The Diversity of the Pollen Tube Pathway in Plants: Toward an Increasing Control by the Sporophyte

Abstract

Plants, unlike animals, alternate multicellular diploid, and haploid generations in their life cycle. While this is widespread all along the plant kingdom, the size and autonomy of the diploid sporophyte and the haploid gametophyte generations vary along evolution. Vascular plants show an evolutionary trend toward a reduction of the gametophyte, reflected both in size and lifespan, together with an increasing dependence from the sporophyte. This has resulted in an overlooking of the importance of the gametophytic phase in the evolution of higher plants. This reliance on the sporophyte is most notorious along the pollen tube journey, where the male gametophytes have to travel a long way inside the sporophyte to reach the female gametophyte. Along evolution, there is a change in the scenery of the pollen tube pathway that favors pollen competition and selection. This trend, toward apparently making complicated what could be simple, appears to be related to an increasing control of the sporophyte over the gametophyte with implications for understanding plant evolution.

The role of the integuments in pollen tube guidance in flowering plants

“…In flowering plants, during the progamic phase before fertilization, the pollen tube has to travel through the stigma and the style of the flower to reach the female gametophyte inside the ovule. During the first interaction between the pollen tube and the sporophytic tissue of the stigma, an abundant extracellular secretion from the stigma exudate that supports heterotrophic pollen tube growth is typically observed in angiosperms with wet stigmas (Heslop-Harrison & Shivanna, 1977;Herrero, 1992;Lora et al, 2016). After pollen germination, the pollen tube grows through the style, and several molecules, such as reactive oxygen species (ROS) (McInnis et al, 2006;Hiscock, 2008;Zafra et al, 2010), esterases (Hiscock et al, 2002), lipids (Wolters-Arts et al, 1998;Hiscock, 2008), calcium (Ge et al, 2007(Ge et al, , 2009 and arabinogalactan proteins (AGPs) (Edlund et al, 2004;Hiscock, 2008), have been reported to be essential for pollen tube growth and guidance.…”

Morphological diversity and function of the stigma in Ficus species (Moraceae)

“…This control over the access of pollen tubes to style and ovary and, consequently, to ovules, is evidenced by systems of pollen-stigma recognition and compatibility (Heslop-Harrison, 1982;Heslop-Harrison et al, 1975). It should be noted that the selective role in pollen tube growth is not restricted to the stigma (Erbar, 2003;Lora et al, 2016) but is also performed by the compitum (Endress, 1982;Wang et al, 2012). The compitum (from the Latin crossing or crossroads) is a term applied to places of convergence of several growing pollen tubes, forming a competition arena.…”

Pollen-Pistil Interactions and Their Role in Mate Selection

“…However, the pistil also is a venue for mate selection at the interspecies level, since it is an arena for postmating, prezygotic barriers that rely on pollen-pistil interactions. This class of interspecific reproductive barriers includes conspecific pollen precedence, the preferential success of conspecific pollen compared with heterospecific pollen (Howard, 1999;Fishman et al, 2008;Lora et al, 2016), and pollen tube guidance and reception. Here, we focus on outright interspecific pollen tube rejection.…”

“…It serves a protective role and functions as a conduit for pollen tubes to grow to the ovary, but it also provides a venue for pollen-pistil interactions that regulate pollen tube growth and, hence, fertilization. Although the earliest diverging angiosperm lineages do not possess the full set of canonical angiosperm pistil traits (Endress and Doyle, 2009;Endress, 2011Endress, , 2015Lora et al, 2016), the core lineages (which display the most diversity) have a stigma specialized for the receipt of pollen and a style that pollen tubes must traverse before fertilization can occur. Some authors attribute angiosperm diversity to phenomena that depend on pollen-pistil interactions taking place in stigmas and styles, such as pollen competition and self-incompatibility (SI; Mulcahy and Mulcahy, 1988;Williams, 2012).…”