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Embryology of Manekia naranjoana (Piperaceae) and the origin of tetrasporic, 16-nucleate female gametophytes in Piperales¹

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

ABSTRACT

The vast majority of flowering plant seeds contain a triploid endosperm formed by fertilization of a monosporic, Polygonum-type female gametophyte. However, evolutionary transitions to six other genetic constructs of endosperm are widespread, and six of seven known patterns are found in the order Piperales. Within Piperaceae, Manekia has not been described, and we report its female gametophyte to be tetrasporic and 16-nucleate at maturity. Manekia ontogeny is generally characterized by early establishment of a bipolar or weakly bipolar body plan and a binucleate central cell at maturity (Drusa-type pattern); however, ca. 16% of early stages had distinctly tetrapolar organization, and ca. 21% of mature specimens had a tetranucleate central cell (Penaea-type pattern, not previously reported in Piperaceae). An evolutionary developmental analysis indicates heterochrony, heterotopy, novelties, and sequence deletions have each played roles in modulating variation within Piperales. Our data suggest the common ancestor of Piperaceae was tetrasporic and retained a plesiomorphic bipolar body plan, producing a "functionally bisporic" form of triploid endosperm derived from the lineal descendants of two megaspores and a sperm. Developmental modifications of this tetrasporic, bipolar ontogeny can account for the origin of all three other known "true" tetrasporic endosperm genetic constructs, formed from derivatives of all four megaspores and a sperm. These derived endosperms in turn have higher ploidy, higher potential heterozygosity, and reduced genetic conflicts.

Key Words: Costa Rica • endosperm • evolution of development • heterochrony • Manekia • Piperaceae • Piperales • tetraspory

Received for publication 14 June 2007. Accepted for publication 20 January 2008.

FOOTNOTES

¹ The authors thank B. Hilje for help in the field in Costa Rica and T. Feild, P. Rudall, E. Schilling, M. Taylor, and one anonymous reviewer for helpful comments on the manuscript. They are grateful for financial support from the McClure Fund (International Center, University of Tennessee), the Department of Ecology and Evolutionary Biology, and IdeaWild (Fort Collins, CO) to T.A. and from the National Science Foundation (DEB 0640792) to J.H.W.

² Author for correspondence (e-mail: tavd4{at}mizzou.edu); present address: 109 Tucker Hall, Division of Biological Sciences, University of Missouri, Columbia, MO 65211 USA

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