a,b b c a,1 - plant physiology · 137 in rice, over 50% of genes show h3k4 methylation (zong et...

1

The COMPASS-like complex promotes flowering and panicle branching in rice 1 2 Pengfei Jianga,b, Shiliang Wanga,b, Haiyang Jiangb, Beijiu Cheng b, Keqiang Wuc, and Yong Dinga,1 3 4 a CAS Center for Excellence in Molecular Plant Sciences, School of Life Sciences, University of 5

Science & Technology of China, Hefei, Anhui, China 230027 6 b National Engineering Laboratory of Crop Stress Resistance/ Key Laboratory of Crop Biology of 7

Anhui Province, School of Life Sciences, Anhui Agricultural University, Hefei, Anhui, China 8

230036 9 c Institute of Plant Biology, College of Life Science, National Taiwan University, Taipei, Taiwan 10

10617 11

12 1 Address correspondence to [email protected] 13 14 15 16 17 1Corresponding author: 18 19 Yong Ding 20 School of Life Sciences, 21 University of Science & Technology of China 22 443 Huangshang Road 23 Hefei, Anhui, China 230027 24 25 Email: [email protected] 26 27 Short title: COMPASS-like complex in rice development 28 29 30 One-sentence summary: OsWDR5a and OsTrx1/SDG723 form the core components 31 of the COMPASS-like complex to positively regulate the flowering time and panicle 32 branching in rice. 33 34 35 36 37 Author Contributions 38

Y.D. and P.J. conceived the study and designed the experiments. P.J. performed most 39

of the experiments, Y.D. wrote the manuscript. 40 41 42

Plant Physiology Preview. Published on February 12, 2018, as DOI:10.1104/pp.17.01749

Copyright 2018 by the American Society of Plant Biologists

www.plantphysiol.orgon April 9, 2020 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

http://www.plantphysiol.org

2

Abstract 43

Flowering time (heading date) and panicle branch number are important agronomic 44

traits that determine yield in rice (Oryza sativa). The activation of flowering requires 45

histone methylation, but the roles of tri-methylation of lysine 4 of histone 3 46

(H3K4me3) in modulating heading date and panicle development are unclear. Here, 47

we showed that the COMPASS-like complex promotes flowering and panicle 48

branching. The rice WD40 protein OsWDR5a interacts with the TRITHORAX-like 49

protein OsTrx1/SDG723 to form the core components of the COMPASS-like 50

complex. Plants in which OsWDR5a or OsTrx1 expression was decreased by RNA 51

interference produced fewer secondary branches and less grain, and exhibited a 52

delayed heading date under long-day and short-day conditions, whereas loss of 53

OsWDR5a function resulted in embryo lethality. OsWDR5a binds to Early heading 54

date 1 (Ehd1) to regulate its H3K4me3 and expression levels. Together, our results 55

show that the COMPASS-like complex promotes flowering and panicle development, 56

and suggest that modulation of H3K4me3 levels by the COMPASS-like complex is 57

critical for rice development. 58

59

60

61

62

63

64

65

66

67

68

69

70

71

72



3

Introduction 73

The timing of flowering is an important agricultural trait not only for successful 74

reproduction, but also for balancing vegetative growth with reproductive 75

growth. Heading date1 (Hd1) encodes a zinc finger protein, an ortholog of 76

Arabidopsis CONSTANS (CO). Hd1, which is controlled by photoperiod, promotes 77

floral transition under short-day (SD) conditions and represses it strongly under 78

long-day (LD) conditions. Hd1 regulates homologs of Arabidopsis FLOWERING 79

LOCUS T (FT), Heading date 3a (Hd3a) and RICE FLOWERING TIME LOCUS T1 80

(RFT1), encoding proteins that function as SD and long-day (LD) florigens in rice, , 81

respectively. In addition to the Hd1 pathway, rice has a unique, independent 82

flowering-time pathway mediated by Early heading date 1 (Ehd1). Ehd1 encodes a 83

B-type response regulator that promotes flowering by controlling the expression of 84

Hd3a and RFT1 under SDs and LDs (Doi et al., 2004). Ehd1, a central integrator 85

involved in flowering time, is activated by Ehd2 under LD and SD, and by 86

OsMADS50 under LD conditions, whereas it is repressed by Grain number, plant 87

height, and heading date 7 (Ghd7) (Matsubara et al., 2008; Itoh et al., 2010). 88

OsMADS56 interacts with OsMADS50 in vitro; these two MADS-box proteins form 89

a heterodimer and function antagonistically through the OsLFL1-Ehd1 pathway 90

under LD (RYU et al., 2009). OsMADS51, another MADS-box gene, promotes 91

Ehd1 expression under SD (Kim et al., 2007). In addition to being activated by 92

MADs-box proteins, Ehd1 is suppressed by Grain Number Plant Height and Heading 93

date7 (Ghd7), which encodes a CCT domain protein (Xue et al., 2008). Ghd7 is 94

activated by EL1 (Early flowering 1)/Hd16, which encodes a casein kinase I protein 95

(Dai and Xue, 2010), and suppressed by Ehd3 (Matsubara et al., 2011). 96

The activation of flowering time also requires the histone methylation modulated 97

by SET-domain group proteins (SDG) (Sun et al., 2012; Sui et al., 2013; Choi et al., 98

2014; Liu et al., 2015). SDG701, related to Arabidopsis SDG2, regulates the 99

tri-methylation of lysine 4 of histone 3 (H3K4me3) at Hd3a and RFT1 (Liu et al., 100

2017). OsTrx1/SDG723, encoded by LOC_Os09g04890, a rice homolog of the 101

TRITHORAX-like protein, interacts with Ehd3 to boost flowering by negatively 102



4

regulating the expression of Ghd7 (Choi et al., 2014). SDG724, SDG725, and 103

SDG708 encode proteins that belong to SET domain family II, which function in di- 104

and tri-methylation modifications of lysine 36 of H3 (H3K36me2/3). Loss of function 105

of any of these proteins results in late flowering in both LD and SD (Sun et al., 2012; 106

Sui et al., 2013; Choi et al., 2014; Liu et al., 2015). 107

The yeast (Saccharomyces cerevisiae) trithorax protein SET1 is the sole 108

methyltransferase acting on lysine 4 of histone H3, and is responsible for the mono, 109

di-, and tri-methylation of H3K4 (Bernstein et al., 2002; Santos-Rosa et al., 2002). 110

Set1 forms a multi-protein complex known as COMPASS (COMplex 111

of Proteins Associated with Set1), which functions as a H3K4 methylase in yeast 112

(Briggs et al., 2001; Shilatifard, 2012). The COMPASS complex is highly 113

evolutionarily conserved from yeast to humans to plants. The shared subunits between 114

yeast COMPASS and the metazoan Set1/MLL (Mixed lineage leukemia 115

protein)/COMPASS-like complexes include ASH2, RbBP5, and Wdr5 (Takahashi et 116

al., 2011; Shilatifard, 2012). In mammalian cells, mammalian TRITHORAX protein 117

MLL1 activates Hox expression and tri-methylates less than 5% of human genes 118

(Milne et al., 2002). WDR5, a WD40 protein, is conserved from yeast to mammals to 119

plants. Earlier studies suggested that WDR5 interacts with methylated H3K4 to 120

catalyze H3K4me3 (Wysocka et al., 2005; Dou et al., 2006), but subsequent work 121

demonstrated that it binds an arginine-bearing motif in MLL1, which is independent 122

of methylated H3K4 (Couture et al., 2006; Trievel and Shilatifard, 2009). WDR5 and 123

RbBP5 stabilize the WDR5–RbBP5–MLL1 complex, whereas Ash2L has no obvious 124

structural role in this complex. Knockdown of Ash2L, RbBP5, or WDR5 decreased 125

the global H3K4me2/3 level (Dou et al., 2006). In Arabidopsis, the 126

ATX1/COMPASS-like complex comprises the conserved subunits ASH2, RbBP5, 127

and AtWDR5a (Jiang et al., 2009; Jiang et al., 2011; Ding et al., 2012). Arabidopsis 128

TRITHORAX-like protein ATX1 tri-methylates H3K4 at specific genes involved in 129

multiple biological processes, such as flowering time, dehydration stress responses, 130

and flower organ development (Alvarez-Venegas et al., 2003; Pien et al., 2008; Ding 131

et al., 2011, 2011; Ding et al., 2012; Ding et al., 2012). AtWDR5a associates with 132



5

ATX1 to form a pre-initiation complex that promotes transcription with recruitment 133

of high levels of RNA polymerase II (Ding et al., 2011; Ding et al., 2012). AtWDR5a 134

negatively regulates flowering time by inducing H3K4me3 and RNA polymerase II at 135

FLOWERING LOCUS C (FLC) (Jiang et al., 2009; Ding et al., 2012). 136

In rice, over 50% of genes show H3K4 methylation (Zong et al., 2013), 137

suggesting that H3K4 methylation has widespread functions in many biological 138

processes. However, the roles of H3K4 methylation modulated by the 139

COMPASS-like complex in flowering time and panicle branching are yet to be 140

determined in rice. Here, we report that OsWDR5a interacts with OsTrx1/SDG723 141

and functions as a core component of the COMPASS-like complex. OsWDR5a binds 142

Ehd1 to regulate its H3K4me3 and transcription levels. Knockdown of OsWDR5a or 143

OsTrx1/SDG723 result in a late heading date (i.e., induction of flowering) under LD 144

and SD conditions, and a reduction of secondary branches. 145

146

147



6

Results 148

Characterization of an OsWDR5a mutant in rice 149

The rice genome encodes two WD40 proteins related to Arabidopsis WDR5: 150

OsWDR5a and OsWDR5b. OsWDR5a is a 324-amino acid protein encoded by 151

LOC_Os03g51550. Phylogenetic analysis showed that OsWDR5a and OsWDR5b are 152

conserved in yeast, Drosophila, mammals, and plants (Supplemental Figure 1A). To 153

characterize the function of OsWDR5a in rice, we identified a mutant with a T-DNA 154

insertion in this gene from the T-DNA Tagged Rice Service Center (TTRSC) (Hsing 155

et al., 2007). Genotypic analysis showed that the T-DNA is inserted in exon 1 of 156

OsWDR5a (Supplemental Figure 2A). We investigated the segregation ratio of 157

progeny from self-pollinated F1 plants heterozygous for OsWDR5a. In the F2 158

population, 85 plants without T-DNA insertions and 180 heterozygous plants were 159

obtained, but no homozygous mutants were identified. Therefore, OsWDR5a behaved 160

like a recessive gene, with a segregation ratio of 2:1 (180:85; χ2 = 0.1377; P > 0.05) in 161

the F2 population, indicating that the mutant phenotype is attributed to a single locus 162

and that the loss of OsWDR5a function is lethal. Self-pollination of the F1 progeny of 163

heterozygous OsWDR5a plants produced many green seeds, all of which aborted 164

(Figure 1A and B). 165

F1 progenies derived from pollination of heterozygous OsWDR5a plants with 166

wild-type pollen or from pollination of wild-type plants with heterozygous OsWDR5a 167

pollen were indistinguishable from progenies derived from self-pollination of the wild 168

type, suggesting that OsWDR5a might not be involved in floral organogenesis. We 169

dissected inflorescences from wild-type and heterozygous OsWDR5a plants. Spikelets 170

from heterozygous OsWDR5a plants contained various organs that were similar to 171

those of the wild type (Supplemental Figure 2B). In addition, the mature pollen grains 172

from heterozygous OsWDR5a plants were similar to those of the wild type 173

(Supplemental Figure 2C). These results suggested that OsWDR5a might instead be 174

involved in embryogenesis. 175

To confirm the lethal phenotype caused by the oswdr5a mutation, we generated 176

full-length OsWDR5a cDNA fused to GFP driven by the maize Ubiquitin promoter 177



7

(ProUBI:GFP-OsWDR5a) and transformed this construct into the progenies of the 178

heterozygous OsWDR5a plants. The lethal phenotype of homozygous oswdr5a plants 179

was completely rescued by exogenous expression of OsWDR5a (Supplemental Figure 180

2D, E, and F), indicating that GFP-OsWDR5a retains the function of OsWDR5a. 181

182

Loss of OsWDR5a function leads to the termination of embryogenesis 183

We investigated seed development at different days after fertilization (DAF). 184

There was no difference between wild-type and heterozygous OsWDR5a plants 185

during the first 3 DAF. After 5 DAF, the seeds from heterozygous OsWDR5a plants 186

became shrunken, which persisted until 10 DAF, whereas normal, rounded seeds were 187

observed in the wild type at this stage (Figure 1C). 188

To investigate how the OsWDR5a mutation affects embryo development, we 189



8

observed embryogenesis in the wild-type and heterozygous OsWDR5a plants. We 190

detected 37 aborted embryos and 119 well-developed embryos from the progeny of 191

heterozygous OsWDR5a plants (3:1 ratio, χ2 = 0.0769; P > 0.05), which is consistent 192

with the high ratio of aborted seeds described above, suggesting that the loss of 193

OsWDR5a function is lethal. At 3 days after pollination (DAP), the wild-type zygote 194

divided quickly to form a globular embryo, in which only the epidermal cells 195

differentiated. The globular embryos of progeny of heterozygous OsWDR5a plants 196

were indistinguishable from those of wild type at 2 and 3 DAP (Figure 1 D; a–d). At 4 197

DAP, the first morphogenetic events occurred in wild type: the formation of the shoot 198

apical meristem, coleoptile primordium, and radicle primordium. However, embryos 199

from plants harboring a mutation in OsWDR5a failed to differentiate and resembled 200

an undifferentiated mass of cells (Figure 1 D; e and f). We obtained more evidence for 201

the lack of differentiation caused by the mutation of OsWDR5a at 5 to 10 DAP, when 202

all embryonic organs had formed and embryogenesis was completed in wild type 203

(Figure 1 D; g–j). These results indicate that the embryo lethality mediated by 204

OsWDR5a occurs at an early stage of embryogenesis. 205

206

OsWDR5a binds Histone H3 207

In mammalian cells, WDR5 binds the N-terminus of H3 independently of 208

H3K4 methylation (Couture et al., 2006; Song and Kingston, 2008). We investigated 209

whether OsWDR5 can bind H3 substrate. A protein containing OsWDR5a fused to 210

GST bound to beads containing a His fused to H3, but did not bind H2A, H2B, or H4 211

(Figure 2A). In a complementary experiment, bead-attached GST-OsWDR5a bound 212

to the soluble His-tagged H3, but not to other histones (Figure 2B). Therefore, we 213

concluded that OsWDR5a interacts with H3. 214

215

Knockdown of OsWDR5a results in a late heading date and small panicles 216

To investigate the biological roles of OsWDR5a in rice at the vegetative stage, we 217

selected a non-conserved region at the N-terminus of OsWDR5a to ensure sequence 218

specificity and generated a knockdown mutant via RNA interference (RNAi) (Figure 219



9

3A). We introduced a hairpin construct driven by the maize Ubiquitin promoter into 220

rice explants and successfully selected and regenerated transgenic lines (Figure 3B). 221



10

As shown in Figure 3C, the transcript levels of OsWDR5a, but not OsWDR5b, were 222

significantly reduced in the OsWDR5aIR (RNAi plant) transformants, as revealed by 223

RT-PCR analyses, suggesting that we successfully obtained OsWDR5-knockdown 224

plants by RNAi. After regeneration from T1 plants, the OsWDR5aIR transformants 225

were found to have an obvious late-heading date phenotype when grown under both 226

LD (Hefei) and SD (Lingshui) conditions (Figure 3D and E). We examined the 227

panicle branches and grain number, and found that the secondary branches and grain 228

number, but not primary branches, were reduced in OsWDR5aIR transformants 229

(Figure 3F–I). 230

OsWDR5b, which is encoded by LOC_Os07g38430, is closely related to 231

OsWDR5a with 61% sequence identity and 75% similarity (Supplemental Figure 1B). 232

Plants with knocked-down expression of OsWDR5b displayed a similar flowering 233



11

time to that of the wild type in LDs and SDs (Supplemental Figure 3). We therefore 234

concluded that OsWDR5a, but not OsWDR5b, is required for proper heading date and 235

panicle development. 236

237

OsWDR5a interacts with OsTrx1 238

OsWDR5a is closely related to WDR5 from Arabidopsis and humans, based on the 239

alignment of WDR5 protein sequences, suggesting that OsWDR5a might interact with 240

rice TRITHORAX family proteins. The rice genome encodes 39 SET domain proteins, 241

three of which belong to the TRITHORAX-like family (Ding et al., 2007; Ng et al., 242

2007; Avramova, 2009). We generated fusion proteins containing full-length 243

TRITHORAX-like proteins with the binding domain (BD) for yeast two-hybrid 244

analysis with activation domain-tagged OsWDR5a (AD-OsWDR5a). The results 245

revealed that OsTrx1 bound strongly to OsWDR5a, but not to OsWDR5b (Figure 246

4A). 247

This yeast two-hybrid interaction was confirmed by bimolecular fluorescence 248

complementation (BiFC) and co-immunoprecipitation analyses. Functional YFP in 249

the nucleus was observed when OsTrx1-YFPN (fused with the N-terminal half of 250

yellow fluorescent protein) was co-expressed with OsWDR5a-YFPC (fused with the 251

C-terminal half of YFP), but not in the controls (Figure 4B). Immunoprecipitation 252

using FLAG antibody revealed that SDG7213 bound to OsWDR5a in rice protoplasts 253

co-transformed with FLAG-OsWDR5a and GFP-OsTrx1 (Figure 4C). These results 254

indicated that OsTrx1 interacts with OsWDR5a in vitro and in vivo. 255

Next, we tested which domain is critical for the interaction of OsWDR5a with 256

OsTrx1. OsTrx1 contains PWWP, DAST, ePHD, and SET domains (Figure 4D). Both 257

the N-terminus and C-terminus of OsTrx1 were fused with BD. The C-terminus of 258

OsTrx1 (OsTrx1C), but not its N-terminus (OsTrx1N), bound to OsWDR5a (Figure 259

4D and E). In mammals, WDR5 preferentially recognizes the WDR5 Interaction (Win) 260

motif, which is located in the N-terminal SET region of MLL1 and other SET1 family 261

members (Patel et al., 2008; Dharmarajan et al., 2012). We detected the conserved 262

Win motif (containing five amino acids) in OsTrx1 in an alignment with 263



12

TRITHORAX proteins from mammalian cells to plants (Figure 4F). Within OsTrx1C, 264

the SETWin and Win motifs bound to OsWDR5a, but DAST and the ePHD domain 265

(OsTrx1DH) or SET domain (SET) alone did not (Figure 4E). These yeast two-hybrid 266

interactions were further validated by a pull-down assay. Beads attached to 267

His-SETWin and the His-Win motif bound to soluble GST-OsWDR5a, but His-SET 268

did not (Figure 4G), suggesting that the Win motif of OsTrx1 is sufficient for the 269

interaction between OsTrx1 and OsWDR5a. 270

271

OsWDR5a are involved in the Ehd1–RFT1 pathway 272

To investigate the roles of OsWDR5a in the flowering-time network, we isolated total 273

RNA from leaves of 80-day-old plants and subjected it to quantitative RT-PCR 274

analysis. Ehd1 and Hd1 transcript levels exhibited a strong diurnal rhythmic pattern in 275

wild-type plants. Ehd1, but not Hd1, was markedly reduced in the OsWDR5a RNAi 276

lines, suggesting that OsWDR5a might not be involved in the photoperiod pathway 277



13

(Figure 5A). These results are consistent to the late-flowering time phenotype of 278

OsWDR5aIRs under LDs and SDs. 279

We measured the mRNA levels of RFT1 and Hd3a, and found that the 280

expression of RFT1 and Hd3a was abolished in the OsWDR5aIR RNAi lines. 281

Ghd7, which acts as a negative regulator of Ehd1, was highly induced in the 282

transformants. Next, we examined the expression of Ehd2, Ehd3, Ehd4, and OsEL1, 283

and found that these genes were not affected in the transformants compared to the 284

wild type. The SD flowering activator OsMADS51, but not OsMADS50 or OsMADs26, 285

was downregulated in OsWDR5aIRs (Figure 5A). The upregulated and downregulated 286



14

genes are similar to those in OsTrx1 knockdown lines (Choi et al., 2014). These 287

results suggested that OsWDR5a and OsTrx1 function together and might be involved 288

in regulating heading date in rice through the Ehd1–RFT1 pathway under LD 289

conditions. 290

We generated an OsTrx1 knockdown mutant using the RNAi approach. RT-PCR 291

revealed that OsTrx1 transcript levels were strongly downregulated in two different 292

RNAi lines (Supplemental Figure 4 A, B, and C). The OsTrx1IR (RNAi plant) 293

transformants displayed a late-flowering phenotype under LD and SD conditions 294

(Supplemental Figure 4D and E), suggesting that OsTrx1 might be involved in a 295

photoperiod-independent pathway. 296

We then examined the pinnacle and grain number and found that the secondary 297

branches and grain number, but not primary branches, were reduced in the OsTrx1IR 298

lines (Figure 5B–E). These results suggested that OsTrx1 is required for proper 299

flowering time and panicle development in rice. 300

301

OsWDR5a is required for H3K4me3 deposition at Ehd1 302

To elucidate the possible relationship between OsTrx1 and OsWDR5a, we crossed 303

the OsWDR5IR transformants with the OsTrx1IR lines and generated plants with 304

knocked down expression of both OsTrx1 and OsWDR5a. The double knockdown 305

plants had a late-flowering phenotype similar to that of the OsTrx1IR lines under LDs 306

(Figure 6A and B), suggesting that OsTrx1 functions in the same pathway as 307

OsWDR5a. Since OsTrx1 is a homolog of ATX1, we investigated whether global 308

H3K4me3 and H3K4me2 levels are affected by OsWDR5a and OsTrx1. Immunoblot 309

analysis revealed no global changes in H3K4me2 or H3K4me3 in the transformants 310

(Figure 6C), suggesting that OsWDR5a and OsTrx1 might regulate specific genes. 311

Next, we investigated if the reduced transcript levels of the genes were due to 312

attenuated H3K4me3 in OsWDR5aIRs. We investigated the distribution of H3K4me3 313

by chromatin immunoprecipitation (ChIP), followed by quantitative PCR analysis of 314

DNA enrichment. H3K4me3 levels were reduced at Ehd1, RFT1, and Hd3a in the 315

OsWDR5aIR lines, indicating that OsWDR5a is required for H3K4me3 (Figure 6D 316



15

and E, and Supplemental Figure 5A and B). Since loss of OsTrx1 function led to 317

upregulation of Ghd7 (Choi et al., 2014), we investigated H3K4me3 levels at Ghd7 318

and found that H3K4me3 levels of Ghd7 were upregulated in OsTrx1IR and 319

OsWDR5aIR plants (Supplemental Figure 5D-F). 320

321

Next, we examined whether OsWDR5a directly targets these genes. We assessed 322

the distribution of OsWDR5a in complemented plants harboring 323

ProUBI:GFP-OsWDR5a using ChIP analysis with a specific GFP antibody, followed 324

by quantitative PCR analysis of the DNA enrichment at multiple points along the 325

Ehd1 promoter. OsWDR5a was highly enriched along the promoter and coding region 326



16

of Ehd1 in two transgenic lines harboring ProUBI:GFP-OsWDR5a, but not in the 327

control (Figure 6F). However, OsWDR5a was not enriched along RFT1, Hd3a, or 328

Ghd7 (Supplemental Figure 5C and G). These results indicated that OsWDR5a 329

directly targets Ehd1 and activates the H3K4me3 of Ehd1. 330

331

332

333



17

Discussion 334

In this study, we found that the COMPASS-like complex modulates panicle 335

development and the induction of flowering in rice. OsWDR5a binds to OsTrx1, and 336

these two factors form core components of the rice COMPASS-like complex. Defects 337

in OsWDR5a and OsTrx1 result in a reduction of secondary branching and a late 338

heading date under both LD and SD conditions, and these two factors are involved in 339

the Ehd1–RFT1 pathway. These results were further supported by the finding that 340

OsWDR5a induced the expression and H3K4me3 enrichment of Ehd1. Together, 341

these results suggest that the COMPASS-like complex modulates heading date and 342

panicle branching in rice. 343

WDR5, a WD40 protein, is conserved from yeast to mammals to plants. Yeast 344

Cps30, a homolog of WDR5, is essential for COMPASS complex formation/stability 345

and for full histone methyltransferase activity in this complex. In mammals, MLL1 346

and WDR5 are critical for the integrity of the MLL1 complex, and therefore, its 347

methyltransferase activity (Dou et al., 2006, Patel et al., 2008 and Song and Kingston, 348

2008). WDR5 was originally identified as an interactor of methylated lysine 4 of H3; 349

the following results indicated that this interaction is dependent on the H3 motif, but 350

not the methylated lysine 4 of H3 (Song and Kingston, 2008; Trievel and Shilatifard, 351

2009). Our study also suggested that OsWDR5a bound to H3, but not the other 352

histones. WDR5 interacts with the Win motif of MLL1, including the arginine-bearing 353

motif, which is critical for this binding (Patel et al., 2008; Patel et al., 2008; 354

Dharmarajan et al., 2012). Sequence alignment showed that the Win motif is 355

conserved in mammals and plants. Although Arabidopsis WDR5a interacts with many 356

SET domain proteins (Jiang et al., 2011), our results showed that the interaction 357

between OsWDR5a and OsTrx1 depends on the presence of the conserved Win motif. 358

The interaction between OsWDR5a and OsTrx1 was also supported by the similar 359

phenotypes of OsWDR5aIR and OsTrx1IR plants and the down-regulation of 360

flowering network genes in these lines. The OsTrx1IR plants displayed a slight late- 361

flowering phenotype under SD (Lingshui) conditions; one possibility is that the 362

daylight in Lingshui for rice growth was around 11 hours (Supplemental File 1). 363



18

In addition to the altered flowering time and panicle branches, the loss of 364

OsWDR5a function leads to the termination of embryo development, indicating that 365

OsWDR5a plays two distinct roles at the vegetative phase and reproductive phase. 366

Therefore, OsWDR5a is involved in more developmental processes than OsTrx1. Loss 367

of OsWDR5a function resulted in termination of embryogenesis at 4 DAP (early 368

embryo differentiation), suggesting that OsWDR5a might be involved in the initiation 369

of embryogenesis in rice. Even though OsWDR5b is closely related to OsWDR5a, 370

OsWDR5b was not observed to interact with SDG723. Knockdown of OsWDR5b did 371

not result in notable changes in flowering time, suggesting that OsWDR5b evolutes 372

the divergent functions with OsWDR5a. In mammalian cells, WDR5 residues 373

Tyr-191, Pro-173, Phe-149, and Asp-172 line the A-pocket, and residues Tyr-191, 374

Pro-216, and Leu-234 line the B-pocket. Both pockets are critical for MLL1 375

interaction (Dharmarajan et al., 2012). The Tyr-191 and Pro-216 were conserved in 376

OsWDR5a, but not in OsWDR5b. The functions of these two amino acids in protein 377

interaction and developmental regulation merit further study. 378

The COMPASS-like complex is highly evolutionarily conserved from yeast to 379

humans to plants. In mammalian cells, knockdown of WDR5 expression led to 380

reduced H3K4me3 levels and expression levels of Hox-a9 and Hox-c8, as was also 381

observed in the absence of MLL1 (Wysocka et al., 2005). Defects in any components 382

of the Arabidopsis COMPASS-like complex reduced the transcription level and 383

H3K4me3 level at FLC, resulting in early flowering, which suggested that the 384

Arabidopsis COMPASS-like complex suppresses flowering time (Jiang et al., 2011). 385

By contrast, OsWDR5a and OsTrx1 promoted flowering time in rice. Arabidopsis and 386

rice contain different flowering pathways. FLC is central regulator suppressing floral 387

transition in Arabidopsis, which is not known in rice. Mutations in ATX1 and 388

knockdown of WDR5a lead to early flowering due to reduced transcript levels of FLC. 389

Rice, a model SD plant, contains two major flowering pathways: a conserved 390

photoperiod pathway and a unique photoperiod-independent flowering-time pathway. 391

Ehd1 is an evolutionarily unique gene in rice that does not have an ortholog in 392

Arabidopsis (Doi et al., 2004; Tsuji et al., 2011). In the current study, OsWDR5a was 393



19

identified as a factor that positively regulates Ehd1 transcription and histone 394

modification level. OsWDR5a bound to Ehd1, but not RTF1, or Hd3a. This 395

possibility of the specificity is that the transcriptional factors interact with the subunits 396

of the COMPASS-like complex and trigger OsWDR5a to target Ehd1. Our recent 397

study suggested the transcriptional factors are critical for flowering time and 398

hypocotyl elongation modulated by histone phosphrylation (Su et al., 2017; Zheng et 399

al., 2017). A previous study suggested that OsTrx1 regulates flowering time via 400

repressing the transcription of Ghd7 (Choi et al., 2014). Our study suggests that the 401

H3K4me3 levels of Ghd7 were reduced in OsWDR5aIR and OsTrx1IR plants. The 402

activated transcription levels of Ghd7 in the OsTrx1IR and OsWDR5aIR lines indicate 403

that Ghd7 might not be the direct target of OsTrx1. Together, our findings indicate 404

that the COMPASS-like complex promotes H3K4me3 at Ehd1 to regulate heading 405

date and panicle branching in rice. 406

407

408



20

Methods 409

Materials 410

The plants used in this study are in the Oryza sativa ssp. japonica cv. Nipponbare 411

background, except for the T-DNA mutant Oswdr5a, which is in the Tainung 67 412

background and was obtained from the T-DNA Tagged Rice Service Center (TTRSC) 413

(Hsing et al., 2007). The seeds of the T-DNA mutant, Oswdr5a, were a gift from 414

Professor Keqiang Wu from National Taiwan University. All plants were regenerated 415

from callus as described (Xu et al., 2015). T1 generation plants were generated from 416

the seeds of self-pollinated T0 plants. The plants were grown in fields from April 20 to 417

October at Hefei (Anhui) and from November 20 to February at Lingshui (Hainan), 418

China. The detailed photoperiod for rice growth at Hefei and Lingshui are described 419

in Supplemental File 1. 420

421

Plasmid constructs 422

The plasmids were constructed using the DNA primers and protocols described in 423

Supplemental File 2. All cloned DNA was confirmed by DNA sequencing. 424

425

Pollen fertility 426

Ten panicles each from the wild type (WT) (TN67) and heterozygous OsWDR5a 427

plants were sampled at 1 or 2 days before flowering to determine the pollen fertility. 428

Six florets per panicle were sampled from the upper, middle, and lower portions of the 429

panicle. One anther per floret was collected, and six anthers from the same panicle 430

were mixed and spread onto a slide. The pollen grains on the slide were stained with 1% 431

IK-I2 and the darkness of the staining was used as an indicator of pollen fertility. Four 432

views per slide were obtained under a microscope (Leica, M165FC), resulting in 40 433

views per hybrid. 434

435

Histological analyses 436

Panicles from WT (TN67) and heterozygous OsWDR5a plants were fixed in FAA (3.7% 437

formaldehyde, 5% acetic acid, and 50% ethanol) at 4°C overnight. The samples were 438



21

auto-dehydrated in a LEICA ASP200S tissue processor, embedded in paraffin 439

(Sigma-Aldrich), and sectioned to 8-μm thicknesses using a LEICA RM2255 rotary 440

microtome. After dewaxing with xylene and hematoxylin-eosin staining, the sections 441

were observed under a light microscope (Zeiss, Axioscope A1 polarized light 442

microscope). 443

444

Protein pull-down assays, Co-IP, and immunoblot assays 445

For the pull-down assay, beads were incubated with 3 µg of the fusion protein, 446

washed, and incubated with 3 µg of soluble protein overnight at 4°C. Mock controls 447

included extracts prepared from either the His-Tag or GST vectors. The beads were 448

washed five times with a solution containing 20 mM Tris (pH 7.4), 150 mM NaCl, 449

and 0.05% Tween 20, separated on an SDS-PAGE gel, and analyzed by immunoblot 450

using an anti-GST antibody (GenScript; A00866-100, Lot: 13D000626) or an anti-His 451

antibody (Abmart; M30111M, Lot: 273884). 452

For the Co-IP, OsWDR5a and OsTrx1 were fused with FLAG or GFP and 453

cloned into the pUC19 vector. The Co-IP was performed as described previously (Su 454

et al., 2017; Zheng et al., 2017). Briefly, 1×106 rice protoplasts were lysed with 455

PEN-140 buffer (140 mM NaCl, 2.7 mM KCl, 25 mM Na2HPO4, 1.5 mM KH2PO4, 456

0.01 mM EDTA, and 0.05% CA-630). The supernatant was pre-cleared with Protein 457

G and precipitated with anti-FLAG antibody (Sigma-Aldrich; H6908, Lot: 458

SLBQ7119V). The protein complexes were isolated by binding to protein G beads 459

(Santa Cruz; Sc-2002) and washed five times with PEN-400 buffer (400 mM NaCl, 460

2.7 mM KCl, 25 mM Na2HPO4, 1.5 mM KH2PO4, 0.01 mM EDTA, and 0.05% 461

CA-630). The samples were analyzed by protein gel blot analysis using an anti-GFP 462

antibody (Clontech Laboratories, Inc.; JL-8, Lot: A5033481) or anti-FLAG 463

antibody. 464

465

Transient expression in N. benthamiana leaves and BIFC 466

Rice OsWDR5 and OsTrx1 were cloned into pUC-SPYCE (aa 156–239) or 467

pUC-SPYNE (aa 1–155), respectively. Transient expression assays were performed as 468



22

described previously (Lu et al., 2017). Briefly, Agrobacterium colonies were grown 469

overnight in 10 mL of medium plus antibiotics. The cells were collected and 470

re-suspended in an equal volume of induction medium (60 mM K2HPO4, 33 mM 471

KH2PO4, 7.5mM (NH4)SO4, 1.7 mM Na citrate · 2H2O, 10 mM MES, 1 mM MgSO4, 472

0.2% glucose, 0.5% glycerol, antibiotics, and 50 µg/mL acetosyringone). After 473

shaking for 6 hours, the cells were re-suspended to an OD of 0.6 in infiltration 474

medium (10 mM MgCl2, 10 mM N-morpholino-ethanesulfonic acid, 150 µM 475

acetosyringone) and used to inject the abaxial surfaces of N. benthamiana leaves. YFP 476

signals were visualized 24–48 h after inoculation by confocal laser scanning 477

microscopy (Zeiss, LSM700). 478

479

Reverse Transcription and Quantitative PCR 480

Total RNA was isolated from the leaves of 80-day-old plants and reverse transcribed 481

with oligo(dT) primers (Promega), and the amounts of individual gene transcripts 482

were measured with gene-specific primers. Quantitative PCR analysis was performed 483

with the CFX real-time PCR instrument (Bio-Rad) and SYBR Green mixture (Roche). 484

The relative expression of the genes was quantitated with the 2-ΔΔCT Ct calculation, 485

using UBIQUITIN as the reference housekeeping gene for the expression analyses. 486

The enrichment of DNA at specific genes was quantified with the 2-ΔΔCT Ct 487

calculation, using UBIQUITIN as the reference housekeeping gene for chromatin 488

immunoprecipitation assays. See Supplemental File 2 for primers. 489

490

ChIP Assay 491

ChIP was performed as described (Lu et al., 2017; Su et al., 2017; Zheng et al., 2017). 492

Briefly, 3 g of leaves were ground in powder, then fixed with 1% formaldehyde for 10 493

min and quenched in 0.125 M glycine. The pellet was homogenized in buffer I (0.4 M 494

sucrose, 10 mM Tris (pH 8.0), 5 mM β-mercaptoethanol, 0.1 mM PMSF, and protease 495

inhibitor cocktail) and filtered through Miracloth. After centrifugation, the pellet was 496

extracted with buffer II (0.25 M sucrose, 10 mM Tris (pH 8.0), 10 mM MgCl2, 1% 497

Triton X-100, 5 mM β-mercaptoethanol, 0.1 mM PMSF, and protease inhibitor 498



23

cocktail) and then with buffer III (1.7 M sucrose, 10 mM Tris (pH 8.0), 10 mM MgCl2, 499

1% Triton X-100, 5 mM β-mercaptoethanol, 0.1 mM PMSF, and protease inhibitor 500

cocktail). The nuclei were then lysed in lysis buffer (50 mM Tris (pH 8.0), 10 mM 501

EDTA, 1% SDS, 5 mM β-mercaptoethanol, 0.1 mM PMSF, and protease inhibitor 502

cocktail) and the extract was sonicated to fragment the DNA to a size range of 300 to 503

500 bp. After centrifugation, the supernatant was diluted using dilution buffer (1.1% 504

Triton X-100, 1.2 mM EDTA, 16.7 mM Tris (pH 8.0), 167 mM NaCl, 0.1 mM PMSF, 505

and protease inhibitor cocktail) and pre-cleared with protein A or protein G magnetic 506

beads. Specific antibodies anti-H3K4me3 (Abcam; ab8580, lot; GR273043-6) and 507

anti-GFP (Clontech Laboratories, Inc.; JL-8, Lot: A5033481) or control IgG serum 508

were added to the pre-cleared supernatants for an overnight incubation at 4°C. The 509

antibody-protein complexes were isolated by binding to protein A or protein G beads. 510

The washed beads were heated at 65°C for 8 h with proteinase K to reverse the 511

formaldehyde cross-linking and digest proteins. The sample was then extracted with 512

phenol/chloroform and the DNA was precipitated in ethanol and resuspended in water. 513

The purified DNA was analyzed by quantitative PCR with the gene-specific primers 514

shown in Supplemental File 2. 515

516

Accession Numbers 517

Sequence data from this article can be found in the GenBank/EMBL data libraries 518

under accession numbers listed below: OsTrx1/SDG723 (Os09g0134500), OsWDR5a 519

(Os03g0725400), OsWDR5b (Os07g0572000). 520

521

522

Supplemental Data 523

Supplmental Figure 1. Phylogenetic analysis of WDR5 from yeast, human, 524

Arabidopsis, and rice. 525

Supplemental Figure 2. Characterization of OsWDR5a. 526

Supplemental Figure 3. Generation of OsWDR5bIRs 527

Supplemental Figure 4. Generation of OsTrx1 transformants using RNA 528



24

interference approach. 529

Supplemental Figure 5. H3K4me3 profiles at RFT1, Hd3a and Ghd7 in wild type 530

and OsWDR5aIRs. 531 Supplemental File1. The average daylight in 10-day intervals in 2017 at Hefei 532 and Lingshui, China 533 Supplemental File 2. Plasmids and primers 534 535 Acknowledgments 536

We are grateful to Dr. Peng-Cheng Wei, Hao Li, and Ya-chun Yang from Anhui 537

Academy of Agricultural Sciences for kindly helping us with rice transformation and 538

cultivation, Professor Keqiang Wu from National Taiwan University for kindly 539

providing the Oswdr5a seeds, and to all members of the Ding group for their helpful 540

discussions. This work was supported by the National Natural Science Foundation of 541

China (9143510, 31571315, and 31371306 to YD) and the Strategic Priority Research 542

Program “Molecular Mechanisms of Plant Growth and Development” of CAS (grant 543

no. XDPB04). 544 545

Competing financial interests 546

The authors claim no competing financial interests. 547

548

549

Figure 1. Loss of OsWDR5a function results in embryo lethality. 550

(A) Panicles from F1 progeny of wild-type and heterozygous OsWDR5a plants. The 551

green seeds are indicated by arrows. 552

(B) Mature seeds from wild-type and heterozygous OsWDR5a plants. Seeds at 30 553

days after fertilization (DAF) are shown. 554

(C) Seed development in wild-type and heterozygous OsWDR5a plants. Seed 555

morphology at 1 day after fertilization (DAF) to 10 DAF is shown. 556

(D) Morphogenesis of wild-type and oswdr5a mutant embryos. 557

Embryo morphology at 2 days after pollination (DAP) and 3 DAP (a–d). The 4 DAP 558

wild-type embryo has a differentiating coleoptile primordium (black arrow), shoot 559

apical meristem (white arrow), and radicle primordium (white arrowhead) (e and f). 560

The 5 DAP wild-type embryo shows a differentiating first leaf primordium (arrow) (g 561

and h). Morphologically complete 10 DAP embryos (i and j). SC, scutellum; CO, 562

coleoptile; EP, epiblast; RA, radicle. 563

Bars = 50 μm (A–D), 100 μm (E, F), and 200 μm (G–J). 564

565



25

Figure 2. OsWDR5a binds to histone H3. 566

(A) Beads containing His fused with H2A, H2B, H3, and H4 were assessed for their 567

ability to bind to soluble GST-OsWDR5a and detected with the antibody to GST 568

(Anti-GST). 569

(B) Beads containing GST fused with OsWDR5a were assessed for the ability to bind 570

to soluble His fused with H2A, H2B, H3, and H4, and detected with the antibody to 571

His (Anti-His). 572

573

Figure 3. OsWDR5aIR transformants and phenotypes of OsWDR5aIR plants. 574

(A) Gene structure of OsWDR5a. Exons are indicated by boxes and introns are 575

indicated by lines. The region used for knockdown is indicated by a line below the 576

diagram. 577

(B) Diagram of the OsWDR5a RNAi constructs. Fragments containing the OsWDR5a 578

fragment in the sense and antisense orientation separated by an unrelated spacer were 579

cloned under the control of the maize Ubiquitin promoter. 580

(C) OsWDR5a and OsWDR5b transcript levels in wild-type and OsWDR5aIR plants. 581

(D) Representative image of 120-day-old wild-type and OsWDR5aIR plants grown in 582

LD conditions (Hefei). 583

(E) Days to heading in wild-type and OsWDR5aIR plants in both LDs (Hefei) and 584

SDs (Lingshui). Values shown are mean ± standard deviation of heading days; 20 585

plants were scored per line. 586

(F) The panicles of wild-type and OsWDR5aIR plants in LDs (Hefei). 587

(G – I) The branch number (G) and (H), and grain number (I) of wild-type and 588

OsWDR5aIR plants. Values shown are mean ± standard deviation of branch number 589

and grain number; 20 plants were scored per line. 590

591

Figure 4. OsWDR5a interacts with OsTrx1. 592

(A) Yeast two-hybrid assay revealing an interaction between OsWDR5a and OsTrx1. 593

The growth of two dilutions (2×10-2 and 2×10-3) of yeast culture on SD medium 594

lacking Trp, Leu, His, and adenine is shown. 595

(B) The N-terminus of YFP or OsWDR5a fused to the N-terminus of YFP was tested 596

for its ability to bind to the C-terminus of YFP or the C-terminus of YFP fused to 597



26

OsTrx1. Yellow fluorescence (YFP) and a bright-field image (DIC) were recorded and 598

the resulting images were merged. 599

(C) Co-immunoprecipitation of OsWDR5a and OsTrx1. GFP-OsWDR5a and 600

FLAG-OsTrx1 were co-transformed into rice protoplasts, and the expressed proteins 601

were immunoprecipitated using an anti-FLAG antibody and detected with anti-Flag 602

and anti-GFP antibodies. 603

(D) Diagram of OsTrx1 showing its different domains. 604

(E) Activating domain (AD) fused to the different domains shown in (C) was tested 605

for its ability to bind to BD (Binding domain)-OsWDR5a. The growth of two 606

dilutions (2×10-2 and 2×10-3) of yeast culture on SD medium lacking Trp, Leu, His, 607

and adenine is shown. 608

(F) Alignment of the Win motif with other closely related TRITHORAX proteins 609

using ClustalW. The amino acid sequence from rice OsTrx1 (amino acids 765–785), 610

Arabidopsis ATX1 (amino acids 808–828), and human MLL1 (amino acids 3754–611

3774). The Win motifs are shown in-frame and the conserved amino acids are 612

indicated in red. 613

(G) Beads containing the His-fused SETWin, Win, and SET domains of OsTrx1 were 614

assessed for their ability to bind soluble His-fused OsWDR5a and detected with an 615

antibody to His (anti-His). 616

617

618

Figure 5. Transcript levels of flowering network genes in OsWDR5aIR plants. 619

(A) Transcript levels of flowering network genes. 620

RNA isolated from leaves of 80-day-old plants was used for RT-qPCR. The black bars 621

indicate the dark period and the white bars indicate the light period. ZT, Zeitgeber 622

time. The y-axis shows the transcript level relative to rice Actin expression. The 623

experiments were repeated at least three times, and each experiment included three 624

replicates, n = 3. 625

(B) The panicles of wild-type and OsTrx1IR plants in LD conditions. 626

(C – E) The branch number (C) and (D), and grain number (E) of wild-type and 627

OsTrx1IR plants. Values shown are mean ± standard deviation of branch number and 628

grain number; 20 plants were scored per line. 629



27

630

631

Figure 6. OsWDR5a is required for H3K4me3 at Ehd1. 632

(A) Representative image of 125-day-old wild-type, OsWDR5aIR, OsTrx1IR, and 633

OsTrx1IR OsWDR5aIR plants in LD conditions. Values shown are mean ± standard 634

deviation of branch number and grain number; 20 plants were scored per line. 635

636

(B) Days to heading of wild-type, OsWDR5aIR, OsTrx1IR, and OsTrx1IR 637

OsWDR5aIR plants. 638

(C) Global H3K4me2 and H3K4me3 levels in wild-type, OsWDR5aIR, and OsTrx1IR 639

plants. 640

(D) Gene structure of Ehd1. Exons are indicated by boxes and introns are indicated by 641

lines. The locations of the gene regions analyzed by ChIP-PCR are shown below the 642

diagram. P1–P4 indicates regions in the promoter and E1–E4 indicates regions in the 643

coding region. 644

(E) Relative H3K4me3 levels at different regions of the genes in wild-type and 645

OsWDR5aIR plants. Experiments were repeated at least three times, and the values 646

shown indicate the mean ± SE, n = 3 replicates. 647

(F) Relative OsWDR5a expression levels in plants complemented by 648

ProUBI:GFP-OsWDR5a and the wild type. The T3 (complementary line 3 for oswdr5a) 649

and T20 are indicated in Supplemental Figure 2. Experiments were repeated at least 650

three times, and the values shown indicate the mean ± SE, n = 3 replicates. 651

652

653

654

655

656

657

658 659

660

661



28

662 663



Parsed CitationsAlvarez-Venegas R, Pien S, Sadder M, Witmer X, Grossniklaus U, Avramova Z (2003) ATX-1, an Arabidopsis homolog of trithorax,activates flower homeotic genes. Current Biology 13: 627-637

Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Avramova Z (2009) Evolution and pleiotropy of TRITHORAX function in Arabidopsis. International Journal of Developmental Biology 53:371-381


Bernstein BE, Humphrey EL, Erlich RL, Schneider R, Bouman P, Liu JS, Kouzarides T, Schreiber SL (2002) Methylation of histone H3Lys 4 in coding regions of active genes. Proceedings of the National Academy of Sciences 99: 8695-8700


Briggs SD, Bryk M, Strahl BD, Cheung WL, Davie JK, Dent SY, Winston F, Allis CD (2001) Histone H3 lysine 4 methylation is mediatedby Set1 and required for cell growth and rDNA silencing in Saccharomyces cerevisiae. Genes & development 15: 3286-3295


Choi SC, Lee S, Kim S-R, Lee Y-S, Liu C, Cao X, An G (2014) Trithorax group protein Oryza sativa Trithorax1 controls flowering time inrice via interaction with early heading date3. Plant physiology 164: 1326-1337


Couture J-F, Collazo E, Trievel RC (2006) Molecular recognition of histone H3 by the WD40 protein WDR5. Nature structural &molecular biology 13: 698-703


Dai C, Xue HW (2010) Rice early flowering1, a CKI, phosphorylates DELLA protein SLR1 to negatively regulate gibberellin signalling.The EMBO Journal 29: 1916-1927


Dharmarajan V, Lee J-H, Patel A, Skalnik DG, Cosgrove MS (2012) Structural basis for WDR5 interaction (Win) motif recognition inhuman SET1 family histone methyltransferases. Journal of Biological Chemistry 287: 27275-27289


Ding Y, Avramova Z, Fromm M (2011) The Arabidopsis trithorax‐like factor ATX1 functions in dehydration stress responses via ABA‐dependent and ABA‐independent pathways. The Plant Journal 66: 735-744


Ding Y, Avramova Z, Fromm M (2011) Two distinct roles of ARABIDOPSIS HOMOLOG OF TRITHORAX1 (ATX1) at promoters and withintranscribed regions of ATX1-regulated genes. The plant cell 23: 350-363


Ding Y, Fromm M, Avramova Z (2012) Multiple exposures to drought'train'transcriptional responses in Arabidopsis. NatureCommunications 3: 740


Ding Y, Ndamukong I, Xu Z, Lapko H, Fromm M, Avramova Z (2012) ATX1-generated H3K4me3 is required for efficient elongation oftranscription, not initiation, at ATX1-regulated genes. PLoS Genet 8: e1003111



http://www.ncbi.nlm.nih.gov/pubmed?term=Alvarez%2DVenegas R%2C Pien S%2C Sadder M%2C Witmer X%2C Grossniklaus U%2C Avramova Z %282003%29 ATX%2D1%2C an Arabidopsis homolog of trithorax%2C activates flower homeotic genes%2E Current Biology 13%3A 627%2D637&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Alvarez-Venegas R, Pien S, Sadder M, Witmer X, Grossniklaus U, Avramova Z (2003) ATX-1, an Arabidopsis homolog of trithorax, activates flower homeotic genes. Current Biology 13: 627-637

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

http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Alvarez-Venegas&as_ylo=2003&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Avramova Z %282009%29 Evolution and pleiotropy of TRITHORAX function in Arabidopsis%2E International Journal of Developmental Biology 53%3A 371%2D381&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Avramova Z (2009) Evolution and pleiotropy of TRITHORAX function in Arabidopsis. International Journal of Developmental Biology 53: 371-381

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

http://scholar.google.com/scholar?as_q=Evolution and pleiotropy of TRITHORAX function 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=Evolution and pleiotropy of TRITHORAX function in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Avramova&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Bernstein BE%2C Humphrey EL%2C Erlich RL%2C Schneider R%2C Bouman P%2C Liu JS%2C Kouzarides T%2C Schreiber SL %282002%29 Methylation of histone H3 Lys 4 in coding regions of active genes%2E Proceedings of the National Academy of Sciences 99%3A 8695%2D8700&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Bernstein BE, Humphrey EL, Erlich RL, Schneider R, Bouman P, Liu JS, Kouzarides T, Schreiber SL (2002) Methylation of histone H3 Lys 4 in coding regions of active genes. Proceedings of the National Academy of Sciences 99: 8695-8700

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

http://scholar.google.com/scholar?as_q=Methylation of histone H3 Lys 4 in coding regions of active genes&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=Methylation of histone H3 Lys 4 in coding regions of active genes&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Bernstein&as_ylo=2002&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Briggs SD%2C Bryk M%2C Strahl BD%2C Cheung WL%2C Davie JK%2C Dent SY%2C Winston F%2C Allis CD %282001%29 Histone H3 lysine 4 methylation is mediated by Set1 and required for cell growth and rDNA silencing in Saccharomyces cerevisiae%2E Genes %26 development 15%3A 3286%2D3295&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Briggs SD, Bryk M, Strahl BD, Cheung WL, Davie JK, Dent SY, Winston F, Allis CD (2001) Histone H3 lysine 4 methylation is mediated by Set1 and required for cell growth and rDNA silencing in Saccharomyces cerevisiae. Genes & development 15: 3286-3295

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

http://scholar.google.com/scholar?as_q=Histone H3 lysine 4 methylation is mediated by Set1 and required for cell growth and rDNA silencing in Saccharomyces cerevisiae&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=Histone H3 lysine 4 methylation is mediated by Set1 and required for cell growth and rDNA silencing in Saccharomyces cerevisiae&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Briggs&as_ylo=2001&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Choi SC%2C Lee S%2C Kim S%2DR%2C Lee Y%2DS%2C Liu C%2C Cao X%2C An G %282014%29 Trithorax group protein Oryza sativa Trithorax1 controls flowering time in rice via interaction with early heading date3%2E Plant physiology 164%3A 1326%2D1337&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Choi SC, Lee S, Kim S-R, Lee Y-S, Liu C, Cao X, An G (2014) Trithorax group protein Oryza sativa Trithorax1 controls flowering time in rice via interaction with early heading date3. Plant physiology 164: 1326-1337

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

http://scholar.google.com/scholar?as_q=Trithorax group protein Oryza sativa Trithorax1 controls flowering time in rice via interaction with early heading date3&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=Trithorax group protein Oryza sativa Trithorax1 controls flowering time in rice via interaction with early heading date3&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Choi&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Couture J%2DF%2C Collazo E%2C Trievel RC %282006%29 Molecular recognition of histone H3 by the WD40 protein WDR5%2E Nature structural %26 molecular biology 13%3A 698%2D703&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Couture J-F, Collazo E, Trievel RC (2006) Molecular recognition of histone H3 by the WD40 protein WDR5. Nature structural & molecular biology 13: 698-703

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

http://scholar.google.com/scholar?as_q=Molecular recognition of histone H3 by the WD40 protein WDR5&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=Molecular recognition of histone H3 by the WD40 protein WDR5&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Couture&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Dai C%2C Xue HW %282010%29 Rice early flowering1%2C a CKI%2C phosphorylates DELLA protein SLR1 to negatively regulate gibberellin signalling%2E The EMBO Journal 29%3A 1916%2D1927&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Dai C, Xue HW (2010) Rice early flowering1, a CKI, phosphorylates DELLA protein SLR1 to negatively regulate gibberellin signalling. The EMBO Journal 29: 1916-1927

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


http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Dai&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Dharmarajan V%2C Lee J%2DH%2C Patel A%2C Skalnik DG%2C Cosgrove MS %282012%29 Structural basis for WDR5 interaction %28Win%29 motif recognition in human SET1 family histone methyltransferases%2E Journal of Biological Chemistry 287%3A 27275%2D27289&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Dharmarajan V, Lee J-H, Patel A, Skalnik DG, Cosgrove MS (2012) Structural basis for WDR5 interaction (Win) motif recognition in human SET1 family histone methyltransferases. Journal of Biological Chemistry 287: 27275-27289

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

http://scholar.google.com/scholar?as_q=Structural basis for WDR5 interaction (Win) motif recognition in human SET1 family histone methyltransferases&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=Structural basis for WDR5 interaction (Win) motif recognition in human SET1 family histone methyltransferases&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Dharmarajan&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Ding Y%2C Avramova Z%2C Fromm M %282011%29 The Arabidopsis trithorax�?�like factor ATX1 functions in dehydration stress responses via ABA�?�dependent and ABA�?�independent pathways%2E The Plant Journal 66%3A 735%2D744&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Ding Y, Avramova Z, Fromm M (2011) The Arabidopsis trithorax?like factor ATX1 functions in dehydration stress responses via ABA?dependent and ABA?independent pathways. The Plant Journal 66: 735-744

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

http://scholar.google.com/scholar?as_q=The Arabidopsis trithoraxâ�?�like factor ATX1 functions in dehydration stress responses via ABAâ�?�dependent and ABAâ�?�independent pathways&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The Arabidopsis trithoraxâ�?�like factor ATX1 functions in dehydration stress responses via ABAâ�?�dependent and ABAâ�?�independent pathways&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ding&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Ding Y%2C Avramova Z%2C Fromm M %282011%29 Two distinct roles of ARABIDOPSIS HOMOLOG OF TRITHORAX1 %28ATX1%29 at promoters and within transcribed regions of ATX1%2Dregulated genes%2E The plant cell 23%3A 350%2D363&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Ding Y, Avramova Z, Fromm M (2011) Two distinct roles of ARABIDOPSIS HOMOLOG OF TRITHORAX1 (ATX1) at promoters and within transcribed regions of ATX1-regulated genes. The plant cell 23: 350-363


http://scholar.google.com/scholar?as_q=Two distinct roles of ARABIDOPSIS HOMOLOG OF TRITHORAX1 (ATX1) at promoters and within transcribed regions of ATX1-regulated genes&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=Two distinct roles of ARABIDOPSIS HOMOLOG OF TRITHORAX1 (ATX1) at promoters and within transcribed regions of ATX1-regulated genes&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ding&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Ding Y%2C Fromm M%2C Avramova Z %282012%29 Multiple exposures to drought%27train%27transcriptional responses in Arabidopsis%2E Nature Communications 3%3A 740&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Ding Y, Fromm M, Avramova Z (2012) Multiple exposures to drought'train'transcriptional responses in Arabidopsis. Nature Communications 3: 740


http://scholar.google.com/scholar?as_q=Multiple exposures to drought'train'transcriptional responses 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=Multiple exposures to drought'train'transcriptional responses in Arabidopsis.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ding&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Ding Y%2C Ndamukong I%2C Xu Z%2C Lapko H%2C Fromm M%2C Avramova Z %282012%29 ATX1%2Dgenerated H3K4me3 is required for efficient elongation of transcription%2C not initiation%2C at ATX1%2Dregulated genes%2E PLoS Genet 8%3A e1003111&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Ding Y, Ndamukong I, Xu Z, Lapko H, Fromm M, Avramova Z (2012) ATX1-generated H3K4me3 is required for efficient elongation of transcription, not initiation, at ATX1-regulated genes. PLoS Genet 8: e1003111


http://scholar.google.com/scholar?as_q=ATX1-generated H3K4me3 is required for efficient elongation of transcription, not initiation, at ATX1-regulated genes.&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=ATX1-generated H3K4me3 is required for efficient elongation of transcription, not initiation, at ATX1-regulated genes.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ding&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1


Ding Y, Wang X, Su L, Zhai J, Cao S, Zhang D, Liu C, Bi Y, Qian Q, Cheng Z (2007) SDG714, a histone H3K9 methyltransferase, isinvolved in Tos17 DNA methylation and transposition in rice. The Plant Cell 19: 9-22


Doi K, Izawa T, Fuse T, Yamanouchi U, Kubo T, Shimatani Z, Yano M, Yoshimura A (2004) Ehd1, a B-type response regulator in rice,confers short-day promotion of flowering and controls FT-like gene expression independently of Hd1. Genes & Development 18: 926-936


Dou Y, Milne TA, Ruthenburg AJ, Lee S, Lee JW, Verdine GL, Allis CD, Roeder RG (2006) Regulation of MLL1 H3K4 methyltransferaseactivity by its core components. Nature structural & molecular biology 13: 713-719


Hsing Y-I, Chern C-G, Fan M-J, Lu P-C, Chen K-T, Lo S-F, Sun P-K, Ho S-L, Lee K-W, Wang Y-C (2007) A rice gene activation/knockoutmutant resource for high throughput functional genomics. Plant molecular biology 63: 351-364


Itoh H, Nonoue Y, Yano M, Izawa T (2010) A pair of floral regulators sets critical day length for Hd3a florigen expression in rice. Naturegenetics 42: 635-638


Jiang D, Gu X, He Y (2009) Establishment of the winter-annual growth habit via FRIGIDA-mediated histone methylation at FLOWERINGLOCUS C in Arabidopsis. The plant cell 21: 1733-1746


Jiang D, Kong NC, Gu X, Li Z, He Y (2011) Arabidopsis COMPASS-like complexes mediate histone H3 lysine-4 trimethylation to controlfloral transition and plant development. PLoS Genet 7: e1001330


Kim SL, Lee S, Kim HJ, Nam HG, An G (2007) OsMADS51 is a short-day flowering promoter that functions upstream of Ehd1,OsMADS14, and Hd3a. Plant Physiology 145: 1484-1494


Liu B, Wei G, Shi J, Jin J, Shen T, Ni T, Shen WH, Yu Y, Dong A (2015) SET DOMAIN GROUP 708, a histone H3 lysine 36‐specificmethyltransferase, controls flowering time in rice (Oryza sativa). New Phytologist


Liu K, Yu Y, Dong A, Shen WH (2017) SET DOMAIN GROUP701 encodes a H3K4‐methytransferase and regulates multiple keyprocesses of rice plant development. New Phytologist


Lu C, Tian Y, Wang S, Su Y, Mao T, Huang T, Chen Q, Xu Z, Ding Y (2017) Phosphorylation of SPT5 by CDKD; 2 is required for VIP5recruitment and normal flowering in Arabidopsis thaliana. The Plant Cell 29: 277-291


Matsubara K, Yamanouchi U, Nonoue Y, Sugimoto K, Wang ZX, Minobe Y, Yano M (2011) Ehd3, encoding a plant homeodomain finger‐containing protein, is a critical promoter of rice flowering. The Plant Journal 66: 603-612


Matsubara K, Yamanouchi U, Wang Z-X, Minobe Y, Izawa T, Yano M (2008) Ehd2, a rice ortholog of the maize INDETERMINATE1 gene,promotes flowering by up-regulating Ehd1. Plant physiology 148: 1425-1435


http://www.ncbi.nlm.nih.gov/pubmed?term=Ding Y%2C Wang X%2C Su L%2C Zhai J%2C Cao S%2C Zhang D%2C Liu C%2C Bi Y%2C Qian Q%2C Cheng Z %282007%29 SDG714%2C a histone H3K9 methyltransferase%2C is involved in Tos17 DNA methylation and transposition in rice%2E The Plant Cell 19%3A 9%2D22&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Ding Y, Wang X, Su L, Zhai J, Cao S, Zhang D, Liu C, Bi Y, Qian Q, Cheng Z (2007) SDG714, a histone H3K9 methyltransferase, is involved in Tos17 DNA methylation and transposition in rice. The Plant Cell 19: 9-22



http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ding&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Doi K%2C Izawa T%2C Fuse T%2C Yamanouchi U%2C Kubo T%2C Shimatani Z%2C Yano M%2C Yoshimura A %282004%29 Ehd1%2C a B%2Dtype response regulator in rice%2C confers short%2Dday promotion of flowering and controls FT%2Dlike gene expression independently of Hd1%2E Genes %26 Development 18%3A 926%2D936&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Doi K, Izawa T, Fuse T, Yamanouchi U, Kubo T, Shimatani Z, Yano M, Yoshimura A (2004) Ehd1, a B-type response regulator in rice, confers short-day promotion of flowering and controls FT-like gene expression independently of Hd1. Genes & Development 18: 926-936

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


http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Doi&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Dou Y%2C Milne TA%2C Ruthenburg AJ%2C Lee S%2C Lee JW%2C Verdine GL%2C Allis CD%2C Roeder RG %282006%29 Regulation of MLL1 H3K4 methyltransferase activity by its core components%2E Nature structural %26 molecular biology 13%3A 713%2D719&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Dou Y, Milne TA, Ruthenburg AJ, Lee S, Lee JW, Verdine GL, Allis CD, Roeder RG (2006) Regulation of MLL1 H3K4 methyltransferase activity by its core components. Nature structural & molecular biology 13: 713-719

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

http://scholar.google.com/scholar?as_q=Regulation of MLL1 H3K4 methyltransferase activity by its core components&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=Regulation of MLL1 H3K4 methyltransferase activity by its core components&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Dou&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Hsing Y%2DI%2C Chern C%2DG%2C Fan M%2DJ%2C Lu P%2DC%2C Chen K%2DT%2C Lo S%2DF%2C Sun P%2DK%2C Ho S%2DL%2C Lee K%2DW%2C Wang Y%2DC %282007%29 A rice gene activation%2Fknockout mutant resource for high throughput functional genomics%2E Plant molecular biology 63%3A 351%2D364&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Hsing Y-I, Chern C-G, Fan M-J, Lu P-C, Chen K-T, Lo S-F, Sun P-K, Ho S-L, Lee K-W, Wang Y-C (2007) A rice gene activation/knockout mutant resource for high throughput functional genomics. Plant molecular biology 63: 351-364

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

http://scholar.google.com/scholar?as_q=A rice gene activation/knockout mutant resource for high throughput functional genomics&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 rice gene activation/knockout mutant resource for high throughput functional genomics&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Hsing&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Itoh H%2C Nonoue Y%2C Yano M%2C Izawa T %282010%29 A pair of floral regulators sets critical day length for Hd3a florigen expression in rice%2E Nature genetics 42%3A 635%2D638&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Itoh H, Nonoue Y, Yano M, Izawa T (2010) A pair of floral regulators sets critical day length for Hd3a florigen expression in rice. Nature genetics 42: 635-638

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

http://scholar.google.com/scholar?as_q=A pair of floral regulators sets critical day length for Hd3a florigen expression 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=A pair of floral regulators sets critical day length for Hd3a florigen expression in rice&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Itoh&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Jiang D%2C Gu X%2C He Y %282009%29 Establishment of the winter%2Dannual growth habit via FRIGIDA%2Dmediated histone methylation at FLOWERING LOCUS C in Arabidopsis%2E The plant cell 21%3A 1733%2D1746&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Jiang D, Gu X, He Y (2009) Establishment of the winter-annual growth habit via FRIGIDA-mediated histone methylation at FLOWERING LOCUS C in Arabidopsis. The plant cell 21: 1733-1746

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

http://scholar.google.com/scholar?as_q=Establishment of the winter-annual growth habit via FRIGIDA-mediated histone methylation at FLOWERING LOCUS C 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=Establishment of the winter-annual growth habit via FRIGIDA-mediated histone methylation at FLOWERING LOCUS C in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Jiang&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Jiang D%2C Kong NC%2C Gu X%2C Li Z%2C He Y %282011%29 Arabidopsis COMPASS%2Dlike complexes mediate histone H3 lysine%2D4 trimethylation to control floral transition and plant development%2E PLoS Genet 7%3A e1001330&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Jiang D, Kong NC, Gu X, Li Z, He Y (2011) Arabidopsis COMPASS-like complexes mediate histone H3 lysine-4 trimethylation to control floral transition and plant development. PLoS Genet 7: e1001330

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

http://scholar.google.com/scholar?as_q=Arabidopsis COMPASS-like complexes mediate histone H3 lysine-4 trimethylation to control floral transition and plant development.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Arabidopsis COMPASS-like complexes mediate histone H3 lysine-4 trimethylation to control floral transition and plant development.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Jiang&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Kim SL%2C Lee S%2C Kim HJ%2C Nam HG%2C An G %282007%29 OsMADS51 is a short%2Dday flowering promoter that functions upstream of Ehd1%2C OsMADS14%2C and Hd3a%2E Plant Physiology 145%3A 1484%2D1494&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kim SL, Lee S, Kim HJ, Nam HG, An G (2007) OsMADS51 is a short-day flowering promoter that functions upstream of Ehd1, OsMADS14, and Hd3a. Plant Physiology 145: 1484-1494

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=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kim&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Liu B%2C Wei G%2C Shi J%2C Jin J%2C Shen T%2C Ni T%2C Shen WH%2C Yu Y%2C Dong A %282015%29 SET DOMAIN GROUP 708%2C a histone H3 lysine 36�?�specific methyltransferase%2C controls flowering time in rice %28Oryza sativa%29%2E New Phytologist&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Liu B, Wei G, Shi J, Jin J, Shen T, Ni T, Shen WH, Yu Y, Dong A (2015) SET DOMAIN GROUP 708, a histone H3 lysine 36?specific methyltransferase, controls flowering time in rice (Oryza sativa). New Phytologist

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

http://scholar.google.com/scholar?as_q=SET DOMAIN GROUP 708, a histone H3 lysine 36â�?�specific methyltransferase, controls flowering time 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=SET DOMAIN GROUP 708, a histone H3 lysine 36â�?�specific methyltransferase, controls flowering time in rice (Oryza sativa).&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Liu&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Liu K%2C Yu Y%2C Dong A%2C Shen WH %282017%29 SET DOMAIN GROUP701 encodes a H3K4�?�methytransferase and regulates multiple key processes of rice plant development%2E New Phytologist&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Liu K, Yu Y, Dong A, Shen WH (2017) SET DOMAIN GROUP701 encodes a H3K4?methytransferase and regulates multiple key processes of rice plant development. New Phytologist

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

http://scholar.google.com/scholar?as_q=SET DOMAIN GROUP701 encodes a H3K4â�?�methytransferase and regulates multiple key processes of rice plant development.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=SET DOMAIN GROUP701 encodes a H3K4â�?�methytransferase and regulates multiple key processes of rice plant development.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Liu&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Lu C%2C Tian Y%2C Wang S%2C Su Y%2C Mao T%2C Huang T%2C Chen Q%2C Xu Z%2C Ding Y %282017%29 Phosphorylation of SPT5 by CDKD%3B 2 is required for VIP5 recruitment and normal flowering in Arabidopsis thaliana%2E The Plant Cell 29%3A 277%2D291&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Lu C, Tian Y, Wang S, Su Y, Mao T, Huang T, Chen Q, Xu Z, Ding Y (2017) Phosphorylation of SPT5 by CDKD; 2 is required for VIP5 recruitment and normal flowering in Arabidopsis thaliana. The Plant Cell 29: 277-291

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

http://scholar.google.com/scholar?as_q=Phosphorylation of SPT5 by CDKD; 2 is required for VIP5 recruitment and normal flowering in Arabidopsis thaliana&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Phosphorylation of SPT5 by CDKD; 2 is required for VIP5 recruitment and normal flowering in Arabidopsis thaliana&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Lu&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Matsubara K%2C Yamanouchi U%2C Nonoue Y%2C Sugimoto K%2C Wang ZX%2C Minobe Y%2C Yano M %282011%29 Ehd3%2C encoding a plant homeodomain finger�?�containing protein%2C is a critical promoter of rice flowering%2E The Plant Journal 66%3A 603%2D612&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Matsubara K, Yamanouchi U, Nonoue Y, Sugimoto K, Wang ZX, Minobe Y, Yano M (2011) Ehd3, encoding a plant homeodomain finger?containing protein, is a critical promoter of rice flowering. The Plant Journal 66: 603-612

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


http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Matsubara&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1



Milne TA, Briggs SD, Brock HW, Martin ME, Gibbs D, Allis CD, Hess JL (2002) MLL targets SET domain methyltransferase activity toHox gene promoters. Molecular cell 10: 1107-1117


Ng DW, Wang T, Chandrasekharan MB, Aramayo R, Kertbundit S, Hall TC (2007) Plant SET domain-containing proteins: structure,function and regulation. Biochimica et Biophysica Acta (BBA)-Gene Structure and Expression 1769: 316-329


Patel A, Dharmarajan V, Cosgrove MS (2008) Structure of WDR5 bound to mixed lineage leukemia protein-1 peptide. Journal ofBiological Chemistry 283: 32158-32161


Patel A, Vought VE, Dharmarajan V, Cosgrove MS (2008) A conserved arginine-containing motif crucial for the assembly and enzymaticactivity of the mixed lineage leukemia protein-1 core complex. Journal of Biological Chemistry 283: 32162-32175


Pien S, Fleury D, Mylne JS, Crevillen P, Inze D, Avramova Z, Dean C, Grossniklaus U (2008) ARABIDOPSIS TRITHORAX1 dynamicallyregulates FLOWERING LOCUS C activation via histone 3 lysine 4 trimethylation. The Plant Cell 20: 580-588


RYU CH, Lee S, CHO LH, Kim SL, LEE YS, Choi SC, Jeong HJ, Yi J, Park SJ, HAN CD (2009) OsMADS50 and OsMADS56 functionantagonistically in regulating long day (LD)‐dependent flowering in rice. Plant, cell & environment 32: 1412-1427


Santos-Rosa H, Schneider R, Bannister AJ, Sherriff J, Bernstein BE, Emre NT, Schreiber SL, Mellor J, Kouzarides T (2002) Activegenes are tri-methylated at K4 of histone H3. Nature 419: 407-411


Shilatifard A (2012) The COMPASS family of histone H3K4 methylases: mechanisms of regulation in development and diseasepathogenesis. Annual review of biochemistry 81: 65


Song J-J, Kingston RE (2008) WDR5 interacts with mixed lineage leukemia (MLL) protein via the histone H3-binding pocket. Journal ofBiological Chemistry 283: 35258-35264


Su Y, Wang S, Zhang F, Zheng H, Liu Y, Huang T, Ding Y (2017) Phosphorylation of Histone H2A at Serine 95: A Plant-specific MarkInvolved in Flowering Time Regulation and H2A. Z Deposition. The Plant Cell Online: tpc. 00266.02017


Sui P, Shi J, Gao X, Shen W-H, Dong A (2013) H3K36 methylation is involved in promoting rice flowering. Molecular plant 6Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Sun C, Fang J, Zhao T, Xu B, Zhang F, Liu L, Tang J, Zhang G, Deng X, Chen F (2012) The histone methyltransferase SDG724 mediatesH3K36me2/3 deposition at MADS50 and RFT1 and promotes flowering in rice. The Plant Cell 24: 3235-3247


Takahashi Y-h, Westfield GH, Oleskie AN, Trievel RC, Shilatifard A, Skiniotis G (2011) Structural analysis of the core COMPASS family www.plantphysiol.orgon April 9, 2020 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

http://www.ncbi.nlm.nih.gov/pubmed?term=Matsubara K%2C Yamanouchi U%2C Wang Z%2DX%2C Minobe Y%2C Izawa T%2C Yano M %282008%29 Ehd2%2C a rice ortholog of the maize INDETERMINATE1 gene%2C promotes flowering by up%2Dregulating Ehd1%2E Plant physiology 148%3A 1425%2D1435&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Matsubara K, Yamanouchi U, Wang Z-X, Minobe Y, Izawa T, Yano M (2008) Ehd2, a rice ortholog of the maize INDETERMINATE1 gene, promotes flowering by up-regulating Ehd1. Plant physiology 148: 1425-1435

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


http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Matsubara&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Milne TA%2C Briggs SD%2C Brock HW%2C Martin ME%2C Gibbs D%2C Allis CD%2C Hess JL %282002%29 MLL targets SET domain methyltransferase activity to Hox gene promoters%2E Molecular cell 10%3A 1107%2D1117&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Milne TA, Briggs SD, Brock HW, Martin ME, Gibbs D, Allis CD, Hess JL (2002) MLL targets SET domain methyltransferase activity to Hox gene promoters. Molecular cell 10: 1107-1117

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

http://scholar.google.com/scholar?as_q=MLL targets SET domain methyltransferase activity to Hox gene promoters&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=MLL targets SET domain methyltransferase activity to Hox gene promoters&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Milne&as_ylo=2002&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Ng DW%2C Wang T%2C Chandrasekharan MB%2C Aramayo R%2C Kertbundit S%2C Hall TC %282007%29 Plant SET domain%2Dcontaining proteins%3A structure%2C function and regulation%2E Biochimica et Biophysica Acta %28BBA%29%2DGene Structure and Expression 1769%3A 316%2D329&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Ng DW, Wang T, Chandrasekharan MB, Aramayo R, Kertbundit S, Hall TC (2007) Plant SET domain-containing proteins: structure, function and regulation. Biochimica et Biophysica Acta (BBA)-Gene Structure and Expression 1769: 316-329

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

http://scholar.google.com/scholar?as_q=Plant SET domain-containing proteins: structure, function and regulation&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=Plant SET domain-containing proteins: structure, function and regulation&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ng&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Patel A%2C Dharmarajan V%2C Cosgrove MS %282008%29 Structure of WDR5 bound to mixed lineage leukemia protein%2D1 peptide%2E Journal of Biological Chemistry 283%3A 32158%2D32161&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Patel A, Dharmarajan V, Cosgrove MS (2008) Structure of WDR5 bound to mixed lineage leukemia protein-1 peptide. Journal of Biological Chemistry 283: 32158-32161

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

http://scholar.google.com/scholar?as_q=Structure of WDR5 bound to mixed lineage leukemia protein-1 peptide&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=Structure of WDR5 bound to mixed lineage leukemia protein-1 peptide&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Patel&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Patel A%2C Vought VE%2C Dharmarajan V%2C Cosgrove MS %282008%29 A conserved arginine%2Dcontaining motif crucial for the assembly and enzymatic activity of the mixed lineage leukemia protein%2D1 core complex%2E Journal of Biological Chemistry 283%3A 32162%2D32175&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Patel A, Vought VE, Dharmarajan V, Cosgrove MS (2008) A conserved arginine-containing motif crucial for the assembly and enzymatic activity of the mixed lineage leukemia protein-1 core complex. Journal of Biological Chemistry 283: 32162-32175

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

http://scholar.google.com/scholar?as_q=A conserved arginine-containing motif crucial for the assembly and enzymatic activity of the mixed lineage leukemia protein-1 core complex&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 conserved arginine-containing motif crucial for the assembly and enzymatic activity of the mixed lineage leukemia protein-1 core complex&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Patel&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Pien S%2C Fleury D%2C Mylne JS%2C Crevillen P%2C Inze D%2C Avramova Z%2C Dean C%2C Grossniklaus U %282008%29 ARABIDOPSIS TRITHORAX1 dynamically regulates FLOWERING LOCUS C activation via histone 3 lysine 4 trimethylation%2E The Plant Cell 20%3A 580%2D588&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Pien S, Fleury D, Mylne JS, Crevillen P, Inze D, Avramova Z, Dean C, Grossniklaus U (2008) ARABIDOPSIS TRITHORAX1 dynamically regulates FLOWERING LOCUS C activation via histone 3 lysine 4 trimethylation. The Plant Cell 20: 580-588

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

http://scholar.google.com/scholar?as_q=ARABIDOPSIS TRITHORAX1 dynamically regulates FLOWERING LOCUS C activation via histone 3 lysine 4 trimethylation&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=ARABIDOPSIS TRITHORAX1 dynamically regulates FLOWERING LOCUS C activation via histone 3 lysine 4 trimethylation&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Pien&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=RYU CH%2C Lee S%2C CHO LH%2C Kim SL%2C LEE YS%2C Choi SC%2C Jeong HJ%2C Yi J%2C Park SJ%2C HAN CD %282009%29 OsMADS50 and OsMADS56 function antagonistically in regulating long day %28LD%29�?�dependent flowering in rice%2E Plant%2C cell %26 environment 32%3A 1412%2D1427&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=RYU CH, Lee S, CHO LH, Kim SL, LEE YS, Choi SC, Jeong HJ, Yi J, Park SJ, HAN CD (2009) OsMADS50 and OsMADS56 function antagonistically in regulating long day (LD)?dependent flowering in rice. Plant, cell & environment 32: 1412-1427

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

http://scholar.google.com/scholar?as_q=OsMADS50 and OsMADS56 function antagonistically in regulating long day (LD)â�?�dependent flowering 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=OsMADS50 and OsMADS56 function antagonistically in regulating long day (LD)â�?�dependent flowering in rice&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=RYU&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Santos%2DRosa H%2C Schneider R%2C Bannister AJ%2C Sherriff J%2C Bernstein BE%2C Emre NT%2C Schreiber SL%2C Mellor J%2C Kouzarides T %282002%29 Active genes are tri%2Dmethylated at K4 of histone H3%2E Nature 419%3A 407%2D411&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Santos-Rosa H, Schneider R, Bannister AJ, Sherriff J, Bernstein BE, Emre NT, Schreiber SL, Mellor J, Kouzarides T (2002) Active genes are tri-methylated at K4 of histone H3. Nature 419: 407-411

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

http://scholar.google.com/scholar?as_q=Active genes are tri-methylated at K4 of histone H3&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=Active genes are tri-methylated at K4 of histone H3&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Santos-Rosa&as_ylo=2002&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Shilatifard A %282012%29 The COMPASS family of histone H3K4 methylases%3A mechanisms of regulation in development and disease pathogenesis%2E Annual review of biochemistry 81%3A 65&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Shilatifard A (2012) The COMPASS family of histone H3K4 methylases: mechanisms of regulation in development and disease pathogenesis. Annual review of biochemistry 81: 65

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

http://scholar.google.com/scholar?as_q=The COMPASS family of histone H3K4 methylases: mechanisms of regulation in development and disease pathogenesis.&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 COMPASS family of histone H3K4 methylases: mechanisms of regulation in development and disease pathogenesis.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Shilatifard&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Song J%2DJ%2C Kingston RE %282008%29 WDR5 interacts with mixed lineage leukemia %28MLL%29 protein via the histone H3%2Dbinding pocket%2E Journal of Biological Chemistry 283%3A 35258%2D35264&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Song J-J, Kingston RE (2008) WDR5 interacts with mixed lineage leukemia (MLL) protein via the histone H3-binding pocket. Journal of Biological Chemistry 283: 35258-35264

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

http://scholar.google.com/scholar?as_q=WDR5 interacts with mixed lineage leukemia (MLL) protein via the histone H3-binding pocket&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=WDR5 interacts with mixed lineage leukemia (MLL) protein via the histone H3-binding pocket&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Song&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Su Y%2C Wang S%2C Zhang F%2C Zheng H%2C Liu Y%2C Huang T%2C Ding Y %282017%29 Phosphorylation of Histone H2A at Serine 95%3A A Plant%2Dspecific Mark Involved in Flowering Time Regulation and H2A%2E Z Deposition%2E The Plant Cell Online%3A tpc%2E 00266%2E02017&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Su Y, Wang S, Zhang F, Zheng H, Liu Y, Huang T, Ding Y (2017) Phosphorylation of Histone H2A at Serine 95: A Plant-specific Mark Involved in Flowering Time Regulation and H2A. Z Deposition. The Plant Cell Online: tpc. 00266.02017

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


http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Su&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Sui P%2C Shi J%2C Gao X%2C Shen W%2DH%2C Dong A %282013%29 H3K36 methylation is involved in promoting rice flowering%2E Molecular plant 6&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Sui P, Shi J, Gao X, Shen W-H, Dong A (2013) H3K36 methylation is involved in promoting rice flowering. Molecular plant 6

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

http://scholar.google.com/scholar?as_q=H3K36 methylation is involved in promoting rice flowering.&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=H3K36 methylation is involved in promoting rice flowering.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Sui&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Sun C%2C Fang J%2C Zhao T%2C Xu B%2C Zhang F%2C Liu L%2C Tang J%2C Zhang G%2C Deng X%2C Chen F %282012%29 The histone methyltransferase SDG724 mediates H3K36me2%2F3 deposition at MADS50 and RFT1 and promotes flowering in rice%2E The Plant Cell 24%3A 3235%2D3247&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Sun C, Fang J, Zhao T, Xu B, Zhang F, Liu L, Tang J, Zhang G, Deng X, Chen F (2012) The histone methyltransferase SDG724 mediates H3K36me2/3 deposition at MADS50 and RFT1 and promotes flowering in rice. The Plant Cell 24: 3235-3247

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

http://scholar.google.com/scholar?as_q=The histone methyltransferase SDG724 mediates H3K36me2/3 deposition at MADS50 and RFT1 and promotes flowering 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 histone methyltransferase SDG724 mediates H3K36me2/3 deposition at MADS50 and RFT1 and promotes flowering in rice&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Sun&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1


of histone H3K4 methylases from yeast to human. Proceedings of the National Academy of Sciences 108: 20526-20531Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Trievel RC, Shilatifard A (2009) WDR5, a complexed protein. Nature structural & molecular biology 16: 678-680Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Tsuji H, Taoka K-i, Shimamoto K (2011) Regulation of flowering in rice: two florigen genes, a complex gene network, and naturalvariation. Current opinion in plant biology 14: 45-52


Wysocka J, Swigut T, Milne TA, Dou Y, Zhang X, Burlingame AL, Roeder RG, Brivanlou AH, Allis CD (2005) WDR5 associates withhistone H3 methylated at K4 and is essential for H3 K4 methylation and vertebrate development. cell 121: 859-872


Xu R-F, Li H, Qin R-Y, Li J, Qiu C-H, Yang Y-C, Ma H, Li L, Wei P-C, Yang J-B (2015) Generation of inheritable and “transgene clean”targeted genome-modified rice in later generations using the CRISPR/Cas9 system. Scientific reports 5


Xue W, Xing Y, Weng X, Zhao Y, Tang W, Wang L, Zhou H, Yu S, Xu C, Li X (2008) Natural variation in Ghd7 is an important regulator ofheading date and yield potential in rice. Nature genetics 40: 761-767


Zheng H, Zhang F, Wang S, Su Y, Jiang P, Cheng R, Ji X, Hou S, Ding Y (2017) MLK1 and MLK2 coordinate RGA and CCA1 activity toregulate hypocotyl elongation in Arabidopsis thaliana. The Plant Cell: tpc. 00830.02017


Zong W, Zhong X, You J, Xiong L (2013) Genome-wide profiling of histone H3K4-tri-methylation and gene expression in rice underdrought stress. Plant molecular biology 81: 175-188



http://www.ncbi.nlm.nih.gov/pubmed?term=Takahashi Y%2Dh%2C Westfield GH%2C Oleskie AN%2C Trievel RC%2C Shilatifard A%2C Skiniotis G %282011%29 Structural analysis of the core COMPASS family of histone H3K4 methylases from yeast to human%2E Proceedings of the National Academy of Sciences 108%3A 20526%2D20531&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Takahashi Y-h, Westfield GH, Oleskie AN, Trievel RC, Shilatifard A, Skiniotis G (2011) Structural analysis of the core COMPASS family of histone H3K4 methylases from yeast to human. Proceedings of the National Academy of Sciences 108: 20526-20531

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

http://scholar.google.com/scholar?as_q=Structural analysis of the core COMPASS family of histone H3K4 methylases from yeast to human&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=Structural analysis of the core COMPASS family of histone H3K4 methylases from yeast to human&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Takahashi&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Trievel RC%2C Shilatifard A %282009%29 WDR5%2C a complexed protein%2E Nature structural %26 molecular biology 16%3A 678%2D680&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Trievel RC, Shilatifard A (2009) WDR5, a complexed protein. Nature structural & molecular biology 16: 678-680

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


http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Trievel&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Tsuji H%2C Taoka K%2Di%2C Shimamoto K %282011%29 Regulation of flowering in rice%3A two florigen genes%2C a complex gene network%2C and natural variation%2E Current opinion in plant biology 14%3A 45%2D52&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Tsuji H, Taoka K-i, Shimamoto K (2011) Regulation of flowering in rice: two florigen genes, a complex gene network, and natural variation. Current opinion in plant biology 14: 45-52

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

http://scholar.google.com/scholar?as_q=Regulation of flowering in rice: two florigen genes, a complex gene network, and natural variation&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=Regulation of flowering in rice: two florigen genes, a complex gene network, and natural variation&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Tsuji&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Wysocka J%2C Swigut T%2C Milne TA%2C Dou Y%2C Zhang X%2C Burlingame AL%2C Roeder RG%2C Brivanlou AH%2C Allis CD %282005%29 WDR5 associates with histone H3 methylated at K4 and is essential for H3 K4 methylation and vertebrate development%2E cell 121%3A 859%2D872&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Wysocka J, Swigut T, Milne TA, Dou Y, Zhang X, Burlingame AL, Roeder RG, Brivanlou AH, Allis CD (2005) WDR5 associates with histone H3 methylated at K4 and is essential for H3 K4 methylation and vertebrate development. cell 121: 859-872

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

http://scholar.google.com/scholar?as_q=WDR5 associates with histone H3 methylated at K4 and is essential for H3 K4 methylation and vertebrate development&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=WDR5 associates with histone H3 methylated at K4 and is essential for H3 K4 methylation and vertebrate development&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wysocka&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Xu R%2DF%2C Li H%2C Qin R%2DY%2C Li J%2C Qiu C%2DH%2C Yang Y%2DC%2C Ma H%2C Li L%2C Wei P%2DC%2C Yang J%2DB %282015%29 Generation of inheritable and �??transgene clean�?� targeted genome%2Dmodified rice in later generations using the CRISPR%2FCas9 system%2E Scientific reports 5&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Xu R-F, Li H, Qin R-Y, Li J, Qiu C-H, Yang Y-C, Ma H, Li L, Wei P-C, Yang J-B (2015) Generation of inheritable and ?transgene clean? targeted genome-modified rice in later generations using the CRISPR/Cas9 system. Scientific reports 5

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

http://scholar.google.com/scholar?as_q=Generation of inheritable and â�?�?transgene cleanâ�?� targeted genome-modified rice in later generations using the CRISPR/Cas9 system.&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=Generation of inheritable and â�?�?transgene cleanâ�?� targeted genome-modified rice in later generations using the CRISPR/Cas9 system.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Xu&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Xue W%2C Xing Y%2C Weng X%2C Zhao Y%2C Tang W%2C Wang L%2C Zhou H%2C Yu S%2C Xu C%2C Li X %282008%29 Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice%2E Nature genetics 40%3A 761%2D767&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Xue W, Xing Y, Weng X, Zhao Y, Tang W, Wang L, Zhou H, Yu S, Xu C, Li X (2008) Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nature genetics 40: 761-767

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

http://scholar.google.com/scholar?as_q=Natural variation in Ghd7 is an important regulator of heading date and yield potential 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=Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Xue&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zheng H%2C Zhang F%2C Wang S%2C Su Y%2C Jiang P%2C Cheng R%2C Ji X%2C Hou S%2C Ding Y %282017%29 MLK1 and MLK2 coordinate RGA and CCA1 activity to regulate hypocotyl elongation in Arabidopsis thaliana%2E The Plant Cell%3A tpc%2E 00830%2E02017&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zheng H, Zhang F, Wang S, Su Y, Jiang P, Cheng R, Ji X, Hou S, Ding Y (2017) MLK1 and MLK2 coordinate RGA and CCA1 activity to regulate hypocotyl elongation in Arabidopsis thaliana. The Plant Cell: tpc. 00830.02017

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

http://scholar.google.com/scholar?as_q=MLK1 and MLK2 coordinate RGA and CCA1 activity to regulate hypocotyl elongation in Arabidopsis thaliana.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=MLK1 and MLK2 coordinate RGA and CCA1 activity to regulate hypocotyl elongation in Arabidopsis thaliana.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zheng&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zong W%2C Zhong X%2C You J%2C Xiong L %282013%29 Genome%2Dwide profiling of histone H3K4%2Dtri%2Dmethylation and gene expression in rice under drought stress%2E Plant molecular biology 81%3A 175%2D188&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zong W, Zhong X, You J, Xiong L (2013) Genome-wide profiling of histone H3K4-tri-methylation and gene expression in rice under drought stress. Plant molecular biology 81: 175-188

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

http://scholar.google.com/scholar?as_q=Genome-wide profiling of histone H3K4-tri-methylation and gene expression in rice under drought 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=Genome-wide profiling of histone H3K4-tri-methylation and gene expression in rice under drought stress&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zong&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1


a,b b c a,1 - plant physiology · 137 in rice, over 50% of genes show h3k4 methylation (zong et...

Documents