Abstract
The transition to flowering in winter wheat requires prolonged exposure to low temperature, a process called vernalization. This process is regulated by a genetic pathway that involves at least three genes, Triticum aestivum VERNALIZATION 1 (TaVRN1), Triticum aestivum VERNALIZATION 2 (TaVRN2) and Triticum aestivum FLOWERING LOCUS T-like 1 (TaFT1). These genes regulate flowering by integrating environmental and developmental cues. To determine whether the expression of these genes is associated with the chromatin methylation state during vernalization in wheat, the level of two markers of histone modifications, the activator histone H3 trimethylation of lysine 4 (H3K4me3) and the repressor histone H3 trimethylation of lysine 27 (H3K27me3) were measured at the promoter regions of these three genes. Bioinformatics analysis of these promoters demonstrates the presence of conserved cis-acting elements in the promoters of the three vernalization genes, TaVRN1, TaVRN2 and TaFT1. These elements are targeted by common transcription factors in the vernalization responsive cereals. These promoters also contain the functional “units” PRE/TRE targeted by Polycomb and Trithorax proteins that maintain repressed or active transcription states of developmentally regulated genes. These proteins are known to be associated with the regulation of H3K4me3 and H3K27me3. Expression studies indicate that TaVRN1 and TaFT1 are up-regulated by vernalization in winter wheat. This up-regulation is associated with increased level of the activator H3K4me3 with no change in the level of the repressor H3K27me3 at the promoter region. This study shows that the flowering transition induced by vernalization in winter wheat is associated with histone methylation at the promoter level of TaVRN1 and TaFT1 while the role of these markers is less evident in TaVRN2 repression. This may represent part of the cellular memory of vernalization in wheat.
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References
Alonso-Peral M, Oliver S, Casao M, Greenup A, Trevaskis B (2011) The promoter of the cereal VERNALIZATION1 gene is sufficient for transcriptional induction by prolonged cold. PLoS One 6:e29456
Barski A, Cuddapah S, Cui K, Roh T, Schones D, Wang Z, Wei G, Chepelev I, Zhao K (2007) High-resolution profiling of histone methylations in the human genome. Cell 129:823–837
Bastow R, Mylne J, Lister C, Lippman Z, Martienssen R, Dean C (2004) Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427:164–167
Beales J, Turner A, Griffiths S, Snape J, Laurie D (2007) A pseudo-response regulator is misexpressed in the photoperiod insensitive Ppd-D1a mutant of wheat (Triticum aestivum L.). Theor Appl Genet 115:721–733
Bernstein B, Kamal M, Toh L, Bekiranov S, Bailey D, Huebert D, McMahon S, Karlsson E, Kulbokas E, Gingeras T, Schreiber S, Lander E (2005) Genomic maps and comparative analysis of histone modifications in human and mouse. Cell 120:169–181
Bernstein B, Mikkelsen T, Xie X, Kamal M, Huebert D, Cuff J, Fry B, Meissner A, Wernig M, Plath K (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125:315–326
Bhaumik S, Smith E, Shilatifard A (2007) Covalent modifications of histones during development and disease pathogenesis. Nat Struct Mol Biol 14:1008–1016
Brudno M, Malde S, Poliakov A, Do C, Couronne O, Dubchak I, Batzoglou S (2003) Glocal alignment: finding rearrangements during alignment. Bioinformatics 19:i54–i62
Chinwalla V, Jane E, Harte P (1995) The Drosophila trithorax protein binds to specific chromosomal sites and is co-localized with Polycomb at many sites. EMBO J 14:2056–2065
Danyluk J, Kane N, Breton G, Limin A, Fowler D, Sarhan F (2003) TaVRT-1, a putative transcription factor associated with vegetative to reproductive transition in cereals. Plant Physiol 132(4):1849–1860
Diallo A, Kane N, Agharbaoui Z, Badawi M, Sarhan F (2010) Heterologous expression of Wheat VERNALIZATION 2 (TaVRN2) gene in Arabidopsis delays flowering and enhances freezing tolerance. PLoS One 5:e8690
Finnegan E, Dennis E (2007) Vernalization-induced trimethylation of histone H3 lysine 27 at FLC is not maintained in mitotically quiescent cells. Curr Biol 17:1978–1983
Fowler D, Limin A, Wang S, Ward R (1996) Relationship between low-temperature tolerance and vernalization response in wheat and rye. Can J Plant Sci 76:37–42
Frazer K, Pachter L, Poliakov A, Rubin E, Dubchak I (2004) VISTA: computational tools for comparative genomics. Nucleic Acids Res 32(Web Server issue W273–W279):W273–W279
Fu D, Dunbar M, Dubcovsky J (2007) Wheat VIN3-like PHD finger genes are up-regulated by vernalization. Mol Genet Genomics 277(3):301–313
Golovnina K, Kondratenko E, Blinov A, Goncharov N (2010) Molecular characterization of vernalization loci VRN1 in wild and cultivated wheats. BMC Plant Biol 2010:10. doi:10.1186/1471-2229-10-168):168
Hanson R, Hess J, Yu B, Ernst P, Lohuizen M, Berns A, van der Lugt N, Shashikant C, Ruddle F, Seto M, Korsmeyer S (1999) Mammalian Trithorax and Polycomb-group homologues are antagonistic regulators of homeotic development. Proc Natl Acad Sci USA 96:14372–14377
Helliwell C, Wood C, Robertson M, Peacock W, Dennis E (2006) 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 46:183–192
Hemming M, Peacock W, Dennis E, Trevaskis B (2008) Low-temperature and daylength cues are integrated to regulate FLOWERING LOCUS T in barley. Plant Physiol 147:355–366
Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Res 27:297–300
Johnson L, Mollah S, Garcia B, Muratore T, Shabanowitz J, Hunt D, Jacobsen S (2004) Mass spectrometry analysis of Arabidopsis histone H3 reveals distinct combinations of post-translational modifications. Nucleic Acids Res 32:6511–6518
Jones R, Gelbart W (1993) The Drosophila Polycomb-group gene enhancer of zeste contains a region with sequence similarity to trithorax. Mol Cell Biol 13:6357–6366
Kane N, Danyluk J, Tardif G, Ouellet F, Laliberte J, Limin A, Fowler D, Sarhan F (2005) TaVRT-2, a member of the StMADS-11 clade of flowering repressors, is regulated by vernalization and photoperiod in wheat. Plant Physiol 138(4):2354–2363
Kane N, Agharbaoui Z, Diallo A, Adam H, Tominaga Y, Ouellet F, Sarhan F (2007) TaVRT2 represses transcription of the wheat vernalization gene TaVRN1. Plant J 51(4):670–680
Kardailsky I, Shukla V, Ahn H, Dagenais N, Christensen S, Nguyen J, Chory J, Harrison M, Weigel D (1999) Activation tagging of the floral inducer FT. Science 286:1962–1965
Kohler C, Villar C (2008) Programming of gene expression by Polycomb group proteins. Trends Cell Biol 18:236–243
Kouzarides T (2007) Chromatin modifications and their function. Cell 128:693–705
Kroslak T, Koch T, Kahl E, Ho V (2001) Human phosphatidylethanolamine-binding protein facilitates heterotrimeric G protein-dependent signaling. J Biol Chem 276:39772–39778
Larkin M, Blackshields G, Brown N, Chenna R, McGettigan P, McWilliam H, Valentin F, Wallace I, Wilm A, Lopez R, Thompson J, Gibson T, Higgins D (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23(21):2947–2948
Lescot M, Dehais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouze P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327
Luger K, Mader A, Richmond R, Sargent D, Richmond T (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389:251–260
Mantovani R (1999) The molecular biology of the CCAAT-binding factor NF-Y. Gene 239:15–27
Murai K, Miyamae M, Kato H, Takumi S, Ogihara Y (2003) WAP1, a wheat APETALA1 homolog, plays a central role in the phase transition from vegetative to reproductive growth. Plant Cell Physiol 44(12):1255–1265
Oliver S, Finnegan E, Dennis E, Peacock W, Trevaskis B (2009) Vernalization-induced flowering in cereals is associated with changes in histone methylation at the VERNALIZATION1 gene. Proc Nat Acad Sci USA 106:8386–8391
Pfaffl M (2001) A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res 29(900):2002–2007
Pfluger J, Wagner D (2007) Histone modifications and dynamic regulation of genome accessibility in plants. Curr Opin Plant Biol 10:645–652
Pidal B, Yan L, Fu D, Zhang F, Tranquilli G, Dubcovsky J (2009) The CArG-Box located upstream from the transcriptional start of wheat vernalization gene VRN1 is not necessary for the vernalization response. J Hered 100(3):355–364
Pien S, Fleury D, Mylne J, Crevillen P, Inze D, Avramova Z, Dean C, Grossniklaus U (2008) ARABIDOPSIS TRITHORAX1 dynamically regulates FLOWERING LOCUS C activation via histone 3 lysine 4 trimethylation. Plant Cell 49:580–588
Preston J, Kellogg E (2006) Reconstructing the evolutionary history of paralogous APETALA1/FRUITFULL-Like genes in grasses (Poaceae). Genetics 174:421–437
Ringrose L, Paro R (2004) Epigenetic regulation of cellular memory by the Polycomb and Trithorax group proteins. Annu Rev Genet 38:413–443
Roh T, Cuddapah S, Cui K, Zhao K (2006) The genomic landscape of histone modifications in human T cells. Proc Natl Acad Sci USA 103:15782–15787
Schumacher A, Magnuson T (1997) Murine Polycomb- and trithorax-group genes regulate homeotic pathways and beyond. Trends Genet 13:167–170
Schwartz Y, Pirrotta V (2008) Polycomb complexes and epigenetic states. Curr Opin Cell Biol 20:266–273
Searle I, He Y, Turck F, Vincent C, Fornara F, Kröber S, Amasino R, Coupland G (2006) The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis. Genes Dev 20:898–912
Sheldon C, Rouse D, Finnegan E, Peacock W, Dennis E (2000) The molecular basis of vernalization: the central role of FLOWERING LOCUS C (FLC). Proc Natl Acad Sci USA 97:3753–3758
Sheldon C, Hills M, Lister C, Dean C, Dennis E, Peacock W (2008) Resetting of FLOWERING LOCUS C expression after epigenetic repression by vernalization. Proc Natl Acad Sci USA 105:2214–2219
Shimada S, Ogawa T, Kitagawa S, Suzuki T, Ikari C, Shitsukawa N, Abe T, Kawahigashi H, Kikuchi R, Handa H, Murai K (2009) A genetic network of flowering time genes in wheat leaves, in which an APETALA1/FRUITFULL-like gene, VRN1, is upstream of FLOWERING LOCUS T. Plant J 58:668–681
Springer N, Napoli C, Selinger D, Pandey R, Cone K, Chandler V, Kaeppler H, Kaeppler S (2003) Comparative analysis of SET domain proteins in maize and Arabidopsis reveals multiple duplications preceding the divergence of monocots and dicots. Plant Physiol 132:907–925
Sung S, Amasino R (2004) Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427:159–164
Sung S, Amasino R (2006) Molecular genetic studies of the memory of winter. J Exp Bot 57:3369–3377
Sung S, He Y, Eshoo T, Tamada Y, Johnson L, Nakahigashi K, Goto K, Jacobsen S, Amasino R (2006) Epigenetic maintenance of the vernalized state in Arabidopsis thaliana requires LIKE HETEROCHROMATIN PROTEIN 1. Nat Genet 38:706–710
Trevaskis B, Hemming M, Dennis E, Peacock W (2007) The molecular basis of vernalization-induced flowering in cereals. Trends Plants Sci 12:352–357
Wei G, Wei L, Zhu J, Zang C, Hu-Li J, Yao Z, Cui K, Kanno Y, Roh T-Y, Watford W, Schones D, Peng W, Sun H, Paul W, O’Shea J, Zhao K (2009) Global mapping of H3K4me3 and H3K27me3 reveals specificity and plasticity in lineage fate determination of differentiating CD4+ T cells. Immunity 30(1):155–167
Winfield M, Lu C, Wilson I, Coghill J, Edwards K (2009) Cold- and light-induced changes in the transcriptome of wheat leading to phase transition from vegetative to reproductive growth. BMC Plant Biol 9:55. doi:10.1186/1471-2229-9-55
Yamaguchi-Shinozaki K, Shinozaki K (2005) Organization of cis-acting regulatory elements in osmotic- and cold-stressresponsive promoters. Trends Plant Sci 10:88–94
Yan L, Loukoianov A, Tranquilli G, Helguera M, Fahima T, Dubcovsky J (2003) Positional cloning of the wheat vernalization gene VRN1. Proc Natl Acad Sci USA 100(10):6263–6268
Yan L, Loukoianov A, Blechl A, Tranquilli G, Ramakrishna W, SanMiguel P, Bennetzen JL, Echenique V, Dubcovsky J (2004) The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science 303(5664):1640–1644
Yeung K, Seitz T, Li S, Janoschk P, McFerrank B, Kaiser C, Feek F, Katsanakisk K, Rose D, Mischak H, Sedivy J, Kolch W (1999) Suppression of Raf-1 kinase activity and MAP kinase signalling by RKIP. Nature 401:173–177
Zhang K, Sridhar V, Zhu J, Kapoor A, Zhu J (2007) Distinctive core histone post-translational modification patterns in Arabidopsis thaliana. PLoS One 2:e1210
Acknowledgments
The authors thank Dr. Ndjido Ardo Kane, Dr. Zahra Agharbaoui (UQAM) and Dr. Yoko Tominaga (UQAM) for their valuable advices. This work was supported by a Natural Sciences and Engineering Research Council of Canada discovery grant to Dr. Fathey Sarhan.
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Communicated by S. Hohmann.
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Diallo, A.O., Ali-Benali, M.A., Badawi, M. et al. Expression of vernalization responsive genes in wheat is associated with histone H3 trimethylation. Mol Genet Genomics 287, 575–590 (2012). https://doi.org/10.1007/s00438-012-0701-0
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DOI: https://doi.org/10.1007/s00438-012-0701-0