Russian Journal of Plant Physiology

, Volume 60, Issue 2, pp 279–289 | Cite as

Molecular characterization of the flowering time gene FRIGIDA in Brassica genomes A and C

  • O. A. FadinaEmail author
  • A. A. Pankin
  • E. E. Khavkin
Research Papers


An important determinant of flowering time variation in Arabidopsis, the FRIGIDA (FRI) gene has not been until recently investigated in economically important Brassica species. In diploid Brassica species, this gene exists as two paralogous loci on chromosomes A3 and A4 (B. rapa; A genome), and C3 and C9 (B. oleracea; C genome). Each locus is represented by several genome-specific alleles, which are discerned primarily by polymorphisms in C- and especially N-terminal regions. Locus- and genome-specific sequences of two FRI paralogues are conserved almost completely in the subgenomes A and C of tetraploid B. napus. The phylogenetic analysis of available FRI sequences presumes that the duplication of FRI loci preceded speciation in the genus Brassica.


Arabidopsis Brassica napus B. oleracea B. rapa FRIGIDA vernalization gene divergence allelic polymorphism 


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  1. 1.
    Greenup, A., Peacock, W.J., Dennis, E.S., and Trevaskis, B., The Molecular Biology of Seasonal Flowering-Responses in Arabidopsis and the Cereals, Ann. Bot., 2009, vol. 103, pp. 1165–1172.PubMedCrossRefGoogle Scholar
  2. 2.
    Amasino, R., Seasonal and Developmental Timing of Flowering, Plant J., 2010, vol. 61, pp. 1001–1013.PubMedCrossRefGoogle Scholar
  3. 3.
    Wilczek, A.M., Burghardt, L.T., Cobb, A.R., Cooper, M.D., Welch, S.M., and Schmitt, J., Genetic and Physiological Bases for Phenological Responses to Current and Predicted Climates, Phil. Trans. R. Soc. B., 2010, vol. 365, pp. 3129–3147.PubMedCrossRefGoogle Scholar
  4. 4.
    Weigel, D., Natural Variation in Arabidopsis: From Molecular Genetics to Ecological Genomics, Plant Physiol., 2012, vol. 158, pp. 2–22.PubMedCrossRefGoogle Scholar
  5. 5.
    Geraldo, N., Bäurle, I., Kidou, S.K., Hu, X., and Dean, C., FRIGIDA Delays Flowering in Arabidopsis via a Co-Transcriptional Mechanism Involving Direct Interaction with the Nuclear Cap Binding Complex, Plant Physiol., 2009, vol. 150, pp. 1611–1618.PubMedCrossRefGoogle Scholar
  6. 6.
    Choi, K., Kim, J., Hwang, H.J., Kim, S., Park, C., Kim, S.Y., and Lee, I., The FRIGIDA Complex Activates Transcription of FLC, a Strong Flowering Repressor in Arabidopsis, by Recruiting Chromatin Modification Factors, Plant Cell, 2011, vol. 23, pp. 289–303.PubMedCrossRefGoogle Scholar
  7. 7.
    Johanson, U., West, J., Lister, C., Michaels, S., Amasino, R., and Dean, C., Molecular Analysis of FRIGIDA, a Major Determinant of Natural Variation in Arabidopsis Flowering Time, Science, 2000, vol. 290, pp. 344–347.PubMedCrossRefGoogle Scholar
  8. 8.
    Le Corre, V., Roux, F., and Reboud, X., DNA Polymorphism at the FRIGIDA Gene in Arabidopsis thaliana: Extensive Nonsynonymous Variation Is Consistent with Local Selection for Flowering Time, Mol. Biol. Evol., 2002, vol. 19, pp. 1261–1271.PubMedCrossRefGoogle Scholar
  9. 9.
    Le Corre, V., Variation at Two Flowering Time Genes within and among Populations of Arabidopsis thaliana: Comparison with Markers and Traits, Mol. Ecol., 2005, vol. 14, pp. 4181–4192.PubMedCrossRefGoogle Scholar
  10. 10.
    Lempe, J., Balasubramanian, S., Sureshkumar, S., Singh, A., Schmid, M., and Weigel, D., Diversity of Flowering Responses in Wild Arabidopsis thaliana Strains, PLoS Genet., 2005, vol. 1: e6.CrossRefGoogle Scholar
  11. 11.
    Shindo, C., Aranzana, M.J., Lister, C., Baxter, C., Nicholls, C., Nordborg, M., and Dean, C., Role of FRIGIDA and FLOWERING LOCUS C in Determining Variation in Flowering Time of Arabidopsis, Plant Physiol., 2005, vol. 138, pp. 1163–1173.PubMedCrossRefGoogle Scholar
  12. 12.
    Caicedo, A.L., Stinchcombe, J.R., Olsen, K.M., Schmitt, J., and Purugganan, M.D., Epistatic Interaction between Arabidopsis FRI and FLC Flowering Time Genes Generates a Latitudinal Cline in a Life History Trait, Proc. Natl. Acad. Sci. USA, 2004, vol. 101, pp. 15670–15675.PubMedCrossRefGoogle Scholar
  13. 13.
    Stinchcombe, J.R., Weinig, C., Ungerer, M., Olsen, K.M., Mays, C., Halldorsdottir, S.S., Purugganan, M.D., and Schmitt, J., A Latitudinal Cline in Flowering Time in Arabidopsis thaliana Modulated by the Flowering Time Gene FRIGIDA, Proc. Natl. Acad. Sci. USA, 2004, vol. 101, pp. 4712–4717.PubMedCrossRefGoogle Scholar
  14. 14.
    Mendez-Vigo, B., Picó, F.X., Ramiro, M., Martínez-Zapater, J.M., and Alonso-Blanco, C., Altitudinal and Climatic Adaptation Is Mediated by Flowering Traits and FRI, FLC and PhyC Genes in Arabidopsis thaliana, Plant Physiol., 2011, vol. 157, pp. 1942–1955.PubMedCrossRefGoogle Scholar
  15. 15.
    Kuittinen, H., Niittyvuopio, A., Rinne, P., and Savolainen, O., Natural Variation in Arabidopsis lyrata Vernalization Requirement Conferred by a FRIGIDA Indel Polymorphism, Mol. Biol. Evol., 2008, vol. 25, pp. 319–329.PubMedCrossRefGoogle Scholar
  16. 16.
    Werner, J.D., Borevitz, J.O., Uhlenhaut, N.H., Ecker, J.R., Chory, J., and Weigel, D., FRIGIDA-Independent Variation in Flowering Time of Natural Arabidopsis thaliana Accessions, Genetics, 2005, vol. 170, pp. 1197–1207.PubMedCrossRefGoogle Scholar
  17. 17.
    Strange, A., Li, P., Lister, C., Anderson, J., Warthmann, N., Shindo, C., Irwin, J., Nordborg, M., and Dean, C., Major-Effect Alleles at Relatively Few Loci Underlie Distinct Vernalization and Flowering Variation in Arabidopsis Accessions, PLoS ONE, 2011, vol. 6: e19 949.CrossRefGoogle Scholar
  18. 18.
    Korves, T.M., Schmid, K.J., Caicedo, A.L., Mays, C., Stinchcombe, J.R., Purugganan, M.D., and Schmitt, J., Fitness Effects Associated with the Major Flowering Time Gene FRIGIDA in Arabidopsis thaliana in the Field, Am. Nat., 2007, vol. 169, pp. 141–157.CrossRefGoogle Scholar
  19. 19.
    Scarcelli, N., Cheverud, J.M., Schaal, B.A., and Kover, P.X., Antagonistic Pleiotropic Effects Reduce the Potential Adaptive Value of the FRIGIDA Locus, Proc. Natl. Acad. Sci. USA, 2007, vol. 104, pp. 16 986–16 991.CrossRefGoogle Scholar
  20. 20.
    Brock, M.T., Stinchcombe, J.R., and Weinig, C., Indirect Effects of FRIGIDA: Floral Trait (Co)Variances Are Altered by Seasonally Variable Abiotic Factors Associated with Flowering Time, J. Evol. Biol., 2009, vol. 22, pp. 1826–1838.PubMedCrossRefGoogle Scholar
  21. 21.
    Brachi, B., Faure, N., Horton, M., Flahauw, E., Vazquez, A., Nordborg, M., Bergelson, J., Cuguen, J.L., and Roux, F., Linkage and Association Mapping of Arabidopsis thaliana Flowering Time in Nature, PloS Genet., 2010, vol. 6: e1 000 940.CrossRefGoogle Scholar
  22. 22.
    Moore, S. and Lukens, L., An Evaluation of Arabidopsis thaliana Hybrid Traits and Their Genetic Control, G3 (Bethesda, Maryland), 2011, vol. 1, pp. 571–579.Google Scholar
  23. 23.
    Wang, J., Tian, L., Lee, H.S., and Chen, Z.J., Nonadditive Regulation of FRI and FLC Loci Mediates Flowering-Time Variation in Arabidopsis Allopolyploids, Genetics, 2006, vol. 173, pp. 965–974.PubMedCrossRefGoogle Scholar
  24. 24.
    Fadina, O.A., Pankin, A.A., Khavkin, E.E. Homologues of Gene FRIGIDA in Cultivated Species of Brassica, Mater. dokl. VII S“ezda Ob-va fiziologov rastenii Rossii “Fiziologiya rastenii — fundamental’naya osnova ekologii i innovatsionnykh biotekhnologii” (4–10 July 2011) (Proc. VII Congr. of Plant Physiologists in Russia Plant Physiology — Fundamental Basics of Ecology and Innovative Biotechnology, July 4–10, 2011), Nizhnii Novgorod, 2011, pp. 712–713.Google Scholar
  25. 25.
    Wang, N., Qian, W., Suppanz, I., Wei, L., Mao, B., Long, Y., Meng, J., Mueller, A., and Jung, C., Flowering Time Variation in Oilseed Rape (Brassica napus L.) Is Associated with Allelic Variation in the FRIGIDA Homologue BnaA.FRI.a, J. Exp. Bot., 2011, vol. 62, pp. 5641–5658.PubMedCrossRefGoogle Scholar
  26. 26.
    Irwin, J.A., Lister, C., Soumpourou, E., Zhang, Y., Howell, E.C., Teakle, G., and Dean, C., Functional Alleles of the Flowering Time Regulator FRIGIDA in the Brassica oleracea Genome, BMC Plant Biol., 2012, vol. 12: 21.PubMedCrossRefGoogle Scholar
  27. 27.
    Tamura, K., Peterson, D., Stecher, G., Nei, M., and Kumar, S., MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods, Mol. Biol. Evol., 2011, vol. 28, pp. 2731–2739.PubMedCrossRefGoogle Scholar
  28. 28.
    Ostergaard, L. and King, G., Standardized Gene Nomenclature for the Brassica Genus, Plant Methods, 2008, vol. 4: 10.PubMedCrossRefGoogle Scholar
  29. 29.
    Wang, X., Wang, H., Wang, J., Sun, R., Wu, J., et al., The Genome of the Mesopolyploid Crop Species Brassica rapa, Nat. Genet., 2011, vol. 43, pp. 1035–1039.PubMedCrossRefGoogle Scholar
  30. 30.
    Bancroft, I., Morgan, C., Fraser, F., Higgins, J., Wells, R., Clissold, L., Baker, D., Long, Y., Meng, J., Wang, X., Liu, S., and Trick, M., Dissecting the Genome of the Polyploid Crop Oilseed Rape by Transcriptome Sequencing, Nat. Biotech., 2011, vol. 29, pp. 762–766.CrossRefGoogle Scholar
  31. 31.
    Campbell, M.A., Haas, B.J., Hamilton, J.P., Mount, S.M., and Buell, C.R., Comprehensive Analysis of Alternative Splicing in Rice and Comparative Analyses with Arabidopsis, BMC Genom., 2006, vol. 7: 327.CrossRefGoogle Scholar
  32. 32.
    Risk, J.M., Laurie, R.E., Macknight, R.C., and Day, C.L., FRIGIDA and Related Proteins Have a Conserved Central Domain and Family Specific N- and C-Terminal Regions That Are Functionally Important, Plant Mol. Biol., 2010, vol. 73, pp. 493–505.PubMedCrossRefGoogle Scholar
  33. 33.
    Allender, C.J. and King, G.J., Origins of the Amphiploid Species Brassica napus L. Investigated by Chloroplast and Nuclear Molecular Markers, BMC Plant Biol., 2010, vol. 10: 54.PubMedCrossRefGoogle Scholar
  34. 34.
    Parkin, I.A.P., Gulden, S.M., Sharpe, A.G., Lukens, L., Trick, M., Osborn, T.C., and Lydiate, D.J., Segmental Structure of the Brassica napus Genome Based on Comparative Analysis with Arabidopsis thaliana, Genetics, 2005, vol. 171, pp. 765–781.PubMedCrossRefGoogle Scholar
  35. 35.
    Cheung, F., Trick, M., Drou, N., Lim, Y.P., Park, J.Y., Kwon, S.J., Kim, J.A., Scott, R., Pires, J.C., Paterson, A.H., Town, C., and Bancroft, I., Comparative Analysis between Homoeologous Genome Segments of Brassica napus and Its Progenitor Species Reveals Extensive Sequence-Level Divergence, Plant Cell, 2009, vol. 21, pp. 1912–1928.PubMedCrossRefGoogle Scholar
  36. 36.
    Tang, H., Woodhouse, M.R., Cheng, F., Schnable, J.C., Pedersen, B.S., Conant, G., Wang, X., Freeling, M., and Pires, J.C., Altered Patterns of Fractionation and Exon Deletions in Brassica rapa Support a Two-Step Model of Paleohexaploidy, Genetics, 2012, vol. 190, pp. 1563–1574.PubMedCrossRefGoogle Scholar
  37. 37.
    Beilstein, M.A., Nagalinguma, N.S., Clements, M.D., Manchester, S.R., and Mathews, S., Dated Molecular Phylogenies Indicate a Miocene Origin for Arabidopsis thaliana, Proc. Natl. Acad. Sci. USA, 2010, vol. 107, pp. 18 724–18 728.CrossRefGoogle Scholar
  38. 38.
    Toomajian, C., Hu, T.T., Aranzana, M.J., Lister, C., Tang, C., Zheng, H., Zhao, K., Calabrese, P., Dean, C., and Nordborg, M., A Nonparametric Test Reveals Selection for Rapid Flowering in the Arabidopsis Genome, PLoS Biol., 2006, vol. 4: e137.PubMedCrossRefGoogle Scholar
  39. 39.
    Yuan, Y.X., Wu, J., Sun, R.F., Zhang, X.W., Xu, D.H., Bonnema, G., and Wang, X.W., A Naturally Occurring Splicing Site Mutation in the Brassica rapa FLC1 Gene Is Associated with Variation in Flowering Time, J. Exp. Bot., 2009, vol. 60, pp. 1299–1308.PubMedCrossRefGoogle Scholar
  40. 40.
    Hu, G.L., Hu, Z.L., Li, Y., Gu, F., Zhao, Z.P., and Chen, G.P., A Splicing Site Mutation in BrpFLC1 and Repressed Expression of BrpFLC Genes Are Associated with the Early Flowering of Purple Flowering Stalk, Russ. J. Plant Physiol., 2011, vol. 58, pp. 431–438.CrossRefGoogle Scholar
  41. 41.
    Slotte, T., Huang, H.-R., Holm, K., Ceplitis, A., Onge, S., Chen, J., Lagercrantz, U., and Lascoux, M., Splicing Variation at a FLOWERING LOCUS C Homeolog Is Associated with Flowering Time Variation in the Tetraploid Capsella bursa-pastoris, Genetics, 2009, vol. 183, pp. 337–345.PubMedCrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2013

Authors and Affiliations

  1. 1.Institute of Agricultural BiotechnologyRussian Academy of Agricultural SciencesMoscowRussia

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