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Amborella trichopoda (Amborellaceae) and the evolutionary developmental origins of the angiosperm progamic phase¹

Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, Tennessee 37996 USA

ABSTRACT

A remarkable number of the defining features of flowering plants are expressed during the life history stage between pollination and fertilization. Hand pollinations of Amborella trichopoda (Amborellaceae) in New Caledonia show that when the stigma is first receptive, the female gametophyte is near maturity. Pollen germinates within 2 h, and pollen tubes with callose walls and plugs grow entirely within secretions from stigma to stylar canal and ovarian cavity. Pollen tubes enter the micropyle within 14 h, and double fertilization occurs within 24 h. Hundreds of pollen tubes grow to the base of the stigma, but few enter the open stylar canal. New data from Amborella, combined with a review of fertilization biology of other early-divergent angiosperms, show that an evolutionary transition from slow reproduction to rapid reproduction occurred early in angiosperm history. I identify increased pollen tube growth rates within novel secretory carpel tissues as the primary mechanism for such a shift. The opportunity for prezygotic selection through interactions with the stigma is also an important innovation. Pollen tube wall construction and substantial modifications of the ovule and its associated structures greatly facilitated a new kind of reproductive biology.

Key Words: Amborella • callose plug • carpel • double fertilization • evolution of development • heterochrony • novelty • origin of angiosperms • pollen tube growth • stigma

Received for publication 21 February 2008. Accepted for publication 22 August 2008.

FOOTNOTES

¹ The author thanks T. Jaffré (L’Institut de Recherche pour le Développement, Noumea, New Caledonia) for logistical support and T. Arias and M. L. Taylor for laboratory assistance. H. G. Dickinson, A. N. Doust, T. S. Feild, W. E. Friedman, and L. Hufford provided many helpful comments. Funding was provided by the University of Tennessee and the National Science Foundation (DEB 0640792). The author especially thanks W. E. Friedman for encouragement and for travel support in New Caledonia.

² E-mail: joewill{at}utk.edu

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