Plant Molecular Biology

, Volume 63, Issue 5, pp 637–650 | Cite as

The FT/TFL1 gene family in grapevine

  • María José Carmona
  • Myriam Calonje
  • José Miguel Martínez-Zapater
Article

Abstract

The FT/TFL1 gene family encodes proteins with similarity to phosphatidylethanolamine binding proteins which function as flowering promoters and repressors. We show here that the FT/TFL1 gene family in Vitis vinifera is composed of at least five genes. Sequence comparisons with homologous genes identified in other dicot species group them in three major clades, the FT, MFT and TFL1 subfamilies, the latter including three of the Vitis sequences. Gene expression patterns are in agreement with a role of VvFT and VvMFT as flowering promoters; while VvTFL1A, VvTFL1B and VvTFL1C could be associated with vegetative development and maintenance of meristem indetermination. Overexpression of VvFT in transgenic Arabidopsis plants generates early flowering phenotypes similar to those produced by FT supporting a role for this gene in flowering promotion. Overexpression of VvTFL1A does not affect flowering time but the determination of flower meristems, strongly altering inflorescence structure, which is consistent with the biological roles assigned to similar genes in other species.

Keywords

Flowering transition FT/TFL1 gene family Grapevine Inflorescence meristem identity Juvenile phase 

Abbreviations

SAM

shoot apical meristem

Notes

Acknowledgments

We thank Félix Cabello and the Instituto Madrileño de Investigación y Desarrollo Rural Agrario y Alimentario (IMIDRA, Alcalá de Henares, Madrid) for providing plant materials for this research, Gemma Bravo for her excellent technical assistance with the transformation experiments, and Diego Lijavetsky for his help with the MEGA software. We also thank Cheo Machín for careful editing of the manuscript. This research was supported by grants GEN2003-2023-CO2-01 and BIO2005-07612-C02-01 from Spanish Ministerio de Educación y Ciencía and GRAPEGEN from a collaborative agreement between Genoma España and Genome Canada.

References

  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 309:1052–1056PubMedCrossRefGoogle Scholar
  2. 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 25:605–614PubMedCrossRefGoogle Scholar
  3. Ausín I, Alonso-Blanco C, Martínez-Zapater JM (2005) Environmental regulation of flowering. Int J Dev Biol 49:689–705PubMedCrossRefGoogle Scholar
  4. Baggiolini M (1952) Les stades repères dans le développement de la vigne et leur utilisation pratique. Rev Romande Agric Vitic Arbor 8:4–6Google Scholar
  5. Banfield MJ, Brady RL (2000) The structure of Antirrhinum CENTRORADIALIS protein (CEN) suggests a role as a kinase regulator. J Mol Biol 297:1159–1170PubMedCrossRefGoogle Scholar
  6. Böhlenius H, Huang T, Charbonnel-Campaa L, Brunner AM, Jansson S, Strauss SH, Nilsson O (2006) CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312:1040–1043PubMedCrossRefGoogle Scholar
  7. Boss PK, Sreekantan L, Thomas MR (2006) A grapevine TFL1 homologue can delay flowering and alter floral development when overexpressed in heterologous species. Funct Plant Biol 33:31–41CrossRefGoogle Scholar
  8. Boss PK, Bastow RM, Mylne JS, Dean C (2004) Multiple pathways in the decision to flower: enabling, promoting, and resetting. Plant Cell 16(Suppl):S18–31PubMedCrossRefGoogle Scholar
  9. Bradley D, Carpenter R, Copsey L, Vincent C, Rothstein S, Coen E (1996) Control of inflorescence architecture in Antirrhinum. Nature 379:791–797PubMedCrossRefGoogle Scholar
  10. Bradley D, Ratcliffe O, Vincent C, Carpenter R, Coen E (1997) Inflorescence commitment and architecture in Arabidopsis. Science 275:80–83PubMedCrossRefGoogle Scholar
  11. Brunner AM, Nilsson O (2004) Revisiting tree maturation and floral initiation in the poplar functional genomics era. New Phytol. 164:43–51CrossRefGoogle Scholar
  12. Calonje M, Cubas P, Martínez-Zapater JM, Carmona MJ (2004) Floral meristem identity genes are expressed during tendril development in grapevine. Plant Physiol 135:1491–1501PubMedCrossRefGoogle Scholar
  13. Carmel-Goren L, Liu YS, Lifschitz E, Zamir D (2003) The SELF PRUNING gene family in tomato. Plant Mol Biol 52:1215–1222PubMedCrossRefGoogle Scholar
  14. Carmona MJ, Cubas P, Martínez-Zapater JM (2002) VFL, the grapevine FLORICAULA/LEAFY ortholog, is expressed in meristematic regions independently of their fate. Plant Physiol 130:68–77PubMedCrossRefGoogle Scholar
  15. Carmona MJ, Cubas P, Calonje M, Martínez-Zapater JM (2007) Flowering transition in grapevine (Vitis vinifera L.). Can J Bot (in press)Google Scholar
  16. Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11:113–116Google Scholar
  17. Chardon F, Damerval C (2005) Phylogenomic analysis of the PEBP gene family in cereals. J Mol Evol 61:579–590PubMedCrossRefGoogle Scholar
  18. Church JM, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci USA 81:1991–1995PubMedCrossRefGoogle Scholar
  19. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743PubMedCrossRefGoogle Scholar
  20. Endo T, Shimada T, Fujii H, Kobayashi Y, Araki T, Omura M (2005) Ectopic expression of an FT homolog from Citrus confers an early flowering phenotype on trifoliate orange (Poncirus trifoliata L. Raf.). Transgenic Res 14:703–712PubMedCrossRefGoogle Scholar
  21. Foucher F, Morin J, Courtiade J, Cadioux S, Ellis N, Banfield MJ, Rameau C (2003) DETERMINATE and LATE FLOWERING are two TERMINALFLOWER1/CENTRORADIALIS homologs that control two distinct phases of flowering initiation and development in pea. Plant Cell 15:2742–2754PubMedCrossRefGoogle Scholar
  22. Frohman MA, Dush MK, Martin GR (1988) Rapid production of full length cDNA from rare transcripts: amplification using a single gene specific oligonucleotide primer. Proc Natl Acad Sci USA 85:8998–9002PubMedCrossRefGoogle Scholar
  23. Gerrath JM, Lacroix CR, Posluszny U (1998) Phyllotaxis in the Vitaceae. In: Jean RV, Barabe D (eds), Simmetry in Plants, World Scientific, Singapore, pp89–107Google Scholar
  24. Hanzawa Y, Money T, Bradley D (2005) A single amino acid converts a repressor to an activator of flowering. Proc Natl Acad Sci USA 102:7748–7753PubMedCrossRefGoogle Scholar
  25. Hsu C-Y, Liu Y, Luthe DS, Yuceer C (2006) Poplar FT2 shortens the juvenile phase and promotes seasonal flowering. Plant Cell 18:1846–1861PubMedCrossRefGoogle Scholar
  26. 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 309:1694–1696PubMedCrossRefGoogle Scholar
  27. Joly D, Perrin M, Gertz C, Kronenberger J, Demangeat G, Masson E (2004) Expression analysis of flowering genes from seedling-stage to vineyard life of grapevine cv. Riesling Plant Sci 166:1427–1436CrossRefGoogle Scholar
  28. 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 286:1962–1965PubMedCrossRefGoogle Scholar
  29. Kobayashi Y, Kaya H, Goto K, Iwabuchi M, Araki T (1999) A pair of related genes with antagonistic roles in mediating flowering signals. Science 286:1960–1962PubMedCrossRefGoogle Scholar
  30. Kotoda N, Wada M (2005) MdTFL1, a TFL1-like gene of apple, retards the transition from the vegetative to reproductive phase in transgenic Arabidopsis. Plant Sci 168:95–104CrossRefGoogle Scholar
  31. Kotoda N, Iwanami H, Takahashi S, Abe K (2006) Antisense expression of MdTFL1, a TFL1-like gene, reduces the juvenile phase in apple. J Amer Soc Hort Sci 131:74–81Google Scholar
  32. Kumar S, Tamura K, Nei M (2004) MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163PubMedCrossRefGoogle Scholar
  33. 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 103:6398–6403PubMedCrossRefGoogle Scholar
  34. Martin-Trillo M, Martinez-Zapater JM (2002) Growing up fast: manipulating the generation time of trees. Curr Op Biotechnol 13:151–155CrossRefGoogle Scholar
  35. Michaels SD, Himelblau E, Kim SY, Schomburg FM, Amasino RM (2005) Integration of flowering signals in winter-annual Arabidopsis. Plant Physiol 137:149–156PubMedCrossRefGoogle Scholar
  36. Mimida N, Goto K, Kobayashi Y, Araki T, Ahn JH, Weigel D, Murata M, Motoyoshi F, Sakamoto W (2001) Functional divergence of the TFL1-like gene family in Arabidopsis revealed by characterization of a novel homologue. Genes Cells 6:327–336PubMedCrossRefGoogle Scholar
  37. Mullins MG, Bouquet A, Williams LE (1992) Biology of the Grapevine. Cambridge University Press, Cambridge, UKGoogle Scholar
  38. Parcy F (2005) Flowering: a time for integration. Int J Dev Biol 49:585–593PubMedCrossRefGoogle Scholar
  39. Pillitteri LJ, Lovatt CJ, Walling LL (2004) Isolation and characterization of a TERMINAL FLOWER 1 homolog and its correlation with juvenility in Citrus. Plant Physiol 135:1540–1551PubMedCrossRefGoogle Scholar
  40. Pratt C (1971) Reproductive anatomy of cultivated grapes—a review. Am J Enol Viticult 22:92–109Google Scholar
  41. Putterill J, Laurie R, Macknight R (2004) It’s time to flower: the genetic control of flowering time. Bioessays 26:363–373PubMedCrossRefGoogle Scholar
  42. Ratcliffe OJ, Amaya I, Vincent CA, Rothstein S, Carpenter R, Coen ES, Bradley DJ (1998) A common mechanism controls the life cycle and architecture of plants. Development 125:1609–1615PubMedGoogle Scholar
  43. Ruíz García L, Madueño F, Wilkinson M, Haughn G, Salinas J, Martínez-Zapater JM (1997) Different roles of flowering-time genes in the activation of floral initiation genes in Arabidopsis. Plant Cell 9:1921–1934PubMedCrossRefGoogle Scholar
  44. Shannon S, Meeks-Wagner DR (1993) Genetic interactions that regulate inflorescence development in Arabidopsis. Plant Cell 5:639–655PubMedCrossRefGoogle Scholar
  45. Takada S, Goto K (2003) TERMINAL FLOWER 2, an Arabidopsis homolog of HETEROCHROMATIN PROTEIN 1, counteracts the activation of FLOWERING LOCUS T by CONSTANS in the vascular tissues of leaves to regulate flowering time. Plant Cell 15:2856–2865PubMedCrossRefGoogle Scholar
  46. Yamaguchi A, Kobayashi Y, Goto K, Abe M, Araki T (2005) TWIN SISTER OF FT (TSF) acts as a floral pathway integrator redundantly with FT. Plant Cell Physiol 46:1175–1189PubMedCrossRefGoogle Scholar
  47. Yeung K, Seitz T, Li S, Janosch P, McFerran B, Kaiser C, Fee F, Katsanakis KD, Rose DW, Mischak H (1999) Suppression of Raf-1 kinase activity and MAP kinase signaling by RKIP. Nature 401:173–177PubMedCrossRefGoogle Scholar
  48. 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 17:95–101PubMedGoogle Scholar
  49. Wigge PA, Kim MC, Jaeger KE, Busch W, Schmid M, Lohmann JU, Weigel D (2005) Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309:1056–1059PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2006

Authors and Affiliations

  • María José Carmona
    • 1
  • Myriam Calonje
    • 1
    • 3
  • José Miguel Martínez-Zapater
    • 2
  1. 1.Departamento de Biotecnología, Escuela Técnica Superior de Ingenieros AgrónomosUniversidad Politécnica de Madrid, Ciudad UniversitariaMadridSpain
  2. 2.Departamento de Genética Molecular de PlantasCentro Nacional de Biotecnología, Consejo Superior de Investigaciones CientíficasMadridSpain
  3. 3.Department of Plant and Microbial BiologyUniversity of CaliforniaBerkeleyUSA

Personalised recommendations