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First published online February 24, 2006; 10.1104/pp.105.073486 Plant Physiology 140:1397-1405 (2006) © 2006 American Society of Plant Biologists
HvVRN2 Responds to Daylength, whereas HvVRN1 Is Regulated by Vernalization and Developmental Status1Commonwealth Scientific and Industrial Research Organization, Division of Plant Industry, Canberra, Australian Capital Territory 2601, Australia
Two genetic loci control the vernalization response in winter cereals; VRN1, which encodes an AP1-like MADS-box transcription factor, and VRN2, which has been mapped to a chromosome region containing ZCCT zinc finger transcription factor genes. We examined whether daylength regulates expression of HvVRN1 and HvVRN2. In a vernalization-responsive winter barley (Hordeum vulgare), expression of HvVRN1 is regulated by vernalization and by development, but not by daylength. Daylength affected HvVRN1 expression in only one of six vernalization-insensitive spring barleys examined and so cannot be a general feature of regulation of this gene. In contrast, daylength is the major determinant of expression levels of two ZCCT genes found at the barley VRN2 locus, HvZCCTa and HvZCCTb. In winter barley, high levels of HvZCCTa and HvZCCTb expression were detected only when plants were grown in long days. During vernalization in long-day conditions, HvVRN1 is induced and expression of HvZCCTb is repressed. During vernalization under short days, induction of HvVRN1 occurs without changes in HvZCCTa and HvZCCTb expression. Analysis of HvZCCTa and HvZCCTb expression levels in a doubled haploid population segregating for different vernalization and daylength requirements showed that HvVRN1 genotype determines HvZCCTa and HvZCCTb expression levels. We conclude that the vernalization response is mediated through HvVRN1, whereas HvZCCTa and HvZCCTb respond to daylength cues to repress flowering under long days in nonvernalized plants.
In winter cereal crops, such as wheat (Triticum spp.) and barley (Hordeum vulgare), flowering can be promoted by extended exposure to low temperatures (vernalization) and by long daylengths (for review, see Law, 2000  ; Snape et al., 2001). Physiological studies of plants grown in controlled conditions have shown that vernalization is a prerequisite for induction of flowering by long days and that a memory of vernalization can be maintained for prolonged periods (for review, see Sung and Amasino, 2004, 2005). Vernalization may predispose the apex to undergo floral transition in response to inductive long-day conditions, but the mechanism for this is unclear.
Response to vernalization or long daylengths is subject to genetic variation. Breeders have used this natural genetic variation to produce two major classes of cereals, termed winter and spring, with different flowering-time behavior. Winter varieties have a requirement for vernalization and are typically sensitive to inductive long days, while spring varieties do not require vernalization and are often daylength insensitive. These differences in flowering-time behavior have been important for adapting cereal cultivars to different agricultural regions (Kato and Yokoyama, 1992
Two main loci, VRN1 and VRN2, determine the vernalization requirement of the diploid winter cereals barley (Takahashi and Yasuda, 1971
The VRN1 gene encodes an AP1-like MADS-box transcription factor (Danyluk et al., 2003
Expression of VRN1 occurs without any requirement for vernalization in plants that have dominant spring alleles of VRN1. This constitutive expression of VRN1 can substitute for vernalization to accelerate flowering in plants that have not been vernalized and explains the dominant gene action of VRN1 spring alleles. In hexaploid wheat (Triticum aestivum), dominant spring alleles of VRN1 have been identified in all three genomes (Pugsley, 1971
Expression of VRN1 can also be regulated by daylength. The barley VRN1 gene, HvVRN1 (see note on gene nomenclature in "Materials and Methods"), is strongly induced by long days in the daylength-responsive barley cultivar Dicktoo (Danyluk et al., 2003
One potential regulator of VRN1 is the VRN2 gene (Yan et al., 2004b The model for the molecular basis of the vernalization response in winter cereals outlined above does not address the potential for daylength regulation of VRN1 or VRN2. We have examined regulation of HvVRN1 and of ZCCT genes found at the HvVRN2 locus of barley (see note on gene nomenclature in "Materials and Methods") by both vernalization and daylength. We show that HvVRN1 is regulated primarily by vernalization and developmental cues, whereas daylength is the major determinant of HvZCCTa and HvZCCTb gene expression, and on the basis of these data we suggest an alternative model for the molecular basis of the vernalization response in winter cereals.
HvVRN1 Is Regulated by Development and Vernalization, But Not by Daylength, in Most Barley Varieties The effect of daylength on HvVRN1 expression was initially examined in vernalization and daylength-responsive winter barley (cv Sonja). Plants (nonvernalized) were grown under either long or short days and HvVRN1 expression levels in plants from each daylength condition were compared at a number of time points. HvVRN1 expression was initially low in both conditions, but increased gradually during development (Fig. 1A ). HvVRN1 expression increased more rapidly in long days. Expression of HvVRN1 was detectable by RNA gel blots after 10 weeks in long-day-grown plants, but was only faintly detectable after 12 weeks in short-day-grown plants. This correlates with earlier flowering in long-day conditions (Fig. 1B). The effect on HvVRN1 expression of shifting plants from short days to long days was also examined. Plants were grown under short days for 21 d, then either kept in short days or shifted to long days. HvVRN1 expression was not detected by RNA gel-blot analysis in plants after 14 d in either treatment, but weak expression of HvVRN1 could be detected by real-time reverse transcription (RT)-PCR. The level of expression was similar in both daylength treatments (Fig. 1C).
HvVRN1 expression can be induced in this winter barley by vernalization (Trevaskis et al., 2003 ). The effects of different daylengths on the induction of HvVRN1 by vernalization were examined. Plants (21-d-old) were vernalized under either long or short daylengths for up to 9 weeks, and HvVRN1 expression levels were compared. Strong induction of HvVRN1 was evident after 7 weeks of vernalization in both daylength conditions (Fig. 1D). Real-time RT-PCR analysis of HvVRN1 expression levels showed that at the end of the vernalization treatment induction of HvVRN1 was slightly higher in plants vernalized under short days (Fig. 1E). Expression of HvVRN1 increased further when plants were returned to glasshouse temperatures regardless of daylength conditions (Fig. 1E). Regulation of HvVRN1 expression by daylength was examined in seven spring barley varieties that express HvVRN1 without any requirement for vernalization. HvVRN1 expression levels were compared in plants that had been grown for 14 d in either long- or short-day conditions. In six varieties (Chame 11, Sikangense, Himalayense type 15, Golden Promise, Morex, and Olli) daylength had no effect on HvVRN1 expression. In one variety (cv Icheon Naked), HvVRN1 expression was higher in long-day-grown plants (Fig. 2 ). All varieties flowered earlier under long days than short days and Icheon Naked flowered approximately 2 weeks earlier in long days than other spring barleys with the same genotypes for HvVRN1 and HvVRN2.
Expression of HvZCCTa and HvZCCTb Is Daylength Responsive
Two homologs of the T. monococcum VRN2 gene (TmZCCT1) have been identified at the orthologous HvVRN2 locus of barley. These genes have been designated HvZCCTa and HvZCCTb (Yan et al., 2004b
The effects of changes in daylength on HvZCCTa and HvZCCTb expression were then examined using RT-PCR with gene-specific primers. Plants were grown for 21 d under short days, then shifted to long days and harvested at different time points. Exposure to a single long day induced expression of both HvZCCTa and HvZCCTb (Fig. 4A ). Expression remained high in the plants shifted to long days at all subsequent time points analyzed (Fig. 4A). The increase in HvZCCTa and HvZCCTb transcript levels in plants shifted to long-day conditions showed no relationship with HvVRN1 expression levels, which remained constant (Fig. 1C).
Because HvZCCTa and HvZCCTb have similar responses to daylength, changes in expression levels of HvZCCTa and HvZCCTb were quantified using quantitative RT-PCR with highly efficient primers that amplify both genes. In short-day-grown plants, expression of HvZCCTa and HvZCCTb was weak. Within the period of a single long-day treatment, expression of HvZCCTa and HvZCCTb increased dramatically (Fig. 4B). These results are consistent with those obtained for each gene independently using gene-specific primers (Fig. 4A). A rapid decrease in expression of both HvZCCTa and HvZCCTb occurred when plants were shifted from long days to short days in both glasshouse and vernalizing conditions (Fig. 4C). After a week in short-day conditions, expression of both HvZCCTa and HvZCCTb was too low to be detected by RT-PCR with gene-specific primers regardless of temperature. This suggests that the effect of daylength on HvZCCTa and HvZCCTb expression overrides that of temperature. A feature of many daylength-responsive genes is an expression pattern that follows a diurnal rhythm. The expression levels of HvZCCTa and HvZCCTb were examined at 2-h intervals throughout a 24-h cycle in nonvernalized plants grown under long- or short-day conditions. Under long days, expression of these genes showed a strong diurnal rhythm (Fig. 5 ). Maximal expression levels were observed at the end of the light period and expression decreased with the onset of darkness. Expression levels remained low throughout the dark period, but increased when the plants were reexposed to light. Using gene-specific RT-PCR primers, expression of both HvZCCTa and HvZCCTb could be detected at the time points when high expression levels were detected by quantitative RT-PCR. In short days, expression of HvZCCTa and HvZCCTb remained low throughout the 24-h cycle (Fig. 5).
Vernalization of Plants in Short-Day Conditions Induces HvVRN1 and Promotes Flowering, whereas Expression of HvZCCTa and HvZCCTb Remains Low Vernalization of plants in short days promotes flowering (Fig. 1B). HvVRN1 was induced by this treatment (Fig. 1, D and E), but the expression levels of HvZCCTa and HvZCCTb remained low (Fig. 6 ). This suggests that repression of HvZCCTa and HvZCCTb may not be associated with induction of HvVRN1 by vernalization in short-day conditions. Vernalization did not block induction of HvZCCTa or HvZCCTb by long days. Expression of both genes increased when plants that had been vernalized under short days were moved to normal glasshouse temperatures with long days (Fig. 6).
Expression of HvZCCTb Is Regulated by Vernalization in Long Days in Winter Barley
Expression of HvZCCTa and HvZCCTb was examined during vernalization under long days using real-time RT-PCR. The total level of HvZCCTa and HvZCCTb expression was lower in vernalized plants than in control plants grown in glasshouse conditions for the same length of time (Fig. 7A
). RT-PCR with gene-specific primers showed that the drop in expression detected by quantitative RT-PCR was due primarily to a decrease in HvZCCTb expression during the course of the vernalization treatment (Fig. 7B). Expression of both genes remained high in control plants maintained under normal long-day glasshouse temperatures for the same period of time (Fig. 7B). The decrease in expression of HvZCCTb during vernalization under long days is similar to that reported previously for the ZCCT1 and ZCCT2 genes of T. monococcum during vernalization under similar daylength conditions (Yan et al., 2004b
HvVRN1 Genotype Is a Major Determinant of HvZCCTa and HvZCCTb Expression in Nonvernalized Plants
Regulatory interactions between HvZCCTa, HvZCCTb, and HvVRN1 were examined in nonvernalized plants from a doubled haploid population derived from a cross between winter barley (cv Halcyon) and spring barley (cv Sloop). This population segregates for vernalization requirements at both HvVRN1 and HvVRN2 (Read et al., 2003
By examining the effects of different combinations of daylength and vernalization treatments on expression of HvVRN1 and HvVRN2 (HvZCCTa and HvZCCTb) in barley, we have found that these genes are, to a large extent, regulated by different environmental cues. Typically, vernalization had the greatest effect on HvVRN1 expression, whereas daylength had the greatest effect on expression of HvZCCTa and HvZCCTb. For both genes, however, the effect of each environmental cue is dependent on the genetic background of the varieties tested. In a vernalization-responsive barley cultivar (cv Sonja), vernalization had the largest effect on HvVRN1, causing strong induction of HvVRN1 expression. Expression of HvVRN1 increased further after vernalized plants were returned to glasshouse temperatures. This might imply autoregulation of HvVRN1, such that once HvVRN1 is expressed beyond a certain threshold, it causes further activation of its own expression (Fig. 1E). Expression of HvVRN1 also increased slowly during development in plants that had not been vernalized (Fig. 1A). Daylength conditions did not affect induction of HvVRN1 by vernalization or HvVRN1 expression postvernalization, but did affect the degree to which HvVRN1 expression increased during development, with HvVRN1 expression occurring earlier when plants were grown under long days (Fig. 1A).
Expression of HvVRN1 was not affected by daylength in most spring varieties examined. Daylength activation of HvVRN1 expression occurred in only one of seven spring barleys examined (Fig. 2). The daylength response of HvVRN1 expression seen in Icheon Naked and reported for Dicktoo (Danyluk et al., 2003
For the HvZCCTa and HvZCCTb genes found at the HvVRN2 locus in barley, daylength is the major environmental cue regulating gene expression in vernalization-responsive winter barley (cv Sonja). Expression of both genes was high in long days and low in short days (Fig. 3B). Vernalization affected expression of only the HvZCCTb gene, and only when plants were grown under long days (Fig. 7B). The effect of vernalization on HvZCCTb expression was much slower than that of daylength (Figs. 4A and 7B). On the basis of this expression pattern, we predict that HvVRN2 (HvZCCTa and HvZCCTb) operates as a repressor of flowering only under long-day conditions. It has recently been shown that HvVRN2 genotype influences flowering time predominantly in long-day conditions (Karsai et al., 2005
It has been proposed that VRN2 acts to repress VRN1, and that a decrease in VRN2 expression during vernalization leads to induction of VRN1 (Yan et al., 2004b
In the Sloop x Halcyon doubled haploid population, expression of HvVRN1 in lines carrying a spring HvVRN1 allele represses expression of HvZCCTa and HvZCCTb. A similar effect was observed in both diploid and hexaploid wheat lines carrying spring alleles of VRN1 (Loukoianov et al., 2005
Our data are difficult to reconcile with the current model of the vernalization response pathway. We suggest an alternative model to explain interactions between VRN1 and VRN2 (Fig. 9
). We propose that flowering in winter cereals can be triggered by vernalization, daylength, or developmentally regulated (autonomous) pathways, as is the case in Arabidopsis (Arabidopsis thaliana; see Mouradov et al., 2002
VRN2, which is regulated primarily by daylength cues but also by vernalization, may play an important role in integrating daylength and vernalization pathways in winter cereals. This is different from Arabidopsis, where integration of daylength and vernalization pathways is mediated by regulatory interactions between a vernalization-responsive repressor of flowering, FLOWERING LOCUS C, and the daylength-responsive promoters of flowering, FLOWERING LOCUS T and SUPPRESSOR OF OVEREXPRESSION OF CO1 (Michaels et al., 2005 ). The vernalization response has apparently evolved separately in monocots and dicots, resulting in different regulatory interactions between the vernalization response pathway and other molecular pathways controlling the timing of flowering. Identification of regulatory targets of VRN2 will be important in understanding the control of flowering time in winter cereals.
HvVRN1 expression is induced by vernalization under long days in barley varieties that carry deletions at the HvVRN2 locus (e.g. Perga and Dunja; Trevaskis et al., 2003
Plant Growth Plants were grown in pots of soil in sunlit glasshouses under long days (16-h light/8-h dark, with supplementary lighting used when natural light levels dropped below 200 µE) or short days (8-h light/16-h dark). Plants were harvested at the middle of the light period for both treatments. Glasshouses had an average temperature of 19°C. For vernalization treatments, plants were maintained at an average temperature of 8°C under the same light regimes as outlined above for 9 weeks.
Total RNA was extracted from whole seedlings, excluding root tissue, using the method of Chang et al. (1993)
An oligo(T) primer (T18[G/C/A]) was used to prime first-strand cDNA synthesis from 5 µg of total RNA by using the SuperScript reverse transcriptase enzyme (Invitrogen) according to the manufacturer's instructions. A single RT reaction was performed for each RNA sample. RT-PCR was performed using Amplitaq DNA polymerase (Applied Biosystems) in the buffer supplied by the manufacturer with 1.5 mM MgCl2. Cycling conditions were 40 cycles (except for ACTIN, 25 cycles) of 30 s at 94°C, 30 s at 55°C, and 30 s at 72°C. Fragments were visualized by agarose gel electrophoresis. Real-time PCR was performed using SYBR Green JumpStart Taq ReadyMix (Sigma) in 20-µL reactions, consisting of 1x SYBR Green JumpStart Taq ReadyMix, 1 µM of each primer, and cDNA corresponding to 62.5 ng of total RNA. Reactions were run on a Rotor-Gene 2000 or 3000 Real-Time Cycler (Corbett Research). Cycling conditions were 10 min at 95°C, 40 cycles of 10 s at 95°C, 15 s at 60°C, and 20 s at 72°C. This was followed by a melting-curve program (72°C–95°C, with a 5-s hold at each temperature). Fluorescence data were acquired at the 72°C step and during the melting-curve program. Three replicate reactions for each cDNA-primer combination were performed for each sample in the same run. For each cDNA sample, ACTIN levels were also quantified in the same run in three replicate reactions. Expression levels relative to ACTIN were then calculated using the ROTORGENE6 software package (Corbett Research), which compares reaction takeoff points (cycle number). Amplification efficiencies of each primer set are considered. A technical repeat is defined as quantification of one replicate reaction for a gene of interest relative to one ACTIN reaction from the same sample. Two biological repeats were carried out for each experiment. All experiments showed similar trends in separate biological repeats. For RT-PCR, primers were designed to be cDNA specific by flanking introns or crossing exon-exon boundaries. For HvVRN1, primers 5'-TGAAGCTCAGAAATGGATTCG-3' and 5'-TATGAGCGCTACTCTTATGC-3' were used for both RT-PCR and real-time PCR. Gene-specific primer pairs 5'-ATCACCATCATCAGGAACAC-3'/5'-CTCGCAGAATGGCACGATG-3' and 5'-ATCACCATCATCAGGAACATCG-3'/5'-GGCGGAATGGCACGATGG-3', designed to sequence AY485977 and AY485978, were used to amplify the HvZCCTa and HvZCCTb cDNAs, respectively. Amplified fragments were cloned and sequenced to verify the specificity of primers. For real-time PCR, a primer pair (5'-GAGCCACCATCGTGCCATTC-3'/5'-GCCGCTTCTTCCTCTTCTC-3') that was designed to amplify both HvZCCTa and HvZCCTb was used. For HvZCCTc, primers 5'-AATCATGACTATTGACACAGAGACG-3' and 5'-AGCTGGAGGCGACGGCGGTG-3', designed to sequence AY687931, were used for RT-PCR. As this primer pair is not cDNA specific, first-strand cDNA synthesis was primed from total RNA that had been Dnase treated using RQ1 RNase-Free DNase (Promega) according to the manufacturer's instructions. Expression of a barley (Hordeum vulgare) ACTIN gene (AY145451) was used as a control to normalize for the amount of cDNA present in each sample. Primers 5'-GCCGTGCTTTCCCTCTATG-3' and 5'-GCTTCTCCTTGATGTCCCTTA-3' were used to amplify AY145451 for both RT-PCR and real-time PCR. To genotype lines from the Halycon x Sloop doubled haploid population, primer pairs 5'-AAGAACCATCCGAGGTGAAGTTTACTAGG-3'/5'-TCTGCTACCCACAAGAAAAG-3' and 5'-AAGAACCATCCGAGGTGAAGTTTACTAGG-3'/5'-TAAACACTGTACTACTCTCACCATTG-3' were used for HvZCCTa and HvZCCTb, respectively. Primers described in Fu et al. (2005)
The barley VRN1 gene (GenBank AY750993) has been previously referred to as Sh2 (Takahashi and Yasuda, 1971
Daylength regulation of the VRN2 gene of wheat has been reported recently (Dubcovsky J, Loukioanov A, Fu D, Valarik M, Sanchez A, Yan L [2006] Effect of photoperiod on the regulation of wheat vernalization genes VRN1 and VRN2. Plant Mol Biol 60: 469–480). Similar induction of the HvVRN1 gene by vernalization under short- or long-day conditions also was reported (von Zitzewitz J, Szücs P, Dubcovsky J, Yan L, Francia E, Pecchioni N, Casas A, Chen THH, Hayes PM, Skinner JSS [2005] Molecular and structural characterization of barley vernalization genes. Plant Mol Biol 59: 449–467).
We thank New South Wales Department of Primary Industries for providing the Sloop x Halycon doubled haploid population and marker scores and the Australian Winter Cereal Collection for providing the barley cultivars used in this study. We would also like to thank Dr. E.J. Finnegan and Dr. C. Sheldon for useful discussions, and Ms. S. Stops for technical assistance. Received October 27, 2005; returned for revision February 9, 2006; accepted February 9, 2006.
1 This work was supported by the Commonwealth Scientific and Industrial Research Organization (postdoctoral fellowships to B.T. and M.H.). 
2 These authors contributed equally to the paper. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Elizabeth S. Dennis (liz.dennis{at}csiro.au). Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.105.073486. * Corresponding author; e-mail liz.dennis{at}csiro.au; fax 61–2–6246–5000.
Ausubel FM, Brenton R, Kingston RE, Moore DD, Siedman JG, Smyth JA, Struhl K (1994) Current Protocols in Molecular Biology. John Wiley and Sons, New York Berbel A, Navarro C, Ferrandiz C, Canas LA, Madueno F, Beltran JP (2001) Analysis of PEAM4, the pea AP1 functional homologue, supports a model for AP1-like genes controlling both floral meristem and floral organ identity in different plant species. Plant J 25: 441–451[CrossRef][Web of Science][Medline] Chang S, Puryear J, Cairney K (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11: 113–116[CrossRef] Danyluk J, Kane NA, Breton G, Limin AE, Fowler DB, Sarhan F (2003) TaVRT-1, a putative transcription factor associated with vegetative to reproductive transition in cereals. Plant Physiol 132: 1849–1860 Dolferus R, Jacobs M, Peacock WJ, Dennis ES (1994) Differential interactions of promoter elements in the stress response of the Arabidopsis alcohol dehydrogenase gene. Plant Physiol 105: 1075–1087[Abstract] Dubcovsky J, Chen C, Yan L (2005) Molecular characterization of the allelic variation at the VRN-H2 vernalization locus in barley. Mol Breed 15: 395–407[CrossRef] Dubcovsky J, Lijavetzky D, Appendino L, Tranquilli G (1998) Comparative RFLP mapping of Triticum monococcum genes controlling vernalization requirement. Theor Appl Genet 97: 968–975[CrossRef][Web of Science] Fu D, Szücs P, Yan L, Helguera M, Skinner JS, Von Zitzewitz J, Hayes PM, Dubcovsky J (2005) Large deletions within the first intron in VRN-1 are associated with spring growth habit in barley and wheat. Mol Genet Genomics 273: 54–65[CrossRef][Web of Science][Medline] Gocal GF, King RW, Blundell CA, Schwartz OM, Andersen CH, Weigel D (2001) Evolution of floral meristem identity genes: analysis of Lolium temulentum genes related to APETALA1 and LEAFY of Arabidopsis. Plant Physiol 125: 1788–1801 Iwaki K, Haruna S, Niwa T, Kato K (2001) Adaptation and ecological differentiation in wheat with special reference to geographical variation of growth habit and Vrn genotype. Plant Breed 120: 107–114[CrossRef] Jang S, Hong MY, Chung YY, An G (1999) Ectopic expression of tobacco MADS genes modulates flowering time and plant architecture. Mol Cells 9: 576–586[Web of Science][Medline] Jeon JS, Lee S, Jung KH, Yang WS, Yi GH, Oh BG, An G (2000) Production of transgenic rice plants showing reduced heading date and plant height by ectopic expression of rice MADS box genes. Molecular Breeding: New Strategies in Plant Improvement 6: 581–592 Kane NA, Danyluk J, Tardif G, Ouellet F, Laliberte JF, Limin AE, Fowler DB, Sarhan F (2005) TaVRT-2, a member of the StMADS-11 clade of flowering repressors, is regulated by vernalization and photoperiod in wheat. Plant Physiol 138: 2354–2363 Karsai I, Szucs P, Meszaros K, Filichkina T, Hayes PM, Skinner JS, Lang L, Bedo Z (2005) The Vrn-H2 locus is a major determinant of flowering time in a facultative x winter growth habit barley (Hordeum vulgare L.) mapping population. Theor Appl Genet 110: 1458–1466[CrossRef][Web of Science][Medline] Kato K, Yokoyama H (1992) Geographical variation in heading characters among wheat landraces, Triticum aestivum L., and its implication for their adaptability. Theor Appl Genet 84: 259–265 Kyozuka J, Harcourt R, Peacock WJ, Dennis ES (1997) Eucalyptus has functional equivalents of the Arabidopsis AP1 gene. Plant Mol Biol 35: 573–584[CrossRef][Web of Science][Medline] Laurie DA, Pratchett N, Bezant JH, Snape JW (1995) RFLP mapping of five major genes and eight quantitative trait loci controlling flowering time in a winter x spring barley (Hordeum vulgare L.) cross. Genome 38: 575–585[Medline] Law CN (2000) The genetic control of flowering time in wheat. Flowering Newsletter 29: 22–25 Loukoianov A, Yan L, Blechl B, Sanchez A, Dubcovsky J (2005) Regulation of VRN-1 vernalization genes in normal and transgenic polyploid wheat. Plant Physiol 138: 2364–2373 Mandel MA, Yanofsky MF (1995) A gene triggering flower formation in Arabidopsis. Nature 377: 522–524[CrossRef][Medline] Michaels SD, Himmelblau E, Kim SY, Schomburg FM, Amasino RM (2005) Integration of flowering signals in winter-annual Arabidopsis. Plant Physiol 137: 149–156 Mouradov A, Cremer F, Coupland G (2002) Control of flowering time: interacting pathways as a basis for diversity. Plant Cell 14 (Suppl): S111–S130 Murai K, Miyamae M, Kato H, Takumi S, Ogihara Y (2003) WAP1, a wheat APETALA1 homolog, plays a central role in the phase transition from vegetative to reproductive growth. Plant Cell Physiol 44: 1255–1265 Pugsley AT (1971) A genetic analysis of the spring-winter habit of growth in wheat. Aust J Agric Res 22: 21–31[CrossRef][Web of Science] Read BJ, Raman H, McMichael G, Chalmers KJ, Ablett GA, Platz GJ, Raman R, Genger RK, Boyd WJR, Li CD, et al (2003) Mapping and QTL analysis of the barley population Sloop x Halcyon. Aust J Agric Res 45: 1145–1153[CrossRef] Schmitz J, Franzen R, Ngyuen TH, Garcia-Maroto F, Pozzi C, Salamini F, Rohde W (2000) Cloning, mapping and expression analysis of barley MADS-box genes. Plant Mol Biol 42: 899–913[CrossRef][Web of Science][Medline] Snape JW, Butterworth K, Whitechurch E, Worland AJ (2001) Waiting for fine times: genetics of flowering time in wheat. Euphytica 119: 185–190[CrossRef][Web of Science] Sung S, Amasino RM (2004) Vernalization and epigenetics: how plants remember winter. Curr Opin Plant Biol 7: 4–10[CrossRef][Web of Science][Medline] Sung S, Amasino RM (2005) Remembering winter: toward a molecular understanding of vernalization. Annu Rev Plant Biol 56: 491–508[CrossRef][Medline] Takahashi R, Yasuda S (1971) Genetics of earliness and growth habit in barley. In RA Nilan, ed, Barley Genetics II. Proceedings of the Second International Barley Genetics Symposium. Washington State University Press, Pullman, WA, pp 388–408 Tranquilli G, Dubcovsky J (2000) Epistatic interaction between vernalization genes Vrn-Am1 and Vrn-Am2 in diploid wheat. J Hered 91: 304–306 Trevaskis B, Bagnall DJ, Ellis MH, Peacock WJ, Dennis ES (2003) MADS box genes control vernalization-induced flowering in cereals. Proc Natl Acad Sci USA 100: 13099–13104 Yan L, Helguera M, Kato K, Fukuyama S, Sherman J, Dubcovsky J (2004a) Allelic variation at the VRN-1 promoter region in polyploid wheat. Theor Appl Genet 109: 1677–1686[CrossRef][Web of Science][Medline] Yan L, Loukoianov A, Blechl A, Tranquilli G, Ramakrishna W, SanMiguel P, Bennetzen JL, Echenique V, Dubcovsky J (2004b) The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science 303: 1640–1644 Yan L, Loukoianov A, Tranquilli G, Helguera M, Fahima T, Dubcovsky J (2003) Positional cloning of the wheat vernalization gene VRN1. Proc Natl Acad Sci USA 100: 6263–6268 This article has been cited by other articles:
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) or SD (
) that were harvested at 2-h intervals throughout a 24-h period. The indicated error is the SD for three technical repeats. Light and dark periods are indicated below graph as white or black bars, respectively, for both LD and SD treatments. LD, Long day; SD, short day.
