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Development Genes and Evolution

, Volume 218, Issue 7, pp 341–351 | Cite as

Expression differentiation of CYC-like floral symmetry genes correlated with their protein sequence divergence in Chirita heterotricha (Gesneriaceae)

  • Qiu Gao
  • Ju-Hong Tao
  • Dan Yan
  • Yin-Zheng Wang
  • Zhen-Yu Li
Original Article

Abstract

CYCLOIDIEA (CYC) and its homologues have been studied intensively in the model organism Antirrhinum majus and related species regarding their function in controlling floral dorsoventral (adaxial–abaxial) asymmetry, including aborting the adaxial and lateral stamens. This raises the question whether the same mechanism underlies the great morphological diversity of zygomorphy in angiosperms, especially in Lamiales sensu lato, a major clade predominantly with zygomorphic flowers. To address this, we selected a representative in Gesneriaceae, the sister to the remainder of Lamiales s.l., to isolate CYC homologues and further investigate their expression patterns using locus-specific semiquantitative reverse transcriptase polymerase chain reaction. Our results showed that four CYC homologues in Chirita heterotricha differentiated spatially and temporally in expression, in which ChCYC1D was only expressed in the adaxial regions, and transcripts of ChCYC1C were distributed in both the adaxial and lateral regions, while ChCYC2A and ChCYC2B transcripts were only detected in the young inflorescences. ChCYC1C expression in the lateral regions correlated with abortion of the lateral stamens in C. heterotricha hinted at its gain of function, i.e., expanding from the adaxial to the lateral regions in expression. Correlatively, the protein sequences of ChCYC genes exhibited remarkable divergences, in which some lineage-specific amino acids between GCYC1 and GCYC2 in conserved functional domains and two sublineage-specific motifs between GCYC1C and GCYC1D in GCYC1 genes had further been identified. Our results indicated that ChCYC genes had probably undergone an expressional differentiation and specialization in establishing the floral dorsoventral asymmetry in C. heterotricha responding to different selective pressure after gene duplication.

Keywords

Dorsoventral asymmetry CYC-like gene RT-PCR expression differentiation Gesneriaceae Chirita heterotricha 

Notes

Acknowledgments

We are grateful to James F. Smith for critical comments and improvements on our manuscript, especially in language editing. We also thank Mr. Chen Yan for assistance in the greenhouse. This research was supported by CAS Grant KSCX2-YW-R-135 and National Natural Science Foundation of China Grant, nos. 30770147, 30121003.

References

  1. Burtt BL (1990) Gesneriaceae of the Old World. I. New and little-known species of Cyrtandra from Malesia. Edinburgh J Bot 47:201–233Google Scholar
  2. Citerne HL, Möller M, Cronk QCB (2000) Diversity of CYCLOIDEA-like genes in Gesneriaceae in relation to floral symmetry. Ann Bot 86:167–176CrossRefGoogle Scholar
  3. Cubas P, Lauter N, Doebley J, Coen ES (1999) The TCP domain: a motif found in proteins regulating plant growth and development. Plant J 18:215–222PubMedCrossRefGoogle Scholar
  4. Cubas P, Coen E, Zapater JMM (2001) Ancient asymmetries in the evolution of flowers. Curr Biol 11:1050–1052PubMedCrossRefGoogle Scholar
  5. Damerval C, Guilloux ML, Jager M, Charon C (2007) Diversity and evolution of CYCLOIDEA-like TCP genes in relation to flower development in Papaveraceae. Plant Physiol 143:759–772PubMedCrossRefGoogle Scholar
  6. Doebley J, Stec A, Gustus C (1995) Teosinte branched1 and the origin of maize: evidence for epistasis and the evolution of dominance. Genetics 141:333–346PubMedGoogle Scholar
  7. Doebley J, Stec A, Hubbard L (1997) The evolution of apical dominance in maize. Nature 386:485–488PubMedCrossRefGoogle Scholar
  8. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15Google Scholar
  9. Du ZY, Wang YZ (2008) Significance of RT-PCR expression patterns of CYC-like genes in Oreocharis benthamii (Gesneriaceae). Journal of Systematics and Evolution 46:23–31Google Scholar
  10. Endress PK (1998) Antirrhinum and Asteridae—evolutionary changes of floral symmetry. Symp Soc Exp Biol 51:133–140PubMedGoogle Scholar
  11. Endress PK (1999) Symmetry in flowers: diversity and evolution. Int J Plant Sci 160:S3–S23PubMedCrossRefGoogle Scholar
  12. Feng XZ, Zhao Z, Tian ZX, Xu SL, Luo YH, Cai ZG, Wang YM, Yang J, Wang Z, Weng L, Chen JH, Zheng LY, Guo XZ, Luo JH, Sato S, Tabata S, Ma W, Cao XL, Hu XH, Sun CR, Luo D (2006) Control of petal shape and floral zygomorphy in Lotus japonicus. Proc Natl Acad Sci USA 103:4970–4975PubMedCrossRefGoogle Scholar
  13. Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531–1545PubMedGoogle Scholar
  14. Gu ZL, Cavalcanti A, Chen FC, Bouman P, Li WH (2002) Extent of gene duplication in the genomes of Drosophila, nematode, and yeast. Mol Biol Evol 19:256–262PubMedGoogle Scholar
  15. Guindon S, Gascuel O (2003) A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Syst Biol 52:696–704PubMedCrossRefGoogle Scholar
  16. Guindon S, Lethiec F, Duroux P, Gascuel O (2005) PHYML Online: a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res 33:557–559CrossRefGoogle Scholar
  17. He XL, Zhang JZ (2005) Rapid subfunctionalization accompanied by prolonged and substantial neofunctionalization in duplicate gene evolution. Genetics 169:1157–1164PubMedCrossRefGoogle Scholar
  18. Hileman LC, Kramer EM, Baum DA (2003) Differential regulation of symmetry genes and the evolution of floral morphologies. Proc Natl Acad Sci USA 100:12814–12819PubMedCrossRefGoogle Scholar
  19. Howarth DG, Donoghue MJ (2005) Duplications in CYC-like genes from Dipsacales correlate with floral form. Int J Plant Sci 166:357–370CrossRefGoogle Scholar
  20. Howarth DG, Donoghue MJ (2006) Phylogenetic analysis of the “ECE” (CYC/TB1) clade reveals duplications predating the core eudicots. Proc Natl Acad Sci USA 103:9101–9106PubMedCrossRefGoogle Scholar
  21. Hsia CC, McGinnis W (2003) Evolution of transcription factor function. Curr Opin Genet Dev 13:199–206PubMedCrossRefGoogle Scholar
  22. Hubbard L, McSteen P, Doebley J, Hake S (2002) Expression patterns and mutant phenotype of teosinte branched 1 correlate with growth suppression in maize and teosinte. Genetics 162:1927–1935PubMedGoogle Scholar
  23. Kölsch A, Gleissberg S (2006) Diversification of CYCLOIDEA-like TCP genes in the basal eudicot families Fumariaceae and Papaveraceae s.str. Plant Biol 8:680–687PubMedCrossRefGoogle Scholar
  24. Kosugi S, Ohashi Y (1997) PCF1 and PCF2 specifically bind to cis elements in the rice proliferating cell nuclear antigen gene. Plant Cell 9:1607–1619PubMedCrossRefGoogle Scholar
  25. Kosugi S, Ohashi Y (2002) DNA binding and dimerization specificity and potential targets for the TCP protein family. Plant J 30:337–348PubMedCrossRefGoogle Scholar
  26. Kreitman M, Comeron JM (1999) Coding sequence evolution. Curr Opin Genet Dev 9:637–641PubMedCrossRefGoogle Scholar
  27. Li ZY, Wang YZ (2004) Plants of Gesneriaceae in China. Henan Science and Technology publishing house, Zhengzhou, ChinaGoogle Scholar
  28. Luo D, Carpenter R, Vincent C, Copsey L, Coen ES (1996) Origin of floral asymmetry in Antirrhinum. Nature 383:794–799PubMedCrossRefGoogle Scholar
  29. Luo D, Carpenter R, Copsey L, Vincent C, Clark J, Coen ES (1999) Control of organ asymmetry in flowers of Antirrhinum. Cell 99:367–376PubMedCrossRefGoogle Scholar
  30. Möller M, Clokie M, Cubas P, Cronk QCB (1999) Integrating molecular phylogenies and developmental genetics: a Gesneriaceae case study. In: Hollingsworth PM, Bateman RM, Gornall RJ (eds) Molecular systematics and plant evolution. Taylor and Francis, London, pp 375–402Google Scholar
  31. Moore RC, Purugganan MD (2003) The early stages of duplicate gene evolution. Proc Natl Acad Sci USA 100:15682–15687PubMedCrossRefGoogle Scholar
  32. Ohno S (1970) Euolution by gene duplication. Springer, New YorkGoogle Scholar
  33. Prasad K, Sriram P, Kumar SC, Kushalappa K, Vijayraghavan U (2001) Ectopic expression of rice OsMADS1 reveals a role in specifying the lemma and palea, grass floral organs analogous to sepals. Dev Genes Evol 211:281–290PubMedCrossRefGoogle Scholar
  34. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitutions. Bioinformatics 14:817–818PubMedCrossRefGoogle Scholar
  35. Ramsay NA, Glover BJ (2005) MYB–bHLH–WD40 protein complex and the evolution of cellular diversity. Trends Plant Sci 10:63–70PubMedCrossRefGoogle Scholar
  36. Swofford DL (2002) PAUP*. Phylogenetic Analysis Using Parsimony software (*and other methods) version 4.0b10. Available at: http://paup.csit.fsu.edu/
  37. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882PubMedCrossRefGoogle Scholar
  38. Wang CN, Möller M, Cronk QCB (2004) Phylogenetic position of Titanotrichum oldhamii (Gesneriaceae) inferred from four different gene regions. Syst Bot 29:407–418CrossRefGoogle Scholar
  39. Wang WT, Pan KY, Li ZY (1992) Keys to the Gesneriaceae of China. Edinburgh J Bot 49:5–74CrossRefGoogle Scholar
  40. Weber A (2004) Gesneriaceae. In: Kubitzki K, Kadereit JW (eds) The families and genera of vascular plants. Springer, Berlin, pp 63–158Google Scholar
  41. Xia X, Xie Z (2001) DAMBE: Software package for data analysis in molecular biology and evolution. J Heredity 92:371–373CrossRefGoogle Scholar
  42. Zhang JZ (2003) Evolution by gene duplication: an update. Trends Ecol Evol 18:292–298CrossRefGoogle Scholar
  43. Zhou XR, Wang YZ, Smith JF, Chen RJ (2008) Altered expression patterns of TCP and MYB genes relating to the floral developmental transition from initial zygomorphy to actinomorphy in Bournea (Gesneriaceae). New Phytol 178:532–543PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  1. 1.State Key Laboratory of Systematic and Evolutionary Botany, Institute of BotanyChinese Academy of SciencesBeijingChina

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