhanga, Ling Jianga, Jiulin Wangb, Cailin Leib, Xin 5

Zhangb, Xiuping Guob, Haiyang Wangb, and Jianmin Wana,b,2 6

7 a State Key Laboratory for Crop Genetics and Germplasm Enhancement, Jiangsu Plant 8

Gene Engineering Research Center, Nanjing Agricultural University, Nanjing 210095, 9

China 10 b National Key Facility for Crop Gene Resources and Genetic Improvement, Institute 11

of Crop Science, Chinese Academy of Agricultural Sciences, Beijing 100081, China 12 c College of Horticulture, Nanjing Agricultural University, Nanjing 210095, China 13 1 These authors contributed equally to this work. 14 2 Address correspondence to [email protected]. 15

The author responsible for distribution of materials integral to the findings presented 16

in this article in accordance with the policy described in the Instructions for Authors 17

(www.plantcell.org) is: Jianmin Wan ([email protected]). 18

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Short title: OsSHI1 regulates plant architecture in rice 20

One-sentence summary: OsSHI1 represses the DNA binding activity of IPA1 to 21

regulate plant architecture in rice. 22

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ABSTRACT 24

Tillering and panicle branching are important determinants of plant architecture and 25

yield potential in rice (Oryza sativa). IDEAL PLANT ARCHITECTURE1 (IPA1) 26

encodes OsSPL14, which acts as a key transcription factor regulating tiller outgrowth 27

and panicle branching by directly activating the expression of OsTB1 and OsDEP1，28

thereby influencing grain yield in rice. Here, we report the identification of a rice 29

mutant named shi1 that is characterized by dramatically reduced tiller number, 30

enhanced culm strength and increased panicle branch number. Map-based cloning 31

revealed that OsSHI1 encodes a plant-specific transcription factor of the SHORT 32

INTERNODES (SHI) family with a characteristic family-specific IGGH domain and 33

a conserved zinc-finger DNA binding domain. Consistent with the mutant phenotype, 34

OsSHI1 is predominantly expressed in axillary buds and young panicle, and its 35

encoded protein is exclusively targeted to the nucleus. We show that OsSHI1 36

physically interacts with IPA1 both in vitro and in vivo. Moreover, OsSHI1 could bind 37

directly to the promoter regions of both OsTB1 and OsDEP1 through a previously 38

unrecognized cis-element (T/GCTCTAC motif). OsSHI1 repressed the transcriptional 39

activation activity of IPA1 by affecting its DNA binding activity towards the 40

promoters of both OsTB1 and OsDEP1, resulting in increased tiller number and 41

Plant Cell Advance Publication. Published on March 25, 2019, doi:10.1105/tpc.19.00023

©2019 American Society of Plant Biologists. All Rights Reserved

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diminished panicle size. Taken together, our results demonstrate that OsSHI1 42

regulates plant architecture through modulating the transcriptional activity of IPA1 43

and provide insight into the establishment of plant architecture in rice. 44

45

Key words: Rice (Oryza sativa), SHORT INTERNODE1 (OsSHI1), IDEAL PLANT 46

ARCHITECTURE1 (IPA1), Tillering, Panicle branching 47

48

INTRODUCTION 49

As a major staple crop worldwide, the yield of rice is multiplicatively determined by 50

three major agronomic traits: panicle number, grain number per panicle and grain 51

weight. The numbers of panicles and grains per panicle are mainly determined by the 52

ability of the plant to produce tillers, the primary and secondary branches of the 53

panicle. These traits are also important determinants of overall plant architecture in 54

rice (Wang and Li, 2008; Xing and Zhang, 2010; Wang et al., 2018a). 55

The formation of a tiller can be divided into two consecutive steps: tiller bud 56

formation and outgrowth, both of which are regulated by elaborate cross-talk between 57

hormonal, developmental and environmental factors (Domagalska and Leyser, 2011). 58

Recent molecular and genetic studies have revealed much insight into the control of 59

bud formation in both dicots and monocots. Rice MONOCULM1 (MOC1) encodes a 60

transcription factor of the GRAS family orthologous to LS of tomato (Solanum 61

lycopersicum) and LAS of Arabidopsis (Arabidopsis thaliana) (Schumacher et al., 62

1999; Greb et al., 2003; Li et al., 2003). The rice moc1 mutant has no tillers due to the 63

defect in axillary meristem (AM) formation which is similar to the phenotype of the 64

tomato ls mutant, implying that LS/LAS/MOC1 plays a conserved role in maintaining 65

the potential for AM initiation in both monocots and dicots. Further studies 66

demonstrated that TAD1 (also named TE) acts as a component of the APC/CTAD1/TE 67

E3 ligase to modulate tiller bud formation by facilitating the degradation of MOC1 68

(Lin et al., 2012; Xu et al., 2012). 69

Studies of various branching mutants, such as the dwarf (d) mutants in rice (Arite et 70

al., 2007 and 2009; Gao et al., 2009; Lin et al., 2009; Jiang et al., 2013; Zhou et al., 71

2013), more axillary growth (max) mutants in Arabidopsis (Sorefan et al., 2003; 72

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Booker et al., 2004 and 2005; Stirnberg et al., 2007), ramosus (rms) mutants in pea 73

(Pisum sativum) (Sorefan et al., 2003; Johnson et al., 2006) and decreased apical 74

dominance (dad) mutants in petunia (Petunia hybrida) (Snowden et al., 2005) 75

revealed an essential role of the plant hormone strigolactones (SLs) in bud outgrowth. 76

Deficiencies in both SL production and signaling lead to excessive outgrowth of the 77

axillary buds (Smith and Li, 2014). Recent studies have demonstrated that SLs repress 78

tiller outgrowth through promoting the degradation of a central repressor protein, D53 79

(Jiang et al., 2013; Zhou et al., 2013). 80

SQUAMOSA PROMOTER BINDING PROTEIN-box genes (SBP-box genes) 81

encode plant-specific transcription factors that share a highly conserved DNA binding 82

domain, the SBP domain. At least 18 putative SPL genes exist in the rice genome, and 83

most of them are regulatory targets of OsmiR156 (Xie et al., 2006). Several members 84

of the SPL family, OsSPL7, OsSPL13, OsSPL14, OsSPL16 and OsSPL17, have been 85

shown to regulate vegetative and inflorescence architecture in rice (Jiao et al., 2010; 86

Miura et al., 2010；Wang et al., 2012; Wang et al., 2015a; Wang et al., 2015b; Liu et 87

al., 2016; Si et al., 2016; Wang et al., 2017a). Among these factors, OsSPL14，also 88

known as IDEAL PLANT ARCHITECTURE1 (IPA1) or WEALTHY FARMER’S 89

PANICLE (WFP), is the best studied so far (we use IPA1 hereafter). It is 90

predominantly expressed in the shoot apex at both the vegetative and reproductive 91

stages. A C-to-T SNP (Single Nucleotide Polymorphism) that escapes miR156 92

targeting or increasing IPA1 expression via epigenetic regulation confers an ideal 93

plant architecture to rice, including reduced tiller number, stronger culm, enlarged 94

panicle and ultimately, enhanced grain yield (Jiao et al., 2010; Miura et al., 2010). 95

IPA1 binds directly to the promoter regions of several important regulators of rice 96

plant architecture, including TEOSINTE BRANCHED1 (OsTB1), DENSE AND 97

ERECT PANICLE1 (OsDEP1), LONELY GUY (LOG), SLENDER RICE1 (SLR1) and 98

PIN-FORMED (PIN1b) (Lu et al., 2013), as well as WRKY45 to promote both yield 99

and immunity in rice (Wang et al., 2018b). OsTB1, a transcription factor of the TCP 100

family, is also referred to as FINE CULM1 (FC1) and was initially identified as a 101

counterpart of maize (Zea mays) TEOSINTE BRANCHED 1 (TB1), which is involved 102

4

in inhibiting lateral branching in maize (Doebley et al., 1995; Lukens et al., 2001; 103

Dong et al., 2017). Later studies confirmed that OsTB1 also acts to suppress axillary 104

buds outgrowth in rice (Takeda et al., 2003; Minakuchi et al., 2010). OsDEP1 encodes 105

the γ subunit of the heterotrimeric G protein complex. Gain-of-function mutation of 106

OsDEP1 results in increased primary and secondary branches and number of grains 107

per panicle and consequently, increased grain yield (Huang et al., 2009). In addition, 108

recent studies implicated OsDEP1 in regulating nitrogen-use efficiency and grain size 109

determinacy in rice (Sun et al., 2014; Liu et al., 2018; Sun et al., 2018). 110

The Arabidopsis SHI family contains ten members referred to as SHORT 111

INTERNODES (SHI), STYLISH1 (STY1), STYLISH2 (STY2), SHI-RELATED 112

SEQUENCE 3 to 8 (SRS3 to SRS8) and LATERAL ROOT PRIMORDIUM1 (LRP1). 113

This gene family encodes plant-specific transcription factors characterized by a 114

conserved zinc finger domain of cysteine/histidine consensus sequence C3HC3H and a 115

unique IGGH domain (Fridborg et al., 2001). Genetic studies of shi-related mutants 116

implied that SHI family members play indispensable roles for gynoecium and leaf 117

development and photomorphogenesis in Arabidopsis, probably by regulating auxin 118

homeostasis or expression of HY5, BBX21, and BBX22 (Smith and Fedoroff, 1995; 119

Fridborg et al., 1999 and 2001; Kuusk et al., 2002 and 2006; Sohlberg et al., 2006; 120

Eklund et al., 2010; Baylis et al., 2013; Yuan et al., 2018). In addition, SHORT AWN 2 121

(LKS2) and SIX-ROWED SPIKE 2 (VRS2), encoding two SHI family transcription 122

factors, regulate awn elongation, pistil morphology and inflorescence patterning in 123

barley (Hordeum vulgare) (Yuo et al., 2012; Youssef et al., 2017). However, the 124

precise roles and significance of this gene family in regulating rice development and 125

plant architecture establishment are still not well characterized. 126

In this study, we characterize a rice mutant named short internode1 (shi1), which 127

has significantly reduced tiller number, enhanced culm strength and increased panicle 128

branch numbers. Molecular cloning revealed that the mutant defects are caused by 129

deletion of the SHI family gene OsSHI1. We show that OsSHI1 regulates tillering and 130

panicle branching through physical interacting with IPA1 and modulating its 131

transcriptional activity on downstream target genes. 132

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RESULTS 135

Characterization of the shi1 Mutant Phenotype 136

In a screen for regulators of plant architecture in rice, we identified the shi1 mutant 137

from a 60Co-γ irradiation-induced mutant population of the indica cultivar 9311. 138

Compared with the wild type, shi1 exhibited dramatically reduced tiller number from 139

the 4th-leaf stage to the mature stage (Figure 1A to 1H). Histological analysis 140

revealed that axillary bud initiation was largely normal; however, the outgrowth of 141

axillary buds was obviously delayed in the shi1 mutant (Supplemental Figure 1). 142

Notably, shi1 had a more compact plant architecture with significantly reduced tiller 143

number at the reproductive developmental stage, compared with the wild-type plant 144

(Figure 1H and 1I). Panicles of shi1 were also more compact and erect with slightly 145

increased primary branch number and substantially increased secondary branch and 146

spikelet numbers (Figure 1J to 1N). However, due to the trade-off between spikelet 147

number and grain size and various defects in floral organ development, the grain size, 148

1,000-grain weight as well as the seed setting rate of shi1 were significantly reduced 149

(Supplemental Figure 2A to 2C). Leaves of shi1 were shorter but wider, especially for 150

the flag leaves (Supplemental Figure 2D to 2F), and more dark-green with increased 151

chlorophyll contents (Supplemental Figure 2G). More strikingly, the culm diameters 152

of shi1 were greatly increased due to the increased parenchyma tissue layers and 153

vascular bundles (Supplemental Figure 2H to 2M). These observations suggest that 154

OsSHI1 plays a pleiotropic role in regulating plant architecture establishment in rice. 155

156

Map-based Cloning of OsSHI1 157

Genetic analysis of two F2 populations derived from the reciprocal crosses between 158

shi1 and WT (9311) indicated that the shi1 phenotype is controlled by a single 159

recessive nuclear locus, given that the numbers of wild-type and mutant individuals 160

approximately fit the expected 3:1 ratio (Supplemental Table 1). 161

To identify the causal gene, an F2 population was generated from a cross between 162

shi1 and 02428 (O. sativa L. ssp. japonica). Linkage analysis revealed that the 163

OsSHI1 locus is associated with the Simple Sequence Repeat (SSR) markers RM107 164

7and RM189 on the long arm of chromosome 9. Subsequent fine-mapping using 7,547 165

8progeny from the F2 population delimited the OsSHI1 locus to a 50 kb region with 4 166

9

predicted Open Reading Frames (ORFs) (Figure 2A). Sequencing and PCR analysis 167

revealed that a ~18 kb genomic region covering ORF2 is deleted in the shi1 mutant 168

(Figure 2A and 2B), but no DNA sequence alterations were found in the promoter and 169

coding regions of ORF1, ORF3 and ORF4. Further, reverse transcriptase (RT)-PCR 170

analysis and immunoblot analysis using anti-OsSHI1 specific polyclonal antibodies 171

confirmed no expression of ORF2 in the shi1 mutant (Figure 2C and 2D). These 172

results suggest that ORF2 likely corresponds to OsSHI1. 173

To verify whether ORF2 is indeed responsible for the shi1 phenotype, a ~5 kb 174

genomic fragment of ORF2 (full length ORF2 including 3 kb promoter, two exons, 175

one intron and a 400 bp downstream region) was transformed into shi1. As expected, 176

positive transgenic plants displayed normal plant development with recovered tiller 177

numbers (Figure 2E and 2F). Moreover, ORF2 knockout transgenic plants generated 178

by CRISPR/Cas9 genome-editing approach (in Kitaake background, O. sativa L. ssp. 179

japonica) showed reduced tiller number, but increased panicle branch number, 180

compared with the wild-type plants (Kitaake) (Supplemental Figure 3). On the 181

contrary, the ORF2 overexpression lines had reduced plant height (Supplemental 182

Figure 4A and 4B) and ectopic tillers usually formed at the upper internodes 183

(Supplemental Figure 4C and 4D). At the reproductive developmental stage, the 184

primary and especially secondary branch numbers of ORF2 overexpression lines were 185

remarkably decreased (Supplemental Figure 4E to 4G). Taken together, these 186

molecular and genetic lines of evidence confirmed that ORF2 indeed represents 187

OsSHI1. 188

189

Expression Pattern of OsSHI1 190

Sequence analysis revealed that OsSHI1 encodes a transcription factor homologous to 191

the Arabidopsis SHI family with the intrinsic C3HC3H zinc finger domain and the SHI 192

family-specific IGGH domain (Figure 3A, Supplemental Figure 5). Consistent with its 193

function as a transcription factor, transient expression analysis in rice protoplasts 194

showed that the OsSHI1-GFP fusion protein was exclusively localized to the nucleus 195

(Figure 3B). The transactivation activity assay indicated that OsSHI1 exhibited weak 196

10transcriptional activation activity in yeast cells (Supplemental Figure 6) and was 197

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capable of forming homodimer via its C terminus (Figure 3C). RT-qPCR analysis 198

revealed that OsSHI1 was expressed in various tissues, with higher transcript 199

abundance being detected in root, young panicle and axillary buds (Figure 3D). 200

Histochemical staining analysis of the pOsSHI1:GUS transgenic plants showed strong 201

GUS staining in root, young panicle and axillary buds, but not in the culm, leaf blade 202

or leaf sheath, further confirming that the OsSHI1 promoter is active in these tissues 203

(Supplemental Figure 7). Moreover, immunoblot analysis using anti-OsSHI1 specific 204

antibodies (Supplemental Figure 8) validated that OsSHI1 protein was mainly 205

accumulated in young panicle and axillary buds, consistent with its role in regulating 206

tiller and panicle development (Figure 3E). 207

208

OsSHI1 Physically Interacts with IPA1 209

To elucidate the regulatory mechanism of OsSHI1 on rice tiller and panicle 210

development, a yeast two-hybrid screening was performed to identify the interacting 211

partners of OsSHI1 (Supplemental Table 2). Intriguingly, two positive clones 212

containing the coding region of IPA1 were isolated. Considering that IPA1 plays a 213

critical role in the establishment of rice plant architecture, we pursued their interaction 214

and physiological significance further. Dissection of their interactive domains showed 215

that both the N and C terminal regions of OsSHI1 could interact with the C-terminus, 216

but not the SBP domain of IPA1 (Figure 4A and 4B). The interaction between IPA1 217

and OsSHI1 was further confirmed by in vitro pull-down assay (Figure 4C, 218

Supplemental Figure 9), in vivo bimolecular fluorescence complementation (BiFC) 219

assay in leaf epidermal cells of Nicotiana benthamiana (Figure 4D) and 220

co-immunoprecipitation (Co-IP) assay in axillary buds of wild-type seedlings (Figure 221

4E). 222

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OsSHI1 Directly and Negatively Regulates the Expression of OsTB1 and OsDEP1 224

Previous reports revealed that IPA1 directly activates the expression of OsTB1 and 225

OsDEP1, two key regulators for tiller and panicle development in rice (Jiao et al., 226

2010; Lu et al., 2013). The SBP-box of IPA1 functions as the conserved DNA binding 227

12domain and its C-terminus confers transcriptional activation activity (Lu et al., 2013). 228

13As the shi1 mutants exhibited reduced tillers and increased panicle branch number, we 229

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speculated that OsSHI1 may act together with IPA1 to co-regulate the expression of 230

OsTB1 and OsDEP1. In support of this notion, RT-qPCR analysis revealed that indeed, 231

the expression levels of both OsTB1 and OsDEP1 were significantly increased in the 232

shi1 background (Figure 5A and 5B). Sequence analysis identified two and one 233

T/GCTCTAC motifs in the promoter regions of OsTB1 and OsDEP1, respectively. 234

Notably, these elements are quite similar to the binding motif (ACTCTAC) of the 235

Arabidopsis AtSTY1 homologous protein (Eklund et al., 2010). Intriguingly, these 236

T/GCTCTAC motifs are located near the IPA1 recognition sites (GTAC) in the 237

promoter regions of both OsTB1 (59 bp) and OsDEP1 (113 bp) (Supplemental 238

Figures 10 and 11), hinting that OsSHI1 and IPA1 may coordinately regulate the 239

expression of OsTB1 and OsDEP1 to affect plant architecture. 240

To test this, we first performed yeast one-hybrid assay to test for direct binding of 241

OsSHI1 to the OsTB1 and OsDEP1 promoters. As shown in Figure 5C and 5D, 242

OsSHI1 bound directly to the F4 (-1~-336) and F3 (-1274~-1578) promoter regions of 243

OsTB1 and OsDEP1, respectively, where the three OsSHI1 recognition cis-elements 244

reside. We further used electrophoretic mobility shift assay (EMSA) to verify the 245

binding specificity of OsSHI1 to these motifs. Full-length recombinant OsSHI1 246

proteins (fused with GST or MBP tags) were expressed in E.coli BL21 (DE3) and 247

affinity purified (Supplemental Figure 9). We found that the GST- or MBP-OsSHI1 248

fusion proteins could bind DNA probes containing the T/GCTCTAC motifs. Moreover, 249

non-labeled competing probes could effectively reduce the binding ability of OsSHI1 250

in a dosage-dependent manner and mutation of the core sequence (T/GCTCTAC 251

mutated to T/GAAAAAC) abolished the binding (Figure 5E to 5G). Furthermore, 252

chromatin immunoprecipitation assay (ChIP) using anti-OsSHI1 specific polyclonal 253

antibodies verified that OsSHI1 could be specifically recruited to the P3 promoter 254

regions of OsTB1 and OsDEP1, adjacent to the IPA1 recognition sites (Figure 5H and 255

5I). Moreover, ChIP-reChIP analysis with chromatin immunoprecipitated sequentially 256

by OsSHI1 and IPA1 specific polyclonal antibodies showed that OsSHI1 and IPA1 257

co-occupy common target promoters (OsTB1 and OsDEP1) in vivo (Figure 5J, 258

Supplemental Figure 12). Further domain dissection analysis revealed that the 259

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N-terminal region of OsSHI1 (containing the conserved C3HC3H zinc finger domain) 260

confers the DNA binding ability (Supplemental Figure 13). 261

262

OsSHI1 Represses the DNA Binding Activity of IPA1 to the Promoters of OsTB1 263

and OsDEP1 264

Previous studies demonstrated that IPA1 acts as a transcriptional activator, promoting 265

the accumulation of OsTB1 and OsDEP1 transcripts (Lu et al., 2013). The 266

up-regulation of OsTB1 and OsDEP1 in the shi1 background indicates that OsSHI1 267

and IPA1 act antagonistically in regulating the expression of OsTB1 and OsDEP1. We 268

thus performed transient dual-LUC assay in rice protoplasts to evaluate the 269

transcriptional regulatory relationship between OsSHI1 and IPA1. As shown in Figure 270

6A to 6C, IPA1 alone greatly enhanced the expression of the luciferase (LUC) 271

reporter gene driven by the OsTB1 and OsDEP1 promoters, while OsSHI1 alone had 272

no significant effect. However, when co-expressed with OsSHI1, the transcriptional 273

activation activity of IPA1 was significantly attenuated. Moreover, mutations of the 274

T/GCTCTAC motifs did not compromise the effect of OsSHI1-mediated repression of 275

the transcriptional activation of OsTB1 conferred by IPA1 (Figure 6D). To test 276

whether OsSHI1 affects the DNA binding affinity of IPA1, in vitro EMSA assays were 277

performed. As previously reported, IPA1 could bind directly to the GTAC motifs in 278

the OsTB1 and OsDEP1 promoter regions, and no shifted bands were observed for 279

OsSHI1 to the GTAC motifs (Figure 6E and 6F). However, the presence of increasing 280

amounts of OsSHI1 protein in the reactions significantly reduced the binding ability 281

of IPA1 to the target probes, independent of OsSHI1 binding (Figure 6E and 6F, 282

Supplemental Figure 14), indicating that OsSHI1 could interfere with the DNA 283

binding ability of IPA1. Moreover, immunoblot analysis using anti-IPA1 specific 284

polyclonal antibodies (Supplemental Figure 12) revealed that no differences of IPA1 285

protein abundance were observed in either the young seedling or young panicle 286

tissues of WT and shi1 (Figure 6G and 6H). However, in vivo ChIP-qPCR assay 287

performed with DNA precipitated by anti-IPA1 antibodies revealed that the P3 and P4 288

promoter regions of OsTB1 and OsDEP1 were significantly more enriched in the shi1 289

16mutant (Figure 6I and 6J), which is consistent with the up-regulation of expression 290

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levels of OsTB1 and OsDEP1 in shi1 mentioned above. 291

To further investigate the biological significance of the OsSHI1 and IPA1 292

interaction, we generated 35S:IPA1-Flag transgenic plants, which displayed 293

significantly repressed tiller development as expected (Figure 7A and 7B). We further 294

overexpressed OsSHI1 under the control of the ACTIN1 promoter in the 295

35S:IPA1-Flag transgenic background (Figure 7C). Immunoblot analysis showed that 296

OsSHI1 accumulation did not obviously affect the stability or abundance of IPA1 297

protein (Figure 7C). In vivo ChIP-qPCR carried out with DNA precipitated by 298

anti-Flag antibody from the 35S:IPA1-Flag transgenic plants revealed that the P3 299

promoter region of OsTB1 (where the two IPA1 recognition sites reside) was 300

predominantly enriched (Figure 7D). However, the enrichment of the P3 promoter 301

region was significantly reduced in the Actin1:OsSHI1/35S:IPA1-Flag transgenic 302

plants, when compared with the scenario of 35S:IPA1-Flag transgenic plants (Figure 303

7D). Consistent with this, the Actin1:OsSHI1/35S:IPA1-Flag transgenic plants 304

displayed obviously reduced plant height and somewhat recovered tiller development, 305

as well as significantly reduced expression levels of OsTB1, compared to the 306

35S:IPA1-Flag parental plants (Figure 7E and 7F). Taken together, these results 307

support the conclusion that OsSHI1 negatively regulates the transcriptional activation 308

activity of IPA1 on OsTB1 and OsDEP1 by repressing its DNA binding activity. 309

310

IPA1 Acts Downstream of OsSHI1 to Regulate Plant Architecture in Rice 311

To determine the genetic relationship of OsSHI1 and IPA1, a series of shi1, ipa1, tb1, 312

dep1, ipa1 shi1, tb1 shi1 and dep1 shi1 mutants were generated in the same genetic 313

background (Kitaake) using CRISPR/Cas9-mediated genome-editing approach 314

(Supplemental Figure 15). As expected, shi1 mutant exhibited reduced tillering and 315

increased panicle branching (Supplemental Figure 3). In contrast to the phenotype of 316

shi1 mutant, the tiller number of ipa1 mutant was significantly increased, 317

accompanied with diminished panicle size. Tiller development was greatly intensified 318

in the tb1 mutant. Panicle branching was compromised in both the tb1 and dep1 319

mutants, similar to ipa1 mutant (Figure 8A and 8B). Further phenotypic observations 320

18of the ipa1 shi1, tb1 shi1 and dep1 shi1 double mutants revealed their similarity to the 321

19ipa1, tb1 and dep1 single mutant, respectively (characterized by enhanced tillering 322

20

and compromised panicle branching) (Figure 8A and 8B). These observations support 323

the conclusion that OsSHI1 functions upstream of IPA1, OsTB1 and OsDEP1 to 324

regulate plant architecture in rice. 325

326

327

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DISCUSSION 328

OsSHI1 Acts Antagonistically with IPA1 in Regulating Plant Architecture in Rice 329

Tiller number and panicle size are critical determinants of plant architecture and crop 330

yield. To meet the constantly increasing demand for food productivity, a new breeding 331

approach of the “New Plant Type (NPT)” or “Ideal Plant Architecture (IPA)” strategy 332

has been proposed (Khush, 2001; Wang and Li, 2008). The IPA traits characterized by 333

fewer sterile tillers, larger panicles and stronger culms are closely correlated with the 334

accumulation of IPA1 protein, which further activates the expression of OsTB1 and 335

OsDEP1 to regulate plant architecture in rice (Jiao et al., 2010; Miura et al., 2010; Lu 336

et al., 2013). Notably, several aspects of the shi1 mutant phenotype (remarkably 337

reduced tiller number, enlarged panicles and enhanced culm strength) (Figure 1H to 338

1N, Supplemental Figure 2H to 2M) are reminiscent of the effects of IPA1 339

overexpression. Furthermore, OsSHI1 overexpression lines exhibit significantly 340

reduced plant height, ectopically formed tillers and diminished panicle size 341

(Supplemental Figure 4), similar to the previously reported IPA1 transgenic RNAi 342

plants (Wang et al., 2015a). In addition, OsSHI1 is predominantly expressed in 343

axillary buds and young panicle (Figure 3D and 3E, Supplemental Figure 7) and its 344

expression pattern partially overlaps with that of IPA1 (Jiao et al., 2010; Miura et al., 345

2010; Lu et al., 2013). These observations hint that OsSHI1 and IPA1 may 346

antagonistically regulate plant architecture in rice. This notion is further supported by 347

the observation that the expression levels of OsTB1 and OsDEP1, two positively 348

regulated targets of IPA1, are significantly upregulated in shi1 (Figure 5A and 5B). 349

Moreover, the Actin1:OsSHI1/35S:IPA1-Flag double-overexpression plants exhibit 350

significant dwarfism and somewhat increased tiller number, in comparison with the 351

35S:IPA1-Flag parental plants (Figure 7A and 7E). Further, in contrast to the 352

repressed tiller development and enlarged panicle architecture of shi1, the tiller and 353

panicle branch numbers of ipa1 shi1, tb1 shi1 and dep1 shi1 double mutants are 354

significantly increased or reduced, similar to the scenario of ipa1, tb1 or dep1 single 355

mutants (Figure 8). These results together suggest that OsSHI1 acts antagonistically 356

and upstream of IPA1 to regulate plant architecture in rice. 357

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358

OsSHI1 Represses the Transcriptional Activity of IPA1 by Interfering with Its 359

DNA-binding Activity 360

Recent studies have identified three IPA1-interacting proteins, OsIPI1, OsOTUB1 and 361

OsD53, and demonstrated their roles in regulating plant architecture in rice (Jiang et 362

al., 2013; Zhou et al., 2013; Song et al., 2017; Wang et al., 2017b; Wang et al., 2017c). 363

OsIPI1 acts as a RING-type E3 ligase to promote the degradation of IPA1 in panicles 364

by adding K48-linked poly-ubiquitin chains while stabilizing IPA1 in shoot apexes by 365

mediating K63-linked poly-ubiquitin modification (Wang et al., 2017b). OsOTUB1 is 366

a deubiquitinating enzyme with both K48- and K63-linked poly-ubiquitin cleavage 367

activities, and OsOTUB1-IPA1 interaction limits the K63-linked ubiquitination of 368

IPA1 which in turn promotes K48Ub-dependent proteasomal degradation of IPA1 369

(Wang et al., 2017c). Thus, both OsIPI1 and OsOTUB1 are enzymes involved in the 370

post-transcriptional poly-ubiquitin modification of IPA1. Recent studies also showed 371

that OsD53 represses the transcriptional activation activity of IPA1 by interacting with 372

the TPL transcriptional co-repressors, which in turn recruit HDAC complexes to 373

modulate local chromatin status, thereby influencing downstream target gene 374

expression. The degradation of OsD53 by the 26S proteasome system releases IPA1 to 375

proceed with the activation of downstream target genes (like OsTB1), allowing tiller 376

development (Jiang et al., 2013; Zhou et al., 2013; Song et al., 2017). Notably, OsIPI1, 377

OsOTUB1 and OsD53 all interact with IPA1 through the conserved SBP domain and 378

they do not affect the DNA binding ability of IPA1 (Song et al., 2017; Wang et al., 379

2017b; Wang et al., 2017c). 380

In this study, we used various assays to show that OsSHI1 is an interacting partner 381

of IPA1 (Figure 4, Supplemental Table 2). In contrast to the previous identified IPA1 382

interacting partners, we showed that OsSHI1 interacts with IPA1 through the C 383

terminal region but not the SBP domain (Figure 4B). In addition, we showed that the 384

levels of IPA1 transcript and IPA1 protein are not affected in the shi1 mutant (Figure 385

6G and 6H, Supplemental Figure 16), suggesting that OsSHI1 regulates IPA1 through 386

a previously uncharacterized mechanism. In support of this notion, our transient 387

23

analysis revealed that OsSHI1 represses the transcriptional activation activity of IPA1 388

in protoplasts (Figure 6B and 6C). Further, both in vitro EMSA and in vivo ChIP 389

assays revealed that the OsSHI1-IPA1 interaction reduces the binding affinity of IPA1 390

to the promoter regions of both OsTB1 and OsDEP1 (Figure 6E, 6F, 6I, 6J and 7D), 391

but no obvious effect of IPA1 on the DNA binding ability of OsSHI1 was observed 392

(Supplemental Figure 17). Compromised DNA binding affinity of IPA1 conferred by 393

OsSHI1 was partially independent of its binding to its own cis-element (Figure 6D, 394

Supplemental Figure 14). 395

Based on our findings, we propose a model to illustrate how OsSHI1 and IPA1 act 396

cooperatively to regulate plant architecture in rice (Supplemental Figure 18). In 397

wild-type plants, OsSHI1/IPA1 heterodimer formation reduces the DNA binding 398

ability of IPA1 to modulate the expression of downstream target genes and plant 399

architecture. However, in shi1, the absence of OsSHI1 enhances the binding of IPA1 400

to the promoter regions of OsTB1 and OsDEP1 to up-regulate their expression levels, 401

consequently altering plant architecture. Taken together, our results suggest that 402

OsSHI1 regulates IPA1 activity through affecting its transcriptional activity. However, 403

other possibilities exist, such as that the formation of a OsSHI1-IPA1 complex may 404

alter the protein/DNA conformation of target genes thus reducing the access of IPA1 405

or block the transcriptional activation activity conferred by the C terminal region of 406

IPA1 or interfere with the interaction of IPA1 with other proteins (such as chromatin 407

remodeling factors). Given the demonstration that plant architecture could be 408

improved through fine-tuning the tissue-specific expression or protein accumulation 409

pattern of IPA1 (Wang and Wang, 2017a), our findings may provide new alternative 410

approaches to modify the activity of IPA1 and thus bear important implications for 411

genetic improvement of rice plant architecture in future breeding. 412

413

414

24

METHODS 415

Plant Materials and Growth Conditions 416

The shi1 mutant was initially isolated from a mutant library of 9311 (O. sativa L. ssp. 417

indica) mutagenized by 60Co-γ irradiation. Two F2 populations derived from the 418

reciprocal crosses between shi1 and WT (9311) were utilized for genetic analysis of 419

segregation. For map-based cloning, an F2 population was generated from the cross 420

between shi1 and cv. 02428 (O. sativa L. ssp. japonica). Plants were grown in the 421

paddy fields at the Chinese Academy of Agricultural Sciences (Beijing, China) and 422

Nanjing Agricultural University (Nanjing, China) under natural conditions with 423

conventional management. 424

425

EdU Staining Observation 426

Wild-type and shi1 young seedlings were incubated in the MS solution with the EdU 427

substrate overnight. Shoot bases with axillary buds were carefully dissected and fixed 428

in the FAA fixative solution (50% ethanol, 5% acetic acid and 10% formaldehyde) at 429

4°C overnight. Samples were rehydrated through the 70%, 50%, 30%, 15% and 0% 430

ethanol series (each for 15 mins) and incubated in 1% Triton X-100 for 2 h. Then the 431

samples were incubated in a staining solution (1× Click-iT reaction buffer, 100 mM 432

CuSO4, 10 mM Alexa Fluor azide and 1× Reaction buffer additive) for 3 h in darkness. 433

The samples were subsequently washed 3 times in water and dehydrated through the 434

15%, 30%, 50%, 70%, 85% and 95% ethanol series (each for 20 mins) followed by 435

incubating with 100% ethanol for 2 h. After sufficient dehydration, samples were 436

hyalinized through the 2:1, 1:1, 1:2 and 0:1 ethanol:methyl salicylate series (each for 437

1 h). Fluorescence signals were observed using a confocal laser scanning microscope 438

(LSM 700, Carl Zeiss). 439

440

Paraffin Section Analysis 441

Shoot bases with axillary buds were carefully dissected and fixed in the FAA solution 442

at 4°C for 24-72 h. Samples were dehydrated through the 70%, 80%, 90% and 100% 443

ethanol series (each for 60 mins). After sufficient dehydration, samples were 444

25

hyalinized through the 1:2, 1:1, 2:1 and 1:0 xylene:ethanol series (each for 45 mins). 445

Samples were then incubated in the 1:1 ethanol: Paraplast Plus solution at 42°C for 24 446

h and repeated once, after which samples were embedded in Paraplast Plus at 60°C 447

for 4 d. Then the samples were sectioned into 8 µm-thick sections using a Leica 448

RM2245 rotary microtome. After the removal of Paraplast Plus by series of xylene 449

and ethanol solutions, sections were stained with toluidine blue before pictures taken 450

using a Leica ICC50 HD microscope. The images were processed using the ACDSee 451

software. 452

453

Map-based Cloning of OsSHI1 454

A total of 137 genome-wide primer pairs that exhibit polymorphisms between 9311 455

and 02428 were identified from our primer library. The OsSHI1 locus was initially 456

mapped to an interval between the simple sequence repeat (SSR) markers RM107 and 457

RM189 on the long arm of chromosome 9 using 180 F2 mutant plants. Subsequent 458

fine-mapping based on 7,547 progeny delimited the mutant locus to a ~50 kb genomic 459

region with additional newly developed molecular markers (Supplemental Table 3). 460

cDNAs of the 4 ORFs in the fine-mapped region were amplified from both WT and 461

the shi1 mutant (primer pairs listed in Supplemental Table 3), and the PCR products 462

were confirmed by sequencing. 463

464

RT-PCR and Quantitative RT-PCR Analyses 465

Total RNA was extracted from various tissues using the ZR Plant RNA MiniPrep Kit 466

(Zymo research) following the manufacturer’s recommendations. The first-strand 467

cDNA was synthesized based on the QuantiTect Reverse Transcription Kit (Qiagen). 468

RT-PCR with 28 cycles was performed to amplify the 4 ORFs in the fine-mapped 469

region and 24 cycles for ACTIN2 (which was used as the endogenous control). RT- 470

quantitative PCR was performed on an ABI7500 Real-Time PCR System using SYBR 471

Premix Ex Taq (Takara, Japan) with rice Ubiquitin as the endogenous control. 472

Relative changes in gene expression levels were quantitated based on three biological 473

replicates via the 2-△△Ct method (Livak and Schmittgen, 2001). All primer pairs used 474

26

for RT-PCR and RT-qPCR are listed in Supplemental Tables 3 and 4. 475

476

Vector Construction and Plant Transformation 477

A ~5 kb genomic DNA fragment (consisting of a 2.9 kb upstream region, the entire 478

OsSHI1 coding region including two exons, one intron and a 400 bp downstream 479

region) was amplified with the primer pair OsSHI1-COM (Supplemental Table 5) and 480

inserted into the HindIII/BamHI restriction sites of the pCUbi1390 binary vector to 481

generate the proOsSHI1:OsSHI1 construct, which was introduced into the calli of shi1 482

via Agrobacterium-mediated transformation using a previously described method 483

(Hiei et al., 1994). 484

To knock out the OsSHI1, IPA1, OsTB1 and OsDEP1 genes, 20-bp gene-specific 485

spacer sequences were cloned into the sgRNA-Cas9 vector (Miao et al., 2013) and 486

subsequently introduced into the calli of Kitaake (or OsSHI1-CRISPR-#1), a japonica 487

variety suitable for transformation, via Agrobacterium-mediated transformation. 488

Positive transgenic individuals were identified by sequencing or immunoblot 489

analyses. 490

To verify the expression pattern of OsSHI1, ~2 kb promoter fragment upstream of 491

the ATG start codon was amplified using the primer pair OsSHI1-GUS (Supplemental 492

Table 5) and the PCR product was fused into the EcoRI/NcoI restriction sites of the 493

binary vector pCAMBIA1305. The generated pOsSHI1:GUS construct was 494

introduced into the calli of Kitaake via Agrobacterium-mediated transformation to 495

generate the pOsSHI1:GUS reporter lines. 496

To generate the IPA1-overexpressing plants, full-length cDNA of IPA1 was 497

amplified using the primer pair IPA1-Flag (Supplemental Table 5) and fused into the 498

XbaI restriction site of the 1300-221-3×Flag binary vector. The generated 35S: 499

IPA1-Flag construct was introduced into the calli of Kitaake via 500

Agrobacterium-mediated transformation. 501

To determine the effect of OsSHI1 overexpression, full-length cDNA of OsSHI1 502

was amplified using the primer pair OsSHI1-OE (Supplemental Table 5). The PCR 503

product was inserted into the SmaI restriction site of the pCAMBIA2300 binary 504

27

vector to generate the Actin1:OsSHI1-OE construct, which was subsequently 505

introduced into the calli of Kitaake or 35S:IPA1-Flag transgenic plants via 506

Agrobacterium-mediated transformation. 507

508

Subcellular Localization 509

For subcellular localization of OsSHI1 protein, the 945 bp coding region of OsSHI1 510

was inserted into the XbaI restriction site upstream of GFP in the transient expression 511

vector pAN580 driven by the double CaMV35S promoter to generate the 512

OsSHI1-GFP construct (primer pair OsSHI1-GFP in Supplemental Table 5). The 513

OsSHI1-GFP plasmid was introduced into the rice protoplasts according to protocols 514

described previously (Zhang et al., 2011). Fluorescence of GFP was observed using a 515

confocal laser scanning microscope (LSM 700, Carl Zeiss). 516

517

Transactivation Activity Assay 518

The full-length OsSHI1 coding region was cloned into the pGBKT7 (Clontech) vector 519

at the EcoRI/PstI restriction sites (primer pair OsSHI1-BD in Supplemental Table 5) 520

to generate the OsSHI1-BD construct which was then transformed into the 521

Saccharomyces cerevisiae strain MAV203. Transactivation activity assay was 522

performed in the absence of Trp and Ura in solid medium followed with quantitative 523

β-gal assay of the LacZ reporter gene using CPRG as the substrate. OsEhd1 (Cho et 524

al., 2016) and the empty pGBKT7 vector were used as the positive and negative 525

control, respectively. All procedures were performed according to the manufacturer’s 526

recommendations (Clontech). 527

528

Yeast Two-hybrid Assay (Y2H) 529

The coding region of OsSHI1 was fused to the GAL4-binding domain of the ‘bait’ 530

pGBKT7 vector (Clotech) (primer pairs listed in Supplemental Table 5). A cDNA 531

library prepared from rice young inflorescences was used to perform the yeast 532

two-hybrid screening and positive clones were identified by sequencing. Full-length 533

and various truncated versions of IPA1 were inserted into the EcoRI/XhoI restriction 534

28

sites of the ‘prey’ pGADT7 vector (Clontech) (primer pairs listed in Supplemental 535

Table 5). Series of combined bait and prey constructs were co-transformed into the 536

yeast strain AH109 (Clontech). After growing on SD -Trp / -Leu plates for 3 days at 537

30°C, interactions between baits and preys were examined on the selective medium 538

SD –Leu / -Trp / -His / -Ade. Yeast strain containing OsSHI1-BD in combination with 539

the empty pGADT7 vector was used as the negative control. Detailed procedures 540

were performed according to the manufacturer’s recommendations (Clontech). 541

542

GUS Staining Assay 543

GUS histochemical staining was performed according to the previously described 544

method (Duan et al., 2016). Briefly, various tissues of the pOsSHI1:GUS transgenic 545

plants were detached and incubated in the GUS staining buffer overnight. Tissues 546

were then transferred into alcohol solution to extract the chlorophyll before pictures 547

taken using a Leica ICC50 HD microscope. The images were processed using the 548

ACDSee software. 549

550

In vitro Pull-down Assay 551

Full-length coding sequences of OsSHI1 and IPA1 were cloned into the expression 552

vectors pGEX4T-1 and pMAL-c2x, respectively (primer pairs listed in Supplemental 553

Table 5), to generate GST or MBP tag fusion proteins. Expression of GST, 554

GST-OsSHI1 and MBP-IPA1 in E.coli BL21 (DE3) cells (TransGen, Beijing) was 555

induced by 0.4 mM isopropyl-β-D-thiogalactoside (IPTG) at 18°C for 16 h. Fusion 556

proteins were purified using the GST Bind Resin (Novagen) or Amylose Resin (NEB) 557

according to the manufacturer’s protocols, and protein concentrations were 558

determined by the BSA quantitative assay. 559

For pull-down assay, roughly equal amounts of purified GST and GST-OsSHI1 560

proteins were incubated with 30 µL GST Bind Resin in 1 mL PBS solution for 30 561

mins with gentle rotation, after which ~2 µg IPA1-MBP fusion protein was added. 562

After a further incubation for 60 mins, the resin was washed five times with PBS, 563

diluted in 50 µL 1× Protein Loading Buffer and denatured at 100°C for 10 mins 564

29

before separation on 10% SDS-PAGE gel. Proteins were then transferred to the NC 565

membrane, detected with HRP conjugated anti-GST (MBL, PM013-7) or anti-MBP 566

(NEB, E8032L) antibodies at 1:5000 dilutions and visualized with enhanced 567

chemiluminescence reagent (GE Healthcare). 568

569

Bimolecular Fluorescence Complementation Assay (BiFC) 570

Full-length coding region of OsSHI1 was amplified (primer pair listed in 571

Supplemental Table 5) and cloned into the EcoRI/SalI restriction sites of the 572

pSPYNE173 (eYNE) expression vector to generate the OsSHI1-eYNE construct. 573

Full-length coding regions of IPA1 and OsSPL16 were amplified (primer pair listed in 574

Supplemental Table 5) and inserted into the EcoRI/SalI restriction sites of the 575

pSPYCE (eYCE) expression vector to generate the IPA1-eYCE or OsSPL16-eYCE 576

constructs. For transient expression, A. tumefaciens strain EHA105 carrying the 577

combined constructs mentioned above was co-infiltrated with the p19 strain into 578

leaves of 5-week-old N. benthamiana. The YFP fluorescent signals were monitored 579

48-72 h after infiltration using a laser confocal scanning microscope (ZEISS 580

Microsystems LSM 700). 581

582

Preparation and Determination of OsSHI1- and IPA1-Specific Antibodies 583

The synthetic peptides of OsSHI1 (Os09g0531600, SRDPTKRPRARPSATTP) and 584

IPA1 (Os08g0509600, RIDPGSGSTFDQTSNTMD) were injected into rabbits to 585

generate the corresponding polyclonal antibodies at ABclonal Tech Co (Wuhan, 586

China). The specificities of anti-OsSHI1 and anti-IPA1 polyclonal antibodies were 587

determined by immunoblot analysis using wild-type young panicle tissues. Samples 588

were ground into fine powder in liquid nitrogen, suspended in 2 × volumes of Protein 589

Extraction Buffer (50 mM Tris–HCl pH 8.0, 150 mM NaCl, 10 mM MgCl2, 1 mM 590

EDTA, 10% glycerol and 1 × Protease inhibitor cocktail) and incubated at 4°C for 591

30 mins with rotation. After centrifuging at 12,000 g at 4°C for 10 min, the 592

supernatant was boiled in 1× Protein Loading Buffer before separation on 10% 593

SDS-PAGE gel. Proteins were then transferred to the NC membrane, detected with 594

30

anti-OsSHI1 or anti-IPA1 antibodies at 1:1000 dilutions and visualized with enhanced 595

chemiluminescence reagent (GE Healthcare). HSP antibody (Beijing Protein 596

Innovation, AbM51099-31-PU) was used as the endogenous control. 597

598

In vivo Co-IP Assay 599

Axillary buds of wild-type seedlings were carefully detached and ground into fine 600

powder in liquid nitrogen. Samples were suspended in 4 × volumes of Protein 601

Extraction Buffer (50 mM Tris–HCl pH 8.0, 150 mM NaCl, 10 mM MgCl2, 1 mM 602

EDTA, 10% glycerol and 1 × Protease inhibitor cocktail) and incubated at 4°C for 603

30 mins with rotation. After centrifuging at 12,000 g for 10 min at 4°C, the 604

supernatant was mixed with 30 μL Protein A beads (Millipore) and incubated with 605

rotation at 4°C for 1 h. Beads were pelleted and the cleaned supernatant were 606

incubated with 10 μL anti-IPA1 specific polyclonal antibodies for at least 2 h at 4°C 607

with gentle rotation. 30 µL Protein A beads were added to precipitate the protein 608

complex with rotation at 4°C for 1 h. Beads were pelleted and washed four times with 609

pre-chilled Protein Extraction Buffer. The bound proteins were eluted from the beads 610

with 1 × Protein Loading Buffer by boiling at 100°C for 10 mins. Protein samples 611

were then separated by 10% SDS-PAGE gel, transferred to NC membrane and 612

immunoblotted with anti-IPA1 and anti-OsSHI1 specific polyclonal antibodies. 613

614

Yeast One-hybrid Assay (Y1H) 615

Y1H analysis was performed according to the previously described method (Lin et al., 616

2007). Briefly, the full-length coding region of OsSHI1 was cloned into the pB42AD 617

vector at the EcoRI restriction site to generate the AD-OsSHI1 construct (primer pair 618

OsSHI1-42AD in Supplemental Table 5). The full ~2 kb and various truncated 619

versions of promoter regions of OsTB1 or OsDEP1 were amplified (primer pairs 620

listed in Supplemental Table 5) and ligated into the XhoI restriction site of the pLacZi 621

reporter vector. Constructs were then co-transformed into the yeast strain EGY48. 622

Transformants were grown on SD -Trp / -Ura plates for 3 days at 30°C and then 623

transferred onto X-gal (5-bromo-4-chloro-3-indolyl-β-d-galactopyranoside) plates for 624

31

blue color development. Yeast strains containing the empty pB42AD in combination 625

with the LacZ reporter constructs were used as negative controls. 626

627

Transient Expression Assay in Protoplasts and LUC Activity Determination 628

~1 kb and ~2 kb promoter regions of OsTB1 and OsDEP1 were amplified using the 629

primer pairs OsTB1-LUC or OsmTB1-LUC and OsDEP1-LUC (primer pairs listed in 630

Supplemental Table 5) and cloned into the upstream of LUC reporter gene to generate 631

the OsTB1-LUC or OsmTB1-LUC and OsDEP1-LUC reporter constructs. The 632

luciferase gene from Renilla reniformis (Ren) under the control of CaMV35S 633

promoter was used as the internal control. Full-length cDNAs of OsSHI1 and IPA1 634

were amplified (primer pairs listed in Supplemental Table 5) and inserted into the 635

BamHI/PstI restriction sites of the pAN580 vector to generate the d35S:OsSHI1 and 636

d35S:IPA1 effector constructs, respectively. The combined reporter and effector 637

plasmids were co-transformed into the rice protoplasts according to a protocol 638

described previously (Zhang et al., 2011). The LUC activity was quantified with a 639

Dual-luciferase Assay Kit (Promega) following the manufacturer’s recommendations 640

and the relative LUC activity is calculated as the ratio of LUC/Ren. 641

642

Chromatin Immunoprecipitation Assay (ChIP) 643

To assess the enrichment of OsSHI1 or IPA1 at the promoter regions of OsTB1 and 644

OsDEP1 in vivo, chromatin immunoprecipitation (ChIP) assays were carried out 645

using anti-OsSHI1 or anti-IPA1 specific polyclonal antibodies. About 4 g of wild-type 646

axillary buds or young panicle tissues (1-2 g for transgenic plants) were ground into 647

fine powder in liquid nitrogen, resuspended in 20 mL Extraction buffer 1 (0.4 M 648

sucrose, 10 mM Tris-HCl, pH 8.0, 10 mM MgCl2, 5 mM β-mercaptoethanol [β-ME], 649

0.1 mM phenylmethylsulfonyl fluoride [PMSF], 1× proteinase inhibitor and 1% 650

formaldehyde) and thoroughly mixed to release the nuclei. After incubation under 651

vacuum conditions for 30 mins, 0.125 M glycine was added and incubated for another 652

5 mins to stop the crosslink reaction. The solution was filtered by two layers of 653

Miracloth (Millipore) and centrifuged at 3,000 g at 4°C for 20 mins to remove the 654

32

supernatant. The pellet was resuspended in 1 mL Extraction buffer 2 (0.25 M sucrose, 655

10 mM Tris-HCl, pH 8.0, 10 mM MgCl2, 1% Triton X-100, 5 mM β-ME, 0.1 mM 656

PMSF and 1× proteinase inhibitor) and centrifuged at 12,000 g at 4°C for 10 mins. 657

The pellet was resuspended in 300 µL Extraction buffer 3 (1.7 M sucrose, 10 mM 658

Tris-HCl, pH 8.0, 2 mM MgCl2, 0.15% Triton X-100, 5 mM β-ME, 0.1 mM PMSF 659

and 1× proteinase inhibitor), laid on top of another clean 300 µL of Extraction buffer 660

3 and centrifuged at 15,000 g at 4°C for 1 h. The chromatin pellet was resuspended in 661

200 µL Nuclei lysis buffer (50 mM Tris-HCl, pH 8.0, 10 mM EDTA, 1% SDS and 1× 662

proteinase inhibitor) and sonicated to 200~500 bp with 3 s burst / 7 s interval 663

frequency at 2 W power for 33 mins. After centrifugation at 12,000 g at 4℃ for 10 664

mins, the chromatin supernatant was diluted with Dilution buffer (0.01% SDS, 1.1% 665

Triton X-100, 1.2 mM EDTA, 16.7 mM Tris-HCl, pH 8.0 and 167 mM NaCl) and 1 666

mL of the diluted chromatin sample was precleared with 20 µL Protein A beads 667

(Millipore) for 1 h at 4°C with rotation. Then 10 µL anti-OsSHI1 or anti-IPA1 specific 668

polyclonal antibodies together with 10 µL BSA (10 mg/mL) were added to the 669

precleared sample and incubated overnight with gentle rotation. 1 µL salmon sperm 670

DNA (10 mg/mL) was added as the blocking reagent and the immune complexes were 671

collected by 30 µL Protein A beads for 1 h at 4°C with rotation. The Protein A beads 672

were washed stepwise with a low salt wash buffer (0.1% SDS, 1% Triton X-100, 2 673

mM EDTA, 20 mM Tris-HCl, pH 8.0 and 150 mM NaCl), a high salt wash buffer (0.1% 674

SDS, 1% Triton X-100, 2 mM EDTA, 20 mM Tris-HCl, pH 8.0 and 500 mM NaCl), 675

the LiCl wash buffer (0.25 M LiCl, 1% NP40, 1% deoxycholic acid sodium, 1 mM 676

EDTA and 20 mM Tris-HCl, pH 8.0) and TE buffer (10 mM Tris-HCl, pH 8.0 and 1 677

mM EDTA) each two times. The immune complexes were eluted from the Protein A 678

beads by incubating with 250 µL Elution buffer (0.1 M NaHCO3 and 1% SDS) at 679

65°C for 20 min with agitation. The supernatant was transferred to another tube to 680

repeat elution and the two eluates were combined. 20 µL NaCl (5 M), 10 µL RNAse A 681

(10 mg/mL) and 2.5 µL protease K (10 mg/mL) were added to the eluted solution (for 682

the input sample, two volume amounts were added) and incubated at 65°C for at least 683

6 h with agitation. The immunoprecipitated DNA was extracted with isopropyl 684

33

alcohol precipitation. The recovered DNA was used as the template for ChIP-qPCR 685

and the enrichment was calculated as the ratio of IP to Input. The ChIP-reChIP assay 686

was carried out according to the previously reported protocol (Furlan-Magaril et al., 687

2009). All primer pairs are listed in Supplemental Table 6. 688

689

Electrophoretic Mobility Shift Assay (EMSA) 690

3ʹ-DIG-labeled probes containing the putative OsSHI1 binding sites were synthesized 691

by Invitrogen (Shanghai, China) (primer pairs listed in Supplemental Table 7). EMSA 692

assays were performed with the DIG Gel Shift Kit (Roche) following the 693

manufacturer’s recommendations. Briefly, equal amounts of complementary 694

oligonucleotides were incubated at 95°C for 10 mins, cooled down slowly to 15°C 695

(0.1 °C/1s) and diluted to 50 fmol/µL final concentrations. The DNA binding reaction 696

was performed with 100 fmol probe, 2 µg poly (dI-dC) and 100 ng purified MBP or 697

MBP-OsSHI1 proteins and incubated at room temperature for 30 mins. Then the 698

samples were immediately applied to the pre-run native polyacrylamide gel 699

containing 6.5% acrylamide in 0.5× TBE buffer. After electro-blotting onto a nylon 700

membrane (Millipore), the oligonucleotides were crosslinked using UV-light. The 701

membrane was incubated in a blocking solution for 30 mins, followed by incubating 702

in a DIG antibody solution for another 30 mins. After intensive washing with a 703

washing buffer, CSPD working solution was applied to the membrane to visualize the 704

signal. 705

706

Accession Numbers 707

Sequence data from this article can be found in the EMBL/GenBank data libraries 708

under the following accession numbers: OsSHI1, Os09g0531600; IPA1, 709

Os08g0509600; OsSPL16, Os08g0531600; OsTB1, Os03g0706500; OsDEP1, 710

Os09g0441900; UBIQUITIN, Os03g0234200 and ACTIN2, Os03g0718100. 711

712

Supplemental Data 713

Supplemental Figure 1. Normal Initiation of Axillary Buds in shi1. 714

34

Supplemental Figure 2. Grain, Leaf and Culm Morphologies of WT and shi1. 715

Supplemental Figure 3. Phenotypes of ORF2 (OsSHI1) Knockout Plants. 716

Supplemental Figure 4. Phenotypes of ORF2 (OsSHI1) Overexpression Plants. 717

Supplemental Figure 5. Characterization and Sequence Analysis of OsSHI1. 718

Supplemental Figure 6. OsSHI1 Exhibits Weak Transcriptional Activation Activity 719

in Yeast Cells. 720

Supplemental Figure 7. Histochemical Staining of the pOsSHI1:GUS Transgenic 721

Plants. 722

Supplemental Figure 8. Specificity Tests of the Anti-OsSHI1 Polyclonal Antibodies 723

Used for ChIP and Immunoblot Analyses. 724

Supplemental Figure 9. Protein Induction and Purification Used for Immunoblot and 725

EMSA Assays. 726

Supplemental Figure 10. Schematic Depictions of the Cis-elements in the Promoter 727

Regions of OsTB1 and OsDEP1. 728

Supplemental Figure 11. Sequence Analysis of the Promoter Regions of OsTB1 and 729

OsDEP1. 730

Supplemental Figure 12. Specificity Tests of the Anti-IPA1 Polyclonal Antibodies 731

Used for ChIP and Immunoblot Analyses. 732

Supplemental Figure 13. The Zinc Finger Domain Is Indispensable for the DNA 733

Binding Ability of OsSHI1. 734

Supplemental Figure 14. OsSHI1 Represses the DNA Binding Ability of IPA1 735

Independent of OsSHI1 Binding. 736

Supplemental Figure 15. Generation and Identification of Mutants Generated by 737

CRISPR/Cas9 Genome-editing Approach. 738

Supplemental Figure 16. OsSHI1 Does Not Affect the Expression Level of IPA1. 739

Supplemental Figure 17. IPA1 Does Not Interfere with the DNA Binding Ability of 740

OsSHI1. 741

Supplemental Figure 18. A Proposed Working Model for OsSHI1 in the Regulation 742

of Plant Architecture in Rice. 743

Supplemental Table 1. Phenotypic Segregation Identified by Test for 744

35

Goodness-of-fit. 745

Supplemental Table 2. Putative Interacting Partners of OsSHI1 Identified by Y2H 746

Screening. 747

Supplemental Table 3. Primers Used for Map-based Cloning. 748

Supplemental Table 4. Primers for Detection of the RNA Levels of Selected Genes. 749

Supplemental Table 5. Primers Used for Vector Construction. 750

Supplemental Table 6. Primers Used for ChIP-qPCR Analyses. 751

Supplemental Table 7. DIG-labeled Oligonucleotides Used for EMSA Assays. 752

753

ACKNOWLEDGEMENTS 754

This research was supported by grants from the National Key Research and 755

Development Program of China (2016YFD010091), the National Natural Science 756

Foundation of China (31671769), Guangdong Province-National Natural Science 757

Foundation of China (U1701232) and the National Transgenic Science and 758

Technology Program (2016ZX08001004-002). 759

760

AUTHOR CONTRIBUTIONS 761

J.W. supervised the project. L.J., H.W. and J.W. designed the research. E.D., X.L., 762

Q.L., T.Z., Y.W., C.Z. and H.Z. performed research. E.D., X.L., T.Z. and J.W. 763

analyzed data. Y.W. provided the plant material. C.L. and J.W. cultivated the 764

transgenic plants in the field. X.Z. and X.G. generated the transgenic plants. E.D. 765

drafted the manuscript. H.W. and J.W. revised the manuscript. 766

767

FIGURE LEGENDS 768

Figure 1. Phenotypic Characterization of the shi1 Mutant. 769

(A to G) Tillering phenotypes of WT (9311) and shi1 at 2 WAG (weeks after 770

germination) (A), 3 WAG (B and C), 4 WAG (D), 5 WAG (E), 6 WAG (F) and 7 771

WAG (G). (C) is the enlarged image of the dotted box in (B). White arrows indicate 772

the tillers. Bars=2 cm (A and B), 1 cm (C), 5 cm (D to G). 773

(H) Plant architectures of WT and shi1 at the grain-filling stage. Bar=20 cm. 774

36

(I) Statistical analysis of tiller numbers of WT and shi1. Values are presented as 775

means ± SD, and the statistically significant differences were determined by Students 776

t-test (n = 15, **P<0.01). 777

(J) Panicle morphologies of WT and shi1 at the mature stage. Bar=5 cm. 778

(K) Panicle branch architectures of WT and shi1 with grains removed. Bar=5 cm. 779

(L to N) Statistical analysis of the primary branch numbers (L), secondary branch 780

numbers (M) and spikelet numbers per panicle (N) of WT and shi1. Values are 781

presented as means ± SD, and the statistically significant differences were determined 782

by Students t-test (n = 10, *P<0.05, **P<0.01). 783

784

Figure 2. Map-based Cloning of OsSHI1. 785

(A) OsSHI1 was narrowed down to a ~50 kb region of chromosome 9 containing 4 786

ORFs. A genomic region of about 18 kb is deleted in shi1. The markers, BACs and 787

numbers of recombinants are indicated. 788

(B) PCR amplifications by primer pairs located at the flanking boundaries of the 789

deleted region. No PCR product could be amplified from WT due to the large size of 790

genomic region using the primer pair F48 and R56. 791

(C) RT-PCR analysis of the 4 ORFs. Expression of ORF2 was not detected in shi1. 792

Actin2 was used as an endogenous control. 793

(D) Protein levels of OsSHI1 in the panicle tissues of WT and shi1 detected by 794

immunoblot using anti-OsSHI1 specific polyclonal antibodies. HSP was used as the 795

loading control. Molecular weights of proteins (kDa) are shown on the left. 796

(E) Plant phenotypes of WT, shi1 and two independent complementation lines before 797

the heading stage. Bar=10 cm. 798

(F) Tiller numbers of the complemented transgenic lines compared to the WT and 799

mutant levels. Values are presented as means ± SD, and the statistically significant 800

differences were determined by Students t-test (n = 5, **P<0.01). 801

802

Figure 3. Expression Analysis of OsSHI1 and Functional Characterization of OsSHI1 803

Protein. 804

37

(A) Schematic representation of the OsSHI1 protein. The conserved zinc finger 805

domain and IGGH domain are indicated. 806

(B) Subcellular localization of the OsSHI1-GFP fusion protein in rice protoplast. 807

OsD53-mCherry was used as the nuclear marker. Bar=20 μm. 808

(C) OsSHI1 is capable of forming homodimer through the C terminus in yeast cells. 809

Transformed yeast cells were spotted on the control medium DDO (SD / -Trp / -Leu) 810

and selective medium QDO (SD / -Trp / -Leu / -His / -Ade). AD was used as the 811

negative control. OsSHI1-N and OsSHI1-C indicate the N and C terminal regions of 812

OsSHI1 including the zinc finger domain and IGGH domain, respectively. 813

(D) RT-qPCR analysis of the expression pattern of OsSHI1 in various tissues. R: root, 814

C: culm, LB: leaf blade, LS: leaf sheath, YP: young panicle, MP: mature panicle, AB: 815

axillary buds. Values are presented as means ± SD (n=3). 816

(E) Immunoblot analysis showing the accumulation of OsSHI1 protein in various 817

tissues. HSP was used as the loading control. Molecular weights of proteins (kDa) are 818

shown on the left. R: root, C: culm, LB: leaf blade, LS: leaf sheath, YP: young panicle, 819

MP: mature panicle, AB: axillary buds. 820

821

Figure 4. OsSHI1 Physically Interacts with IPA1. 822

(A) Schematic representation of the various truncated visions of OsSHI1 and IPA1 823

proteins. The conserved zinc finger, IGGH and SBP domains are indicated. 824

(B) Both the N and C terminal regions of OsSHI1 interact with the C terminus of 825

IPA1 in yeast cells. Transformed cells were spotted on the control medium (DDO: SD 826

/ -Leu / -Trp) and selective medium (QDO: SD / -Leu / -Trp / -His / -Ade). AD was 827

used as the negative control. 828

(C) In vitro pull-down assay confirms that OsSHI1-GST, but not GST itself, could 829

precipitate IPA1 as detected by anti-MBP antibody. – and + indicate the absence and 830

presence of the corresponding proteins. 831

(D) BiFC assay verifies the interaction between OsSHI1 and IPA1 in the nuclei of 832

epidermal cells of N. benthamiana. OsSHI1 and IPA1 were fused with the N and C 833

terminus of YFP, respectively. eYNE and eYCE were used as the negative controls. 834

38

OsSPL16, a homologous protein of IPA1, was also used as a negative control to 835

demonstrate the specific interaction between OsSHI1 and IPA1. DIC, differential 836

interference contrast. Merged, merged images of YFP channel and DIC. Bar=30 μm. 837

(E) In vivo Co-IP assay shows that OsSHI1 interacts with IPA1 in the axillary buds of 838

wild-type seedlings. Total protein extracts were immunoprecipitated by the anti-IPA1 839

specific polyclonal antibodies and analyzed by immunoblot probed with the anti-IPA1 840

and anti-OsSHI1 polyclonal antibodies. lgG was used as the negative control. 841

842

Figure 5. OsSHI1 Binds Directly to the Promoter Regions of OsTB1 and OsDEP1. 843

(A and B) RT-qPCR analysis of OsTB1 (A) and OsDEP1 (B) expression levels in WT 844

and shi1 axillary buds or young panicle tissues, respectively. Values are presented as 845


t-test (n = 4， *P<0.05, **P<0.01). 847

(C and D) Yeast one-hybrid assays to dissect the binding regions of OsSHI1 in the 848

promoter regions of OsTB1 (C) and OsDEP1 (D). Series of promoter fragments of 849

OsTB1 and OsDEP1 were fused to the upstream region of the LacZ reporter gene and 850

tested for OsSHI1 binding. AD was used as the negative control. FL, full length. 851

(E to G) EMSA assays to test OsSHI1 binding to the two TCTCTAC (E and F) and 852

one GCTCTAC (G) motifs in the OsTB1 and OsDEP1 promoters, respectively. The 853

T/GCTCTAC motif was mutated into T/GAAAAAC to test for sequence specificity. 854

The triangles indicate increased amounts of competing probes. GST or MBP proteins 855

were used as the negative controls. – and + indicate the absence and presence of the 856

corresponding proteins or probes. 857

(H and I) ChIP-qPCR analyses of the P3 promoter regions of OsTB1 (H) and 858

OsDEP1 (I) in ChIP samples precipitated by anti-OsSHI1 specific polyclonal 859

antibodies. The fold enrichment was calculated as IP/Input. Values are presented as 860


t-test (n = 4, **P<0.01). 862

(J) ChIP-reChIP analysis of IPA1 and OsSHI1 co-occupy common target promoters. 863

The chromatin of wild-type plants was first immunoprecipitated by anti-OsSHI1 864

39

specific polyclonal antibodies and then by anti-IPA1 specific polyclonal antibodies, 865

and the precipitated DNA was quantified by qPCR analysis. The fold enrichment was 866

calculated as IP/Input and normalized to that of the UBIQUITIN promoter region as 867

an internal control. Values are presented as means ± SD, and the statistically 868

significant differences were determined by Students t-test (n = 4, **P<0.01). 869

870

Figure 6. OsSHI1 Represses the DNA Binding Activity of IPA1. 871

(A) Schematic representation of the effector and reporter constructs. Full-length 872

coding regions of OsSHI1 and IPA1 under control of the double 35S promoter were 873

used as the effectors. The Firefly luciferase gene LUC driven by the OsTB1 or 874

OsmTB1 and OsDEP1 promoters and the Renilla luciferase gene Ren driven by the 875

35S promoter were used as the reporter and internal control, respectively. d35S, 876

double 35S promoter. 877

(B to D) OsSHI1 represses the transcriptional activation activities of IPA1 on OsTB1 878

(B), OsDEP1 (C) and OsmTB1 (D) promoters in rice protoplasts. Relative LUC 879

activity was calculated by LUC/Ren and normalized to that of vector control which 880

was set as 1. Values are presented as means ± SD, and the statistically significant 881

differences were determined by Students t-test (n = 3, **P<0.01). 882

(E and F) EMSA assays show that OsSHI1-IPA1 interaction attenuates the DNA 883

binding activity of IPA1 to the GTAC motifs in the promoter regions of OsTB1 (E) 884

and OsDEP1 (F). The triangles indicate increased amounts of OsSHI1 proteins. MBP 885

proteins were used as negative controls. – and + indicate the absence and presence of 886

the corresponding proteins. 887

(G and H) Immunoblot analyses of IPA1 protein accumulation in young seedling (G) 888

and young panicle (H) tissues of WT and shi1. HSP was used as the loading control. 889

The molecular weights of proteins (kDa) are shown on the left. 890

(I and J) ChIP assays of the P3 and P4 promoter regions of OsTB1 (I) and OsDEP1 891

(J) in shi1 compared with the wild type. DNAs precipitated from axillary buds or 892

young panicle tissues of WT and shi1 by anti-IPA1 specific polyclonal antibodies 893

were subjected into ChIP-qPCR analysis. Values are presented as means ± SD, and the 894

40

statistically significant differences were determined by Students t-test (n = 4, 895

**P<0.01). 896

897

Figure 7. OsSHI1 Acts Antagonistically with IPA1 to Regulate Tillering in Rice. 898

(A) Plant morphologies of Kitaake, 35S:IPA1-Flag and 899

Actin1:OsSHI1/35S:IPA1-Flag transgenic lines at the heading stage. Bar=10 cm. 900

(B) Determination of IPA1-Flag protein accumulation in the 35S:IPA1-Flag 901

transgenic young seedlings. IPA1-Flag protein was detected using anti-Flag antibody. 902

HSP was used as the loading control. The molecular weights of proteins (kDa) are 903

shown on the left. 904

(C) Immunoblot analyses showing the accumulation of OsSHI1 and IPA1-Flag 905

proteins in the Actin1:OsSHI1/35S:IPA1-Flag transgenic seedlings. OsSHI1 and 906

IPA1-Flag proteins were detected with anti-OsSHI1 specific polyclonal antibodies and 907

anti-Flag antibody, respectively. HSP was used as the loading control. The molecular 908

weights of proteins (kDa) are shown on the left. 909

(D) OsSHI1 reduces the enrichment of the promoter region of OsTB1 910

immunoprecipitated by IPA1. DNAs precipitated from 35S:IPA1-Flag and 911

Actin1:OsSHI1/35S:IPA1-Flag transgenic seedlings by anti-Flag antibody were 912

subjected into ChIP-qPCR analysis. Values are presented as means ± SD, and the 913

statistically significant differences were determined by Students t-test (n = 4, 914

*P<0.05). 915

(E) Overexpression of OsSHI1 in the 35S:IPA1-Flag transgenic background results in 916

increased tiller number. Values are presented as means ± SD, and the statistically 917

significant differences were determined by Students t-test (n = 5 independent plants, 918

*P<0.05, **P<0.01). 919

(F) RT-qPCR analysis showing OsTB1 expression levels in Kitaake, 35S:IPA1-Flag 920

and Actin1:OsSHI1/35S:IPA1-Flag transgenic lines. Values are presented as means ± 921

SD, and the statistically significant differences were determined by Students t-test (n 922

= 4, **P<0.01). 923

924

41

Figure 8. OsSHI1 Acts Upstream of IPA1 to Regulate Plant Architecture in Rice. 925

(A) Plant morphologies of Kitaake, shi1, ipa1, tb1, dep1, ipa1 shi1, tb1 shi1 and dep1 926

shi1 mutants at the heading stage. Bar=10 cm. 927

(B) Panicle architectures of Kitaake, shi1, ipa1, tb1, dep1, ipa1 shi1, tb1 shi1 and 928

dep1 shi1 mutants. Grains were removed to show the primary and secondary branch 929

patterns of the panicles. Bar=2 cm. 930

931

932

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DOI 10.1105/tpc.19.00023; originally published online March 25, 2019;Plant Cell

Zhang, Ling Jiang, Jiulin Wang, Cailin Lei, Xin Zhang, Xiuping Guo, Haiyang Wang and Jianmin WanErchao Duan, Yihua Wang, Xiaohui Li, Qibing Lin, Ting Zhang, Yupeng Wang, Chunlei Zhou, Huan

RiceOsSHI1 Regulates Plant Architecture Through Modulating the Transcriptional Activity of IPA1 in

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