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First published online December 11, 2008; doi:10.3732/ajb.0800027 American Journal of Botany 96: 67-82 (2009) © 2009 Botanical Society of America, Inc.

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Nonflowers near the base of extant angiosperms? Spatiotemporal arrangement of organs in reproductive units of Hydatellaceae and its bearing on the origin of the flower¹

² Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3AB, UK ³ Department of Higher Plants, Biological Faculty, Moscow State University 119991, Moscow, Russia ⁴ The University of Western Australia, Crawley, Washington 6009, Australia

ABSTRACT

Reproductive units (RUs) of Trithuria, the sole genus of the early-divergent angiosperm family Hydatellaceae, are compared with flowers of their close relatives in Cabombaceae (Nymphaeales). Trithuria RUs combine features of flowers and inflorescences. They differ from typical flowers in possessing an "inside-out" morphology, with carpels surrounding stamens; furthermore, carpels develop centrifugally, in contrast to centripetal or simultaneous development in typical flowers. Trithuria RUs could be interpreted as pseudanthia of two or more cymose partial inflorescences enclosed within an involucre, but the bractlike involucral phyllomes do not subtend partial inflorescences and hence collectively resemble a typical perianth. Teratological forms of T. submersa indicate a tendency to fasciation and demonstrate that the inside-out structure—the primary feature that separates RUs of Hydatellaceae from more orthodox angiosperm flowers—can be at least partially modified, thus producing a morphology that is closer to an orthodox flower. The Trithuria RU could be described as a "nonflower", i.e., a structure that contains typical angiosperm carpels and stamens but does not allow recognition of a typical angiosperm flower. The term nonflower could combine cases of secondary loss of flower identity and cases of a prefloral condition, similar to those that gave rise to the angiosperm flower. Nonhomology among some angiosperm flowers could be due to iterative shifts between nonfloral construction and flower/inflorescence organization of reproductive organs. Potential testing of these hypotheses using evolutionary-developmental genetics is explored using preliminary data from immunolocalization of the floral meristem identity gene LEAFY in T. submersa, which indicated protein expression at different hierarchical levels.

Key Words: angiosperm • development • evo-devo • flower • Hydatellaceae • immunolocalization • inflorescence • LEAFY • ontogeny • pseudanthium • Trithuria

Received for publication 21 January 2008. Accepted for publication 11 June 2008.

FOOTNOTES

¹ The authors thank R. Bateman, P. Endress, T. Ezhova, and M. Logacheva for helpful discussion, J. Bogner for fixed material of Ceratophyllum and Chloranthus from Munich Botanic Garden, and Y. Pillon for fixed flowers of Amborella. T. Macfarlane provided ongoing support in Australia. The Darwin Herbarium (DNA) gave permission to examine herbarium material of Trithuria. D. Baum supplied the LEAFY antibodies, and I. Cacho provided help to GP with immunolocalization protocols. M. Ramsay propagated Trithuria at Kew. R. Bateman took the plant photographs in Fig. 2A, B. The authors thank the staff of the Cross-Departmental Laboratory of Electron Microscopy at Moscow University for their assistance. The research was partly supported by a 2007 CoSyst grant, funded by BBSRC. M.V.R. and D.D.S. acknowledge support from RFBR (grant no. 06-04-48113).

⁵ Author for correspondence (e-mail p.rudall{at}kew.org)

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