Capsella as a model system to study the evolutionary relevance of floral homeotic mutants

  • P. Nutt
  • J. Ziermann
  • M. Hintz
  • B. Neuffer
  • G. Theißen


Several lines of evidence suggest that homeotic changes played a considerable role during the evolution of flowers. This, however, is difficult to reconcile with the predominant evolutionary theory which rejects any drastic, saltational change of the phenotype as reasonable mode of evolution due to its assumed negative impact on the fitness of the affected organism. A better understanding of the evolutionary potential of homeotic transitions requires a study of the performance of respective mutant varieties in the wild. Here we introduce ``Stamenoid petals'' (Spe), a variety of Capsella bursa-pastoris (shepherd's purse), as a suitable model to study the evolutionary potential of floral homeotic mutants. In the flowers of the Spe variety all petals are transformed into stamens, while all other floral organs are unaffected. In contrast to most other homeotic mutants the Spe variety occurs on several locations in relatively large and stable populations in the wild. Due to its close relationship to the model plant Arabidopsis thaliana, the Spe variety of C. bursa-pastoris can be rigorously studied, from the molecular genetic basis of the phenotype to its consequences on the fitness in wild habitats. Investigations on Spe may thus help to clarify whether homeotic transformations have the potential to contribute to macroevolution.


ABC model Capsella bursa-pastoris flower development homeosis macroevolution MADS-box genes stamenoid petals 


  1. Acarkan, A., Roßberg, M., Koch, M., Schmidt, R. 2000Comparative genome analysis reveals extensive conservation of genome organisation for Arabidopsis thaliana and Capsella rubella Plant J.235562PubMedCrossRefGoogle Scholar
  2. Albert, V. A., Gustaffson, M. H. G., Di, Laurenzio L. 1998Ontogenetic systematics, molecular developmental genetics, and the angiosperm petalSoltis, D. E.Soltis, P. S.Doyle, J. J. eds. Molecular systematics of plants IIKluwer Academic PublishersBoston, USA349374Google Scholar
  3. Ambrose, B. A., Espinosa-Matías, S., Vázquez-Santana, S., Vergara-Silva, F., Martínez, E., Márquez-Guzmán, J., Alvarez-Buylla, E. R. 2006Comparative developmental series of the Mexican triurids support a euanthial interpretation for the unusual reproductive axes of Lacandonia schismatica (Triuridaceae)Amer. J. Bot.931535Google Scholar
  4. Angenent, G. C., Colombo, L. 1996Molecular control of ovule developmentTrends Pl. Sci.1228232Google Scholar
  5. Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815.Google Scholar
  6. Arthur, W. 2002The emerging conceptual framework of evolutionary developmental biologyNature415757764PubMedGoogle Scholar
  7. Barrett, S. C. H. 2002The evolution of plant sexual diversityNat. Rev. Genet.3274284PubMedCrossRefGoogle Scholar
  8. Bateman, R. M., DiMichele, W. A. 2002Generating and filtering major phenotypic novelties: neoGoldschmidtian saltation revisitedCronk, Q. C. B.Bateman, R. M.Hawkins, J. A. eds. Developmental genetics and plant evolutionTaylor & FrancisLondon109159Google Scholar
  9. Baum, D. A., Donoghue, M. J. 2002Transference of function, heterotopy and the evolution of plant developmentCronk, Q. C. B.Bateman, R. M.Hawkins, J. A. eds. Developmental genetics and plant evolutionTaylor & FrancisLondon5269Google Scholar
  10. Becker, A., Theißen, G. 2003The major clades of MADS-box genes and their role in the development and evolution of flowering plantsMolec. Phylogenet. Evol.29464489PubMedCrossRefGoogle Scholar
  11. Bomblies, K., Dagenais, N., Weigel, D. 1999Redundant enhancers mediate transcriptional repression of AGAMOUS by APETALA2 Dev. Biol.216260264PubMedCrossRefGoogle Scholar
  12. Bowman, J. L. 1997Evolutionary conservation of angiosperm flower development at the molecular and genetic levelsJ. Biosci.22515527Google Scholar
  13. Bowman J. L. (2006) Comparative developmental genetics of the Brassicaceae. Pl. Syst. Evol. 259.Google Scholar
  14. Bradley, D., Carpenter, R., Sommer, H., Hartley, N., Coen, E. 1993Complementary floral homeotic phenotypes result from opposite orientations of a transposon at the plena locus of Antirrhinum Cell728595PubMedCrossRefGoogle Scholar
  15. Carroll, S. B. 2001Chance and necessity: the evolution of morphological complexity and diversityNature40911021109PubMedCrossRefGoogle Scholar
  16. Coen, E. 2001Goethe and the ABC model of flower developmentC.R. Acad. Sci. Paris, Sciences de la vie32418Google Scholar
  17. Coen, E. S., Meyerowitz, E. M. 1991The war of the whorls: genetic interactions controlling flower developmentNature3533137PubMedCrossRefGoogle Scholar
  18. Conner, J., Liu, Z. 2000 LEUNIG, a putative transcriptional corepressor that regulates AGAMOUS expression during flower developmentProc. Natl. Acad. Sci. USA971290212907PubMedCrossRefGoogle Scholar
  19. Coquillat, M. 1951Sur les plants les plus communes de la surface du globeBull. Mens. Soc. Linn. Lyon20165170Google Scholar
  20. Cubas, P., Vincent, C., Coen, E. 1999An epigenetic mutation responsible for natural variation in floral symmetryNature401157161PubMedCrossRefGoogle Scholar
  21. Dahlgren, K. V. O. 1919Erblichkeitsversuche mit einer dekandrischen Capsella bursa-pastoris (L.)Svensk Bot. Tidskr.134860Google Scholar
  22. Darwin, C. 1876The variation of animals and plants under domestication. 2nd edD. AppletonNew YorkGoogle Scholar
  23. Bodt, S., Raes, J., Peer, Y., Theissen, G. 2003And then there were many: MADS goes genomicTrends Pl. Sci.8475483CrossRefGoogle Scholar
  24. Deyholos, M. K., Sieburth, L. E. 2000Separable whorl-specific expression and negative regulation by enhancer elements within the AGAMOUS second intronPlant Cell1217991810PubMedCrossRefGoogle Scholar
  25. Dietrich, M. R. 2003Richard Goldschmidt: hopeful monsters and other `heresies'Nature Rev. Genet.46874CrossRefPubMedGoogle Scholar
  26. Ditta, G., Pinyopich, A., Robles, P., Pelaz, S., Yanofsky, M. F. 2004The SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identityCurr. Biol.1419351940PubMedCrossRefGoogle Scholar
  27. Drews, G. N., Bowman, J. L., Meyerowitz, E. M. 1991Negative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETALA2 productCell659911002PubMedCrossRefGoogle Scholar
  28. Egea-Cortines, M., Saedler, H., Sommer, H. 1999Ternary complex formation between the MADS-box proteins SQUAMOSA, DEFICIENS and GLOBOSA is involved in the control of floral architecture in Antirrhinum majus EMBO J.1853705379PubMedCrossRefGoogle Scholar
  29. Favaro, R., Pinyopich, A., Battaglia, R., Kooiker, M., Borghi, L., Ditta, G., Yanofsky, M. F., Kater, M. M., Colombo, L. 2003MADS-box protein complexes control carpel and ovule development in Arabidopsis Pl. Cell1526032611CrossRefGoogle Scholar
  30. Ferrario, S., Immink, R. G., Angenent, G. C. 2004Conservation and diversity in flower landCurr. Opin. Pl. Biol.78491CrossRefGoogle Scholar
  31. Ford, V. S., Gottlieb, L. D. 1992 Bicalyx is a natural homeotic floral variantNature358671673CrossRefGoogle Scholar
  32. Franks, R. G., Wang, C., Levin, J. Z., Liu, Z. 2002 SEUSS, a member of a novel family of plant regulatory proteins, repress floral homeotic gene expression with LEUNIG Development129253263PubMedGoogle Scholar
  33. Fray, M. J., Puangsomlee, P., Goodrich, J., Coupland, G., Evans, E. J., Arthur, A. E., Lydiate, D. J. 1997The genetics of stamenoid petal production in oilseed rape (Brassica napus) and equivalent variant in Arabidopsis thaliana Theor. Appl. Genet.94731736CrossRefGoogle Scholar
  34. Gilbert, S. F., Opitz, J. M., Raff, R. A. 1996Resynthesizing evolutionary and developmental biologyDev. Biol.173357372PubMedCrossRefGoogle Scholar
  35. Goodrich, J., Puangsomlee, P., Martin, M., Long, D., Meyerowitz, E., Coupland, G. 1997A Polycomb-group gene regulates gene expression in Arabidopsis Nature3864451PubMedCrossRefGoogle Scholar
  36. Gottschalk, W. 1971Die Bedeutung der Genmutation für die Evolution der PflanzeGustav FischerStuttgartGoogle Scholar
  37. Gould, S. J. 1977Ontogeny and phylogenyHarvard University PressCambridge, MA, USAGoogle Scholar
  38. Haag, E. S., True, J. R. 2001From mutants to mechanisms? Assessing the candidate gene paradigm in evolutionary biologyEvolution5510771084PubMedGoogle Scholar
  39. Hill, T. A., Day, C. D., Zondlo, S. C., Thackeray, A. G., Irish, V. F. 1998Discrete spatial and temporal cis-acting elements regulate transcription of the Arabidopsis floral homeotic gene APETALA3 Development12517111721PubMedGoogle Scholar
  40. Hoffmann, M. H., Bremer, M., Schneider, K., Burger, F., Stolle, E., Moritz, G. 2003Flower visitors in a natural population of Arabidopsis thaliana Pl. Biol.5491494CrossRefGoogle Scholar
  41. Honma, T., Goto, K. 2001Complexes of MADS-box proteins are sufficient to convert leaves into floral organsNature409525529PubMedCrossRefGoogle Scholar
  42. Hurka, H., Freundner, S., Brown, A. H. D., Plantholt, U. 1989Aspartat aminotransferase isozymes in the genus Capsella (Brassicaceae): subcellular location, gene duplication and polymorphismBiochem. Genet.277790PubMedCrossRefGoogle Scholar
  43. Hurka, H., Düring, S. 1994Genetic control of plastidic L-glutamate dehydrogenase isozymes in the genus Capsella (Brassicaceae)Heredity72126131Google Scholar
  44. Hurka, H., Neuffer, B. 1997Evolutionary processes in the genus Capsella (Brassicaceae)Pl. Syst. Evol.206295316CrossRefGoogle Scholar
  45. Hurka, H., Bleeker, W., Neuffer, B. 2003Evolutionary process associated with biological invasions in the BrassicaceaeBiol. Invasions5281292CrossRefGoogle Scholar
  46. Hurka, H., Paetsch, M., Bleeker, W., Neuffer, B. 2005Evolution within the BrassicaceaeNova Acta Leopoldina NF92, Nr.342113127Google Scholar
  47. Iltis, H. H. 2000Homeotic sexual translocation and the origin of maize (Zea mays, Poaceae): a new look at an old problemEconomic Bot.54742Google Scholar
  48. Jack, T., Sieburth, L., Meyerowitz, E. 1997Targeted misexpression of AGAMOUS in whorl 2 of Arabidopsis flowersPlant J.11825839PubMedCrossRefGoogle Scholar
  49. Kanno, A., Saeki, H., Kameya, T., Saedler, H., Theißen, G. 2003Heterotopic expression of class B floral homeotic genes supports a modified ABC model for tulip (Tulipa gesneriana)Pl. Molec. Biol.52831841CrossRefGoogle Scholar
  50. Kellogg, E. A. 2000The grasses: A case study in macroevolutionAnnual Rev. Ecol. Syst.31217238CrossRefGoogle Scholar
  51. Koch, M. A., Kiefer, M. 2005Genome evolution among Cruciferous plants: a lecture from the comparison of the genetic maps of three diploid species – Capsella rubella, Arabidopsis lyrata ssp. petraea, and A. thaliana Amer. J. Bot.92761767Google Scholar
  52. Kramer, E. M., Di, Stilio V. S., Schluter, P. M. 2003Complex patterns of gene duplication in the APETALA3 and PISTILLATA lineages of the RanunculaceaeIntern. J. Pl. Sci.164111CrossRefGoogle Scholar
  53. Krizek, B. A., Fletcher, J. C. 2005Molecular mechanisms of flower development: An armchair guideNature Rev. Genet.6688698CrossRefPubMedGoogle Scholar
  54. Krizek, B. A., Meyerowitz, E. M. 1996The Arabidopsis homeotic genes APETALA3 and PISTILLATA are sufficient to provide the B class organ identity functionDevelopment1221122PubMedGoogle Scholar
  55. Lee, J.-Y., Mummenhoff, K., Bowman, J. L. 2002Allopolyploidization and evolution of species with reduced floral structures in Lepidium L. (Brassicaceae)Proc. Natl. Acad. Sci. USA991683516840PubMedCrossRefGoogle Scholar
  56. Lewis, E. B. 1994Homeosis: the first 100 yearsTrends Genet.10341343PubMedCrossRefGoogle Scholar
  57. Liu, Z., Meyerowitz, E. M. 1995 LEUNIG regulates AGAMOUS expression in Arabidopsis flowersDevelopment121975991PubMedGoogle Scholar
  58. Liu, Z., Franks, R.G., Klink, V.P. 2000Regulation of gynoecium marginal tissue formation by LEUNIG and AINTEGUMENTA Plant Cell1218791892PubMedCrossRefGoogle Scholar
  59. Mable, B. K., Robertson, A. V., Dart, S., di, Berardo C., Witham, L. 2005Breakdown of self-incompatibility in the perennial Arabidopsis lyrata (Brassicaceae) and its genetic consequencesEvolution5914371448PubMedGoogle Scholar
  60. Masters, M. T. 1869Vegetable teratology: an account of the principle deviations from the usual construction of plantsRay SocietyLondonGoogle Scholar
  61. Mauricio, R. 2001Mapping quantitative trait loci in plants: uses and caveats for evolutionary biologyNature Rev. Genet.2370381CrossRefPubMedGoogle Scholar
  62. Meyerowitz, E. M., Smyth, D. R., Bowman, J. L. 1989Abnormal flowers and pattern formation in floral developmentDevelopment106209217Google Scholar
  63. Mitchell-Olds, T. 2001 Arabidopsis thaliana and its wild relatives: a model system for ecology and evolutionTrends Ecol. Evol.16693700CrossRefGoogle Scholar
  64. Murbeck S. V. (1918) Über staminale Pseudapetalie und deren Bedeutung für die Frage nach der Herkunft der Blütenkrone. Lunds Universitets Arsskrift N.F. Avd. 2, Bd. 14, Nr. 25, Lund.Google Scholar
  65. Opiz P. M. (1821) 2. Capsella apetala Opiz. Eine neue merkwürdige Pflanze. Flora Nr. 28, oder: Botanische Zeitung, Regensburg, 28. Juli 1821.Google Scholar
  66. Pelaz, S., Ditta, G. S., Baumann, E., Wisman, E., Yanofsky, M. F. 2000B and C floral organ identity functions require SEPALLATA MADS-box genesNature405200203PubMedCrossRefGoogle Scholar
  67. Pinyopich, A., Ditta, G. S., Savidge, B., Liljegren, S. J., Baumann, E., Wisman, E., Yanofsky, M. F. 2003Assessing the redundancy of MADS-box genes during carpel and ovule developmentNature4248588PubMedCrossRefGoogle Scholar
  68. Reichert, H. 1998Eine kronblattlose Sippe des Hirtentäschels (Capsella bursa-pastoris) seit Jahren bestandsbildend bei Gau-Odernheim/RheinhessenHessische Floristische Rundbriefe475355Google Scholar
  69. Riechmann, J. L., Meyerowitz, E. M. 1997MADS domain proteins in plant developmentBiol. Chem.37810791101PubMedCrossRefGoogle Scholar
  70. Riedl, R. 1977A systems-analytical approach to macro-evolutionary phenomenaQuarterly Rev. Biol.52351370CrossRefGoogle Scholar
  71. Ronse, De Craene L. P. 2003The evolutionary significance of homeosis in flowers: a morphological perspectiveInt. J. Pl. Sci.164S225S230CrossRefGoogle Scholar
  72. Rudall, P. J. 2003Monocot pseudanthia revisited: floral structure of the mycoheterotrophic family TriuridaceaeInt. J. Pl. Sci.164S307S320CrossRefGoogle Scholar
  73. Rudall, P. J., Bateman, R. M. 2002Roles of synorganisation, zygomorphy and heterotopy in floral evolution: the gynostemium and labellum of orchids and other lilioid monocotsBiol. Rev.77403441PubMedCrossRefGoogle Scholar
  74. Rudall, P. J., Bateman, R. 2003Evolutionary change in flowers and inflorescences: evidence from naturally occurring terataTrends Pl. Sci.87682CrossRefGoogle Scholar
  75. Rutishauser, R., Moline, P. 2005Evo-devo and the search for homology (“sameness”) in biological systemsTheory Biosci.124213241CrossRefPubMedGoogle Scholar
  76. Sattler, R. 1988Homeosis in plantsAmer. J. Bot.7516061617CrossRefGoogle Scholar
  77. Schlechtendal, D. E. L. (1823) Flora Berolinensis. Berolini 1823.Google Scholar
  78. Shimizu, K. K., Purugganan, M. D. 2005Evolutionary and ecological genomics of ArabidopsisPl. Physiol.138578584CrossRefGoogle Scholar
  79. Shimizu, K., Cork, J. M., Caicedo, A. L., Mays, C. A., Moore, R. C., Olsen, K. M., Ruzsa, S., Coop, G., Bustamante, C. D., Awadalla, P., Purugganan, M. D. 2004Darwinian selection on a selfing locusScience30620812084PubMedCrossRefGoogle Scholar
  80. Shull, G. H. 1914Duplicate genes for capsule-form in Capsella bursa-pastoris Z. Abst. u. Vererbl.1297149CrossRefGoogle Scholar
  81. Stebbins, G. L. 1950Variation and evolution in plantsColumbia University. PressNew YorkGoogle Scholar
  82. Steimer, A., Schöb, H., Grossniklaus, U. 2004Epigenetic control of plant development: new layers of complexityCurr. Opin. Plant Biol.71119PubMedCrossRefGoogle Scholar
  83. Theißen, G. 2000Evolutionary developmental genetics of floral symmetry: the revealing power of Linnaeus' monstrous flowerBioessays22209213PubMedCrossRefGoogle Scholar
  84. Theißen G. (2001a) Development of floral organ identity: stories from the MADS house. Curr. Opin. Pl. Biol. 4: 75–85.Google Scholar
  85. Theißen G. (2001b) Flower development: genetics of identity. Nature 414: 491.Google Scholar
  86. Theißen, G. 2005Birth, life and death of developmental control genes: New challenges for the homology conceptTheory Biosci.124199212PubMedGoogle Scholar
  87. Theißen, G. 2006The proper place of hopeful monsters in evolutionary biologyTheory Biosci.124349369CrossRefPubMedGoogle Scholar
  88. Theißen, G., Saedler, H. 2001Floral quartetsNature409469471PubMedCrossRefGoogle Scholar
  89. Theißen, G., Becker, A., Di, Rosa A., Kanno, A., Kim, J. T., Münster, T., Winter, K.-U., Saedler, H. 2000A short history of MADS-box genes in plantsPl. Molec. Biol.42115149CrossRefGoogle Scholar
  90. Trattinnick L. (1821) Botanische Bemerkungen. Flora 1821, p. 723.Google Scholar
  91. Vergara-Silva, F. 2003Plants and the conceptual articulation of evolutionary developmental biologyBiol. Philos.18249284CrossRefGoogle Scholar
  92. Wagner, G. P. 2000What is the promise of developmental evolution: Part I: Why lis developmental biology necessary to explain evolutionary innovations?J. Exp. Zool. (Mol. Dev. Evol.)2889598CrossRefGoogle Scholar
  93. Wagner, G. P., Laubichler, M. D. 2004Rupert Riedl and the re-synthesis of evolutionary and developmental biology: body plan and evolvabilityJ. Exp. Zool. (Mol. Dev. Evol.)302B92102CrossRefGoogle Scholar
  94. Wagner, G. P., Müller, G. B. 2002Evolutionary innovations overcome ancestral constraints: a re-examination of character evolution in male sepsid flies (Diptera: Sepsidae)Evol. Dev.416PubMedCrossRefGoogle Scholar
  95. Westrich, P. 1990Die Wildbienen Baden-Württembergs: Allgemeiner Teil: Lebensräume, Verhalten, Ökologie, SchutzUlmerStuttgartGoogle Scholar
  96. Wiegmann, A. F. (1823) Correspondenz. Flora 1823.Google Scholar
  97. Xing, S., Rosso, M. G., Zachgo, S. 2005 ROXY1, a member of the plant glutaredoxin family, is required for petal development in Arabidopsis thaliana Development13215551565PubMedCrossRefGoogle Scholar
  98. Zunk, K., Mummenhoff, K., Hurka, H. 1999Phylogenetic relationship in tribe Lepidieae (Brassicaceae) based on chloroplast DNA restriction site variationCanad. J. Bot.7715041512CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Wien 2006

Authors and Affiliations

  • P. Nutt
    • 1
  • J. Ziermann
    • 1
  • M. Hintz
    • 1
  • B. Neuffer
    • 2
  • G. Theißen
    • 1
  1. 1.Lehrstuhl für GenetikFriedrich-Schiller-Universität JenaJenaGermany
  2. 2.Fachbereich Biologie/Chemie, Spezielle BotanikUniversität OsnabrückOsnabrückGermany

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