The Evolution of Sexual Fluids in Gymnosperms From Pollination Drops to Nectar.

Natalie A. Prior,Stefan A. Little,Patrick von Aderkas

doi:10.3389/fpls.2018.01844

Abstract

A current synthesis of data from modern and fossil plants paints a new picture of sexual fluids, including nectar, as a foundational component of gymnosperm reproductive evolution. We review the morpho-anatomical adaptations, their accompanying secretions, and the functional compounds involved. We discuss two types of secretions: (1) those involved in fertilization fluids produced by gametophytes and archegonia of zooidogamous gymnosperms, i.e., Ginkgo and cycads, and (2) those involved in pollen capture mechanisms (PCMs), i.e., pollination drops. Fertilization fluids provide both liquid in which sperm swim, as well as chemotactic signals that direct sperm to the egg. Such fertilization fluids were probably found among many extinct plants such as ancient cycads and others with swimming sperm, but were subsequently lost upon the evolution of siphonogamy (direct delivery of sperm to the egg by pollen tubes), as found in modern gnetophytes, conifers, and Pinaceae. Pollination drops are discussed in terms of three major types of PCMs and the unique combinations of morphological and biochemical adaptations that define each. These include their amino acids, sugars, calcium, phosphate and proteins. The evolution of PCMs is also discussed with reference to fossil taxa. The plesiomorphic state of extant gymnosperms is a sugar-containing pollination drop functioning as a pollen capture surface, and an in ovulo pollen germination medium. Additionally, these drops are involved in ovule defense, and provide nectar for pollinators. Pollination drops in anemophilous groups have low sugar concentrations that are too low to provide insects with a reward. Instead, they appear to be optimized for defense and microgametophyte development. In insect-pollinated modern Gnetales a variety of tissues produce sexual fluids that bear the biochemical signature of nectar. Complete absence of fluid secretions is restricted to a few, poorly studied modern conifers, and is presumably derived. Aspects of pollination drop dynamics, e.g., regulation of secretion and retraction, are reviewed. Lastly, we discuss pollination drops’ control of pollen germination. Large gaps in our current knowledge include the composition of fertilization fluids, the pollination drops of Podocarpaceae, and the overall hydrodynamics of sexual fluids in general.

Highlights

Fluids play major roles during reproduction of gymnosperms
Ovule-derived fluids are almost universally found in pollen capture mechanisms (PCMs)
In our simplified classification of PCMs, we present two other basic types of PCMs, β and γ that relate to both primary pollen capture surface and clade

Summary

Introduction

Fluids play major roles during reproduction of gymnosperms. Ovule-derived fluids are almost universally found in pollen capture mechanisms (PCMs). A critical feature of gymnosperm pollination is that in almost all species the primary capture surface for pollen is an ovular secretion (Williams, 2009). This is called a pollination drop (Singh, 1978). Pollination drops are a common part of extant gymnosperm pollination biology (Figure 1), and are found in all modern clades: Ginkgo (Figure 2A), cycads (Figure 2B), conifers (Figures 2C–E), and Gnetales (Figures 2F–I). These liquidbased interactions between ovule and pollen are likely to be of ancient origin. Pollination drops provide ovule defense against microbes during reproduction (Little et al, 2014)

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Conclusion