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.

Epigenetic maintenance of the vernalized state in Arabidopsis thaliana requires LIKE HETEROCHROMATIN PROTEIN 1

Abstract

Vernalization is the process by which sensing a prolonged exposure to winter cold leads to competence to flower in the spring. In winter annual Arabidopsis thaliana accessions, flowering is suppressed in the fall by expression of the potent floral repressor FLOWERING LOCUS C (FLC)1. Vernalization promotes flowering via epigenetic repression of FLC2. Repression is accompanied by a series of histone modifications of FLC chromatin that include dimethylation of histone H3 at Lys9 (H3K9) and Lys27 (H3K27)3,4. Here, we report that A. thaliana LIKE HETEROCHROMATIN PROTEIN 1 (LHP1) is necessary to maintain the epigenetically repressed state of FLC upon return to warm conditions typical of spring. LHP1 is enriched at FLC chromatin after prolonged exposure to cold, and LHP1 activity is needed to maintain the increased levels of H3K9 dimethylation at FLC chromatin that are characteristic of the vernalized state.

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

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: The vernalization response is impaired in lhp1 mutants.
Figure 2: Role of LHP1 in FLC repression.
Figure 3: ChIP analyses of FLC chromatin.
Figure 4: A region in the first intron of FLC is essential for maintenance of the vernalized state.

References

  1. Michaels, S.D. & Amasino, R.M. Memories of winter: vernalization and the competence to flower. Plant Cell Environ. 23, 1145–1154 (2000).

    Article  Google Scholar 

  2. Sung, S. & Amasino, R.M. REMEMBERING WINTER: Toward a molecular understanding of vernalization. Annu. Rev. Plant Biol. 56, 491–508 (2005).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  5. 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  Google Scholar 

  6. 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).

    Article  CAS  Google Scholar 

  7. 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  Google Scholar 

  8. Ringrose, L. & Paro, R. Epigenetic regulation of cellular memory by the Polycomb and Trithorax group proteins. Annu. Rev. Genet. 38, 413–443 (2004).

    Article  CAS  Google Scholar 

  9. Schubert, D., Clarenz, O. & Goodrich, J. Epigenetic control of plant development by Polycomb-group proteins. Curr. Opin. Plant Biol. 8, 553–561 (2005).

    Article  CAS  Google Scholar 

  10. Gaudin, V. et al. Mutations in LIKE HETEROCHROMATIN PROTEIN 1 affect flowering time and plant architecture in Arabidopsis. Development 128, 4847–4858 (2001).

    CAS  PubMed  Google Scholar 

  11. Kotake, T., Takada, S., Nakahigashi, K., Ohto, M. & Goto, K. Arabidopsis TERMINAL FLOWER 2 gene encodes a heterochromatin protein 1 homolog and represses both FLOWERING LOCUS T to regulate flowering time and several floral homeotic genes. Plant Cell Physiol. 44, 555–564 (2003).

    Article  CAS  Google Scholar 

  12. Maison, C. & Almouzni, G. HP1 and the dynamics of heterochromatin maintenance. Nat. Rev. Mol. Cell Biol. 5, 296–304 (2004).

    Article  CAS  Google Scholar 

  13. Liu, L.P., Ni, J.Q., Shi, Y.D., Oakeley, E.J. & Sun, F.L. Sex-specific role of Drosophila melanogaster HP1 in regulating chromatin structure and gene transcription. Nat. Genet. 37, 1361–1366 (2005).

    Article  CAS  Google Scholar 

  14. Nielsen, S.J. et al. Rb targets histone H3 methylation and HP1 to promoters. Nature 412, 561–565 (2001).

    Article  CAS  Google Scholar 

  15. Nakahigashi, K., Jasencakova, Z., Schubert, I. & Goto, K. The Arabidopsis HETEROCHROMATIN PROTEIN1 homolog (TERMINAL FLOWER2) silences genes within euchromatic region but not genes positioned in heterochromatin. Plant Cel. Physiol. 46, 1747–1756 (2005).

    Article  CAS  Google Scholar 

  16. Libault, M. et al. The Arabidopsis LHP1 protein is a component of euchromatin. Planta 222, 910–925 (2005).

    Article  CAS  Google Scholar 

  17. Zemach, A. et al. Different domains control the localization and mobility of LIKE HETEROCHROMATIN PROTEIN1 in Arabidopsis nuclei. Plant Cell 18, 133–145 (2006).

    Article  CAS  Google Scholar 

  18. Lindroth, A.M. et al. Dual histone H3 methylation marks at lysines 9 and 27 required for interaction with CHROMOMETHYLASE3. EMBO J. 23, 4286–4296 (2004).

    Article  CAS  Google Scholar 

  19. Lee, I. & Amasino, R.M. Effect of vernalization, photoperiod, and light quality on the flowering phenotype of Arabidopsis plants containing the FRIGIDA gene. Plant Physiol. 108, 157–162 (1995).

    Article  CAS  Google Scholar 

  20. 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  Google Scholar 

  21. Valverde, F. et al. Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science 303, 1003–1006 (2004).

    Article  CAS  Google Scholar 

  22. Huang, T., Bohlenius, H., Eriksson, S., Parcy, F. & Nilsson, O. The mRNA of the Arabidopsis gene FT moves from leaf to shoot apex and induces flowering. Science 309, 1694–1696 (2005).

    Article  CAS  Google Scholar 

  23. 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).

    Article  CAS  Google Scholar 

  24. Baumbusch, L.O. et al. The Arabidopsis thaliana genome contains at least 29 active genes encoding SET domain proteins that can be assigned to four evolutionarily conserved classes. Nucleic Acids Res. 29, 4319–4333 (2001).

    Article  CAS  Google Scholar 

  25. Dejardin, J. et al. Recruitment of Drosophila Polycomb group proteins to chromatin by DSP1. Nature 434, 533–538 (2005).

    Article  CAS  Google Scholar 

  26. He, Y., Doyle, M.R. & Amasino, R.M. PAF1-complex-mediated histone methylation of FLOWERING LOCUS C chromatin is required for the vernalization-responsive, winter-annual habit in Arabidopsis. Genes Dev. 18, 2774–2784 (2004).

    Article  CAS  Google Scholar 

  27. Krogan, N.J. et al. The Paf1 complex is required for histone H3 methylation by COMPASS and Dot1p: linking transcriptional elongation to histone methylation. Mol. Cell 11, 721–729 (2003).

    Article  CAS  Google Scholar 

  28. Kim, S.Y. et al. Establishment of the vernalization-responsive, winter-annual habit in Arabidopsis requires a putative histone H3 methyl transferase. Plant Cell 17, 3301–3310 (2005).

    Article  CAS  Google Scholar 

  29. Jenuwein, T. & Allis, C.D. Translating the histone code. Science 293, 1074–1080 (2001).

    Article  CAS  Google Scholar 

  30. Johnson, L., Cao, X. & Jacobsen, S. Interplay between two epigenetic marks. DNA methylation and histone H3 lysine 9 methylation. Curr. Biol. 12, 1360–1367 (2002).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to S. Woody, R. Schmitz and R. Rodman for their comments on the manuscript. Research in the laboratory of R.M.A. was supported by the College of Agricultural and Life Sciences of the University of Wisconsin and by grants from the US Department of Agriculture National Research Initiative Competitive Grants Program and the National Science Foundation. Research in the laboratory of S.E.J. was supported by US National Institute of Health grant GM060398.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Richard M Amasino.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

LHP1 localization. (PDF 257 kb)

Supplementary Table 1

Primers used for ChIP and RT-PCR. (PDF 38 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Sung, S., He, Y., Eshoo, T. et al. Epigenetic maintenance of the vernalized state in Arabidopsis thaliana requires LIKE HETEROCHROMATIN PROTEIN 1. Nat Genet 38, 706–710 (2006). https://doi.org/10.1038/ng1795

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ng1795

This article is cited by

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