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Detection of QTLs for flowering date in three mapping populations of the model legume species Medicago truncatula

Theoretical and Applied Genetics volume 117, pages 609–620 (2008)Cite this article

Abstract

Adaptation to the environment and reproduction are dependent on the date of flowering in the season. The objectives of this paper were to evaluate the effect of photoperiod on flowering date of the model species for legume crops, Medicago truncatula and to describe genetic architecture of this trait in multiple mapping populations. The effect of photoperiod (12 and 18 h) was analysed on eight lines. Quantitative variation in three recombinant inbred lines (RILs) populations involving four parental lines was evaluated, and QTL detection was carried out. Flowering occurred earlier in long than in short photoperiods. Modelling the rate of progression to flowering with temperature and photoperiod gave high R², with line-specific parameters that indicated differential responses of the lines to both photoperiod and temperature. QTL detection showed a QTL on chromosome 7 that was common to all populations and seasons. Taking advantage of the multiple mapping populations, it was condensed into a single QTL with a support interval of only 0.9 cM. In a bioanalysis, six candidate genes were identified in this interval. This design also indicated other genomic regions that were involved in flowering date variation more specifically in one population or one season. The analysis on three different mapping populations detected more QTLs than on a single population, revealed more alleles and gave a more precise position of the QTLs that were common to several populations and/or seasons. Identification of candidate genes was a result of integration of QTL analysis and genomics in M. truncatula.

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References

  • 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

    PubMed  Article  CAS  Google Scholar 

  • Aitken Y (1955) Flower initiation in pasture legumes. I. Factors affecting flower initiation in Trifolium subterraneum. Aust J Agric Res 26:212–244

    Google Scholar 

  • Arcade A, Labourdette A, Falque M, Mangin B, Chardon F, Charcosset A, Joets J (2004) BioMercator: integrating genetic maps and QTL towards discovery of candidate genes. Bioinformatics 20:2324–2326

    PubMed  Article  CAS  Google Scholar 

  • Aubert G, Morin J, Jacquin F, Loridon K, Quillet MC, Petit A, Rameau C, Lejeune-Henaut I, Huguet T, Burstin J (2006) Functional mapping in pea, as an aid to the candidate gene selection and for investigating synteny with the model legume Medicago truncatula. Theor Appl Genet 112:1024–1041

    PubMed  Article  CAS  Google Scholar 

  • Aydi S, Drevon JJ, Abdelly C (2004) Effect of salinity on root-nodule conductance to the oxygen diffusion in the Medicago truncatula-Sinorhibobium meliloti symbiosis. Plant Physiol Biochem 42:833–840

    PubMed  Article  CAS  Google Scholar 

  • Basten CJ, Weir BS, Zeng ZB (1994) Zmap—a QTL cartographer. Guelph, Ontario, pp 65–66

    Google Scholar 

  • Basten CJ, Weir BS, Zeng ZB (2002) QTL Cartographer, Version 1.16 North Carolina State University, Department of Statistics, Raleigh, NC

  • Baurle I, Dean C (2006) The timing of developmental transitions in plants. Cell 125:655–664

    PubMed  Article  CAS  Google Scholar 

  • Bell CJ, Dixon RA, Farmer AD, Flores R, Inman J, Gonzales RA, Harrison MJ, Paiva NL, Scott AD, Weller JW, May GD (2001) The Medicago Genome initiative: a model legume database. Nucleic Acids Res 29:114–117

    PubMed  Article  CAS  Google Scholar 

  • Beveridge CA, Murfet IC (1996) The gigas mutant in pea is deficient in the floral stimulus. Physiol Plant 96:637–645

    Article  CAS  Google Scholar 

  • Blanc G, Charcosset A, Mangin B, Gallais A, Moreau L (2006) Connected populations for detecting quantitative trait loci and testing for epistasis: an application in maize. Theor Appl Genet 113:206–224

    PubMed  Article  CAS  Google Scholar 

  • Blazquez MA (2005) The right time and place for making flowers. Science 309:1024–1025

    PubMed  Article  Google Scholar 

  • Blondon F, Marie D, Brown S, Kondorosi A (1994) Genome size and base composition in Medicago sativa and M. truncatula species. Genome 37:264–270

    PubMed  Article  CAS  Google Scholar 

  • Chabaud M, Lichtenzveig J, Ellwood S, Pfaff T, Journet EP (2006) Vernalization, crossings and testing for pollen variability. http://www.noble.org/MedicagoHandbook/pdf/Vernalization.pdf

  • Chardon F, Virlon B, Moreau L, Falque M, Joets J, Decousset L, Murigneux A, Charcosset A (2004) Genetic architecture of flowering time in maize as inferred from quantitative trait loci meta-analysis and synteny conservation with the rice genome. Genetics 168:2169–2185

    PubMed  Article  CAS  Google Scholar 

  • Choi HK, Kim D, Uhm T, Limpens E, Lim H, Mun JH, Kaló P, Penmetsa RV, Seres A, Kulikova O, Roe BA, Bisseling T, Kiss GB, Cook DR (2004a) A sequence-based genetic map of Medicago truncatula and comparison of marker colinearity with M. sativa. Genetics 166:1463–1502

    PubMed  Article  CAS  Google Scholar 

  • Choi HK, Mun JH, Kim DJ, Zhu H, Baek JM, Mudge J, Roe B, Ellis N, Doyle J, Kiss GB, Young ND, Cook DR (2004b) Estimating genome conservation between crop and model legume species. Proc Natl Acad Sci USA 101:15289–15294

    PubMed  Article  CAS  Google Scholar 

  • Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971

    PubMed  CAS  Google Scholar 

  • Clarkson NM, Russell JS (1975) Flowering responses to vernalization and photoperiod in annual medics (Medicago ssp.). Aust J Agric Res 26:831–838

    Article  Google Scholar 

  • Delalande M, Ronfort J, Prosperi JM (2004) Diversity for flowering time in a large collection of Medicago truncatula Gaertn. Québec, http://www.naaic.org/Meetings/National/2004NAAIC&TC/2004abstracts/jprosperi.pdf

  • El Lithy ME, Clerkx EJM, Ruys GJ, Koornneef M, Vreugdenhil D (2004) Quantitative trait locus analysis of growth-related traits in a new Arabidopsis recombinant. Plant Physiol 135:444–458

    PubMed  Article  CAS  Google Scholar 

  • El-Assal SED, Alonso-Blanco C, Peeters AJM, Raz V, Koornneef M (2001) A QTL for flowering time in Arabidopsis reveals a novel allele of CRY2. Nat Genet 29:435–440

    Article  CAS  Google Scholar 

  • Ellwood SR, D’Souza NK, Kamphuis LG, Burgess TI, Nair RM, Oliver RP (2006) SSR analysis of the Medicago truncatula SARDI core collection reveals substantial diversity and unusual genotype dispersal throughout the Mediterranean basin. Theor Appl Genet 112:977–983

    PubMed  Article  CAS  Google Scholar 

  • Erskine W, Ellis RH, Summerfield RJ, Roberts EH, Hussain A (1990) Characterization of responses to temperature and photoperiod for time to flowering in a world lentil collection. TAG Theor Appl Genet 80:193–199

    Google Scholar 

  • Fankhauser C, Yeh KC, Lagarias JC, Zhang H, Elich TD, Chory J (1999) PKS1, a substrate phosphorylated by phytochrome that modulates light signaling in Arabidopsis. Science 284:1539–1541

    PubMed  Article  CAS  Google Scholar 

  • Hayama R, Coupland G (2004) The molecular basis of diversity in the photoperiodic flowering responses of Arabidopsis and rice. Plant Physiol 135:677–684

    PubMed  Article  CAS  Google Scholar 

  • 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

    PubMed  Article  CAS  Google Scholar 

  • Huang T, Bohlenius H, Eriksson S, Parcy F, Nilsson O (2005) The mRNA of the Arabidopsis gene FT moves from leaf to shoot apex and induces flowering. Science 309:1694–1696

    PubMed  Article  CAS  Google Scholar 

  • Imaizumi T, Kay SA (2006) Photoperiodic control of flowering: not only by coincidence. Trends Plant Sci 11:550–558

    PubMed  Article  CAS  Google Scholar 

  • Jourjon MF, Jasson S, Marcel J, Ngom B, Mangin B (2005) MCQTL: multi-allelic QTL mapping in multi-cross design. Bioinformatics 21:128–130

    PubMed  Article  CAS  Google Scholar 

  • Julier B, Flajoulot S, Barre P, Cardinet G, Santoni S, Huguet T, Huyghe C (2003) Construction of two genetic linkage maps in cultivated tetraploid alfalfa (Medicago sativa) using microsatellite and AFLP markers. BMC Plant Biol 3:9

    PubMed  Article  Google Scholar 

  • Julier B, Huguet T, Chardon F, Ayadi R, Pierre JB, Prosperi JM, Barre P, Huyghe C (2007) Identification of quantitative trait loci influencing aerial morphogenesis in the model legume Medicago truncatula. Theor Appl Genet 114:1391–1406

    PubMed  Article  Google Scholar 

  • Knapp E, Teuber L (1990) Environmental factors and plant phenotype affect alfalfa floret tripping. Crop Sci 30:270–275

    Google Scholar 

  • Kole C, Williams PH, Rimmer SR, Osborn TC (2002) Linkage mapping of genes controlling resistance to white rust (Albugo candida) in Brassica rapa (syn. campestris) and comparative mapping to Brassica napus and Arabidopsis thaliana. Genome 45:22–27

    PubMed  Article  CAS  Google Scholar 

  • Komeda Y (2004) Genetic regulation of time to flower in Arabidopsis thaliana. Annu Rev Plant Biol 55:521–535

    PubMed  Article  CAS  Google Scholar 

  • Kottapalli KR, Sarla N, Kikuchi S (2006) In silico insight into two rice chromosomal regions associated with submergence tolerance and resistance to bacterial leaf blight and gall midge. Biotechnol Adv 24:561–589

    PubMed  Article  CAS  Google Scholar 

  • Krüger GHJ (1984) Effect of photoperiod on initiation of staminate inflorescence in different hybrids of Zea mays. S Afr J Bot 3:81–82

    Google Scholar 

  • Lander ES, Botstein D (1989) Mapping mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121:185–199

    PubMed  CAS  Google Scholar 

  • Lee S, Reth A, Meletzus D, Sevilla M, Kennedy C (2000) Characterization of a major cluster of nif, fix, and associated genes in a sugarcane endophyte, Acetobacter diazotrophicus. J Bacteriol 182:7088–7091

    PubMed  Article  CAS  Google Scholar 

  • Levy YY, Dean C (1998) The transition to flowering. Plant Cell 10:1973–1989

    PubMed  Article  CAS  Google Scholar 

  • Loudet O, Gaudon V, Trubuil A, Daniel-Vedele F (2005) Quantitative trait loci controlling root growth and architecture in Arabidopsis thaliana confirmed by heterogeneous inbred family. Theor Appl Genet 110:742–753

    PubMed  Article  CAS  Google Scholar 

  • Moreau D, Salon C, Munier-Jolain N (2007) A model-based framework for the phenotypic characterisation of the flowering of Medicago truncatula. Plant Cell Environ 30:213–224

    PubMed  Article  Google Scholar 

  • Muranty H (1996) Power of tests for quantitative trait loci detection using full-sib families in different schemes. Heredity 76:156–165

    Article  Google Scholar 

  • Pflieger S, Lefebvre V, Causse M (2001) The candidate gene approach in plant genetics: a review. Mol Breed 7:275–291

    Article  CAS  Google Scholar 

  • Putterill J, Robson F, Lee K, Simon R, Coupland G (1995) The Constans gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc-finger transcription factors. Cell 80:847–857

    PubMed  Article  CAS  Google Scholar 

  • Rebai A, Goffinet B (1993) Power of tests for QTL detection using replicated progenies derived from a diallel cross. Theor Appl Genet 86:1014–1022

    Article  Google Scholar 

  • Ronfort J, Bataillon T, Santoni S, Delalande M, David JL, Prosperi JM (2006) Microsatellite diversity and broad scale geographic structure in a model legume: building a set of nested core collection for studying naturally occurring variation in Medicago truncatula. BMC Plant Biol 6:28

    PubMed  Article  Google Scholar 

  • Roux F, Touzet P, Cuguen J, Le Corre V (2006) How to be early flowering: an evolutionary perspective. Trends Plant Sci 11:375–381

    PubMed  Article  CAS  Google Scholar 

  • Schmitz RJ, Amasino RM (2007) Vernalization: a model for investigating epigenetics and eukaryotic gene regulation in plants. Biochim Biophys Acta Gene Struct Expr 1769:269–275

    CAS  Google Scholar 

  • Searle I, Coupland G (2004) Induction of flowering by seasonal changes in photoperiod. EMBO J 23:1217–1222

    PubMed  Article  CAS  Google Scholar 

  • Summerfield RJ, Muehlbauer F, Roberts EH (1985) Lens culinaris medic. In: Havely A (ed) A handbook of flowering. CRC Press, Florida, pp 118–124

    Google Scholar 

  • Thomas B, Vince-Prue D (1997) Photoperiodism in plants. Academic Press, London

    Google Scholar 

  • Thomson MJ, Edwards JD, Septiningsih EM, Harrington SE, McCouch SR (2006) Substitution mapping of dth1.1, a flowering-time quantitative trait locus (QTL) associated with transgressive variation in rice, reveals multiple sub-QTL. Genetics 172:2501–2514

    PubMed  Article  CAS  Google Scholar 

  • Thoquet P, Ghérardi M, Journet EP, Kereszt A, Ané JM, Prosperi JM, Huguet T (2002) The molecular genetic linkage map of the model legume Medicago truncatula: an essential tool for comparative legume genomics and the isolation of agronomically important genes. BMC Plant Biol 2:1

    PubMed  Article  Google Scholar 

  • Torregrosa C, Cluzet S, Fournier J, Huguet T, Gamas P, Prosperi JM, Esquerre-Tugaye MT, Dumas B, Jacquet C (2004) Cytological, genetic, and molecular analysis to characterize compatible and incompatible interactions between Medicago truncatula and Colletotrichum trifolii. Mol Plant Microbe Interact 17:909–920

    PubMed  Article  CAS  Google Scholar 

  • 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

    PubMed  Article  CAS  Google Scholar 

  • van Heerden JM (1984) Influence of temperature and daylength on the phenological development of annual Medicago species with particular reference to M. truncatula, cv. Jemalong. S Afr J Plant Soil 1:73–78

    Google Scholar 

  • Wricke G, Weber WE (1986) Quantitative genetics and selection in plant breeding. Walter de Gryter, Berlin

    Google Scholar 

  • Yano M, Katayose Y, Ashikari M, Yamanouchi U, Monna L, Fuse T, Baba T, Yamamoto K, Umehara Y, Nagamura Y, Sasaki T (2000) Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell 12:2473–2483

    PubMed  Article  CAS  Google Scholar 

  • Yoo SY, Kardailsky I, Lee JS, Weigel D, Ahn JH (2004) Acceleration of flowering by overexpression of MFT (MOTHER of FT and TFL1). Mol Cells 17:95–101

    PubMed  CAS  Google Scholar 

  • Zhou Y, Sun XD, Ni M (2007) Timing of photoperiodic flowering: light perception and circadian clock. J Integr Plant Biol 49:28–34

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Jean-Marie Prosperi and Magalie Delalande from the Biological Resources Center at INRA Montpellier (France), and Alon Samach at the University of Jerusalem (Israel) for providing RILs populations and lines, respectively. We thank Jean-François Bourcier, Aline Gilly and Joël Jousse for phenotyping the plants, Franck Gelin and René Minault for greenhouse management and Michèle Gherardi for genotyping. We are grateful to Françoise Durand and Chrystel Gibelin for the SSR mapping. We thank also Isabelle Litrico, Jean-Paul Sampoux, Ela Frak, Jean-Louis Durand and Delphine Moreau for discussion on the modelling, and Fabien Chardon for advices on multi-population QTL detection. J.B. Pierre received a PhD grant from INRA and Region Poitou-Charentes (France).

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Affiliations

  1. INRA, UR4, Unité de Recherche Pluridisciplinaire Prairies et Plantes Fourragères, BP 6, 86600, Lusignan, France

    Jean-Baptiste Pierre, Philippe Barre, Christian Huyghe & Bernadette Julier

  2. INRA-CNRS, LIPM BP27, 31326, Castanet-Tolosan Cedex, France

    Thierry Huguet

  3. INP-ENSAT, Laboratoire Symbiose et Pathologie des Plantes, 31326, Castanet-Tolosan, France

    Thierry Huguet

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  1. Jean-Baptiste Pierre
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  2. Thierry Huguet
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  3. Philippe Barre
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  4. Christian Huyghe
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  5. Bernadette Julier
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Correspondence to Bernadette Julier.

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Communicated by C. Gebhardt.

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Pierre, JB., Huguet, T., Barre, P. et al. Detection of QTLs for flowering date in three mapping populations of the model legume species Medicago truncatula . Theor Appl Genet 117, 609–620 (2008). https://doi.org/10.1007/s00122-008-0805-4

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Keywords

  • Mapping Population
  • Flowering Date
  • Short Photoperiod
  • Support Interval
  • Floral Identity Gene