Transmitting tissue architecture in basal‐relictual angiosperms: Implications for transmitting tissue origins

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.

The effect of high temperature stress on male and female reproduction in plants

“…High temperature, pollen germination, tube growth and ovule development, and ovule penetration by pollen tubes Successful pollen germination on the stigma and growth of the pollen tube to the female gametophyte to deliver sperm is dependent on cell-to-cell interactions between the pollen grain/tube and transmitting tissues (stigma, style, and ovary; Sage et al, 2009;Chae and Lord, 2011). In comparison to anther and pollen development, few studies have examined the effect of HT on transmitting tissue and ovule development and in vivo post-pollination events.…”

Homogalacturonan deesterification during pollen–ovule interaction in Larix decidua Mill.: an immunocytochemical study

“…However, in both angiosperms and gymnosperms, ecm of the female reproductive organs should provide specific ions and molecules necessary for nutrition, attraction and guidance of the male gametophyte. Many studies in angiosperms have shown that the pollen–pistil interaction involves such ecm components as homogalacturonan, arabinogalactan proteins and calcium ions (Cheung et al 1995; Jauh and Lord 1996; Mollet et al 2000; Lenartowska et al 2001; Zhao et al 2004; Bednarska et al 2005; Hristova et al 2005; Coimbra et al 2007; Ge et al 2009; Sage et al 2009; Costa et al 2013). …”

Female gamete competition in an ancient angiosperm lineage

“…In addition, the differentiation of a transmitting tissue within the carpel that supports pollen tube growth to the ovule has long been viewed as promoting male competition and increasing maternal choice of sperm donors (7,8). The formation of callose plugs within pollen tubes recently has been hypothesized to have enabled male gametophytes to grow at higher rates and compete over greater distances than was the case for the immediate ancestors of angiosperms (8,9).…”

“…Finally, the evolution of insect pollination in conjunction with the early diversification of floral morphology and anatomy are widely viewed to have led to increased levels of pollen reception and hence, male-male competition (4). Collectively, the evolution of the carpel, extragynoecial compitum, transmitting tissue, callose plugs, and insect pollination seems to have resulted in significantly enhanced levels of prefertilization male competition and maternal choice, and thus may have played a major role in the early diversification of angiosperms (4)(5)(6)(7)(8)(9).…”