The central role of the VERNALIZATION1 gene in the vernalization response of cereals
Ben TrevaskisA CSIRO Division of Plant Industry, GPO Box 1600, Canberra, ACT 2601, Australia. Email: ben.trevaskis@csiro.au
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 https://doi.org/10.1071/FP10056
Submitted: 12 March 2010 Accepted: 18 April 2010 Published: 20 May 2010
Abstract
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.
Acknowledgements
I thank my friends and colleagues Steve Swain, Aaron Greenup, Sarah Fieg, Sandra Oliver and Megan Hemming for reading drafts of this manuscript and providing constructive suggestions. I also gratefully acknowledge both the Commonwealth Scientific and Industrial Research Organisation, and the Grains Research and development Corporation for long-term support of this research.
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Amasino RM
(2004) Vernalization, competence, and the epigenetic memory of winter. The Plant Cell 16, 2553–2559.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Chouard P
(1960) Vernalization and its relation to dormancy. Annual Review of Plant Physiology 11, 191–238.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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 in press. ,
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Distelfeld A,
Li C, Dubcovsky J
(2009) Regulation of flowering in temperate cereals. Current Opinion in Plant Biology 12, 178–184.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
Faure S,
Higgins J,
Turner A, Laurie DA
(2007) The FLOWERING LOCUS T-like gene family in Barley (Hordeum vulgare). Genetics 176, 599–609.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gregory FG, Purvis ON
(1936) Vernalisation of winter rye during ripening. Nature [Abstract] 138, 973.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
King RW, Heide OM
(2009) Seasonal flowering and evolution: the heritage from Charles Darwin. Functional Plant Biology 36, 1027–1036.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Li CX, Dubcovsky J
(2008) Wheat FT protein regulates VRN1 transcription through interactions with FDL2. The Plant Journal 55, 543–554.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
McKinney HH
(1940) Vernalization and the growth phase concept. Botanical Review 6, 25–47.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref |
PubMed |
Michaels SD,
Himelblau E,
Kim SY,
Schomburg FM, Amasino RM
(2005) Integration of flowering signals in winter-annual Arabidopsis. Plant Physiology 137, 149–156.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
Prasil IT,
Prasilova P, Pankova K
(2004) Relationships among vernalization, shoot apex development and frost tolerance in wheat. Annals of Botany 94, 413–418.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pugsley AT
(1971) A genetic analysis of the spring–winter habit of growth in wheat. Australian Journal of Agricultural Research 22, 21–31.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref |
PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tamaki S,
Matsuo S,
Wong HL,
Yokoi S, Shimamoto K
(2007) Hd3a protein is a mobile flowering signal in rice. Science 316, 1033–1036.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Teper-Bamnolker P, Samach A
(2005) The flowering integrator FT regulates SEPALLATA3 and FRUITFULL accumulation in Arabidopsis leaves. The Plant Cell 17, 2661–2675.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Trevaskis B,
Hemming MN,
Dennis ES, Peacock WJ
(2007a) The molecular basis of vernalization-induced flowering in cereals. Trends in Plant Science 12, 352–357.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Trevaskis B,
Tadege M,
Hemming MN,
Peacock WJ,
Dennis ES, Sheldon C
(2007b)
Short Vegetative Phase-like MADS-box genes inhibit floral meristem identity in barley. Plant Physiology 143, 225–235.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Yan L,
Loukoianov A,
Blechl A,
Tranquilli G,
Ramakrishna W,
SanMiguel P,
Bennetzen JL,
Echenique V, Dubcovsky J
(2004a) The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science 303, 1640–1644.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Yan L,
Helguera M,
Kato K,
Fukuyama S,
Sherman J, Dubcovsky J
(2004b) Allelic variation at the VRN-1 promoter region in polyploid wheat. Theoretical and Applied Genetics 109, 1677–1686.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Zadoks JC,
Chang TT, Konzak CF
(1974) A decimal code for the growth stages of cereals. Weed Research 14, 415–421.
| Crossref | GoogleScholarGoogle Scholar |
Zeevaart JA
(2008) Leaf-produced floral signals. Current Opinion in Plant Biology 11, 541–547.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
