Abstract
To ensure flowering in favourable conditions, many plants flower only after an extended period of cold, namely winter. In Arabidopsis, the acceleration of flowering by prolonged cold, a process called vernalization, involves downregulation of the protein FLC, which would otherwise prevent flowering1,2. This lowered FLC expression is maintained through subsequent development by the activity of VERNALIZATION (VRN) genes3,4. VRN1 encodes a DNA-binding protein4 whereas VRN2 encodes a homologue of one of the Polycomb group proteins, which maintain the silencing of genes during animal development3. Here we show that vernalization causes changes in histone methylation in discrete domains within the FLC locus, increasing dimethylation of lysines 9 and 27 on histone H3. Such modifications identify silenced chromatin states in Drosophila and human cells5,6,7. Dimethylation of H3 K27 was lost only in vrn2 mutants, but dimethylation of H3 K9 was absent from both vrn1 and vrn2, consistent with VRN1 functioning downstream of VRN2. The epigenetic memory of winter is thus mediated by a ‘histone code’ that specifies a silent chromatin state conserved between animals and plants.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Rent or buy this article
Prices vary by article type
from$1.95
to$39.95
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Sheldon, C. C. et al. The FLF MADS box gene: a repressor of flowering in Arabidopsis regulated by vernalization and methylation. Plant Cell 11, 445–458 (1999)
Michaels, S. D. & Amasino, R. M. FLOWERING LOCUSC encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11, 949–956 (1999)
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)
Levy, Y. Y., Mesnage, S., Mylne, J. S., Gendall, A. R. & Dean, C. Multiple roles of Arabidopsis VRN1 in vernalization and flowering time control. Science 297, 243–246 (2002)
Cao, R. et al. Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298, 1039–1043 (2002)
Müller, J. et al. Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell 111, 197–208 (2002)
Rea, S. et al. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406, 593–599 (2000)
Henderson, I., Shindo, C. & Dean, C. The need for winter in the switch to flowering. Annu. Rev. Genet. 37, 371–392 (2003)
Kobayashi, Y., Kaya, H., Goto, K., Iwabuchi, M. & Araki, T. A pair of related genes with antagonistic roles in mediating flowering signals. Science 286, 1960–1962 (1999)
Kardailsky, I. et al. Activation tagging of the floral inducer FT. Science 286, 1962–1965 (1999)
Samach, A. et al. Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288, 1613–1616 (2000)
Lee, H. et al. The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes Dev. 14, 2366–2376 (2000)
Hepworth, S. R., Valverde, F., Ravenscroft, D., Mouradov, A. & Coupland, G. Antagonistic regulation of flowering-time gene SOC1 by CONSTANS and FLC via separate promoter motifs. EMBO J. 21, 4327–4337 (2002)
Burn, J. E., Bagnall, D. J., Metzger, J. D., Dennis, E. S. & Peacock, W. J. DNA methylation, vernalization, and the initiation of flowering. Proc. Natl Acad. Sci. USA 90, 287–291 (1993)
Chandler, J., Wilson, A. & Dean, C. Arabidopsis mutants showing an altered response to vernalization. Plant J. 10, 637–644 (1996)
Birve, A. et al. Su(z)12, a novel Drosophila Polycomb group gene that is conserved in vertebrates and plants. Development 128, 3371–3379 (2001)
Fischle, W., Wang, Y. & Allis, C. Binary switches and modification cassettes in histone biology and beyond. Nature 425, 475–479 (2003)
Czermin, B. et al. Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell 111, 185–196 (2002)
Kuzmichev, A., Nishioka, K., Erdjument-Bromage, H., Tempst, P. & Reinberg, D. Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein. Genes Dev. 16, 2893–2905 (2002)
Bannister, A. J. et al. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410, 120–124 (2001)
Lachner, M., O'Carroll, D., Rea, S., Mechtler, K. & Jenuwein, T. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410, 116–120 (2001)
Jenuwein, T. & Allis, C. D. Translating the histone code. Science 293, 1074–1080 (2001)
Sims, R. J. III, Nishioka, K. & Reinberg, D. Histone lysine methylation: a signature for chromatin function. Trends Genet. 19, 629–639 (2003)
Gazzani, S., Gendall, A. R., Lister, C. & Dean, C. Analysis of the molecular basis of flowering time variation in Arabidopsis accessions. Plant Physiol. 132, 1107–1114 (2003)
Michaels, S. D., He, Y., Scortecci, K. C. & Amasino, R. M. Attenuation of FLOWERING LOCUS C activity as a mechanism for the evolution of a summer-annual flowering behavior in Arabidopsis. Proc. Natl Acad. Sci. USA 100, 10102–10107 (2003)
Gendrel, A.-V., Lippman, Z., Yordan, C., Colot, V. & Martienssen, R. A. Dependence of heterochromatic histone H3 methylation patterns on the Arabidopsis gene DDM1. Science 297, 1871–1873 (2002)
Sheldon, C. C., Conn, A. B., Dennis, E. S. & Peacock, W. J. Different regulatory regions are required for the vernalization-induced repression of FLOWERING LOCUS C and for the epigenetic maintenance of repression. Plant Cell 14, 2527–2537 (2002)
Rigaut, G. et al. A generic protein purification method for protein complex characterization and proteome exploration. Nature Biotechnol. 17, 1030–1032 (1999)
Goodrich, J. & Tweedie, S. Remembrance of things past: chromatin remodeling in plant development. Annu. Rev. Cell Dev. Biol. 18, 707–746 (2002)
Acknowledgements
The authors thank J. Goodrich for excellent comments on the manuscript and J. Finnegan and R. Amasino for allowing us to cite their work as personal communications. This work was supported by a Core Strategic Grant to the John Innes Centre from the Biotechnology and Biological Sciences Research Council and a European Union Framework V grant to C.D.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare that they have no competing financial interests.
Supplementary information
41586_2004_BFnature02269_MOESM1_ESM.jpg
Supplementary Figure 1: H3 dimethyl K4 and H3 dimethyl K9 histone modifications at FLC are associated with vernalization and are dependent on the VRN genes. (JPG 118 kb)
41586_2004_BFnature02269_MOESM2_ESM.jpg
Supplementary Figure 2: The H3 dimethyl K27 histone modification at FLC is associated with vernalization and is dependent on VRN2, but not VRN1. (JPG 114 kb)
41586_2004_BFnature02269_MOESM4_ESM.jpg
Supplementary Figure 4: PCR analysis to show the amplification efficiency of all primer pairs used in the chromatin immunoprecipitation analysis. (JPG 79 kb)
Rights and permissions
About this article
Cite this article
Bastow, R., Mylne, J., Lister, C. et al. Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427, 164–167 (2004). https://doi.org/10.1038/nature02269
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/nature02269
This article is cited by
-
Epigenetics: Toward improving crop disease resistance and agronomic characteristics
Plant Biotechnology Reports (2024)
-
Transcriptome analysis of critical genes related to flowering in Mikania micrantha at different altitudes provides insights for a potential control
BMC Genomics (2023)
-
HDF1, a novel flowering time regulator identified in a mutant suppressing sensitivity to red light reduced 1 early flowering
Scientific Reports (2023)
-
Epigenetic malleability at core promoter initiates tobacco PR-1a expression post salicylic acid treatment
Molecular Biology Reports (2023)
-
Epigenomics in stress tolerance of plants under the climate change
Molecular Biology Reports (2023)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.