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PMID: 19416817 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Vernalization-induced flowering in cereals is associated with changes in histone methylation at the VERNALIZATION1 gene.

Oliver SN, Finnegan EJ, Dennis ES, Peacock WJ, Trevaskis B

Abstract

Prolonged exposure to low temperatures (vernalization) accelerates the transition to reproductive growth in many plant species, including the model plant Arabidopsis thaliana and the economically important cereal crops, wheat and barley. Vernalization-induced flowering is an epigenetic phenomenon. In Arabidopsis, stable down-regulation of FLOWERING LOCUS C (FLC) by vernalization is associated with changes in histone modifications at FLC chromatin. In cereals, the vernalization response is mediated by stable induction of the floral promoter VERNALIZATION1 (VRN1), which initiates reproductive development at the shoot apex. We show that in barley (Hordeum vulgare), repression of HvVRN1 before vernalization is associated with high levels of histone 3 lysine 27 trimethylation (H3K27me3) at HvVRN1 chromatin. Vernalization caused increased levels of histone 3 lysine 4 trimethylation (H3K4me3) and a loss of H3K27me3 at HvVRN1, suggesting that vernalization promotes an active chromatin state at VRN1. Levels of these histone modifications at 2 other flowering-time genes, VERNALIZATION2 and FLOWERING LOCUS T, were not altered by vernalization. Our study suggests that maintenance of an active chromatin state at VRN1 is likely to be the basis for epigenetic memory of vernalization in cereals. Thus, regulation of chromatin state is a feature of epigenetic memory of vernalization in Arabidopsis and the cereals; however, whereas vernalization-induced flowering in Arabidopsis is mediated by epigenetic regulation of the floral repressor FLC, this phenomenon in cereals is mediated by epigenetic regulation of the floral activator, VRN1.

MeSH Terms
Arabidopsis Proteins/genetics DNA-Binding Proteins/genetics Edible Grain/genetics,physiology Epigenesis, Genetic Flowers/growth & development Gene Expression Regulation, Plant Histones/metabolism Methylation Plant Physiological Phenomena Repressor Proteins/genetics
Chemicals
Arabidopsis Proteins DNA-Binding Proteins Histones Repressor Proteins VRN1 protein, Arabidopsis
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Oliver Sandra N
CSIRO Plant Industry, Canberra ACT 2601, Australia.
Finnegan E Jean
Dennis Elizabeth S
Peacock W James
Trevaskis Ben
References (49)
49 references, click to expand
  1. Vernalization-induced trimethylation of histone H3 lysine 27 at FLC is not maintained in mitotically quiescent cells.
    Curr Biol. 2007 Nov 20;17(22):1978-83 PMID: 17980595
  2. HvVRN2 responds to daylength, whereas HvVRN1 is regulated by vernalization and developmental status.
    Plant Physiol. 2006 Apr;140(4):1397-405 PMID: 16500994
  3. Large deletions within the first intron in VRN-1 are associated with spring growth habit in barley and wheat.
    Mol Genet Genomics. 2005 Mar;273(1):54-65 PMID: 15690172
  4. The molecular basis of vernalization-induced flowering in cereals.
    Trends Plant Sci. 2007 Aug;12(8):352-7 PMID: 17629542
  5. Low-temperature and daylength cues are integrated to regulate FLOWERING LOCUS T in barley.
    Plant Physiol. 2008 May;147(1):355-66 PMID: 18359843
  6. The Arabidopsis thaliana vernalization response requires a polycomb-like protein complex that also includes VERNALIZATION INSENSITIVE 3.
    Proc Natl Acad Sci U S A. 2006 Sep 26;103(39):14631-6 PMID: 16983073
  7. Genome regulation by polycomb and trithorax proteins.
    Cell. 2007 Feb 23;128(4):735-45 PMID: 17320510
  8. The VERNALIZATION 2 gene mediates the epigenetic regulation of vernalization in Arabidopsis.
    Cell. 2001 Nov 16;107(4):525-35 PMID: 11719192
  9. Reconstructing the evolutionary history of paralogous APETALA1/FRUITFULL-like genes in grasses (Poaceae).
    Genetics. 2006 Sep;174(1):421-37 PMID: 16816429
  10. Repression of FLOWERING LOCUS C and FLOWERING LOCUS T by the Arabidopsis Polycomb repressive complex 2 components.
    PLoS One. 2008;3(10):e3404 PMID: 18852898
  11. The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis.
    Genes Dev. 2006 Apr 1;20(7):898-912 PMID: 16600915
  12. The Arabidopsis FLC protein interacts directly in vivo with SOC1 and FT chromatin and is part of a high-molecular-weight protein complex.
    Plant J. 2006 Apr;46(2):183-92 PMID: 16623882
  13. FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering.
    Plant Cell. 1999 May;11(5):949-56 PMID: 10330478
  14. Profiling histone modification patterns in plants using genomic tiling microarrays.
    Nat Methods. 2005 Mar;2(3):213-8 PMID: 16163802
  15. The molecular basis of vernalization: the central role of FLOWERING LOCUS C (FLC).
    Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3753-8 PMID: 10716723
  16. Polycomb-group proteins repress the floral activator AGL19 in the FLC-independent vernalization pathway.
    Genes Dev. 2006 Jun 15;20(12):1667-78 PMID: 16778081
  17. Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis.
    PLoS Biol. 2007 May;5(5):e129 PMID: 17439305
  18. Different regulatory regions are required for the vernalization-induced repression of FLOWERING LOCUS C and for the epigenetic maintenance of repression.
    Plant Cell. 2002 Oct;14(10):2527-37 PMID: 12368502
  19. Histone arginine methylation is required for vernalization-induced epigenetic silencing of FLC in winter-annual Arabidopsis thaliana.
    Proc Natl Acad Sci U S A. 2008 Jan 15;105(2):411-6 PMID: 18178621
  20. TaVRT-1, a putative transcription factor associated with vegetative to reproductive transition in cereals.
    Plant Physiol. 2003 Aug;132(4):1849-60 PMID: 12913142
  21. The downregulation of FLOWERING LOCUS C (FLC) expression in plants with low levels of DNA methylation and by vernalization occurs by distinct mechanisms.
    Plant J. 2005 Nov;44(3):420-32 PMID: 16236152
  22. The PHD finger protein VRN5 functions in the epigenetic silencing of Arabidopsis FLC.
    Curr Biol. 2007 Jan 9;17(1):73-8 PMID: 17174094
  23. A PHD-polycomb repressive complex 2 triggers the epigenetic silencing of FLC during vernalization.
    Proc Natl Acad Sci U S A. 2008 Nov 4;105(44):16831-6 PMID: 18854416
  24. Positional cloning of the wheat vernalization gene VRN1.
    Proc Natl Acad Sci U S A. 2003 May 13;100(10):6263-8 PMID: 12730378
  25. Wheat VIN3-like PHD finger genes are up-regulated by vernalization.
    Mol Genet Genomics. 2007 Mar;277(3):301-13 PMID: 17123111
  26. WAP1, a wheat APETALA1 homolog, plays a central role in the phase transition from vegetative to reproductive growth.
    Plant Cell Physiol. 2003 Dec;44(12):1255-65 PMID: 14701921
  27. High-resolution profiling of histone methylations in the human genome.
    Cell. 2007 May 18;129(4):823-37 PMID: 17512414
  28. MADS box genes control vernalization-induced flowering in cereals.
    Proc Natl Acad Sci U S A. 2003 Oct 28;100(22):13099-104 PMID: 14557548
  29. Comparative analysis of SET domain proteins in maize and Arabidopsis reveals multiple duplications preceding the divergence of monocots and dicots.
    Plant Physiol. 2003 Jun;132(2):907-25 PMID: 12805620
  30. The wheat VRN2 gene is a flowering repressor down-regulated by vernalization.
    Science. 2004 Mar 12;303(5664):1640-4 PMID: 15016992
  31. Molecular and structural characterization of barley vernalization genes.
    Plant Mol Biol. 2005 Oct;59(3):449-67 PMID: 16235110
  32. A high-resolution map of active promoters in the human genome.
    Nature. 2005 Aug 11;436(7052):876-80 PMID: 15988478
  33. Vernalization requires epigenetic silencing of FLC by histone methylation.
    Nature. 2004 Jan 8;427(6970):164-7 PMID: 14712277
  34. Mammalian Trithorax and polycomb-group homologues are antagonistic regulators of homeotic development.
    Proc Natl Acad Sci U S A. 1999 Dec 7;96(25):14372-7 PMID: 10588712
  35. Validation of the VRN-H2/VRN-H1 epistatic model in barley reveals that intron length variation in VRN-H1 may account for a continuum of vernalization sensitivity.
    Mol Genet Genomics. 2007 Mar;277(3):249-61 PMID: 17151889
  36. Haplotype analysis of vernalization loci in European barley germplasm reveals novel VRN-H1 alleles and a predominant winter VRN-H1/VRN-H2 multi-locus haplotype.
    Theor Appl Genet. 2007 Nov;115(7):993-1001 PMID: 17713756
  37. The einkorn wheat (Triticum monococcum) mutant, maintained vegetative phase, is caused by a deletion in the VRN1 gene.
    Genes Genet Syst. 2007 Apr;82(2):167-70 PMID: 17507783
  38. The Arabidopsis homologs of trithorax (ATX1) and enhancer of zeste (CLF) establish 'bivalent chromatin marks' at the silent AGAMOUS locus.
    Nucleic Acids Res. 2007;35(18):6290-6 PMID: 17881378
  39. The genomic landscape of histone modifications in human T cells.
    Proc Natl Acad Sci U S A. 2006 Oct 24;103(43):15782-7 PMID: 17043231
  40. Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3.
    Nature. 2004 Jan 8;427(6970):159-64 PMID: 14712276
  41. Resetting of FLOWERING LOCUS C expression after epigenetic repression by vernalization.
    Proc Natl Acad Sci U S A. 2008 Feb 12;105(6):2214-9 PMID: 18250331
  42. The wheat and barley vernalization gene VRN3 is an orthologue of FT.
    Proc Natl Acad Sci U S A. 2006 Dec 19;103(51):19581-6 PMID: 17158798
  43. The influence of vernalization and daylength on expression of flowering-time genes in the shoot apex and leaves of barley (Hordeum vulgare).
    J Exp Bot. 2009;60(7):2169-78 PMID: 19357429
  44. Remembering winter: toward a molecular understanding of vernalization.
    Annu Rev Plant Biol. 2005;56:491-508 PMID: 15862105
  45. Interplay between two epigenetic marks. DNA methylation and histone H3 lysine 9 methylation.
    Curr Biol. 2002 Aug 20;12(16):1360-7 PMID: 12194816
  46. ARABIDOPSIS TRITHORAX1 dynamically regulates FLOWERING LOCUS C activation via histone 3 lysine 4 trimethylation.
    Plant Cell. 2008 Mar;20(3):580-8 PMID: 18375656
  47. Cloning, mapping and expression analysis of barley MADS-box genes.
    Plant Mol Biol. 2000 Apr;42(6):899-913 PMID: 10890536
  48. Epigenetic maintenance of the vernalized state in Arabidopsis thaliana requires LIKE HETEROCHROMATIN PROTEIN 1.
    Nat Genet. 2006 Jun;38(6):706-10 PMID: 16682972
  49. A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling.
    Nature. 2006 Jul 6;442(7098):86-90 PMID: 16728976
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2009-05-19
Epub
2009-00-04
Pages
8386-91
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC2677093
Subset
IM
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