Plant Molecular Biology

, Volume 71, Issue 3, pp 241–250 | Cite as

Evolution of flower shape in Plantago lanceolata

  • Wesley Reardon
  • David A. Fitzpatrick
  • Mario A. Fares
  • Jacqueline M. Nugent


Plantago lanceolata produces small actinomorphic (radially symmetric), wind-pollinated flowers that have evolved from a zygomorphic, biotically pollinated ancestral state. To understand the developmental mechanisms that might underlie this change in flower shape, and associated change in pollination syndrome, we analyzed the role of CYC-like genes in P. lanceolata. Related zygomorphic species have two CYC-like genes that are expressed asymmetrically in the dorsal region of young floral meristems and in developing flowers, where they affect the rate of development of dorsal petals and stamens. Plantago has a single CYC-like gene (PlCYC) that is not expressed in early floral meristems and there is no apparent asymmetry in the pattern of PlCYC expression during later flower development. Thus, the evolution of actinomorphy in Plantago correlates with loss of dorsal-specific CYC-like gene function. PlCYC is expressed in the inflorescence stem, in pedicels, and relatively late in stamen development, suggesting a novel role for PlCYC in compacting the inflorescence and retarding stamen elongation in this wind pollinated species.


Plantago Flower shape Protogyny Wind pollination CYCLOIDEA 



We thank Gwyneth Ingram, Justin Goodrich and Andrew Hudson for all their help with the in situ hybridizations, William Thompson for help with the initial amino acid alignment, Benjamin Pommerrenig for recommending the Fructose 1-6 bisphosphate aldolase primers for RT-PCR, Andrew Hudson, Dick Olmstead and Brenda Malloy for critical comments on the manuscript, Ica Dix for help with photography, and David Rawlinson for artwork. We acknowledge the SFI/HEA Irish Centre for High-End Computing (ICHEC) for the provision of computational facilities and support. This work was funded by a Basic Science Research Grant from Enterprise Ireland (JN).


  1. Bello MA, Rudall PJ, Gonzalez F, Fernandez-Alonso JL (2004) Floral morphology and development in Aragoa (Plantaginaceae) and related members of the order Lamiales. Int J Plant Sci 16:723–738CrossRefGoogle Scholar
  2. Bertin RI, Newman CM (1993) Dichogamy in angiosperms. Bot Rev 59:112–159CrossRefGoogle Scholar
  3. Bremer B, Bremer K, Heidari N, Erixon P, Olmstead RG, Anderberg AA, Kallersjo M, Barkhordarian E (2002) Phylogenetics of asterids based on 3 coding and 3 non-coding chloroplast DNA markers and the utility of non-coding DNA at higher taxonomic levels. Mol Phylogen Evol 24:274–301CrossRefGoogle Scholar
  4. Busch A, Zachgo S (2007) Control of corolla monosymmetry in the Brassicaceae Iberis amara. Proc Natl Acad Sci 104:16714–16719PubMedCrossRefGoogle Scholar
  5. Carpenter R, Coen E (1990) Floral homeotic mutations produced by transposon-mutagenesis in Antirrhinum majus. Genes Dev 4:1483–1493PubMedCrossRefGoogle Scholar
  6. Citerne HL, Pennington RT, Cronk QC (2006) An apparent reversal in floral symmetry in the legume Cadia is a homeotic transformation. Proc Natl Acad Sci 103:12017–12020PubMedCrossRefGoogle Scholar
  7. Clark JI, Coen E (2002) The cycloidea gene can respond to a common dorsoventral prepattern in Antirrhinum. Plant J 30:639–648PubMedCrossRefGoogle Scholar
  8. Corley SB, Carpenter R, Copsey L, Coen E (2005) Floral asymmetry involves an interplay between TCP and MYB transcription factors in Antirrhinum. Proc Natl Acad Sci 102:5068–5073PubMedCrossRefGoogle Scholar
  9. Cubas P (2004) Floral zygomorphy, the recurring evolution of a successful trait. BioEssays 26:1175–1184PubMedCrossRefGoogle Scholar
  10. Cubas P, Lauter N, Doebley J, Coen E (1999a) The TCP domain: a motif found in proteins regulating plant growth and development. Plant J 18:215–222PubMedCrossRefGoogle Scholar
  11. Cubas P, Vincent C, Coen E (1999b) An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401:157–161PubMedCrossRefGoogle Scholar
  12. Cubas P, Coen E, Zapater JMM (2001) Ancient asymmetries in the evolution of flowers. Curr Biol 11:1050–1052PubMedCrossRefGoogle Scholar
  13. Culley TM, Weller SG, Sakai AK (2002) The evolution of wind pollination in angiosperms. Trends in Ecol & Evol 17:361–369CrossRefGoogle Scholar
  14. Doebley J, Stec A, Hubbard L (1997) The evolution of apical dominance in Maize. Nature 386:485–488PubMedCrossRefGoogle Scholar
  15. Donoghue MJ, Ree RH, Baum DA (1998) Phylogeny and the evolution of flower symmetry in the Asteridae. Trends Plant Sci 3:311–317CrossRefGoogle Scholar
  16. Endress PK (1997) Antirrhinum and Asteridae-evolutionary changes of floral symmetry. Symp Ser Soc Exp Biol 53:133–140Google Scholar
  17. Endress PK (2001) Evolution of floral symmetry. Curr Opin Plant Biol 4:86–91PubMedCrossRefGoogle Scholar
  18. Feng X, Zhao Z, Tian Z, Xu S, Luo Y, Cai Z, Wang Y, Yang J, Wang Z, Weng L, Chen J, Zheng L, Guo X, Luo J, Sato S, Tabata S, Ma W, Cao X, Hu X, Sun C, Luo D (2006) Control of petal shape and floral zygomorphy in Lotus japonicus. Proc Natl Acad Sci 103:4970–4975PubMedCrossRefGoogle Scholar
  19. Friedman J, Barrett SCH (2008) A phylogenetic analysis of the evolution of wind pollination in the angiosperms. Intl J Plant Sci 169:49–58CrossRefGoogle Scholar
  20. Gaudin V, Lunness PA, Fobert PR, Towers M, Riou-Khamlichi C, Murray JA, Coen E, Doonan JH (2000) The expression of D-cyclin genes defines distinct developmental zones in snapdragon apical meristems and is locally regulated by the Cycloidea gene. Plant Physiol 122:1137–1148PubMedCrossRefGoogle Scholar
  21. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704PubMedCrossRefGoogle Scholar
  22. Henderson LB (1926) Floral anatomy of several species of Plantago. Am J Bot 13:397–406CrossRefGoogle Scholar
  23. Hileman LC, Baum DA (2003) Why do paralogs persist? Molecular evolution of CYCLOIDEA and related floral symmetry genes in Antirrhinae (Veronicaceae). Mol Biol Evol 20:591–600PubMedCrossRefGoogle Scholar
  24. Hileman LC, Kramar EM, Baum DA (2003) Differential regulation of symmetry genes and the evolution of floral morphologies. Proc Natl Acad Sci 100:12814–12819PubMedCrossRefGoogle Scholar
  25. Hubbard L, McSteen P, Doebley J, Hake S (2002) Expression patterns and mutant phenotype of teosinte branched1 correlate with growth suppression in maize and teosinte. Genetics 162:1927–1935PubMedGoogle Scholar
  26. Kalisz S, Ree RH, Sargent RD (2006) Linking floral symmetry genes to breeding system evolution. Trends Plant Sci 11:568–573PubMedCrossRefGoogle Scholar
  27. Katoh K, Kuma K, Toh H, Miyata T (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33:511–518PubMedCrossRefGoogle Scholar
  28. Keane TM, Creevey CJ, Pentony MM, Naughton TJ, McInerney JO (2006) Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evol Biol 6:29PubMedCrossRefGoogle Scholar
  29. Lartillot N, Brinkmann H, Philippe H (2007) Suppression of long-branch attraction artefacts in the animal phylogeny using a site-heterogeneous model. BMC Evol Biol 7(Suppl 1):S4PubMedCrossRefGoogle Scholar
  30. Lewis JM, Mackintosh CA, Shin S, Gilding E, Kravchenko S, Baldridge G, Zeyen R, Muehlbauer GJ (2008) Overexpression of the maize Teosinte Branched1 gene in wheat suppresses tiller development. Plant Cell Rep 27:1217–1225PubMedCrossRefGoogle Scholar
  31. Lincoln C, Long J, Yamaguchi J, Serikawa K, Hake S (1994) A knotted1-like homeobox gene in Arabidopsis is expressed in the vegetative meristem and dramatically alters leaf morphology when overexpressed in transgenic plants. Plant Cell 6:1859–1876PubMedCrossRefGoogle Scholar
  32. Luo D, Carpenter R, Vincent C, Copsey L, Coen E (1996) Origin of floral asymmetry in Antirrhinum. Nature 383:794–799PubMedCrossRefGoogle Scholar
  33. Luo D, Carpenter R, Copsey L, Vincent C, Clark J, Coen E (1999) Control of organ asymmetry in flowers of Antirrhinum. Cell 99:367–376PubMedCrossRefGoogle Scholar
  34. Notredame C, Higgins DG, Heringa J (2000) T-Coffee: A novel method for fast and accurate multiple sequence alignment. J Mol Biol 302:205–217PubMedCrossRefGoogle Scholar
  35. Olmstead RG, Jansen RK, Kim K-J, Wagstaff SJ (2000) The phylogeny of the Asteridae s.l. based on chloroplast ndhF sequences. Mol Phylogenet Evol 16:96–112PubMedCrossRefGoogle Scholar
  36. Olmstead RG, dePamphilis CW, Wolfe AD, Young ND, Elisons WJ, Reeves PA (2001) Disintegration of the Scrophulariaceae. Am J Bot 88:348–361PubMedCrossRefGoogle Scholar
  37. Reeves PA, Olmstead RG (2003) Evolution of the TCP gene family in Asteridae: Cladistic and network approaches to understanding regulatory gene family diversification and its impact on morphological evolution. Mol Biol Evol 20:1997–2009PubMedCrossRefGoogle Scholar
  38. Shimodaira H (2002) An approximately unbiased test of phylogenetic tree selection. Syst Biol 51:492–508PubMedCrossRefGoogle Scholar
  39. Stebbins GL (1974) Flowering plants: evolution above the species level. Harvard University Press, USAGoogle Scholar
  40. Swofford DL (1998) PAUP*: phylogenetic analysis using parsimony (*and other methods). Sinquer Sunderland, UKGoogle Scholar
  41. Vieira C, Vieira J, Charlesworth D (1999) Evolution of the Cycloidea gene family in Antirrhinum and Misopates. Mol Biol Evol 16:1474–1483PubMedGoogle Scholar
  42. Wang Z, Luo Y, Li X, Wang L, Xu S, Yang J, Weng L, Sato S, Tabata S, Ambrose M, Rameau C, Feng X, Hu X, Luo D (2008) Genetic control of floral zygomorphy in pea (Pisum sativum L.). Proc Natl Acad Sci 105:10414–10419PubMedCrossRefGoogle Scholar
  43. Weller SG, Sakai AK, Culley TM, Campbell DR, Dunbar-Wallis AK (2006) Predicting the pathway to wind pollination: heritabilities and genetic correlations of inflorescence traits associated with wind pollination in Schiedea salicaria (Caryophyllaceae). Jour Evol Bio 19:331–342CrossRefGoogle Scholar
  44. Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum likelihood computer applications in the biosciences. Cabios 13:555–556PubMedGoogle Scholar
  45. Yang Z, Nielsen R, Goldman N, Pedersen AM (2000) Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155:431–449PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Wesley Reardon
    • 1
  • David A. Fitzpatrick
    • 1
  • Mario A. Fares
    • 2
  • Jacqueline M. Nugent
    • 1
  1. 1.Department of BiologyNational University of IrelandMaynoothIreland
  2. 2.Department of Genetics, Smurfit Institute of GeneticsTrinity CollegeDublinIreland

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