, Volume 197, Issue 1, pp 1–26 | Cite as

Flowering time in wheat (Triticum aestivum L.): a key factor for global adaptability

  • Atif Kamran
  • Muhammad Iqbal
  • Dean Spaner


Wheat is one of the most widely cultivated crops and, being the staple diet of more than 40 countries, it plays an imperative role in food security. Wheat has remarkable genetic potential to synchronize its flowering time with favourable environmental conditions. This ability to time its flowering is a key factor for its global adaptability and enables wheat plant to produce satisfactory grain yield under very diverse temperature and soil moisture conditions. Vernalization (Vrn), photoperiod (Ppd) and earliness per se (Eps) are the three genetic systems controlling flowering time in wheat. The objective of this review is to provide comprehensive information on the physiological, molecular and biological aspects of the three genetic constituents of flowering and maturity time in wheat. Reviews written in the past have covered either one of the aspects; and generally focused on one of the three genetic constituents of the flowering time. The current review provides (a) a detailed overview of all three gene systems (vernalization, photoperiod and earliness per se) controlling flowering time, (b) details of the primer sequences, their annealing temperatures and expected amplicon sizes for all known markers of detecting vernalization and photoperiod alleles, and (c) an up to date list of QTLs affecting flowering and/or maturity time in wheat.


Flowering Maturity Wheat Vernalization Photoperiod Earliness per se 


  1. Ali ML, Baenziger PS, Ajlouni ZA, Campbell BT, Gill KS, Eskridge KM, Mujeeb-Kazi A, Dweikat I (2011) Mapping QTL for agronomic traits on wheat chromosome 3A and a comparison of recombinant inbred chromosome line populations. Crop Sci 51:553–566Google Scholar
  2. Amir J, Sinclair TR (1991) A model of temperature and solar radiation effects on spring wheat growth and yield. Field Crops Res 28:47–58Google Scholar
  3. Andeden EE, Yediay FE, Baloch FS, Shaaf S, Kilian B, Nachit M, Özkan H (2011) Distribution of vernalization and photoperiod genes (Vrn-A1, Vrn-B1, Vrn-D1, Vrn-B3, Ppd-D1) in Turkish bread wheat cultivars and landraces. Cereal Res Commun 39:352–364Google Scholar
  4. Beales J, Turner A, Griffiths S, Snape JW, Laurie DA (2007) A pseudo-response regulator is mis-expressed in photoperiod insensitive Ppd-D1a mutant of wheat (Triticum aestivum). Theor Appl Genet 115:721–733PubMedGoogle Scholar
  5. Bennett D, Izanloo A, Edwards J, Kuchel H, Chalmers K, Tester M, Reynolds M, Schnurbusch T, Langridge P (2012) Identification of novel quantitative trait loci for days to ear emergence and flag leaf glaucousness in a bread wheat (Triticum aestivum L.) population adapted to southern Australian conditions. Theor Appl Genet 124:697–711PubMedGoogle Scholar
  6. Bentley AR, Turner AS, Gosman N, Leigh FJ, Maccaferri M, Dreisigacker S, Greenland A, Laurie DA (2011) Frequency of photoperiod-insensitive Ppd-A1a alleles in tetraploid, hexaploid and synthetic hexaploid wheat germplasm. Plant Breeding 130:10–15Google Scholar
  7. Berry GJ, Salisbury PA, Halloran GM (1980) Expression of vernalization genes in near-isogenic wheat lines: duration of vernalization period. Ann Bot 46:235–241Google Scholar
  8. Bonnin I, Rousset M, Madur D, Sourdille P, Dupuits C, Brunel D, Goldringer I (2008) FT genome A and D polymorphisms are associated with the variation of earliness components in hexaploid wheat. Theor Appl Genet 116:383–394PubMedGoogle Scholar
  9. Borner A, Korzun V, Worland AJ (1998) Comparative genetic mapping of loci affecting plant height and development in cereals. Euphytica 100:245–248Google Scholar
  10. Börner A, Schumann E, Fürste A, Cöster H, Leithold B, Röder M (2002) Mapping of quantitative trait loci determining agronomic important characters in hexaploid wheat (Triticum aestivum L.). Theor Appl Genet 105:921–936Google Scholar
  11. Briggs WR, Olney MA (2001) Photoreceptors in plant photomorphogenesis to date. Five phytochromes, two cryptochromes, one phototropin, and one superchrome. Plant Physiol 125:85–88PubMedCentralPubMedGoogle Scholar
  12. Brooking IR (1996) Temperature response of vernalization in wheat: a developmental analysis. Ann Bot 78:507–512Google Scholar
  13. Bullrich L, Appendino ML, Tranquilli G, Lewis S, Dubcovsky J (2002) Mapping of a thermo-sensitive earliness per se gene on Triticum monococcum chromosome 1Am. Theor Appl Genet 105:585–593PubMedGoogle Scholar
  14. Busch RH, Elsayed FA, Heiner RE (1984) Effect of daylength insensitivity on agronomic traits and grain protein in hard red spring wheat. Crop Sci 24:1106–1109Google Scholar
  15. Bushuk W (1998) Wheat breeding for end product use. Euphytica 100:137–145Google Scholar
  16. Carter AH, Garland-Campbell K, Kidwell KK (2011) Genetic mapping of quantitative trait loci associated with important agronomic traits in the spring wheat (Triticum aestivum L.) cross ‘Louise’ × ‘Penawawa’. Crop Sci 51:84–95Google Scholar
  17. Cashmore AR, Jarillo JA, Wu YJ, Liu D (1999) Cryptochromes: blue light receptors for plants and animals. Science 284:760–765PubMedGoogle Scholar
  18. Chen F, Gao M, Zhang J, Zuo A, Shang X, Cui D (2013) Molecular characterization of vernalization response genes in bread wheat from the Yellow and Huai Valley of China. BMC Plant Biol 13:199PubMedGoogle Scholar
  19. Chouard P (1960) Vernalization and its relation to dormancy. Annu Rev Plant Physiol 11:191–237Google Scholar
  20. Chu CG, Xu SS, Friesen TL, Faris JD (2008) Whole genome mapping in a wheat doubled haploid population using SSRs and TRAPs and the identification of QTL for agronomic traits. Mol Breed 22:251–266Google Scholar
  21. Cooper JP (1956) Developmental analysis of populations in the cereals and herbage grasses. 1. Methods and techniques. J Agric Sci 47:262–279Google Scholar
  22. Curtis BC (2002) Wheat in the world. In: Curtis BC, Rajaram S, Macpherson HG (eds) Bread wheat: improvement and production. FAO, ItalyGoogle Scholar
  23. 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 Physiol 132:1849–1860PubMedCentralPubMedGoogle Scholar
  24. Davidson JL, Christian KR, Jones DB, Bremner PM (1985) Responses of wheat to vernalization and photoperiod. Aust J Agric Res 36:347–359Google Scholar
  25. Devos KM (2005) Updating the ‘crop circle’. Curr Opin Plant Biol 8:155–162PubMedGoogle Scholar
  26. Devos KM, Dolezel J, Feullet C (2009) Genome organization and comparative genomics. In: Carver BF (ed) Wheat: science and trade. Wiley Blackwell, Danvers, pp 327–368Google Scholar
  27. Diallo AO, Ali-Benali MA, Badawi M, Houde M, Sarhan F (2012) Expression of vernalization responsive genes in wheat is associated with histone H3 trimethylation. Mol Genet Genomics 287:575–590PubMedGoogle Scholar
  28. Distelfeld A, Li C, Dubcovsky J (2009a) Regulation of flowering in temperate cereals. Curr Opin Plant Biol 12:178–184Google Scholar
  29. Distelfeld A, Tranquilli G, Li C, Yan L, Dubcovsky J (2009b) Genetic and Molecular Characterization of the VRN2 Loci in Tetraploid Wheat. Plant Physiol 149:245–257Google Scholar
  30. Dubcovsky J, Lijavetzky D, Appendino L, Tranquilli G, Dvorak JD (1998) Comparative RFLP mapping of Triticum monococcum genes controlling vernalization requirement. Theor Appl Genet 97:968–975Google Scholar
  31. Dubcovsky J, Chen C, Yan L (2005) Molecular characterization of the allelic variation at the VRN-H2 vernalization locus in barley. Mol Breed 15:395–407Google Scholar
  32. Dvorak J, Zhang HB (1990) Variation in repeated nucleotide sequences sheds light on the phylogeny of the wheat B and G genomes. Proc Natl Acad Sci USA 87:9640–9644PubMedCentralPubMedGoogle Scholar
  33. Dvorak J, Di Terlizzi P, Zhang HB, Resta P (1993) The evolution of polyploid wheats: identification of the A genome donor species. Genome 36:21–31PubMedGoogle Scholar
  34. Dyck JA, Matus-Cádiz MA, Hucl P, Talbert L, Hunt T, Dubuc JP, Nass H, Clayton G, Dobb J, Quick J (2004) Agronomic performance of hard red spring wheat isolines sensitive and insensitive to photoperiod. Crop Sci 44:1976–1981Google Scholar
  35. FAO (2009) FAOSTAT database. Agricultural crops: wheat: area harvested/yield.
  36. Ferrándiz C, Gu Q, Martienssen R, Yanofsky MF (2000) Redundant regulation of meristem identity and plant architecture by FRUITFULL, APETALA1 and CAULIFLOWER. Development 127:725–734PubMedGoogle Scholar
  37. Flood RG, Halloran GM (1986a) The influence of genes for vernalization response on development and growth in wheat. Ann Bot 58:505–513Google Scholar
  38. Flood RG, Halloran GM (1986b) Genetics and physiology of vernalization response in wheat. Adv Agron 39:87–125Google Scholar
  39. Ford MA, Austin RB, Angus WJ, Sage GCM (1981) Relationship between the responses of spring wheat genotypes to temperature and photoperiodic treatments and their performance in the field. J Agric Sci 96:623–634Google Scholar
  40. Fosket DE (1994) Plant growth & development, a molecular approach. Academic Press, San DiegoGoogle Scholar
  41. Foulkes MJ, Sylvester-Bradley R, Worland AJ, Snape JW (2004) Effect of a photoperiod response gene Ppd-D1 on yield potential and drought resistance in UK winter wheat. Euphytica 135:63–73Google Scholar
  42. Fu D, Szűcs P, Yan L, Helguera M, Skinner JS, von Zitzewitz J, Hays PM, Dubcovsky J (2005) Large deletions within the first intron in VRN-1 are associated with spring growth habit in barley and wheat. Mol Genet Genomics 273:54–65PubMedGoogle Scholar
  43. Goncharov NP (1998) Genetic resources of wheat related species: the Vrn genes controlling growth habit (spring vs winter). Euphytica 100:371–376Google Scholar
  44. Goncharov NP (2004) Response to vernalization in wheat: its quantitative or qualitative nature. Cereal Res Commun 32:323–330Google Scholar
  45. Goncharov NP, Shitova IP (1999) The inheritance of growth habit in old local varieties and landraces of hexaploid wheat. Genetika (Russian) 35:386–392Google Scholar
  46. Gonzalez FG, Slafer GA, Miralles DJ (2002) Vernalization and photoperiod responses during wheat pre-flowering reproductive phases. Field Crops Res 74:183–195Google Scholar
  47. Gonzalez FG, Slafer GA, Miralles DJ (2003a) Grain and floret numbering response to photoperiod during stem elongation in fully and slightly vernalized wheats. Field Crops Res 81:17–27Google Scholar
  48. Gonzalez FG, Slafer GA, Miralles DJ (2003b) Floret development and spike growth as affected by photoperiod during stem elongation in wheat. Field Crops Res 81:29–38Google Scholar
  49. Gororo NN, Flood RG, Eastwood RF, Eagles HA (2001) Photoperiod and vernalization responses in T. turgidum × T. tauschii synthetic hexaploid wheats. Ann Bot (Lond) 88:947–952Google Scholar
  50. Gotoh T (1979) Genetic studies on growth habit of some important spring wheat cultivars in Japan, with special reference to the identification of the spring genes involved. Jpn J Breed 29:133–145Google Scholar
  51. Griffiths S, Simmonds J, Leverington M, Wang Y, Fish L, Sayers L, Alibert L, Orford S, Wingen L, Herry L, Faure S, Laurie D, Bilham L, Snape J (2009) Meta-QTL analysis of the genetic control of ear emergence in elite European winter wheat germplasm. Theor Appl Genet 119:383–395PubMedGoogle Scholar
  52. Gustafson PO, Raskina O, Ma X, Nevo E (2009) Wheat evolution, domestication and improvement. In: Carver BF (ed) Wheat: science and trade. Wiley Blackwell, Danvers, pp 5–30Google Scholar
  53. Halloran GM (1975) Genotype differences in photoperiodic sensitivity and vernalization response in wheat. Ann Bot 39:845–851Google Scholar
  54. Hanocq E, Niarquin M, Heumez E, Rousset M, Le Gouis J (2004) Detection and mapping of QTL for earliness components in a bread wheat recombinant inbred lines population. Theor Appl Genet 110:106–115PubMedGoogle Scholar
  55. Hanocq E, Laperche A, Jaminon O, Laine AL, Le Gouis J (2007) Most significant genome regions involved in the control of earliness traits in bread wheat, as revealed by QTL meta-analysis. Theor Appl Genet 114:569–584PubMedGoogle Scholar
  56. Hay RKM, Kirby EJM (1991) Convergence and synchrony: a review of the coordination of development in wheat. Aust J Agric Res 42:661–700Google Scholar
  57. Herndl M, White JW, Graef S, Claupein W (2008) The impact of vernalization requirement, photoperiod sensitivity and earliness per se on grain protein content of bread wheat (Triticum aestivum L.). Euphytica 163:309–320Google Scholar
  58. Hoogendoorn J (1985) A reciprocal F1 monosomic analysis of the genetic control of time of ear emergence, number of leaves and number of spikelets in wheat (Triticum aestivum L.). Euphytica 34:545–558Google Scholar
  59. Huang XQ, Cloutier S, Lycar L, Radovanovic N, Humphreys DG, Noll JS, Somers DJ, Brown PD (2006) Molecular detection of QTLs for agronomic and quality traits in a doubled haploid population derived from two Canadian wheats (Triticum aestivum L.). Theor Appl Genet 113:753–766PubMedGoogle Scholar
  60. Hunt LA (1979) Photoperiodic responses of winter wheats from different climatic regions. J Plant Breed 82:70–80Google Scholar
  61. Iqbal M, Navabi A, Salmon DF, Yang R-C, Spaner D (2006) A genetic examination of early flowering and maturity in Canadian spring wheats. Can J Plant Sci 86:995–1004Google Scholar
  62. Iqbal M, Navabi A, Yang R-C, Salmon DF, Spaner D (2007) Molecular characterization of vernalization response genes in Canadian spring wheat. Genome 50:511–516PubMedGoogle Scholar
  63. Iqbal M, Shahzad A, Ahmed I (2011) Allelic variation at the Vrn-A1, Vrn-B1, Vrn-D1, Vrn-B3 and Ppd-D1a loci of Pakistani spring wheat cultivars. Electron J Biotechnol 14. doi: 10.2225/vol14-issue1-fulltext-6
  64. Iwaki K, Nakagawa K, Kuno H, Kato K (2000) Ecogeo-graphical differentiation in East Asian wheat, revealed from the geographical variation of growth habit and Vrn genotype. Euphytica 111:137–143Google Scholar
  65. Iwaki K, Haruna S, Niwa T, Kato K (2001) Adaptation and ecological differentiation in wheat with special reference to geographical variation of growth habit and Vrn genotype. Plant Breeding 120:107–114Google Scholar
  66. Jedel PE, Evans LE, Scarth R (1986) Vernalization responses of a selected group of spring wheats (Tritium aestivum L.) cultivars. Can J Plant Sci 66:1–9Google Scholar
  67. Kamran A, Randhawa HS, Pozniak C, Spaner D (2013a) Phenotypic effects of the flowering gene complex in Canadian spring wheat germplasm. Crop Sci 53:84–94Google Scholar
  68. Kamran A, Iqbal M, Navabi A, Randhawa HS, Pozniak C, Spaner D (2013b) Earliness per QTLs and their interaction with photoperiod insensitive allele Ppd-D1a in Cutler × AC Barrie spring wheat population. Theor Appl Genet 126:1965–1976PubMedGoogle Scholar
  69. Kato K, Wada T (1999) Genetic analysis and selection experiment for narrow-sense earliness in wheat by using segregating hybrid progenies. Breed Sci 49:233–238Google Scholar
  70. Kato K, Miura H, Akiyama M, Kuroshima M, Sawada S (1998) RFLP mapping of the three major genes, Vrn-A1, Q and B1, on the long arm of chromosome 5A of wheat. Euphytica 101:91–95Google Scholar
  71. Kato K, Miura H, Sawada S (1999a) Detection of an earliness per se quantitative trait locus in the proximal region of wheat chromosome 5AL. Plant Breeding 118:391–394Google Scholar
  72. Kato K, Miura H, Sawada S (1999b) QTL mapping of genes controlling ear emergence time and plant height on chromosome 5A of wheat. Theor Appl Genet 98:472–477Google Scholar
  73. Kato K, Taketa S, Ban T, Iriki N, Miura K (2001) The influence of a spring habit gene, Vrn-D1, on heading time in wheat. Plant Breeding 120:115–120Google Scholar
  74. Kato K, Yamashita M, Ishimoto K, Yoshino H, Fujita M (2003) Genetic analysis of two genes for vernalization response, the former Vrn2 and Vrn4, by using PCR based molecular markers. In: Pogna NE, Romano M, Pogna EA, Galterio G (eds) Proceedings of the 10th international wheat genetics symposium. Instituto Sperimentale per la Cerealicoltura, Paestum, vol 3, pp 971–973Google Scholar
  75. Khlestkina EK, Giura A, Roder MS, Borner A (2009) A new gene controlling the flowering response to photoperiod in wheat. Euphytica 165:579–585Google Scholar
  76. Kirby EJM (1988) Analysis of leaf, stem and ear growth in wheat from terminal spikelet stage to anthesis. Field Crops Res 18:127–140Google Scholar
  77. Kirby EJM (1990) Co-ordination of leaf emergence and leaf and spikelet primordium initiation in wheat. Field Crops Res 25:253–264Google Scholar
  78. Klaimi YY, Qualset CO (1974) Genetics of time of heading in wheat (Triticum aestivum L.) II. The inheritance of vernalization response. Genetics 76:119–133PubMedCentralPubMedGoogle Scholar
  79. Knott DR (1986) Effects of genes for photoperiodism, semi-dwarfism, and awns on agronomic characters in a wheat cross. Crop Sci 26:1158–1162Google Scholar
  80. Kosner J, Pankova K (1998) The detection of allelic variants at the recessive vrn loci of winter wheat. Euphytica 101:9–16Google Scholar
  81. Kosner J, Zurkova D (1996) Photoperiodic response and its relation to earliness in wheat. Euphytica 89:59–64Google Scholar
  82. Kulwal PL, Roy JK, Balyan HS (2003) QTL mapping for growth and leaf characters in bread wheat. Plant Sci 164:267–277Google Scholar
  83. Kuspira J, Maclagan J, Kirby K, Bhambhani RN (1986) Genetic and cytogenetic analyses of the A genome of Triticum monococcum L. II. The mode of inheritance of spring versus winter growth habit. Can J Genet Cytol 28:88–95Google Scholar
  84. Laurie DA, Pratchett N, Bezant JH, Snape JW (1995) RFLP mapping of five major genes and eight quantitative trait loci controlling flowering time in a winter 9 spring barley (Hordeum vulgare L) cross. Genome 38:575–585PubMedGoogle Scholar
  85. Law CN, Worland AJ (1997) Genetic analysis of some flowering time and adaptive traits in wheat. New Phytol 137:19–28Google Scholar
  86. Law CN, Worland AJ, Giorgi B (1976) The genetic control of ear emergence time by chromosomes 5A and 5D of wheat. Heredity 36:49–58Google Scholar
  87. Law CN, Sutka J, Worland AJ (1978) A genetic study of day length response in wheat. Heredity 41:575–585Google Scholar
  88. Law CN, Suarez E, Miller TE, Worland AJ (1998) The influence of the group 1 chromosomes of wheat on ear-emergence times and their involvement with vernalization and day length. Heredity 41:185–191Google Scholar
  89. Leonova I, Pestsova E, Salina E, Efremova T, Roder M, Borner A (2003) Mapping of the Vrn-B1 gene in Triticum aestivum using microsatellite markers. Plant Breeding 122:209–212Google Scholar
  90. Levy J, Peterson ML (1972) Responses of spring wheats to vernalization and photoperiod. Crop Sci 12:487–490Google Scholar
  91. Lewis S, Faricelli ME, Appendino ML, Valarik M, Dubcovsky J (2008) The chromosome region including the earliness per se locus Eps-Am1 affects the duration of early developmental phases and spikelet number in diploid wheat. J Exp Bot 59:3595–3607PubMedCentralPubMedGoogle Scholar
  92. Li C, Dubcovsky J (2008) Wheat FT protein regulates VRN1 transcription through interactions with FDL2. Plant J 55:543–554PubMedGoogle Scholar
  93. Lin F, Xue DG, Tian CJ, Cao Y, Zhang ZZ, Zhang ZQ, Ma ZQ (2008) Mapping chromosomal regions affecting flowering time in a spring wheat RIL population. Euphytica 164:768–777Google Scholar
  94. Loukoianov A, Yan L, Blechl A, Sanchez A, Dubcovsky J (2005) Regulation of VRN-1 vernalization genes in normal and transgenic polyploid wheat. Plant Physiol 138:2364–2373PubMedCentralPubMedGoogle Scholar
  95. Maccaferri M, Sanguineti MC, Corneti S, Ortega JLA, Salem MB, Bort J, DeAmbrogio E, del Moral LFG, Demontis A, El-Ahmed A, Maalouf F, Machlab H, Martos V, Moragues M, Motawaj J, Nachit M, Nserallah N, Ouabbou H, Royo C, Slama A, Tuberosa R (2008) Quantitative trait loci for grain yield and adaptation of durum wheat (Triticum durum Desf.) across a wide range of water availability. Genetics 178:489–511PubMedCentralPubMedGoogle Scholar
  96. 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 Organ Cult 41:285–288Google Scholar
  97. Marshall L, Busch R, Cholick F, Edwards I, Frohberg R (1989) Agronomic performance of spring wheat isolines differing for day length response. Crop Sci 29:752–757Google Scholar
  98. Martinic ZF (1975) Life cycle of common wheat varieties in natural environments as related to their response to shortened photoperiod. J Plant Breed 75:237–251Google Scholar
  99. McIntosh RA, Devos KM, Dubcovsky J, Rogers WJ, Morris CF, Appels R, Sommers DJ Anderson OA (2007) Catalogue of gene symbols for wheat (supplement). USDA-ARS, Washington, DC.
  100. Miglietta F (1989) Effect of photoperiod and temperature on leaf initiation rates in wheat (Triticum spp.). Field Crops Res 21:121–130Google Scholar
  101. Milec Z, Tomková L, Sumíková T, Pánková K (2012) A new multiplex PCR test for the determination of Vrn-B1 alleles in bread wheat (Triticum aestivum L.). Mol Breed 30:317–323Google Scholar
  102. Milec Z, Sumíková T, Tomkova L, Pánková K (2013) Distribution of different Vrn-B1 alleles in hexaploid spring wheat germplasm. Euphytica 192:371–378Google Scholar
  103. Miralles DJ, Richards RA (2000) Responses of leaf and tiller emergence and primordium initiation in wheat and barley to interchanged photoperiod. Ann Bot 85:655–663Google Scholar
  104. Miralles DJ, Katz SD, Colloca A, Slafer GA (1998) Floret development in near isogenic wheat lines differing in plant height. Field Crops Res 59:21–30Google Scholar
  105. Miralles DJ, Richards RA, Slafer GA (2000) Duration of stem elongation period influences the number of fertile florets in wheat and barley. Aust J Plant Physiol 27:931–941Google Scholar
  106. Miura H, Nakagawa M, Worland AJ (1999) Control of ear emergence time by chromosome 3A of wheat. Plant Breeding 118:85–87Google Scholar
  107. Miura H, Worland AJ (1994) Genetic control of vernalization, day-length response, and earliness per se by homoeologous group-3 chromosomes in wheat. Plant Breeding 113:160–169Google Scholar
  108. Miura H, Parker BB, Snape JW (1992) The location of major genes and associated quantitative trait loci on chromosome arm 5BL of wheat. Theor Appl Genet 85:197–204PubMedGoogle Scholar
  109. Mizuno T (1998) His-Asp phosphotransfer signal transduction. J Biochem 123:555–563PubMedGoogle Scholar
  110. Mizuno T, Nakamichi N (2005) Pseudo-response regulators (PRRs) or true oscillator components (TOCs). Plant Cell Physiol 46:677–685PubMedGoogle Scholar
  111. Moore G (1995) Cereal genome evolution: pastoral pursuits with ‘Lego’ genomes. Curr Opin Genet Dev 5:717–724PubMedGoogle Scholar
  112. 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 44:1255–1265PubMedGoogle Scholar
  113. Naranjo T, Corredor E (2004) Clustering of centromeres precedes bivalent chromosome pairing of polyploidy wheats. Trends Plant Sci 9:214–217PubMedGoogle Scholar
  114. Neff MM, Fankhauser C, Chory J (2000) Light: an indicator of time and place. Genes Dev 14:257–271PubMedGoogle Scholar
  115. 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. Proc Natl Acad Sci USA 106:8386–8391PubMedCentralPubMedGoogle Scholar
  116. Ortiz-Ferrara G, Mosaad MG, Mahalakshmi V, Rajaram S (1998) Photoperiod and vernalization response of Mediterranean wheats, and implications for adaptation. Euphytica 100:377–384Google Scholar
  117. Paterson AH, Bowers JE, Burow MD, Draye X, Elsik CG, Jiang CX, Katsar CS, Lan TH, Lin YR, Ming R, Wright RJ (2000) Comparative genomics of plant chromosomes. Plant Cell 12:1523–1539PubMedCentralPubMedGoogle Scholar
  118. 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 100:355–364Google Scholar
  119. Porter JR, Gawith M (1999) Temperatures and the growth and development of wheat: a review. Eur J Agron 10:23–36Google Scholar
  120. Pugsely AT (1966) The photoperiodic sensitivity of some spring wheats with special reference to the variety Thatcher. Aust J Agric Res 17:591–599Google Scholar
  121. Pugsley AT (1971) A genetic analysis of the spring–winter habit of growth in wheat. Aust J Agric Res 22:21–31Google Scholar
  122. Pugsley AT (1972) Additional genes inhibiting winter habit in wheat. Euphytica 21:547–552Google Scholar
  123. Rahman MS (1980) Effect of photoperiod and vernalization on the rate of development and spikelet number per ear in 30 varieties of wheat. J Aust Inst Agric Sci 46:68–70Google Scholar
  124. Rawson HM, Richards RA (1993) Effects of high temperature and photoperiod on floral development in wheat isolines differing in vernalisation and photoperiod genes. Field Crops Res 32:181–192Google Scholar
  125. Rawson HM, Zajac M, Penrose LDJ (1998) Effect of seedling temperature and its duration on development of wheat cultivars differing in vernalizing response. Field Crops Res 57:289–300Google Scholar
  126. Riley R, Chapman V (1958) Genetic control of the cytologically diploid behavior of hexaploid wheat. Nature 182:713–715Google Scholar
  127. Roberts DWA, Larson RI (1985) Vernalization and photoperiod responses of selected chromosome substitution lines derived from ‘Rescue’, ‘Cadet’ and ‘Cypress’ wheats. Can J Genet Cytol 27:586–591Google Scholar
  128. Santra DK, Santra M, Allan RE, Campbell KG, Kidwell KK (2009) Genetic and molecular characterization of vernalization genes Vrn-A1, Vrn-B1, and Vrn-D1 in spring wheat germplasm from the Pacific Northwest Region of the U.S.A. Plant Breeding 128:576–584Google Scholar
  129. Sarma RN, Fish L, Gill BS, Snape JW (2000) Physical characterization of the homoeologous Group 5 chromosomes of wheat in terms of rice linkage blocks, and physical mapping of some important genes. Genome 43:191–198Google Scholar
  130. Sasani S, Hemming MN, Oliver S, Greenup A, Tavakkol-Afshari R (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). J Exp Bot 60:2169–2178PubMedCentralPubMedGoogle Scholar
  131. Scarth R, Law CN (1983) The location of the photoperiod gene Ppd-B1 and an additional genetic factor for ear emergence time on chromosome 2B of wheat. Heredity 51:607–619Google Scholar
  132. Serrago RA, Miralles DJ, Slafer GA (2008) Floret fertility in wheat as affected by photoperiod during stem elongation and removal of spikelets at booting. Eur J Agron 28:301–308Google Scholar
  133. Shah MM, Gill KS, Yen Y, Kaeppler SM, Ariyarathne HM (1999) Molecular mapping of loci for agronomic traits on chromosome 3A of bread wheat. Crop Sci 39:1728–1732Google Scholar
  134. Shcherban AB, Emtseva MV, Efremova TT (2012) Molecular genetical characterization of vernalization genes Vrn-A1, Vrn-B1 and Vrn-D1 in spring wheat germplasm from Russia and adjacent regions. Cereal Res Commun 40:351–361Google Scholar
  135. Shimada S, Ogawa T, Kitagawa S, Suzuki T, Ikari C, Shitsukawa N, Abe T, Kawahigashi H, Kikuchi R, Handa H (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 58:668–681PubMedCentralPubMedGoogle Scholar
  136. Shindo C, Sasakuma T, Tsujimoto H (2003) Segregation analysis of heading traits in hexaploid wheat utilizing recombinant inbred lines. Heredity 90:56–63PubMedGoogle Scholar
  137. Singh SK, Singh AM, Jain N, Singh GP, Ahlawat AK, Ravi I (2013) Molecular characterization of vernalization and photoperiod genes in wheat varieties from different agro-climatic zones of India. Cereal Res Commun 41: 376–38Google Scholar
  138. Slafer GA (2003) Genetic basis of yield as viewed from a crop physiologist’s perspective. Ann Appl Biol 142:117–128Google Scholar
  139. Slafer GA, Rawson HM (1994) Sensitivity of wheat phasic development to major environmental factors: a re-examination of some assumptions made by physiologists and modelers. Aust J Plant Physiol 21:393–426Google Scholar
  140. Slafer GA, Rawson HM (1995) Photoperiod × temperature interactions in contrasting wheat genotypes: time to heading and final leaf number. Field Crops Res 44:73–83Google Scholar
  141. Slafer GA, Rawson HM (1996) Responses to photoperiod change with phenophase and temperature during wheat development. Field Crops Res 46:1–13Google Scholar
  142. Slafer GA, Calderini DF, Miralles DJ (1996) Yield components and compensation in wheat: opportunities for further increasing yield potential. In: Reynolds MP, Rajaram S, McNab A (eds) Increasing yield potential in wheat: breaking the barriers, CIMMYT, pp 101–133Google Scholar
  143. Slafer GA, Araus JL, Royo C, Garcia del Moral LF (2005) Promising ecophysiological traits for genetic improvement of cereal yields in Mediterranean environments. Ann Appl Biol 146:61–70Google Scholar
  144. Snape JW, Law CN, Parker BB, Worland AJ (1985) Genetical analysis of chromosome 5 A of wheat and its influence on important agronomic characters. Theor Appl Genet 71:518–526PubMedGoogle Scholar
  145. Snape JW, Butterworth K, Whitechurch E, Worland AJ (2001) Waiting for fine times: genetics of flowering time in wheat. Euphytica 119:185–190Google Scholar
  146. Sourdille P, Cadalen T, Guyomarc’h H, Snape JW, Perretant MR, Charmet G, Boeuf C, Bernard S, Bernard M (2003) An update of the Courtot-Chinese Spring intervarietal molecular marker linkage map for the QTL detection of agronomic traits in wheat. Theor Appl Genet 106:530–538PubMedGoogle Scholar
  147. Statistics Canada (2011) Field crop reporting series.
  148. Stelmakh AF (1990) Geographic distribution of Vrn genes in landraces and improved varieties of spring bread wheat. Euphytica 45:113–118Google Scholar
  149. Stelmakh AF (1993) Genetic effect of Vrn genes on heading date and agronomic traits in bread wheat. Euphytica 65:53–60Google Scholar
  150. Stelmakh AF (1998) Genetic systems regulating flowering response in wheat. Euphytica 100:359–369Google Scholar
  151. Streck NA, Weiss A, Baenziger PS (2003) Wheat: a generalized vernalization response function for winter wheat. Agron J 95:155–159Google Scholar
  152. Syme JR (1968) Ear emergence of Australian, Mexican and European wheats in relation to time of sowing and their response to vernalization and day length. Aust J Exp Agric Anim Husb 8:578–581Google Scholar
  153. Takahashi R, Yasuda S (1971) Genetics of earliness and growth habit in barley. In: Nilan RA (ed) Barley genetics II (Proceeding of second international barley genetics symposium). Washington State University Press, Pullman, pp 388–408Google Scholar
  154. Toth B, Galiba G, Fe′her E, Sutka J, Snape JW (2003) Mapping genes affecting flowering time and frost resistance on chromosome 5B of wheat. Theor Appl Genet 107:509–514PubMedGoogle Scholar
  155. Trevaskis B (2010) The central role of the VERNALIZATION1 gene in the vernalization response of cereals. Funct Plant Biol 37:479–487Google Scholar
  156. Trevaskis B, Bagnall DJ, Ellis MH, Peacock WJ, Dennis ES (2003) MADS box genes control vernalization-induced flowering in cereals. Proc Natl Acad Sci 100:13099–13104PubMedCentralPubMedGoogle Scholar
  157. Trevaskis B, Hemming MN, Dennis ES, Peacock WJ (2007) The molecular basis of vernalization-induced flowering in cereals. Trends Plant Sci 12:351–357Google Scholar
  158. Turner A, Beales J, Faure S, Dunford RP, Laurie DA (2005) The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science 310:1031–1034PubMedGoogle Scholar
  159. van Beem J, Mohler V, Lukman R, van Ginkel M, William M, Crossa J, Worland AJ (2005) Analysis of genetic factors influencing the developmental rate of globally important CIMMYT wheat cultivars. Crop Sci 45:2113–2119Google Scholar
  160. Wang E, Engel T (1998) Simulation of phenological development of wheat crops. Agric Syst 58:1–24Google Scholar
  161. Wang SY, Ward RW, Ritchie JT, Fisher RA, Schulthess U (1995a) Vernalization in wheat I. A model based on the interchangeability of plant age and vernalization duration. Field Crops Res 41:91–100Google Scholar
  162. Wang SY, Ward RW, Ritchie JT, Fisher RA, Schulthess U (1995b) Vernalization in wheat I. A model based on interchangeability of plant age and vernalization duration. Field Crops Res 41:91–100Google Scholar
  163. Wang RX, Hai L, Zhang XY, You GX, Yan CS, Xiao SH (2009) QTL mapping for grain filling rate and yield-related traits in RILs of the Chinese winter wheat population Heshangmai × Yu8679. Theor Appl Genet 118:313–325Google Scholar
  164. Whitechurch EM, Slafer GA (2002) Contrasting Ppd alleles in wheat: effects on sensitivity to photoperiod in different phases. Field Crops Res 73:95–105Google Scholar
  165. Whitechurch EM, Snape JW (2003) Developmental responses to vernalization in wheat deletion lines for chromosomes 5A and 5D. Plant Breeding 122:35–39Google Scholar
  166. Wilsie CP (1962) Crop adaptation and distribution. Freeman, San FranciscoGoogle Scholar
  167. Worland AJ (1996) The influence of the flowering time genes on environmental adaptability in European wheats. Euphytica 89:49–57Google Scholar
  168. Worland T, Snape JW (2001) Genetic basis of worldwide wheat varietal improvement. In: Bonjean AP, Angus WJ (eds) The world wheat book: a history of wheat breeding. Intercept Ltd., London, pp 61–67Google Scholar
  169. Worland AJ, Appendino ML, Sayers EJ (1994) The distribution, in European winter wheats, of genes that influence ecoclimatic adaptability whist determining photoperiodic insensitivity and plant height. Euphytica 80:219–228Google Scholar
  170. Worland AJ, Börner A, Korzun V, Li WM, Petrovíc S, Sayers EJ (1998a) The influence of photoperiod genes on the adaptability of European winter wheats. Euphytica 100:385–394Google Scholar
  171. Worland AJ, Korzum V, Röder MS, Ganal MW, Law CN (1998b) Genetic analysis of the dwarfing gene (Rht8) in wheat. Part II. The distribution and adaptive significance of allelic variants at the Rht8 locus of wheat as revealed by microsatellite screening. Theor Appl Genet 96:1110–1120Google Scholar
  172. Yan L, Loukoianov A, Tranquilli G, Helguera M, Fahima T, Dubcovsky J (2003) Positional cloning of wheat vernalization gene VRN1. Proc Natl Acad Sci USA 100:6263–6268PubMedCentralPubMedGoogle Scholar
  173. Yan L, Helguera M, Kato K, Fukuyama S, Sherman J, Dubcovsky J (2004a) Allelic variation at the VRN-1 promoter region in polyploidy wheat. Theor Appl Genet 109:1677–1686PubMedGoogle Scholar
  174. Yan L, Loukoianov A, Blechl A, Tranquilli G, Ramakrishna W, SanMiguel P, Bennetzen JL, Echenique V, Dubcovsky J (2004b) The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science 303:1640–1644PubMedGoogle Scholar
  175. Yan L, Fu D, Li C, Blechl A, Tranquilli G, Bonafede M, Sanchez A, Valarik M, Dubcovsky J (2006) The wheat and barley vernalization gene VRN3 is an orthologue of FT. Proc Natl Acad Sci USA 103:19581–19586PubMedCentralPubMedGoogle Scholar
  176. Yang FP, Zhang XK, Xia XC, Laurie DA, Yang WX, He ZH (2009) Distribution of photoperiod insensitive Ppd-D1a allele in Chinese wheat cultivars. Euphytica 165:445–452Google Scholar
  177. Yoshida T, Nishida H, Zhu J, Nitcher R, Distelfeld A, Akashi Y, Kato K, Dubcovsky J (2010) Vrn-D4 is a vernalization gene located on the centromeric region of chromosome 5D in hexaploid wheat. Theor Appl Genet 120:543–552PubMedGoogle Scholar
  178. Zadoks JC, Chang TT, Konzak CF (1974) A decimal code for the growth stages of cereals. Weed Res 14:415–421Google Scholar
  179. Zhang XK, Xiao YG, Zhang Y, Xia XC, Dubcovsky J, He ZH (2008) Allelic variation at the vernalization genes Vrn-A1, Vrn-B1, Vrn-D1, and Vrn-B3 in Chinese wheat cultivars and their association with growth habit. Crop Sci 48:458–470Google Scholar
  180. Zhang K, Tian J, Zhao L, Liu B, Chen G (2009) Detection of quantitative trait loci for heading date based on the doubled haploid progeny of two elite Chinese wheat cultivars. Genetica 135:257–265Google Scholar
  181. Zhang J, Wang Y, Wu S, Yang J, Liu H, Zhou Y (2012) A single nucleotide polymorphism at the Vrn-D1 promoter region in common wheat is associated with vernalization response. Theor Appl Genet 125:1697–1704PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  1. 1.Department of Agricultural Food and Nutritional ScienceUniversity of AlbertaEdmontonCanada
  2. 2.Seed Centre, Department of BotanyUniversity of the PunjabLahorePakistan
  3. 3.National Institute for Genomics & Advanced BiotechnologyNational Agricultural Research CentreIslamabadPakistan

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