Journal of Molecular Evolution

, Volume 61, Issue 5, pp 579–590 | Cite as

Phylogenomic Analysis of the PEBP Gene Family in Cereals

  • Fabien Chardon
  • Catherine DamervalEmail author


The TFL1 and FT genes, which are key genes in the control of flowering time in Arabidopsis thaliana, belong to a small multigene family characterized by a specific phosphatidylethanolamine-binding protein domain, termed the PEBP gene family. Several PEBP genes are found in dicots and monocots, and act on the control of flowering time. We investigated the evolution of the PEBP gene family in cereals. First, taking advantage of the complete rice genome sequence and EST databases, we found 19 PEBP genes in this species, 6 of which were not previously described. Ten genes correspond to five pairs of paralogs mapped on known duplicated regions of the rice genome. Phylogenetic analysis of Arabidopsis and rice genes indicates that the PEBP gene family consists of three main homology classes (the so-called TFL1-LIKE, MFT-LIKE, and FT-LIKE subfamilies), in which gene duplication and/or loss occurred independently in Arabidopsis and rice. Second, phylogenetic analyses of genomic and EST sequences from five cereal species indicate that the three subfamilies of PEBP genes have been conserved in cereals. The tree structure suggests that the ancestral grass genome had at least two MFT-like genes, two TFL1-like genes, and eight FT-like genes. A phylogenomic approach leads to some hypotheses about conservation of gene function within the subfamilies.


Flowering time Gene duplication Comparative biology FT/TFL1-LIKE gene family Poaceae 



We are grateful to Domenica Manicacci, Maud Tenaillon, and Alain Charcosset for critical reading of the manuscript. This research was supported by a grant to Fabien Chardon from the Génoplante programme.


  1. Adams KL, Cronn R, Percifield R, Wendel JF (2003) Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing Proc Natl Acad Sci USA 100:4649–4654CrossRefPubMedGoogle Scholar
  2. Amaya I, Ratcliffe OJ, Bradley DJ (1999) Expression of CENTRORADIALIS (CEN) and CEN-like genes in tobacco reveals a conserved mechanism controlling phase change in diverse species Plant Cell 11:1405–1418CrossRefPubMedGoogle Scholar
  3. Araki T (2001) Transition from vegetative to reproductive phase Curr Opin Plant Biol 4:63–68CrossRefPubMedGoogle Scholar
  4. Armstead IP, Turner LB, Farrell M, Skot L, Gomez P, Montoya T, Donnison IS, King IP, Humphreys MO (2004) Synteny between a major heading-date QTL in perennial ryegrass (Lolium perenne L.) and the Hd3 heading-date locus in rice Theor Appl Genet 108:822–828CrossRefPubMedGoogle Scholar
  5. Banfield MJ, Barker JJ, Perry AC, Brady RL (1998) Function from structure? The crystal structure of human phosphatidylethanolamine-binding protein suggests a role in membrane signal transduction Structure 6:1245–1254CrossRefPubMedGoogle Scholar
  6. Bradley D, Carpenter R, Copsey L, Vincent C, Rothstein S, Coen E (1996) Control of inflorescence architecture in Antirrhinum Nature 379:791–797CrossRefPubMedGoogle Scholar
  7. Carmel-Goren L, Liu YS, Lifschitz E, Zamir D (2003) The SELF-PRUNING gene family in tomato Plant Mol Biol 52:1215–1222CrossRefPubMedGoogle Scholar
  8. Citerne HL, Luo D, Pennington RT, Coen E, Cronk QCB (2003) A phylogenomic investigation of CYCLOIDEA-like TCP genes in the Leguminosae Plant Physiol. 131:1042–1053CrossRefPubMedGoogle Scholar
  9. Doi K, Izawa T, Fuse T, Yamanouchi U, Kubo T, Shimatani Z, Yano M, Yoshimura A (2004) Ehd1, a B-type response regulator in rice, confers short-day promotion of flowering and controls FT-like gene expression independently of Hd1. Genes Dev 18:926–936CrossRefPubMedGoogle Scholar
  10. Eisen JA (1998) Phylogenomics: Improving functional predictions for uncharacterized genes by evolutionary analysis Genome Res 8:163–167PubMedGoogle Scholar
  11. Foucher F, Morin J, Courtiade J, Cadioux S, Ellis N, Banfield MJ, Rameau C (2003) DETERMINATE and LATE FLOWERING are two TERMINAL FLOWER1/CENTRORADIALIS homologues that control two distinct phases of flowering initiation and development in pea Plant Cell 15:2742–2754CrossRefPubMedGoogle Scholar
  12. Gaut BS, Doebley JF (1997) DNA sequence evidence for the segmental allotetraploid origin of maize Proc Natl Acad Sci USA 94:6809–6814CrossRefPubMedGoogle Scholar
  13. Hall TA (1991) BioEdit: A user-friendly biological sequence alignment editor and analysis. Ibis Theropeutics, Carlsbad, CAGoogle Scholar
  14. Hileman LC, Baum DA (2003) Why do paralogs persist? Molecular evolution of CYCLOIDEA and related floral symmetry genes in Antirrhineae (Veronicaceae) Mol Biol Evol 20:591–600CrossRefPubMedGoogle Scholar
  15. Izawa T, Oikawa T, Sugiyama N, Tanisaka T, Yano M, Shimamoto K (2002) Phytochrome mediates the external light signal to repress FT orthologues in photoperiodic flowering of rice Genes Dev 16:2006–2020CrossRefPubMedGoogle Scholar
  16. Izawa T, Takahashi Y, Yano M (2003) Comparative biology comes into bloom: genomic and genetic comparison of flowering pathways in rice and Arabidopsis Curr Opin Plant Biol 6:113–120CrossRefPubMedGoogle Scholar
  17. Jensen CS, Salchert K, Nielsen KK (2001) A terminal Flower1–like gene from perennial ryegrass involved in floral transition and axillary meristem identity Plant Physiol 125:1517–1528CrossRefPubMedGoogle Scholar
  18. 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 286:1962–1965CrossRefPubMedGoogle Scholar
  19. Kobayashi Y, Kaya H, Goto K, Iwabuchi M, Araki T (1999) A pair of related genes with antagonistic roles in mediating flowering signals Science 286:1960–1962CrossRefPubMedGoogle Scholar
  20. Kojima S, Takahashi Y, Kobayashi Y, Monna L, Sasaki T, Araki T, Yano M (2002) Hd3a, a rice orthologue of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions Plant Cell Physiol 43:1096–1105CrossRefPubMedGoogle Scholar
  21. Koornneef M, Alonso–Blanco C, Peeters AJ, Soppe W (1998) Genetic control of flowering time in Arabidopsis Annu Rev Plant Physiol Plant Mol Biol 49:345–370CrossRefPubMedGoogle Scholar
  22. Koornneef M, Hanhart CJ, Van der Veen JH (1991) A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana Mol Gen Genet 229:57–66CrossRefPubMedGoogle Scholar
  23. Kroslak T, Koch T, Kahl E, Hollt V (2001) Human phosphatidylethanolamine–binding protein facilitates heterotrimeric g protein-dependent signaling J Biol Chem 276:39772–39778CrossRefPubMedGoogle Scholar
  24. Kumar S, Tamura K, Jakobsen IB, Nei M (2001) MEGA2: Molecular Evolutionary Genetics Analysis software. Arizona State University, TempeGoogle Scholar
  25. Lynch M, Force A (2000) The probability of duplicate gene preservation by subfunctionalization Genet Soc Am 154:459–473Google Scholar
  26. 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 homologueue Genes Cells 6:327–336CrossRefPubMedGoogle Scholar
  27. Mouradov A, Cremer F, Coupland G (2002) Control of flowering time: interacting pathways as a basis for diversity Plant Cell 14(Suppl): S111–S130PubMedGoogle Scholar
  28. Nakagawa M, Shimamoto K, Kyozuka J (2002) Overexpression of RCN1 and RCN2, rice TERMINAL FLOWER 1/CENTRORADIALIS homologues, confers delay of phase transition and altered panicle morphology in rice Plant J 29:743–750CrossRefPubMedGoogle Scholar
  29. Ohno (1970) Evolution by gene duplication Springer-Verlag, BerlinGoogle Scholar
  30. Ohta T (2000) Evolution of gene families Gene 259:45–52CrossRefPubMedGoogle Scholar
  31. Olsen KM, Womack A, Garrett AR, Suddith JI, Purugganan MD (2002) Contrasting evolutionary forces in the Arabidopsis thaliana floral developmental pathway Genetics 160:1641–1650PubMedGoogle Scholar
  32. Paterson AH, Bowers JE, Peterson DG, Estill JC, Chapman BA (2003) Structure and evolution of cereal genomes Curr Opin Genet Dev 13:644–650CrossRefPubMedGoogle Scholar
  33. Pnueli L, Carmel-Goren L, Hareven D, Gutfinger T, Alvarez J, Ganal M, Zamir D, Lifschitz E (1998) The SELF-PRUNING gene of tomato regulates vegetative to reproductive switching of sympodial meristems and is the orthologue of CEN and TFL1 Development 125:1979–1989PubMedGoogle Scholar
  34. Posada D, Crandall K (1998) MODELTEST: testing the model of DNA substitution Bioinformatics 14:817–818CrossRefPubMedGoogle Scholar
  35. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models Bioinformatics 19:1572–1574CrossRefPubMedGoogle Scholar
  36. Salse J, Piegu B, Cooke R, Delseny M (2004) New in silico insight into the synteny between rice (Oryza sativa L.) and maize (Zea mays L.) highlights reshuffling and identifies new duplications in the rice genome Plant J 38:396–409CrossRefPubMedGoogle Scholar
  37. Serre L, Vallee B, Bureaud N, Schoentgen F, Zelwer C (1998) Crystal structure of the phosphatidylethanolamine-binding protein from bovine brain: a novel structural class of phospholipid-binding proteins. Structure 6:1255–1265CrossRefPubMedGoogle Scholar
  38. Shannon S, Meeks-Wagner DR (1991) A mutation in the Arabidopsis TFL1 gene affects inflorescence meristem development Plant Cell 3:877–892CrossRefPubMedGoogle Scholar
  39. Tadege M, Sheldon CC, Helliwell CA, Upadhyaya NM, Dennis ES, Peacock WJ (2003) Reciprocal control of flowering time by OsSOC1 in transgenic Arabidopsis and by FLC in transgenic rice Null 1:361–369Google Scholar
  40. Vandepoele K, Simillion C, Van de Peer Y (2003) Evidence that rice and other cereals are ancient aneuploids Plant Cell 15:2192–2202CrossRefPubMedGoogle Scholar
  41. 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 QTL in rice, is closely related to the Arabidopsis flowering time gene CONSTANS Plant Cell 12:2473–2483CrossRefPubMedGoogle Scholar
  42. 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

Copyright information

© Springer Science+Business Media, Inc. 2005

Authors and Affiliations

  1. 1.Station de génétique végétaleUMR de Génétique Végétale, INRA/UPS/CNRS/INAPGFrance

Personalised recommendations