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.

  • Letter
  • Published:

Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3

Nature volume 427, pages 159–164 (2004)Cite this article

Abstract

In biennials and winter annuals, flowering is typically blocked in the first growing season. Exposure to the prolonged cold of winter, through a process called vernalization, is required to alleviate this block and permit flowering in the second growing season1. In winter-annual types of Arabidopsis thaliana, a flowering repressor, FLOWERING LOCUS C (FLC), is expressed at levels that inhibit flowering in the first growing season2. Vernalization promotes flowering by causing a repression of FLC that is mitotically stable after return to warm growing conditions2. Here we identify a gene with a function in the measurement of the duration of cold exposure and in the establishment of the vernalized state. We show that this silencing involves changes in the modification of histones in FLC chromatin.

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

Figure 1: Characterization of vernalization-insensitive 3 mutants.
Figure 2: VIN3 cloning and expression pattern.
Figure 3: ChIP assays in wild-type winter-annual Arabidopsis.
Figure 4: Chromatin immunoprecipitation (ChIP) assays in vernalization mutants.

Similar content being viewed by others

References

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  3. Lee, I., Michaels, S. D., Masshardt, A. S. & Amasino, R. M. The late-flowering phenotype of FRIGIDA and LUMINIDEPENDENS is suppressed in the Landsberg erecta strain of Arabidopsis. Plant J. 6, 903–909 (1994)

    Article  CAS  Google Scholar 

  4. Michaels, S. & Amasino, R. 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 

  5. 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 

  6. Sheldon, C. C., Rouse, D. T., Finnegan, E. J., Peacock, W. J. & Dennis, E. S. The molecular basis of vernalization: the central role of FLOWERING LOCUS C (FLC). Proc. Natl Acad. Sci. USA 97, 3753–3758 (2000)

    Article  ADS  CAS  Google Scholar 

  7. Michaels, S. D. & Amasino, R. M. Loss of FLOWERING LOCUS C activity eliminates the late-flowering phenotype of FRIGIDA and autonomous pathway mutations but not responsiveness to vernalization. Plant Cell 13, 935–942 (2001)

    Article  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  9. 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)

    Article  CAS  Google Scholar 

  10. Michaels, S. D., He, Y., Scortecci, K. C. & Amasino, R. M. Attenuation of FLOWERING LOCUS C activity as a mechanism for the evolution of summer-annual flowering behavior in Arabidopsis. Proc. Natl Acad. Sci. USA 100, 10102–10107 (2003)

    Article  ADS  CAS  Google Scholar 

  11. 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 

  12. 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)

    Article  ADS  CAS  Google Scholar 

  13. Simpson, G. G. & Dean, C. Arabidopsis, the Rosetta stone of flowering time? Science 296, 285–289 (2002)

    Article  ADS  CAS  Google Scholar 

  14. Fair, K. et al. Protein interactions of the MLL PHD fingers modulate MLL target gene regulation in human cells. Mol. Cell. Biol. 21, 3589–3597 (2001)

    Article  CAS  Google Scholar 

  15. Main, A. L., Harvey, T. S., Baron, M., Boyd, J. & Campbell, I. D. The three-dimensional structure of the tenth type III module of fibronectin: an insight into RGD-mediated interactions. Cell 71, 671–678 (1992)

    Article  CAS  Google Scholar 

  16. Wellensiek, S. J. Dividing cells as the locus for vernalization. Nature 195, 307–308 (1962)

    Article  ADS  Google Scholar 

  17. 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)

    Article  ADS  CAS  Google Scholar 

  18. Kuzmichev, A. R. D., 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)

    Article  CAS  Google Scholar 

  19. Richards, E. J. & Elgin, S. C. Epigenetic codes for heterochromatin formation and silencing: rounding up the usual suspects. Cell 108, 489–500 (2002)

    Article  CAS  Google Scholar 

  20. Kehle, J. et al. dMi-2, a hunchback-interacting protein that functions in polycomb repression. Science 282, 1897–1900 (1998)

    Article  ADS  CAS  Google Scholar 

  21. 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 

  22. Lang, A. & Melchers, G. Vernalisation und Devernalisation bei einer zweijahrigen Pflanze. Z. Naturforsch 2b, 444–449 (1947)

    Article  Google Scholar 

  23. Lang, A. in Encyclopedia of Plant Physiology Vol. 15 Part 1 (ed. Ruhland, W.) 1371–1536 (Springer, Berlin, 1965)

    Google Scholar 

  24. Reyes, J. C., Hennig, L. & Gruissem, W. Chromatin-remodeling and memory factors. New regulators of plant development. Plant Physiol. 130, 1090–1101 (2002)

    Article  CAS  Google Scholar 

  25. Thomashow, M. F. So what's new in the field of plant cold acclimation? Lots! Plant Physiol. 125, 89–93 (2001)

    Article  CAS  Google Scholar 

  26. Gozani, O. et al. The PHD finger of the chromatin-associated protein ING2 functions as a nuclear phosphoinositide receptor. Cell 114, 99–111 (2003)

    Article  CAS  Google Scholar 

  27. Weigel, D. et al. Activation tagging in Arabidopsis. Plant Physiol. 122, 1003–1013 (2000)

    Article  CAS  Google Scholar 

  28. Michaels, S. D. & Amasino, R. M. The gibberellic acid biosynthesis mutant ga1-3 of Arabidopsis thaliana is responsive to vernalization. Dev. Genet. 25, 194–198 (1999)

    Article  CAS  Google Scholar 

  29. Michaels, S. D. et al. AGL24 acts as a promoter of flowering in Arabidopsis and is positively regulated by vernalization. Plant J. 33, 867–874 (2003)

    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 thank S. Michaels for creating and helping to screen the mutant populations that provided the vin3 mutant, for the FLC–GUS construct, and for advice and insight; and M. Doyle for help in the preparation of the manuscript. R.M.A. thanks C. O. Miller and J. A. D. Zeevaart for encouragement and mentoring in flowering-time regulation. This work was supported by the College of Agricultural and Life Sciences and the Graduate School of the University of Wisconsin, by the United States Department of Agriculture National Research Initiative Competitive Grants Program, and by a grant to R.M.A. from the National Science Foundation. The creation of insertion mutant lines was supported by a National Science Foundation grant.

Author information

Authors and Affiliations

  1. Department of Biochemistry, University of Wisconsin–Madison, 433 Babcock Drive, Madison, Wisconsin, 53706, USA

    Sibum Sung & Richard M. Amasino

Authors
  1. Sibum Sung
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Richard M. Amasino
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Richard M. Amasino.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sung, S., Amasino, R. Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427, 159–164 (2004). https://doi.org/10.1038/nature02195

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature02195

This article is cited by

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.

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