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

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.

Pollen Developmental Arrest: Maintaining Pollen Fertility in a World With a Changing Climate

“…Bi-cellular pollen is immature and loses water upon dehiscence in the atmosphere. This pollen is rehydrated when it is captured by the stigma of a receptor plant before the second asymmetric mitotic division occurs (Nepi et al, 2009; Von Aderkas et al, 2018; Williams and Brown, 2018). The interruption in pollen development observed for bi-cellular pollen is similar to a true DA situation because the cell cycle is arrested.…”

Pollination Drop Proteome and Reproductive Organ Transcriptome Comparison in Gnetum Reveals Entomophilous Adaptation

“…Pollination drops are essential in gymnosperm reproduction, providing a site for pollen attachment and a medium for germination [22,23,24,25,26]. Gymnosperm pollination drops are composed of carbohydrates, minerals, lipids, amino acids and proteins [25,26,27,28]. Among these chemicals, sugars such as sucrose are the main reward for insect pollinators, and are therefore comparable to floral nectar in angiosperms [25,26,27,29].…”

Insect pollination of cycads

“…One trait of gymnosperms, pollination droplets or micropylar droplets has been proposed as a potential mechanism involved in the origin of insect pollination (Labandeira et al 2007;Nepi et al 2009). Pollination droplets, produced and secreted by the ovule of most gymnosperms, are used for pollen capture (Labandeira et al 2007;von Aderkas et al 2018). Most species secrete a pollination droplet from the ovule through a narrow canal (the micropylar tube): the droplet captures pollen and is then withdrawn, transporting the pollen to the nucellus where the pollen produces pollen tubes (Nepi et al 2009).…”

“…2007; von Aderkas et al . 2018). Most species secrete a pollination droplet from the ovule through a narrow canal (the micropylar tube): the droplet captures pollen and is then withdrawn, transporting the pollen to the nucellus where the pollen produces pollen tubes (Nepi et al .…”

“…Pollen capture using pollination droplets appears to be an ancestral trait of gymnosperms (von Aderkas et al . 2018), but it is not known whether pollination droplets were present in the common ancestor of all seed plants or are a synapomorphy for gymnosperms.…”