: Plants of the usually perennial autotetraploid Arabidopsis … · 99 2015). Distinct genetic...

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Short title: The evolution of weediness in Arabidopsis arenosa 1

* Author for correspondence, Kirsten Bomblies: [email protected] 2

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Title: HABITAT-ASSOCIATED LIFE HISTORY AND STRESS-TOLERANCE VARIATION IN 4

ARABIDOPSIS ARENOSA 5

Pierre Baduel1, 2, Brian Arnold1,3, Cara M. Weisman4, Ben Hunter1,5, Kirsten Bomblies*, 1, 6 6

1. 1. Department of Organismic and Evolutionary Biology, Harvard University, 7

Cambridge, MA, USA 8

2. 2. École des Mines de Paris, Paris, France 9

3. 3. Present address: Center for Communicable Disease Dynamics and Department 10

of Epidemiology, Harvard T.H Chan School of Public Health, Boston, MA, USA 11

4. 4. Harvard Biophysics Program, Harvard Medical School, Boston, MA, USA 12

5. 5. Present address: Monsanto Holland B.V., Bergschenhoek, Netherlands 13

6. 6. Present address: Department of Cell and Developmental Biology, John Innes 14

Centre, Norwich, UK 15

* Author for correspondence, Kirsten Bomblies: [email protected] 16

Author Contributions 17

P.B. and K.B. conceived of the original research plan and strategy; P.B. conducted most of the 18

experiments with help from B.H.; P.B. analysed most of the data with help from B.A. for analyses of 19

divergence and selection; C.W. provided sequencing information; P.B. and K.B. wrote the article with 20

contributions from all authors. 21

Funding information: This work was funded by a National Science Foundation grant to KB 22

(IOS – 1146465) and an award from the Jean Gaillard Memorial Fellowship Fund to PB. 23

Plant Physiology Preview. Published on March 3, 2016, as DOI:10.1104/pp.15.01875

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One sentence summary: Plants of the usually perennial autotetraploid Arabidopsis arenosa 25

that colonized railways became vernalization insensitive, early and perpetually flowering, and 26

constitutively heat and cold stress tolerant. 27



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ABSTRACT 28

Weediness in ephemeral plants is commonly characterized by rapid cycling, prolific “all in” 29

flowering, and loss of perenniality. Many species made transitions to weediness of this sort, 30

which can be advantageous in high-disturbance or human associated habitats. The molecular 31

basis of this shift, however, remains mostly mysterious. Here we use transcriptome sequencing, 32

genome resequencing scans for selection, and stress tolerance assays to study a weedy 33

population of the otherwise non-weedy Arabidopsis arenosa, an obligately outbreeding relative 34

of A. thaliana. Though weedy A. arenosa is widespread, a single genetic lineage colonized 35

railways throughout central and northern Europe. We show that railway plants, in contrast to 36

plants from sheltered outcrops in hill/mountain regions, are rapid cycling, have lost vernalization 37

requirement, show prolific flowering, and do not return to vegetative growth. Comparing 38

transcriptomes of railway and mountain plants across timecourses with and without 39

vernalization, we found railway plants have sharply abrogated vernalization responsiveness, 40

and high constitutive expression of heat and cold-responsive genes. Railway plants also have 41

strong constitutive heat shock and freezing tolerance compared with mountain plants, where 42

tolerance must be induced. We found 20 genes with good evidence of selection in the railway 43

population. One of these, LATE ELONGATED HYPOCOTYL (LHY) is known in A. thaliana to 44

regulate many stress response genes we found to be differentially regulated among the distinct 45

habitats. Our data suggest that beyond life history regulation, other traits like basal stress 46

tolerance are also associated with the evolution of weediness in A. arenosa. 47



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INTRODUCTION 48

Life-history traits differ between and within plant species and commonly reflect requirements of 49

the habitats in which they are found (Baker, 1974; Weinig et al., 2003; Grime, 2006). Depending 50

on abiotic and biotic conditions, a variety of strategies can be favored and “weeds” are 51

accordingly phenotypically diverse. In environments that are unpredictable with frequent 52

occurrences of stresses like drought, temperature fluctuations, or human-associated 53

perturbations, rapid cycling and early flowering are common (e.g. Wu et al., 2010; Hall and 54

Willis, 2006; Franks et al., 2007; Sherrard and Maherali, 2006). Life history adaptations can help 55

mediate trade-offs between resource accumulation and stress-avoidance and are important for 56

wild species as well as for crops (Jung and Müller, 2009). Comparing results among species, as 57

well as the correlates of these traits with other fitness-related traits, promises new insights into 58

the mechanisms of adaptation to unpredictable habitats. 59

A common phenotype of plants in unpredictable habitats is early and prolific flowering relative to 60

related populations in more stable habitats (Baker, 1965; Grotkopp et al., 2002; Blair and Wolfe, 61

2004; Burns, 2004; Hall and Willis, 2006; Sherrard and Maherali, 2006; Franks et al., 2007). The 62

complex genetic architecture of flowering has been well studied in the annual Arabidopsis 63

thaliana (Andrés and Coupland, 2012), where independent changes in two genes in particular, 64

FLOWERING LOCUS C (FLC) and FRIGIDA (FRI), have been repeatedly found to underlie 65

natural variation in flowering time and vernalization responsiveness (Michaels and Amasino, 66

1999; Johanson et al., 2000; Le Corre et al., 2002; Gazzani et al., 2003; Lempe et al., 2005; 67

Shindo et al., 2005; Werner et al., 2005; Brachi et al., 2010; Méndez-Vigo et al., 2011; Salomé 68

et al., 2011; Song et al., 2013; Méndez-Vigo et al., 2015). The same genes are also important in 69

the closely related Arabidopsis lyrata (Kuittinen et al., 2008) and in other species in the 70

Brassicaceae (Slotte et al., 2009; Wang et al., 2009; Guo et al., 2012). Active FRI alleles 71

enhance expression of FLC, which in turn represses floral activators including FLOWERING 72



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LOCUS T (FT) and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1 (SOC1) 73

(Michaels and Amasino, 1999; Searle et al., 2006). A. thaliana accessions with functional alleles 74

of both FRI and FLC are late-flowering in the lab, but prolonged exposure to cold (vernalization) 75

epigenetically represses FLC expression allowing flowering upon return to warm temperatures 76

(Song et al., 2013). Many independent disruptions of FRI or FLC have been identified in A. 77

thaliana (Johanson et al., 2000; Le Corre et al., 2002; Gazzani et al., 2003; Shindo et al., 2005; 78

Werner et al., 2005; Méndez-Vigo et al., 2011) that result in reduced or abrogated FLC 79

expression, leading to earlier flowering and reduced need for vernalization. However, non-80

functional FRI alleles are associated with negative pleiotropic effects on branching and fitness, 81

likely limiting the adaptive potential of the FRI locus (Scarcelli et al., 2007). Natural variation in 82

FLC and FRI also affects other important life-history traits including seed germination (Chiang et 83

al., 2009), water-use efficiency, which is a major dehydration avoidance mechanism (Mckay et 84

al., 2003), and even flower tolerance to heat-shocks (Bac-Molenaar et al., 2015). FLC also plays 85

a role in more long-lived plants: In the perennial Arabis alpina, an ortholog of FLC, PERPETUAL 86

FLOWERING 1 (PEP1), contributes to late flowering and vernalization requirement as it does in 87

A. thaliana, but also promotes a return to vegetative development after each flowering episode, 88

which is an important feature of perennial life-cycles (Wang et al., 2009). Variation in PEP1 89

activity is associated with distinct life-histories in different A. alpina accessions (Albani et al., 90

2012). 91

Arabidopsis arenosa is a close relative of A. thaliana and A. lyrata (O’Kane, 1997; Clauss and 92

Koch, 2006). In contrast to A. thaliana, A. arenosa is a perennial obligate outcrosser with high 93

genetic diversity and both diploid and tetraploid variants (Hollister et al., 2012; Schmickl et al., 94

2012). The autotetraploid A. arenosa arose from a single diploid population closely related to 95

populations found today in the Carpathian Mountains of Slovakia around 19,000 generations 96

ago; by 15,000 generations ago, autotetraploid lineages had begun radiating across the 97



6

landscape into the distinct types found in diverse habitats across Europe today (Arnold et al., 98

2015). Distinct genetic lineages correlate with geography and habitat. Rocky outcrops are 99

generally populated by a perennial “mountain” form while ruderal settings, especially railways, 100

are colonized by an annual, “flatland” form (Scholz, 1962). Though the mountain form comprises 101

at least four distinct genetic lineages associated with geography, we found previously that 102

railway populations from geographically distant locations are extremely closely related, 103

suggesting this habitat was colonized just once by a single genetic lineage that subsequently 104

spread along this habitat (Arnold et al., 2015). 105

Here we study representative populations of the perennial mountain form and the flatland form 106

of A. arenosa. Specifically we use phenotypic, genomic and transcriptomic experiments to 107

assess flowering time, vernalization responsiveness, and stress resilience. We found that 108

populations from ruderal sites are rapid cycling, do not require vernalization, and do not resume 109

vegetative growth after a single flowering episode, while mountain populations remain 110

vernalization responsive. We compared transcriptomes of early flowering (railway) and late-111

flowering (mountain) plants across time series that were either vernalized or not. We found that 112

rapid-cycling plants from railway populations have very low FLC expression and a sharply 113

abrogated vernalization response, while plants from a mountain population show transient 114

repression of FLC by vernalization similar to what was described in A. alpina (Wang et al., 2009; 115

Albani et al., 2012). We also found constitutive differences in expression of cold- and heat-116

stress-response genes. Consistent with the expression data, we found that railway plants had 117

higher basal heat and cold stress tolerance than mountain plants. A genome-resequencing scan 118

for divergence identified 20 loci with evidence of positive selection in the weedy railway lineage. 119

Among these is the circadian clock regulator, LATE ELONGATED HYPOCOTYL (LHY), which 120

regulates many of the cold and heat responsive genes we found to be differentially expressed in 121

these two A. arenosa types. Our data suggest that in addition to flowering behavior, traits like 122



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flowering induction, and heat-and cold-stress tolerance that are environmentally inducible in 123

mountain plants became constitutive in the weedy railway plants. 124

125



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RESULTS 126

Flowering time and vernalization response in A. arenosa 127

We grew plants from seeds sampled from five mountain and four railway populations of A. 128

arenosa in controlled conditions from seeds collected from wild plants (Fig. 1A). We measured 129

flowering time (as days from germination to first open flower) for plants grown with or without an 130

eight-week vernalization period that consisted of a cold treatment (4°C) under short-day 131

conditions (8 hours of light instead of 16, see Methods). All mountain populations flowered 132

significantly later than all railway populations when unvernalized (Fig. 1B), but all populations 133

flowered similarly when vernalized. This shows that all sampled railway populations are rapid 134

cycling and have lost vernalization responses while all mountain populations retain them and 135

flower late without cold treatments. We previously showed that the railway plants are all 136

extremely closely related, suggesting a single colonization event that is consistent with the 137

genetic similarity of the different railway populations (Arnold et al. 2015). 138

We selected a single railway population (TBG) and a single mountain population (KA) as 139

representative of the two types to analyze in more depth the molecular basis of their phenotypic 140

differences. TBG is from a railway at Triberg railway station in southwest Germany. KA is from a 141

limestone outcrop on Kasparstein Mountain, near Loschental, Austria (Fig. 1A). These 142

populations are members of genetically distinct “mountain” and “railway” lineages with no 143

evidence of recent gene flow between them (Arnold et al. 2015). Among unvernalized plants, 144

those from KA flowered much later than those from the TBG (Wilcoxon p<10e-6): Days to open 145

flower averaged 56 days for unvernalized TBG plants, while 67% of KA plants had not yet 146

flowered by 200 days, at which point we ended the experiment (Fig. 1B). There was no 147

significant difference in flowering times of cold-treated (vernalized) plants from the two 148

populations (Fig 1B; Wilcoxon p>0.08). We confirmed the similarity of flowering behavior of the 149



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two vernalized populations using a Mann-Whitney U-test (p>0.6). Vernalization had no 150

significant effect on the mean flowering time of TBG, though there was a reduction in the 151

standard deviation from 12 days (non-vernalized) to 4 days (vernalized), implying that TBG 152



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plants, though lacking a true vernalization response, still show a residual response to prolonged 153

cold treatment. The difference in flowering behavior persists in subsequent generations in the 154

lab showing that this is not merely a maternal environmental effect resulting from differences in 155

conditions in wild populations (not shown). 156

After flowering, vernalized KA plants reverted to vegetative growth while TBG flowered 157

continuously until senescence (Fig. 1C), paralleling the distinction between “perpetual” and 158

“episodic” flowering previously described in Arabis alpina (Wang et al., 2009). Furthermore, from 159

our initial phenotyping of 13 KA plants and 20 TBG plants, it was also clear that TBG plants 160

grew more rosette inflorescence branches (RB in Fig. 1D; average rosette inflorescences longer 161

then 5cm at 20 days after flowering =14.35) compared to KA, which usually had none or only 162

one (average rosette branches longer then 5cm at 20 days after flowering =0.54; t-test p=8 x 10-163

7). The number of inflorescence branches (PB in Fig. 1D) also differs similarly dramatically (0.23 164

branches in KA, vs. 18.15 branches in TBG; p=1.7 x 10-9). Thus TBG plants show common 165

“weedy” phenotypic characteristics including rapid cycling, and bushy and abundant 166

inflorescence growth (Baker, 1965; Grotkopp et al., 2002; Blair and Wolfe, 2004; Burns, 2004; 167

Hall and Willis, 2006). 168

Abrogated vernalization responsiveness and loss of FLC expression in a railway 169

accession 170

To compare the vernalization responses of KA and TBG we analyzed the transcriptomes of 171

plants from these two populations by RNA-seq at four timepoints (3, 4, 9 and 13 weeks) with or 172

without a six-week vernalization period at weeks 4-10 (see Methods). We quantified expression 173

by read depth after aligning to the A. lyrata reference genome (Hu et al., 2011), which includes 174

32,670 annotated genes (see Methods). We first examined expression of 151 A. lyrata 175

homologs of 174 genes associated with flowering regulation in A. thaliana (Fornara et al., 2010). 176



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Among these, FLOWERING LOCUS C (FLC) was the most differentially expressed between the 177

two vernalized time-series of KA and TBG, with virtually undetectable expression in TBG. FLC 178

showed initially strong expression in KA followed by a clear suppression by vernalization, but a 179



12

subsequent return to pre-vernalization levels after plants were returned to warmer conditions. 180

We confirmed this expression profile by q-RT-PCR with a finer sampling resolution (Fig. 2A). 181

In the A. arenosa genome, FLC is present in two full-length and one truncated duplicate copies 182

(Nah and Chen, 2010), but only one copy was annotated in the version of the A. lyrata genome 183

we used for mRNA-seq mapping (scaffold 6: 4040170-4045798). Since finalizing this work, a 184

newer annotation has been published (Rawat et al., 2015) that recognizes two FLC genes in A. 185

lyrata. Because of the very close similarity between the two genes, we could not use our 186

coverage estimates from read alignments to A. lyrata or to the A. arenosa BAC to differentiate 187

the expression of the two copies. Thus to estimate relative expression levels we genotyped our 188

read alignments for polymorphisms that distinguish the two full-length FLC copies. We found a 189

total of nine single nucleotide polymorphisms (SNPs) that differ between the paralogues in our 190

transcriptome samples (Fig. 2B). Seven of these SNPs had been previously identified in a BAC 191

sequence of the A. arenosa FLC locus from the Care-1 strain (Nah and Chen, 2010). Only 3 192

were among the 16 polymorphisms differentiating the two A. lyrata paralogs. At all nine 193

positions, the nucleotides characteristic of AaFLC2 were at low frequency in our transcriptome 194

alignments relative to those characteristic of AaFLC1, indicating low expression of AaFLC2 195

relative to AaFLC1. 196

To more finely quantify the differential expression of AaFLC1 and AaFLC2 we mapped our 197

RNA-seq data on the BAC sequence and followed a previously described method for detection 198

of allelic expression differences (Perez et al., 2015), estimating expression of the two transcripts 199

with MMSEQ (Turro et al., 2011). This approach confirmed the differential expression of 200

AaFLC1 and AaFLC2 in the KA samples (where sufficient levels of expression were detected). 201

In the two time-series of this population, AaFLC1 contributed to an average of 77% of the total 202

AaFLC expression. The relative ratios of the duplicates remain consistent in our time series, 203

indicating that although AaFLC1 dominates in terms of total expression, both paralogues 204



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respond similarly to vernalization in KA (Fig. 2C). 205

As expected, positive regulators of flowering showed opposite trends to the floral repressor 206

FLC, including SOC1, SQUAMOSA PROMOTER BINDING PROTEIN-LIKE 15 (SPL15), and 207

SPL4, which were all expressed throughout the timecourse in TBG, but only after vernalization 208

in KA. The expression profile of SOC1, a flowering promoter, was especially strongly anti-209

correlated with FLC expression (Fig. S1; Pearson correlation: -0.87). VERNALIZATION 210

INSENSITIVE 3 (VIN3), which encodes a component of the Polycomb Repressive Complex 2 211

(PRC2) responsible for establishing the repression of FLC during vernalization is up-regulated 212

by vernalization in A. thaliana (Sung and Amasino, 2004). VIN3 is similarly up-regulated in both 213

TBG and KA (Fig. S1), but the magnitude of the response is lower in TBG than in KA, consistent 214

with the hypothesis that TBG maintains some vernalization responsiveness, albeit in a strongly 215

abrogated form, and that the cause of this abrogation may lie upstream of VIN3. 216

Vernalization-response differences 217

We next set out to characterize the vernalization responsive subset of genes within the entire 218

transcriptomes of KA and TBG with two goals: (1) to understand the vernalization response in A. 219

arenosa, and (2) to compare the responsiveness of the two accessions qualitatively and 220

quantitatively. Within each genotype, we identified vernalization-response genes as the 221

intersection of genes that differ between growth conditions (vernalized vs non-vernalized) and 222

those that change expression through the time-course within each of the conditions. We used a 223

non-parametric ranking test (see Methods) to identify significantly differentially expressed 224

vernalization responsive genes. We considered genes to be vernalization responsive if they 225

showed a differential expression during the vernalized time series, and had a significant growth 226

condition interaction. This category includes genes that are (Fig. 3A – “a”) or are not (Fig. 3A – 227

“b”) differentially expressed at different time points in the non-vernalized time series. 228



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Using our criteria, we identified 1088 genes as “vernalization responsive” in KA, almost 6 times 229

more than the 187 found in TBG (Table S1). Only a small percentage of transcripts 230

(representing 53 genes) are vernalization responsive in both accessions (Fig. 3B), but when we 231



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compared expression ratios between vernalized and non-vernalized time points in KA and in 232

TBG, 60% of these genes showed a significant correlation (R2=0.83) between the two 233

accessions. The slope of the log regression was significantly higher than 1 (1.62), suggesting 234

that TBG does still have some vernalization responsiveness, but that the magnitude of the 235

response is strongly dampened relative to that in KA (Fig. 3C). This reduced responsiveness 236

likely explains the lower number of genes passing our thresholds of detection for vernalization 237

responsiveness in TBG. 238

Gene Ontology (GO) analysis of KA vernalization responsive genes showed a very strong 239

representation of genes implicated in light sensitivity and abiotic stress responses. The light-240

related GO terms included response to UV (GO:0009411; p=0.002), response to light stimulus 241

(GO:0009416; p=0.007), and long-day photoperiod flowering (GO:0048574; p=2 x 10-5); these 242

were equally divided between the two categories (a and b) of the KA vernalization response 243

(Fig. 3B). On the other hand, the cold-stress terms, including cold response (GO:0009409; p=1 244

x 10-8), water deprivation response (GO:0009414; p=0.03), salt stress response (GO:0009651; 245

p=5 x 10-8), and hyperosmotic stress response (GO:0006972; p=6 x 10-5), were mainly present 246

in the b category, meaning that their expression shifts over the vernalized timecourse, but not 247

over the non-vernalized timecourse (Fig. 3B), suggesting they might be co-regulated with or by 248

the vernalization response. In particular the cold acclimation term was only enriched in the b 249

category (GO:0009631; p=0.003) and included well-known cold-regulated genes like COLD-250

REGULATED 47 (COR47), EARLY RESPONSIVE TO DEHYDRATION (ERD10), LOW 251

TEMPERATURE-INDUCED (LTI30), and KINASE 1 (KIN1) (Maruyama et al., 2004). The b 252

category also included other known components of the cold response of A. thaliana such as 253

COR15A, COR15B, COR78, and PSEUDO-RESPONSE REGULATOR 9 (PRR9). These genes 254

have been shown to confer different degrees of freezing tolerance (Artus et al., 1996; Jaglo-255

Ottosen, 1998; Steponkus et al., 1998) as well as acclimation, the capacity to increase freezing 256



16

tolerance after exposure to non-freezing cold temperatures (Thomashow, 1999). 257

In our two A. arenosa populations the magnitude of the response of most of the vernalization 258

genes is amplified in KA relative to TBG, but the non-vernalized “basal” levels of expression of 259

stress-responsive genes are higher in TBG (slope of 0.79 in NV expression levels, R2=0.75; Fig. 260

4A). The core cold-responsive genes previously highlighted are outliers from this correlation, 261

with an even stronger tendency to be highly expressed in TBG. This relationship is inverted by 262

cold-treatment, due to the stronger magnitude of the KA response to vernalization treatment 263

(slope of 1.2 in V expression levels, R2=0.95; Fig. 4B). 264

The expression results led us to hypothesize that there might be a difference in the constitutive 265

and acquired freezing tolerance of KA and TBG. To test this, we quantified freezing tolerance of 266

these two accessions by measuring electrolyte leakage from detached leaves of vernalized and 267

non-vernalized plants exposed to freezing (Sukumuran and Weiser, 1972). Leaves from non-268

vernalized KA plants showed a very high electrolyte leakage at -6°C (72%) while TBG leaves 269

were significantly lower, at 33% (one-tailed t-test p < 0.005). Both accessions showed a 270

significant reduction of leakage after 1 week of vernalization to 18% and 16% for KA and TBG 271

respectively (Fig. 4C). This suggests that while tolerance is constitutively higher in TBG than in 272

KA, after prior exposure to 4°C, KA can achieve levels of freezing tolerance comparable to TBG. 273

In addition, tolerance of TBG also increases further with cold exposure, again consistent with 274

the hypothesis that it retains some ability to respond to cold. 275

276

Global TBG-KA expression differences 277

We next compared the overall transcriptomes of the KA and TBG time-series for both the non-278

vernalized and vernalized samples (Fig. 5). For each comparison we obtained a q-value (FDR-279



17

corrected, see methods) for every gene annotated in the A. lyrata reference genome (Hu et al., 280

2011). Out of the 326 genes that comprise the 1% most strongly differentially expressed genes 281

between TBG and KA, 35 have no orthologues in A. thaliana (Fig. 5A and Table S2), even 282



18

though orthologue-less genes more frequently display null mean and variance of expression 283

levels than genes with orthologues (Fig. S2). Over the whole genome, the expression difference 284

of FLC ranked third in comparisons of TBG and KA in both vernalized and unvernalized time 285



19

series, making it the most differentially expressed gene between these accessions overall. The 286

only genes more highly ranked for differential expression between TBG and KA in the non-287

vernalized series are ALPHA TUBULIN 1 (TUA1) a pollen specific alpha-tubulin gene (Kim and 288

An, 1992) and BTB AND TAZ DOMAIN PROTEIN 4 (AtBT4). In the vernalized series the top 289

two differentially expressed genes are At4g10320 (which encodes a tRNA synthetase) and 290

g932613 (which has no A. thaliana homologue). 291

We next asked if there are any GO terms for biological processes (BP) enriched in the 1% top 292

differentially expressed genes between KA and TBG in both time series. The significantly over-293

represented categories include several stimulus-response gene categories, including: heat 294

response (GO:0009408; p=0.023), protein unfolding (GO:0043335; p=0.015), Golgi vesicle 295

transport (GO:0048193; p=0.02), detection of visible light (GO:0009584; p=0.001) and DNA 296

repair (GO:0006281; p=0.044). Overall, these categories point to a generalized elevation of 297

stress-associated genes in TBG. The GO category detection of visible light (GO:0009584) has 298

the most significant p-value in our analysis. Among differentially expressed genes in this 299

category are PHYTOCHROME C (PHYC) and PHYD, two of the four phytochromes annotated 300

in the A. lyrata genome. Both are involved in light signaling (Hu et al., 2013) and are expressed 301

at lower levels in TBG. Mutation of PHYC leads to early-flowering in A. thaliana (Monte et al., 302

2003) while polymorphisms in PHYC are thought to be involved in climatic adaptation 303

(Balasubramanian et al., 2006; Samis et al., 2008; Méndez-Vigo et al., 2011). PALE CRESS 304

(PAC), which in A. thaliana is important in chloroplast development and in regulating levels of 305

carotenoids and chlorophyll (Reiter et al., 1994), is more highly expressed in KA relative to TBG. 306

Carotenoids are known to be important in the chloroplast capacity to respond to high light stress 307

(Havaux, 1998). In parallel, several genes implicated in DNA repair and recombination also 308

show significant differential expression between KA and TBG in both time series, including DNA 309

LIGASE 6 (LIG6), MMS ZWEI HOMOLOGUE 2 (MMZ2), AT3G07930 (MBD4L), REPLICATION 310



20

PROTEIN A 1B (RPA1B), RECQ HELICASE SIM (RECQSIM) and Y-FAMILY DNA 311

POLYMERASE H (POLH). All but RECQSIM, have lower expression in TBG than in KA. POLH 312

and RPA1B in particular are known to be involved in the DNA repair response to UV damage 313

(Ishibashi et al., 2005; Anderson et al., 2008). 314

A number of heat responsive proteins are differentially expressed in TBG and KA, including 315

HEAT SHOCK FACTOR 1 (HSF1) and HEAT SHOCK PROTEIN 101 (HSP101), which are both 316

expressed at higher levels in TBG, and HSFA1D which is expressed at lower levels in TBG than 317

in KA (Fig. 5B). HSF1 and HSFA1D are members of a four-gene family of Class A heat shock 318

factors, which are regulators of heat-shock response and other abiotic stress responses (Liu et 319

al., 2011; Yoshida et al., 2011). Overexpression of HSF1 in A. thaliana induces tolerance to 320

heat shocks (Qian et al., 2014) but its absence does not completely impede acquired thermo-321

tolerance (Liu and Charng, 2012). HSP101 also plays a role in acquired thermotolerance 322

(Gurley, 2000; Hong and Vierling, 2000; Queitsch et al., 2000; Hong and Vierling, 2001). 323

Additional modulators of thermotolerance FK506 BINDING PROTEIN 62 (FKBP62), 324

GALACTINOL SYNTHASE 1 (GOLS1), and VPS53 (Lobstein et al., 2004; Lee et al., 2006; 325

Wang et al., 2011), are also among our top differentially expressed genes. 326

The generally high constitutive expression of heat responsive genes in TBG led us to 327

hypothesize that heat tolerance of TBG might be elevated relative to KA. To test this, we 328

exposed 5-day-old KA and TBG seedlings to a 45°C heat shock for 1 hour, with or without an 329

acclimation treatment at 37°C for 3 hours (see methods), which allows us to assay basal and 330

acquired tolerance, respectively. After a five-day recovery period at 20°C, we screened 331

seedlings for partially or totally bleached cotyledons. After heat shock without prior acclimation 332

fewer than 20% of TBG seedlings showed signs of bleaching after five days, while more than 333

95% of KA seedlings were partially or entirely bleached (Fig. 6). When acclimated at 37°C two 334



21

days before heat-shock, both lines performed similarly with little or no bleaching. This fits with 335

constitutive differences in expression of heat response genes between KA and TBG associated 336

with higher basal tolerance to heat-shock by the railway line, while KA retains a capacity for 337

acquired tolerance. 338

Evidence of selection in the railway population 339

We next looked for evidence of genetic differentiation that might be responsible for the 340

abrogation of the vernalization response and/or constitutive induction of stress responses in 341

TBG relative to KA. To do so we first complemented our previously generated genome 342



22

sequence data for A. arenosa (Hollister et al., 2012) by sequencing a total of 8 KA and 7 TBG 343

individuals, which samples 32 and 28 copies of each chromosome, respectively. To identify 344

candidate genomic regions showing habitat-associated genetic differentiation, we used FST 345

(Weir, 1990), which is generally low among tetraploid A. arenosa populations (0.047 - 0.063) 346

(Hollister et al., 2012), as well as Fay and Wu’s H, a statistic sensitive to an excess of high-347

frequency variants compared to neutral expectations (Fay and Wu, 2000). 348

We identified 20 genes that showed evidence of strong differentiation between TBG and KA 349

(Table 1). With respect to the expression differences in cold and heat response, one candidate 350

stood out: LATE ELONGATED HYPOCOTYL (LHY) which plays a central role in the regulation 351

of the plant circadian clock (Alabadí et al., 2001), but is also known to broadly affect 352

downstream cold-response genes (Vogel et al., 2005; Bieniawska et al., 2008). LHY is an outlier 353

for Fay and Wu’s H in TBG but not in KA; nucleotide diversity measured by the number of 354

pairwise differences (π) is lower in TBG than in KA (Fig. S3A), and 22 derived polymorphisms 355

have significantly higher frequencies in TBG than in KA (average 82% vs 37%) in a region 356

concentrated around exons 6 and 7 (Fig. S3B). These patterns are consistent with the 357

hypothesis that TBG experienced positive selection on LHY. 20 of these polymorphisms fall 358

within the coding sequence of LHY and 14 are non-synonymous. These 14 polymorphisms are 359

all distributed along exons 6 and 7 with a dense cluster positioned at the beginning of exon 7 360

(Fig. S3C). Of these 14 polymorphisms, two induce a strong change of hydrophobicity of the 361

amino-acids they encode: acidic glutamic acid (E) vs. hydrophobic glycine (G) and one a charge 362

change: glutamic acid (E) vs basic lysine (K) (Fig. S3C). 363

To ask whether the amino acids changes in TBG all lie on the same haplotype, we first cloned 364

and sequenced a fosmid of the LHY locus from a TBG individual. The fosmid clone carried the 365

derived alleles at all 22 positions, showing that the derived polymorphisms are all found together 366

on a single haplotype that seems to have been the target of selection in TBG. We then cloned 367



23

and sequenced additional PCR products from another TBG plant and found the same to be true 368

for the exon 6/7 region in this individual as well. Since the derived polymorphisms were all 369

present also in KA, albeit at low frequency, we asked if there were also all found on a single 370

haplotype in KA identical to the haplotype found in KA. We cloned and sequenced PCR 371

products from the exon 6/7 region and confirmed first that the derived polymorphisms were rare 372

in KA, but also that no KA haplotype within our sampling had all of the derived polymorphisms 373

together. The rare derived polymorphisms in KA are in blocks of up to 18 of the 22 derived 374

polymorphisms (Fig. S4). In each case, a single recombination event between two haplotypes 375

would suffice to toggle between the haplotype found in TBG and rare haplotypes present in KA. 376

377

378



24

DISCUSSION 379

Here we investigated the molecular basis of phenotypic differences between two A. arenosa 380

populations, one of which has “weedy” traits associated with colonization of railways in flatland 381

Europe. The ancestral form usually inhabits shaded sites in hills or mountains, often in forests. 382

These two distinct types correspond to a previously recognized distinction between a “flatland” 383

and “mountain” type within A. arenosa (Scholz, 1962). We previously showed that all railway 384

plants we have sampled are members of a single genetically distinct lineage within tetraploid A. 385

arenosa that diverged from mountain lineages fewer than 15,000 generations ago (Arnold et al., 386

2015). This suggests that the “weedy” phenotype of railway plants evolved once within A. 387

arenosa, followed by spread of this lineage throughout flatland Europe. We show here that the 388

“weedy” phenotype of A. arenosa includes rapid cycling, abundant inflorescence growth, a loss 389

of vernalization requirement, loss of other traits associated with perenniality, and constitutive 390

stress tolerance. These are hallmarks of an “all-in” phenotype commonly observed in weedy 391

colonizers (Baker, 1965; Grotkopp et al., 2002; Blair and Wolfe, 2004; Burns, 2004; Hall and 392

Willis, 2006). The phenotypes observed in weedy A. arenosa likely reflect that railway sites are 393

sunnier and more exposed to other abiotic stresses, including more rapid temperature 394

fluctuations than would generally be experienced in the usually forested outcrop sites where 395

most other A. arenosa populations are found. Though these types of adaptations are not 396

uncommon for plants found in unpredictable and often human-associated habitats, their 397

molecular basis has remained largely unknown. 398

Using transcriptome and phenotypic analyses we found evidence that a major feature of 399

colonization of ruderal railway sites in A. arenosa is that responses to heat and cold that are 400

inducible in mountain accessions became constitutive in railway accessions. These features 401

include reproductive initiation, heat shock resistance, and freezing tolerance. Railway plants 402

also exhibit perpetual flowering and are heavily branched, while mountain plants flower more 403



25

modestly and return to vegetative growth after flowering, paralleling a distinction previously 404

described in A. alpina of episodic vs perpetual flowering (Wang et al., 2009). This fits with the 405

description of mountain accessions as perennial and ruderal railway accessions as rapid-cycling 406

annuals, suggesting that loss of perennial life history traits also accompanied the transition to 407

weediness in A. arenosa. 408

One of the most differentially expressed genes when comparing railway and mountain plants 409

was FLC, which is almost undetectable at any timepoint in the rapid-cycling railway plants. This 410

gene has been frequently identified as a cause for independent transitions to rapid cycling and 411

loss of vernalization sensitivity in A. thaliana (Méndez-Vigo et al., 2011; Guo et al., 2012). In A. 412

alpina, an ortholog of FLC, PEP1, has been linked to a switch between late flowering perennial 413

life habits and rapid and perpetual flowering (Wang et al., 2009; Albani et al., 2012), but whether 414

this FLC homologue is causal in A. arenosa remains to be tested. The low expression of FLC in 415

the railway form, or its downregulation in the mountain form upon vernalization, is strongly 416

correlated with an up-regulation of floral promoters, including SOC1. This is also consistent with 417

the known repression exerted by the FLC-SVP complex on SOC1 in A. thaliana (Michaels, 418

2001; Li et al., 2008). Similarly, SPL transcription factors which redundantly promote both 419

vegetative phase change and flowering in A. thaliana (Schwarz et al., 2008; Wang et al., 2008) 420

are constitutively expressed in railway plants, and are initially absent but upregulated during the 421

vernalization period in the mountain plants. Thus in general floral promoters are constitutively 422

expressed in the railway accession, and induced by vernalization in the mountain form, where 423

their expression is anticorrelated with FLC expression. This suggests that the vernalization and 424

flowering responses in A. arenosa, as well as the implication of FLC in life history changes is 425

consistent with findings in A. thaliana and related species. 426

In plants from the KA mountain site, FLC is initially expressed at very high levels and rapidly 427

repressed during exposure to prolonged cold, just as it is in A. thaliana (Sung and Amasino, 428



26

2004; Coustham et al., 2012). However, as the plants begin to flower after a return to warm 429

conditions, FLC expression returns to pre-vernalization levels within about three weeks. This 430

suggests a mechanism similar to what is found in A. alpina, where meristems switch from 431

vegetative to reproductive fate during vernalization, and any meristem arising during or after 432

vernalization remains vegetative, leading to episodic flowering cycles characteristic of 433

perennials (Wang et al., 2009). This cylical FLC expression could explain the formation of 434

secondary rosettes as branches from basal rosettes in A. arenosa (Fig 1). We also observed 435

this phenotype in diploid A. arenosa suggesting it is ancestral (not shown). Paralleling 436

phenotypes reported in A. alpina (Albani et al., 2012), these secondary rosettes require an 437

additional vernalization treatment to flower. These secondary rosettes can form roots and allow 438

the plants to make use of vegetative reproduction. In A. alpina there are two PEP1 transcripts 439

and these show different expression patterns thought to be associated with the perennial life-440

cycle of this species (Albani et al., 2012). In A. arenosa there are also two full-length FLC genes 441

(Nah and Chen, 2010) but we detected no significant difference in the response of the two 442

paralogs to vernalization: AaFLC1 was expressed at higher levels than AaFLC2, but this 443

difference remains consistent over our time-course. 444

From our transcriptome analyses, we found that the railway plants have a generally strongly 445

dampened vernalization response. Almost 6 times more genes were vernalization responsive in 446

the mountain accession KA than the railway accession TBG, but for 60% of them, the stronger 447

magnitude of response in KA is nonetheless log-linearly correlated with a weaker response in 448

railway plants, suggesting that the vernalization response is strongly abrogated but not 449

completely absent in the railway plants. 450

We also found that reduced vernalization responsiveness in railway plants was coupled with a 451

constitutively high expression of a number of cold- and heat-response genes. A cross-talk 452

between flowering and cold-response has been described in A. thaliana and is associated with 453



27

the flowering regulators SOC1, FLC and FVE (Kim et al., 2004; Seo et al., 2009; Richter et al., 454

2013). Several COR genes are induced during vernalization in mountain A. arenosa plants, 455

including COR15A, COR15B, COR47, COR314, and COR78 and reach higher levels after 456

vernalization in mountain than in railway plants. COR genes are an essential component of the 457

cold-acclimation response (Thomashow, 1999). The same genes, however, show higher 458

expression before vernalization in railway plants than in mountain plants. The ability to cold-459

acclimate increases freezing tolerance of a plant after exposure to low-temperature, and 460

freezing tolerance has been shown to correlate with winter temperatures in natural accessions 461

of A. thaliana (Hannah et al., 2006). For A. arenosa, we found that (fitting with COR gene 462

expression trends) the mountain accession showed a much greater capacity to cold-acclimate 463

than the railway accession, but among un-acclimated plants, those from railways had a higher 464

basal tolerance to freezing than mountain plants. This is consistent with results from expression 465

a CBF1 overexpressing A. thaliana mutant which has high expression of the COR genes as well 466

as enhanced freezing tolerance (Jaglo-Ottosen, 1998), as well as findings that naturally 467

increased non-acclimated freezing tolerance can result from the constitutive activation of the 468

CBF pathway (Hannah et al., 2006). 469

The COR genes are also implicated in the response to dehydration (Liu, 1998; Shinozaki and 470

Yamaguchi-Shinozaki, 2000). GALACTINOL SYNTHASE 1 (AtGOLS1), which is constitutively 471

over-expressed in the railway plants, is involved in the accumulation of galactinol and raffinose 472

(Panikulangara et al., 2004), two compounds known for their protective properties against 473

oxidative stress (Nishizawa et al., 2008) and is involved in drought, cold and high-salinity 474

stresses (Taji et al., 2002). Therefore constitutive over-expression of the COR genes, as well as 475

AtGOLS1, could possibly also reflect selection for higher drought tolerance in the railway 476

environment, where soil is drier and more exposed to water loss in the heat of summer. Perhaps 477

constitutive freezing and drought tolerance could both have arisen as pleiotropic effects of 478



28

alterations of COR gene expression during adaptation to railway habitats. 479

In addition to cold tolerance genes, we saw a similar shift toward constitutive expression in 480

railway plants of heat-response associated genes. This includes HSF1, known in A. thaliana to 481

be involved in thermo-tolerance (Qian et al., 2014), and HSP101, a key component of acquired 482

thermotolerance (Gurley, 2000; Hong and Vierling, 2000; Queitsch et al., 2000; Hong and 483

Vierling, 2001). Heat shock proteins (HSPs) are molecular chaperones rapidly activated by the 484

binding of heat shock transcription factors (HSFs) in response to environmental stresses such 485

as heat-stress or other proteotoxic stresses as drought or freezing (Schoffl, 1998). 21 HSFs 486

genes have been annotated in A. thaliana (Nover et al., 2001), but the HSFA1s (a, b, c, and d) 487

constitute the main transcriptional activators in response to heat-shock (Yoshida et al., 2011). 488

Overexpression of HSF1 (HSFA1a) leads to stronger induction of HSPs by heat-shock and 489

increased stress-tolerance, but not to acquisition of basal thermo-tolerance as observed in 490

HSFA1b over-expressing plants (Prändl et al., 1998; Qian et al., 2014). Indeed, HSF1 requires 491

stress-induced formation of homo-trimers to be activated and accumulate in the nucleus 492

(Yoshida et al., 2011; Liu et al., 2013). Here, we observed in the railway accession constitutively 493

high expression of HSF1 and HSP101 correlated with an increased basal thermo-tolerance. 494

Together, these patterns of over-expression of heat-shock genes suggest a constitutive 495

activation of the heat-shock response pathway in the railway accession, which was corroborated 496

by high basal heat shock tolerance of these plants: seedlings of railway plants show stronger 497

heat-shock tolerance than those of mountain plants, but we detected no difference in the 498

acquired thermo-tolerance of the two types. Acquisition of constitutive thermo-tolerance, thus 499

bypassing the requirement for a priming event, may be a significant advantage for populations 500

colonizing habitats like railways, where they are more likely to be exposed to abrupt 501

temperature fluctuations (Zerebecki and Sorte, 2011). 502

Given that the mountain and railway A. arenosa plants show clearly distinct environmental 503



29

response phenotypes that are likely adaptive to their respective habitats, we used a genome-504

scanning approach to ask if any genomic regions show evidence of selection. By our criteria, 20 505

genes in the genome showed evidence of having been under selection in the railway population. 506

The encoded proteins are important for a variety of processes, and a few have possible 507

implications for the differences between railway and mountain types: CATION/H+ EXCHANGER 508

6B (ATCHX6B) and ORGANIC CATION TRANSPORTER4 (AtOCT4) are both members of 509

gene families involved in cation transmembrane transport (Remy et al., 2012; Ye et al., 2013), 510

and NITRITE REDUCTASE 1 (ATHNIR) is involved in nitrate response (Konishi and 511

Yanagisawa, 2010) which together hint at possible adaptation to substrate differences. This may 512

be relevant as KA from a high pH limestone site (which is likely the ancestral habitat for A. 513

arenosa) and TBG is from railway ballast in the Black Forest, an acidic silicaceous region. LA 514

RELATED PROTEIN 1A (ATLARP1A) is required for the heat-dependent degradation of mRNA 515

involved in thermotolerance of A. thaliana, with consequences for its acclimation capacity 516

(Merret et al., 2013). AUTOPHAGY 9 (APG9) mutants have accelerated seed set and 517

senescence (Hanaoka et al., 2002), which may be related to the senescence difference 518

between the rapid-cycling TBG and the perennial mountain type, KA. 519

For the overall control of stress responsiveness, one candidate target of selection stood out: the 520

circadian clock regulator LHY. In A. thaliana LHY is known to affect flowering, albeit indirectly 521

(Schaffer et al., 1998; Mizoguchi et al., 2002), but also cold-responsiveness (Vogel et al., 2005; 522

Bieniawska et al., 2008) and freezing tolerance (Bieniawska et al., 2008; Espinoza et al., 2008; 523

Nakamichi et al., 2009; Dong et al., 2011). Double mutants for LHY and another circadian 524

regulator, CCA1, show a greatly diminished induction of cold responses and the COR genes 525

including COR15A, COR47, and COR78 (Dong et al., 2011) that were differentially expressed 526

among our A. arenosa strains. Thus it is enticing to hypothesize that the derived variant of LHY 527

that seems to have been under selection in railway plants may somehow lead to a change in the 528



30

regulation of downstream stress tolerance, as well as possibly flowering responses. Whether 529

LHY variation is actually responsible for the phenotypic differences in stress tolerance or 530

flowering we observe between these mountain and railway populations remains to be tested. 531

Overall, we found that an A. arenosa lineage that adapted to railway sites in flatland Europe 532

evolved features commonly observed in “weedy” plants found in human-associated habitats 533

including rapid cycling, perpetual flowering, extensive inflorescence growth, and constitutive 534

heat and cold tolerance (Baker, 1965; Grotkopp et al., 2002; Blair and Wolfe, 2004; Burns, 535

2004; Hall and Willis, 2006). These phenotypes are all inducible in the mountain accession. 536

Thus there is a general trend that normally inducible phenotypes have become constitutive in 537

the weedy A. arenosa form, which was likely important in the colonization of a volatile and risky 538

human associated habitat. The fact that these A. arenosa populations are autotetraploids 539

appears to be in line with a strong potential for habitat colonization and transitions to weediness 540

by polyploids (Soltis and Soltis, 2000; Pandit et al., 2006; Prentis et al., 2008). However, it is 541

clear that in this case, neither weediness nor other traits associated with the ruderal railway 542

habitats were immediate consequences of genome duplication. Among five tetraploid A. 543

arenosa lineages we have sampled, only one successfully colonized ruderal habitats (Arnold et 544

al., 2015), and we show here it has distinct phenotypic traits consistent with specific adaptations 545

to that habitat not shared by other tetraploids. Thus, while colonization of the railway habitat was 546

perhaps facilitated by e.g. increased genetic diversity available in tetraploids (Otto et al., 2007; 547

Hollister et al., 2012; Arnold et al., 2015), the autotetraploids as a group are not globally tolerant 548

of ruderal habitats and adaptation was required post-polyploidy for this colonization. 549

550

MATERIALS AND METHODS 551

Plant materials and growth conditions 552



31

We collected seeds from natural populations in June and July 2009 – 2011. All populations are 553

autotetraploid; all originate from regions where only autotetraploids occur (Jørgensen et al., 554

2011) and ploidy of a subset of individuals from each population was confirmed using flow 555

cytometry (Hollister et al., 2012). For flowering time phenotyping, we grew 48 single progeny 556

from each of several individuals per population. Plants were grown as previously described 557

(Hollister et al., 2012) in Conviron MTPC-144 chambers with 8 hours dark at 12°C, 4 hours light 558

(Cool-white fluorescent bulbs) at 18°C, 8 hours light at 20°C, 4 hours light at 18°C. A subset 559

(24) of four week old plants were transferred to a chamber running with a constant temperature 560

of 4°C and short days (8 hours light) for eight weeks and then returned to warm and long-day 561

conditions. 562

For the transcriptomic time-series, we grew arrays of 48 siblings from seeds harvested from 563

single individuals growing in nature. Plants were grown under similar growth conditions in three 564

flats in which we mixed TBG and KA plants in order to avoid flat effects. Half of the plants from 565

each flat were vernalized for 6 weeks before being returned to their flat of origin. For our RNA 566

extractions, we used tissue from young rosette leaves from both vernalized and unvernalized 567

plants using one biological replicate from each flat. Leaves were harvested every 7-days after 9 568

to 10 hours from Zeitgeber time (ZT) = 0 in long-days conditions, and after 5 to 6 hours in short-569

days. ZT = 0 is defined as the time of lights-on. 570

Phenotyping of flowering time 571

Using germination date recorded as the first date when root tip emergence was evident on agar 572

plates, we measured flowering time as the time to first open flower. We calculated flowering 573

time for vernalized plants based on the total number of growing days excluding the cold 574

treatment. For plants that had not flowered by experiment end (200 days) we assigned these 575

cutoff values. Phenotypic values for time to first open flower were not normally distributed even 576



32

after transformation (Shapiro-Wilk W test, p < 0.0001), so we used non-parametric Wilcoxon-577

tests to assess the significance of differences among populations. 578

RNA isolation, sequencing and expression analysis 579

We extracted RNA using the RNeasy Plant Mini Kit (Qiagen). We synthesized single strand 580

cDNA from 500ng of total RNA using VN-anchored poly-T(23) primers with MuLV Reverse 581

Transcriptase (Enzymatics) according to the manufacturer’s recommendations. q-PCR was 582

carried out on a Stratagene Mx3005P machine (Stratagene) with an annealing temperature of 583

55°C by using Taq DNA polymerase (New-England BioLabs). Reactions were carried out in 584

triplicate, and we normalized FLC expression against expression of ACTIN using the 2–CT 585

method taking into account each primer’s efficiency as described in BIO-RAD Real Time PCR 586

Applications Guide. The standard deviation of each biological replicate was calculated using a 587

first order propagation of error formula on the variance of the technical replicates. We used 588

cDNA-specific primers 5’-CAGCTTCTCCTCCGGCGATAACCTGG-3’ and 5’-589

GGCTCTGGTTACGGAGAGGGCA-3’ for FLC (87% efficiency) and 5’-590

CGTACAACCGGTATTGTGCTGGAT-3’ and 5’-ACAATTTCCCGCTCTGCTGTTGTG-3’ for ACT 591

(91% efficiency). 592

We prepared RNAseq libraries using the TruSeq RNA Sample Prep Kit v2 (Illumina) on RNA 593

samples from both vernalized and unvernalized plants at four time points (3, 4, 9 and 13 594

weeks). Libraries were sequenced on an Illumina HiSeq 2000 with 50bp single-end reads. We 595

sequenced between 9.8 and 18.8 million reads (avg 13.6 million). We aligned reads to the A. 596

lyrata genome (Hu et al., 2011) using TopHat2 (Kim et al., 2013) and re-aligned unmapped 597

reads using Stampy (Lunter and Goodson, 2011). We acquired read counts for each of the 598

32,670 genes using HTseq-count (Anders et al., 2015) with A. lyrata gene models (Hu et al., 599

2011). We normalized for sequencing depth using DEseq2 in R (Anders and Huber, 2010). 600



33

Further analyses were performed in MATLAB (MathWorks) except gene-ontology (GO) 601

enrichment analyses realized with Bioconductor package GOstats (Falcon and Gentleman, 602

2006) in RStudio (RStudio). RNAseq read data have been deposited in the NCBI SRA database 603

under accession number SRP070489 within the NCBI BioProject PRJNA312410. 604

605

We obtained estimates of differential expression through the time-series using a combination of 606

two tests, a Kruskall-Wallis and a 2-way ANOVA coded on MATLAB. We used the first as a 607

non-parametric ranking test within each condition and accession, and this allowed us to detect 608

significant effects of time on the expression level of each gene within a time-series without 609

assuming normal distribution of gene counts. We then used a 2-way ANOVA to account for 610

paired data, screen for time-series effects and generate comparisons of gene expression 611

profiles between time series. We combined the results of these tests into 7 categories of gene 612

expression profiles for each pairwise comparison between time-series, of which two reflect the 613

response to vernalization (Fig. 3A - “a” and “b”). 614

Global expression differences were estimated using a Kruskall-Wallis tests between TBG and 615

KA within each condition (vernalized and non-vernalized). The p-values obtained were then 616

corrected for False Discovery Rate (FDR) using the linear step-up (LSU) procedure originally 617

introduced by (Benjamini and Hochberg, 1995). For each gene, the two q-values thus obtained 618

for each condition were then summed in order to establish the 1% most differentiated genes 619

with the lowest sum (QQ50 in Table S2). Genes with a normalized gene count below 50 across 620

all time-points, genotypes, and conditions were excluded in order to filter from this 1%-subset 621

genes with high relative but low absolute differences. 622

Heat Stress 623



34

We adapted a protocol by (Meiri and Breiman, 2009) to Arabidopsis arenosa. Seedlings were 624

germinated on plates containing MS medium, for 5–14 days. After 1 week at 4°C in the dark for 625

stratification, seeds were grown on plates at 20°C under long-day conditions (16 h light, 8 h 626

dark). 3-day-old seedlings were incubated for 3 h at 37°C in an incubator, and then returned to 627

recovery conditions of 22°C under long days (16 h light, 8 h dark) for 2 days (see figure 628

legends). For thermotolerance bioassays, the plates were then incubated for 60 min at 45°C 629

under light. After the 45°C treatment, the plates were incubated at 20°C for recovery under long-630

day conditions (16 h light, 8 h dark) for another 5 days. 631

Freezing Tolerance 632

Cold tolerance was assessed after a week of acclimation at 4°C. Fully expanded leaves of 7 633

weeks old plants were harvested and placed in glass test tubes containing 0.4 mL deionized 634

water. The tubes were placed on ice and extracellular freezing of the leaf tissues was initiated 635

by the addition of deionized ice chips to each tube. After transfer to the controlled freezing bath 636

set at 0°C, and a 1 hour equilibration period, the samples were cooled at 2°C/h to - 6°C. The 637

tubes were withdrawn after 30 mins at - 6°C, placed on ice and thawed overnight at 4°C. After 638

thawing, 12 ml deionized water was added to each tube, and tubes were shaken gently (200 639

rpm) at room temperature for 3 hours. Conductivity of the extraction solution was measured with 640

an Orion conductimeter (model 105), and the leaves were frozen at -80°C for 1h30. The same 641

extraction solution was re-added to each tube after 30 mins re-equilibration at room temperature 642

and shaken for 2h30, and conductivity of the solution was measured once again to normalize by 643

the total amount of electrolytes. 644

Fosmid libraries 645

We extracted DNA from three-week-old TBG plants using a large-scale CTAB protocol 646

(Porebski et al., 1997) including treatment with pectinase (Rogstad et al., 2001). We constructed 647



35

a fosmid library using the Copy Control Fosmid Library Production Kit (Epicentre) and screened 648

it as previously described (Bomblies et al., 2007), using DIG-labeled (Roche) PCR probes to 649

LHY (primers 5’-ACGCGGTTCAAGATGCTCCCA-3’ and 5’-GCTGCAGCATGAGCAGCAGGA-650

3’). We bar-coded positive clones as in (Peterson et al., 2012), and sequenced 100bp paired-651

end reads on an Illumina HiSeq 2000. We assembled reads de novo using Velvet (Zerbino and 652

Birney, 2008). 653

Differentiation analysis 654

To test for genetic differentiation, we used our previously published genomic short read 655

sequences for A. arenosa (Yant et al. 2013; Hollister et al. 2012) that we complemented with 656

similarly processed genomes to reach a total of 8 KA and 7 TBG individuals. We aligned reads 657

to the A. lyrata genome (Hu et al., 2011) using BWA (Li and Durbin, 2009) and re-aligned 658

unmapped reads using Stampy (Lunter and Goodson, 2011). We calculated FST (Weir, 1990) 659

and Fay and Wu’s H (Fay and Wu, 2000) after genotyping the alignments with GATK (McKenna 660

et al., 2010). LHY haplotypes were sequenced from one TBG fosmid (see Fosmid libraries) and 661

PCR clones obtained from cDNA of three KA and one TBG individuals. The PCR products 662

amplified with primers 5’- TTTCCACGCGGGTATTGTGA-3’ (forward) and 5’- 663

TGTGTTCCCAACTTGGCTCT-3' (reverse) were then ligated in pBlueScript and sequenced 664

from both ends with M13 forward and reverse primers. Where more than 4 clones were 665

sequenced per individuals, only 4 different haplotypes were reported. 666

List of supplemental materials 667

Figure S1: RNA-seq expression of SOC1 and VIN3. 668

Figure S2: Marks of selection on a derived haplotype of LHY in the railway accession. 669

Figure S3: High frequency of null expression levels and/or variance among genes without 670 orthologues. 671

Figure S4: LHY haplotypes in KA and TBG. 672



36

Table S1: Vernalization Response Genes (a)+(b) 673

Table S2: 1% Most Differentially Expressed Genes 674

675

Acknowledgments 676

We thank Mary Gehring and Elena Kramer for comments and discussion on this manuscript. 677

We thank Missy Holbrook and her lab for support with stress tolerance assays, Nimrod 678

Rubinstein for his help with paralogue specific expression analyses, and Kevin Wright for helpful 679

advice across all dimensions of this work. This work was funded by a National Science 680

Foundation grant to KB (IOS – 1146465) and an award from the Jean Gaillard Memorial 681

Fellowship Fund to PB. The funders played no role in study design or interpretation. 682

683 Table 1: List of 1% Genomic Outliers for FST and Fay and Wu’s H. 684

685 TAIR ID Common Name

AT3G03510

AT3G56670

AT1G01060 LHY

AT1G08135 ATCHX6B

AT1G48090

AT1G72300 PSY1R

AT1G78770 APC6

AT3G14980 IDM1

AT2G17140

AT2G31260 APG9

AT2G41700 ABCA1

AT3G56900

AT5G10560 AT5G21160 AtLARP1a



37

AT4G32410 ANY1

AT4G25970 PSD3 AT2G24680

AT3G20660 AtOCT4

AT2G15620 ATHNIR AT3G57590

686

687

FIGURE LEGENDS 688

Figure 1. Phenotypes of railway and mountain A. arenosa plants. (A) Map of central Europe 689

with location of A. arenosa populations sampled from railway (yellow) and mountain (green) 690

sites. (B) Box plots showing flowering phenotypes of plants grown from seeds collected from 691

railway and mountain populations. Flowering time was quantified as the time from germination 692

to the first open flower for Vernalized (left) and Non-Vernalized (right) plants from both 693

accessions. Plants that did not flower by the end of the experiment (200 days) were assigned 694

200 days as their flowering date. (C) Pictures of two representative vernalized individuals taken 695

at 38 weeks. TBG plants continuously flower while KA plants revert to vegetative growth after an 696

episode of flowering. The development of secondary rosettes along branched stems of KA 697

plants can then be observed. (D) Representative greenhouse grown A. arenosa indicating 698

scored phenotypes of primary inflorescence branches (PB) and rosette branches (RB). PI 699

indicates the primary inflorescence. 700

Figure 2: Differential FLC expression and responsiveness to vernalization. (A) q-RT-PCR 701

of FLC expression relative to actin in vernalized KA and TBG plants. While undetectable in 702

TBG, FLC is suppressed by vernalization in KA but comes back to unvernalized levels after 703

plants are returned to warm conditions. (B) Single nucleotide differences between the coding 704

sequence of the two AaFLC1 and AaFLC2 paralogues in our sample. Grey boxes are exons. 705



38

Yellow = differences between AaFLC1 and AaFLC2 present in our samples as well as the 706

published BAC sequence (Nah and Chen, 2010). Black = differences between AaFLC1 and 707

AaFLC2 in the BAC not found in our accessions. Red = differences between AaFLC1 and 708

AaFLC2 in our samples but not present in the BAC. Blue = differences between AaFLC1 and 709

AaFLC2 where both paralogues differ from the BAC. (C) Expression levels of AaFLC1 as a 710

proportion of total AaFLC locus expression across the vernalized and non-vernalized time 711

series, showing the relative expression of the two FLC copies does not change by treatment or 712

through the time series. 713

Figure 3: Vernalization response differences between KA and TBG mainly due to a 714

reduced magnitude of response in TBG. (A) Venn diagram representing the 7 categories of 715

differential responses for each accession. Upper circle (grey bold) includes genes with 716

significant differential expression when comparing the vernalized and unvernalized time-series. 717

Left circle contains genes with significant differential expression among timepoints in the. 718

unvernalized time-series. Right circle contains genes with significantly different expression 719

among timepoints in the vernalized time-series. Cartoon curves show schematic vernalized 720

(black) and unvernalized (grey) expression profiles of genes found in each category. 721

“Vernalization-responsive” genes are found for each accession at the intersection between 722

upper and right circles. Within these pattern a represents genes that change across the 723

timeseries in both vernalized and unvernalized plants, but in distinct ways, while pattern b 724

includes genes that show changes in the vernalized timeseries, but not the unvernalized 725

timeseries. (B) Decomposition of each vernalization response response showing which genes 726

change in both accessions (yellow) and which are accession-specific (blue) and how they are 727

partitioned between a-category and b-category patterns (camembert diagrams). Almost 6 times 728

more genes are identified as vernalization responsive in KA compared to TBG. (C) Comparison 729

of vernalization-responsiveness in KA versus TBG. The responsiveness of a gene is calculated 730



39

for each accession as the log2 ratio of vernalized over non-vernalized expression levels. Only 731

ratios significantly different from 1 (log2 ratios different from 0) in both accessions are displayed. 732

Several genes discussed in the text are highlighted. Colors signify plot density. Dotted line 733

indicates linear regression fit line based on N=608 datapoints. The slope and R2 value for the fit 734

are given on the chart. 735

Figure 4: Expression of vernalization responsive genes in KA vs TBG. (A) Expression 736

levels of vernalization responsive genes in unvernalized KA plotted against their levels in 737

unvernalized TBG. The slope of the linear regression (0.79 with R2=0.75) indicates that 738

vernalization responsive genes have a higher expression in TBG in unvernalized plants. Known 739

cold-responsive genes are highlighted in red and in particular COR15A, COR15B, COR47, and 740

RD29A show even stronger bias toward higher constitutive expression in TBG. (B) Expression 741

levels of vernalization responsive genes in vernalized KA versus vernalized TBG. Due to the 742

stronger vernalization response in KA, the relationship is inversed compared to A (slope of 1.2 743

with R2=0.95). (C) Electrolyte leakage measured after freezing at -6°C of leaves from 7-weeks 744

old KA and TBG plants vernalized for 1 week (V; darker blue) or not vernalized (NV; light blue). 745

Two stars indicate significant differences of vernalized KA and nonvernalized TBG highlight 746

compared to the high leakage of unvernalized KA plants (t-test p-value <1%). One star denotes 747

a significant difference of vernalized TBG from the controlled leakage of unvernalized TBG (t-748

test p-value <5%). 749

Figure 5: Overall transcriptome differential expression between KA and TBG. (A) 750

Genome-wide distribution of q-values comparing KA and TBG Non-Vernalized (NV, x axis) and 751

Vernalized (V, y axis) time-series. FLC is highlighted as it is ranked third in both comparisons, 752

which makes it the most differentiated expression pattern overall. The top 1% (326 genes) 753

overall (sum of both q-values) are colored in red if a homologue is known in A. thaliana and in 754

black if not. Yellow dots represent genes with low expression across all time-points, genotypes, 755



40

and conditions and therefore excluded from further consideration in the top 1% subset. (B) 756

Expression heatmap of genes that are both within the 1% most differentiated and associated 757

with the GO category “Response to Stimulus” (GO:0050896). For each gene, the mean 758

expression of both vernalized (V) and non-vernalized (NV) time-series is given for KA and TBG. 759

Expression is given in normalized gene counts. 760

Figure 6: Constitutive heat-shock tolerance in railway plants. Percentage of seedlings 761

showing partial or total bleaching of their cotyledons and leaves after heat shock treatment. H = 762

healthy after treatment (green), B = bleached after treatment (orange). “Acclimated” seedlings 763

were submitted to a 3-hour 37°C pre-treatment two days prior to one hour heat shock at 45°C, 764

while “non-acclimated” seedlings were directly incubated for 1 hour at 45°C. Bleaching was 765

often non-lethal even for KA plants. 766

767

768

769

770



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http://scholar.google.com/scholar?as_q=Identification of a nitrate-responsive cis-element in the Arabidopsis NIR1 promoter defines the presence of multiple cis-regulatory elements for nitrogen response&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Konishi&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Mol Biol Evol%5BTitle%5D%29 AND 25%5BVolume%5D AND 319%5BPagination%5D AND Kuittinen H%2C Niittyvuopio A%2C Rinne P%2C Savolainen O%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kuittinen H, Niittyvuopio A, Rinne P, Savolainen O (2008) Natural variation in Arabidopsis lyrata vernalization requirement conferred by a FRIGIDA indel polymorphism. Mol Biol Evol 25: 319-329

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

http://scholar.google.com/scholar?as_q=Natural variation in Arabidopsis lyrata vernalization requirement conferred by a FRIGIDA indel polymorphism&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Natural variation in Arabidopsis lyrata vernalization requirement conferred by a FRIGIDA indel polymorphism&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kuittinen&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Mol Biol Evol%5BTitle%5D%29 AND 19%5BVolume%5D AND 1261%5BPagination%5D AND Le Corre V%2C Roux F%2C Reboud X%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Le Corre V, Roux F, Reboud X (2002) DNA polymorphism at the FRIGIDA gene in Arabidopsis thaliana: Extensive nonsynonymous variation is consistent with local selection for flowering time. Mol Biol Evol 19: 1261-1271

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

http://scholar.google.com/scholar?as_q=DNA polymorphism at the FRIGIDA gene in Arabidopsis thaliana: Extensive nonsynonymous variation is consistent with local selection for flowering time&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=DNA polymorphism at the FRIGIDA gene in Arabidopsis thaliana: Extensive nonsynonymous variation is consistent with local selection for flowering time&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Le&as_ylo=2002&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Planta%5BTitle%5D%29 AND 224%5BVolume%5D AND 330%5BPagination%5D AND Lee C%2DF%2C Pu H%2DY%2C Wang L%2DC%2C Sayler RJ%2C Yeh C%2DH%2C Wu S%2DJ%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Lee C-F, Pu H-Y, Wang L-C, Sayler RJ, Yeh C-H, Wu S-J (2006) Mutation in a homolog of yeast Vps53p accounts for the heat and osmotic hypersensitive phenotypes in Arabidopsis hit1-1 mutant. Planta 224: 330-338

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

http://scholar.google.com/scholar?as_q=Mutation in a homolog of yeast Vps53p accounts for the heat and osmotic hypersensitive phenotypes in Arabidopsis hit1-1 mutant&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=Mutation in a homolog of yeast Vps53p accounts for the heat and osmotic hypersensitive phenotypes in Arabidopsis hit1-1 mutant&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Lee&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28PLoS Genet%5BTitle%5D%29 AND 1%5BVolume%5D AND 109%5BPagination%5D AND Lempe J%2C Balasubramanian S%2C Sureshkumar S%2C Singh A%2C Schmid M%2C Weigel D%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Lempe J, Balasubramanian S, Sureshkumar S, Singh A, Schmid M, Weigel D (2005) Diversity of flowering responses in wild Arabidopsis thaliana strains. PLoS Genet 1: 109-118

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

http://scholar.google.com/scholar?as_q=Diversity of flowering responses in wild Arabidopsis thaliana strains&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=Diversity of flowering responses in wild Arabidopsis thaliana strains&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Lempe&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Dev Cell%5BTitle%5D%29 AND 15%5BVolume%5D AND 110%5BPagination%5D AND Li D%2C Liu C%2C Shen L%2C Wu Y%2C Chen H%2C Robertson M%2C Helliwell CA%2C Ito T%2C Meyerowitz E%2C Yu H%5BAuthor%5D&dopt=abstract

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

http://scholar.google.com/scholar?as_q=A repressor complex governs the integration of flowering signals in Arabidopsis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=A repressor complex governs the integration of flowering signals in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Li&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Bioinformatics%5BTitle%5D%29 AND 25%5BVolume%5D AND 1754%5BPagination%5D AND Li H%2C Durbin R%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=Fast and accurate short read alignment with Burrows-Wheeler transform&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=Fast and accurate short read alignment with Burrows-Wheeler transform&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Li&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1


Liu H, Charng Y (2012) Acquired thermotolerance independent of heat shock factor A1 (HsfA1), the master regulator of the heatstress response. Plant Signal Behav 7: 547-550


Liu H-C, Liao H-T, Charng Y-Y (2011) The role of class A1 heat shock factors (HSFA1s) in response to heat and other stresses inArabidopsis. Plant Cell Environ 34: 738-751


Liu Q (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signaltransduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391-1406


Liu Y, Zhang C, Chen J, Guo L, Li X, Li W, Yu Z, Deng J, Zhang P, Zhang K, et al (2013) Arabidopsis heat shock factor HsfA1a directlysenses heat stress, pH changes, and hydrogen peroxide via the engagement of redox state. Plant Physiol Biochem 64: 92-98


Lobstein E, Guyon A, Férault M, Twell D, Pelletier G, Bonhomme S (2004) The putative Arabidopsis homolog of yeast vps52p isrequired for pollen tube elongation, localizes to Golgi, and might be involved in vesicle trafficking. Plant Physiol 135: 1480-1490


Lunter G, Goodson M (2011) Stampy: A statistical algorithm for sensitive and fast mapping of Illumina sequence reads. GenomeRes 21: 936-939


Maruyama K, Sakuma Y, Kasuga M, Ito Y, Seki M, Goda H, Shimada Y, Yoshida S, Shinozaki K, Yamaguchi-Shinozaki K (2004)Identification of cold-inducible downstream genes of the Arabidopsis DREB1A/CBF3 transcriptional factor using two microarraysystems. Plant J 38: 982-993


Mckay JK, Richards JH, Mitchell-Olds T (2003) Genetics of drought adaptation in Arabidopsis thaliana: I. Pleiotropy contributes togenetic correlations among ecological traits. Mol Ecol 12: 1137-1151


McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, et al (2010)The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20:1297-1303


Meiri D, Breiman A (2009) Arabidopsis ROF1 (FKBP62) modulates thermotolerance by interacting with HSP90.1 and affecting theaccumulation of HsfA2-regulated sHSPs. Plant J 59: 387-99


Méndez-Vigo B, Picó FX, Ramiro M, Martínez-Zapater JM, Alonso-Blanco C (2011) Altitudinal and climatic adaptation is mediated byflowering traits and FRI, FLC, and PHYC genes in Arabidopsis. Plant Physiol 157: 1942-1955


Méndez-Vigo B, Savic M, Ausín I, Ramiro M, Martín B, Picó FX, Alonso-Blanco C (2015) Environmental and genetic interactionsreveal FLOWERING LOCUS C as a modulator of the natural variation for the plasticity of flowering in Arabidopsis. Plant CellEnviron 39: 282-294


Merret R, Descombin J, Juan Y, Favory J-J, Carpentier M-C, Chaparro C, Charng Y, Deragon J-M, Bousquet-Antonelli C (2013)XRN4 and LARP1 are required for a heat-triggered mRNA decay pathway involved in plant acclimation and survival during thermalstress. Cell Rep 5: 1279-1293

Pubmed: Author and Title www.plantphysiol.orgon July 4, 2020 - Published by Downloaded from Copyright © 2016 American Society of Plant Biologists. All rights reserved.

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Signal Behav%5BTitle%5D%29 AND 7%5BVolume%5D AND 547%5BPagination%5D AND Liu H%2C Charng Y%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Liu H, Charng Y (2012) Acquired thermotolerance independent of heat shock factor A1 (HsfA1), the master regulator of the heat stress response. Plant Signal Behav 7: 547-550

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

http://scholar.google.com/scholar?as_q=Acquired thermotolerance independent of heat shock factor A1 (HsfA1), the master regulator of the heat stress 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

http://scholar.google.com/scholar?as_q=Acquired thermotolerance independent of heat shock factor A1 (HsfA1), the master regulator of the heat stress response&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Liu&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell Environ%5BTitle%5D%29 AND 34%5BVolume%5D AND 738%5BPagination%5D AND Liu H%2DC%2C Liao H%2DT%2C Charng Y%2DY%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Liu H-C, Liao H-T, Charng Y-Y (2011) The role of class A1 heat shock factors (HSFA1s) in response to heat and other stresses in Arabidopsis. Plant Cell Environ 34: 738-751


http://scholar.google.com/scholar?as_q=The role of class A1 heat shock factors (HSFA1s) in response to heat and other stresses in Arabidopsis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The role of class A1 heat shock factors (HSFA1s) in response to heat and other stresses in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Liu&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Two%5BTitle%5D%29 AND 2%5BVolume%5D AND with an EREBP%2FAP2 DNA binding domain separate two cellular signal transduction pathways in drought%5BPagination%5D AND Liu Q%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Liu Q (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10: 1391-1406



http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Liu&as_ylo=1998&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Physiol Biochem%5BTitle%5D%29 AND 64%5BVolume%5D AND 92%5BPagination%5D AND Liu Y%2C Zhang C%2C Chen J%2C Guo L%2C Li X%2C Li W%2C Yu Z%2C Deng J%2C Zhang P%2C Zhang K%2C et al%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Liu Y, Zhang C, Chen J, Guo L, Li X, Li W, Yu Z, Deng J, Zhang P, Zhang K, et al (2013) Arabidopsis heat shock factor HsfA1a directly senses heat stress, pH changes, and hydrogen peroxide via the engagement of redox state. Plant Physiol Biochem 64: 92-98


http://scholar.google.com/scholar?as_q=Arabidopsis heat shock factor HsfA1a directly senses heat stress, pH changes, and hydrogen peroxide via the engagement of redox state&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Arabidopsis heat shock factor HsfA1a directly senses heat stress, pH changes, and hydrogen peroxide via the engagement of redox state&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Liu&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Physiol%5BTitle%5D%29 AND 135%5BVolume%5D AND 1480%5BPagination%5D AND Lobstein E%2C Guyon A%2C F�rault M%2C Twell D%2C Pelletier G%2C Bonhomme S%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Lobstein E, Guyon A, F�rault M, Twell D, Pelletier G, Bonhomme S (2004) The putative Arabidopsis homolog of yeast vps52p is required for pollen tube elongation, localizes to Golgi, and might be involved in vesicle trafficking. Plant Physiol 135: 1480-1490

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

http://scholar.google.com/scholar?as_q=The putative Arabidopsis homolog of yeast vps52p is required for pollen tube elongation, localizes to Golgi, and might be involved in vesicle trafficking&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 putative Arabidopsis homolog of yeast vps52p is required for pollen tube elongation, localizes to Golgi, and might be involved in vesicle trafficking&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Lobstein&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Genome Res%5BTitle%5D%29 AND 21%5BVolume%5D AND 936%5BPagination%5D AND Lunter G%2C Goodson M%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Lunter G, Goodson M (2011) Stampy: A statistical algorithm for sensitive and fast mapping of Illumina sequence reads. Genome Res 21: 936-939

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

http://scholar.google.com/scholar?as_q=Stampy: A statistical algorithm for sensitive and fast mapping of Illumina sequence reads&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=Stampy: A statistical algorithm for sensitive and fast mapping of Illumina sequence reads&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Lunter&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant J%5BTitle%5D%29 AND 38%5BVolume%5D AND 982%5BPagination%5D AND Maruyama K%2C Sakuma Y%2C Kasuga M%2C Ito Y%2C Seki M%2C Goda H%2C Shimada Y%2C Yoshida S%2C Shinozaki K%2C Yamaguchi%2DShinozaki K%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Maruyama K, Sakuma Y, Kasuga M, Ito Y, Seki M, Goda H, Shimada Y, Yoshida S, Shinozaki K, Yamaguchi-Shinozaki K (2004) Identification of cold-inducible downstream genes of the Arabidopsis DREB1A/CBF3 transcriptional factor using two microarray systems. Plant J 38: 982-993

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

http://scholar.google.com/scholar?as_q=Identification of cold-inducible downstream genes of the Arabidopsis DREB1A/CBF3 transcriptional factor using two microarray systems&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=Identification of cold-inducible downstream genes of the Arabidopsis DREB1A/CBF3 transcriptional factor using two microarray systems&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Maruyama&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Pleiotropy contributes to genetic correlations among ecological traits%2E Mol Ecol%5BTitle%5D%29 AND 12%5BVolume%5D AND 1137%5BPagination%5D AND Mckay JK%2C Richards JH%2C Mitchell%2DOlds T%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Mckay JK, Richards JH, Mitchell-Olds T (2003) Genetics of drought adaptation in Arabidopsis thaliana: I. Pleiotropy contributes to genetic correlations among ecological traits. Mol Ecol 12: 1137-1151

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

http://scholar.google.com/scholar?as_q=Genetics of drought adaptation in Arabidopsis thaliana: I&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=Genetics of drought adaptation in Arabidopsis thaliana: I&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Mckay&as_ylo=2003&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Genome Res%5BTitle%5D%29 AND 20%5BVolume%5D AND 1297%5BPagination%5D AND McKenna A%2C Hanna M%2C Banks E%2C Sivachenko A%2C Cibulskis K%2C Kernytsky A%2C Garimella K%2C Altshuler D%2C Gabriel S%2C Daly M%2C et al%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, et al (2010) The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20: 1297-1303

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

http://scholar.google.com/scholar?as_q=The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=McKenna&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%281 and affecting the accumulation of HsfA2%2Dregulated sHSPs%2E Plant J%5BTitle%5D%29 AND 59%5BVolume%5D AND 387%5BPagination%5D AND Meiri D%2C Breiman A%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Meiri D, Breiman A (2009) Arabidopsis ROF1 (FKBP62) modulates thermotolerance by interacting with HSP90.1 and affecting the accumulation of HsfA2-regulated sHSPs. Plant J 59: 387-99

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

http://scholar.google.com/scholar?as_q=Arabidopsis ROF1 (FKBP62) modulates thermotolerance by interacting with HSP90&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Arabidopsis ROF1 (FKBP62) modulates thermotolerance by interacting with HSP90&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Meiri&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Physiol%5BTitle%5D%29 AND 157%5BVolume%5D AND 1942%5BPagination%5D AND M�ndez%2DVigo B%2C Pic� FX%2C Ramiro M%2C Mart�nez%2DZapater JM%2C Alonso%2DBlanco C%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=M�ndez-Vigo B, Pic� FX, Ramiro M, Mart�nez-Zapater JM, Alonso-Blanco C (2011) Altitudinal and climatic adaptation is mediated by flowering traits and FRI, FLC, and PHYC genes in Arabidopsis. Plant Physiol 157: 1942-1955

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=M�ndez-Vigo&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Altitudinal and climatic adaptation is mediated by flowering traits and FRI, FLC, and PHYC genes 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=Altitudinal and climatic adaptation is mediated by flowering traits and FRI, FLC, and PHYC genes in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=M�ndez-Vigo&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell Environ%5BTitle%5D%29 AND 39%5BVolume%5D AND 282%5BPagination%5D AND M�ndez%2DVigo B%2C Savic M%2C Aus�n I%2C Ramiro M%2C Mart�n B%2C Pic� FX%2C Alonso%2DBlanco C%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=M�ndez-Vigo B, Savic M, Aus�n I, Ramiro M, Mart�n B, Pic� FX, Alonso-Blanco C (2015) Environmental and genetic interactions reveal FLOWERING LOCUS C as a modulator of the natural variation for the plasticity of flowering in Arabidopsis. Plant Cell Environ 39: 282-294

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=M�ndez-Vigo&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Environmental and genetic interactions reveal FLOWERING LOCUS C as a modulator of the natural variation for the plasticity of flowering in Arabidopsis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Environmental and genetic interactions reveal FLOWERING LOCUS C as a modulator of the natural variation for the plasticity of flowering in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=M�ndez-Vigo&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Cell Rep%5BTitle%5D%29 AND 5%5BVolume%5D AND 1279%5BPagination%5D AND Merret R%2C Descombin J%2C Juan Y%2C Favory J%2DJ%2C Carpentier M%2DC%2C Chaparro C%2C Charng Y%2C Deragon J%2DM%2C Bousquet%2DAntonelli C%5BAuthor%5D&dopt=abstract


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Michaels SD (2001) Loss of FLOWERING LOCUS C activity eliminates the late-flowering phenotype of FRIGIDA and autonomouspathway mutations but not responsiveness to vernalization. Plant Cell 13: 935-942


Michaels SD, Amasino RM (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor offlowering. Plant Cell 11: 949-956


Mizoguchi T, Wheatley K, Hanzawa Y, Wright L, Mizoguchi M, Song H-R, Carré IA, Coupland G (2002) LHY and CCA1 are partiallyredundant genes required to maintain circadian rhythms in Arabidopsis. Dev Cell 2: 629-641


Monte E, Alonso JM, Ecker JR, Zhang Y, Li X, Young J, Austin-Phillips S, Quail PH (2003) Isolation and characterization of phyCmutants in Arabidopsis reveals complex crosstalk between phytochrome signaling pathways. Plant Cell 15: 1962-1980


Nah G, Jeffrey Chen Z (2010) Tandem duplication of the FLC locus and the origin of a new gene in Arabidopsis related species andtheir functional implications in allopolyploids. New Phytol 186: 228-238


Nakamichi N, Kusano M, Fukushima A, Kita M, Ito S, Yamashino T, Saito K, Sakakibara H, Mizuno T (2009) Transcript profiling of anArabidopsis PSEUDO RESPONSE REGULATOR arrhythmic triple mutant reveals a role for the circadian clock in cold stressresponse. Plant Cell Physiol 50: 447-462


Nishizawa A, Yabuta Y, Shigeoka S (2008) Galactinol and raffinose constitute a novel function to protect plants from oxidativedamage. Plant Physiol 147: 1251-1263


Nover L, Bharti K, Döring P, Mishra SK, Ganguli A, Scharf KD (2001) Arabidopsis and the heat stress transcription factor world:how many heat stress transcription factors do we need? Cell Stress Chaperones 6: 177-189


O'Kane SL (1997) A synopsis of Arabidopsis (Brassicaceae). Novon 7: 323-327Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Otto CR V, Snodgrass JW, Forester DC, Mitchell JC, Miller RW (2007) Climatic variation and the distribution of an amphibianpolyploid complex. J Anim Ecol 76: 1053-1061


Pandit MK, Tan HTW, Bisht MS (2006) Polyploidy in invasive plant species of Singapore. Bot J Linn Soc 151: 395-403Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Panikulangara TJ, Eggers-Schumacher G, Wunderlich M, Stransky H, Schöffl F (2004) Galactinol synthase1. A novel heat shockfactor target gene responsible for heat-induced synthesis of raffinose family oligosaccharides in Arabidopsis. Plant Physiol 136:3148-3158


Perez JD, Rubinstein ND, Fernandez DE, Santoro SW, Needleman LA, Ho-Shing O, Choi JJ, Zirlinger M, Chen S-K, Liu JS, et al(2015) Quantitative and functional interrogation of parent-of-origin allelic expression biases in the brain. Elife 4: e07860



http://search.crossref.org/?page=1&rows=2&q=Merret R, Descombin J, Juan Y, Favory J-J, Carpentier M-C, Chaparro C, Charng Y, Deragon J-M, Bousquet-Antonelli C (2013) XRN4 and LARP1 are required for a heat-triggered mRNA decay pathway involved in plant acclimation and survival during thermal stress. Cell Rep 5: 1279-1293

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

http://scholar.google.com/scholar?as_q=XRN4 and LARP1 are required for a heat-triggered mRNA decay pathway involved in plant acclimation and survival during thermal stress&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=XRN4 and LARP1 are required for a heat-triggered mRNA decay pathway involved in plant acclimation and survival during thermal stress&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Merret&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell%5BTitle%5D%29 AND 13%5BVolume%5D AND 935%5BPagination%5D AND Michaels SD%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Michaels SD (2001) Loss of FLOWERING LOCUS C activity eliminates the late-flowering phenotype of FRIGIDA and autonomous pathway mutations but not responsiveness to vernalization. Plant Cell 13: 935-942

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

http://scholar.google.com/scholar?as_q=Loss of FLOWERING LOCUS C activity eliminates the late-flowering phenotype of FRIGIDA and autonomous pathway mutations but not responsiveness to 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=Loss of FLOWERING LOCUS C activity eliminates the late-flowering phenotype of FRIGIDA and autonomous pathway mutations but not responsiveness to vernalization&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Michaels&as_ylo=2001&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell%5BTitle%5D%29 AND 11%5BVolume%5D AND 949%5BPagination%5D AND Michaels SD%2C Amasino RM%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Michaels SD, Amasino RM (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11: 949-956

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

http://scholar.google.com/scholar?as_q=FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of 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=FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Michaels&as_ylo=1999&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Dev Cell%5BTitle%5D%29 AND 2%5BVolume%5D AND 629%5BPagination%5D AND Mizoguchi T%2C Wheatley K%2C Hanzawa Y%2C Wright L%2C Mizoguchi M%2C Song H%2DR%2C Carr� IA%2C Coupland G%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Mizoguchi T, Wheatley K, Hanzawa Y, Wright L, Mizoguchi M, Song H-R, Carr� IA, Coupland G (2002) LHY and CCA1 are partially redundant genes required to maintain circadian rhythms in Arabidopsis. Dev Cell 2: 629-641

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

http://scholar.google.com/scholar?as_q=LHY and CCA1 are partially redundant genes required to maintain circadian rhythms 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=LHY and CCA1 are partially redundant genes required to maintain circadian rhythms in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Mizoguchi&as_ylo=2002&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell%5BTitle%5D%29 AND 15%5BVolume%5D AND 1962%5BPagination%5D AND Monte E%2C Alonso JM%2C Ecker JR%2C Zhang Y%2C Li X%2C Young J%2C Austin%2DPhillips S%2C Quail PH%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Monte E, Alonso JM, Ecker JR, Zhang Y, Li X, Young J, Austin-Phillips S, Quail PH (2003) Isolation and characterization of phyC mutants in Arabidopsis reveals complex crosstalk between phytochrome signaling pathways. Plant Cell 15: 1962-1980

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

http://scholar.google.com/scholar?as_q=Isolation and characterization of phyC mutants in Arabidopsis reveals complex crosstalk between phytochrome signaling pathways&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Isolation and characterization of phyC mutants in Arabidopsis reveals complex crosstalk between phytochrome signaling pathways&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Monte&as_ylo=2003&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28New Phytol%5BTitle%5D%29 AND 186%5BVolume%5D AND 228%5BPagination%5D AND Nah G%2C Jeffrey Chen Z%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Nah G, Jeffrey Chen Z (2010) Tandem duplication of the FLC locus and the origin of a new gene in Arabidopsis related species and their functional implications in allopolyploids. New Phytol 186: 228-238

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

http://scholar.google.com/scholar?as_q=Tandem duplication of the FLC locus and the origin of a new gene in Arabidopsis related species and their functional implications in allopolyploids&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=Tandem duplication of the FLC locus and the origin of a new gene in Arabidopsis related species and their functional implications in allopolyploids&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Nah&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell Physiol%5BTitle%5D%29 AND 50%5BVolume%5D AND 447%5BPagination%5D AND Nakamichi N%2C Kusano M%2C Fukushima A%2C Kita M%2C Ito S%2C Yamashino T%2C Saito K%2C Sakakibara H%2C Mizuno T%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Nakamichi N, Kusano M, Fukushima A, Kita M, Ito S, Yamashino T, Saito K, Sakakibara H, Mizuno T (2009) Transcript profiling of an Arabidopsis PSEUDO RESPONSE REGULATOR arrhythmic triple mutant reveals a role for the circadian clock in cold stress response. Plant Cell Physiol 50: 447-462

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

http://scholar.google.com/scholar?as_q=Transcript profiling of an Arabidopsis PSEUDO RESPONSE REGULATOR arrhythmic triple mutant reveals a role for the circadian clock in cold stress 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

http://scholar.google.com/scholar?as_q=Transcript profiling of an Arabidopsis PSEUDO RESPONSE REGULATOR arrhythmic triple mutant reveals a role for the circadian clock in cold stress response&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Nakamichi&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Physiol%5BTitle%5D%29 AND 147%5BVolume%5D AND 1251%5BPagination%5D AND Nishizawa A%2C Yabuta Y%2C Shigeoka S%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Nishizawa A, Yabuta Y, Shigeoka S (2008) Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol 147: 1251-1263

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

http://scholar.google.com/scholar?as_q=Galactinol and raffinose constitute a novel function to protect plants from oxidative damage&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=Galactinol and raffinose constitute a novel function to protect plants from oxidative damage&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Nishizawa&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Cell Stress Chaperones%5BTitle%5D%29 AND 6%5BVolume%5D AND 177%5BPagination%5D AND Nover L%2C Bharti K%2C D�ring P%2C Mishra SK%2C Ganguli A%2C Scharf KD%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Nover L, Bharti K, D�ring P, Mishra SK, Ganguli A, Scharf KD (2001) Arabidopsis and the heat stress transcription factor world: how many heat stress transcription factors do we need? Cell Stress Chaperones 6: 177-189

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

http://scholar.google.com/scholar?as_q=Arabidopsis and the heat stress transcription factor world: how many heat stress transcription factors do we need&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=%28Novon%5BTitle%5D%29 AND 7%5BVolume%5D AND 323%5BPagination%5D AND O%27Kane SL%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=O'Kane SL (1997) A synopsis of Arabidopsis (Brassicaceae). Novon 7: 323-327

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

http://scholar.google.com/scholar?as_q=A synopsis of Arabidopsis (Brassicaceae)&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 synopsis of Arabidopsis (Brassicaceae)&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=O'Kane&as_ylo=1997&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28J Anim Ecol%5BTitle%5D%29 AND 76%5BVolume%5D AND 1053%5BPagination%5D AND Otto CR V%2C Snodgrass JW%2C Forester DC%2C Mitchell JC%2C Miller RW%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Otto CR V, Snodgrass JW, Forester DC, Mitchell JC, Miller RW (2007) Climatic variation and the distribution of an amphibian polyploid complex. J Anim Ecol 76: 1053-1061

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

http://scholar.google.com/scholar?as_q=Climatic variation and the distribution of an amphibian polyploid complex&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Climatic variation and the distribution of an amphibian polyploid complex&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Otto&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Bot J Linn Soc%5BTitle%5D%29 AND 151%5BVolume%5D AND 395%5BPagination%5D AND Pandit MK%2C Tan HTW%2C Bisht MS%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Pandit MK, Tan HTW, Bisht MS (2006) Polyploidy in invasive plant species of Singapore. Bot J Linn Soc 151: 395-403

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

http://scholar.google.com/scholar?as_q=Polyploidy in invasive plant species of Singapore&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=Polyploidy in invasive plant species of Singapore&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Pandit&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28A novel heat shock factor target gene responsible for heat%2Dinduced synthesis of raffinose family oligosaccharides in Arabidopsis%2E Plant Physiol%5BTitle%5D%29 AND 136%5BVolume%5D AND 3148%5BPagination%5D AND Panikulangara TJ%2C Eggers%2DSchumacher G%2C Wunderlich M%2C Stransky H%2C Sch�ffl F%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Panikulangara TJ, Eggers-Schumacher G, Wunderlich M, Stransky H, Sch�ffl F (2004) Galactinol synthase1. A novel heat shock factor target gene responsible for heat-induced synthesis of raffinose family oligosaccharides in Arabidopsis. Plant Physiol 136: 3148-3158

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

http://scholar.google.com/scholar?as_q=Galactinol synthase1&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=Galactinol synthase1&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Panikulangara&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Quantitative and functional interrogation of parent%2Dof%2Dorigin allelic expression biases in the brain%2E%5BTitle%5D%29 AND Perez JD%2C Rubinstein ND%2C Fernandez DE%2C Santoro SW%2C Needleman LA%2C Ho%2DShing O%2C Choi JJ%2C Zirlinger M%2C Chen S%2DK%2C Liu JS%2C et al%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Perez JD, Rubinstein ND, Fernandez DE, Santoro SW, Needleman LA, Ho-Shing O, Choi JJ, Zirlinger M, Chen S-K, Liu JS, et al (2015) Quantitative and functional interrogation of parent-of-origin allelic expression biases in the brain. Elife 4: e07860

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

http://scholar.google.com/scholar?as_q=Quantitative and functional interrogation of parent-of-origin allelic expression biases in the brain.&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=Quantitative and functional interrogation of parent-of-origin allelic expression biases in the brain.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Perez&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1


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