Skip to main content

A CONSTANS-like gene candidate that could explain most of the genetic variation for flowering date in Medicago truncatula

Molecular Breeding volume 28, pages 25–35 (2011)Cite this article

Abstract

Flowering is a critical period during a plant’s life cycle, and thus the identification and characterization of genes involved in flowering date control are of great importance in agronomy, breeding, population genetics and ecology. The model species Medicago truncatula can be used to detect genes explaining the variation for flowering date, which could also explain this variation in legume crops. The objective of this study was to identify the most promising candidate gene explaining a major quantitative trait locus (QTL) for flowering date previously found in three M. truncatula mapping populations. Fine mapping and bioinformatic analysis of bacterial artificial chromosomes (BACs) in the confidence interval of the QTL showed six genes potentially involved in the control of flowering date. Two of these genes, similar to CONSTANS and FT of Arabidopsis thaliana respectively, had genomic mutations when compared to the parents. The transcriptomic study of these genes by semi-quantitative RT-PCR in leaves and flowers sampled at two developmental stages showed that the CONSTANS-like gene was differentially expressed in the two parental lines. A gene belonging to the CONSTANS-like family could explain the major QTL for flowering date segregating in M. truncatula progenies.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price includes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3

References

  • 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 

  • Barker D, Bianchi S, Blondon F, Dattée Y, Duc G, Essad S, Flament P, Gallusci P, Génier G, Guy P, Muel X, Tourneur J, Denarie J, Huguet T (1990) Medicago truncatula, a model plant for studying the molecular genetics of the Rhizobium-legume symbiosis. Plant Mol Biol Rep 8:40–49

    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 

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

    PubMed  Article  Google Scholar 

  • Broman KW, Wu H, Sen S, Churchill GA (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 19:889–890

    PubMed  Article  CAS  Google Scholar 

  • Chabaud M, Larsonneau C, Marmouget C, Huguet T (1996) Transformation of barrel medic (Medicago truncatula Gaertn) by Agrobacterium tumefaciens and regeneration via somatic embryogenesis of transgenic plants with the MtENOD12 nodulin promoter fused to the gus reporter gene. Plant Cell Rep 15:305–310

    CAS  Google Scholar 

  • Cheng XF, Wang ZY (2005) Overexpression of COL9, a CONSTANS-LIKE gene, delays flowering by reducing expression of CO and FT in Arabidopsis thaliana. Plant J 43:758–768

    PubMed  Article  CAS  Google Scholar 

  • Cheung W, Hubert N, Landry B (1993) A simple and rapid DNA microextraction method for plant, animal, and insect suitable for RAPD and other PCR analyses. PCR Methods Appl 3:69–70

    PubMed  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 (2004) Estimating genome conservation between crop and model legume species. Proc Natl Acad Sci USA 101:15289–15294

    PubMed  Article  CAS  Google Scholar 

  • Cook DR (1999) Medicago truncatula—a model in the making!. Curr Opin Plant Biol 2:301–304

    PubMed  Article  CAS  Google Scholar 

  • Crespi MD, Jurkevitch E, Poiret M, Daubentoncarafa Y, Petrovics G, Kondorosi E, Kondorosi A (1994) Enod40, a gene expressed during nodule organogenesis, codes for a nontranslatable RNA involved in plant-growth. EMBO J 13:5099–5112

    PubMed  CAS  Google Scholar 

  • de Givry S, Bouchez M, Chabrier P, Milan D, Schiex T (2005) CAR(H)(T)AGene: multipopulation integrated genetic and radiation hybrid mapping. Bioinformatics 21:1703–1704

    PubMed  Article  Google Scholar 

  • De Vienne D (1998) Les marqueurs moléculaires en génétique et biotechnologies végétales. INRA, Paris

    Google Scholar 

  • Delalande M, Ronfort J, Prosperi JM (2004) Diversity for flowering time in a large collection of Medicago truncatula Gaertn. North American Alfalfa Improvement Conference, Québec

    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 

  • Flint-Garcia SA, Thornsberry JM, Buckler ES IV (2003) Structure of linkage disequilibrium in plants. Annu Rev Plant Biol 54:357–374

    PubMed  Article  CAS  Google Scholar 

  • Gamas P, Debellé F, Berges H, Godiard L, Niebel A, Journet EP, Gouzy J (2006) Medicago truncatula cDNA and genomic libraries. Medicago truncatula Handbook

  • Griffiths S, Dunford RP, Coupland G, Laurie DA (2003) The evolution of CONSTANS-like gene families in barley, rice, and Arabidopsis. Plant Physiol 131:1855–1867

    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 

  • Huguet T, Gherardi M, Chardon F, Sartorel E, Prosperi JM, Chennaoui-Kourda H, Aouani ME (2007) Creation of a consensus genetic-physical (CGPM) for the identification of Medicago truncatula genes involved in natural variation. In: Huguet T, Aouani ME (eds), Model legume congress, 24–28 mars 2007 et Tunis. LILM-CECB, Tunis, pp 12

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

    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 

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

    PubMed  Article  CAS  Google Scholar 

  • Koornneef M, Hanhart CJ, Vanderveen JH (1991) A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Mol Gen Genet 229:57–66

    PubMed  Article  CAS  Google Scholar 

  • Lagercrantz U, Putterill J, Coupland G, Lydiate D (1996a) Comparative mapping in Arabidopsis and Brassica, fine scale genome collinearity and congruence of genes controlling flowering time. Plant J 9:13–20

    PubMed  Article  CAS  Google Scholar 

  • Lagercrantz U, Putterill J, Coupland G, Lydiate D (1996b) Comparative mapping in Arabidopsis and Brassica, fine scale genome collinearity and congruence of genes controlling flowering time. Plant J 9:13–20

    PubMed  Article  CAS  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 

  • Le Corre V (2005) Variation at two flowering time genes within and among populations of Arabidopsis thaliana: comparison with markers and traits. Mol Ecol 14:4181–4192

    PubMed  Article  CAS  Google Scholar 

  • Li Y, Roycewicz P, Smith E, Borevitz JO (2006) Genetics of local adaptation in the laboratory: flowering time quantitative trait loci under geographic and seasonal conditions in Arabidopsis. PLOS One 1:e105

    PubMed  Article  Google Scholar 

  • Lifschitz E, Eviatar T, Rozman A, Shalit A, Goldshmidt A, Amsellem Z, Alvarez JP, Eshed Y (2006) The tomato FT ortholog triggers systemic signals that regulate growth and flowering and substitute for diverse environmental stimuli. Proc Natl Acad Sci USA 103:6398–6403

    PubMed  Article  CAS  Google Scholar 

  • Locatelli AB, Federizzi LC, Milach SCK, Wight CP, Molnar SJ, Chapados JT, Tinker NA (2006) Loci affecting flowering time in oat under short-day conditions. Genome 49:1528–1538

    PubMed  Article  CAS  Google Scholar 

  • Manichaikul A, Dupuis J, Sen S, Broman KW (2006) Poor performance of bootstrap confidence intervals for the location of a quantitative trait locus. Genetics 174:481–489

    PubMed  Article  Google Scholar 

  • Marone M, Mozzetti S, De Ritis D, Pierelli L, Scambia G (2001) Semiquantitative RT-PCR analysis to assess the expression levels of multiple transcripts from the same sample. Biol Proced Online 3:19–25

    PubMed  Article  CAS  Google Scholar 

  • Moreau D, Salon C, Munier-Jolain N (2006) Using a standard framework for the phenotypic analysis of Medicago truncatula: an effective method for characterizing the plant material used for functional genomics approaches. Plant Cell Environ 29:1087–1098

    PubMed  Article  CAS  Google Scholar 

  • Nam YW, Penmetsa RV, Endre G, Uribe P, Kim D, Cook DR (1999) Construction of a bacterial artificial chromosome library of Medicago truncatula and identification of clones containing ethylene-response genes. Theor Appl Genet 98:638–646

    Article  CAS  Google Scholar 

  • O’Shea-Greenfield A, Smale ST (1992) Roles of TATA and initiator elements in determining the start site location and direction of RNA polymerase II transcription. J Biol Chem 267:1391–1402

    PubMed  Google Scholar 

  • Park SY, Nam YW (2006) Construction of a bacterial artificial chromosome library containing large BamHI genomic fragments from Medicago truncatula and identification of clones linked to hypernodulating genes. J Microbiol Biotechnol 16:256–263

    CAS  Google Scholar 

  • Pierre JB, Huguet T, Barre P, Huyghe C, Julier B (2008) Detection of QTLs for flowering date in three mapping populations of the model legume species Medicago truncatula. Theor Appl Genet 117:609–620

    PubMed  Article  CAS  Google Scholar 

  • Putterill J, Laurie R, Macknight R (2004a) It’s time to flower: the genetic control of flowering time. Bioessays 26:363–373

    PubMed  Article  CAS  Google Scholar 

  • Putterill J, Laurie R, Macknight R (2004b) It’s time to flower: the genetic control of flowering time. Bioessays 26:363–373

    PubMed  Article  CAS  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 

  • Salathia N, Davis SJ, Lynn JR, Michaels SD, Amasino RM, Millar AJ (2006) FLOWERING LOCUS C-dependent and -independent regulation of the circadian clock by the autonomous and vernalization pathways. BMC Plant Biol 6:10

    PubMed  Article  Google Scholar 

  • Skot L, Humphreys MO, Armstead I, Heywood S, Skot KP, Sanderson R, Thomas ID, Chorlton KH, Hamilton NRS (2005) An association mapping approach to identify flowering time genes in natural populations of Lolium perenne (L.). Mol Breed 15:233–245

    Article  CAS  Google Scholar 

  • Tadege M, Ratet P, Mysore K (2005) Insertional mutagenesis: a Swiss Army knife for functional genomics of Medicago truncatula. Trends Plant Sci 10:229–235

    PubMed  Article  CAS  Google Scholar 

  • Tjaden G, Edwards JW, Coruzzi GM (1995) Cis-elements and trans-acting factors affecting regulation of a nonphotosynthetic light-regulated gene for chloroplast glutamine-synthetase. Plant Physiol 108:1109–1117

    PubMed  Article  CAS  Google Scholar 

  • Trinh TH, Ratet P, Kondorosi E, Durand P, Kamate K, Bauer P, Kondorosi A (1998) Rapid and efficient transformation of diploid Medicago truncatula and Medicago sativa ssp falcata lines improved in somatic embryogenesis. Plant Cell Rep 17:345–355

    Article  CAS  Google Scholar 

  • Yamanaka N, Watanabe S, Toda K, Hayashi M, Fuchigami H, Takahashi R, Harada K (2005) Fine mapping of the FT1 locus for soybean flowering time using a residual heterozygous line derived from a recombinant inbred line. Theor Appl Genet 110:634–639

    PubMed  Article  CAS  Google Scholar 

  • Young ND, Cannon SB, Sato S, Kim D, Cook DR, Town CD, Roe BA, Tabata S (2005) Sequencing the genespaces of Medicago truncatula and Lotus japonicus. Plant Physiol 137:1174–1181

    PubMed  Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors are very grateful to F. Durand, C. Gibelin and D. Cadier for their help in genotyping recombinants, gene sequencing and RT-PCRs, to J.F. Bourcier and J. Jousse for phenotyping the plants, to R. Minault and F. Gelin for greenhouse management and to M.R. Perretan and G. Boutet at INRA of Clermont-Ferrand for pseudo-F2 genotyping. J.B. Pierre received a Ph.D. grant from Région Poitou-Charentes.

Author information

Author notes

  1. Jean-Baptiste Pierre

    Present address: ARVALIS-Institut du végétal, Pôle Variétés, Semences et Génétique, 91720, Boigneville, France

  2. Matthieu Bogard

    Present address: INRA, UMR1095 Génétique Diversité et Ecophysiologie des Céréales, Site de Crouël 234 avenue du Brézet, 63100, Clermont-Ferrand, France

  3. Doris Herrmann

    Present address: Ecole Polytechnique Fédérale de Lausanne, Indo Swiss Collaboration in Biotechnology, Lausanne, Switzerland

  4. Christian Huyghe

    Present address: INRA, Présidence Centre Inra Poitou-Charentes, BP6, 86600, Lusignan, France

Authors and Affiliations

  1. INRA, UR 4, Unité de Recherche Pluridisciplinaire Prairies et Plantes Fourragères, BP6, 86600, Lusignan, France

    Jean-Baptiste Pierre, Matthieu Bogard, Doris Herrmann, Christian Huyghe & Bernadette Julier

Authors
  1. Jean-Baptiste Pierre
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Matthieu Bogard
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Doris Herrmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Christian Huyghe
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bernadette Julier
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bernadette Julier.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Pierre, JB., Bogard, M., Herrmann, D. et al. A CONSTANS-like gene candidate that could explain most of the genetic variation for flowering date in Medicago truncatula . Mol Breeding 28, 25–35 (2011). https://doi.org/10.1007/s11032-010-9457-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11032-010-9457-6

Keywords

  • Fine mapping
  • Expression study
  • Legume
  • QTL