Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology

The central role of the VERNALIZATION1 gene in the vernalization response of cereals

Ben Trevaskis

A CSIRO Division of Plant Industry, GPO Box 1600, Canberra, ACT 2601, Australia. Email:

This paper originates from the Peter Goldacre Award 2009 of the Australian Society of Plant Scientists that was received by the author.

Functional Plant Biology 37(6) 479-487
Submitted: 12 March 2010  Accepted: 18 April 2010   Published: 20 May 2010


Many varieties of wheat (Triticum spp.) and barley (Hordeum vulgare L.) require prolonged exposure to cold during winter in order to flower (vernalization). In these cereals, vernalization-induced flowering is controlled by the VERNALIZATION1 (VRN1) gene. VRN1 is a promoter of flowering that is activated by low temperatures. VRN1 transcript levels increase gradually during vernalization, with longer cold treatments inducing higher expression levels. Elevated VRN1 expression is maintained in the shoot apex and leaves after vernalization, and the level of VRN1 expression in these organs determines how rapidly vernalized plants flower. Some alleles of VRN1 are expressed without vernalization due to deletions or insertions within the promoter or first intron of the VRN1 gene. Varieties of wheat and barley with these alleles flower without vernalization and are grown where vernalization does not occur. The first intron of the VRN1 locus has histone modifications typically associated with the maintenance of an inactive chromatin state, suggesting this region is targeted by epigenetic mechanisms that contribute to repression of VRN1 before winter. Other mechanisms are likely to act elsewhere in the VRN1 gene to mediate low-temperature induction. This review examines how understanding the mechanisms that regulate VRN1 provides insights into the biology of vernalization-induced flowering in cereals and how this will contribute to future cereal breeding strategies.

Additional keywords: barley, flowering, wheat.


Abe M Kobayashi Y Yamamoto S Daimon Y Yamaguchi A Ikeda Y Ichinoki H Notaguchi M Goto K Araki T 2005 FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science 309 1052 1056 doi:10.1126/science.1115983

Amasino RM 2004 Vernalization, competence, and the epigenetic memory of winter. The Plant Cell 16 2553 2559 doi:10.1105/tpc.104.161070

An H Roussot C Suarez-Lopez P Corbesier L Vincent C et al 2004 CONSTANS acts in the phloem to regulate a systemic signal that induces photoperiodic flowering of Arabidopsis. Development 131 3615 3626 doi:10.1242/dev.01231

Bonnet OT 1935 The development of the barley spike. Journal of Agricultural Research 51 451 457

Bonnet OT 1936 The development of the wheat spike. Journal of Agricultural Research 53 445 451

Cao R Wang L Wang H Xia L Erdjument-Bromage H Tempst P Jones RS Zhang Y 2002 Role of histone H3 lysine 27 methylation in polycomb-group silencing. Science 298 1039 1043

Chouard P 1960 Vernalization and its relation to dormancy. Annual Review of Plant Physiology 11 191 238 doi:10.1146/annurev.pp.11.060160.001203

Cockram J Chiapparino E Taylor S Stamati K Donini P Laurie D O’Sullivan D 2007 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. Theoretical and Applied Genetics 115 993 1001 doi:10.1007/s00122-007-0626-x

Corbesier L Vincent C Jang S Fornara F Fan Q et al 2007 FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316 1030 1033 doi:10.1126/science.1141752

Danyluk J Kane NA Breton G Limin AE Fowler DB Sarhan F 2003 TaVRT-1, a putative transcription factor associated with vegetative to reproductive transition in cereals. Plant Physiology 132 1849 1860 doi:10.1104/pp.103.023523

De Lucia F Crevillen P Jones AME Greb T Dean C 2008 A PHD-polycomb repressive complex 2 triggers the epigenetic silencing of FLC during vernalization. Proceedings of the National Academy of Sciences of the United States of America 105 16 831 16 836 doi:10.1073/pnas.0808687105

Distelfeld A Dubcovsky J 2010 Characterization of the maintained vegetative phase deletions from diploid wheat and their effect on VRN2 and FT transcript levels. Molecular Genetics and Genomics doi:10.1007/s00438-009-0510-2 in press.

Distelfeld A Li C Dubcovsky J 2009 Regulation of flowering in temperate cereals. Current Opinion in Plant Biology 12 178 184 doi:10.1016/j.pbi.2008.12.010

Dubcovsky J Lijavetzky D Appendino L Tranquilli G 1998 Comparative RFLP mapping of Triticum monococcum genes controlling vernalization requirement. Theoretical and Applied Genetics 97 968 975 doi:10.1007/s001220050978

Dubcovsky J Loukoianov A Fu D Valarik M Sanchez A Yan L 2006 Effect of photoperiod on the regulation of wheat vernalization genes VRN1 and VRN2. Plant Molecular Biology 60 469 480 doi:10.1007/s11103-005-4814-2

Eagles HA Cane K Neil V 2009 The flow of alleles of important photoperiod and vernalisation genes through Australian wheat. Crop and Pasture Science 60 646 657 doi:10.1071/CP09014

Faure S Higgins J Turner A Laurie DA 2007 The FLOWERING LOCUS T-like gene family in Barley (Hordeum vulgare). Genetics 176 599 609 doi:10.1534/genetics.106.069500

Ferrándiz C Gu Q Martienssen R Yanofsky MF 2000 Redundant regulation of meristem identity and plant architecture by FRUITFULL, APETALA1 and CAULIFLOWER. Development 127 725 734

Finnegan EJ Dennis ES 2007 Vernalization-induced trimethylation of histone H3 lysine 27 at FLC is not maintained in mitotically quiescent cells. Current Biology 17 1978 1983

Flood RG Halloran GM 1984 The nature and duration of gene action for vernalization response in wheat. Annals of Botany 53 363 368

Fowler DB Chauvin LP Limin AE Sarhan F 1996 The regulatory role of vernalization in the expression of low-temperature-induced genes in wheat and rye. Theoretical and Applied Genetics 93 554 559

Fu DL Szucs P Yan LL Helguera M Skinner JS von Zitzewitz J Hayes PM Dubcovsky J 2005 Large deletions within the first intron in VRN-1 are associated with spring growth habit in barley and wheat. Molecular Genetics and Genomics 273 54 65 doi:10.1007/s00438-004-1095-4

Galiba G Vagujfalvi A Li C Soltesz A Dubcovsky J 2009 Regulatory genes involved in the determination of frost tolerance in temperate cereals. Plant Science 176 12 19 doi:10.1016/j.plantsci.2008.09.016

Gassner G 1918 Beitraege zur physiologischen charakteristik sommer- und winterannueller gewaechse in besondere der getreidepflanzen. Zeitschrift für Botanik 10 417 480

Gocal GFW King RW Blundell CA Schwartz OM Andersen CH Weigel D 2001 Evolution of floral meristem identity genes: analyses of Lolium temulentum genes related to APETALA1 and LEAFY of Arabidopsis. Plant Physiology 125 1788 1801

Gott MB Gregory FG Purvis ON 1955 Studies in vernalization of cereals VIII. Photoperiodic control of stage in flowering between initiation and ear formation in vernalised and unvernalised petkus winter rye. Annals of Botany 21 87 126

Greenup A Peacock WJ Dennis ES Trevaskis B 2009 The molecular biology of seasonal flowering-responses in Arabidopsis and the cereals. Annals of Botany 103 1165 1172

Gregory FG Purvis ON 1936 Vernalisation of winter rye during ripening. Nature 138 973 doi:10.1038/138973a0 [Abstract]

Hayes PM Blake T Chen THH Tragoonrung S Chen F Pan A Liu B 1993 Quantitative trait loci on barley (Hordeum vulgare L.) chromosome 7 associated with components of winter hardiness. Genome 36 66 71 doi:10.1139/g93-009

Helliwell CA Wood CC Robertson M Peacock WJ Dennis ES 2006 The Arabidopsis FLC protein interacts directly in vivo with SOC1 and FT chromatin and is part of a high-molecular-weight protein complex. The Plant Journal 46 183 192 doi:10.1111/j.1365-313X.2006.02686.x

Hemming MN Peacock WJ Dennis ES Trevaskis B 2008 Low-temperature and daylength cues are integrated to regulate FLOWERING LOCUS T in barley. Plant Physiology 147 355 366 doi:10.1104/pp.108.116418

Hemming MN Fieg S Peacock WJ Dennis ES Trevaskis B 2009 Regions associated with repression of the barley (Hordeum vulgare) VERNALIZATION1 gene are not required for cold induction. Molecular Genetics and Genomics 282 107 117 doi:10.1007/s00438-009-0449-3

Kane NA Agharbaoui Z Diallo AO Adam H Tominaga Y Ouellet F Sarhan F 2007 TaVRT2 represses transcription of the wheat vernalization gene TaVRN1. The Plant Journal 51 670 680 doi:10.1111/j.1365-313X.2007.03172.x

Kardailsky I Shukla VK Ahn JH Dagenais N Christensen SK Nguyen JT Chory J Harrison MJ Weigel D 1999 Activation tagging of the floral inducer FT. Science 286 1962 1965 doi:10.1126/science.286.5446.1962

Karsai I Szucs P Meszaros K Filichkina T Hayes PM Skinner JS Lang L Bedo Z 2005 The Vrn-H2 locus is a major determinant of flowering time in a facultative × winter growth habit barley (Hordeum vulgare L.) mapping population. Theoretical and Applied Genetics 110 1458 1466 doi:10.1007/s00122-005-1979-7

King RW Heide OM 2009 Seasonal flowering and evolution: the heritage from Charles Darwin. Functional Plant Biology 36 1027 1036 doi:10.1071/FP09170

Kobayashi Y Kaya H Goto K Iwabuchi M Araki T 1999 A pair of related genes with antagonistic roles in mediating flowering signals. Science 286 1960 1962 doi:10.1126/science.286.5446.1960

Koemel JE Guenzi AC Anderson JA Smith EL 2004 Cold hardiness of wheat near-isogenic lines differing in vernalization alleles. Theoretical and Applied Genetics 109 839 846 doi:10.1007/s00122-004-1686-9

Li CX Dubcovsky J 2008 Wheat FT protein regulates VRN1 transcription through interactions with FDL2. The Plant Journal 55 543 554 doi:10.1111/j.1365-313X.2008.03526.x

Limin AE Fowler DB 2006 Low-temperature tolerance and genetic potential in wheat (Triticum aestivum L.): response to photoperiod, vernalization, and plant development. Planta 224 360 366 doi:10.1007/s00425-006-0219-y

Loukoianov A Yan L Blechl A Sanchez A Dubcovksy J 2005 Regulation of VRN-1 vernalization genes in normal and transgenic polyploid wheat. Plant Physiology 138 2364 2373 doi:10.1104/pp.105.064287

Mahfoozi S Limin AE Fowler DB 2001 Influence of vernalization and photoperiod responses on cold hardiness in winter cereals. Crop Science 41 1006 1011

Marcińska I Dubert F Biesaga-Koscielniak J 1995 Transfer of the ability to flower in winter wheat via callus tissue regenerated from immature inflorescences. Plant Cell, Tissue and Organ Culture 41 285 288

McKinney HH 1940 Vernalization and the growth phase concept. Botanical Review 6 25 47 doi:10.1007/BF02879295

Michaels SD Amasino RM 1999 FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. The Plant Cell 11 949 956

Michaels SD Himelblau E Kim SY Schomburg FM Amasino RM 2005 Integration of flowering signals in winter-annual Arabidopsis. Plant Physiology 137 149 156

Oliver SN Finnegan EJ Dennis ES Peacock WJ Trevaskis B 2009 Vernalization-induced flowering in cereals is associated with changes in histone methylation at the VERNALIZATION1 gene. Proceedings of the National Academy of Sciences of the United States of America 106 8386 8391 doi:10.1073/pnas.0903566106

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. Heredity 100 355 364 doi:10.1093/jhered/esp002

Prasil IT Prasilova P Pankova K 2004 Relationships among vernalization, shoot apex development and frost tolerance in wheat. Annals of Botany 94 413 418 doi:10.1093/aob/mch158

Preston JC Kellogg EA 2008 Discrete developmental roles for temperate cereal grass VERNALIZATION1/FRUITFULL-like genes in flowering competency and the transition to flowering. Plant Physiology 146 265 276 doi:10.1104/pp.107.109561

Pugsley AT 1971 A genetic analysis of the spring–winter habit of growth in wheat. Australian Journal of Agricultural Research 22 21 31 doi:10.1071/AR9710021

Purvis ON 1934 An analysis of the influence of temperature during germination on the subsequent development of certain winter cereals and its relation to the effect of length of day. Annals of Botany 48 919 955

Roberts DWA 1979 Duration of hardening and cold hardiness in winter wheat. Canadian Journal of Botany 57 1511 1517

Roberts DWA 1990 Identification of loci on chromosome 5A of wheat involved in control of cold hardiness, vernalization, leaf length, rosette growth habit, and height of hardened plants. Genome 33 247 259

Sasani S Hemming MN Oliver S Greenup A Tavakkol-Afshari R et al 2009 The influence of vernalization and daylength cues on the expression of flowering-time genes in the leaves and shoot apex of barley (Hordeum vulgare). Journal of Experimental Botany 60 2169 2178

Schubert D Primavesi L Bishopp A Roberts G Doonan J Jenuwein T Goodrich J 2006 Silencing by plant polycomb-group genes requires dispersed trimethylation of histone H3 at lysine 27. The EMBO Journal 25 4638 4649 doi:10.1038/sj.emboj.7601311

Sheldon CC Burn JE Perez PP Metzger J Edwards JA Peacock WJ Dennis ES 1999 The FLF MADS box gene, a repressor of flowering in Arabidopsis regulated by vernalization and methylation. The Plant Cell 11 445 458

Shitsukawa N Ikari C Shimada S Kitagawa S Sakamoto K et al 2007 The einkorn wheat (Triticum monococcum) mutant, maintained vegetative phase, is caused by a deletion in the VRN1 gene. Genes & Genetic Systems 82 167 170

Stockinger EJ Skinner JS Gardner KG Francia E Pecchioni N 2007 Expression levels of barley Cbf genes at the frost resistance-H2 locus are dependent upon alleles at Fr-H1 and Fr-H2. The Plant Journal 51 308 321 doi:10.1111/j.1365-313X.2007.0141.x

Suárez-López P Wheatley K Robson F Onouchi H Valverde F Coupland G 2001 CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410 1116 1120 doi:10.1038/35074138

Sung SB Schmitz RJ Amasino RM 2006 A PHD finger protein involved in both the vernalization and photoperiod pathways in Arabidopsis. Genes & Development 20 3244 3248 doi:10.1101/gad.1493306

Szucs P Skinner JS Karsai I Cuesta-Marcos A Haggard KG Corey AE Chen TH Hayes PM 2007 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. Molecular Genetics and Genomics 277 249 261 doi:10.1007/s00438-006-0195-8

Takahashi R , Yasuda S (1971) Genetics of earliness and growth habit in barley. In ‘Barley genetics II (proceedings of the second international barley genetics symposium)’. (Ed. RA Nilan) pp. 388–408. (Washington State University Press: Pullman, WA)

Tamaki S Matsuo S Wong HL Yokoi S Shimamoto K 2007 Hd3a protein is a mobile flowering signal in rice. Science 316 1033 1036 doi:10.1126/science.1141753

Teper-Bamnolker P Samach A 2005 The flowering integrator FT regulates SEPALLATA3 and FRUITFULL accumulation in Arabidopsis leaves. The Plant Cell 17 2661 2675 doi:10.1105/tpc.105.035766

Thomas B , Vince-Prue D (1997) ‘Photoperiodism in plants.’ (Academic Press: New York)

Trevaskis B Bagnall DJ Ellis MH Peacock WJ Dennis ES 2003 MADS box genes control vernalization-induced flowering in cereals. Proceedings of the National Academy of Sciences of the United States of America 100 13 099 13 104 doi:10.1073/pnas.1635053100

Trevaskis B Hemming MN Peacock WJ Dennis ES 2006 HvVRN2 responds to daylength, whereas HvVRN1 is regulated by vernalization and developmental status. Plant Physiology 140 1397 1405 doi:10.1104/pp.105.073486

Trevaskis B Hemming MN Dennis ES Peacock WJ 2007 a The molecular basis of vernalization-induced flowering in cereals. Trends in Plant Science 12 352 357 doi:10.1016/j.tplants.2007.06.010

Trevaskis B Tadege M Hemming MN Peacock WJ Dennis ES Sheldon C 2007 b Short Vegetative Phase-like MADS-box genes inhibit floral meristem identity in barley. Plant Physiology 143 225 235 doi:10.1104/pp.106.090860

Turner A Beales J Faure S Dunford RP Laurie DA 2005 The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science 310 1031 1034 doi:10.1126/science.1117619

Valverde F Mouradov A Soppe W Ravenscroft D Samach A Coupland G 2004 Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science 303 1003 1006 doi:10.1126/science.1091761

von Zitzewitz J Szucs P Dubcovsky J Yan LL Francia E Pecchioni N Casas A Chen THH Hayes PM Skinner JS 2005 Molecular and structural characterization of barley vernalization genes. Plant Molecular Biology 59 449 467 doi:10.1007/s11103-005-0351-2

Whelan EDP Schaalje GB 1992 Vernalization of embryogenic callus from immature embryos of winter wheat. Crop Science 32 78 80

Wigge PA Kim MC Jaeger KE Busch W Schmid M Lohmann JU Weigel D 2005 Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309 1056 1059

Wood CC Robertson M Tanner G Peacock WJ Dennis ES Helliwell CA 2006 The Arabidopsis thaliana vernalization response requires a polycomb-like protein complex that also includes VERNALIZATION INSENSITIVE 3. Proceedings of the National Academy of Sciences of the United States of America 103 14 631 14 636 doi:10.1073/pnas.0606385103

Yan L Loukoianov A Tranquilli G Helguera M Fahima T Dubcovsky J 2003 Positional cloning of the wheat vernalization gene VRN1. Proceedings of the National Academy of Sciences of the United States of America 100 6263 6268 doi:10.1073/pnas.0937399100

Yan L Loukoianov A Blechl A Tranquilli G Ramakrishna W SanMiguel P Bennetzen JL Echenique V Dubcovsky J 2004 a The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science 303 1640 1644 doi:10.1126/science.1094305

Yan L Helguera M Kato K Fukuyama S Sherman J Dubcovsky J 2004 b Allelic variation at the VRN-1 promoter region in polyploid wheat. Theoretical and Applied Genetics 109 1677 1686 doi:10.1007/s00122-004-1796-4

Yan L Fu D Li C Blechl A Tranquilli G Bonafede M Sanchez A Valarik M Yasuda S Dubcovsky J 2006 The wheat and barley vernalization gene VRN3 is an orthologue of FT. Proceedings of the National Academy of Sciences of the United States of America 103 19 581 19 586 doi:10.1073/pnas.0607142103

Zadoks JC Chang TT Konzak CF 1974 A decimal code for the growth stages of cereals. Weed Research 14 415 421 doi:10.1111/j.1365-3180.1974.tb01084.x

Zeevaart JA 2008 Leaf-produced floral signals. Current Opinion in Plant Biology 11 541 547 doi:10.1016/j.pbi.2008.06.009

Zhang XK Xiao TG Zhang Y Xia XC Dubcovsky J He ZH 2008 Allelic variation at the vernalization gene Vrn-A1, Vrn-B1, VRN-D1 and Vrn-B3 in Chinese wheat cultivars and their association with growth habit. Crop Science 48 458 470 doi:10.2135/cropsci2007.06.0355

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