A Flowering time locus C homolog is a vernalization-regulated ...2016/12/29 · 167 flowering following a 0, 2, 4, 6, 10 or 12 weeks treatment of cold of three-week-old 168 plants

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A Flowering time locus C homolog is a vernalization-regulated repressor in 1 Brachypodium and is cold-regulated in wheat 2 3 Authors: Neha Sharma*1, Philip Ruelens*1, Mariëlla D'hauw2, Thomas Maggen2, Niklas 4

Dochy1, Sanne Torfs1, Kerstin Kaufmann3, Antje Rohde2, Koen Geuten1 5

6 1

Department of Biology, KU Leuven, Kasteelpark Arenberg 31, B-3001 Leuven, 7

Belgium. 8

2 Bayer Crop Science NV, Technologiepark 38, B-9052 Gent, Belgium. 9

3 Institute for Biochemistry and Biology, Potsdam University, 14476 Potsdam-Golm, 10

Germany 11

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* Contributed equally 13

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Corresponding author 15

Koen Geuten, 16

Department of Biology, 17

KU Leuven, Kasteelpark Arenberg 31, B-3001 18

Leuven, Belgium 19

[email protected] 20

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Running Title: An FLC homolog in Brachypodium and Wheat 22

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Summary 24

Our study reveals that ODDSOC2/TaAGL33 functions in vernalization-responsive 25

flowering of Poaceae in a similar but also unique manner compared to its Arabidopsis 26

homolog, FLOWERING LOCUS C. 27

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Plant Physiology Preview. Published on December 29, 2016, as DOI:10.1104/pp.16.01161

Copyright 2016 by the American Society of Plant Biologists

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Author contributions: KG, AR, PR, NS, KK designed the research; NS, PR, ND, ST, 29

MD, TM performed research; NS, PR, MD, TM, AR, KG analyzed data; NS, PR, KK, 30

AR, KG wrote the paper. 31

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Funding information: This research was supported by FWO grant G065713N from 33

which NS was supported. PR was supported by a fellowship from IWT and currently 34

holds a postdoctoral fellowship from the KU Leuven (PDM/15/104). ND is supported by 35

an IWT fellowship. 36

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Abstract 38

Winter cereals require prolonged cold to transition from vegetative to reproductive 39

development. This process, referred to as vernalization, has been extensively studied in 40

Arabidopsis thaliana. In Arabidopsis, a key flowering repressor called FLOWERING 41

LOCUS C (FLC) quantitatively controls the vernalization requirement. By contrast, in 42

cereals, the vernalization response is mainly regulated by the VERNALIZATION genes, 43

VRN1 and VRN2. Here we characterize ODDSOC2, a recently identified FLC ortholog 44

in monocots, for the first time knowing that it belongs to the FLC lineage. By studying its 45

expression in a diverse set of Brachypodium accessions, we find that it is a good 46

predictor of the vernalization requirement. Analyses of transgenics demonstrated that 47

BdODDSOC2 functions as a vernalization-regulated flowering repressor. In most 48

Brachypodium accessions BdODDSOC2 is downregulated by cold and in one of the 49

winter accessions in which this downregulation was evident, BdODDSOC2 responded 50

to cold before BdVRN1. When stably downregulated, the mechanism is associated with 51

spreading H3K27me3 modifications at the BdODDSOC2 chromatin. Finally, homeolog-52

specific gene expression analyses identifies TaAGL33 and its splice variant TaAGL22 53

as the FLC orthologs in Triticum behaving most similar to Brachypodium ODDSOC2. 54

Overall our study suggests that ODDSOC2 is not only phylogenetically related to FLC in 55

eudicots, but also functions as a flowering repressor in the vernalization pathway of 56

Brachypodium and likely other temperate grasses. These novel insights could prove 57

useful in breeding efforts to refine the vernalization requirement of temperate cereals 58

and adapt varieties to changing climates. 59



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60

Introduction 61

Optimal adaptation to the environment is a vital factor in the survival of all living 62

organisms. Plants have evolved various mechanisms to sense environmental signals, 63

which help them to synchronize their development to environmental changes. Among 64

environmental cues, seasonal temperature and photoperiod variation play a decisive 65

role in determining the optimal time to flower. Many plants adapted to temperate 66

climates flower only after a prolonged exposure to cold to prevent the premature 67

flowering during warm autumn days, a process referred to as vernalization (Chouard, 68

1960, Kim et al., 2009). A better understanding of this process can have a significant 69

impact on crop yield as temperate winter cereals grow vegetatively without vernalization 70

and transition to their reproductive state only after their vernalization requirement is 71

saturated. 72

73

The process of vernalization has been traditionally studied in economically important 74

temperate cereals like wheat and barley (Chouard, 1960), yet its regulation has been 75

most extensively investigated in Arabidopsis. In winter-annual Arabidopsis ecotypes, 76

FLOWERING LOCUS C (FLC) is a central repressor of flowering (Michaels and 77

Amasino, 1999, Sheldon et al., 2000), which represses the flowering pathway 78

integrators FLOWERING LOCUS T (FT) and SUPPRESSOR OF OVEREXPRESSION 79

OF CONSTANS1 (SOC1) (Michaels et al., 2005). Prolonged cold results in epigenetic 80

silencing of FLC, which releases repression of FT and SOC1 in order to enable 81

flowering after return to warm conditions (Bastow et al., 2004, De Lucia et al., 2008). By 82

contrast, in temperate cereals such as wheat and barley, vernalization is mainly 83

governed by two key genes, namely VERNALIZATION1 (VRN1) and VRN2, which 84

regulate flowering integrator VRN3 (Dennis and Peacock, 2009, Greenup et al., 2009). 85

VRN1, a MADS-box transcription factor related to Arabidopsis APETALA1 (AP1), is a 86

promoter of flowering. In varieties that require vernalization, VRN1 is upregulated in 87

response to cold while in spring varieties VRN1 is expressed without vernalization, 88

which reduces or eliminates their vernalization requirement (Danyluk et al., 2003, 89

Preston and Kellogg, 2006, Trevaskis et al., 2003, Yan et al., 2003, Preston and 90



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Kellogg, 2008). Analogous to the epigenetic regulation of FLC, VRN1 upregulation in 91

winter varieties is associated with low levels of the repressed chromatin state 92

H3K27me3 and high levels of the active chromatin mark H3K4me3 (Oliver et al., 2009). 93

The subsequent stable high expression level of VRN1 results in the downregulation of 94

the flowering repressor VRN2 after prolonged cold (Distelfeld et al., 2009, Hemming et 95

al., 2008, Trevaskis et al., 2006, Yan et al., 2004b). However, more recently it was 96

shown that VRN1 is not essential for flowering or for the downregulation of VRN2 during 97

vernalization, suggesting that additional genes control VRN2 downregulation when 98

exposed to cold (Chen and Dubcovsky, 2012). Finally, downregulation of VRN2 99

releases VRN3, a homolog of FT in Arabidopsis, which induces flowering after cold and 100

in response to long days (Distelfeld et al., 2009, Trevaskis et al., 2007, Turner et al., 101

2005, Yan et al., 2006). 102

103

One reason why it is thought that the vernalization response evolved independently in 104

Arabidopsis and temperate cereals has been the difficulty of identifying FLC-like genes 105

in monocots by sequence homology searches (Alexandre and Hennig, 2008, Hemming 106

and Trevaskis, 2011, Kim et al., 2009). However, we recently identified three 107

paralogous FLC gene lineages, i.e. ODDSOC1, ODDSOC2 and MADS37 in Pooideae 108

(Ruelens et al., 2013). In Brachypodium distachyon (hereafter referred as 109

Brachypodium), BdODDSOC2 and BdMADS37 expressions levels are downregulated in 110

response to cold analogous to FLC in Arabidopsis, while BdODDSOC1 expression does 111

not change in response to cold in the spring accession Bd21 (Ruelens et al., 2013). The 112

cold response of BdODDSOC2 in Brachypodium Bd21 is similar to Hordeum vulgare cv. 113

Golden Promise (Greenup et al., 2010) and it has been shown that overexpression of 114

HvODDSOC2 delays flowering and reduces spike growth, stem and leaf length. 115

However, HvODDSOC2 RNAi transgenic lines did not show a phenotypic effect in the 116

spring accession Golden promise. Recently, it was reported that VRN1 can bind to the 117

promoter of ODDSOC2 in Hordeum and ODDSOC2 expression is upregulated in VRN1 118

mutants in Triticum, though not before or during vernalization (Greenup et al., 2010, 119

Deng et al., 2015). 120

121



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Natural variation in the vernalization requirement allows plants to adapt to local climate 122

conditions as the presence and duration of the cold season represents a crucial cue 123

influencing the optimal flowering time (Kim et al., 2009). In Arabidopsis, natural variation 124

in flowering time through vernalization is correlated with allelic variation at the FLC and 125

FRIGIDA (FRI) loci (Shindo et al., 2005). Moreover, loss-of-function mutations at the 126

FLC locus have been linked to the early flowering phenotype of many Arabidopsis 127

spring accessions. The FLC locus of these accessions typically contains independent 128

insertions of a transposon in the first regulatory intron resulting in weak or nonfunctional 129

FLC alleles (Gazzani et al., 2003, Michaels et al., 2003b). However, in economically 130

important crops like wheat and barley, mainly allelic variation at the VRN1 and VRN2 131

loci govern the natural variation in vernalization mediated flowering (Trevaskis et al., 132

2003, Yan et al., 2004b, Yan et al., 2003). For instance, natural allelic variation at the 133

VRN1 locus is associated with differences in the vernalization requirement between 134

spring and winter cereals (Trevaskis et al., 2003, Yan et al., 2004a, Yan et al., 2003). 135

Furthermore, spring varieties often also have mutations or deletions in the CCT domain 136

of VRN2 (Dubcovsky et al., 2005, Yan et al., 2004b). Similar to cereals, different natural 137

accessions of Brachypodium have a widely varying vernalization requirement, however 138

the genetic determinants for this variation are not well defined (Schwartz et al., 2010, 139

Tyler et al., 2014). Likewise, whether FLC-like genes in monocots contribute to the 140

variation in vernalization requirement has not been explored. 141

142

To better understand the function of these genes, we functionally characterized 143

ODDSOC2, one of the FLC homologs in grasses, in the model Brachypodium 144

distachyon. Like FLC, BdODDSOC2 functions as a vernalization-responsive repressor 145

of flowering. In addition, natural variation in the vernalization requirement among 146

different Brachypodium accessions can be attributed to BdODDSOC2 pre-vernalization 147

expression levels. During cold, BdODDSOC2 is downregulated in most accessions and 148

this response occurs hours before BdVRN1. We show that stable downregulation is 149

associated with the spreading of histone methylation across the ODDSOC2 locus. 150

Consistent with a conserved role of ODDSOC2 genes among cereals, the Triticum 151



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aestivum ODDSOC2 ortholog TaAGL33 exhibits an expression pattern similar to FLC in 152

response to vernalization. 153

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5

Results 157

BdODDSOC2 expression linked to vernalization requirement among 158

Brachypodium accessions 159

To evaluate the role of BdODDSOC2 in the vernalization response, we studied its 160

expression in response to cold in a set of Brachypodium inbred lines derived from plants 161

originating from different climatic regions (Supplemental Table 1). Although previous 162

studies already investigated the vernalization requirement of numerous Brachypodium 163

accessions (Ream et al., 2014, Schwartz et al., 2010), we first assessed the 164

vernalization requirement of the selected accessions in our laboratory conditions. 165

Vernalization requirement was analyzed by determining the number of days until 166

flowering following a 0, 2, 4, 6, 10 or 12 weeks treatment of cold of three-week-old 167

plants. Subsequently, we assigned each accession a vernalization requirement as the 168

minimum number of weeks of vernalization that results in the largest decrease in days 169

to flowering. This analysis corroborates previous results reporting a large variation in 170

vernalization requirement among Brachypodium accessions (Supplemental Table 1) 171

(Schwartz et al., 2010). Furthermore, vernalization requirement shows the expected 172

positive correlation with the latitude of origin (Pearson, r=0.504, p=0.007), indicating 173

that in general accessions with a long vernalization requirement originate from more 174

northern latitudes while accessions from southern latitudes possess a short 175

vernalization requirement. 176

177

To assess to what extent BdODDSOC2 downregulation in response to cold is 178

conserved among Brachypodium accessions, we examined the expression level of 179

BdODDSOC2 before vernalization (three week old plants, 23°C, 16h light/ 8h dark) and 180

following four weeks of vernalization in 25 different accessions (4°C, 8h light/ 16h dark). 181

Our results show that in 18 out of 25 accessions BdODDSOC2 expression levels 182

decrease in response to cold (Fig. 1A). In 11 accessions, this expression is significantly 183

downregulated (Student’s t-test, p<0.05, Supplemental Table 1). In seven accessions 184

BdODDSOC2 levels increase (Fig. 1A), however, only two accessions, Bd1-1 and 185

BdTR9K, exhibited a significant increase following four weeks at 4°C compared to pre-186

vernalization (Student’s t-test, p<0.05, Supplemental Table 1). BdVRN1 expression 187



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increased in all accessions in response to cold and 19 accessions exhibited a significant 188

increase (Student’s t-test, p<0.05, Supplemental Table 1). To study the response of 189

BdODDSOC2 to cold in more detail, we monitored BdODDSOC2 expression levels 190

during 0, 2, 4, 6, 10 weeks of cold in six different accessions (Fig. 1B). In Bd3-1 and 191

Adi10, BdODDSOC2 expression during vernalization did not significantly change 192

compared to non-vernalization. Expression levels of BdODDSOC2 in BdTR2B, 193

BdTR2G, Kah-1 and BdTR5I exhibited clear downregulation, although expression 194

during vernalization in Kah-1 did not significantly change compared to non-vernalization. 195

In the accessions Bd3-1 and Adi10, for which ODDSOC2 did not change following four 196

weeks of vernalization, a longer cold period also did not lead to cold induced 197

downregulation. 198

199

Previous studies in Arabidopsis showed a significant correlation between the expression 200

level of FLC in non-vernalized plants and the vernalization response (Sheldon et al., 201

2000, Shindo et al., 2005). Therefore we analyzed whether this correlation is also 202

present in Brachypodium. Specifically, we performed regression analyses between the 203

expression level of ODDSOC2 in non-vernalized plants or four week vernalized plants 204

and vernalization requirement. These analyses show that vernalization requirement is 205

significantly correlated with the expression level of BdODDSOC2 before vernalization 206

(Fig. 1C). Moreover, BdODDSOC2 transcript level before vernalization is a good 207

predictor of the length of vernalization (R2=0.50, p<0.001). However, expression levels 208

of BdODDSOC2 in plants exposed to four weeks of cold could not predict the 209



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vernalization requirement (R2=0.044, p=0.32). This suggests that mRNA transcript 210

downregulation of BdODDSOC2 by itself cannot explain the vernalization length 211

requirement. We also performed a regression analyses between vernalization 212

requirement and BdVRN1 expression, which in wheat plays a pivotal role in the 213

vernalization response and explains part of the variation in vernalization requirement. 214

However, in Brachypodium the expression level of BdVRN1 before cold is not 215

significantly correlated with the vernalization requirement (R2= 0.13, p= 0.067). Our 216

analyses did detect a correlation between the expression level of BdVRN1 of vernalized 217

plants and vernalization requirement, albeit only marginally significant and poorly 218

predictive (R2= 0.15, p= 0.047, Fig. 1C). 219



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220

BdODDSOC2 overexpression plants exhibit delayed flowering and are 221

unresponsive to vernalization 222

To investigate BdODDSOC2’s role during vernalization, we first overexpressed 223

BdODDSOC2 cDNA in Brachypodium accession Bd21-3 which is amenable to 224

Agrobacterium-mediated transformation (Vogel and Hill, 2008). Bd21-3 is a facultative 225

winter accession that flowers without vernalization after 125 days (16h light/ 8h dark 226

photoperiod), but exposure to two weeks of cold significantly accelerates flowering by 227

64 days (Fig. 2A). To assess how BdODDSOC2 responds to cold in Bd21-3, we 228

examined its expression using qRT-PCR prior to vernalization (NV), following two 229

weeks of vernalization (2wV) and after one week return to warm conditions (1wPV). Our 230

results show that BdODDSOC2 mRNA levels are not significantly altered following 231

vernalization (Fig. 2B). However, relative expression of BdODDSOC2 prior to 232

vernalization in Bd21-3, which requires two weeks of cold to saturate its vernalization 233

requirement, is lower compared to most accessions requiring a longer cold exposure 234

(Fig. 1C, red dot). 235

236

We generated and transformed a construct expressing BdODDSOC2 cDNA from the 237

constitutively active Zea mays UBIQUITIN promoter, for which we obtained 17 238

overexpression lines. Ten lines with maximum seed yield were chosen for detailed 239

characterization (see Methods). In all ten overexpression lines, the BdODDSOC2 240

transcript level was increased as determined by semiquantitative RT-PCR 241

(Supplemental Fig. 1). In order to test whether BdODDSOC2 affected flowering time, T2 242

overexpression transgenic lines were grown and phenotyped together with non-243

transgenic controls and wild-type Bd21-3 plants in two different conditions (see 244

Methods). Non-transgenic controls (NC) were plants that went through transformation 245

but did not carry the transgene in T0. In non-vernalized conditions (NV), all 246

BdODDSOC2 overexpression plants carrying the transgene flowered at the same time 247

as the control plants (Fig. 2C, Supplemental Fig. 2A). By contrast, when vernalized (V), 248

eight out of ten BdODDSOC2 overexpression lines exhibited a significant delay in 249

flowering time. Out of these eight lines, line 3, 11, 11.1, 16 and 17 flowered on average 250



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62 days later than control plants which is similar to the delay in flowering of wild-type 251

Bd21-3 plants without undergoing vernalization (Fig. 2D). Lines 8, 14 and 17.1 flowered 252

on average 41 days later (Supplemental Fig. 2B). The two lines showing no delay in 253



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flowering, lines 10 and 12 (Supplemental Fig. 2B), did show the least increase in 254

BdODDSOC2 expression level, suggesting flowering time is affected by BdODDSOC2 255

in a dosage-sensitive manner (Supplemental Fig. 1A). In agreement with their 256

phenotype, late-flowering lines also had significantly more total numbers of leaves 257

compared to control plants in the vernalized condition (Fig. 2H, Supplemental Fig. 2E). 258

No difference in leaf number could be detected between transgenic lines and control 259

plants grown in NV condition (Fig 2G, Supplemental Fig. 2G). Other differences, 260

developmental or morphological, were not detected in the analyzed transgenic lines 261

compared to their null-siblings. These results show that BdODDSOC2 overexpression 262

plants did not respond to vernalization and flowered at a similar time as wild type Bd21-263

3 grown without vernalization. 264

265

RNAi-mediated knockdown of BdODDSOC2 results in accelerated flowering 266

We also analyzed flowering time in both vernalized and non-vernalized conditions for 267

plants that ectopically express a hairpin construct in Bd21-3 intended to knock down 268

endogenous BdODDSOC2 transcripts. Semiquantitative RT-PCR revealed that out of 269

ten lines, eight lines exhibited a reduction in BdODDSOC2 expression levels 270

(Supplemental Fig. 1B), while lines 14 and 22 did not show a measurable BdODDSOC2 271

knockdown. When grown in non-vernalized conditions five RNAi lines exhibited 272

significantly earlier flowering compared to control plants (Fig. 2E, Supplemental Fig. 273

2C). Out of these five lines, RNAi lines 4 and 5 flowered 20 and 27 days earlier 274

respectively, while lines 3, 8 and 19 flowered on average 12 days earlier. When 275

vernalized, BdODDSOC2 RNAi-knockdown lines flowered at the same time as their 276

non-transgenic control or wild type plants (Fig. 2F, Supplemental Fig. 2C). This might be 277

explained by the fact that two weeks of vernalization almost completely saturates the 278

vernalization requirement of Bd21-3 masking any further, especially partial, acceleration 279

of flowering (Schwartz et al., 2010). Surprisingly, although not all RNAi-mediated 280

knockdown lines show early flowering in NV conditions, except for line 3, all lines have a 281

smaller number of leaves in comparison with the controls in NV condition (Fig. 2I, 282

Supplemental Fig. 2F). Yet leaf number was similar in transgenic RNAi and control 283

plants under vernalized conditions (V) (Fig. 2J, Supplemental Fig. 2H). Transgenic RNAi 284



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plants did not exhibit any morphological or developmental changes except for those 285

described here. To conclude, BdODDSOC2 RNAi lines exhibit early flowering when 286

grown without vernalization while flowering is similar to wild type Bd21-3 in the 287

vernalized condition. 288

289

BdODDSOC2 responds earlier than BdVRN1 in a vernalization responsive 290

accession BdTR3C 291

To investigate the early vernalization response mechanism, we analyzed the expression 292

level of BdODDSOC2 and BdVRN1 after 0, 6, 12, 24 and 48 hours of cold in the 293

vernalization sensitive winter accession BdTR3C. We used this accession because 294

Bd21-3 is a facultative winter accession and does not have mandatory cold requirement 295

while BdTR3C is a winter accession requiring six weeks of cold (Supplemental Table 1). 296

Our results revealed that expression of BdODDSOC2 is already significantly down after 297

six hours of cold and remained significantly down after 12, 24 and 48 hours of cold (Fig. 298

3A). By contrast, expression of BdVRN1 was not altered after 6 or 12 hours of cold (Fig. 299

3B), BdVRN1 responded to cold only after 24 hours of cold and expression remained 300

significantly higher after 48 hours of cold (Fig. 3B). This suggests that BdODDSOC2’s 301

response to cold is earlier than BdVRN1 in a vernalization responsive accession 302

(BdTR3C). While it is known for Brachypodium and barley that VRN1 is a negative 303

regulator of ODDSOC2, our observation makes it less likely that BdVRN1 is causing the 304

early transcriptional downregulation of BdODDSOC2 or sets the ODDSOC2 initial 305

expression level (Deng et al., 2015, Woods et al., 2016). 306

307

BdODDSOC2 downregulation is stably maintained after vernalization in a winter 308

accession BdTR3C, but not in a spring accession Bd21 309

To assess whether downregulation of BdODDSOC2 and upregulation of BdVRN1 in 310

response to vernalization is maintained after returning the plants to warm conditions in a 311

winter compared to a spring accession, we performed expression analysis of 312

BdODDSOC2 and BdVRN1 in the spring accession Bd21, in which BdODDSOC2 is 313

downregulated in response to cold (Ruelens et al., 2013) and compared this to the 314

winter accession BdTR3C. We collected samples before cold (NV), after two weeks of 315



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cold for Bd21, six weeks of cold for BdTR3C and after 1, 2, 3, 4, 5, 6, and 7 weeks 316

postvernalization. Our results show that expression of BdODDSOC2 is significantly 317

downregulated after two (Bd21) and six (BdTR3C) weeks of vernalization in both 318

accessions, but this downregulation is stably maintained only in the winter accession 319



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BdTR3C (Fig. 3C-D). However, in the spring accession Bd21, expression of 320

BdODDSOC2 increased again when plants were returned to warm temperatures for one 321

week (PV) (Fig. 3C). As expected, expression of BdVRN1 was significantly higher after 322

vernalization (2wV and 6wV) and also remained significantly higher during 323

postvernalization in both Brachypodium accessions (Bd21 and BdTR3C) (Fig. 3D, F). 324

Interestingly, expression levels of BdVRN1 in postvernalization stages (1wPV to 7wPV) 325

were low in comparison to BdVRN1 expression level during cold in Bd21 (Fig. 3D). 326

Overall, these results suggest that BdODDSOC2 downregulation is stably maintained 327

long after vernalization in the winter accession BdTR3C but not in the spring accession 328

Bd21. 329

330

Downregulation of BdODDSOC2 is associated with H3K27me3 enrichment at 331

BdODDSOC2 chromatin 332

To investigate the mechanism related to the downregulation of ODSSCO2, we 333

performed chromatin immunoprecipitation experiments (ChIP). In Arabidopsis, stable 334

downregulation of FLC is associated with H3K27me3 (histone 3 lysine 27 trimethylation) 335

enrichment at the FLC chromatin (Bastow et al., 2004, Sung and Amasino, 2004). To 336

determine whether downregulation of BdODDSOC2 in response to vernalization is 337

associated with H3K27me3 modifications, we analyzed H3K27me3 modification in the 338

spring Brachypodium accession Bd21 and the winter accession BdTR3C before cold 339

(NV), after two weeks for Bd21 and six weeks of vernalization for BdTR3C and one 340

week after returning the plants to warm conditions (PV). H3K27me3 modification is 341

associated with repression of transcription (Barski et al., 2007, Zhang et al., 2007). Our 342

results show that H3K27me3 levels were high at BdODDSOC2 chromatin in response 343

to vernalization in Bd21 and BdTR3C (Fig. 3I, K). However, H3K27me3 enrichment was 344

significant mainly near the transcription start site or ‘nucleation region’ in the spring 345

accession Bd21 (region upB, A, B, C, D) while in the winter accession BdTR3C, 346

significant H3K27me3 enrichment spanned the entire BdODDSOC2 locus during 347

vernalization (region upB, A, B, C, D, E, F, G, H). In addition, H3K27me3 modification 348

was also maintained at BdODDSOC2 chromatin one week after return to warm 349

conditions (PV), but only locally in the spring accession Bd21 (region upB, B, C) and 350



14

across the locus in the winter accession BdTR3C (region upB, A, B, C, E, G, H). These 351

results suggest that enrichment of H3K27me3 across the BdODDSOC2 locus is 352

responsible for stable downregulation of BdODDSOC2 in BdTR3C. 353

354

In Hordeum, HvVRN1 upregulation in response to vernalization is associated with a 355

decrease in H3K27me3 and an increase in H3K4me3 modification at HvVRN1 (Oliver et 356

al., 2009). Similarly, we analyzed H3K27me3 histone modification at BdVRN1 in Bd21 357

and BdTR3C. BdVRN1 chromatin showed a significant decrease in H3K27me3 358

modifications during vernalization (region upA, C) and postvernalization (region upA, A, 359

C) in the winter accession BdTR3C (Fig. 3L). By contrast, our results did not reveal an 360

effect of vernalization on H3K27me3 histone marks at BdVRN1 chromatin in the spring 361

accession Bd21 (Fig. 3J). 362

363

Altered expression of BdODDSOC2 does not affect mRNA levels of 364

VERNALIZATION1/2/3 365

To understand possible cross-regulation and to identify downstream genes acting in the 366

same pathways as ODDSOC2, we investigated expression of candidate targets in the 367

most severely affected lines. In Hordeum, overexpression of ODDSOC2 downregulates 368

FPF1 (Greenup et al., 2010) while FLC in Arabidopsis is known to repress FT and 369

SOC1 (Michaels et al., 2005). We quantified the transcript levels of their Brachypodium 370

orthologs using qRT-PCR in the two strongest overexpression (line 3 and 11.1) and 371

RNAi (line 4 and 5) lines at three different time points: before cold (NV), after two weeks 372

of vernalization (V) and after two weeks of postvernalization (PV). In addition to 373

BdVRN3, BdFPF1 and BdSOC1, we also evaluated whether expression of BdVRN1 374

and BdVRN2 is affected in BdODDSOC2 transgenic lines. Despite significantly higher 375

and lower transcript levels of BdODDSOC2 in overexpression and RNAi lines 376

respectively (Supplemental Fig.6 A-B), the expression levels of the aforementioned 377

genes were not detectably affected (Supplemental Fig.6 C-G). 378

379

FLC homologs in Triticum aestivum 380



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After exploring the role of BdODDSOC2 in Brachypodium, we further studied the role of 381

FLC homologs in the vernalization response of the economically important crop 382

Triticum. Six gene sequences were previously identified as FLC orthologs in wheat 383

(Ruelens et al., 2013) (Supplemental Fig. 3). These genes were blasted against the 384

available wheat genome sequence of ‘Chinese Spring’, the sequenced reference line 385

(International Wheat Genome Sequencing Consortium (2014, Choulet et al., 2014). Due 386

to the hexaploid nature of wheat (AABBDD genome), each of those genes are in 387

principle present as three homeologous genes. Our search for wheat FLCs showed that 388

TaAGL12, belonging to the MADS37 clade, is the sole FLC homolog located on 389

chromosome 7. All other genes are located on chromosome 3 including the ODDSOC1 390

homolog TaAGL42, and the four ODDSOC2 homologs TaAGL41, TaAGL33, TaAGL22 391

and TaMADS2 (Fig. 4), as identified earlier (Ruelens et al., 2013) (Supplemental Fig. 3). 392

Sequence alignments further revealed that TaAGL42 is located downstream of 393

TaAGL41. TaAGL42 fragments are present in the A and D subgenome, but seem to be 394

absent in the B subgenome of the current genome sequence. TaAGL41 is located 395

immediately downstream of TaAGL33-B and TaAGL22-B in a tandem duplication on the 396

B subgenome (Fig. 4). Curiously, TaAGL33 and TaAGL22 which were previously 397

isolated from wheat cDNA and annotated as separate genes (Zhao et al., 2006) share 398

their promoter and MADS-box domain, yet both variants have different exons coding for 399

the I- K- and C-domains of the protein. These exons of the two variants are located 18 400

kb apart from each other. The fact that two gene variants share the MADS box has to 401

our knowledge not been previously observed in the MADS-box gene family (Fig. 4, 402

inset). Additional searches could not find another MADS-box in the region (Fig. 4, inset). 403

The presence of both transcripts, including the same MADS box and the respectively 404

different exons coding for the I- K- and C-domains (Fig. 4, inset), was verified with 405

cDNA amplification (data not shown). As their encoded proteins consist of the same 406

DNA-binding MADS-domain both proteins likely target the same genes. However, their 407

highly diverged I- and K-domains, which determine protein-protein interaction specificity, 408

could result in the formation of different protein complexes with distinct regulatory 409

functions. Consequently, we refer to TaAGL22 and TaAGL33 as variants from the same 410

transcriptional unit. TaMADS2 appears to be identical to the homeolog of TaAGL33-B 411



16

on the D subgenome, hence is referred to hereafter as TaAGL33-D. In summary, the six 412

previously identified genes are collapsing to four FLC-like genes in Triticum aestivum 413

each on three subgenomes, with exception of TaAGL42 which is only present on the A 414

and D subgenomes. 415

416

Expression of ODDSOC2-like genes in a diverse set of wheat cultivars 417

To assess the role of wheat FLC homologs in vernalization, we studied their expression 418

in ten wheat varieties with high genetic differentiation as measured by FST between 419

winter habit and spring habit (Table 1) (regions as described in (Cavanagh et al., 420

2013)). Since in wheat, VRN1 is most clearly associated to vernalization requirement 421

and PPD is involved in the response to photoperiod after the vernalization requirement 422

is fulfilled, the varieties used were balanced for those loci. Vernalization requirements 423

were established as days to flowering after exposure to 0, 4 and 8 weeks of cold. As 424

expected, days to flowering varied greatly from 30 days to non-flowering (>111 days). 425

Winter accessions (Xiaoyan54, Toisondor, Mendel, Grafton, Kingdom) did flower only 426

after eight weeks of vernalization (Table 1). By contrast, spring accessions (Azhurnaya, 427

Faller, Westonia, Taifun), flowered approximately at the same time regardless 428

vernalization or the duration of vernalization. The facultative accession (Chinese Spring) 429

flowered 31 days earlier when vernalized for eight weeks in comparison to without 430

vernalization (Table 1). 431

432



17

To study the expression of FLC-related homologs, plant samples were collected from 433

three weeks old seedlings prior to cold exposure (NV), after 2, 4, 6 and 8 weeks of cold 434

(2wV, 4wV, 6wV and 8wV) and 2 and 4 weeks after return to warm temperatures 435

(2wPV, 4wPV). As a control, we first characterized the expression of VRN1-A, VRN2 436

and VRN3. As expected, we found that VRN1-A expression is upregulated upon cold 437

exposure and VRN3 starts to peak only after return to warm and long day conditions in 438

all studied Triticum accessions (Fig. 5A, Supplemental Fig. 4). Interestingly, our results 439

show that VRN2 was downregulated during the first two or four weeks of cold in most 440

studied Triticum varieties as expected, but after longer cold exposure VRN2 expression 441

increased higher than pre-vernalization levels in seven of the studied Triticum varieties 442

(Supplemental Fig. 4B). Although this upregulation is unexpected it has to be noted that 443

in our study plants were vernalized under a 12h-photoperiod to mimic the short-days of 444

winter in temperate regions. By contrast, in previous studies in wheat and barley where 445

VRN2 expression was found downregulated in response to cold, expression was 446

determined in long-day conditions (Yan et al., 2004b, Trevaskis et al., 2006). This 447

expression pattern, however, is similar to BdVRN2L behavior in Brachypodium, where it 448

is induced upon cold exposure and functions as a repressor of flowering (Ream et al., 449

2014, Woods et al., 2016), which underlines Brachypodium as a potential model system 450

to further elucidate the evolution and the molecular mechanisms of the vernalization 451

response. 452

453

We first studied the homeolog-aspecific expression patterns for the BdODDSOC1 454

homolog TaAGL42, the BdODDSOC2 homologs TaAGL41, TaAGL33 (and TaAGL22) 455

and the BdMADS37 homolog TaAGL12 (Fig. 5A). We were not able to detect any 456

TaAGL12 expression in leaves at all studied time points. TaAGL42 expression was 457

downregulated after cold only in spring varieties (Fig. 5A). Furthermore, we found that 458

TaAGL41 expression decreased during cold exposure, but downregulation was 459

strongest in spring accessions that also exhibited high expression of TaAGL41 prior to 460

vernalization (Fig. 5A, Supplemental Fig. 5A). As TaAGL33 and its variant TaAGL22 461

exhibited a similar homeolog-aspecific expression pattern as BdODDSOC2 (data not 462

shown), we designed homeolog-specific primers for these genes and performed 463



18

subgenome-specific expression analyses (Fig. 5A, Supplemental Fig. 5B-G). Consistent 464

with TaAGL33 and TaAGL22 sharing a promoter region, expression between variants 465

originating from the same subgenome was very similar. Moreover, the transcript levels 466

of TaAGL33 (A, B, D) and TaAGL22 (A, B, D) were stably downregulated by cold in the 467

majority of accessions (Fig. 5A, Supplemental Fig. 5B-G). Expression of some 468

TaAGL33 and TaAGL22 homeologs did increase during the first two weeks of cold but 469

later decreased during cold treatment. The expression prior to vernalization and the 470

subsequent downregulation varied per subgenome, indicating that each of the 471

subgenomes carries slightly different alleles. When relative expression of TaAGL22 and 472



19

TaAGL33 under non-vernalized conditions is compared between winter and spring 473

varieties a similar pattern is present as in Brachypodium in that winter varieties 474

consistently show a higher expression level than spring varieties (Fig. 5B). Notably, 475

TaAGL22-D and TaAGL33-D exhibited a clearly significant expression difference 476

between winter and spring wheat varieties prior to vernalization (Fig. 5B). Furthermore, 477

TaAGL33-D expression showed the strongest downregulation during vernalization, 478

which is maintained in post vernalization (Fig. 5C). This observation may suggest that 479

the TaAGL33 homeolog from the D subgenome acquired highest functional significance 480

in vernalization-dependent regulation of flowering time. Similar to our observations in 481

Brachypodium, the expression in response to cold first changes for TaAGL33-A and 482

only afterwards for TaVRN1 across the winter accessions (Fig. 5, Supplemental Fig. 4A 483

and 5B-D), emphasizing that prior to the onset of cold ODDSOC2/TaAGL33 is not 484

bound by VRN1. This is in line with the observation that vrn1 mutants do not affect 485

ODDSOC2 before vernalization (Greenup et al., 2010). 486

487

488



20

Discussion 489

Despite FLC being one of the most studied plant genes, orthologs of this flowering 490

repressor have only been recently identified in monocots (Ruelens et al., 2013). Now 491

with the perspective that it is a gene closely related to FLC, we go beyond previous 492

functional characterization of ODDSOC2 in barley by studying this gene in relation to 493

vernalization in Brachypodium (Greenup et al., 2010). We add a quantitative relation 494

between the vernalization length and ODDSOC2 expression before cold, a loss of 495

function phenotype, its early regulation before VRN1 and stable downregulation 496

associated with H3K27me3 spreading at the level of chromatin. In wheat, TaAGL33 497

transcripts, considered to be Type 1 MADS-box genes, had been observed to respond 498

to winter conditions (Winfield et al., 2009). We have added homeolog specific 499

expression and resolved the relation to the TaAGL22 transcript, alternatively generated 500

from the same locus. Based on previous and our data we postulate that ODDSOC2 501

functions as a flowering repressor in the vernalization-pathway of Pooideae similar to its 502

ortholog FLC in Brassicaceae. Here, we further discuss the similarities and differences 503

between these two homologs. 504

505

In Brassicaceae, the need for vernalization is overcome through the downregulation of 506

flowering repressor FLC in response to cold (Sheldon et al., 2000, Wang et al., 2009). 507

Moreover, winter Arabidopsis accessions have dominant FLC alleles while many rapid 508

cycling accessions have non-functional or weak FLC alleles suggesting FLC expression 509

levels determine the vernalization response in a quantitative way (Gazzani et al., 2003, 510

Michaels et al., 2003b, Sheldon et al., 2000, Shindo et al., 2005). Indeed, the 511

expression level of FLC in non-vernalized plants among naturally occurring accessions 512

shows a correlation with their respective vernalization requirement (Shindo et al., 2005). 513

Also in barley and wheat, ODDSOC2/TaAGL33 expression is higher in winter varieties 514

and low in spring varieties (Greenup et al., 2010, Winfield et al., 2009, Trevaskis et al., 515

2003). Similarly, we observe that ODDSOC2 expression before cold in different 516

Brachypodium accessions is correlated with vernalization length, i.e. the duration of cold 517

saturating the vernalization requirement. However, some Brachypodium accessions, 518

including accessions needing a long exposure to cold, exhibit relatively low pre-519



21

vernalization BdODDSOC2 expression levels suggesting additional factors mediate 520

vernalization length, which may be more or less important depending on the accession. 521

The overall strong correlation between ODDSOC2 levels before cold and vernalization 522

length does suggest that BdODDSOC2 expression before cold possibly plays a role in 523

setting the length of the vernalization requirement in a rheostatic manner, i.e. higher 524

ODDSOC2 transcript levels before cold result in a longer cold period needed to saturate 525

the vernalization requirement. Although previous studies have provided evidence that 526

VRN1 can regulate ODDSOC2 in barley and Brachypodium (Deng et al., 2015, Woods 527

et al., 2016), it is unlikely that BdODDSOC2 expression before cold is set by BdVRN1 528

since the latter is only transiently expressed before cold in a 16h-photoperiod and 529

BdODDSOC2 responds earlier than BdVRN1 to cold. In this manner, ODDSOC2 could 530

contribute to an adaptive mechanism by which distinct populations have evolved a 531

different vernalization length. However, it remains unclear how BdODDSOC2 532

expression before vernalization is set and whether this involves FRI-like genes like in 533

Arabidopsis (Michaels and Amasino, 1999). 534

535

Downregulation of FLC by vernalization has been extensively studied in Arabidopsis 536

where it is represents a universal mechanism to relieve the plant from FLC repression 537

after vernalization (Sheldon et al., 2000, Shindo et al., 2006). Previously, it has been 538

shown that ODDSOC2 is downregulated by cold in Brachypodium accession Bd21 and 539

Hordeum vulgare (Greenup et al., 2010, Ruelens et al., 2013). Conversely, our results 540

show that BdODDSOC2 downregulation is not widespread across Brachypodium 541

accessions with only 11 out of 25 accessions showing significant downregulation in 542

response to cold. By contrast, BdVRN1 is upregulated in all accession and significantly 543

increased during vernalization in 19 accessions. We hypothesized that the lack of a 544

uniform BdODDSOC2 response to cold might be linked to their vernalization 545

requirement, however neither the BdODDSOC2 response to cold nor its expression 546

level in vernalized plants could be linked to either spring or winter habit. Possibly, 547

ODDSOC2 functions differently in those accessions in which its expression is not 548

affected or upregulated by cold, or BdODDSOC2 repression might be achieved through 549

post-transcriptional mechanisms like FLM in Arabidopsis (Pose et al., 2013, Lee et al., 550



22

2013). Alternatively, differences in the response of BdODDSOC2 to cold among 551

accessions suggest that the molecular mechanism of its function is different from that of 552

FLC in Arabidopsis. Indeed, while FLC acts directly upon floral integrators FT and 553

SOC1, we found no evidence that BdODDSOC2 regulates BdVRN3 or BdSOC1. 554

555

An important aspect of FLC’s function in Arabidopsis is the ability to “remember” winter, 556

which is molecularly achieved through the addition of mitotically stable repressive 557

H3K27me3 histone marks at the FLC locus during vernalization (Angel et al., 2011, 558

Bastow et al., 2004, Sung and Amasino, 2004). Similar to FLC, downregulation of 559

BdODDSOC2 in Bd21 and BdTR3C in response to cold is associated with an increase 560

in H3K27me3 at the BdODDSOC2 locus indicating that BdODDSOC2 in these 561

accessions is epigenetically silenced. By contrast, in Hordeum downregulation of 562

ODDSOC2 during cold could not be associated with alteration of H3K27me3 levels 563

although in this case only a single region at the transcription start site was analyzed 564

(Greenup et al., 2010). However, to truly “remember” winter, it is important that when 565

the plants are returned to warm, these histone marks are retained or even spread 566

throughout the locus. Only in the case of BdTR3C, H3K27me3 marks were retained at 567

the BdODDSOC2 locus following cold exposure suggesting the vernalized state is 568

maintained at the BdODDSOC2 chromatin. Previously, it has been shown in Hordeum 569

that upregulation of VRN1 is associated with an increase in H3K4me3 and decrease in 570

H3K27me3 at the VRN1 chromatin (Oliver et al., 2009). Likewise in BdTR3C, 571

H3K27me3 marks decreased during cold exposure and were retained post-vernalization 572

indicating epigenetic upregulation of VRN1 is conserved throughout Pooideae. 573

Together, these results suggest that both ODDSOC2 and VRN1 might be involved in 574

remembering winter in Brachypodium. However, the fact that not all Brachypodium 575

winter accessions exhibit downregulation of ODDSOC2 indicates that the epigenetic 576

regulation of winter memory cannot be –even partially– through ODDSOC2 in all 577

accessions. Furthermore, in the spring accession KU104-2 of Triticum monococcum, 578

TmODDSOC2 repression in vernalized plants is only maintained when TmVRN1 is 579

present (Greenup et al., 2010). Future research in winter accessions of Brachypodium 580



23

will help further elucidate the role of VRN1 and ODDSOC2 in the memory of 581

vernalization in Pooideae. 582

583

Complementary with the overall expression pattern of ODDSOC2 in Brachypodium, we 584

show that BdODDSOC2 acts as a repressor of flowering through vernalization. Plants 585

overexpressing BdODDSOC2 exhibited delayed flowering when vernalized. Since 586

overexpression plants flowered at the same time as wild type Bd21-3 plants without 587

vernalization, BdODDSOC2 overexpression plants are rendered unresponsive to 588

vernalization. BdODDSOC2 RNAi lines flowered earlier than control plants when grown 589

without vernalization treatment. In contrast to the overexpression phenotype, these 590

early flowering lines are still vernalization responsive. This partial phenotype could be 591

the results of the limitations of RNAi knockdown and a more pronounced effect could 592

possibly be demonstrated using a full knockout, e.g. via the CRISPR-Cas9 system. 593

Alternatively, the partial effect might indicate that additional pathways, likely involving 594

other vernalization regulators, control the vernalization response in Brachypodium. A 595

previous study already demonstrated that the functions of VRN1 and VRN3 are 596

conserved between Brachypodium and cereals suggesting that the VRN1-VRN3 597

regulatory interaction of the vernalization pathway is likewise conserved (Ream et al., 598

2014). Moreover, it was shown that BdVRN1 knockdown in Bd21-3 resulted in 599

increased ODDSOC2 levels and in Hordeum vulgare cv. Golden Promise HvVRN1 can 600

bind to the promoter of HvODDSOC2 (Deng et al., 2015, Woods et al., 2016). In 601

addition, winter Hordeum with low basal VRN1 expression exhibit high expression of 602

ODDSOC2 (Deng et al., 2015). These data suggest that ODDSOC2 is downstream of 603

VRN1, which together with the fact that altered BdODDSOC2 levels do not affect 604

BdVRN3 transcript levels indicate that a VRN1-ODDSOC2 interaction might regulate 605

vernalization-induced flowering parallel to the floral integrator VRN3. Another line of 606

evidence for a pathway parallel to VRN1-VRN3 is the observation that BdODDSOC2 607

overexpression plants flower similar to non-vernalized wild type plants. This observation 608

is very different from Arabidopsis where overexpression of FLC delays flowering even 609

without vernalization (Michaels and Amasino, 1999). However in Arabidopsis, FLC 610

represses two central flowering integrators preventing parallel pathways to induce 611



24

flowering. As BdODDSOC2 does not target BdVRN3, the photoperiod pathway possibly 612

takes over. This might be specific to Bd21-3, which has a strong photoperiod pathway 613

that could override the repression by ODDSOC2 (Ream et al., 2014). Such a 614

mechanism might represent a fail-safe system, allowing flowering following an unusually 615

mild winter. 616

617

To explore the extent by which our results in Brachypodium can be translated to wheat, 618

an economically important crop, we performed expression analyses of ODDSOC2 619

homologs in different Triticum aestivum accessions. We show that specifically TaAGL33 620

and its splice variant TaAGL22 are stably downregulated in response to prolonged cold 621

in the majority of Triticum accessions. Additionally, in winter Triticum accessions 622

TaAGL33 and TaAGL22 expression is high before cold while their expression is low in 623

spring accessions suggesting that these genes function similar to ODDSOC2 in 624

Brachypodium. This pattern was most pronounced for TaAGL22 and TaAGL33 625

transcribed from the D subgenome. As the introduction of the D genome resulted in a 626

broader radiation of hexaploid Triticum aestivum into temperate regions than its 627

tetraploid progenitor, which is mostly cultivated in semi-arid regions (Dubcovsky and 628

Dvorak, 2007), it is interesting to speculate that the introduction of TaAGL22-D and 629

TaAGL33-D might have contributed in part to the increased adaptability to more 630

temperate climates. Similar results were obtained from genome-wide expression 631

analysis of the floral transition in wheat, in which a TaAGL33 transcript was higher in 632

two winter wheat varieties than in a spring accession. Expression of TaAGL33 declined 633

after five weeks, already suggesting TaAGL33 is a repressor of flowering (Winfield et 634

al., 2009). 635

636

Together with previous results from barley (Greenup et al., 2010), our results suggest 637

that ODDSOC2’s role as a repressor of flowering is conserved among core Pooideae, 638

which include important cereal crops such as wheat, oats and rye. In a larger 639

evolutionary context, it is interesting to note that ODDSOC2’s homolog in rice, 640

OsMADS51, functions as short-day promoter of flowering (Kim et al., 2007). Given their 641

close relationship to core eudicot FLC-like genes, it is most parsimonious to assume 642



25

that the promoter function of OsMADS51 evolved independently after the Oryzoideae 643

branched off from the stem lineage towards the Pooideae. This model in which a 644

promoter function evolved from an ancestral repressor function does not have to be 645

surprising as the FLC clade itself is sister to the APETALA1 (AP1) clade which includes 646

flowering promoters AP1 in Arabidopsis and VRN1 in Pooideae (Ruelens et al., 2013). 647

Other examples of flowering regulators switching between a repressing or promoting 648

function include BvFT1 and BvFT2 in beet and AGL24 and SVP in core eudicots 649

(Hartmann et al., 2000, Michaels et al., 2003a, Pin et al., 2010). Since VRN1 also 650

confers vernalization responsiveness and given the FLC/ODDSOC2-VRN1/AP1 651

phylogenetic sister relationship (Ruelens et al., 2013), one could speculate that the 652

absence of a vernalization role for AP1, and its paralogs FUL and AGL79, in 653

Arabidopsis, is derived from an ancestral AP1/VRN1 gene functioning in vernalization-654

mediated flowering before the monocot-dicot split, similar to VRN1 in Poaceae. 655

656

In conclusion, our findings suggest a key role for ODDSOC2 in the vernalization 657

response of Brachypodium and identify TaAGL33 as a good candidate for performing a 658

similar function in wheat. We highlight the previously underestimated similarities 659

between FLC in Arabidopsis and ODDSOC2/TaAGL33 in monocots, which sheds light 660

on the evolution of the vernalization mediated flowering. The provided knowledge can 661

possibly be utilized in the future for crop improvement in order to adapt the vernalization 662

requirement of elite varieties to changing climates. Key future questions to be 663

addressed are whether the molecular mechanisms regulating ODDSOC2 are also 664

similar to FLC in Arabidopsis and how ODDSOC2 exactly represses flowering. 665

666

667

Material and Methods 668

Plant materials and growth conditions of expression study in a set of 669

Brachypodium accessions 670

Information on the accessions used in this study is given in Supplemental Table 1. 671

Seeds of these accessions were obtained from the USDA germplasm, Dr. David Garvin 672

or Dr. Luis Mur after which seeds were propagated in house (Filiz et al., 2009, Mur et 673



26

al., 2011, Vogel et al., 2006). Seeds were first incubated during 24 hours at 23°C in the 674

dark on a Petri dish with filter paper and 2 ml of distilled water to ensure synchronous 675

germination. Imbibed seeds were sown in Slim Rootrainers™ pots filled with a 50:50 676

mix of soil and vermiculite and placed in a growth chamber at 23°C with a 16h-8h light-677

dark cycle and a light intensity of ~60 µmol m-2 s-1 at ground level produced by four 678

fluorescent tubes (two Philips Master TL-D 36W/830 and two Osram L 36W 840 G13 679

Lumilux cool white lights). After three weeks, plants were transferred for vernalization to 680

a Conviron at 4°C and a short-day photoperiod of 8h light and 16h dark. We chose to 681

vernalize during vegetative growth (three-week-old plants) as this represents a realistic 682

growth scenario for winter-annuals (Chouard, 1960). Following this cold treatment, 683

plants were returned to the growth chamber at 23°C with a 16h-8h light-dark cycle. 684

Flowering time was measured as the number of days from return to warm conditions 685

until the spike was approximately 1cm emerged from the plant. For non-vernalized 686

plants, days-to-flowering was between three weeks of age and spike emergence. 687

Accessions were classified into different vernalization classes based on how effective a 688

specific length of cold (weeks: 0, 2, 4, 6, 10, 12) could accelerate flowering 689

(Supplemental Table 1). For expression analysis of BdODDSOC2 and BDVRN1 in NV, 690

V, PV and extended PV (1wPV to 7wPV) in Bd21 and BdTR3C, short-day photoperiod 691

of 8h light and 16h dark were used. Primers used for downstream target of 692

BdODDSOC2 are listed in Supplemental Table 3. 693

694

Generation of BdODDSOC2 overexpression and RNAi transgenic plants 695

Generation of BdODDSOC2 overexpression construct was done by introducing full 696

length BdODDSOC2 cDNA (from accession Bd21-3) into Gateway cloning vector 697

pIPKb002 (Invitrogen). To clone RNAi hairpin construct, gateway cloning vector 698

pIPKb007 was used (Himmelbach et al., 2007). In both vectors transgene expression is 699

driven by the Zea mays (maize) UBIQUITIN promoter. BdODDSOC2 overexpression 700

and RNAi construct were transformed in Brachypodium accession Bd21-3 using 701

Agrobacterium tumefaciens-mediated transformation. We obtained 17 BdODDSOC2 702

overexpression lines. Ten lines with maximum seed yield were chosen for functional 703

characterization. Out of these ten, eight lines were generated from independent 704



27

transformation events while lines 11.1 and 17.1 derived from distinct shoots from the 705

same callus of event 11 and 17 respectively. For BdODDSOC2 RNAi, we generated 23 706

RNAi-mediated knockdown lines, from which 10 lines with maximum seed yield were 707

selected for further study. Out of ten, nine lines were derived from independent 708

transformation events, but line 2.1 was generated from the same callus as line 2, but 709

from a different shoot. 710

711

Phenotyping of transgenic lines 712

Transgenic plants were grown same as plants for expression analysis. T1 plants were 713

screened for the segregation of transgene. Phenotyping was done with T2 plants. Plants 714

which carried the transgene in T2 were only used for the analysis. Seeds from plants 715

without the transgene in T0 were used as non-transgenic control plants. Wild-type Bd21-716

3 plants were used as a second control to compare days to heading and final leaf 717

number. Final leaf number referred to the total number of leaves including those on 718

tillers on the entire plant on the day flowering became visible. 719

All transgenic plants were genotyped by PCR using ZmUBI promoter forward primer (F: 720

5’-TTCCGCAGACGGGATCGATCTAGG-3’) and BdODDSOC2 reverse primer (R: 5’-721

ATCAGTGTTTGCCCACCACCC-3’). Plants that carried the transgene were used for 722

phenotyping. Days to heading were calculated from the day the seed was planted until 723

the appearance of the first inflorescence. 724

725

RNA extraction and qRT-PCR of Brachypodium 726

Samples for total RNA isolation consisted of all above-ground tissues which were snap 727

frozen in liquid nitrogen and stored at -80°C. RNA was extracted using TRIzol according 728

to the manufacturer's instructions (Invitrogen, Carlsbad, USA). To remove any genomic 729

DNA, total RNA was DNase treated with TURBO DNA-free (Ambion, Austin, USA). RNA 730

quality and quantity was analyzed by spectrophotometer. cDNA was synthesized from 731

1μg total RNA by reverse transcription using AMV reverse transcriptase (Promega, 732

Madison, USA). qRT–PCR was performed using 10ng of cDNA on a StepOne Plus 733

(Applied Biosystems, Foster City, USA) with Fast SYBR Green Master Mix following the 734

manufacturer's protocol (Applied Biosystems, Foster City, USA). Relative expression 735



28

levels were calculated using the delta-delta Ct method using UBC18 (ubiquitin-736

conjugating enzyme 18) as a reference gene. The reference sample used depends on 737

the experiment. BdODDSOC2 and BdVRN1 expression levels in the natural variation 738

experiment are relative to a non-vernalized Bd3-1 sample. For expression analysis in 739

Bd21-3, NV plant sample was used as the reference. 740

The following primers were used for qRT-PCR: 741

UBC18: F: 5′-GTCGACTTCCCCGAGCATTA-3′, 742

R: 5′-ATAGGCGCCGGGTTGAG-3′ 743

BdODDSOC2: F: 5′-AAATCCAAGATATTGGCAAAACG-3′, 744

R: 5′-CCTTAGGCTCACTGGAGTTCTCA-3′ 745

BdVRN1: F: 5’-ACCAAGGGCAAGCTCTACGA-3’, 746

R: 5’-GTAGCGCTCATAGCGTTCAAGA-3’ 747

748

Chromatin Immunoprecipitation (ChIP) 749

ChIP was performed as previously described (Kaufmann et al., 2010) using whole plant 750

tissue (without root). Plants were grown under a short-day photoperiod of 8h light and 751

16h dark for NV, V and PV. S-adenosylmethionine decarboxylase (SamDC) gene was 752

used as a reference gene, as this gene was reported as most stable in plants grown 753

under various environmental stress (Hong et al., 2008). The anti-H3K27me3 antibody 754

was obtained from Millipore (Cat. #07-449). Sequences of primers used in ChIP are 755

listed in Supplemental Table 3. 756

757

Semiquantitative RT-PCR 758

Three leaves were collected from T0 transgenic plants. RNA isolation and cDNA 759

preparation was performed as mentioned previously. 10ng of cDNA was used to 760

perform Semiquantitative RT-PCR. Actin was used as the endogenous control to 761

compare expression of transgene. To detect BdODDSOC2 level in overexpression lines 762

32 cycles were used for PCR amplification. For BdODDSOC2 RNAi lines, PCR reaction 763

was done with 35 cycles. Primers used for semi qRT-PCR were as follow. 764

BdODDSOC2: F: 5′-CAGGTGCGCTTCTCCAAG-3′, 765

R: 5′-CTGTCCCTTAGGCTCACTGG-3′ 766



29

ACTIN: F: 5′-GATGGATCCTCCAATCCAGACACTGTA-3′, 767

R: 5′-GTATTGTGTTGGACTCTGGTGATGGTGT-3′ 768

769

Statistics 770

Student’s t-test were performed in excel or R. Linear regressions and Pearson 771

correlation tests were performed in R. 772

773

Wheat vernalization and expression experiment 774

Seedlings of ten wheat lines, with differentiation in winter and spring growth habit, were 775

grown for three weeks at 21°C in long-day conditions (16-h light/8-h dark). After three 776

weeks, seedlings were exposed to either no vernalization or to vernalization treatments 777

of four or eight weeks in a climate chamber at 4°C (12-h light/12-h dark). Afterwards 778

seedlings were transferred to the greenhouse under long days (16-h light/8-h dark, with 779

supplementary lighting when natural light levels dropped below 200 μE). The 780

vernalization treatments were staggered in reverse order, such that all lines entered the 781

greenhouse at the same time. Flowering time was measured as the number of days 782

from return to warm conditions until the spike had emerged. For non-vernalized plants, 783

days to flowering was between three weeks of age and spike emergence. 784

785

RNA extraction and qRT-PCR for Triticum genes 786

Total RNA was isolated using the RNeasy® Plant Mini Kit (Qiagen). After TURBO DNA-787

freeTM treatment, 500ng of RNA was used for cDNA synthesis reaction using RNA to 788

cDNA EcoDry™ Premix (TAKARA Clontech). Gene expression was carried out in two 789

steps. First, sequences were preamplified in a sequence-specific manner using 1,5µl 790

cDNA (25ng/µl), as described in the PreAmp with Fluidigm® PreAmp Master Mix and 791

TaqMan® Assays (PN 100-5876 B1) protocols (www.lifetechnologies.com). In a second 792

step, high-throughput quantitative PCR was carried out using a 1:5 diluted pre-793

amplification product, following the 96.96 IFC Using Standard TaqMan® Assays (PN 794

68000130 D1) protocol (www.fluidigm.com/documents), using the BioMark™ System for 795

fluorescence detection. 796

797



30

Cycling threshold values were calculated with Fluidigm® Real-Time PCR Analysis 798

Software v4.1.2. For further qRT-PCR data analysis, the expression data were 799

normalized using the delta-delta Ct method against the control gene using the 800

Biogazelle qBase+ v2.6.1 software. Transcript levels for ODDSOC2 homologs were 801

monitored in leaves of 3-week-old seedlings, after four and eight weeks of vernalization 802

and two and four weeks post vernalization using quantitative real-time reverse 803

transcription qRT-PCR with TaqMan® assays. The (homeolog-specific) primer and 804

probe sequences for each target gene and the stably expressed control gene 68 kDa 805

protein HP68 (Ta.2776) control gene (Paolacci et al., 2009), are listed in Supplemental 806

Table 2 . 807

808 Acknowledgments 809

This research was supported by FWO grant G065713N from which NS was supported. 810

PR was supported by a fellowship from IWT and currently holds a postdoctoral 811

fellowship from the KU Leuven (PDM/15/104). ND is supported by an IWT fellowship. 812

We thank Anja Vandeperre (KU Leuven) and Véronique Gosselé (Bayer Crop Science) 813

for technical assistance. 814

815

Conflict of interest: KG, KK and PR authored a patent relating to this work 816

(PCT/EP2014/063985). 817

818

Figure Legends 819

Figure 1. BdODDSOC2 response to cold in a set of Brachypodium distachyon 820

accessions. A. Heat map showing the response of BdODDSOC2 and BdVRN1 gene 821

expression in different Brachypodium distachyon accessions following a four week cold 822

period (4wV) relative to the expression prior to vernalization (NV) (log10 fold change). 823

Vern. R. depicts the vernalization requirement in weeks (w) as assessed in this study. 824

B. Expression pattern of BdODDSOC2 during prolonged cold in selected Brachypodium 825

accessions. Bars represent the standard error of mean of 3-5 biological replicates. 826

Asterisks are indicated when p-value < 0.05 of a student’s t-test between NV (0 weeks 827

of cold) and vernalized samples. C. Relationship between vernalization requirement and 828



2

expression of BdODDSOC2 in non-vernalized plants and BdVRN1 of plants grown 829

during a four week cold period. Each dot represents the mean of BdODDSOC2 or 830

BdVRN1 relative expression of 2-5 biological replicates. R2 and p depicts the square of 831

the Pearson correlation coefficient and its associated p-value respectively. The solid 832

lines represent linear regression trend lines. NV: non-vernalized three week old plants, 833

4wV: during a vernalization period of four weeks. The red dot in the upper panel 834

highlights BdODDSOC2 expression in Brachypodium Bd21-3. 835

836

Figure 2: BdODDSOC2 as a repressor of flowering. A. Days to heading for wild type 837

Bd21-3 without and with vernalization (NV and V), B. BdODDSOC2 expression in NV, 838

2wV and 1wPV. C-D. Days to heading for BdODDSOC2 overexpression without 839

vernalization (NV, C.) and with two weeks vernalization treatment (V, D.). E-F. Days to 840

heading for BdODDSOC2 RNAi lines in NV (E.) and with vernalization (F.). G-H. Final 841

leaf number for BdODDSOC2 overexpression (NV, G.) and with vernalization (H.). I-J 842

Final leaf number for BdODDSOC2 RNAi (NV, I.) and with V (J.). Asterisks indicate p-843

value of Student's t-test: * p<0.05,** p<0.01, ***p<0.001. The t-tests were conducted to 844

compare transgenic lines with both non-transgenic control (NC) and wild type Bd21-3. 845

Error bars represent s.e.m. of four biological replicates for BdODDSOC2 expression 846

and for phenotyping s.e.m of 4-15 biological replicates. 847

848

Figure 3: Expression of BdODDSOC2 and BdVRN1 in response to vernalization 849

and H3K27me3 histone modifications at BdODDSOC2 and BdVRN1 in Bd21 and 850

BdTR3C. A-B. Expression of BdODDSOC2 and BdVRN1 before cold (NV), after 0, 6, 851

12, 24 and 48 hours of cold in BdTR3C. C-D. Expression of BdODDSOC2 and BdVRN1 852

in Bd21 E-F. BdODDSOC2 and BdVRN1 in BdTR3C, before cold (NV), after two (Bd21) 853

and six weeks (BdTR3C) of cold and after 1, 2, 3, 4, 5, 6, 7 weeks of return to warm 854

temperatures (1wPV, 2wPV, 3wPV, 4wPV, 5wPV, 6wPV, 7wPV). G-H. Schematic 855

representation of BdODDSOC2 and BdVRN1 locus. I-J. Relative enrichment of 856

H3K27me3 at BdODDSOC2 and BdVRN1 in Bd21. K-L. H3K27me3 at BdODDSOC2 857

and BdVRN1 in BdTR3C. Asterisks indicate p-value of Student's t-test: * p<0.05,** 858

p<0.01, ***p<0.001. The t-tests were conducted to compare non-vernalized with 859



3

vernalized and postvernalized plants. Error bars represent s.e.m. of four biological 860

replicates for BdODDSOC2 and BdVRN1 expression and for H3K27me3 ChIP s.e.m of 861

2-5 biological replicates. 862

863

Figure 4: FLC-like genes in Triticum aestivum. Genomic localization of ODDSOC1 864

(TaAGL42) and ODDSOC2 (TaAGL22, TaAGL33, TaAGL41) homologs. MADS37 865

ortholog, TaAGL12, is not shown. Inset. Schematic representation of the locus encoding 866

both TaAGL22 and TaAGL33 on pseudochromosome 3B. 867

868

Figure 5: Expression of FLC homologs in response to vernalization in Triticum 869

varieties. A. Sparkline plots showing the expression pattern of VRN and FLC-like 870

genes in 10 different Triticum accession in response to vernalization. VRN1-A, VRN2, 871

VRN3 expression is shown prior to vernalization (NV), after two, four, six and eight 872

weeks of vernalization (2wV, 4wV, 6wV, 8wV) and two and four weeks post 873

vernalization (2wPV, 4wPV). Expression of ODDSOC1/2 genes was assayed prior to 874

vernalization (NV), after four and eight weeks of vernalization (4wV, 8wV) and two and 875

four weeks post vernalization (2wPV, 4wPV). Individual plots with standard error of 876

mean are shown in Supplemental Figure 4 and 5. N/A (Not Available) refers to samples 877

for which expression patterns were not reproducible. B. Box plots comparing the relative 878

expression levels of TaAGL22 and TaAGL33 homeologs in NV between winter and 879

spring Triticum varieties. Student’s t-test was used to compare between groups and 880

resulting p-values are shown above each plot. C. TaAGL33-D expression after four and 881

eight weeks of vernalization (4wV, 8wV) and two and four weeks post vernalization 882

(2wPV, 4wPV). 883

884

Table 1. Vernalization requirement of Triticum varieties used in this study. 885

886

Supplemental information 887 Supplemental Figure 1. Expression of BdODDSOC2 in transgenic lines using 888

semiquantitative PCR. 889

Supplemental Figure 2. Days to heading and leaf number for BdODDSOC2 890

overexpression and RNAi lines. 891



4

Supplemental Figure 3: Phylogenetic tree representing the relationships between 892

angiosperm FLC genes using SQUAMOSA-like genes as the outgroup. 893

Supplemental Figure 4. Expression of VRN1-A homologs prior to vernalization. 894

Supplemental Figure 5. Expression of wheat ODDSOC2 homologs in response to 895

vernalization in different Triticum aestivum varieties. 896

Supplemental Figure 6. Expression analysis of putative targets of BdODDSOC2 in 897

overexpression (line 3 and 11.1) and RNAi (line 4 and 5) in NV, V and PV. 898

Supplemental Table 1. Brachypodium accessions used in this study and vernalization 899

requirement assessed by this study. 900

Supplemental Table 2. List of primer/probe for target genes in Triticum. 901

Supplemental Table 3. List of primers used in the H3K27me3 ChIP and downstream 902

target of BdODDSOC2. 903

904

905

Supplemental Figure 1. Expression of BdODDSOC2 in transgenic lines using 906

semiquantitative PCR. A. BdODDSOC2 overexpression lines. B. BdODDSOC2 RNAi 907

lines. 908

909

Supplemental Figure 2. Days to heading and leaf number for BdODDSOC2 910

overexpression and RNAi lines. A-B. Days to heading for BdODDSOC2 overexpression 911

without vernalization (NV), with vernalization (V). C-D. Days to heading for 912

BdODDSOC2 RNAi NV, with V. E-F. Final leaf number for BdODDSOC2 913

overexpression NV, with V. G-H. Final leaf number for BdODDSOC2 RNAi in NV, with 914

V. Asterisks indicate p-value of Student's t-test: * p<0.05,** p<0.01, ***p<0.001. The t-915

tests were conducted to compare transgenic lines with both non-transgenic control (NC) 916

and wild type Bd21-3. Error bars represent s.e.m. of four biological replicates for 917

BdODDSOC2 expression and for phenotyping s.e.m of 4-15 biological replicates. 918

919

Supplemental Figure 3: Phylogenetic tree representing the relationships between 920

angiosperm FLC genes using SQUAMOSA-like genes as the outgroup. Numbers next 921

to each node indicate bootstrap support values of 100 non-parametric bootstraps. 922



5

Phylogenetic analysis was performed with PhyML 3.0. Dataset from (24) supplemented 923

with additional sequences using BLAST. 924

925

Supplemental Figure 4. Expression of VRN1-A homologs prior to vernalization (NV), 926

after two, four, six and eight weeks of vernalization (2wV, 4wV, 6wV, 8wV), and two and 927

four weeks post vernalization (2wPV, 4wPV) in different Triticum aestivum varieties. 928

Error bar represent standard error of mean of four biological replicates. 929

930

Supplemental Figure 5. Expression of wheat ODDSOC2 homologs in response to 931

vernalization in different Triticum aestivum varieties. A. TaAGL41, B. TaAGL33-A, C. 932

TaAGL33-B, D. TaAGL33-D, E. TaAGL22-A, F. TaAGL22-B, G. TaAGL22-D, prior to 933

vernalization (NV), after four and eight weeks of vernalization 4wV, 8wV and two and 934

four weeks of post vernalization 2wPV, 4wPV. Error bar represent standard error of the 935

mean of 2-4 biological replicates. 936

937

Supplemental Figure 6. Expression analysis of putative targets of BdODDSOC2 in 938

overexpression (line 3 and 11.1) and RNAi (line 4 and 5) in NV, V and PV. A. 939

BdODDSOC2 in overexpression lines, B. BdODDSOC2 in RNAi lines, C. BdVRN1, D. 940

BdVRN2, E. BdVRN3, F. BdFPF1, G. BdSOC1, prior to vernalization (NV), after two 941

weeks of vernalization (V) and two weeks of post vernalization (PV). Asterisks indicate 942

p-value of Student's t-test: * p<0.05,** p<0.01, ***p<0.001. t-test was conducted by 943

comparing transgenic lines with non-transgenic control (NC). Error bar represent 944

standard error of the mean of 3-4 biological replicates. 945

946

Supplemental Table 1. Brachypodium accessions used in this study and vernalization 947

requirement assessed by this study. 948

949

Supplemental Table 2. List of primer/probe for target genes in Triticum. 950

951

Supplemental Table 3. List of primers used in the H3K27me3 ChIP and downstream 952

target of BdODDSOC2. 953

954



1

955



Parsed CitationsALEXANDRE, C. M. & HENNIG, L. 2008. FLC or not FLC: the other side of vernalization. J Exp Bot, 59, 1127-35.

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

ANGEL, A., SONG, J., DEAN, C. & HOWARD, M. 2011. A Polycomb-based switch underlying quantitative epigenetic memory. Nature,476, 105-8.


BARSKI, A., CUDDAPAH, S., CUI, K., ROH, T. Y., SCHONES, D. E., WANG, Z., WEI, G., CHEPELEV, I. & ZHAO, K. 2007. High-resolution profiling of histone methylations in the human genome. Cell, 129, 823-37.


BASTOW, R., MYLNE, J. S., LISTER, C., LIPPMAN, Z., MARTIENSSEN, R. A. & DEAN, C. 2004. Vernalization requires epigeneticsilencing of FLC by histone methylation. Nature, 427, 164-7.


CAVANAGH, C. R., CHAO, S., WANG, S., HUANG, B. E., STEPHEN, S., KIANI, S., FORREST, K., SAINTENAC, C., BROWN-GUEDIRA,G. L., AKHUNOVA, A., SEE, D., BAI, G., PUMPHREY, M., TOMAR, L., WONG, D., KONG, S., REYNOLDS, M., DA SILVA, M. L.,BOCKELMAN, H., TALBERT, L., ANDERSON, J. A., DREISIGACKER, S., BAENZIGER, S., CARTER, A., KORZUN, V., MORRELL, P.L., DUBCOVSKY, J., MORELL, M. K., SORRELLS, M. E., HAYDEN, M. J. & AKHUNOV, E. 2013. Genome-wide comparative diversityuncovers multiple targets of selection for improvement in hexaploid wheat landraces and cultivars. Proc Natl Acad Sci U S A, 110,8057-62.


CHEN, A. & DUBCOVSKY, J. 2012. Wheat TILLING mutants show that the vernalization gene VRN1 down-regulates the floweringrepressor VRN2 in leaves but is not essential for flowering. PLoS Genet, 8, e1003134.


CHOUARD, P. 1960. Vernalization and Its Relations to Dormancy. Annual Review of Plant Physiology and Plant Molecular Biology,11, 191-238.


CHOULET, F., ALBERTI, A., THEIL, S., GLOVER, N., BARBE, V., DARON, J., PINGAULT, L., SOURDILLE, P., COULOUX, A., PAUX,E., LEROY, P., MANGENOT, S., GUILHOT, N., LE GOUIS, J., BALFOURIER, F., ALAUX, M., JAMILLOUX, V., POULAIN, J., DURAND,C., BELLEC, A., GASPIN, C., SAFAR, J., DOLEZEL, J., ROGERS, J., VANDEPOELE, K., AURY, J. M., MAYER, K., BERGES, H.,QUESNEVILLE, H., WINCKER, P. & FEUILLET, C. 2014. Structural and functional partitioning of bread wheat chromosome 3B.Science, 345, 1249721.


DANYLUK, J., KANE, N. A., BRETON, G., LIMIN, A. E., FOWLER, D. B. & SARHAN, F. 2003. TaVRT-1, a putative transcription factorassociated with vegetative to reproductive transition in cereals. Plant Physiol, 132, 1849-60.


DE LUCIA, F., CREVILLEN, P., JONES, A. M., GREB, T. & DEAN, C. 2008. A PHD-polycomb repressive complex 2 triggers theepigenetic silencing of FLC during vernalization. Proc Natl Acad Sci U S A, 105, 16831-6.


DENG, W., CASAO, M. C., WANG, P., SATO, K., HAYES, P. M., FINNEGAN, E. J. & TREVASKIS, B. 2015. Direct links between thevernalization response and other key traits of cereal crops. Nat Commun, 6, 5882.


DENNIS, E. S. & PEACOCK, W. J. 2009. Vernalization in cereals. J Biol, 8, 57.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title


http://www.ncbi.nlm.nih.gov/pubmed?term=ALEXANDRE%2C C%2E M%2E %26 HENNIG%2C L%2E 2008%2E FLC or not FLC%3A the other side of vernalization%2E J Exp Bot%2C 59%2C 1127%2D35%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=ALEXANDRE, C. M. & HENNIG, L. 2008. FLC or not FLC: the other side of vernalization. J Exp Bot, 59, 1127-35.

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

http://scholar.google.com/scholar?as_q=FLC or not FLC: the other side of vernalization&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=FLC or not FLC: the other side of vernalization&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=ALEXANDRE,&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=ANGEL%2C A%2E%2C SONG%2C J%2E%2C DEAN%2C C%2E %26 HOWARD%2C M%2E 2011%2E A Polycomb%2Dbased switch underlying quantitative epigenetic memory%2E Nature%2C 476%2C 105%2D8%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=ANGEL, A., SONG, J., DEAN, C. & HOWARD, M. 2011. A Polycomb-based switch underlying quantitative epigenetic memory. Nature, 476, 105-8.

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

http://scholar.google.com/scholar?as_q=A Polycomb-based switch underlying quantitative epigenetic memory&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 Polycomb-based switch underlying quantitative epigenetic memory&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=ANGEL,&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=BARSKI%2C A%2E%2C CUDDAPAH%2C S%2E%2C CUI%2C K%2E%2C ROH%2C T%2E Y%2E%2C SCHONES%2C D%2E E%2E%2C WANG%2C Z%2E%2C WEI%2C G%2E%2C CHEPELEV%2C I%2E %26 ZHAO%2C K%2E 2007%2E High%2Dresolution profiling of histone methylations in the human genome%2E Cell%2C 129%2C 823%2D37%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=BARSKI, A., CUDDAPAH, S., CUI, K., ROH, T. Y., SCHONES, D. E., WANG, Z., WEI, G., CHEPELEV, I. & ZHAO, K. 2007. High-resolution profiling of histone methylations in the human genome. Cell, 129, 823-37.

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

http://scholar.google.com/scholar?as_q=High-resolution profiling of histone methylations in the human genome&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=High-resolution profiling of histone methylations in the human genome&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=BARSKI,&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=BASTOW%2C R%2E%2C MYLNE%2C J%2E S%2E%2C LISTER%2C C%2E%2C LIPPMAN%2C Z%2E%2C MARTIENSSEN%2C R%2E A%2E %26 DEAN%2C C%2E 2004%2E Vernalization requires epigenetic silencing of FLC by histone methylation%2E Nature%2C 427%2C 164%2D7%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=BASTOW, R., MYLNE, J. S., LISTER, C., LIPPMAN, Z., MARTIENSSEN, R. A. & DEAN, C. 2004. Vernalization requires epigenetic silencing of FLC by histone methylation. Nature, 427, 164-7.

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

http://scholar.google.com/scholar?as_q=Vernalization requires epigenetic silencing of FLC by histone methylation&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=Vernalization requires epigenetic silencing of FLC by histone methylation&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=BASTOW,&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=CAVANAGH%2C C%2E R%2E%2C CHAO%2C S%2E%2C WANG%2C S%2E%2C HUANG%2C B%2E E%2E%2C STEPHEN%2C S%2E%2C KIANI%2C S%2E%2C FORREST%2C K%2E%2C SAINTENAC%2C C%2E%2C BROWN%2DGUEDIRA%2C G%2E L%2E%2C AKHUNOVA%2C A%2E%2C SEE%2C D%2E%2C BAI%2C G%2E%2C PUMPHREY%2C M%2E%2C TOMAR%2C L%2E%2C WONG%2C D%2E%2C KONG%2C S%2E%2C REYNOLDS%2C M%2E%2C DA SILVA%2C M%2E L%2E%2C BOCKELMAN%2C H%2E%2C TALBERT%2C L%2E%2C ANDERSON%2C J%2E A%2E%2C DREISIGACKER%2C S%2E%2C BAENZIGER%2C S%2E%2C CARTER%2C A%2E%2C KORZUN%2C V%2E%2C MORRELL%2C P%2E L%2E%2C DUBCOVSKY%2C J%2E%2C MORELL%2C M%2E K%2E%2C SORRELLS%2C M%2E E%2E%2C HAYDEN%2C M%2E J%2E %26 AKHUNOV%2C E%2E 2013%2E Genome%2Dwide comparative diversity uncovers multiple targets of selection for improvement in hexaploid wheat landraces and cultivars%2E Proc Natl Acad Sci U S A%2C 110%2C 8057%2D62%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=CAVANAGH, C. R., CHAO, S., WANG, S., HUANG, B. E., STEPHEN, S., KIANI, S., FORREST, K., SAINTENAC, C., BROWN-GUEDIRA, G. L., AKHUNOVA, A., SEE, D., BAI, G., PUMPHREY, M., TOMAR, L., WONG, D., KONG, S., REYNOLDS, M., DA SILVA, M. L., BOCKELMAN, H., TALBERT, L., ANDERSON, J. A., DREISIGACKER, S., BAENZIGER, S., CARTER, A., KORZUN, V., MORRELL, P. L., DUBCOVSKY, J., MORELL, M. K., SORRELLS, M. E., HAYDEN, M. J. & AKHUNOV, E. 2013. Genome-wide comparative diversity uncovers multiple targets of selection for improvement in hexaploid wheat landraces and cultivars. Proc Natl Acad Sci U S A, 110, 8057-62.

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

http://scholar.google.com/scholar?as_q=Genome-wide comparative diversity uncovers multiple targets of selection for improvement in hexaploid wheat landraces and cultivars&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Genome-wide comparative diversity uncovers multiple targets of selection for improvement in hexaploid wheat landraces and cultivars&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=CAVANAGH,&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=CHEN%2C A%2E %26 DUBCOVSKY%2C J%2E 2012%2E Wheat TILLING mutants show that the vernalization gene VRN1 down%2Dregulates the flowering repressor VRN2 in leaves but is not essential for flowering%2E PLoS Genet%2C 8%2C e1003134%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=CHEN, A. & DUBCOVSKY, J. 2012. Wheat TILLING mutants show that the vernalization gene VRN1 down-regulates the flowering repressor VRN2 in leaves but is not essential for flowering. PLoS Genet, 8, e1003134.

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=Wheat TILLING mutants show that the vernalization gene VRN1 down-regulates the flowering repressor VRN2 in leaves but is not essential for 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=Wheat TILLING mutants show that the vernalization gene VRN1 down-regulates the flowering repressor VRN2 in leaves but is not essential for flowering&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=CHEN,&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=CHOUARD%2C P%2E 1960%2E Vernalization and Its Relations to Dormancy%2E Annual Review of Plant Physiology and Plant Molecular Biology%2C 11%2C 191%2D238%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=CHOUARD, P. 1960. Vernalization and Its Relations to Dormancy. Annual Review of Plant Physiology and Plant Molecular Biology, 11, 191-238.

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

http://scholar.google.com/scholar?as_q=Vernalization and Its Relations to Dormancy&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=Vernalization and Its Relations to Dormancy&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=CHOUARD,&as_ylo=1960&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=CHOULET%2C F%2E%2C ALBERTI%2C A%2E%2C THEIL%2C S%2E%2C GLOVER%2C N%2E%2C BARBE%2C V%2E%2C DARON%2C J%2E%2C PINGAULT%2C L%2E%2C SOURDILLE%2C P%2E%2C COULOUX%2C A%2E%2C PAUX%2C E%2E%2C LEROY%2C P%2E%2C MANGENOT%2C S%2E%2C GUILHOT%2C N%2E%2C LE GOUIS%2C J%2E%2C BALFOURIER%2C F%2E%2C ALAUX%2C M%2E%2C JAMILLOUX%2C V%2E%2C POULAIN%2C J%2E%2C DURAND%2C C%2E%2C BELLEC%2C A%2E%2C GASPIN%2C C%2E%2C SAFAR%2C J%2E%2C DOLEZEL%2C J%2E%2C ROGERS%2C J%2E%2C VANDEPOELE%2C K%2E%2C AURY%2C J%2E M%2E%2C MAYER%2C K%2E%2C BERGES%2C H%2E%2C QUESNEVILLE%2C H%2E%2C WINCKER%2C P%2E %26 FEUILLET%2C C%2E 2014%2E Structural and functional partitioning of bread wheat chromosome 3B%2E Science%2C 345%2C 1249721%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=CHOULET, F., ALBERTI, A., THEIL, S., GLOVER, N., BARBE, V., DARON, J., PINGAULT, L., SOURDILLE, P., COULOUX, A., PAUX, E., LEROY, P., MANGENOT, S., GUILHOT, N., LE GOUIS, J., BALFOURIER, F., ALAUX, M., JAMILLOUX, V., POULAIN, J., DURAND, C., BELLEC, A., GASPIN, C., SAFAR, J., DOLEZEL, J., ROGERS, J., VANDEPOELE, K., AURY, J. M., MAYER, K., BERGES, H., QUESNEVILLE, H., WINCKER, P. & FEUILLET, C. 2014. Structural and functional partitioning of bread wheat chromosome 3B. Science, 345, 1249721.

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

http://scholar.google.com/scholar?as_q=Structural and functional partitioning of bread wheat chromosome 3B&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 and functional partitioning of bread wheat chromosome 3B&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=CHOULET,&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=DANYLUK%2C J%2E%2C KANE%2C N%2E A%2E%2C BRETON%2C G%2E%2C LIMIN%2C A%2E E%2E%2C FOWLER%2C D%2E B%2E %26 SARHAN%2C F%2E 2003%2E TaVRT%2D1%2C a putative transcription factor associated with vegetative to reproductive transition in cereals%2E Plant Physiol%2C 132%2C 1849%2D60%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=DANYLUK, J., KANE, N. A., BRETON, G., LIMIN, A. E., FOWLER, D. B. & SARHAN, F. 2003. TaVRT-1, a putative transcription factor associated with vegetative to reproductive transition in cereals. Plant Physiol, 132, 1849-60.

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=DANYLUK,&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=DANYLUK,&as_ylo=2003&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=DE LUCIA%2C F%2E%2C CREVILLEN%2C P%2E%2C JONES%2C A%2E M%2E%2C GREB%2C T%2E %26 DEAN%2C C%2E 2008%2E A PHD%2Dpolycomb repressive complex 2 triggers the epigenetic silencing of FLC during vernalization%2E Proc Natl Acad Sci U S A%2C 105%2C 16831%2D6%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=DE LUCIA, F., CREVILLEN, P., JONES, A. M., GREB, T. & DEAN, C. 2008. A PHD-polycomb repressive complex 2 triggers the epigenetic silencing of FLC during vernalization. Proc Natl Acad Sci U S A, 105, 16831-6.

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

http://scholar.google.com/scholar?as_q=A PHD-polycomb repressive complex 2 triggers the epigenetic silencing of FLC during vernalization&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 PHD-polycomb repressive complex 2 triggers the epigenetic silencing of FLC during vernalization&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=DE&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=DENG%2C W%2E%2C CASAO%2C M%2E C%2E%2C WANG%2C P%2E%2C SATO%2C K%2E%2C HAYES%2C P%2E M%2E%2C FINNEGAN%2C E%2E J%2E %26 TREVASKIS%2C B%2E 2015%2E Direct links between the vernalization response and other key traits of cereal crops%2E Nat Commun%2C 6%2C 5882%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=DENG, W., CASAO, M. C., WANG, P., SATO, K., HAYES, P. M., FINNEGAN, E. J. & TREVASKIS, B. 2015. Direct links between the vernalization response and other key traits of cereal crops. Nat Commun, 6, 5882.

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

http://scholar.google.com/scholar?as_q=Direct links between the vernalization response and other key traits of cereal crops&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Direct links between the vernalization response and other key traits of cereal crops&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=DENG,&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=DENNIS%2C E%2E S%2E %26 PEACOCK%2C W%2E J%2E 2009%2E Vernalization in cereals%2E J Biol%2C 8%2C 57%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=DENNIS, E. S. & PEACOCK, W. J. 2009. Vernalization in cereals. J Biol, 8, 57.

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

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


DISTELFELD, A., LI, C. & DUBCOVSKY, J. 2009. Regulation of flowering in temperate cereals. Curr Opin Plant Biol, 12, 178-84.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

DUBCOVSKY, J., CHEN, C. L. & YAN, L. L. 2005. Molecular characterization of the allelic variation at the VRN-H2 vernalizationlocus in barley. Molecular Breeding, 15, 395-407.


DUBCOVSKY, J. & DVORAK, J. 2007. Genome plasticity a key factor in the success of polyploid wheat under domestication.Science, 316, 1862-6.


FILIZ, E., OZDEMIR, B. S., BUDAK, F., VOGEL, J. P., TUNA, M. & BUDAK, H. 2009. Molecular, morphological, and cytological analysisof diverse Brachypodium distachyon inbred lines. Genome, 52, 876-90.


GAZZANI, S., GENDALL, A. R., LISTER, C. & DEAN, C. 2003. Analysis of the molecular basis of flowering time variation inArabidopsis accessions. Plant Physiol, 132, 1107-14.


GREENUP, A., PEACOCK, W. J., DENNIS, E. S. & TREVASKIS, B. 2009. The molecular biology of seasonal flowering-responses inArabidopsis and the cereals. Ann Bot, 103, 1165-72.


GREENUP, A. G., SASANI, S., OLIVER, S. N., TALBOT, M. J., DENNIS, E. S., HEMMING, M. N. & TREVASKIS, B. 2010. ODDSOC2 is aMADS box floral repressor that is down-regulated by vernalization in temperate cereals. Plant Physiol, 153, 1062-73.


HARTMANN, U., HOHMANN, S., NETTESHEIM, K., WISMAN, E., SAEDLER, H. & HUIJSER, P. 2000. Molecular cloning of SVP: anegative regulator of the floral transition in Arabidopsis. Plant J, 21, 351-60.


HEMMING, M. N., PEACOCK, W. J., DENNIS, E. S. & TREVASKIS, B. 2008. Low-temperature and daylength cues are integrated toregulate FLOWERING LOCUS T in barley. Plant Physiol, 147, 355-66.


HEMMING, M. N. & TREVASKIS, B. 2011. Make hay when the sun shines: the role of MADS-box genes in temperature-dependantseasonal flowering responses. Plant Sci, 180, 447-53.


HIMMELBACH, A., ZIEROLD, U., HENSEL, G., RIECHEN, J., DOUCHKOV, D., SCHWEIZER, P. & KUMLEHN, J. 2007. A set of modularbinary vectors for transformation of cereals. Plant Physiol, 145, 1192-200.


HONG, S. Y., SEO, P. J., YANG, M. S., XIANG, F. & PARK, C. M. 2008. Exploring valid reference genes for gene expression studiesin Brachypodium distachyon by real-time PCR. BMC Plant Biol, 8, 112.


International Wheat Genome Sequencing Consortium 2014. A chromosome-based draft sequence of the hexaploid bread wheat(Triticum aestivum) genome. Science, 345, 1251788.


KAUFMANN, K., MUINO, J. M., OSTERAS, M., FARINELLI, L., KRAJEWSKI, P. & ANGENENT, G. C. 2010. Chromatinimmunoprecipitation (ChIP) of plant transcription factors followed by sequencing (ChIP-SEQ) or hybridization to whole genomearrays (ChIP-CHIP). Nat Protoc, 5, 457-72.


http://www.ncbi.nlm.nih.gov/pubmed?term=DISTELFELD%2C A%2E%2C LI%2C C%2E %26 DUBCOVSKY%2C J%2E 2009%2E Regulation of flowering in temperate cereals%2E Curr Opin Plant Biol%2C 12%2C 178%2D84%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=DISTELFELD, A., LI, C. & DUBCOVSKY, J. 2009. Regulation of flowering in temperate cereals. Curr Opin Plant Biol, 12, 178-84.

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

http://scholar.google.com/scholar?as_q=Regulation of flowering in temperate cereals&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 temperate cereals&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=DISTELFELD,&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=DUBCOVSKY%2C J%2E%2C CHEN%2C C%2E L%2E %26 YAN%2C L%2E L%2E 2005%2E Molecular characterization of the allelic variation at the VRN%2DH2 vernalization locus in barley%2E Molecular Breeding%2C 15%2C 395%2D407%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=DUBCOVSKY, J., CHEN, C. L. & YAN, L. L. 2005. Molecular characterization of the allelic variation at the VRN-H2 vernalization locus in barley. Molecular Breeding, 15, 395-407.

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

http://scholar.google.com/scholar?as_q=Molecular characterization of the allelic variation at the VRN-H2 vernalization locus in barley&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 characterization of the allelic variation at the VRN-H2 vernalization locus in barley&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=DUBCOVSKY,&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=DUBCOVSKY%2C J%2E %26 DVORAK%2C J%2E 2007%2E Genome plasticity a key factor in the success of polyploid wheat under domestication%2E Science%2C 316%2C 1862%2D6%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=DUBCOVSKY, J. & DVORAK, J. 2007. Genome plasticity a key factor in the success of polyploid wheat under domestication. Science, 316, 1862-6.

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

http://scholar.google.com/scholar?as_q=Genome plasticity a key factor in the success of polyploid wheat under domestication&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 plasticity a key factor in the success of polyploid wheat under domestication&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=DUBCOVSKY,&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=FILIZ%2C E%2E%2C OZDEMIR%2C B%2E S%2E%2C BUDAK%2C F%2E%2C VOGEL%2C J%2E P%2E%2C TUNA%2C M%2E %26 BUDAK%2C H%2E 2009%2E Molecular%2C morphological%2C and cytological analysis of diverse Brachypodium distachyon inbred lines%2E Genome%2C 52%2C 876%2D90%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=FILIZ, E., OZDEMIR, B. S., BUDAK, F., VOGEL, J. P., TUNA, M. & BUDAK, H. 2009. Molecular, morphological, and cytological analysis of diverse Brachypodium distachyon inbred lines. Genome, 52, 876-90.

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

http://scholar.google.com/scholar?as_q=Molecular, morphological, and cytological analysis of diverse Brachypodium distachyon inbred lines&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, morphological, and cytological analysis of diverse Brachypodium distachyon inbred lines&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=FILIZ,&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=GAZZANI%2C S%2E%2C GENDALL%2C A%2E R%2E%2C LISTER%2C C%2E %26 DEAN%2C C%2E 2003%2E Analysis of the molecular basis of flowering time variation in Arabidopsis accessions%2E Plant Physiol%2C 132%2C 1107%2D14%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=GAZZANI, S., GENDALL, A. R., LISTER, C. & DEAN, C. 2003. Analysis of the molecular basis of flowering time variation in Arabidopsis accessions. Plant Physiol, 132, 1107-14.

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

http://scholar.google.com/scholar?as_q=Analysis of the molecular basis of flowering time variation in Arabidopsis accessions&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=Analysis of the molecular basis of flowering time variation in Arabidopsis accessions&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=GAZZANI,&as_ylo=2003&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=GREENUP%2C A%2E%2C PEACOCK%2C W%2E J%2E%2C DENNIS%2C E%2E S%2E %26 TREVASKIS%2C B%2E 2009%2E The molecular biology of seasonal flowering%2Dresponses in Arabidopsis and the cereals%2E Ann Bot%2C 103%2C 1165%2D72%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=GREENUP, A., PEACOCK, W. J., DENNIS, E. S. & TREVASKIS, B. 2009. The molecular biology of seasonal flowering-responses in Arabidopsis and the cereals. Ann Bot, 103, 1165-72.

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

http://scholar.google.com/scholar?as_q=The molecular biology of seasonal flowering-responses in Arabidopsis and the cereals&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 molecular biology of seasonal flowering-responses in Arabidopsis and the cereals&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=GREENUP,&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

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http://search.crossref.org/?page=1&rows=2&q=GREENUP, A. G., SASANI, S., OLIVER, S. N., TALBOT, M. J., DENNIS, E. S., HEMMING, M. N. & TREVASKIS, B. 2010. ODDSOC2 is a MADS box floral repressor that is down-regulated by vernalization in temperate cereals. Plant Physiol, 153, 1062-73.

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

http://scholar.google.com/scholar?as_q=ODDSOC2 is a MADS box floral repressor that is down-regulated by vernalization in temperate cereals&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=ODDSOC2 is a MADS box floral repressor that is down-regulated by vernalization in temperate cereals&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=GREENUP,&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=HARTMANN%2C U%2E%2C HOHMANN%2C S%2E%2C NETTESHEIM%2C K%2E%2C WISMAN%2C E%2E%2C SAEDLER%2C H%2E %26 HUIJSER%2C P%2E 2000%2E Molecular cloning of SVP%3A a negative regulator of the floral transition in Arabidopsis%2E Plant J%2C 21%2C 351%2D60%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=HARTMANN, U., HOHMANN, S., NETTESHEIM, K., WISMAN, E., SAEDLER, H. & HUIJSER, P. 2000. Molecular cloning of SVP: a negative regulator of the floral transition in Arabidopsis. Plant J, 21, 351-60.

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

http://scholar.google.com/scholar?as_q=Molecular cloning of SVP: a negative regulator of the floral transition 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=Molecular cloning of SVP: a negative regulator of the floral transition in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=HARTMANN,&as_ylo=2000&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=HEMMING%2C M%2E N%2E%2C PEACOCK%2C W%2E J%2E%2C DENNIS%2C E%2E S%2E %26 TREVASKIS%2C B%2E 2008%2E Low%2Dtemperature and daylength cues are integrated to regulate FLOWERING LOCUS T in barley%2E Plant Physiol%2C 147%2C 355%2D66%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=HEMMING, M. N., PEACOCK, W. J., DENNIS, E. S. & TREVASKIS, B. 2008. Low-temperature and daylength cues are integrated to regulate FLOWERING LOCUS T in barley. Plant Physiol, 147, 355-66.

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

http://scholar.google.com/scholar?as_q=Low-temperature and daylength cues are integrated to regulate FLOWERING LOCUS T in barley&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=Low-temperature and daylength cues are integrated to regulate FLOWERING LOCUS T in barley&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=HEMMING,&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=HEMMING%2C M%2E N%2E %26 TREVASKIS%2C B%2E 2011%2E Make hay when the sun shines%3A the role of MADS%2Dbox genes in temperature%2Ddependant seasonal flowering responses%2E Plant Sci%2C 180%2C 447%2D53%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=HEMMING, M. N. & TREVASKIS, B. 2011. Make hay when the sun shines: the role of MADS-box genes in temperature-dependant seasonal flowering responses. Plant Sci, 180, 447-53.

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

http://scholar.google.com/scholar?as_q=Make hay when the sun shines: the role of MADS-box genes in temperature-dependant seasonal flowering responses&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=Make hay when the sun shines: the role of MADS-box genes in temperature-dependant seasonal flowering responses&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=HEMMING,&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=HIMMELBACH%2C A%2E%2C ZIEROLD%2C U%2E%2C HENSEL%2C G%2E%2C RIECHEN%2C J%2E%2C DOUCHKOV%2C D%2E%2C SCHWEIZER%2C P%2E %26 KUMLEHN%2C J%2E 2007%2E A set of modular binary vectors for transformation of cereals%2E Plant Physiol%2C 145%2C 1192%2D200%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=HIMMELBACH, A., ZIEROLD, U., HENSEL, G., RIECHEN, J., DOUCHKOV, D., SCHWEIZER, P. & KUMLEHN, J. 2007. A set of modular binary vectors for transformation of cereals. Plant Physiol, 145, 1192-200.

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

http://scholar.google.com/scholar?as_q=A set of modular binary vectors for transformation of cereals&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 set of modular binary vectors for transformation of cereals&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=HIMMELBACH,&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=HONG%2C S%2E Y%2E%2C SEO%2C P%2E J%2E%2C YANG%2C M%2E S%2E%2C XIANG%2C F%2E %26 PARK%2C C%2E M%2E 2008%2E Exploring valid reference genes for gene expression studies in Brachypodium distachyon by real%2Dtime PCR%2E BMC Plant Biol%2C 8%2C 112%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=HONG, S. Y., SEO, P. J., YANG, M. S., XIANG, F. & PARK, C. M. 2008. Exploring valid reference genes for gene expression studies in Brachypodium distachyon by real-time PCR. BMC Plant Biol, 8, 112.

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

http://scholar.google.com/scholar?as_q=Exploring valid reference genes for gene expression studies in Brachypodium distachyon by real-time PCR&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=Exploring valid reference genes for gene expression studies in Brachypodium distachyon by real-time PCR&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=HONG,&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=International Wheat Genome Sequencing Consortium 2014%2E A chromosome%2Dbased draft sequence of the hexaploid bread wheat %28Triticum aestivum%29 genome%2E Science%2C 345%2C 1251788%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=International Wheat Genome Sequencing Consortium 2014. A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome. Science, 345, 1251788.

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

http://scholar.google.com/scholar?as_q=A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome&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 chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=International&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1



KIM, D. H., DOYLE, M. R., SUNG, S. & AMASINO, R. M. 2009. Vernalization: winter and the timing of flowering in plants. Annu RevCell Dev Biol, 25, 277-99.


KIM, S. L., LEE, S., KIM, H. J., NAM, H. G. & AN, G. 2007. OsMADS51 is a short-day flowering promoter that functions upstream ofEhd1, OsMADS14, and Hd3a. Plant Physiol, 145, 1484-94.


LEE, J. H., RYU, H. S., CHUNG, K. S., POSE, D., KIM, S., SCHMID, M. & AHN, J. H. 2013. Regulation of temperature-responsiveflowering by MADS-box transcription factor repressors. Science, 342, 628-32.


MICHAELS, S. D. & AMASINO, R. M. 1999. FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressorof flowering. Plant Cell, 11, 949-956.


MICHAELS, S. D., DITTA, G., GUSTAFSON-BROWN, C., PELAZ, S., YANOFSKY, M. & AMASINO, R. M. 2003a. AGL24 acts as apromoter of flowering in Arabidopsis and is positively regulated by vernalization. Plant J, 33, 867-74.


MICHAELS, S. D., HE, Y., SCORTECCI, K. C. & AMASINO, R. M. 2003b. Attenuation of FLOWERING LOCUS C activity as amechanism for the evolution of summer-annual flowering behavior in Arabidopsis. Proc Natl Acad Sci U S A, 100, 10102-7.


MICHAELS, S. D., HIMELBLAU, E., KIM, S. Y., SCHOMBURG, F. M. & AMASINO, R. M. 2005. Integration of flowering signals inwinter-annual Arabidopsis. Plant Physiol, 137, 149-56.


MUR, L. A., ALLAINGUILLAUME, J., CATALAN, P., HASTEROK, R., JENKINS, G., LESNIEWSKA, K., THOMAS, I. & VOGEL, J. 2011.Exploiting the Brachypodium Tool Box in cereal and grass research. New Phytol, 191, 334-47.


OLIVER, S. N., FINNEGAN, E. J., DENNIS, E. S., PEACOCK, W. J. & TREVASKIS, B. 2009. Vernalization-induced flowering in cerealsis associated with changes in histone methylation at the VERNALIZATION1 gene. Proc Natl Acad Sci U S A, 106, 8386-91.


PAOLACCI, A. R., TANZARELLA, O. A., PORCEDDU, E. & CIAFFI, M. 2009. Identification and validation of reference genes forquantitative RT-PCR normalization in wheat. BMC Mol Biol, 10, 11.


PIN, P. A., BENLLOCH, R., BONNET, D., WREMERTH-WEICH, E., KRAFT, T., GIELEN, J. J. & NILSSON, O. 2010. An antagonisticpair of FT homologs mediates the control of flowering time in sugar beet. Science, 330, 1397-400.


POSE, D., VERHAGE, L., OTT, F., YANT, L., MATHIEU, J., ANGENENT, G. C., IMMINK, R. G. & SCHMID, M. 2013. Temperature-dependent regulation of flowering by antagonistic FLM variants. Nature, 503, 414-7.


PRESTON, J. C. & KELLOGG, E. A. 2006. Reconstructing the evolutionary history of paralogous APETALA1/FRUITFULL-like genesin grasses (Poaceae). Genetics, 174, 421-37.

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

http://scholar.google.com/scholar?as_q=Chromatin immunoprecipitation (ChIP) of plant transcription factors followed by sequencing (ChIP-SEQ) or hybridization to whole genome arrays (ChIP-CHIP)&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://scholar.google.com/scholar?as_q=Identification and validation of reference genes for quantitative RT-PCR normalization in wheat&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=PAOLACCI,&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=PIN%2C P%2E A%2E%2C BENLLOCH%2C R%2E%2C BONNET%2C D%2E%2C WREMERTH%2DWEICH%2C E%2E%2C KRAFT%2C T%2E%2C GIELEN%2C J%2E J%2E %26 NILSSON%2C O%2E 2010%2E An antagonistic pair of FT homologs mediates the control of flowering time in sugar beet%2E Science%2C 330%2C 1397%2D400%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=PIN, P. A., BENLLOCH, R., BONNET, D., WREMERTH-WEICH, E., KRAFT, T., GIELEN, J. J. & NILSSON, O. 2010. An antagonistic pair of FT homologs mediates the control of flowering time in sugar beet. Science, 330, 1397-400.

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

http://scholar.google.com/scholar?as_q=An antagonistic pair of FT homologs mediates the control of flowering time in sugar beet&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=An antagonistic pair of FT homologs mediates the control of flowering time in sugar beet&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=PIN,&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=POSE%2C D%2E%2C VERHAGE%2C L%2E%2C OTT%2C F%2E%2C YANT%2C L%2E%2C MATHIEU%2C J%2E%2C ANGENENT%2C G%2E C%2E%2C IMMINK%2C R%2E G%2E %26 SCHMID%2C M%2E 2013%2E Temperature%2Ddependent regulation of flowering by antagonistic FLM variants%2E Nature%2C 503%2C 414%2D7%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=POSE, D., VERHAGE, L., OTT, F., YANT, L., MATHIEU, J., ANGENENT, G. C., IMMINK, R. G. & SCHMID, M. 2013. Temperature-dependent regulation of flowering by antagonistic FLM variants. Nature, 503, 414-7.

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

http://scholar.google.com/scholar?as_q=Temperature-dependent regulation of flowering by antagonistic FLM variants&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=Temperature-dependent regulation of flowering by antagonistic FLM variants&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=POSE,&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=PRESTON%2C J%2E C%2E %26 KELLOGG%2C E%2E A%2E 2006%2E Reconstructing the evolutionary history of paralogous APETALA1%2FFRUITFULL%2Dlike genes in grasses %28Poaceae%29%2E Genetics%2C 174%2C 421%2D37%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=PRESTON, J. C. & KELLOGG, E. A. 2006. Reconstructing the evolutionary history of paralogous APETALA1/FRUITFULL-like genes in grasses (Poaceae). Genetics, 174, 421-37.

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

http://scholar.google.com/scholar?as_q=Reconstructing the evolutionary history of paralogous APETALA1/FRUITFULL-like genes in grasses (Poaceae)&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=Reconstructing the evolutionary history of paralogous APETALA1/FRUITFULL-like genes in grasses (Poaceae)&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=PRESTON,&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1


PRESTON, J. C. & KELLOGG, E. A. 2008. Discrete developmental roles for temperate cereal grass VERNALIZATION1/FRUITFULL-like genes in flowering competency and the transition to flowering. Plant Physiol, 146, 265-76.


REAM, T. S., WOODS, D. P., SCHWARTZ, C. J., SANABRIA, C. P., MAHOY, J. A., WALTERS, E. M., KAEPPLER, H. F. & AMASINO, R.M. 2014. Interaction of photoperiod and vernalization determines flowering time of Brachypodium distachyon. Plant Physiol, 164,694-709.


RUELENS, P., DE MAAGD, R. A., PROOST, S., THEISSEN, G., GEUTEN, K. & KAUFMANN, K. 2013. FLOWERING LOCUS C inmonocots and the tandem origin of angiosperm-specific MADS-box genes. Nat Commun, 4, 2280.


SCHWARTZ, C. J., DOYLE, M. R., MANZANEDA, A. J., REY, P. J., MITCHELL-OLDS, T. & AMASINO, R. M. 2010. Natural Variation ofFlowering Time and Vernalization Responsiveness in Brachypodium distachyon. Bioenergy Research, 3, 38-46.


SHELDON, C. C., ROUSE, D. T., FINNEGAN, E. J., PEACOCK, W. J. & DENNIS, E. S. 2000. The molecular basis of vernalization: thecentral role of FLOWERING LOCUS C (FLC). Proc Natl Acad Sci U S A, 97, 3753-8.


SHINDO, C., ARANZANA, M. J., LISTER, C., BAXTER, C., NICHOLLS, C., NORDBORG, M. & DEAN, C. 2005. Role of FRIGIDA andFLOWERING LOCUS C in determining variation in flowering time of Arabidopsis. Plant Physiol, 138, 1163-73.


SHINDO, C., LISTER, C., CREVILLEN, P., NORDBORG, M. & DEAN, C. 2006. Variation in the epigenetic silencing of FLCcontributes to natural variation in Arabidopsis vernalization response. Genes Dev, 20, 3079-83.


SUNG, S. & AMASINO, R. M. 2004. Vernalization and epigenetics: how plants remember winter. Curr Opin Plant Biol, 7, 4-10.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

TREVASKIS, B., BAGNALL, D. J., ELLIS, M. H., PEACOCK, W. J. & DENNIS, E. S. 2003. MADS box genes control vernalization-induced flowering in cereals. Proc Natl Acad Sci U S A, 100, 13099-104.


TREVASKIS, B., HEMMING, M. N., DENNIS, E. S. & PEACOCK, W. J. 2007. The molecular basis of vernalization-induced floweringin cereals. Trends Plant Sci, 12, 352-7.


TREVASKIS, B., HEMMING, M. N., PEACOCK, W. J. & DENNIS, E. S. 2006. HvVRN2 responds to daylength, whereas HvVRN1 isregulated by vernalization and developmental status. Plant Physiol, 140, 1397-405.


TURNER, A., BEALES, J., FAURE, S., DUNFORD, R. P. & LAURIE, D. A. 2005. The pseudo-response regulator Ppd-H1 providesadaptation to photoperiod in barley. Science, 310, 1031-4.


TYLER, L., FANGEL, J. U., FAGERSTROM, A. D., STEINWAND, M. A., RAAB, T. K., WILLATS, W. G. & VOGEL, J. P. 2014. Selectionand phenotypic characterization of a core collection of Brachypodium distachyon inbred lines. BMC Plant Biol, 14, 25.


VOGEL, J. & HILL, T. 2008. High-efficiency Agrobacterium-mediated transformation of Brachypodium distachyon inbred line Bd21-3. Plant Cell Rep, 27, 471-8. www.plantphysiol.orgon October 1, 2020 - Published by Downloaded from

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http://www.ncbi.nlm.nih.gov/pubmed?term=PRESTON%2C J%2E C%2E %26 KELLOGG%2C E%2E A%2E 2008%2E Discrete developmental roles for temperate cereal grass VERNALIZATION1%2FFRUITFULL%2Dlike genes in flowering competency and the transition to flowering%2E Plant Physiol%2C 146%2C 265%2D76%2E&dopt=abstract

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http://search.crossref.org/?page=1&rows=2&q=REAM, T. S., WOODS, D. P., SCHWARTZ, C. J., SANABRIA, C. P., MAHOY, J. A., WALTERS, E. M., KAEPPLER, H. F. & AMASINO, R. M. 2014. Interaction of photoperiod and vernalization determines flowering time of Brachypodium distachyon. Plant Physiol, 164, 694-709.

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

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http://search.crossref.org/?page=1&rows=2&q=RUELENS, P., DE MAAGD, R. A., PROOST, S., THEISSEN, G., GEUTEN, K. & KAUFMANN, K. 2013. FLOWERING LOCUS C in monocots and the tandem origin of angiosperm-specific MADS-box genes. Nat Commun, 4, 2280.

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

http://scholar.google.com/scholar?as_q=FLOWERING LOCUS C in monocots and the tandem origin of angiosperm-specific MADS-box 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

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http://search.crossref.org/?page=1&rows=2&q=SCHWARTZ, C. J., DOYLE, M. R., MANZANEDA, A. J., REY, P. J., MITCHELL-OLDS, T. & AMASINO, R. M. 2010. Natural Variation of Flowering Time and Vernalization Responsiveness in Brachypodium distachyon. Bioenergy Research, 3, 38-46.

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

http://scholar.google.com/scholar?as_q=Natural Variation of Flowering Time and Vernalization Responsiveness in Brachypodium distachyon&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://search.crossref.org/?page=1&rows=2&q=SHELDON, C. C., ROUSE, D. T., FINNEGAN, E. J., PEACOCK, W. J. & DENNIS, E. S. 2000. The molecular basis of vernalization: the central role of FLOWERING LOCUS C (FLC). Proc Natl Acad Sci U S A, 97, 3753-8.

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

http://scholar.google.com/scholar?as_q=The molecular basis of vernalization: the central role of FLOWERING LOCUS C (FLC)&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://search.crossref.org/?page=1&rows=2&q=SHINDO, C., ARANZANA, M. J., LISTER, C., BAXTER, C., NICHOLLS, C., NORDBORG, M. & DEAN, C. 2005. Role of FRIGIDA and FLOWERING LOCUS C in determining variation in flowering time of Arabidopsis. Plant Physiol, 138, 1163-73.

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

http://scholar.google.com/scholar?as_q=Role of FRIGIDA and FLOWERING LOCUS C in determining variation in flowering time of Arabidopsis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

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http://search.crossref.org/?page=1&rows=2&q=SHINDO, C., LISTER, C., CREVILLEN, P., NORDBORG, M. & DEAN, C. 2006. Variation in the epigenetic silencing of FLC contributes to natural variation in Arabidopsis vernalization response. Genes Dev, 20, 3079-83.

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

http://scholar.google.com/scholar?as_q=Variation in the epigenetic silencing of FLC contributes to natural variation in Arabidopsis vernalization response&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://search.crossref.org/?page=1&rows=2&q=SUNG, S. & AMASINO, R. M. 2004. Vernalization and epigenetics: how plants remember winter. Curr Opin Plant Biol, 7, 4-10.

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

http://scholar.google.com/scholar?as_q=Vernalization and epigenetics: how plants remember winter&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://search.crossref.org/?page=1&rows=2&q=TREVASKIS, B., BAGNALL, D. J., ELLIS, M. H., PEACOCK, W. J. & DENNIS, E. S. 2003. MADS box genes control vernalization-induced flowering in cereals. Proc Natl Acad Sci U S A, 100, 13099-104.

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

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http://search.crossref.org/?page=1&rows=2&q=TREVASKIS, B., HEMMING, M. N., DENNIS, E. S. & PEACOCK, W. J. 2007. The molecular basis of vernalization-induced flowering in cereals. Trends Plant Sci, 12, 352-7.


http://scholar.google.com/scholar?as_q=The molecular basis of vernalization-induced flowering in cereals&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://scholar.google.com/scholar?as_q=HvVRN2 responds to daylength, whereas HvVRN1 is regulated by vernalization and developmental status&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://search.crossref.org/?page=1&rows=2&q=TURNER, A., BEALES, J., FAURE, S., DUNFORD, R. P. & LAURIE, D. A. 2005. The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science, 310, 1031-4.

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

http://scholar.google.com/scholar?as_q=The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley&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 pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=TURNER,&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=TYLER%2C L%2E%2C FANGEL%2C J%2E U%2E%2C FAGERSTROM%2C A%2E D%2E%2C STEINWAND%2C M%2E A%2E%2C RAAB%2C T%2E K%2E%2C WILLATS%2C W%2E G%2E %26 VOGEL%2C J%2E P%2E 2014%2E Selection and phenotypic characterization of a core collection of Brachypodium distachyon inbred lines%2E BMC Plant Biol%2C 14%2C 25%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=TYLER, L., FANGEL, J. U., FAGERSTROM, A. D., STEINWAND, M. A., RAAB, T. K., WILLATS, W. G. & VOGEL, J. P. 2014. Selection and phenotypic characterization of a core collection of Brachypodium distachyon inbred lines. BMC Plant Biol, 14, 25.

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

http://scholar.google.com/scholar?as_q=Selection and phenotypic characterization of a core collection of Brachypodium distachyon inbred lines&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=Selection and phenotypic characterization of a core collection of Brachypodium distachyon inbred lines&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=TYLER,&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1



VOGEL, J. P., GARVIN, D. F., LEONG, O. M. & HAYDEN, D. M. 2006. Agrobacterium-mediated transformation and inbred linedevelopment in the model grass Brachypodium distachyon. Plant Cell Tissue and Organ Culture, 84, 199-211.


WANG, R., FARRONA, S., VINCENT, C., JOECKER, A., SCHOOF, H., TURCK, F., ALONSO-BLANCO, C., COUPLAND, G. & ALBANI,M. C. 2009. PEP1 regulates perennial flowering in Arabis alpina. Nature, 459, 423-7.


WINFIELD, M. O., LU, C., WILSON, I. D., COGHILL, J. A. & EDWARDS, K. J. 2009. Cold- and light-induced changes in thetranscriptome of wheat leading to phase transition from vegetative to reproductive growth. BMC Plant Biol, 9, 55.


WOODS, D., MCKEOWN, M., DONG, Y., PRESTON, J. C. & AMASINO, R. M. 2016. Evolution of VRN2/GhD7-like genes invernalization-mediated repression of grass flowering. Plant Physiol.


YAN, L., FU, D., LI, C., BLECHL, A., TRANQUILLI, G., BONAFEDE, M., SANCHEZ, A., VALARIK, M., YASUDA, S. & DUBCOVSKY, J.2006. The wheat and barley vernalization gene VRN3 is an orthologue of FT. Proc Natl Acad Sci U S A, 103, 19581-6.


YAN, L., HELGUERA, M., KATO, K., FUKUYAMA, S., SHERMAN, J. & DUBCOVSKY, J. 2004a. Allelic variation at the VRN-1 promoterregion in polyploid wheat. Theor Appl Genet, 109, 1677-86.


YAN, L., LOUKOIANOV, A., BLECHL, A., TRANQUILLI, G., RAMAKRISHNA, W., SANMIGUEL, P., BENNETZEN, J. L., ECHENIQUE, V.& DUBCOVSKY, J. 2004b. The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science, 303, 1640-4.


YAN, L., LOUKOIANOV, A., TRANQUILLI, G., HELGUERA, M., FAHIMA, T. & DUBCOVSKY, J. 2003. Positional cloning of the wheatvernalization gene VRN1. Proc Natl Acad Sci U S A, 100, 6263-8.


ZHANG, X., CLARENZ, O., COKUS, S., BERNATAVICHUTE, Y. V., PELLEGRINI, M., GOODRICH, J. & JACOBSEN, S. E. 2007. Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis. PLoS Biol, 5, e129.


ZHAO, T., NI, Z., DAI, Y., YAO, Y., NIE, X. & SUN, Q. 2006. Characterization and expression of 42 MADS-box genes in wheat (Triticumaestivum L.). Mol Genet Genomics, 276, 334-50.



http://www.ncbi.nlm.nih.gov/pubmed?term=VOGEL%2C J%2E %26 HILL%2C T%2E 2008%2E High%2Defficiency Agrobacterium%2Dmediated transformation of Brachypodium distachyon inbred line Bd21%2D3%2E Plant Cell Rep%2C 27%2C 471%2D8%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=VOGEL, J. & HILL, T. 2008. High-efficiency Agrobacterium-mediated transformation of Brachypodium distachyon inbred line Bd21-3. Plant Cell Rep, 27, 471-8.

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

http://scholar.google.com/scholar?as_q=High-efficiency Agrobacterium-mediated transformation of Brachypodium distachyon inbred line Bd21-3&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=High-efficiency Agrobacterium-mediated transformation of Brachypodium distachyon inbred line Bd21-3&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=VOGEL,&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=VOGEL%2C J%2E P%2E%2C GARVIN%2C D%2E F%2E%2C LEONG%2C O%2E M%2E %26 HAYDEN%2C D%2E M%2E 2006%2E Agrobacterium%2Dmediated transformation and inbred line development in the model grass Brachypodium distachyon%2E Plant Cell Tissue and Organ Culture%2C 84%2C 199%2D211%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=VOGEL, J. P., GARVIN, D. F., LEONG, O. M. & HAYDEN, D. M. 2006. Agrobacterium-mediated transformation and inbred line development in the model grass Brachypodium distachyon. Plant Cell Tissue and Organ Culture, 84, 199-211.

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

http://scholar.google.com/scholar?as_q=Agrobacterium-mediated transformation and inbred line development in the model grass Brachypodium distachyon&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=Agrobacterium-mediated transformation and inbred line development in the model grass Brachypodium distachyon&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=VOGEL,&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=WANG%2C R%2E%2C FARRONA%2C S%2E%2C VINCENT%2C C%2E%2C JOECKER%2C A%2E%2C SCHOOF%2C H%2E%2C TURCK%2C F%2E%2C ALONSO%2DBLANCO%2C C%2E%2C COUPLAND%2C G%2E %26 ALBANI%2C M%2E C%2E 2009%2E PEP1 regulates perennial flowering in Arabis alpina%2E Nature%2C 459%2C 423%2D7%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=WANG, R., FARRONA, S., VINCENT, C., JOECKER, A., SCHOOF, H., TURCK, F., ALONSO-BLANCO, C., COUPLAND, G. & ALBANI, M. C. 2009. PEP1 regulates perennial flowering in Arabis alpina. Nature, 459, 423-7.

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

http://scholar.google.com/scholar?as_q=PEP1 regulates perennial flowering in Arabis alpina&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=PEP1 regulates perennial flowering in Arabis alpina&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=WANG,&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=WINFIELD%2C M%2E O%2E%2C LU%2C C%2E%2C WILSON%2C I%2E D%2E%2C COGHILL%2C J%2E A%2E %26 EDWARDS%2C K%2E J%2E 2009%2E Cold%2D and light%2Dinduced changes in the transcriptome of wheat leading to phase transition from vegetative to reproductive growth%2E BMC Plant Biol%2C 9%2C 55%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=WINFIELD, M. O., LU, C., WILSON, I. D., COGHILL, J. A. & EDWARDS, K. J. 2009. Cold- and light-induced changes in the transcriptome of wheat leading to phase transition from vegetative to reproductive growth. BMC Plant Biol, 9, 55.

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

http://scholar.google.com/scholar?as_q=Cold- and light-induced changes in the transcriptome of wheat leading to phase transition from vegetative to reproductive growth&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=Cold- and light-induced changes in the transcriptome of wheat leading to phase transition from vegetative to reproductive growth&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=WINFIELD,&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=WOODS%2C D%2E%2C MCKEOWN%2C M%2E%2C DONG%2C Y%2E%2C PRESTON%2C J%2E C%2E %26 AMASINO%2C R%2E M%2E 2016%2E Evolution of VRN2%2FGhD7%2Dlike genes in vernalization%2Dmediated repression of grass flowering%2E Plant Physiol%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=WOODS, D., MCKEOWN, M., DONG, Y., PRESTON, J. C. & AMASINO, R. M. 2016. Evolution of VRN2/GhD7-like genes in vernalization-mediated repression of grass flowering. Plant Physiol.

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

http://scholar.google.com/scholar?as_q=Evolution of VRN2/GhD7-like genes in vernalization-mediated repression of grass 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=Evolution of VRN2/GhD7-like genes in vernalization-mediated repression of grass flowering.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=WOODS,&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=YAN%2C L%2E%2C FU%2C D%2E%2C LI%2C C%2E%2C BLECHL%2C A%2E%2C TRANQUILLI%2C G%2E%2C BONAFEDE%2C M%2E%2C SANCHEZ%2C A%2E%2C VALARIK%2C M%2E%2C YASUDA%2C S%2E %26 DUBCOVSKY%2C J%2E 2006%2E The wheat and barley vernalization gene VRN3 is an orthologue of FT%2E Proc Natl Acad Sci U S A%2C 103%2C 19581%2D6%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=YAN, L., FU, D., LI, C., BLECHL, A., TRANQUILLI, G., BONAFEDE, M., SANCHEZ, A., VALARIK, M., YASUDA, S. & DUBCOVSKY, J. 2006. The wheat and barley vernalization gene VRN3 is an orthologue of FT. Proc Natl Acad Sci U S A, 103, 19581-6.

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

http://scholar.google.com/scholar?as_q=The wheat and barley vernalization gene VRN3 is an orthologue of FT&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=YAN%2C L%2E%2C HELGUERA%2C M%2E%2C KATO%2C K%2E%2C FUKUYAMA%2C S%2E%2C SHERMAN%2C J%2E %26 DUBCOVSKY%2C J%2E 2004a%2E Allelic variation at the VRN%2D1 promoter region in polyploid wheat%2E Theor Appl Genet%2C 109%2C 1677%2D86%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=YAN, L., HELGUERA, M., KATO, K., FUKUYAMA, S., SHERMAN, J. & DUBCOVSKY, J. 2004a. Allelic variation at the VRN-1 promoter region in polyploid wheat. Theor Appl Genet, 109, 1677-86.


http://scholar.google.com/scholar?as_q=Allelic variation at the VRN-1 promoter region in polyploid wheat&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=Allelic variation at the VRN-1 promoter region in polyploid wheat&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=YAN,&as_ylo=2004a&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=YAN%2C L%2E%2C LOUKOIANOV%2C A%2E%2C BLECHL%2C A%2E%2C TRANQUILLI%2C G%2E%2C RAMAKRISHNA%2C W%2E%2C SANMIGUEL%2C P%2E%2C BENNETZEN%2C J%2E L%2E%2C ECHENIQUE%2C V%2E %26 DUBCOVSKY%2C J%2E 2004b%2E The wheat VRN2 gene is a flowering repressor down%2Dregulated by vernalization%2E Science%2C 303%2C 1640%2D4%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=YAN, L., LOUKOIANOV, A., BLECHL, A., TRANQUILLI, G., RAMAKRISHNA, W., SANMIGUEL, P., BENNETZEN, J. L., ECHENIQUE, V. & DUBCOVSKY, J. 2004b. The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science, 303, 1640-4.


http://scholar.google.com/scholar?as_q=The wheat VRN2 gene is a flowering repressor down-regulated by vernalization&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 wheat VRN2 gene is a flowering repressor down-regulated by vernalization&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=YAN,&as_ylo=2004b&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=YAN%2C L%2E%2C LOUKOIANOV%2C A%2E%2C TRANQUILLI%2C G%2E%2C HELGUERA%2C M%2E%2C FAHIMA%2C T%2E %26 DUBCOVSKY%2C J%2E 2003%2E Positional cloning of the wheat vernalization gene VRN1%2E Proc Natl Acad Sci U S A%2C 100%2C 6263%2D8%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=YAN, L., LOUKOIANOV, A., TRANQUILLI, G., HELGUERA, M., FAHIMA, T. & DUBCOVSKY, J. 2003. Positional cloning of the wheat vernalization gene VRN1. Proc Natl Acad Sci U S A, 100, 6263-8.


http://scholar.google.com/scholar?as_q=Positional cloning of the wheat vernalization gene VRN1&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=Positional cloning of the wheat vernalization gene VRN1&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=YAN,&as_ylo=2003&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=ZHANG%2C X%2E%2C CLARENZ%2C O%2E%2C COKUS%2C S%2E%2C BERNATAVICHUTE%2C Y%2E V%2E%2C PELLEGRINI%2C M%2E%2C GOODRICH%2C J%2E %26 JACOBSEN%2C S%2E E%2E 2007%2E Whole%2Dgenome analysis of histone H3 lysine 27 trimethylation in Arabidopsis%2E PLoS Biol%2C 5%2C e129%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=ZHANG, X., CLARENZ, O., COKUS, S., BERNATAVICHUTE, Y. V., PELLEGRINI, M., GOODRICH, J. & JACOBSEN, S. E. 2007. Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis. PLoS Biol, 5, e129.

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

http://scholar.google.com/scholar?as_q=Whole-genome analysis of histone H3 lysine 27 trimethylation 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=Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=ZHANG,&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=ZHAO%2C T%2E%2C NI%2C Z%2E%2C DAI%2C Y%2E%2C YAO%2C Y%2E%2C NIE%2C X%2E %26 SUN%2C Q%2E 2006%2E Characterization and expression of 42 MADS%2Dbox genes in wheat %28Triticum aestivum L%2E%29%2E Mol Genet Genomics%2C 276%2C 334%2D50%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=ZHAO, T., NI, Z., DAI, Y., YAO, Y., NIE, X. & SUN, Q. 2006. Characterization and expression of 42 MADS-box genes in wheat (Triticum aestivum L.). Mol Genet Genomics, 276, 334-50.

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

http://scholar.google.com/scholar?as_q=Characterization and expression of 42 MADS-box genes in wheat (Triticum aestivum L&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Characterization and expression of 42 MADS-box genes in wheat (Triticum aestivum L&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=ZHAO,&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1


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