Abstract
The transition from vegetative to floral meristems in higher plants is determined by the coincidence of internal and environmental signals. Contrary to the photoperiod pathway, convergent evolution of the cold-dependent pathway has implicated different genes between dicots and monocots. Whereas no association between natural variation in vernalization requirement and Flowering time locus T (FT) gene polymorphism has been described in Arabidopsis, recent studies in Triticeae suggest implication of orthologous copies of FT in the cold response. In our study, we show that nucleotide polymorphisms on A and D copies of the wheat FT gene were associated with variations for heading date in a collection of 239 lines representing diverse geographical origins and status (landraces, old or recent cultivars). Interestingly, polymorphisms in the non-coding intronic region were strongly associated to flowering variation observed on plants grown without vernalization. But differently from VRN1, no epistatic interaction between FT homeologous copies was revealed. In agreement with the results of association study, the A and D copies of FT were mapped in regions including major QTLs for earliness traits in hexaploid wheat. This work, by identifying additional homeoalleles involved in wheat vernalization pathway, will contribute to a better understanding of the control of flowering, hence providing tools for the breeding of varieties with enhanced adaptation to changing environments.
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References
Ahmed TA, Tsujimoto H, Sasakuma T (2000) Identification of RFLP markers linked with heading date and its heterosis in hexaploid wheat. Euphytica 116:111–119
Ahn JH, Miller D, Winter VJ, Banfield MJ, Lee JH, Yoo SY, Henz SR, Brady RL, Weigel D (2006) A divergent external loop confers antagonistic activity on floral regulators FT and TFL1. EMBO J 25:605–614
Andersen JR, Jensen LB, Asp T, Lübberstedt T (2006) Vernalization response in perennial ryegrass (Lolium perenne L.) involves orthologues of diploid wheat (Triticum monococcum) VRN1 and rice (Oryza sativa) Hd1. Plant Mol Biol 60:481–494
Ausin I, Alonso-Blanco C, Martinez-Zapater JM (2005) Environmental regulation of flowering. Int J Dev Biol 49:689–705
Badiani K, Arthur G (1995) Evidence for receptor and G-protein regulation of a phosphatidylethanolamine-hydrolysing phospholipase A1 in guinea-pig heart microsomes: stimulation of phospholipase A1 activity by DL-isoprenaline and guanine nucleotides. Biochem J 312:805–809
Bernier G, Périlleux C (2005) A physiological overview of the genetics of flowering time control. Plant Biotechnol J 3:3–16
Breseghello F, Sorrells ME (2006) Association mapping of kernel size and milling quality in wheat (Triticum aestivum L.) cultivars. Genetics 172:1165–1177
Börner A, Schumann E, Fürste A, Cöster H, Leithold B, Röder MS, Weber WE (2002) Mapping of quantitative trait loci determining agronomic important characters in hexaploid wheat (Triticum aestivum L.). Theor Appl Genet 105:921–936
Cadalen T, Boeuf C, Bernard S, Bernard M (1997) An intervarietal molecular marker map in Triticum aestivum L. em. Thell. and comparison with a map from a wide cross. Theor Appl Genet 94:367–377
Carmona MJ, Calonje M, Martinez-Zapater JM (2006) The FT/TFL1 gene family in grapevine. Plant Mol Biol. doi:10.1007/s11103-006-9113-z
Chao S, Zhang W, Dubcovsky J, Sorrells M (2007) Evaluation of genetic diversity and genome-wide linkage disequilibrium among U.S. wheat (Triticum aestivum L.) germplasm representing different market classes. Crop Sci 47:1018–1030
Chautard H, Jacquet M, Schoentgen F, Bureaud N, Bénédetti H (2004) Tfs1p, a member of the PEBP Family, inhibits the Ira2p but not the Ira1p Ras GTPase-activating protein in Saccharomyces cerevisiae. Eukaryot Cell 3:459–470
Ciaffi M, Paolacci AR, D’Aloisio E, Tanzarella OA, Porceddu E (2005) Identification and characterization of gene sequences expressed in wheat spikelets at the heading stage. Gene 346:221–230
Dubcovsky J, Chen C, Yan L (2005) Molecular characterization of the allelic variation at the VRN-H2 vernalization locus in barley. Mol Breed 15:395–407
Fu D, Szucs P, Yan L, Helguera M, Skinner JS, von Zitzewitz J, Hayes PM, Dubcovsky J (2005) Large deletions within the first intron of VRN-1 are associated with spring growth habit in barley and wheat. Mol Gen Genom 273:54–65
Gervais L, Dedryver F, Morlais JY, Bodusseau, Negre S, Bilous M, Groos C, Trottet M (2003) Mapping of quantitative trait loci for field resistance to Fusarium head blight in an European winter wheat. Theor Appl Genet 106:961–970
Goldringer I, Prouin C, Rousset M, Galic N, Bonnin I (2006) Rapid differentiation of experimental populations of wheat for heading time in response to local climatic conditions. Ann Bot 98:805–817
Hanocq E, Niarquin M, Heumez E, Rousset M, Legouis J (2004) Detection and mapping of QTL for earliness components in a bread wheat recombinant inbred lines population. Theor Appl Genet 110:106–115
Hanocq E, Laperche A, Jaminon O, Lainé AL, Legouis 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(3):569–584
Hanzawa Y, Money T, Bradley D (2005) A single amino acid converts a repressor to an activator of flowering. PNAS 102:7748–7753
Haudry A, Cenci A, Ravel C, Bataillon T, Brunel D, Poncet C, Hochu I, Poirier S, Santoni S, Glémin S, David J (2007) Grinding up wheat: a massive loss of nucleotide diversity since domestication. Mol Biol Evol 24(7):1506–1517
Hecht V, Foucher F, Ferrandiz C, Macknight R, Navarro C, Morin J, Vardy ME, Ellis N, Beltran JP, Rameau C, Weller JL (2005) Conservation of Arabidopsis flowering genes in model legumes. Plant Physiol 137:1420–1434
Hedrick PW (1980) Hitchhiking: a comparison of linkage and partial selfing. Genetics 94:791–808
Hsu CY, Liu Y, Luthe DS, Yuceer C (2006) Poplar FT2 shortens the juvenile phase and promotes seasonal flowering. Plant Cell 18:1846–1861
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 113:753–766
Kojima S, Takahashi Y, Kobayashi Y, Monna L, Sasaki T, Araki T, Yano M (2002) Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions. Plant Cell Physiol 43:1096–1105
Koornneef M, Hanhart CJ, van der Veen JH (1991) A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Mol Gen Genet 229:57–66
Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175
Kuchel H, Hollamby G, Landridge P, Williams K, Jefferies SP (2006) Identification of genetic loci associated with ear-emergence in bread wheat. Theor Appl Genet 113:1103–1112
Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163
Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newburg L (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181
Laurie DA, Griffiths S, Dunford RP, Christodoulou V, Taylor SA, Cockram J, Beales J, Turner A (2004) Comparative genetic approaches to the identification of flowering time genes in temperate cereals. Field Crops Res 90:87–99
Law CN (1966) The location of genetic factors affecting a quantitative character in wheat. Genetics 53:487–498
Law CN, Worland AJ (1997) Genetic analysis of some flowering time and adaptative traits in wheat. New Phytol 137:19–28
Nei M (1987) Molecular evolutionary genetics, Columbia University Press, New York
Quarrie SA, Pekic Quarrie S, Radosevic R, Rancic D, Kaminska A, Barnes JD, Leverington M, Ceoloni C, Dodig D (2006) Dissecting a wheat QTL for yield present in a range of environments: from the QTL to candidate genes. J Exp Bot 57(11):2627–2637
Ravel C, Praud S, Murigneux A, Canaguier A, Sapet F, Samson D, Balfourier F, Dufour P, Chalhoub B, Brunel D, Beckert M, Charmet G (2006a) Single-nucleotide polymorphism frequency in a set of selected lines of bread wheat (Triticum aestivum L.). Genome 49:1131–1139
Ravel C, Praud S, Murigneux A, Linossier L, Dardevet M, Balfourier F, Dufour P, Brunel D, Charmet G (2006b) Identification of Glu-B1-1 as a candidate gene for the quantity of high-molecular-weight glutenin in bread wheat (Triticum aestivum L.) by means of an association study. Theor Appl Genet 112:738–743
Rogers SO, Bendich AJ (1985) Extraction of DNA from milligram amounts of fresh, herbarium, and mummified plant tissues. Plant Mol Biol 5:69–76
Rost B, Yachdav G, Liu J (2003) The PredictProtein server. Nucleic Acids Res 32(Web Server issue):W321–W326
Roussel V, Koenig J, Beckert M, Balfourier F (2004) Molecular diversity in French bread wheat accessions related to temporal trends and breeding programmes. Theor Appl Genet 108:920–930
Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497
Samach A, Onouchi H, Gold SE, Ditta GS, Schwarz-Sommer Z, Yanofsky MF, Coupland G (2000) Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288:1613–1616
SAS Institute (2000) SAS/STAT User Guide, Version 8. SAS Publishing, Cary
Schleiff E, Soll J (2005) Membrane protein insertion: mixing eukaryotic and prokaryotic concepts. EMBO 6:1023–1027
Schmolke M, Zimmermann G, Buerstmayr H, Schweizer, Miedaner T, Korzun V, Ebmeyer E, Hartl L (2005) Molecular mapping of Fusarium head blight resistance in the winter wheat population Dream/Lynx. Theor Appl Genet 111:747–756
Shindo C, Tsujimoto, Sasakuma T (2003) Segregation analysis of heading traits in hexaploid wheat utilizing recombinant inbred lines. Heredity 90:56–63
Somers DJ, Isaac P, Edwards K (2004) A high-density microsatellite consensus map for bread wheat (Triticum aestivum L.). Theor Appl Genet 109:1105–1114
Somers DJ, Banks T, DePauw R, Fox S, Clarke J, Pozniak C, McCartney C (2007) Genome-wide linkage disequilibrium analysis in bread wheat and durum wheat. Genome 50:557–567
Sourdille P, Snape JW, Cadalen T, Charmet G, Nakata N, Bernard S, Bernard M (2000) Detection of QTLs for heading time and photoperiod response in wheat using a doubled-haploid population. Genome 43:487–494
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 QTL detection of agronomic traits in wheat. Theor Appl Genet 106:530–538
Sourdille P, Singh S, Cadalen T, Brown-Guedira GL, Gay G, Qi L, Gill BS, Dufour P, Murigneux A, Bernard M (2004) Microsatellite-based deletion mapping system for the establishment of genetic map—physical map relationships in wheat. Funct Integr Genomics 4:12–25
Staden R, Beal KF, Bonfield JK (2000) The Staden package, 1998. Methods Mol Biol 132:115–130
Suarez-Lopez 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
Tang H, Peng J, Wang P, Risch NJ (2005) Estimation of individual admixture: analytical and study design considerations. Genet Epidemiol 28:289–301
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
Worland AJ (1996) The influence of flowering time genes on environmental adaptability in European wheats. Euphytica 89:49–57
Yan L, Loukoianov A, Tranquilli G, Helguera M, Fahima T, Dubcovsky J (2003) Positional cloning of the wheat vernalization gene VRN1. PNAS 100:6263–6268
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
Yan L, Helguera M, Kato K, Fukuyama S, Sherman J, Dubcovsky J (2004b) Allelic variation at the VRN-1 promoter region in polyploid wheat. Theor Appl Genet 109:677–1686
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. PNAS 103:19581–19586
Yang W, Mason C, Pollock S, Lavezzi T, Moroney J, Moore T (2004) Membrane lipid biosynthesis in Chlamydomonas reinhardtii: expression and characterization of CTP phosphoethanolamine cytidylyltransferase. Biochem J 382:51–57
Acknowledgments
The authors would like to thank C. Ridel, S. Mezi, F. Dumas, N. Galic, and M. T. Marcombes for their technical assistance. This work was supported by a French German Gabi-Génoplante project entitled “Bridging genomics and genetic diversity: associations between gene polymorphism and trait variation in cereals”.
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Communicated by M. Morgante.
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Bonnin, I., Rousset, M., Madur, D. et al. FT genome A and D polymorphisms are associated with the variation of earliness components in hexaploid wheat. Theor Appl Genet 116, 383–394 (2008). https://doi.org/10.1007/s00122-007-0676-0
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DOI: https://doi.org/10.1007/s00122-007-0676-0