Evolutionary Genomics of Plant Gametophytic Selection

Abstract

It has long been recognized that natural selection during the haploid gametophytic phase of the plant life cycle may have widespread importance for rates of evolution and the maintenance of genetic variation. Recent theoretical advances have further highlighted the significance of gametophytic selection for diverse evolutionary processes. Genomic approaches offer exciting opportunities to address key questions about the extent and effects of gametophytic selection on plant evolution and adaptation. Here, we review the progress and prospects for integrating functional and evolutionary genomics to test theoretical predictions, and to examine the importance of gametophytic selection on genetic diversity and rates of evolution. There is growing evidence that selection during the gametophyte phase of the plant life cycle has important effects on both gene and genome evolution and is likely to have important pleiotropic effects on the sporophyte. We discuss the opportunities to integrate comparative population genomics, genome-wide association studies, and experimental approaches to further distinguish how differential selection in the two phases of the plant life cycle contributes to genetic diversity and adaptive evolution.

Gametophyte genome activation occurs at pollen mitosis I in maize

“…>10 6 pollen grains per maize plant) and intense competition during dispersal and fertilization. It is thus not surprising that pollen selection has diverse consequences 3 : reducing inbreeding depression 8 , increasing offspring fitness 9 , and contributing to sex chromosome evolution 10 and sex-specific differences in recombination rates 11 . Pollen selection has further been employed in breeding programs to derive cold-tolerant crop varieties 12, 13 .…”

“… AbstractFlowering plants alternate between multicellular haploid (gametophyte) and diploid (sporophyte) generations. One consequence of this life cycle is that plants face substantial selection during the haploid phase 1–3 . Pollen actively transcribes its haploid genome 4 , providing phenotypic diversity even among pollen grains from a single plant.…”

Plant sexual reproduction: perhaps the current plant two-sex model should be replaced with three- and four-sex models?

“…Furthermore, the process of pollination is often regarded as being a part of “fertilization,” thus extending the concept of “fertilization” to include events from pollination through actual zygote formation (Till-Bottraud et al 2005 ; Castilla et al 2016 ; Taiz and Taiz 2017 ) (Table 1 ). Also under the two-sex model there often is consideration of how some angiosperm species are said to carry out “self-fertilization,” by which it is implied that a “hermaphroditic” angiosperm sporophytic individual “mates” with itself in some fashion (Brewbaker and Natarajan 1960 ; Barrett 2002 ; Cruzan and Barrett 2016 ; Grossenbacher et al 2016 ; Beaudry et al 2020 ), and so this one individual sporophytic organism is suggested to achieve zygote formation all by itself.…”

“…The genetic expressions used in sporophytes may well differ from that used in gametophytes. This topic has received some attention as various studies have been done that explore gene expression and other differences between gametophytes and sporophytes, or in gametophytes across time (Bokvaj et al 2015 ; Beaudry et al 2020 ; Liu and Wang 2021 ). Some studies suggest that the development of the angiosperm gametophytes may use distinct systems of differentiation leading to gamete formation relative to the controls used for entry of some sporophytic cells into meiosis (Ranganath 2003 ; Zhao et al 2017 ).…”

Plant Evolutionary Adaptation

“…However, it is important to keep in mind that selection can also act on the gametophytic stage. Furthermore, as pointed out in a review of the genomics of gametophytic selection ( Beaudry et al., 2020 ) in this issue, gametophytes are haploid and lack heterozygosity, so selection will act more efficiently on both deleterious and dominant mutations than in diploid sporophytes. Beaudry et al.…”