Vernalization, the promotion of flowering in response to a prolonged period of growth at low temperatures, is an important adaptation of plants growing in regions where harsh winters are followed by relatively short growing seasons. In these plants, flowering is triggered by long days but only after the vernalization requirement has been met. Thus, the requirement for vernalization prevents flowering in the long days of autumn and ensures that flowering occurs in the warmer days of spring and summer, allowing sufficient time for seed development before the onset of the next winter. Various crop plants, including the winter cereals and canola, must be vernalized if they are to initiate flowering and set seed. The key genes controlling the response to vernalization differ between monocots and dicots suggesting that this response arose independently after the divergence of the monocot and dicot lineages.

Key concepts:

  • Vernalization is the promotion of flowering in response to prolonged periods of low temperatures, such as those experienced in winter.

  • The physiological properties of vernalization are similar in dicots and monocots but the genes controlling this response differ.

  • The vernalized state is inherited through mitotic cell divisions; this memory of winter is provided by epigenetic changes to the chromatin of key genes in the vernalization response, although the nature of these changes differs between monocots and dicots.

  • Epigenetic regulation results in a heritable but potentially reversible change in gene expression that is modulated by changing the accessibility of a gene for transcription.

  • FLOWERING LOCUS C (FLC) is a key regulator of vernalization responsiveness in the Brassicaceae but the role of FLC homologues in other dicots remains to be elucidated.

  • The regulation of FLC expression is complex and involves both genetic and epigenetic mechanisms and FLC has become an important model for studying epigenetic control of plant gene expression.

  • VERNALIZATION INSENSITIVE 3 (VIN3) is induced by cold and the VIN3 protein is incorporated into the Polycomb Repression Complex (PRC2) that regulates FLC.

  • Polycomb proteins are conserved across kingdoms and play a role in gene repression in Drosophila, Caenorhabditis elegans and mammals.

  • The vernalized state is reset each generation; resetting occurs at different times depending on the gamete transmitting FLC.

  • An FLC orthologue conditions the perennial behaviour of Arabis alpina, a relative of Arabidopsis thaliana.

Keywords: Arabidopsis; winter wheat; FLC; epigenetic regulation; chromatin structure

Figure 1.

The flowering pathways in Arabidopsis. Members of the autonomous pathway are indicated in the yellow box. Some members of this pathway, including FRI and the three proteins with which it interacts (FRL1), (FES) and (SUF4), upregulate FLC expression. In contrast, the wild‐type function of other members of this pathway is to downregulate FLC. The activation of FLC expression by the FRI complex and by autonomous pathway mutants is dependent on the activity of proteins of the Paf1 complex ( (VIP3) to VIP6, also known as (ELF8) and ELF7), the SWR1 complex an ATP‐dependent chromatin remodelling complex ( (SUF3), (SWC6), (ARP4), (PIE1)) which deposits the histone variant H2A.Z into chromatin and lysine methyltransferases (ATX1), ATX2 and (EFS), also known as (SDG8). Mono‐ubiquitination of histone H2B is important for FLC activity – this is catalysed by (UBC1), UBC2, HUB1 (HISTONE MONOUBIQUTINATION), and HUB2. Other proteins important for FLC activity are (ESD4), ELF5 and HUA2. The activity of arginine methyltransferases (PRMT) represses FLC expression in nonvernalized plants and may also play a role in the vernalization pathway (reviewed in He, ). The major components of the vernalization pathway are shown in the blue box; (VRN5), also known as (VIL1) is a (PHD) protein related to VIN3. VRN1, a B3 domain DNA‐binding protein, is also required for stable repression of FLC. The daylength (photoperiod) pathway is represented here by CONSTANS (CO), which is upregulated in long days. CO activates the expression of the floral integrators, SUPPRESSOR OF CONSTANS 1 (SOC1) and FT, which integrate the signals from the autonomous pathway and the photoperiod pathway.

Figure 2.

The requirement for vernalization blocks flowering before winter, ensuring that flowering occurs during the longer and warmer days of spring. In Arabidopsis (top), flowering is blocked before winter as high FLC expression blocks the induction of FT. FLC is repressed by the low temperatures during winter, allowing FT (and SOC1) induction in the longer days of spring to promote flowering. In cereals (bottom), VRN2 represses FT expression in long days before winter. During winter, VRN1 is induced; expression of VRN1 remains high after winter when it represses VRN2, allowing long day induction of FT. Flowering is promoted by the combined action of VRN1 and FT proteins. Adapted from Trevaskis et al. , with permission from Elsevier.

Figure 3.

FLC expression is modulated by chromatin structure: (a) In nonvernalized plants, FLC chromatin bears the marks of an active gene – high levels of acetylation of lysine residues in the N‐terminal tails of histones H3 and H4 and high levels of H3K4me3 around the start of transcription and H3K36me3 in the transcribed region of the gene; the blue ovals represent the nucleosomes with the N‐terminal tails indicated as red lines. (b) VIN3 is induced by low temperatures and is required for the changes in histone modifications that are associated with repression of FLC, in plants grown at low temperatures. VIN3 is incorporated into a polycomb repression complex 2 (PRC2) during vernalization. This complex deposits the repressive mark H3K27me3 on chromatin around the start of transcription during growth at low temperatures. Neither the histone deacetylase(s) (HDAC) nor the histone demethylases that remove the active marks have been identified. (c) In vernalized plants that have been returned to warmer temperatures, the repressive mark H3K27me3 spreads bidirectionally across the FLC locus. The PRC2 (lacking VIN3) is associated with the chromatin covering the FLC locus (indicated by the coloured balls). Binding of LHP1 is essential for maintenance of FLC repression.

Figure 4.

FLC:GUS is reset in the somatic and sporogenous tissues in the male reproductive organ, the anther, and the paternally derived gene is expressed in the single‐celled zygotes from vernalized plants. In contrast, the maternally derived FLC:GUS gene is not reset during gametogenesis and is first expressed during embryogenesis. (a) A section through an anther from a vernalized FLC:GUS plant imaged under dark field (GUS crystals are pink). The pollen mother cells (arrow) are entering meiosis. Scale bars in all figures are 50 μm. (b) An ovule from a wild‐type female plant one day after pollination with pollen from a vernalized FLC:GUS plant, imaged under bright field (GUS product is blue). The arrow points to the single‐celled zygote. (c) An ovule from a wild‐type female plant three days after pollination with pollen from a vernalized FLC:GUS plant imaged under bright field (GUS product is blue). The arrow points to the early globular‐stage embryo. (d) A section through an ovule primordia around the time of meiosis (arrow) from a vernalized FLC:GUS plant imaged under dark field. No GUS staining is evident (e). An ovule from a vernalized FLC:GUS female plant one day after pollination with pollen from a wild‐type plant, imaged under bright field. No staining is evident (f). An ovule from a vernalized FLC:GUS female plant three days after pollination with pollen from a wild‐type plant, imaged under bright field (GUS product is blue). The arrow points to the early globular‐stage embryo.

Figure 5.

Integration of photoperiod and vernalization pathways in cereals. The VRN1 gene is induced by low temperatures in a quantitative manner; VRN1 promotes flowering directly and also acts to repress expression of VRN2, which is normally induced by long days. Before winter, VRN2 blocks the long day induction of FT but after winter, when VRN2 is repressed, long days can activate FT expression via the activity of (CO). Flowering is promoted by the combined activities of VRN1 and FT.



Bastow R, Mylne JS, Lister C et al. (2004) Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427: 164–167.

Bender J (2004) DNA methylation and epigenetics. Annual Review of Plant Biology 55: 41–68.

Burn JE, Bagnall DJ, Metzger JM, Dennis ES and Peacock WJ (1993) DNA methylation, vernalization, and the initiation of flowering. Proceedings of the National Academy of Sciences of the USA 90: 287–291.

Dennis ES and Peacock WJ (2007) Epigenetic regulation of flowering. Current Opinion in Plant Biology 10: 520–527.

Fang Q, Xu Z and Song R (2006) Cloning, characterization and genetic engineering of FLC homolog in Thellungiella halophila. Biochemical and Biophysical Research Communications 347: 707–714.

Finnegan EJ and Dennis ES (2007) Vernalization‐induced trimethylation of histone H3 lysine 27 at FLC is not maintained in mitotically quiescent cells. Current Biology 17: 1978–1983.

Finnegan EJ, Kovac KA, Jaligot E et al. (2005) The downregulation of FLOWERING LOCUS C (FLC) expression in plants with low levels of DNA methylation and by vernalization occurs by distinct mechanisms. Plant Journal 44: 420–432.

Gazzani S, Gendall AR, Lister C and Dean C (2003) Analysis of the molecular basis of flowering time variation in Arabidopsis accessions. Plant Physiology 132: 1107–1114.

He Y (2009) Control of the transition to flowering by chromatin modifications. Molecular Plant 2: 554–564.

Helliwell CA, Wood CC, Robertson M et al. (2006) The Arabidopsis FLC protein interacts directly in vivo with SOC1 and FT chromatin and is part of a high‐molecular‐weight complex. Plant Journal 46: 183–192.

Hemming MN, Fieg S, Peacock WJ, Dennis ES and Trevaskis B (2009) Regions associated with repression of the barley (Hordeum vulgare) VERNALIZATION1 gene are not required for cold induction. Molecular Geneticsand Genomics 282: 107–117.

Jenuwein T and Allis CD (2001) Translating the histone code. Science 293: 1074–1080.

Johansen U, West J, Lister C et al. (2001) Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290: 344–347.

Koorneef M, Blankestijn‐de Vries H, Hanhart CJ, Soppe W and Peeters T (1994) The phenotype of some late‐flowering mutants is enhanced by a locus on chromosome 5 that is not effective in the Landsberg‐erecta wild‐type. Plant Journal 6: 911–919.

Koorneef M, Hanhart CJ and van der Veen JH (1991) A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Molecular and General Genetics 229: 57–66.

Lang A (1965) Physiology of flower initiation. In: Ruhland W (ed.) Encyclopedia of Plant Physiology, pp. 1489–1536. Berlin, Germany: Springer.

Li Z, Zhao L, Cui C et al. (2005) Molecular cloning and characterization of an anti‐bolting related gene (BrpFLC) from Brassica rapa ssp. Pikinensis. Plant Science 168: 407–413.

Liu F, Quesada V, Crevillen P et al. (2007) The Arabidopsis RNA‐binding protein FCA requires a lysine‐specific demethylase 1 homolog to downregulate FLC. Molecular Cell 28: 398–407.

de Lucia F, Crevillen P, Jones AME, Greb T and Dean C (2008) A PHD‐polycomb repressive complex 2 triggers the epigenetic silencing of FLC during vernalization. Proceedings of the National Academy of Sciences of the USA 105: 16831–16836.

Michaels SD and Amasino RM (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11: 949–956.

Mylne JS, Barrett L, Tessadori F et al. (2006) LHP1, the Arabidopsis homologue of HETEROCHROMATIN PROTEIN 1, is required for epigenetic silencing of FLC. Proceedings of the National Academy of Sciences of the USA 103: 5012–5017.

Napp‐Zinn K (1987) Vernalization: environmental and genetic regulation. In: Atherton JG (ed.) Manipulation of Flowering, pp. 123–132. London: Butterworths.

Oliver SN, Finnegan EJ, Dennis ES, Peacock WJ and Trevaskis B (2009) Vernalization‐induced flowering in cereals is associated with changes in histone methylation at the VERNALIZATION 1 gene. Proceedings of the National Academy of Sciences of the USA 106: 8386–8391.

Purvis ON and Gregory FG (1937) Studies in vernalization of cereals. I. A comparative study of vernalization on winter rye by low temperatures and by short days. Annals of Botany 16: 569–591.

Reeves PA, He Y, Schmitz RJ et al. (2007) Evolutionary conservation of the FLOWERING LOCUS C‐mediated vernalization response: evidence from sugar beet (Beta vulgaris). Genetics 176: 295–307.

Schwabe WW (1955) Factors controlling flowering in Chrysanthemum IV. The site of vernalization and the translocation of the stimulus. Journal of Experimental Botany 5: 389–400.

Schwabe WW (1986) Historical sketches 16: vernalization. Journal of Experimental Botany 37: 572–573.

Searle I, He Y, Turck F et al. (2006) The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis. Genes & Development 20: 898–912.

Sheldon CC, Burn JE, Perez PP et al. (1999) The FLF MADS box gene: a repressor of flowering in Arabidopsis regulated by vernalization and methylation. Plant Cell 11: 445–458.

Sheldon CC, Hills MJ, Lister C et al. (2008) Resetting of FLOWERING LOCUS C expression after epigenetic repression by vernalization. Proceedings of the National Academy of Sciences of the USA 105: 2214–2219.

Sheldon CC, Rouse DT, Finnegan EJ, Peacock WJ and Dennis ES (2000) The molecular basis of vernalization: the central role of FLOWERING LOCUS C (FLC). Proceedings of the National Academy of Sciences of the USA 97: 3753–3758.

Shindo C, Aranzana MJ, Lister C et al. (2005) Role of FRIGIDA and FLOWERING LOCUS C in determining variation in flowering time in Arabidopsis. Plant Physiology 138: 1163–1173.

Shindo C, Lister C, Crevillen P, Nordborg M and Dean C (2006) Variation in the epigenetic silencing of FLC contributes to natural variation in Arabidopsis vernalization response. Genes & Development 20: 3079–3083.

Simpson GG (2004) The autonomous pathway: epigenetic and post‐transcriptional gene regulation in the control of Arabidopsis flowering time. Current Opinion in Plant Biology 7: 570–744.

Simpson GG and Dean C (2002) Arabidopsis, the Rosetta stone of flowering time? Science 296: 285–289.

Sung S and Amasino RM (2004) Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427: 159–164.

Sung S, He Y, Eshoo TW et al. (2006) Epigenetic maintenance of the vernalized state in Arabidopsis thaliana requires LIKE HETEROCHROMATIN PROTEIN1. Nature Genetics 38: 706–710.

Swiezewski S, Crevillen P, Liu F et al. (2007) Small RNA‐mediated chromatin silencing directed to the 3 region of the Arabidopsis gene encoding the developmental regulator, FLC. Proceedings of the National Academy of Sciences of the USA 104: 3633–3638.

Tadege M, Sheldon CC, Helliwell CA et al. (2001) Control of flowering time by FLC orthologues in Brassica napus. Plant Journal 28: 545–553.

Trevaskis B, Hemming MN, Dennis ES and Peacock WJ (2007) The molecular basis of vernalization‐induced flowering in cereals. Trends in Plant Science 12: 352–357.

Trevaskis B, Hemming MN, Peacock WJ and Dennis ES (2008) Low temperature and daylength cues are integrated to regulate FLOWERING LOCUS T in barley. Plant Physiology 147: 355–366.

Turck F, Fornara F and Coupland G (2008) Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Annual Review of Plant Biology 59: 573–594.

Turck F, Roudier F, Farrona S et al. (2007) Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimeylation of histone H3 lysine 27. PLoS Genetics 6: e86.

Wang R, Farrona S, Vincent C et al. (2009) PEP1 regulates perennial flowering in Arabis alpina. Nature 459: 423–427.

Wellensiek SJ (1964) Dividing cells as the prerequisite for vernalization. Plant Physiology 39: 832–835.

Wood CC, Robertson M, Tanner G et al. (2006) The Arabidopsis thaliana vernalization response requires a polycomb‐like protein complex that also includes VERNALIZATION INSENSITIVE 3. Proceedings of the National Academy of Sciences of the USA 103: 14631–14636.

Yan L, Helguera M, Kato K et al. (2004b) Allelic variation at the VRN‐1 promoter region in polyploid wheat. Theoretical and Applied Genetics 109: 1677–1686.

Yan L, Loukoianov A, Blechl A et al. (2004a) The wheat VRN2 gene is a flowering repressor down‐regulated by vernalization. Science 303: 1640–1644.

Zhang X, Germann S, Blus BJ et al. (2007) The Arabidopsis LHP1 protein colocalizes with histone H3 Lys27 methylation. Nature Structural and Molecular Biology 14: 869–871.

Further Reading

Farrona S, Coupland G and Turck F (2008) The impact of chromatin regulation on the floral transition. Seminars in Cell and Developmental Biology 19: 560–573.

Greenup A, Peacock WJ, Dennis ES and Trevaskis B (2009) The molecular biology of seasonal flowering‐responses in Arabidopsis and the cereals. Annals of Botany (London) 103: 1165–1172.

Hennig L and Derkacheva M (2009) Diversity of polycomb group complexes in plants: same rules, different players? Trends in Genetics 25: 414–423.

Kohler CV and Villar CBR (2009) Programming of gene expression by polycomb group proteins. Trends in Cell Biology 18: 236–242.

Laurie DA, Pratchett N, Bezant JH and Snape JW (1995) RFPL 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.

March‐Diaz J and Reyes JC (2009) The beauty of being a variant: H2A.Z and the SWR1 complex in plants. Molecular Plant 2: 565–577.

Osborn TC, Kole C, Parkin IAP, Sharpe AG and Kuiper M (1997) Comparison of flowering time genes in Brassica rapa, B. napus and Arabidopsis thaliana. Genetics 146: 1123–1129.

Yan L, Loukoianov A, Tranquilli G et al. (2003) Positional cloning of the wheat vernalization gene VRN1. Proceedings of the National Academy of Sciences of the USA 100: 6263–6268.

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Jean Finnegan, E, Helliwell, Chris, Sheldon, Candice, James Peacock, W, and Dennis, Elizabeth S(Mar 2010) Vernalization. In: eLS. John Wiley & Sons Ltd, Chichester. [doi: 10.1002/9780470015902.a0002048.pub3]