Goldacre Paper: The central role of the VERNALIZATION1 gene in the vernalization response of cereals

Functional Plant Biology

Volumn 37, Issue 6, 2010, Pages 479-487

  Trevaskis, Ben ^a  

^a CSIRO   (Australia)

Author keywords

Barley; Flowering; Wheat

Indexed keywords

CEREAL BREEDING; COLD TREATMENTS; EPIGENETIC MECHANISMS; EXPRESSION LEVELS; HISTONE MODIFICATION; HORDEUM VULGARE; LOW TEMPERATURES; SHOOT APEX; TRANSCRIPT LEVEL; TRITICUM SPP;

BIOLOGY;

ALLELE; BARLEY; CULTIVAR; ENVIRONMENTAL CONDITIONS; FLOWERING; GENE EXPRESSION; LOW TEMPERATURE; NUCLEIC ACID; PLANT BREEDING; PROTEIN; VERNALIZATION; WHEAT;

HORDEUM; HORDEUM VULGARE SUBSP. VULGARE; TRITICUM; TRITICUM AESTIVUM;

EID: 77952936186     PISSN: 14454408     EISSN: None     Source Type: Journal    
DOI: 10.1071/FP10056     Document Type: Article

References (83)

1. 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 (Pubitemid 41134458)
2. Amasino RM (2004) Vernalization, competence, and the epigenetic memory of winter. The Plant Cell 16, 2553-2559. doi:10.1105/tpc.104.161070 (Pubitemid 41071345)
3. 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
4. Bonnet OT (1935) The development of the barley spike. Journal of Agricultural Research 51, 451-457.
5. Bonnet OT (1936) The development of the wheat spike. Journal of Agricultural Research 53, 445-451.
6. 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 polycombgroup silencing. Science 298, 1039-1043. doi:10.1126/science.1076997 (Pubitemid 35247314)
7. 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
8. 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 (Pubitemid 47561705)
9. 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
10. 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
11. 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, 16831-16836. doi:10.1073/pnas.0808687105
12. 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. doi:10.1007/s00438-009-0510-2
13. 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
14. 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 (Pubitemid 28519393)
15. Dubcovsky J, Loukoianov A, Fu D, Valarik M, Sanchez A, Yan L (2006) Effect of photo period on there gulation of wheat vernalization genes VRN1 and VRN2. Plant Molecular Biology 60, 469-480. doi:10.1007/s11103-005-4814-2 (Pubitemid 43363224)
16. 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
17. Faure S, Higgins J, Turner A, Laurie DA (2007) The FLOWERING LOCUST-like gene family in Barley (Hordeum vulgare). Genetics 176, 599-609. doi:10.1534/genetics.106.069500 (Pubitemid 350021050)
18. 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.
19. 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. doi:10.1016/j.cub.2007.10.026 (Pubitemid 350088488)
20. Flood RG, Halloran GM (1984) The nature and duration of gene action for vernalization response in wheat. Annals of Botany 53, 363-368.
21. 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. doi:10.1007/BF00417947
22. 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 (Pubitemid 40543932)
23. Galiba G, Vagujfalvi A, Li C, Soltesz A, Dubcovsky J (2009) Regulatory genes involvedinthe determinationoffrost toleranceintemperatecereals. Plant Science 176, 12-19. doi:10.1016/j.plantsci.2008.09.016
24. Gassner G (1918) Beitraege zur physiologischen charakteristik sommer- und winterannueller gewaechse in besondere der getreidepflanzen. Zeitschrift für Botanik 10, 417-480.
25. 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. doi:10.1104/pp. 125.4.1788
26. Gott MB, Gregory FG, Purvis ON (1955) Studies in vernalization of cereals VIII. Photoperiodiccontrolofstage infloweringbetweeninitiationandear formation in vernalised and unvernalised petkus winter rye. Annals of Botany 21, 87-126.
27. 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. doi:10.1093/aob/mcp063
28. Gregory FG, Purvis ON (1936) Vernalisation of winter rye during ripening. Nature 138, 973. [Abstract] doi:10.1038/138973a0
29. 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
30. 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
31. Hemming MN, Peacock WJ, Dennis ES, Trevaskis B (2008) Lowtemperature and daylength cues are integrated to regulate FLOWERING LOCUS T in barley. Plant Physiology 147, 355-366. doi:10.1104/pp. 108.116418
32. 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
33. 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 (Pubitemid 47231192)
34. 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
35. Karsai I, Szucs P, Meszaros K, Filichkina T, Hayes PM, Skinner JS, Lang L, Bedo Z (2005) The Vrn-H2 locus is amajor 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 (Pubitemid 40920009)
36. King RW, Heide OM (2009) Seasonal flowering and evolution: the heritage from Charles Darwin. Functional Plant Biology 36, 1027-1036. doi:10.1071/FP09170
37. 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
38. 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 (Pubitemid 39211093)
39. 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
40. 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 (Pubitemid 43946054)
41. 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
42. Mahfoozi S, Limin AE, Fowler DB (2001) Influence of vernalization and photoperiod responses on cold hardiness in winter cereals. Crop Science 41, 1006-1011.
43. Marcinska 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. doi:10.1007/BF00045094
44. McKinney HH (1940) Vernalization and the growth phase concept. Botanical Review 6, 25-47. doi:10.1007/BF02879295
45. Michaels SD, Amasino RM (1999) FLOWERING LOCUS Cencodesanovel MADS domain protein that actsasarepressor of flowering. The Plant Cell 11, 949-956.
46. Michaels SD, Himelblau E, Kim SY, Schomburg FM, Amasino RM (2005) Integration of flowering signals in winter-annual Arabidopsis. Plant Physiology 137, 149-156. doi:10.1104/pp. 104.052811
47. Oliver SN, Finnegan EJ, Dennis ES, Peacock WJ, Trevaskis B (2009) Vernalization-induced flowering in cereals is associated with changes inhistone 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
48. 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
49. Prasil IT, Prasilova P, Pankova K (2004) Relationships among vernalization, shoot apex development and frosttoleranceinwheat. Annals of Botany94, 413-418. doi:10.1093/aob/mch158 (Pubitemid 41301658)
50. 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
51. 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
52. 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.
53. Roberts DWA (1979) Duration of hardening and cold hardiness in winter wheat. Canadian Journal of Botany 57, 1511-1517. doi:10.1139/b79-188
54. 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.
55. 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. doi:10.1093/jxb/erp098
56. 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 (Pubitemid 44498136)
57. 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.
58. 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. doi:10.1266/ggs.82.167 (Pubitemid 46743511)
59. 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 (Pubitemid 47030126)
60. 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 (Pubitemid 32391045)
61. Sung SB, Schmitz RJ, Amasino RM (2006) A PHD finger protein involved in both the vernalization and photoperiodpathways in Arabidopsis. Genes & Development 20, 3244-3248. doi:10.1101/gad.1493306 (Pubitemid 44904846)
62. 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 (Pubitemid 46348870)
63. 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)
64. Tamaki S, Matsuo S, Wong HL, Yokoi S, Shimamoto K (2007) Hd3a protein isamobileflowering signalinrice. Science 316, 1033-1036. doi:10.1126/science. 1141753 (Pubitemid 46799491)
65. 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
66. Thomas B, Vince-Prue D (1997) 'Photoperiodism in plants.' (Academic Press: New York)
67. 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, 13099-13104. doi:10.1073/pnas.1635053100 (Pubitemid 37340032)
68. 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
69. 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. doi:10.1016/j.tplants.2007.06.010 (Pubitemid 47187749)
70. 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. doi:10.1104/pp. 106.090860
71. Turner A, Beales J, Faure S, Dunford RP, Laurie DA (2005) The pseudoresponse regulator Ppd-H1 provides adaptation to photoperiod in barley. Science 310, 1031-1034. doi:10.1126/science.1117619 (Pubitemid 41611918)
72. Valverde F, Mouradov A, Soppe W, Ravenscroft D, Samach A, Coupland G (2004) Photoreceptor regulationof CONSTANS proteinin photoperiodic flowering. Science 303, 1003-1006. doi:10.1126/science.1091761 (Pubitemid 38209702)
73. 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 (Pubitemid 41464664)
74. Whelan EDP, Schaalje GB (1992) Vernalization of embryogenic callus from immature embryos of winter wheat. Crop Science 32, 78-80.
75. Wigge PA, Kim MC, Jaeger KE, BuschW, Schmid M, Lohmann JU, Weigel D (2005) Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309, 1056-1059. doi:10.1126/science.1114358 (Pubitemid 41134459)
76. 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, 14631-14636. doi:10.1073/pnas.0606385103 (Pubitemid 44484801)
77. 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 (Pubitemid 36576964)
78. 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. doi:10.1126/science.1094305 (Pubitemid 38338316)
79. 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. doi:10.1007/s00122-004-1796-4 (Pubitemid 40024933)
80. 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, 19581-19586. doi:10.1073/pnas.0607142103 (Pubitemid 46026073)
81. 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
82. Zeevaart JA (2008) Leaf-produced floral signals. Current Opinion in Plant Biology 11, 541-547. doi:10.1016/j.pbi.2008.06.009
83. 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 (Pubitemid 351569291)