Vernalization and epigenetics: How plants remember winter

Current Opinion in Plant Biology

Volumn 7, Issue 1, 2004, Pages 4-10

  Sung, Sibum ^a   Amasino, Richard M ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; EMBRYOPHYTA;

EID: 1642485676     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2003.11.010     Document Type: Review

References (36)

1. Chouard P. Vernalization and its relations to dormancy. Annu Rev Plant Physiol. 11:1960;191-238.
2. Lang A: Physiology of flower initiation. In Encyclopedia of Plant Physiology, vol 15. Edited by Ruhland W. Berlin: Springer-Verlag; 1965:1371-1536.
3. Wellensiek S.J. Dividing cells as the locus for vernalization. Nature. 195:1962;307-308.
4. Wellensiek S.J. Dividing cells as the prerequisite for vernalization. Plant Physiol. 39:2001;832-835.
5. 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. 90:1993;287-291.
6. Napp-Zinn K: On the genetical basis of vernalization requirement in Arabidopsis thaliana (L.) Heynh. In La Physiologie de la Floraison. Edited by Champagnat P, Jaques R. Paris: Coll. Int. CNRS; 1979:217-220.
7. Lee I., Bleecker A., Amasino R. Analysis of naturally occurring late flowering in Arabidopsis thaliana. Mol Gen Genet. 237:1993;171-176.
8. Clarke J.H., Dean C. Mapping FRI, a locus controlling flowering time and vernalization response in Arabidopsis thaliana. Mol Gen Genet. 242:1994;81-89.
9. 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. 6:1994;903-909.
10. Koornneef M., Blankestijn-de Vries H., Hanhart C., Soppe W., Peeters T. 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 J. 6:1994;911-919.
11. Michaels S.D., Amasino R.M. FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell. 11:1999;949-956.
12. Sheldon C.C., Burn J.E., Perez P.P., Metzger J., Edwards J.A., Peacock W.J., Dennis E.S. The FLF MADS box gene. A repressor of flowering in Arabidopsis regulated by vernalization and methylation. Plant Cell. 11:1999;445-458.
13. Michaels S.D., Amasino R.M. Memories of winter: vernalization and the competence to flower. Plant Cell Environ. 23:2000;1145-1154.
14. 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. 13:2001;935-942.
15. Johanson U., West J., Lister C., Michaels S., Amasino R., Dean C. Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science. 290:2000;344-347.
16. Gazzani S., Gendall A.R., Lister C., Dean C. Analysis of the molecular basis of flowering time variation in Arabidopsis accessions. Plant Physiol. 132:2003;1107-1114 The authors describe the analysis of additional summer-annual accessions of Arabidopsis. In addition, they identify additional types of lesions in FRI that have led to the conversion of winter-annual to summer-annual types. They also note that some summer-annual accessions have FRI coupled to weak alleles of FLC.
17. 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. 100:2003;10102-10107 This paper provides direct evidence that an insertion in the FLC first intron results in a weak allele that is not as strongly upregulated by FRI. Weak alleles of FLC in other Arabidopsis accessions do not have the same lesion, suggesting that the attenuation of FLC activity to produce a summer-annual habit from a winter-annual type occurred independently at least twice.
18. Thomashow M.F. So what's new in the field of plant cold acclimation? Lots! Plant Physiol. 125:2001;89-93.
19. Thomashow M.F. Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol. 50:1999;571-599.
20. 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. 108:1995;157-162.
21. Liu J., Gilmour S.J., Thomashow M.F., van Nocker S. Cold signalling associated with vernalization in Arabidopsis thaliana does not involve CBF1 or abscisic acid. Physiol Plant. 114:2002;125-134.
22. Lee H., Xiong L., Gong Z., Ishitani M., Stevenson B., Zhu J.K. The Arabidopsis HOS1 gene negatively regulates cold signal transduction and encodes a RING finger protein that displays cold-regulated nucleo cytoplasmic partitioning. Genes Dev. 15:2001;912-924.
23. Sangwan V., Orvar B.L., Beyerly J., Hirt H., Dhindsa R.S. Opposite changes in membrane fluidity mimic cold and heat stress activation of distinct plant MAP kinase pathways. Plant J. 31:2002;629-638.
24. Orvar B.L., Sangwan V., Omann F., Dhindsa R.S. Early steps in cold sensing by plant cells: the role of actin cytoskeleton and membrane fluidity. Plant J. 23:2000;785-794.
25. Turner B.M. Cellular memory and the histone code. Cell. 111:2002;285-291 This paper and [26,27] are excellent recent reviews of how histone modification leads to new epigenetic states of gene expression and cellular memory.
26. Richards E.J., Elgin S.C. Epigenetic codes for heterochromatin formation and silencing: rounding up the usual suspects. Cell. 108:2002;489-500.
27. Grewal S.I.S., Moazed D. Heterochromatin and epigenetic control of gene expression. Science. 301:2003;798-801.
28. Gendall A.R., Levy Y.Y., Wilson A., Dean C. The VERNALIZATION 2 gene mediates the epigenetic regulation of vernalization in Arabidopsis. Cell. 107:2001;525-535.
29. 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. 297:2002;243-246 The authors identify another gene, VRN1, that is required to maintain the repressed state of FLC after vernalization. VRN1 encodes a Myb-related transcription factor.
30. Sung S, Amasino R. Vernalization in Arabidopsis thaliana is mediated by the PHD-finger protein VIN3. Nature 2003, in press.
31. Aasland R., Gibson T.J., Stewart A.F. The PHD finger: implications for chromatin-mediated transcription regulation. Trends Biochem Sci. 20:1995;56-59.
32. Kuzmichev A., Reinberg 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. 16:2002;2893-2905 The human homolog of Su(z)12 is identified as PRC2. This protein has methylating activity towards lysine residues 9 and 27 of histone H3. PRC2 co-purifies with histone deacetylases (HDACs), suggesting that HDAC activity may be required for PRC2-mediated epigenetic repression.
33. Reyes J.C., Hennig L., Gruissem W. Chromatin-remodeling and memory factors. New regulators of plant development. Plant Physiol. 130:2002;1090-1101.
34. Schultz D.C., Ayyanathan K., Negorev D., Maul G.G., Rauscher F.J. III SETDB1: a novel KAP-1-associated histone H3, lysine 9-specific methyltransferase that contributes to HP1-mediated silencing of euchromatin genes by KRAB zinc-finger proteins. Genes Dev. 16:2002;919-932 Lysine 9 methylation of histone H3 is necessary for HP1 to bind to target genes and to form localized heterochromatin in euchromatic regions.
35. 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. 44:2003;555-564 This authors report that the TERMINAL FLOWER 2 (TFL2) gene, which is involved the floral transition in Arabidopsis, encodes a HP1 homolog. The authors suggest that TFL2 in plants, in contrast to HP1 homologs in other organisms, may play a role in the repression of genes in euchromatin. TFL2 delays flowering by repressing the expression of FLOWERING LOCUS T (FLT) and several floral homeotic genes that are downstream of FLT.
36. Yan L., Loukoianov A., Tranquilli G., Helguera M., Fahima T., Dubcovsky J. Positional cloning of the wheat vernalization gene VRN1. Proc Natl Acad Sci USA. 100:2003;6263-6268 The authors of this paper report the identification of the VRN1 gene of wheat, which confers a requirement for vernalization. (The wheat VRN1 has no molecular relatedness to the Arabidopsis VRN1 or to FRI and FLC.) Natural variation exists in both VRN1 in wheat and FRI and FLC in Arabidopsis, and this variation accounts for the difference between vernalization-requiring and summer-annual types. Thus different types of genes account for natural variation in the vernalization-requirement in wheat and Arabidopsis.