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Analysis of a naturally occurring floral homeotic mutant of shepherd's purse (Capsella bursa-pastoris)

Fachliche Zuordnung Zell- und Entwicklungsbiologie der Pflanzen
Förderung Förderung von 2004 bis 2017
Projektkennung Deutsche Forschungsgemeinschaft (DFG) - Projektnummer 5434171
 
Erstellungsjahr 2019

Zusammenfassung der Projektergebnisse

In homeotic mutants some organs are transformed into organs of another type. A textbook example is "Antennapedia" of the fruitfly "Drosophila melanogaster" which has antennae replaced by legs. It is widely believed that due to the drastic change of their body plan, homeotic mutants cannot exist for long in the wild. Hence, they are unable to establish new organismic lineages and are, therefore, of no evolutionary relevance. In this project we have shown that this is not always the case. We have studied a homeotic mutant of shepherd’s purse (Capsella bursa-pastoris), a widely distributed, little weed. In the flowers of the mutant, all petals are transformed into stamens, while the identity of all other organs is unchanged. We hence termed the mutant "Stamenoid petals (Spe)". Plants with a Spe phenotype are known from several places in Europe, where they have existed sometimes at least for several decades, often together with wild type plants. Thus, the fitness of Spe plants cannot be much lower than that of wild-type plants, at least under prevalent growth conditions. Historically, Spe plants have even been described as a different species (Capsella apetala). In our project we wanted to understand why the Spe mutant can successfully co-exist with wild-type plants despite the drastic modification of the floral body plan, and which molecular genetic mechanism generated the mutant phenotype. Some studies on the performance of Spe plants in the wild were conducted in cooperation with a group at the university of Osnabrück. Collectively our data show that, at least under the investigated growth conditions, wild type plants produce more flowers and fruits, but that mutant fruits contain more seeds and/or that these seeds germinate better than wild type seeds. In consequence, both plant variants potentially produce about the same number of seedlings per plant, explaining why they can co-exist. In addition, Spe plants flower later than wild type plants, suggesting that a difference in flowering time is involved in keeping populations of the two plant variants apart. Our genetic data show that the Spe phenotype is based on a dominant mutation, very likely at a single locus. We identified one of the class C floral homeotic genes of C. bursa-pastoris, CbpAGAMOUSa (CbpAGa), as the Spe locus. Class C floral homeotic genes are involved in specifying stamen identity in developing flowers. Our molecular data reveal that a mobile genetic element jumped into the CbpAGa gene. This led to an extension of the expression domain of CbpAGa towards the second floral whorl, such that the primordia of these organs develop into stamens. In the wild type, without class C (CbpAGa) gene activity, petals develop in the second whorl. In summary, our data explain how a homeotic mutant can originate and how it can survive in the wild. Even though homeotic mutants may only very rarely be founders of novel organismic lineages, such cases could be of utmost importance for the evolutionary origin of novelties and, eventually, biodiversity. The data and insights gathered during our project resulted in six publications in international peer reviewed journals up to now, even though almost all data concerning the proximate cause (molecular mechanism) of Spe have not even been published yet; the respective manuscript is currently in preparation.

Projektbezogene Publikationen (Auswahl)

  • (2006). Capsella as a model system to study the evolutionary relevance of floral homeotic mutants. Pl. Syst. Evol. 259, 217-235
    Nutt, P., Ziermann, J., Hintz, M., Neuffer, B., and Theißen, G.
  • (2006). Catching a ‘hopeful monster’: shepherd’s purse (Capsella bursapastoris) as a model system to study the evolution of flower development. J. Exp. Bot. 57, 3531-3542
    Hintz, M., Bartholmes, C., Nutt, P., Ziermann, J., Hameister, S., Neuffer, B., and Theißen, G.
  • (2008). Germline transformation of Shepherd’s purse (Capsella bursa-pastoris) by the floral dip method as a tool for evolutionary and developmental biology. Gene 409, 11-19
    Bartholmes, C., Nutt, P., and Theißen, G.
  • (2009). Floral visitation and reproductive traits of Stamenoid petals, a naturally occuring floral homeotic variant of Capsella bursa-pastoris (Brassicaceae). Planta 230, 1239-1249
    Ziermann, J., Ritz, M., Hameister, S., Abel, C., Hoffmann, M.H., Neuffer, B., and Theißen, G.
  • (2010). Homeosis of the angiosperm flower: Studies on three candidate cases of saltational evolution. Palaeodiversity 3, Supplement: 131-139
    Theißen, G.
  • (2011). The genetics of Capsella. In: Genetics and Genomics of the Brassicaceae (Schmidt, R. and Bancroft I., Eds.), 1st Edition, Plant Genetics and Genomics: Crops and Models, Vol. 9. Springer New York, pp. 373 – 387
    Theißen, G.
  • (2013). Mapping a floral trait in Shepherds purse – ‘Stamenoid petals’ in natural populations of Capsella bursapastoris (L.) Medik. Flora 208, 641-647
    Hameister, S., Nutt, P., Theißen, G., and Neuffer, B.
    (Siehe online unter https://doi.org/10.1016/j.flora.2013.09.008)
 
 

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