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Temporal-Specific Interaction of NF-YC and CURLY LEAF during 1

the Floral Transition Regulates Flowering 2

Xu Liua,3, Yuhua Yanga,b,3, Yilong Hua,b, Limeng Zhoua,b, Yuge Lia, and Xingliang 3

Houa,2 4

a Key Laboratory of South China Agricultural Plant Molecular Analysis and Genetic 5

Improvement & Guangdong Provincial Key Laboratory of Applied Botany, South 6

China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, China 7

b University of the Chinese Academy of Sciences, Beijing 100049, China 8

ORCID IDs: 0000-0003-1970-0608 (X.L.); 0000-0002-3964-2372 (X.H.) 9

1 This work was supported by grants from the National Natural Science Foundation 10

of China (No. 31301055), the Guangdong Science and Technology Department of 11

China (No. 2015B020231009), and Natural Science Foundation of Guangdong 12

Province (No. 2017A030313211). 13

2 Address correspondence to Xingliang Hou ([email protected]) 14

3 These authors contributed equally to this article 15

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

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

Authors (www.plantphysiol.org) is: Xingliang Hou ([email protected]) 18

Author Contributions: X.L. and X.H. designed the research. X.L., Y.Y., Y.H., L.Z., 19

and Y. L. performed the research. X.L. Y.Y., and X.H. analyzed the data. X.L. and 20

X.H. wrote the paper 21

Short title: NF-YC and CLF interact to regulate flowering 22

One-sentence summary: NF-YC proteins interact with the histone methyltransferase 23

Plant Physiology Preview. Published on March 29, 2018, as DOI:10.1104/pp.18.00296

Copyright 2018 by the American Society of Plant Biologists

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CLF and prevent the tri-methylation of H3K27 on chromatin at the FT locus, thereby 24

allowing FT expression and the initiation of flowering.25



3

ABSTRACT 26

The flowering time of higher plants is controlled by environmental cues and intrinsic 27

signals. In Arabidopsis thaliana, flowering is accelerated by exposure to long-day 28

(LD) conditions via the key photoperiod-induced factor FLOWERING LOCUS T 29

(FT). Nuclear Factor-Y C (NF-YC) proteins function as important mediators of 30

epigenetic marks in different plant developmental stages and play an important role in 31

the regulation of FT transcription, but the mechanistic details of this remain unknown. 32

In this study, we show that Arabidopsis NF-YC homologues temporally interact with 33

the histone methyltransferase CURLY LEAF (CLF) during the flowering transition. 34

The binding of NF-YC antagonizes the association of CLF with chromatin and 35

CLF-dependent deposition of H3K27me3, thus relieving repression of FT 36

transcription and facilitating flowering under LD conditions. Our findings reveal a 37

novel mechanism of NF-YC/CLF-mediated epigenetic regulation of FT activation in 38

photoperiod-induced flowering, and consequently contribute to our understanding of 39

how plants control developmental events in a temporal-specific regulatory manner. 40

41



4

INTRODUCTION 42

Flowering is precisely regulated by environmental and endogenous signals (Andres 43

and Coupland, 2012). In Arabidopsis, a facultative long-day (LD) plant, flowering 44

signals are perceived and transmitted by different molecular pathways, including 45

photoperiod, vernalization, thermosensory, aging, autonomous, and gibberellins 46

pathways, which mostly converge to regulate the key flowering integrator gene 47

FLOWERING LOCUS T (FT). FT, the long-sought florigen, functions as a 48

long-distance signal to the shoot apical meristem where it diurnally binds to FD for 49

transcriptional activation of floral meristem identity genes (Kardailsky et al., 1999; 50

Kobayashi et al., 1999; Abe et al., 2005; Wigge et al. 2005; Corbesier et al., 2007). In 51

LD conditions, the main photoperiod-responsive regulator CONSTANS (CO) 52

promotes flowering by directly activating the FT and another floral integrator gene 53

SUPPRESSOR OF OVEREXPRESSION OF CO 1 (SOC1) (Putterill et al., 1995; Lee 54

et al., 2000; Samach et al., 2000; Yoo et al., 2005). In addition, FT could also be 55

regulated by important regulators involved in other flowering pathways, such as 56

FLOWERING LOCUS C (FLC), FLOWERING LOCUS M variants (FLMs), and 57

PHYTOCHROME INTERACTING FACTOR 4 etc., to modulate flowering time 58

(Michaels and Amasino, 1999; Pose et al., 2013; Kumar et al., 2012). So far, recent 59

findings have suggested that FT exerts a central function in the flowering transition. 60

Flowering is genetically controlled by various epigenetic factors that activate or 61

repress transcription of flowering genes (He, 2012). In Arabidopsis, the Polycomb 62

Repressive Complex 2 (PRC2) specifically mediates the histone H3 Lysine 27 63

trimethylation (H3K27me3) that plays extensive regulatory roles in various 64

developmental stages including flowering (Holec and Berger, 2012). CURLY LEAF 65

(CLF) is a conserved component in PRC2, and loss-of-function of CLF causes early 66

flowering phenotype with curled leaves (Goodrich et al., 1997). Previous extensive 67

evidence supported that the FT upregulation is fundamentally required for the early 68

flowering of clf, and CLF retains FT repression through promoting the H3K27me3 69

deposition in FT chromatin (Jiang et al., 2008; Adrian et al., 2010). 70

Nuclear Factor-Y Subunit C (NF-YC), also termed Histone-Associated Protein 5 71



5

(HAP5) or CCAAT Binding Factor C (CBF-C), interacts with NF-YB (HAP3/CBF-A) 72

to form a heterodimer analogous to the core histone 2A/2B dimer with the highly 73

conserved Histone Fold (HF) domain. The NF-YC/YB dimer in turn unites with 74

NF-YA (HAP2/CBF-B) for constituting the NF-Y heterotrimer that canonically binds 75

to CCAAT-box in eukaryotic promoter (Huber et al., 2012; Nardini et al., 2013). In 76

plants, NF-YC subunits are encoded by a multi-gene family and function as important 77

participants in flowering-time control (Petroni et al., 2012; Zhao et al., 2017; Swain et 78

al., 2017). Arabidopsis NF-YC homologues have redundant roles in FT activation of 79

photoperiod-dependent flowering by contributing to forming the canonical 80

NF-YC-YB-YA and specific NF-YC-YB-CO complexes, which recognize the distal 81

CCAAT-box enhancers and the proximal CO-responsive elements (CORE), 82

respectively, within the FT promoter region (Kumimoto et al., 2010; Cao et al., 2014; 83

Gnesutta et al., 2017). Recent studies have demonstrated that NF-Y factors recruit 84

different histone modifiers to regulate various developments in plants (Hou et al., 85

2014; Tang et al., 2017). However, how NF-Y mediates the epigenetic regulation of 86

FT transcription remains unknown. 87

In this study, we demonstrate a CLF-dependent epigenetic mechanism in the 88

NF-YC-mediated FT transcription regulation in Arabidopsis. NF-YC homologues 89

counteract the H3K27me3 deposition in FT chromatin by temporally interacting with 90

CLF to attenuate the association of CLF with the FT locus, thus derepressing FT 91

transcription under LD conditions. Collectively, our findings support that NF-YC 92

proteins function as important modulators of epigenetic marks controlling flowering, 93

promoting the understanding on how plants precisely control developmental events in 94

a temporal-specific regulatory manner. 95

96



6

RESULTS 97

NF-YC interacts with CLF 98

To further investigate the molecular roles of NF-YC proteins, we performed a yeast 99

two-hybrid screening to identify the potential NF-YC-interacting epigenetic partners. 100

Interestingly, CLF, the conserved histone methyltransferase of PRC2, was found to 101

interact strongly with NF-YC3 and NF-YC9, and weakly with NF-YC4, in yeast (Fig. 102

1A). Then, the glutathione S-transferase (GST) pull-down assay showed that the 103

recombinant proteins of His-NF-YC3, His-NF-YC4, and His-NF-YC9 were 104

co-precipitated by GST-CLF fusion proteins but not by GST control, respectively (Fig. 105

1B), indicating the physical interaction between CLF and NF-YC proteins in vitro. 106

Since NF-YC9 could genetically replace the function of the other two homologues 107

(Liu et al., 2016; Tang et al., 2017), we chose NF-YC9 as the representative NF-YC 108

gene for further investigation. 109

According to the conserved regulatory domains in NF-YC and CLF (Holec and 110

Berger, 2012; Liu et al., 2016), we designed various truncated versions of NF-YC9 111

and CLF to identify the necessary domains required for the proteins interaction. This 112

result indicates that the highly conserved CXC-SET domain of CLF and 113

carboxy-terminal of NF-YC9 contribute to the protein interaction (Fig. 1C). 114

Bimolecular fluorescence complementation (BiFC) analysis was conducted in tobacco 115

(Nicotiana tabacum) leaf epidermal cells to examine the interaction between NF-YC9 116

and CLF in vivo. The fluorescence by NF-YC9-nEYFP together with cEYFP-CLF 117

was localized in the cell nuclei (Fig. 1D). Co-immunoprecipitation (Co-IP) analysis 118

using the nuclear extracts of 9-day-old seedlings (clf-28 nf-yc9-1 35S:GFP-CLF 119

pNF-YC9:NF-YC9-FLAG) further confirmed the binding of NF-YC9 to CLF in 120

Arabidopsis (Fig. 1E). Taken together, these data support the direct interaction 121

between NF-YC and CLF proteins in plants. 122

CLF is epistatic to NF-YC 123

As both CLF and NF-YC are involved in flowering control (Goodrich et al., 1997; 124

Kumimoto et al., 2010; Hou et al., 2014), but with little mutual regulation regarding 125



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transcriptional levels (Supplemental Fig. S1), the interaction between CLF and 126

NF-YC proteins let us to investigate whether these two proteins functionally associate 127

to regulate flowering. We examined the genetic connection between NF-Y and CLF by 128

introducing the nf-yc3-2 nf-yc4-1 nf-yc9-1 (nf-ycT) mutations into the clf-28 (clf) 129

mutant background. Under LD conditions, the clf nf-ycT mutants exhibited similar 130

early flowering and upward-curled leaves to clf mutants, whereas nf-ycT showed 131

extreme late flowering as reported previously (Fig. 2A and 2B; Kumimoto et al., 132

2010). Meanwhile, CLF mutation also rescued the late flowering phenotype in 133

loss-of-function mutants of NF-YBs (nf-yb2-1 nf-yb3-1), another subunit of NF-Y 134

involved in flowering control (Supplemental Fig. S2). These observations indicate the 135

genetic function of CLF in flowering control is epistatic to NF-YC/B genes. To further 136

test this, we examined the temporal expression of several flowering genes in various 137

genetic backgrounds. Both FT and SOC1 were significantly upregulated in Col wild 138



8

type during the floral transition under LD conditions. Remarkably, the daily 139

expression of FT was downregulated in nf-ycT but highly upregulated in clf and clf 140

nf-ycT compared with that in the wild type (Fig. 2C; Supplemental Fig. S3), 141

supporting the epistatic role of CLF to NF-YC in FT expression. By contrast, SOC1 142

transcripts were decreased by nf-ycT in either the clf or CLF background, indicating 143

that CLF does not mediate NF-YC-regulated SOC1 expression (Fig. 2C). In addition, 144

CONSTANS (CO), encoding the main regulator of FT transcription, was hardly 145

regulated by NF-YC and CLF (Fig. 2C). FLC, SEP3, and AG genes are known as the 146

direct downstream targets of CLF and are repressed by CLF in flowering (Schubert et 147

al., 2006; Lopez-Vernaza et al., 2012). Our analysis showed that, compared with that 148

in wild type, expression of these genes was remarkably increased in clf and clf nf-ycT 149

but slightly changed (FLC) or not affected (SEP3 and AG) in the nf-ycT background 150

(Supplemental Fig. S4), indicating that it is unlikely NF-YC acts as the main regulator 151

of the CLF targets FLC, SEP3, and AG. Therefore, these results suggest that CLF and 152

NF-YC mediate flowering time primarily by regulating FT. 153

NF-YC mediates CLF-dependent H3K27me3 deposition 154



9

CLF functions in tri-methylation of H3K27 at chromatin of flowering genes 155

(Goodrich et al., 1997; Schubert et al., 2006; Jiang et al., 2008). To learn whether 156

NF-YC affects epigenetic function of CLF, we examined the H3K27me3 levels at 157

several selected FT loci in Col, nf-ycT, clf, and clf nf-ycT plants by chromatin 158

immunoprecipitation (ChIP) assays (Fig. 3A). Notably, H3K27me3 marks in the FT 159

locus were increased in nf-ycT, whereas loss of CLF significantly reduced the levels 160

of H3K27me3 in both the nf-ycT and wild-type background (Fig. 3B). Furthermore, 161

we examined the deposition of H3K27me3 at the selected FLC, AG, and SOC1 loci. 162

Consistent with the expression analysis, H3K27me3 levels in FLC and AG were 163

attenuated in clf and clf nf-ycT (Fig. 2C and 3B). By contrast, loss of NF-YC had only 164

a slight effect or no effect on H3K27me3 deposition in FLC and AG, respectively, but 165

enhanced that in SOC1 (Fig. 3B). These results indicate that NF-YC may repress 166

CLF-dependent H3K27me3 deposition to specifically regulate FT transcription. 167

Loss of NF-YC function elevates CLF enrichment and H3K27me3 deposition on 168

FT chromatin 169

We created nf-ycT clf GFP-CLF by introducing the nf-ycT mutations into clf 170

35S:GFP-CLF plants. Under LD conditions, GFP-CLF could rescue the early 171

flowering phenotype of clf, and nf-ycT clf GFP-CLF exhibited a late flowering 172

phenotype similar to that in nf-ycT (Fig. 4A), suggesting that CLF activity is required 173

for late flowering caused by NF-YC loss of function. We next conducted ChIP assays 174

to examine the association of GFP-CLF with target chromatin in clf GFP-CLF and 175

nf-ycT clf GFP-CLF plants. NF-YC loss of function significantly promoted the 176

binding of GFP-CLF to FT, which was concomitant with higher H3K27me3 levels of 177

FT chromatin and lower FT expression in nf-ycT clf GFP-CLF compared with that in 178

clf GFP-CLF plants (Fig. 4B, 4C and 4D). By contrast, no difference was observed 179

regarding GFP-CLF binding to SOC1 between clf GFP-CLF and nf-ycT clf GFP-CLF 180

plants (Fig. 4C and 4D). These results confirm the repressive role of NF-YC on CLF 181

binding to FT chromatin. 182

Temporal-specific interaction of NF-YC and CLF regulates CLF-dependent 183



10

H3K27me3 deposition in FT chromatin 184

Generally, plants do not immediately enter the flowering transition without 185

undergoing a period of vegetative development. We hence wondered how NF-YC 186

represses CLF function via protein-protein interaction to facilitate flowering at right 187

time. To address this, the temporal pattern of NF-YC-CLF interaction was 188

investigated by a time-course ChIP analysis using developing clf GFP-CLF and 189

nf-ycT clf GFP-CLF seedlings grown under LD conditions. As plant growth 190

progressed, both CLF binding and H3K27me3 deposition in FT gradually decreased 191

during flowering transition stage (9–11 days after germination) (Fig. 5A; 192

Supplemental Fig. S5). It is worth noting that NF-YC loss of function significantly 193

attenuated this declined pattern (Fig. 5A). Furthermore, ChIP assay with a transient 194

expression system showed that the binding of CLF to FT region was dramatically 195

decreased by the full-length NF-YC9 but not by the carboxyl-terminal deleted 196

NF-YC9 which fails to interact with CLF (Fig. 1C; Supplemental Fig. S6A and S6B). 197

These observations support that CLF function may be impaired by enhanced 198

interaction of CLF and NF-YC during flowering transition stage. One possibility is 199

that the varied interaction pattern could be triggered by increasing abundance of 200

NF-YC proteins during plant growth. However, we did not observe obvious increased 201

NF-YC accumulation during the flowering transition stage by immunoblot analysis of 202

clf nf-yc9 GFP-CLF NF-YC9-FLAG seedlings (Fig. 5B). In contrast to the declined 203



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CLF binding and H3K27me3 levels (Fig. 5A), time-course Co-IP analysis showed an 204

increasing interaction between CLF and NF-YC9 during flowering transition (Fig. 205

5B), suggesting other unknown factors determined by flowering signals might be 206

involved in the temporal regulation of NF-YC-CLF interaction. 207

208



12

DISCUSSION 209

In yeast and mammals, NF-Y factors are deemed to make a functional link between 210

chromatin and transcription (Dolfini et al., 2012). Our recent studies have revealed 211

that NF-YC regulates plant developmental stages via mediating epigenetic 212

modifications on target genes (Hou et al., 2014; Tang et al., 2017), implying an 213

important function of NF-YC proteins in epigenetic regulation in plants. In the 214

photoperiod flowering pathway, NF-Y factors are crucial for the chromatin activation 215

of FT, which is simultaneously controlled by various epigenetic regulations (Gu et al., 216

2013; Cao et al., 2014; Bu et al., 2014). However, whether and how NF-YC mediates 217

the epigenetic regulation of FT transcription remains unknown. Here, we reveal a 218

temporal interaction of NF-YC with the histone methyltransferase CLF that 219

specifically counteracts CLF-dependent H3K27me3 deposition to derepress FT 220

transcription, thus promoting flowering under LD conditions. These results illustrate a 221

novel epigenetic regulatory model in the photoperiod flowering pathway and 222

expand our understanding on how plants precisely control developmental events in a 223

temporal-specific manner. 224

In eukaryotes, the PRC2 members are structurally and evolutionarily conserved, in 225

which CLF orthologs function as the core component to catalyze H3K27 methylation. 226

The conserved CXC and SET domains of CLF are necessary for H3K27 227



13

methyltransferase activity and sequence-specific binding (Cao et al., 2002; Müller et 228

al., 2002; Ketel et al., 2005). For example, the gain-of-function allele clf-59, 229

harboring a Pro-to-Ser amino acid mutation in the CXC domain, results in 230

vernalization-independent early flowering in Arabidopsis (Doyle and Amasino, 2009). 231

Like CLF, NF-YC, with an HF domain close to the core histone 2A, is widely 232

conserved in eukaryotic species, and functions as a subunit of NF-Y heterotrimers 233

(Dolfini et al., 2012). In this study, the highly conserved CXC and SET domains of 234

CLF and carboxy-terminal of NF-YC9 contribute to their protein interaction (Fig. 1C), 235

implying that the combination of CLF and NF-YC may frequently present and 236

function in different eukaryotic species, or play distinct roles in various biological 237

processes. Upon our observations, the binding of NF-YC to the CXC-SET domain of 238

CLF impairs DNA affinity of CLF, and thus, restricting CLF function to target 239

chromatins. However, we cannot exclude the possibility that NF-YC might act as a 240

potential catalyzed substrate of CLF to mediate unknown regulations. 241

FT functions as a major output of the photoperiod pathway regulator CO when 242

plants respond to LD conditions (Andres and Coupland, 2012). Recent studies have 243

demonstrated that NF-Y factors are involved in the CO-FT regulatory cascade via 244

direct interaction with CO (Kumimoto et al., 2010; Gnesutta et al., 2017). The 245

identification of NF-Y-mediated chromatin looping at the FT locus and novel 246

sequence-specific NF-YB/YC/CO complex further support that CO regulating FT is 247

primarily dependent on NF-Y(C) functions (Cao et al., 2014; Gnesutta et al., 2017). It 248

was shown that CLF indirectly controls FT expression by epigenetically regulating 249

FLC in different aspects such as the autonomous pathway (Doyle and Amasino, 2009; 250

Lopez-Vernaza et al., 2012; Müller-Xing et al., 2014). However, CLF could directly 251

bind to FT chromatin and mediate H3K27me3 deposition in FT under LD conditions 252

(Fig. 5A; Jiang et al., 2008; Adrian et al., 2010). Similar to clf nf-ycT, clf co double 253

mutants also presented a clf-like early flowering phenotype (Pazhouhandeh et al., 254

2010). Considering the biological interaction between NF-YC and CLF presented in 255

this study, it is quite possible that CO-NF-Y module regulates FT transcription by 256

preventing CLF-dependent H3K27me3 deposition in FT chromatin. Consistently, clf 257



14

could rescue the late flowering phenotype caused by loss of NF-YB2/3 function 258

(Supplemental Fig. S2); however, the question whether NF-YC represses CLF 259

together with NF-YA/B and CO to facilitate flowering requires further investigation. 260

Besides FT, SOC1 acts as another important integrator in flowering control (Lee 261

et al., 2000; Samach et al., 2000). Our previous study showed that SOC1 is directly 262

regulated by CO-NF-Y via the recruitment of a H3K27 demethylase RELATIVE OF 263

EARLY FLOWERING 6 (REF6) under LD conditions (Hou et al., 2014). Although 264

H3K27me3 levels in SOC1 decreases during flowering transition, we did not observe 265

that CLF affects SOC1 gene expression in this study (Fig. 2C), suggesting NF-YC 266

mediates H3K27me3 deposition in SOC1 chromatin primarily by recruiting REF6 267

rather than impairing CLF activity. In addition, we detected gene expression and 268

H3K27me3 levels of FLC, SEP3, and AG genes, which are known as CLF targets 269

(Goodrich et al., 1997; Schubert et al., 2006; Lopez-Vernaza et al., 2012). The results 270

showed that these genes were hardly regulated by NF-YC, implying other factors but 271

not NF-YC might be involved in their regulations by CLF. Furthermore, since the 272

dynamics of H3K27me3 mark regulated by CLF at many genomic loci may only be 273

detected in specific tissues and at specific developmental stages (Liu et al., 2016), it is 274

possible that the NF-YC-CLF module could also contribute to the precise control of 275

other developmental events. 276

In addition to H3K27me3, other histone modifications such as H3K4me3 and 277

histone acetylation are also involved in the regulation of flowering (He et al., 2003; 278

Engelhorn et al., 2017). Generally, repressive H3K27me3 and activation-related 279

H3K4me3 oppositely regulate spatial and temporal expression of genes during 280

specific developmental processes. A recent genome-wide study revealed that the 281

H3K4me3 deposition prevails over H3K27me3 whereas H3K27me3 reduction occurs 282

later during early flower morphogenesis (Engelhorn et al., 2017). Since NF-YC 283

functions with CO to promote FT transcription, whereas CO activates FT by 284

recruiting MRG1/2 proteins, the H3K4me3/H3K36me3 readers (Kumimoto et al., 285

2010; Bu et al., 2014), it could be speculated that H3K4me3 modification might be 286

involved in NF-YC-mediated flowering control. It was reported that several histone 287



15

deacetylases (HDAs) regulate flowering by transcriptional repression of flowering 288

repressor genes such as FLC, MAF1, MAF4, and MAF5 (Wang et al., 2014). Although 289

our previous work revealed that NF-YC regulates photomorphogenesis by 290

HDA15-mediated histone acetylation (Tang et al., 2017), no evidence supports that 291

NF-YC-HDA15 is involved in flowering regulation. However, it is worthwhile 292

investigating whether NF-YC regulates flowering via recruiting other HDAs related to 293

flowering response such as HDA6/9/19 (Wang et al., 2014). 294

It is intriguing that a temporal-specific interaction of NF-YC and CLF was 295

observed by time-course Co-IP assays (Fig. 5B). The increasing interaction during 296

flowering transition under LD conditions results in attenuated CLF binding and 297

H3K27me3 deposition in FT chromatin, which convincingly explains the 298

photoperiod-induced FT upregulation. In the photoperiod pathway, the periodic 299

change of CO protein abundance by light is well-known to underlie the rhythmical 300

expression of FT within a day. However, this does not fully explain FT transcripts 301

increasing day by day under LD conditions, which was previously attributed to FT 302

accumulation or other positive feedback regulations (Suarez-Lopez et al., 2001). Here, 303

the temporal-specific NF-YC-CLF module provides a plausible hypothesis for 304

increasing FT transcript abundance. In this scenario, FT may be induced by a 305

NF-YC-triggered decrease of H3K27me3 when seedlings are ready for flowering. 306

Because we did not observe a significant increase of NF-YC protein level during 307

flowering transition, it raises the question of how appropriate timing of NF-YC 308

interaction with CLF is regulated. We propose that other mediating factors or 309

post-translational modifications, which are induced by the flowering signals, may be 310

included in this process. Previous work reported a functional interaction between the 311

cullin-RING ubiquitin ligase (CUL4–DDB1) and the PRC2 complex (Pazhouhandeh 312

et al., 2010). CO is known to interact with NF-YC, and turnover of the CO proteins 313

are triggered by COP1-SPAs complexes, a central repressor of light signaling, in the 314

dark (Jang et al., 2008; Chen et al., 2010). In addition, it was reported that the 315

CUL4-DDB1 complex is required for FT expression and associates with the 316

COP1-SPA complex (Pazhouhandeh et al., 2010). The interaction of NF-YC-CLF 317



16

may be mediated by CUL4-DDB1, COP1-SPA, or CO in a light-dependent manner, 318

which is worthwhile of future investigation. 319

Taken together, we reveal the temporal-specific regulatory module NF-YC-CLF, 320

through which NF-YC directly counteracts CLF activity to promote FT expression 321

and flowering at an appropriate time. These findings provide novel insight into the 322

molecular mechanisms of how plants precisely control specific development events 323

by temporal regulation of epigenetic factors.324



17

MATERIALS AND METHODS 325

Plant Material and Growth Conditions 326

The plant materials nf-yc3-2 nf-yc4-1 nf-yc9-1 (nf-ycT) and nf-yc9 NF-YC9-FLAG 327

were described previously (Hou et al., 2014; Liu et al., 2016). clf-28 (SALK_139371) 328

seeds were obtained from the Arabidopsis Biological Resource Centre (ABRC). clf 329

GFP-CLF plants were generated by crossing 35S:GFP-CLF (Schubert et al., 2006) 330

with clf-28 in Col background. The nf-ycT clf GFP-CLF and clf nf-yc9 GFP-CLF 331

NF-YC9-FLAG plants were generated by crossing clf GFP-CLF with nf-ycT and 332

nf-yc9 NF-YC9-FLAG plants. Plant growth conditions were described previously 333

(Hou et al., 2014), the flowering transition time of Arabidopsis Col wild type grown 334

under which has been defined to occur during 7–11 days after germination (Liu et al., 335

2008). The average number of rosette leaves calculated from a minimum of 10 plants 336

at bolting was used as an indicator of flowering time. 337

Yeast Two-Hybrid Assay 338

The coding regions of NF-YC3, NF-YC4, NF-YC9, CLF, and truncated versions of 339

NF-YC9 and CLF were amplified and cloned into pGBKT7 (BD) and pGADT7 (AD) 340

vectors (Clontech), respectively. The primers used are listed in Supplementary Table 341

S1. Yeast two-hybrid assays were performed using the Yeastmaker Yeast 342

Transformation System 2 (Clontech). Yeast AH109 cells were co-transformed with the 343

selected BD and AD constructs. The yeast transformants were grown and selected on 344

SD/-Trp/-Leu or SD/-Trp/-Leu/-His/-Ade mediums. 345

BiFC Analysis 346

The coding regions of NF-YC9 and CLF were cloned into the pGreen binary vectors 347

containing C- or N-terminal fusions of enhanced yellow fluorescence protein (EYFP) 348

to generate 35S:NF-YC9-nEYFP and 35S:cEYFP-CLF constructs. Plasmids were 349

co-transformed into tobacco (Nicotiana tabacum) leaf epidermal cell with 350

Agrobacterium tumefaciens strains (GV3101-psoup) as described previously (Tang et 351

al., 2017). The YFP signals were detected by the inverted fluorescence microscope 352

(Leica) in tobacco leaf grown for 48 h after infiltration, while DAPI 353



18

(4′,6-diamidino-2-phenylindole) staining was used as the nuclear localization 354

indicator. 355

Pull-Down Assay 356

Using the designed primers (Supplementary Table S1), the coding regions of NF-YC3, 357

NF-YC4, NF-YC9, and CLF were amplified and cloned into the pQE30 (QIAGEN) 358

and pGEX-4T-1 (Pharmacia) vectors to produce His-NF-YC3, His-NF-YC4, 359

His-NF-YC9, and GST-CLF constructs, respectively. These GST and His recombinant 360

constructs and the empty pGEX-4T-1 plasmid were transformed into E. coli Rosetta 361

cells and then recombinant protein expression was induced by 362

isopropyl-β-d-thiogalactoside (IPTG, Sigma). The purified His-NF-YC3, 363

His-NF-YC4, and His-NF-YC9 proteins were incubated with immobilized GST or 364

GST-CLF using Glutathione Sepharose beads (Amersham Biosciences) and analyzed 365

using immunoblots as described previously (Liu et al., 2016). 366

Co-Immunoprecipitation Assay 367

The clf nf-yc9 GFP-CLF NF-YC9-FLAG seedlings grown in LD conditions were 368

harvested at the indicated growth stages and ground in liquid nitrogen. Nuclear 369

proteins were extracted as previously described (Hou et al., 2014) and then incubated 370

with Protein G PLUS/Protein A-Agarose Suspension (IP10, CALBIOCHEN) plus 371

anti-GFP antibody (ab290, Abcam) or preimmune serum (immunoglobulin G, IgG) in 372

the co-immunoprecipitation buffer (50 mM HEPES pH 7.5, 150 mM KCl, 10 mM 373

ZnSO4, 5 mM MgCl2, and 1% Triton X-100) at 4°C overnight. After 374

immunoprecipitation, the beads were washed and eluted with SDS loading buffer. The 375

precipitated proteins were resolved by SDS-PAGE and immune-detected by anti-GFP 376

and anti-FLAG (F3165, Sigma) antibodies. 377

Gene Expression Analysis 378

Various seedlings grown in LD conditions were harvested at the indicated growth 379

stages for total RNA extracting using the E.Z.N.A. Total RNA Kit I (Omega) and 380

reverse transcribed to cDNA using MMLV-RTase (Promega). Quantitative real-time 381

PCR (qPCR) was performed using a LightCycler 480 thermal cycler system (Roche) 382



19

with KAPA SYBR Fast qPCR Kit Master Mix (KAPA BIO). The difference between 383

the cycle threshold (Ct) of target genes and the Ct of the control gene was calculated 384

by the relative quantification method (2-△△Ct) and used to evaluate quantitative 385

variation. The primers used for gene expression analysis are listed in Supplementary 386

Table S1. All expression analyses were performed with at least three biological 387

replicates (Three replicates of samples were taken from a same batch of seedlings, and 388

total RNA was extracted from the pooled 3~5 seedlings in per independent replicate. 389

The above experiments were independently performed thrice at least and the 390

representative results were shown). The p-value in data statistics was calculated by 391

two-tail Student’s t-test and one-way ANOVA. 392

ChIP Assay 393

ChIP assays were primarily performed as previously described (Hou et al., 2014). The 394

clf GFP-CLF and nf-ycT clf GFP-CLF seedlings grown in LD conditions were 395

collected at the indicated growth stages and fixed for 40 min in 1% formaldehyde. 396

Then, the nuclear proteins were extracted, and chromatin was isolated and sonicated 397

to create DNA fragments approximately 500 bp in length on average. After that, the 398

sonicated chromatin was immunoprecipitated by GFP-Trap (ChromoTek) or Protein G 399

PLUS agarose (16-201, Millipore) plus H3K27me3 antibody (07-449, Millipore) at 400

4°C overnight, and the remaining chromatin was used as an input control. The 401

precipitated DNA was recovered and quantified by qPCR with KAPA SYBR Fast 402

qPCR Kit Master Mix (KAPA BIO). Relative ChIP enrichment was calculated by 403

normalizing the amount of a target DNA fragment against that of a Cinful-like 404

genomic fragment and then against the respective input DNA amount. The primers 405

used for ChIP assay are listed in Supplementary Table S1. All ChIP analyses were 406

performed in three biological replicates (Three replicates of samples were taken from 407

a same batch of seedlings, and chromatins were extracted from the pooled 20-30 408

seedlings in per replicate. The above experiments were independently performed 409

thrice at least and the representative results were shown). The p-value in data statistics 410

was calculated by two-tail Student’s t-test and one-way ANOVA. 411



20

Accession Numbers 412

NF-YC3 (AT1G54830), NF-YC4 (AT5G63470), NF-YC9 (AT1G08970), CLF 413

(AT2G23380), CO (AT5G15840), FT (AT1G65480), FLC (AT5G10140), AG 414

(AT4G18960), SEP3 (AT1G24260), TUB2 (AT5G62690), Cinful-like (AT4G03770), 415

ACT2 (AT5G09810). 416

417

Supplemental Data 418

The following supplemental materials are available. 419

Supplemental Figure S1. Expression analysis of NF-YC3, NF-YC4, NF-YC9, and 420

CLF genes in nf-ycT, clf, and Col plants. 421

Supplemental Figure S2. Loss of NF-YB has a minimal effect on the early flowering 422

of clf mutants. 423

Supplemental Figure S3. Quantitative analysis of FT gene circadian expression in 424

nf-ycT, clf, clf nf-ycT, and Col plants. 425

Supplemental Figure S4. Expression analysis of FLC, AG, and SEP3 genes in nf-ycT, 426

clf, clf nf-ycT, and Col plants. 427

Supplemental Figure. S5. Time-course ChIP analysis of GFP-CLF binding (upper) 428

and H3K27me3 levels (below) at the ACT2 locus. 429

Supplemental Figure S6. ChIP analysis of CLF binding to the FT locus in the 430

presence of the carboxyl-terminal deleted NF-YC9. 431

Supplemental Table S1. List of primers used in this study. 432

433

ACKNOWLEDGMENT 434

We thank the Arabidopsis Biological Resource Centre for providing the mutant seeds 435

used in this study. 436

437

FIGURE LEGENDS 438

439

Figure 1. NF-YCs physically interact with CLF in vitro and in vivo. A, Yeast 440



21

two-hybrid assays show the interactions between CLF and NF-YC proteins. 441

Transformed yeast cells were grown on SD-Trp/-Leu/-His/-Ade and SD-Trp/-Leu 442

medium. B, Pull-down assays show the physical interaction between GST-CLF and 443

His-NF-YC fusion proteins in vitro. His-NF-YC proteins were incubated with 444

immobilized GST or GST-CLF, and immunoprecipitated fractions were detected by 445

anti-His and anti-GST antibodies, respectively. Arrows indicate the specific bands of 446

GST-CLF or GST; the arrowhead indicates the nonspecific bands. C, The domains 447

required for the interaction of CLF and NF-YC proteins. Sketches show the domains 448

of NF-YC9 and CLF and their various deletions. Yeast two-hybrid assays show the 449

interactions between CLF, NF-YC9 and their derivatives. Transformed yeast cells 450

were grown on SD-Trp/-Leu/-His/-Ade and SD-Trp/-Leu medium. D, BiFC analysis 451

of the interaction between NF-YC9-nEYFP and cEYFP-CLF in tobacco leaf 452

epidermal cells. The 4′,6-diamino-2-phenylindol (DAPI) staining indicates the 453

nucleus. Scale bar is 20 μm. E, In vivo interaction of NF-YC9 and CLF in Arabidopsis. 454

Plant nuclear extracts from 9-old-day clf nf-yc9 35S:GFP-CLF 455

pNF-YC9:NF-YC9-FLAG seedlings under LD conditions were immunoprecipitated by 456

either anti-GFP trap or preimmune serum (IgG). The co-immunoprecipitated proteins 457

were detected by anti-FLAG and anti-GFP antibodies. 458

459

Figure 2. Genetic analysis of interaction of CLF and NF-YC. A, The flowering 460

phenotypes of Col, clf, nf-ycT, and clf nf-ycT plants. The seedlings were grown 461

under LD conditions at 22°C for 28 days and selected for photographing. B, The 462

flowering times of Col, clf, nf-ycT, and clf nf-ycT plants under LD conditions at 22°C. 463

The number of rosette leaves in at least 10 plants at bolting was used as an indicator 464

of flowering time. Statistically significant differences are indicated by different 465

lower-case letters (one-way ANOVA, p < 0.05). C, Quantitative RT-PCR analysis of 466

FT, SOC1, and CO temporal expression in developing seedlings of Col, clf, nf-ycT, 467

and clf nf-ycT seedlings. The seedlings were grown under LD conditions at 22°C and 468

collected for RNA extraction at the 12th h in a 24h-period (16 h light / 8 h dark). The 469

TUBULIN 2 gene (TUB2) was used as an internal control. Data represent mean ± SD 470



22

of biological triplicates. 471

472

Figure 3. ChIP analysis of H3K27me3 levels in the relative flowering genes in 473

various mutants. A, Schematic representation of the specific primer positions in the 474

FT, FLC, SOC1, and AG loci used in Fig. 3B, 4B, and 5A. Exons are represented by 475

black rectangles and upstream regions and introns by black lines; the primer 476

fragments used for amplification are indicated by gray lines. B, ChIP analysis of 477

H3K27me3 levels of the relative flowering genes in Col, clf, nf-ycT, and clf nf-ycT 478

plants. Plant nuclear proteins were extracted from 9-old-day seedlings under LD 479

conditions. Relative fold-enrichment values were calculated by normalizing the 480

amount of a target DNA fragment against that of a genomic fragment of a reference 481

gene Cinful-like, and then against the respective input DNA samples. The enrichment 482

of an ACTIN2 (ACT2) genomic fragment was used as the negative control. Data 483

represent mean ± SD of biological triplicates. Statistically significant differences 484

between Col and mutants are indicated by different lower-case letters (one-way 485

ANOVA, p < 0.05). 486

487

Figure 4. Analysis of NF-YC effect on the CLF enrichment and H3K27me3 488

deposition at FT loci. A, Late flowering caused by loss of NF-YC genes requires 489

CLF activity. At least 10 seedlings of Col, clf, nf-ycT, clf GFP-CLF, clf nf-ycT, and 490

nf-ycT clf GFP-CLF plants grown under LD conditions at 22°C were investigated for 491

flowering time determination. B, Quantitative RT-PCR analysis of FT gene expression. 492

The 9-day-old seedlings were grown under LD conditions at 22°C and collected for 493

RNA extraction at 12th hour in a 24 h period (16 h light / 8 h dark). C, ChIP analysis 494

of CLF binding to the FT locus (amplicons defined in Figure 3A). D, Analysis of 495

H3K27me3 levels in FT chromatin. The 9-day-old clf 35S:GFP-CLF and nf-ycT clf 496

35S:GFP-CLF seedlings were grown under LD conditions at 22°C and collected for 497

ChIP assay with anti-GFP and anti-H3K27me3 antibodies, respectively. Data 498

represent mean ± SD of biological triplicates. Statistically significant differences are 499

indicated by different lower-case letters (one-way ANOVA, p < 0.05). Asterisks 500



23

indicate significant changes of enrichment fold between two genetic backgrounds 501

(Student’s t-test, p < 0.05). 502

503

Figure 5. Temporal pattern analysis of NF-YC and CLF regulating 504

CLF-dependent H3K27me3 at the FT locus. A, Time-course ChIP analysis of CLF 505

binding (upper) and H3K27me3 levels (below) in FT chromatin (amplicons defined in 506

Figure 3A). The seedlings of clf 35S:GFP-CLF and nf-ycT clf 35S:GFP-CLF were 507

grown under LD conditions at 22°C and harvested for nuclear protein extractions at 508

the indicated days. The percentages indicate the relative enrichment of the FT-I 509

fragment in clf 35S:GFP-CLF against that in nf-ycT clf 35S:GFP-CLF (designated as 510

100%). B, Co-IP analysis of temporal interaction between NF-YC9 and CLF in 511

developing seedlings. clf nf-yc9 GFP-CLF NF-YC9-FLAG seedlings grown under LD 512

conditions were harvested for nuclear protein extraction as indicated days, and then 513

immunoprecipitated by anti-GFP trap. The co-immunoprecipitated proteins were 514

detected by anti-FLAG and anti-GFP antibodies. 515

516

517



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Cao R, Wang L, Wang H, Xia L, Erdjument-Bromage H, Tempst P, Jones RS, Zhang Y (2002) Role of histone H3 lysine 27 methylation inPolycomb-group silencing. Science 298: 1039-1043


Cao S, Kumimoto RW, Gnesutta N, Calogero AM, Mantovani R, Holt III BF (2014) A distal CCAAT/NUCLEAR FACTOR Y complexpromotes chromatin looping at the FLOWERING LOCUS T promoter and regulates the timing of flowering in Arabidopsis. Plant Cell 26:1009-1017


Chen H, Huang X, Gusmaroli G, Terzaghi W, Lau OS, Yanagawa Y, Zhang Y, Li J, Lee JH, Zhu D, Deng XW (2010) Arabidopsis CULLIN4-damaged DNA binding protein 1 interacts with CONSTITUTIVELY PHOTOMORPHOGENIC1-SUPPRESSOR OF PHYA complexes toregulate photomorphogenesis and flowering time. Plant Cell 22: 108-123


Corbesier L, Vincent C, Jang S, Fornara F, Fan Q, Searle I, Giakountis A, Farrona S, Gissot L, Turnbull C, Coupland G (2007) FT proteinmovement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316: 1030-1033


Dolfini D, Gatta R, Mantovani R (2012) NF-Y and the transcriptional activation of CCAAT promoters. Crit Rev Biochem Mol Biol 47: 29-49


Doyle MR, Amasino RM (2009) A single amino acid change in the enhancer of zeste ortholog CURLY LEAF results in vernalization-independent, rapid flowering in Arabidopsis. Plant Physiol 151: 1688-1697


Engelhorn J, Blanvillain R, Kröner C, Parrinello H, Rohmer M, Posé D, Ott F, Schmid M, Carles CC (2017) Dynamics of H3K4me3chromatin marks prevails over H3K27me3 for gene regulation during flower morphogenesis in Arabidopsis thaliana. Epigenomes 1: 8


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Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.

http://www.ncbi.nlm.nih.gov/pubmed?term=Abe M%2C Kobayashi Y%2C Yamamoto S%2C Daimon Y%2C Yamaguchi A%2C Ikeda Y%2C Ichinoki H%2C Notaguchi M%2C Goto K%2C Araki T %282005%29 FD%2C a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex%2E Science 309%3A 1052%2D1056&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Abe M, Kobayashi Y, Yamamoto S, Daimon Y, Yamaguchi A, Ikeda Y, Ichinoki H, Notaguchi M, Goto K, Araki T (2005) FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science 309: 1052-1056

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

http://scholar.google.com/scholar?as_q=FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=Adrian J%2C Farrona S%2C Reimer JJ%2C Albani MC%2C Coupland G%2C Turck F %282010%29 cis%2DRegulatory elements and chromatin state coordinately control temporal and spatial expression of FLOWERING LOCUS T in Arabidopsis%2E Plant Cell 22%3A 1425%2D1440&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Adrian J, Farrona S, Reimer JJ, Albani MC, Coupland G, Turck F (2010) cis-Regulatory elements and chromatin state coordinately control temporal and spatial expression of FLOWERING LOCUS T in Arabidopsis. Plant Cell 22: 1425-1440

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

http://scholar.google.com/scholar?as_q=cis-Regulatory elements and chromatin state coordinately control temporal and spatial expression of FLOWERING LOCUS T 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=cis-Regulatory elements and chromatin state coordinately control temporal and spatial expression of FLOWERING LOCUS T in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Adrian&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Andres F%2C Coupland G %282012%29 The genetic basis of flowering responses to seasonal cues%2E Nat Rev Genet 13%3A 627%2D639&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Andres F, Coupland G (2012) The genetic basis of flowering responses to seasonal cues. Nat Rev Genet 13: 627-639

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

http://scholar.google.com/scholar?as_q=The genetic basis of flowering responses to seasonal cues&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=Bu Z%2C Yu Y%2C Li Z%2C Liu Y%2C Jiang W%2C Huang Y%2C Dong AW %282014%29 Regulation of Arabidopsis flowering by the histone mark readers MRG1%2F2 via interaction with CONSTANS to modulate FT expression%2E PLoS Genet 10%3A e1004617&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Bu Z, Yu Y, Li Z, Liu Y, Jiang W, Huang Y, Dong AW (2014) Regulation of Arabidopsis flowering by the histone mark readers MRG1/2 via interaction with CONSTANS to modulate FT expression. PLoS Genet 10: e1004617

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

http://scholar.google.com/scholar?as_q=Regulation of Arabidopsis flowering by the histone mark readers MRG1/2 via interaction with CONSTANS to modulate FT expression.&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 Arabidopsis flowering by the histone mark readers MRG1/2 via interaction with CONSTANS to modulate FT expression.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Bu&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Cao R%2C Wang L%2C Wang H%2C Xia L%2C Erdjument%2DBromage H%2C Tempst P%2C Jones RS%2C Zhang Y %282002%29 Role of histone H3 lysine 27 methylation in Polycomb%2Dgroup silencing%2E Science 298%3A 1039%2D1043&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Cao R, Wang L, Wang H, Xia L, Erdjument-Bromage H, Tempst P, Jones RS, Zhang Y (2002) Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298: 1039-1043

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

http://scholar.google.com/scholar?as_q=Role of histone H3 lysine 27 methylation in Polycomb-group silencing&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=Cao S%2C Kumimoto RW%2C Gnesutta N%2C Calogero AM%2C Mantovani R%2C Holt III BF %282014%29 A distal CCAAT%2FNUCLEAR FACTOR Y complex promotes chromatin looping at the FLOWERING LOCUS T promoter and regulates the timing of flowering in Arabidopsis%2E Plant Cell 26%3A 1009%2D1017&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Cao S, Kumimoto RW, Gnesutta N, Calogero AM, Mantovani R, Holt III BF (2014) A distal CCAAT/NUCLEAR FACTOR Y complex promotes chromatin looping at the FLOWERING LOCUS T promoter and regulates the timing of flowering in Arabidopsis. Plant Cell 26: 1009-1017

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

http://scholar.google.com/scholar?as_q=A distal CCAAT/NUCLEAR FACTOR Y complex promotes chromatin looping at the FLOWERING LOCUS T promoter and regulates the timing of flowering 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=A distal CCAAT/NUCLEAR FACTOR Y complex promotes chromatin looping at the FLOWERING LOCUS T promoter and regulates the timing of flowering in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Cao&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Chen H%2C Huang X%2C Gusmaroli G%2C Terzaghi W%2C Lau OS%2C Yanagawa Y%2C Zhang Y%2C Li J%2C Lee JH%2C Zhu D%2C Deng XW %282010%29 Arabidopsis CULLIN4%2Ddamaged DNA binding protein 1 interacts with CONSTITUTIVELY PHOTOMORPHOGENIC1%2DSUPPRESSOR OF PHYA complexes to regulate photomorphogenesis and flowering time%2E Plant Cell 22%3A 108%2D123&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Chen H, Huang X, Gusmaroli G, Terzaghi W, Lau OS, Yanagawa Y, Zhang Y, Li J, Lee JH, Zhu D, Deng XW (2010) Arabidopsis CULLIN4-damaged DNA binding protein 1 interacts with CONSTITUTIVELY PHOTOMORPHOGENIC1-SUPPRESSOR OF PHYA complexes to regulate photomorphogenesis and flowering time. Plant Cell 22: 108-123

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

http://scholar.google.com/scholar?as_q=Arabidopsis CULLIN4-damaged DNA binding protein 1 interacts with CONSTITUTIVELY PHOTOMORPHOGENIC1-SUPPRESSOR OF PHYA complexes to regulate photomorphogenesis and flowering time&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 CULLIN4-damaged DNA binding protein 1 interacts with CONSTITUTIVELY PHOTOMORPHOGENIC1-SUPPRESSOR OF PHYA complexes to regulate photomorphogenesis and flowering time&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Chen&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Corbesier L%2C Vincent C%2C Jang S%2C Fornara F%2C Fan Q%2C Searle I%2C Giakountis A%2C Farrona S%2C Gissot L%2C Turnbull C%2C Coupland G %282007%29 FT protein movement contributes to long%2Ddistance signaling in floral induction of Arabidopsis%2E Science 316%3A 1030%2D1033&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Corbesier L, Vincent C, Jang S, Fornara F, Fan Q, Searle I, Giakountis A, Farrona S, Gissot L, Turnbull C, Coupland G (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316: 1030-1033

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http://scholar.google.com/scholar?as_q=FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Corbesier&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Dolfini D%2C Gatta R%2C Mantovani R %282012%29 NF%2DY and the transcriptional activation of CCAAT promoters%2E Crit Rev Biochem Mol Biol 47%3A 29%2D49&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Dolfini D, Gatta R, Mantovani R (2012) NF-Y and the transcriptional activation of CCAAT promoters. Crit Rev Biochem Mol Biol 47: 29-49

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

http://scholar.google.com/scholar?as_q=NF-Y and the transcriptional activation of CCAAT 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

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http://www.ncbi.nlm.nih.gov/pubmed?term=Doyle MR%2C Amasino RM %282009%29 A single amino acid change in the enhancer of zeste ortholog CURLY LEAF results in vernalization%2Dindependent%2C rapid flowering in Arabidopsis%2E Plant Physiol 151%3A 1688%2D1697&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Doyle MR, Amasino RM (2009) A single amino acid change in the enhancer of zeste ortholog CURLY LEAF results in vernalization-independent, rapid flowering in Arabidopsis. Plant Physiol 151: 1688-1697

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http://www.ncbi.nlm.nih.gov/pubmed?term=Kumimoto RW%2C Zhang Y%2C Siefers N%2C Holt III BF %282010%29 NF%2DYC3%2C NF%2DYC4 and NF%2DYC9 are required for CONSTANS%2Dmediated%2C photoperiod%2Ddependent flowering in Arabidopsis thaliana%2E Plant J 63%3A 379%2D391&dopt=abstract

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Samach A, Onouchi H, Gold SE, Ditta GS, Schwarz-Sommer Z, Yanofsky MF, Coupland G (2000) Distinct roles of CONSTANS targetgenes in reproductive development of Arabidopsis. Science 288: 1613-1616


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Suarez-Lopez P, Wheatley K, Robson F, Onouchi H, Valverde F, Coupland G (2001) CONSTANS mediates between the circadian clockand the control of flowering in Arabidopsis. Nature 410: 1116-1120


Swain S, Myers ZA, Siriwardana CL, Holt BF 3rd (2017) The multifaceted roles of NUCLEAR FACTOR-Y in Arabidopsis thalianadevelopment and stress responses. Biochim Biophys Acta 1860: 636-644


Tang Y, Liu X, Liu X, Li Y, Wu K, Hou X (2017) Arabidopsis NF-YCs mediate the light control of hypocotyl elongation via modulatinghistone acetylation. Mol Plant 10: 260-273


Wigge PA, Kim MC, Jaeger KE, Busch W, Schmid M, Lohmann JU, Weigel D (2005) Integration of spatial and temporal informationduring floral induction in Arabidopsis. Science 309: 1056-1059


Zhao H, Wu D, Kong F, Lin K, Zhang H, Li G (2017) The Arabidopsis thaliana Nuclear Factor Y transcription factors. Front Plant Sci 7:2045



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http://www.ncbi.nlm.nih.gov/pubmed?term=Putterill J%2C Robson F%2C Lee K%2C Simon R%2C Coupland G %281995%29 The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors%2E Cell 80%3A 847%2D857&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Samach A%2C Onouchi H%2C Gold SE%2C Ditta GS%2C Schwarz%2DSommer Z%2C Yanofsky MF%2C Coupland G %282000%29 Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis%2E Science 288%3A 1613%2D1616&dopt=abstract

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http://search.crossref.org/?page=1&rows=2&q=Schubert D, Primavesi L, Bishopp A, Roberts G, Doonan J, Jenuwein T, Goodrich J (2006) Silencing by plant Polycomb-group genes requires dispersed trimethylation of histone H3 at lysine 27. EMBO J 25: 4638-4649

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

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http://search.crossref.org/?page=1&rows=2&q=Suarez-Lopez P, Wheatley K, Robson F, Onouchi H, Valverde F, Coupland G (2001) CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410: 1116-1120

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http://search.crossref.org/?page=1&rows=2&q=Swain S, Myers ZA, Siriwardana CL, Holt BF 3rd (2017) The multifaceted roles of NUCLEAR FACTOR-Y in Arabidopsis thaliana development and stress responses. Biochim Biophys Acta 1860: 636-644

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temporal-specific interaction of nf-yc and curly leaf during … · 2018. 3. 29. · 122 between...

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