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(American Journal of Botany. 2009;96:183-206.) doi: 10.3732/ajb.0800254 © 2009 Botanical Society of America, Inc.

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Transmitting tissue architecture in basal-relictual angiosperms: Implications for transmitting tissue origins¹

² Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Ontario, Canada M5S 3B2 ³ Department of Biology, Saint Louis University, St. Louis, Missouri, USA 63103-2010 ⁴ Royal Botanic Gardens, Mrs. Macquaries Road, Sydney, Australia 2000, Australia

ABSTRACT

Carpel transmitting tissue is a major floral innovation that is essential for angiosperm success. It facilitates the rapid adhesion, hydration, and growth of the male gametophyte to the female gametophyte. As well, it functions as a molecular screen to promote male gametophytic competition and species-specific recognition and compatibility. Here, we characterize the transmitting tissue extracellular matrix (ECM) and pollen tube growth in basal-relictual angiosperms and test the hypothesis that a freely flowing ECM (wet stigma) was ancestral to a cuticle-bound ECM (dry stigma). We demonstrate that the most recent common ancestor of extant angiosperms produced an ECM that was structurally and functionally equivalent to a dry stigma. Dry stigmas are composed of a cuticle and primary wall that contains compounds that facilitate the adhesion and growth of the male gametophyte. These compounds include methyl-esterified homogalacturonans, arabinogalactan-proteins, and lipids. We propose that transmitting tissue evolved in concert with an increase in cuticle permeability that resulted from modifications in the biosynthesis and secretion of fatty acids needed for cuticle construction. Increased cuticle permeability exposed the male gametophyte to pre-existing molecules that enabled rapid male gametophyte adhesion, hydration, and growth as well as species-specific recognition and compatibility.

Key Words: arabinogalactan-proteins • cuticle • dry stigma • homogalacturonans • pollen-carpel interactions • pollination droplet • transmitting tissue • wet stigma

Received for publication 23 July 2008. Accepted for publication 24 November 2008.

FOOTNOTES

¹ This manuscript is dedicated to E. Heij, mentor. The authors thank G. W. Rothwell for helpful discussion, K. Sault for technical assistance, and A. Sage for editorial assistance. This research was funded by a Connaught New Faculty Award, University of Toronto start-up funds, and a Natural Sciences and Engineering Research Council of Canada grant to T.L.S. and a National Geographic Grant (#6974-01) to P.B. and T.L.S.

⁴ Author for correspondence (e-mail: tammy.sage{at}utoronto.ca)

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