Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Remembering winter through vernalisation

Nature Plants volume 4, pages 997–1009 (2018)Cite this article

Subjects

Abstract

Vernalisation is the programmed physiological process in which prolonged cold-exposure provides competency to flower in plants; widely found in winter and biennial species, such as Arabidopsis, fruit trees, vegetables and wheat. This phenomenon is regulated by diverse genetic networks, and memory of vernalisation in a life cycle mainly depends on epigenetic mechanisms. However, less is known about how to count winter-dosage for flowering in plants. Here, we compare the vernalisation genetic framework between the dicots Arabidopsis, temperate grasses, wheat, barley and Brachypodium. We discuss vernalisation mechanisms involving crosstalk between phosphorylation and O-GlcNAcylation modification of key proteins, and epigenetic modifications of the key gene VRN1 in wheat. We also highlight the potential evolutionary origins of vernalisation in various species. Current progress toward understanding the regulation of vernalisation requirements provides insight that will inform the design of molecular breeding strategies for winter crops.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Life-cycle transitions of winter wheat and rice in response to seasonal changes.
Fig. 2: Comparison of the vernalisation gene-regulatory networks of Arabidopsis and wheat.
Fig. 3: Epigenetic silencing of FLC to count the duration of vernalisation.
Fig. 4: The regulatory role of the O-GlcNAc signal in vernalisation.

Similar content being viewed by others

References

  1. Zhu, J. K. Abiotic stress signaling and responses in plants. Cell 167, 313–324 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Guo, X. Y., Liu, D. F. & Chong, K. Cold signaling in plants: insights into mechanisms and regulation. J. Integr. Plant Biol. 60, 745–756 (2018).

    Article  PubMed  Google Scholar 

  3. Liu, J. Y., Shi, Y. T. & Yang, S. H. Insights into the regulation of C-repeat binding factors in plant cold signaling. J. Integr. Plant Biol. 60, 780–795 (2018).

    Article  PubMed  Google Scholar 

  4. Bin Rahman, A. & Zhang, J. Preferential geographic distribution pattern of abiotic stress tolerant rice. Rice 11, 10 (2018).

    Article  Google Scholar 

  5. Kim, H. Y., Ko, J., Kang, S. & Tenhunen, J. Impacts of climate change on paddy rice yield in a temperate climate. Glob. Change Biol. 19, 548–562 (2013).

    Article  Google Scholar 

  6. Laudencia-Chingcuanco, D. et al. Genome-wide gene expression analysis supports a developmental model of low temperature tolerance gene regulation in wheat (Triticum aestivum L.). BMC Genomics 12, 299 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Morran, S. et al. Improvement of stress tolerance of wheat and barley by modulation of expression of DREB/CBF factors. Plant Biotechnol. J. 9, 230–249 (2011).

    Article  CAS  PubMed  Google Scholar 

  8. Deng, W. et al. Direct links between the vernalization response and other key traits of cereal crops. Nat. Commun. 6, 5882 (2015).

    Article  PubMed  Google Scholar 

  9. Fjellheim, S., Boden, S. & Trevaskis, B. The role of seasonal flowering responses in adaptation of grasses to temperate climates. Front Plant Sci. 5, 432 (2014).

    Article  Google Scholar 

  10. Oliver, S. N., Deng, W., Casao, M. C. & Trevaskis, B. Low temperatures induce rapid changes in chromatin state and transcript levels of the cereal VERNALIZATION1 gene. J. Exp. Bot. 64, 2413–2422 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Chouard, P. Vernalization and its relations of dormancy. Annu. Rev. Plant Physiol. Plant Mol. Biol. 11, 191–238 (1960).

    Article  CAS  Google Scholar 

  12. Ma, Y. et al. COLD1 confers chilling tolerance in rice. Cell 160, 1209–1221 (2015).

    Article  CAS  PubMed  Google Scholar 

  13. Zhang, Z. et al. OsMAPK3 phosphorylates OsbHLH002/OsICE1 and inhibits its ubiquitination to activate OsTPP1 and enhances rice chilling tolerance. Dev. Cell 43, 731–743 (2017).

    Article  CAS  PubMed  Google Scholar 

  14. Fowler, D. B., Chauvin, L. P., Limin, A. E. & Sarhan, F. The regulatory role of vernalization in the expression of low-temperature-induced genes in wheat and rye. Theor. Appl. Genet. 93, 554–559 (1996).

    Article  CAS  PubMed  Google Scholar 

  15. Galiba, G. et al. Regulatory genes involved in the determination of frost tolerance in temperate cereals. Plant Sci. 176, 12–19 (2009).

    Article  CAS  Google Scholar 

  16. Shahryar, N. & Maali-Amiri, R. Metabolic acclimation of tetraploid and hexaploid wheats by cold stress-induced carbohydrate accumulation. J. Plant Physiol. 204, 44–53 (2016).

    Article  CAS  PubMed  Google Scholar 

  17. Li, Q. et al. Transcriptomic insights into phenological development and cold tolerance of wheat grown in the field. Plant Physiol. 176, 2376–2394 (2018).

    Article  CAS  PubMed  Google Scholar 

  18. Pearce, S. et al. Large deletions in the CBF gene cluster at the Fr-B2 locus are associated with reduced frost tolerance in wheat. Theor. Appl. Genet. 126, 2683–2697 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  19. Colton-Gagnon, K. et al. Comparative analysis of the cold acclimation and freezing tolerance capacities of seven diploid Brachypodium distachyon accessions. Ann. Bot. 113, 681–693 (2014).

    Article  PubMed  Google Scholar 

  20. Sasaki, K., Christov, N. K., Tsuda, S. & Imai, R. Identification of a novel LEA protein involved in freezing tolerance in wheat. Plant Cell Physiol. 55, 136–147 (2014).

    Article  CAS  PubMed  Google Scholar 

  21. Ying, M. & Kidou, S. Discovery of novel cold-induced CISP genes encoding small RNA-binding proteins related to cold adaptation in barley. Plant Sci. 260, 129–138 (2017).

    Article  CAS  PubMed  Google Scholar 

  22. Shrestha, R., Gomez-Ariza, J., Brambilla, V. & Fornara, F. Molecular control of seasonal flowering in rice, arabidopsis and temperate cereals. Ann. Bot. 114, 1445–1458 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Andres, F. & Coupland, G. The genetic basis of flowering responses to seasonal cues. Nat. Rev. Genet. 13, 627–639 (2012).

    Article  CAS  PubMed  Google Scholar 

  24. Casal, J. J. & Questa, J. I. Light and temperature cues: multitasking receptors and transcriptional integrators. New Phytol. 217, 1029–1034 (2018).

    Article  PubMed  Google Scholar 

  25. Franks, S. J., Sim, S. & Weis, A. E. Rapid evolution of flowering time by an annual plant in response to a climate fluctuation. Proc. Natl Acad. Sci. USA 104, 1278–1282 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Greenup, A., Peacock, W. J., Dennis, E. S. & Trevaskis, B. The molecular biology of seasonal flowering-responses in Arabidopsis and the cereals. Ann. Bot. 103, 1165–1172 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Distelfeld, A., Li, C. & Dubcovsky, J. Regulation of flowering in temperate cereals. Curr. Opin. Plant Biol. 12, 178–184 (2009).

    Article  CAS  PubMed  Google Scholar 

  28. Yan, L. et al. Positional cloning of the wheat vernalization gene VRN1. Proc. Natl Acad. Sci. USA 100, 6263–6268 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Bastow, R. et al. Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427, 164–167 (2004).

    Article  CAS  PubMed  Google Scholar 

  30. Nowak, M. et al. Analysis of VRN1 gene in triticale and common wheat genetic background. Sci. Agricola 71, 380–386 (2014).

    Article  CAS  Google Scholar 

  31. Trevaskis, B. The central role of the VERNALIZATION1 gene in the vernalization response of cereals. Funct. Plant Biol. 37, 479–487 (2010).

    Article  CAS  Google Scholar 

  32. Johanson, U. et al. Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290, 344–347 (2000).

    Article  CAS  PubMed  Google Scholar 

  33. Michaels, S. D. & Amasino, R. M. FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11, 949–956 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Sheldon, C. C. et al. The molecular basis of vernalization: the central role of FLOWERING LOCUS C (FLC). Proc. Natl Acad. Sci. USA 97, 3753–3758 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Choi, K. et al. The FRIGIDA complex activates transcription of FLC, a strong flowering repressor in Arabidopsis, by recruiting chromatin modification factors. Plant Cell 23, 289–303 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Alexandre, C. M. & Hennig, L. FLC or not FLC: the other side of vernalization. J. Exp. Biol. 59, 1127–1135 (2008).

    CAS  Google Scholar 

  37. Michaels, S. D. et al. Integration of flowering signals in winter-annual Arabidopsis. Plant Physiol. 137, 149–156 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Sheldon, C. C., Finnegan, E. J., Dennis, E. S. & Peacock, W. J. Quantitative effects of vernalization on FLC and SOC1 expression. Plant J. 45, 871–883 (2006).

    Article  CAS  PubMed  Google Scholar 

  39. Bond, D. M., Dennis, E. S. & Finnegan, E. J. Hypoxia: a novel function for VIN3. Plant Signal. Behav. 4, 773–776 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Gendall, A. R., Levy, Y. Y., Wilson, A. & Dean, C. The VERNALIZATION 2 gene mediates the epigenetic regulation of vernalization in Arabidopsis. Cell 107, 525–535 (2001).

    Article  CAS  PubMed  Google Scholar 

  41. Levy, Y. Y. et al. Multiple roles of Arabidopsis VRN1 in vernalization and flowering time control. Science 297, 243–246 (2002).

    Article  CAS  PubMed  Google Scholar 

  42. Searle, I. et al. The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis. Genes Dev. 20, 898–912 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Wood, C. C. et al. The Arabidopsis thaliana vernalization response requires a polycomb-like protein complex that also includes VERNALIZATION INSENSITIVE 3. Proc. Natl Acad. Sci. USA 103, 14631–14636 (2006).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  45. Yang, H. et al. Distinct phases of Polycomb silencing to hold epigenetic memory of cold in Arabidopsis. Science 357, 1142–1145 (2017).

    Article  CAS  PubMed  Google Scholar 

  46. Sung, S. & Amasino, R. M. Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427, 159–164 (2004).

    Article  CAS  PubMed  Google Scholar 

  47. Bond, D. M., Dennis, E. S., Pogson, B. J. & Finnegan, E. J. Histone acetylation, VERNALIZATION INSENSITIVE 3, FLOWERING LOCUS C, and the vernalization response. Mol. Plant 2, 724–737 (2009).

    Article  CAS  PubMed  Google Scholar 

  48. Greb, T. et al. The PHD finger protein VRN5 functions in the epigenetic silencing of Arabidopsis FLC. Curr. Biol. 17, 73–78 (2007).

    Article  CAS  PubMed  Google Scholar 

  49. Mylne, J. S. et al. LHP1, the Arabidopsis homologue of HETEROCHROMATIN PROTEIN1, is required for epigenetic silencing of FLC. Proc. Natl Acad. Sci. USA 103, 5012–5017 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Turck, F. et al. Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimethylation of histone H3 lysine 27. PLoS Genet. 3, 855–866 (2007).

    Article  CAS  Google Scholar 

  51. Sung, S. et al. Epigenetic maintenance of the vernalized state in Arabidopsis thaliana requires LIKE HETEROCHROMATIN PROTEIN 1. Nat. Genet. 38, 706–710 (2006).

    Article  CAS  PubMed  Google Scholar 

  52. Yan, L. et al. The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science 303, 1640–1644 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Yan, L. et al. The wheat and barley vernalization gene VRN3 is an orthologue of FT. Proc. Natl Acad. Sci. USA 103, 19581–19586 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Dubcovsky, J. Regulation of flowering time in wheat and barley. Comp. Biochem. Phys. A 141, 263–264 (2005).

    Google Scholar 

  55. Dhillon, T. et al. Regulation of freezing tolerance and flowering in temperate cereals: the VRN-1 connection. Plant Physiol. 153, 1846–1858 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Golovnina, K. A., Kondratenko, E. Y., Blinov, A. G. & Goncharov, N. P. Molecular characterization of vernalization loci VRN1 in wild and cultivated wheats. BMC Plant Biol. 10, 168 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  57. Ferrandiz, C., Gu, Q., Martienssen, R. & Yanofsky, M. F. Redundant regulation of meristem identity and plant architecture by FRUITFULL, APETALA1 and CAULIFLOWER. Development 127, 725–734 (2000).

    Article  CAS  PubMed  Google Scholar 

  58. Konopatskaia, I. et al. VRN1 genes variability in tetraploid wheat species with a spring growth habit. BMC Plant Biol. 16, 244 (2016).

    Article  PubMed  CAS  Google Scholar 

  59. Fu, D. L. et al. 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 (2005).

    Article  CAS  PubMed  Google Scholar 

  60. Yan, L. et al. Allelic variation at the VRN-1 promoter region in polyploid wheat. Theor. Appl. Genet. 109, 1677–1686 (2004).

    Article  CAS  PubMed  Google Scholar 

  61. Muterko, A., Kalendar, R. & Salina, E. Novel alleles of the VERNALIZATION1 genes in wheat are associated with modulation of DNA curvature and flexibility in the promoter region. BMC Plant Biol. 16, 9 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Kamran, A., Randhawa, H. S., Yang, R. C. & Spaner, D. The effect of VRN1 genes on important agronomic traits in high-yielding Canadian soft white spring wheat. Plant Breeding 133, 321–326 (2014).

    Article  CAS  Google Scholar 

  63. Kosner, J. & Pankova, K. The detection of allelic variants at the recessive vrn loci of winter wheat. Euphytica 101, 9–16 (1998).

    Article  Google Scholar 

  64. Shcherban, A. B., Khlestkina, E. K., Efremova, T. T. & Salina, E. A. The effect of two differentially expressed wheat VRN-B1 alleles on the heading time is associated with structural variation in the first intron. Genetica 141, 133–141 (2013).

    Article  CAS  PubMed  Google Scholar 

  65. Xing, L. et al. Phosphorylation modification of wheat lectin VER2 is associated with vernalization-induced O-GlcNAc signaling and intracellular motility. PLoS ONE 4, e4854 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Yong, W. D. et al. Vernalization-induced flowering in wheat is mediated by a lectin-like gene VER2. Planta 217, 261–270 (2003).

    Article  CAS  PubMed  Google Scholar 

  67. Xiao, J. et al. O-GlcNAc-mediated interaction between VER2 and TaGRP2 elicits TaVRN1 mRNA accumulation during vernalization in winter wheat. Nat. Commun. 5, 4572 (2014).

    Article  CAS  PubMed  Google Scholar 

  68. Kippes, N. et al. Fine mapping and epistatic interactions of the vernalization gene VRN-D4 in hexaploid wheat. Mol. Genet. Genomics 289, 47–62 (2014).

    Article  CAS  PubMed  Google Scholar 

  69. Kippes, N. et al. Identification of the VERNALIZATION 4 gene reveals the origin of spring growth habit in ancient wheats from South Asia. Proc. Natl Acad. Sci. USA 112, 5401–5410 (2015).

    Article  CAS  Google Scholar 

  70. Woods, D. P. et al. Establishment of a vernalization requirement in Brachypodium distachyon requires REPRESSOR OF VERNALIZATION1. Proc. Natl Acad. Sci. USA 114, 6623–6628 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Chen, A. & Dubcovsky, J. Wheat TILLING mutants show that the vernalization gene VRN1 down-regulates the flowering repressor VRN2 in leaves but is not essential for flowering. PLoS Genet. 8, e1003134 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Distelfeld, A. et al. Genetic and molecular characterization of the VRN2 loci in tetraploid wheat. Plant Physiol. 149, 245–257 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Dubcovsky, J. et al. Effect of photoperiod on the regulation of wheat vernalization genes VRN1 and VRN2. Plant Mol. Biol. 60, 469–480 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Dubcovsky, J., Chen, C. L. & Yan, L. L. Molecular characterization of the allelic variation at the VRN-H2 vernalization locus in barley. Mol. Breeding 15, 395–407 (2005).

    Article  CAS  Google Scholar 

  75. Li, Y. & Xu, M. CCT family genes in cereal crops: A current overview. Crop J. 5, 449–458 (2017).

    Article  Google Scholar 

  76. Pin, P. A. et al. An antagonistic pair of FT homologs mediates the control of flowering time in sugar beet. Science 330, 1397–1400 (2010).

    Article  CAS  PubMed  Google Scholar 

  77. Abe, M. et al. FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science 309, 1052–1056 (2005).

    Article  CAS  PubMed  Google Scholar 

  78. Li, C. & Dubcovsky, J. Wheat FT protein regulates VRN1 transcription through interactions with FDL2. Plant J. 55, 543–554 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Li, C., Lin, H. & Dubcovsky, J. Factorial combinations of protein interactions generate a multiplicity of florigen activation complexes in wheat and barley. Plant J. 84, 70–82 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Distelfeld, A. & Dubcovsky, J. Characterization of the maintained vegetative phase deletions from diploid wheat and their effect on VRN2 and FT transcript levels. Mol. Genet. Genomics 283, 223–232 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Hemming, M. N., Peacock, W. J., Dennis, E. S. & Trevaskis, B. Low-temperature and daylength cues are integrated to regulate FLOWERING LOCUS T in barley. Plant Physiol. 147, 355–366 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Shimada, S. et al. A genetic network of flowering-time genes in wheat leaves, in which an APETALA1/FRUITFULL-like gene, VRN1, is upstream of FLOWERING LOCUS T. Plant J. 58, 668–681 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Li, C., Distelfeld, A., Comis, A. & Dubcovsky, J. Wheat flowering repressor VRN2 and promoter CO2 compete for interactions with NUCLEAR FACTOR-Y complexes. Plant J. 67, 763–773 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Chen, A. et al. PHYTOCHROME C plays a major role in the acceleration of wheat flowering under long-day photoperiod. Proc. Natl Acad. Sci. USA 111, 10037–10044 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Pearce, S. et al. RNA-seq studies using wheat PHYTOCHROME B and PHYTOCHROME C mutants reveal shared and specific functions in the regulation of flowering and shade-avoidance pathways. BMC Plant Biol. 16, 141 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  86. Muterko, A. F., Balashova, I. A., Fayt, V. I. & Sivolap, Y. M. Molecular-genetic mechanisms of regulation of growth habit in wheat. Cytol. Genet. 49, 58–71 (2015).

    Article  Google Scholar 

  87. Greenup, A. G. et al. ODDSOC2 Is a MADS box floral repressor that is down-regulated by vernalization in temperate cereals. Plant Physiol. 153, 1062–1073 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Sharma, N. et al. A Flowering Locus C homolog is a vernalization-regulated repressor in Brachypodium and is cold regulated in wheat. Plant Physiol. 173, 1301–1315 (2017).

    Article  CAS  PubMed  Google Scholar 

  89. Higgins, J. A., Bailey, P. C. & Laurie, D. A. Comparative genomics of flowering time pathways using Brachypodium distachyon as a model for the temperate grasses. PLoS ONE 5, e10065 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  90. Ream, T. S. et al. Interaction of photoperiod and vernalization determines flowering time of Brachypodium distachyon. Plant Physiol. 164, 694–709 (2014).

    Article  CAS  PubMed  Google Scholar 

  91. Woods, D. P., Ream, T. S. & Amasino, R. M. Memory of the vernalized state in plants including the model grass Brachypodium distachyon. Front Plant Sci. 5, 99 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  92. Woods, D. P. et al. Evolution of VRN2/Ghd7-like genes in vernalization-mediated repression of grass flowering. Plant Physiol. 170, 2124–2135 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Feng, Y., Yin, Y. & Fei, S. BdVRN1 expression confers flowering competency and is negatively correlated with freezing tolerance in Brachypodium distachyon. Front Plant Sci. 8, 1107 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  94. Chen, L. et al. OsMADS57 together with OsTB1 coordinates transcription of its target OsWRKY94 and D14 to switch its organogenesis to defense for cold adaptation in rice. New Phytol. 218, 219–231 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Sung, S. Epigenetic memory of winter by plants. Integr. Comp. Biol. 54, 203 (2014).

    Google Scholar 

  96. Curtis, O. & Chang, H. The relative effectiveness of the temperature of the crown as contrasted with that of the rest of the plant upon the flowering of celery plants. Am. J. Botany, 1047–1048 (1930).

  97. Melchers, G. Versuche zur genetik und entwicklungs-physiologie der blühreife. Biol. Zentralbl. 56, 567–570 (1936).

    Google Scholar 

  98. Crosthwaite, S. K. & Jenkins, G. I. The role of leaves in the perception of vernalizing temperatures in sugar-beet. J. Exp. Bot. 44, 801–806 (1993).

    Article  Google Scholar 

  99. Metzger, J. D. Localization of the site of perception of thermoinductive temperatures in Thlaspi arvense L. Plant Physiol. 88, 424–428 (1988).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Wellensiek, S. J. Dividing cells as locus for vernalization. Nature 195, 307 (1962).

    Article  Google Scholar 

  101. Wellensiek, S. J. Dividing cells as prerequisite for vernalization. Plant Physiol. 39, 832 (1964).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Sung, S. & Amasino, R. M. Vernalization and epigenetics: how plants remember winter. Curr. Opin Plant Biol. 7, 4–10 (2004).

    Article  CAS  PubMed  Google Scholar 

  103. Amasino, R. Vernalization, competence, and the epigenetic memory of winter. Plant Cell 16, 2553–2559 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Lang, A. & Melchers, G. Vernalization und devernalisation bei einer zweijahrigen pelanze. Z. Naturforsch. B 2, 444–449 (1947).

    Article  Google Scholar 

  105. Lang, A. in Encyclopedia of Plant Physiology Vol. 15 (ed. Ruhland, W.) 1380–1536 (Springer-Verlag, Berlin, 1965).

  106. Oliver, S. N. et al. Vernalization-induced flowering in cereals is associated with changes in histone methylation at the VERNALIZATION1 gene. Proc. Natl Acad. Sci. USA 106, 8386–8391 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Yong, W. D. et al. Cloning and characterization of vernalization-related gene (ver203F) cDNA 3’ end. Chinese Science Bulletin 44, 1289–1294 (1999).

    Article  CAS  Google Scholar 

  108. Berr, A. et al. SET DOMAIN GROUP25 encodes a histone methyltransferase and is involved in FLOWERING LOCUS C activation and repression of flowering. Plant Physiol. 151, 1476–1485 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Deal, R. B., Topp, C. N., McKinney, E. C. & Meagher, R. B. Repression of flowering in Arabidopsis requires activation of FLOWERING LOCUS C expression by the histone variant H2A. Z. Plant Cell 19, 74–83 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Pien, S. et al. ARABIDOPSIS TRITHORAX1 dynamically regulates FLOWERING LOCUS C activation via histone 3 lysine 4 trimethylation. Plant Cell 20, 580–588 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Hu, X. et al. Proteasome-mediated degradation of FRIGIDA modulates flowering time in Arabidopsis during vernalization. Plant Cell 26, 4763–4781 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Xiao, J. et al. Cis and trans determinants of epigenetic silencing by Polycomb repressive complex 2 in Arabidopsis. Nat. Genet. 49, 1546–1552 (2017).

    Article  CAS  PubMed  Google Scholar 

  113. Zhou, Y. et al. Telobox motifs recruit CLF/SWN-PRC2 for H3K27me3 deposition via TRB factors in Arabidopsis. Nat. Genet. 50, 638–644 (2018).

    Article  CAS  PubMed  Google Scholar 

  114. Heo, J. B., Lee, Y. S. & Sung, S. Epigenetic regulation by long noncoding RNAs in plants. Chromosome Res. 21, 685–693 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Kim, D. H. & Sung, S. The binding specificity of the PHD-finger domain of VIN3 moderates vernalization response. Plant Physiol. 173, 1258–1268 (2017).

    Article  CAS  PubMed  Google Scholar 

  116. Csorba, T., Questa, J. I., Sun, Q. & Dean, C. Antisense COOLAIR mediates the coordinated switching of chromatin states at FLC during vernalization. Proc. Natl Acad. Sci. USA 111, 16160–16165 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Heo, J. B. & Sung, S. Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331, 76–79 (2011).

    Article  CAS  PubMed  Google Scholar 

  118. Kim, D. H. & Sung, S. Vernalization-triggered intragenic chromatin loop formation by long noncoding RNAs. Dev. Cell 40, 302–312 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Questa, J. I. et al. Arabidopsis transcriptional repressor VAL1 triggers Polycomb silencing at FLC during vernalization. Science 353, 485–488 (2016).

    Article  PubMed  CAS  Google Scholar 

  120. Yuan, W. et al. A cis cold memory element and a trans epigenome reader mediate Polycomb silencing of FLC by vernalization in Arabidopsis. Nat. Genet. 48, 1527–1534 (2016).

    Article  CAS  PubMed  Google Scholar 

  121. Zhu, D., Rosa, S. & Dea, nC. Nuclear organization changes and the epigenetic silencing of FLC during vernalization. J. Mol. Biol. 427, 659–669 (2015).

    Article  CAS  PubMed  Google Scholar 

  122. Kim, D. H., Zografos, B. R. & Sung, S. Mechanisms underlying vernalization-mediated VIN3 induction in Arabidopsis. Plant Signal. Behav. 5, 1457–1459 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Velanis, C. N. & Goodrich, J. Vernalization and epigenetic inheritance: a game of histones. Curr. Biol. 27, 1324–1326 (2017).

    Article  CAS  Google Scholar 

  124. Tao, Z. et al. Embryonic epigenetic reprogramming by a pioneer transcription factor in plants. Nature 551, 124 (2017).

    Article  PubMed  CAS  Google Scholar 

  125. Hepworth, J. & Dean, C. Flowering Locus C’s lessons: conserved chromatin switches underpinning developmental timing and adaptation. Plant Physiol. 168, 1237–1245 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Whittaker, C. & Dean, C. The FLC Locus: a platform for discoveries in epigenetics and adaptation. Ann Rev Cell Dev. Biol. 33, 555–575 (2017).

    Article  CAS  Google Scholar 

  127. Berry, S. et al. Local chromatin environment of a Polycomb target gene instructs its own epigenetic inheritance. eLife 4, e07205 (2015).

    Article  CAS  PubMed Central  Google Scholar 

  128. Crevillen, P. et al. Epigenetic reprogramming that prevents transgenerational inheritance of the vernalized state. Nature 515, 587 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Diallo, A. O. et al. Expression of vernalization responsive genes in wheat is associated with histone H3 trimethylation. Mol. Genet. Genomics 287, 575–590 (2012).

    Article  CAS  PubMed  Google Scholar 

  130. Chittock, E. C., Latwiel, S., Miller, T. & Mueller, C. W. Molecular architecture of polycomb repressive complexes. Biochem. Soc. T 45, 193–205 (2017).

    Article  CAS  Google Scholar 

  131. Simon, J. A. & Tamkun, J. W. Programming off and on states in chromatin: mechanisms of Polycomb and trithorax group complexes. Curr. Opin. Genet. Dev. 12, 210–218 (2002).

    Article  CAS  PubMed  Google Scholar 

  132. Lomax, A. et al. An ortholog of CURLY LEAF/ENHANCER OF ZESTE like-1 is required for proper flowering in Brachypodium distachyon. Plant J. 93, 871–882 (2018).

    Article  CAS  PubMed  Google Scholar 

  133. Huan, Q. et al. Transcriptome-wide analysis of vernalization reveals conserved and species-specific mechanisms in Brachypodium. J. Integr. Plant Biol. 55, 696–709 (2013).

    Article  CAS  PubMed  Google Scholar 

  134. Huan, Q., Mao, Z., Chong, K. & Zhang, J. Global analysis of H3K4me3/H3K27me3 in Brachypodium distachyon reveals VRN3 as critical epigenetic regulation point in vernalization and provides insights into epigenetic memory. New Phytol. 219, 1373–1387 (2018).

    Article  CAS  PubMed  Google Scholar 

  135. Bernier, G. & Perilleux, C. A physiological overview of the genetics of flowering time control. Plant Biotechnol. J. 3, 3–16 (2005).

    Article  CAS  PubMed  Google Scholar 

  136. Trione, E. J. Metabolic changes associated with vernalization of wheat. I. carbohydrate and nitrogen patterns. Plant Physiol. 41, 277–281 (1966).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Teo, C. F., Wollaston-Hayden, E. E. & Wells, L. Hexosamine flux, the O-GlcNAc modification, and the development of insulin resistance in adipocytes. Mol. Cell Endocrinol. 318, 44–53 (2010).

    Article  CAS  PubMed  Google Scholar 

  138. Rafie, K. et al. Recognition of a glycosylation substrate by the O-GlcNAc transferase TPR repeats. Open Biol. 7, 170078 (2017).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  139. Nagel, A. K. & Ball, L. E. O-GlcNAc transferase and O-GlcNAcase: achieving target substrate specificity. Amino Acids 46, 2305–2316 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Hu, P., Shimoji, S. & Hart, G. W. Site-specific interplay between O-GlcNAcylation and phosphorylation in cellular regulation. FEBS Lett. 584, 2526–2538 (2010).

    Article  CAS  PubMed  Google Scholar 

  141. Butkinaree, C., Park, K. & Hart, G. W. O-linked beta-N-acetylglucosamine (O-GlcNAc): extensive crosstalk with phosphorylation to regulate signalling and transcription in response to nutrients and stress. Biochim. Biophys. Acta 1800, 96–106 (2010).

    Article  CAS  PubMed  Google Scholar 

  142. Slawson, C. & Hart, G. W. Dynamic interplay between O-GlcNAc and O-phosphate: the sweet side of protein regulation. Curr. Opin. Struct. Biol. 13, 631–636 (2003).

    Article  CAS  PubMed  Google Scholar 

  143. Olszewski, N. E., West, C. M., Sassi, S. O. & Hartweck, L. M. O-GlcNAc protein modification in plants: Evolution and function. Biochim. Biophys. Acta 1800, 49–56 (2010).

    Article  CAS  PubMed  Google Scholar 

  144. Zentella, R. et al. O-GlcNAcylation of master growth repressor DELLA by SECRET AGENT modulates multiple signaling pathways in Arabidopsis. Genes Dev. 30, 164–176 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Zentella, R. et al. The Arabidopsis O-fucosyltransferase SPINDLY activates nuclear growth repressor DELLA. Nat. Chem. Biol. 13, 479–485 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Xu, S. L. et al. Proteomic analysis reveals O-GlcNAc modification on proteins with key regulatory functions in Arabidopsis. Proc. Natl Acad. Sci. USA 114, 1536–1543 (2017).

    Article  CAS  Google Scholar 

  147. Xing, L. et al. Arabidopsis O-GlcNAc transferase SEC targets histone methyltransferase ATX1 to regulate flowering. EMBO J. 37, e98115 (2018).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  148. Humphreys, A. M. & Linder, H. Evidence for recent evolution of cold tolerance in grasses suggests current distribution is not limited by (low) temperature. New Phytol. 198, 1261–1273 (2013).

    Article  PubMed  Google Scholar 

  149. Poethig, R. S. Phase change and the regulation of developmental timing in plants. Science 301, 334–336 (2003).

    Article  CAS  PubMed  Google Scholar 

  150. McKeown, M. et al. Evidence for an early origin of vernalization responsiveness in temperate pooideae grasses. Plant Physiol. 172, 416–426 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  151. Christin, P. A. et al. Molecular dating, evolutionary rates, and the age of the grasses. Syst. Biol. 63, 153–165 (2014).

    Article  PubMed  Google Scholar 

  152. Zhong, J., Robbett, M., Poire, A. & Preston, J. C. Successive evolutionary steps drove Pooideae grasses from tropical to temperate regions. New Phytol. 217, 925–938 (2018).

    Article  CAS  PubMed  Google Scholar 

  153. Xue, W. et al. Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat. Genet. 40, 761–767 (2008).

    Article  CAS  PubMed  Google Scholar 

  154. Woods, D. P. et al. Genetic architecture of flowering-time variation in Brachypodium distachyon. Plant Physiol. 173, 269–279 (2017).

    Article  CAS  PubMed  Google Scholar 

  155. Tsuji, H. & Taoka, K. Florigen signaling. Enzymes 35, 113–144 (2014).

    Article  CAS  PubMed  Google Scholar 

  156. Shcherban, A. B. & Salina, E. A. Evolution of VRN-1 homoeologous loci in allopolyploids of Triticum and their diploid precursors. BMC Plant Biol. 17, 188 (2017).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  157. Weng, X. et al. Grain number, plant height, and heading date7 is a central regulator of growth, development, and stress response. Plant Physiol. 164, 735–747 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Nelson, M. N. et al. The loss of vernalization requirement in narrow-leafed lupin is associated with a deletion in the promoter and de-repressed expression of a Flowering Locus T (FT) homologue. New Phytol. 213, 220–232 (2017).

    Article  CAS  PubMed  Google Scholar 

  159. Ruelens, P. et al. FLOWERING LOCUS C in monocots and the tandem origin of angiosperm-specific MADS-box genes. Nat. Commun. 4, 2280 (2013).

    Article  PubMed  Google Scholar 

  160. Vogt, S. H. et al. The FLC-like gene BvFL1 is not a major regulator of vernalization response in biennial beets. Front. Plant Sci. 5, 146 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  161. Reeves, P. A. et al. Evolutionary conservation of the FLOWERING LOCUS C-mediated vernalization response: evidence from the sugar beet (Beta vulgaris). Genetics 176, 295–307 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  162. Pfeiffer, N. et al. Genetic analysis of bolting after winter in sugar beet (Beta vulgaris L.). Theor. Appl. Genet. 127, 2479–2489 (2014).

    Article  CAS  PubMed  Google Scholar 

  163. Hecht, V. et al. The pea GIGAS gene is a FLOWERING LOCUS T homolog necessary for graft-transmissible specification of flowering but not for responsiveness to photoperiod. Plant Cell 23, 147–161 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  164. Laurie, R. E. et al. The Medicago FLOWERING LOCUS T homolog, MtFTa1, is a key regulator of flowering time. Plant Physiol. 156, 2207–2224 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  165. Putterill, J. & Varkonyi-Gasic, E. FT and florigen long-distance flowering control in plants. Curr. Opin. Plant Biol. 33, 77–82 (2016).

    Article  CAS  PubMed  Google Scholar 

  166. Turck, F., Fornara, F. & Coupland, G. Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Annu. Rev. Plant Biol. 59, 573–594 (2008).

    Article  CAS  PubMed  Google Scholar 

  167. Oliva, M. et al. FIE, a nuclear PRC2 protein, forms cytoplasmic complexes in Arabidopsis thaliana. J. Exp. Bot. 67, 6111–6123 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  168. Spillane, C. et al. Interaction of the Arabidopsis polycomb group proteins FIE and MEA mediates their common phenotypes. Curr. Biol. 10, 1535–1538 (2000).

    Article  CAS  PubMed  Google Scholar 

  169. Derkacheva, M. et al. Arabidopsis MSI1 connects LHP1 to PRC2 complexes. EMBO J. 32, 2073–2085 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  170. Steinbach, Y. & Hennig, L. Arabidopsis MSI1 functions in photoperiodic flowering time control. Front. Plant Sci. 5, 77 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  171. Kim, S. Y., Zhu, T. & Sung, Z. R. Epigenetic regulation of gene programs by EMF1 and EMF2 in Arabidopsis. Plant Physiol. 152, 516–528 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  172. Luo, M. et al. Expression and parent-of-origin effects for FIS2, MEA, and FIE in the endosperm and embryo of developing Arabidopsis seeds. Proc. Natl Acad. Sci. USA 97, 10637–10642 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  173. Tang, X. et al. Synergistic repression of the embryonic programme by SET DOMAIN GROUP 8 and EMBRYONIC FLOWER 2 in Arabidopsis seedlings. J. Exp. Bot. 63, 1391–1404 (2012).

    Article  CAS  PubMed  Google Scholar 

  174. Spillane, C. et al. Positive darwinian selection at the imprinted MEDEA locus in plants. Nature 448, 349–352 (2007).

    Article  CAS  PubMed  Google Scholar 

  175. Xu, Y. et al. Regulation of vegetative phase change by SWI2/SNF2 chromatin remodeling ATPase BRAHMA. Plant Physiol. 172, 2416–2428 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  176. Yu, X. et al. Modulation of brassinosteroid-regulated gene expression by Jumonji domain-containing proteins ELF6 and REF6 in Arabidopsis. Proc. Natl Acad. Sci. USA 105, 7618–7623 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We gratefully acknowledge funding from NSFC for the basic science centre program (31788103) and the major state basic research program of China (973).

Author information

Authors and Affiliations

  1. Key Laboratory of Plant Molecular Physiology, Institute of Botany, Chinese Academy of Sciences, Beijing, China

    Shujuan Xu & Kang Chong

  2. University of Chinese Academy of Sciences, Beijing, China

    Shujuan Xu & Kang Chong

Authors
  1. Shujuan Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kang Chong
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

S. X. wrote a draft of this article. K. C. designed the outline of the manuscript and polished the article.

Corresponding author

Correspondence to Kang Chong.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xu, S., Chong, K. Remembering winter through vernalisation. Nature Plants 4, 997–1009 (2018). https://doi.org/10.1038/s41477-018-0301-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41477-018-0301-z

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing