Pollen-Specific, but Not Sperm-Specific, Genes Show Stronger Purifying Selection and Higher Rates of Positive Selection Than Sporophytic Genes in Capsella grandiflora

Abstract

Selection on the gametophyte can be a major force shaping plant genomes as 7-11% of genes are expressed only in that phase and 60% of genes are expressed in both the gametophytic and sporophytic phases. The efficacy of selection on gametophytic tissues is likely to be influenced by sexual selection acting on male and female functions of hermaphroditic plants. Moreover, the haploid nature of the gametophytic phase allows selection to be efficient in removing recessive deleterious mutations and fixing recessive beneficial mutations. To assess the importance of gametophytic selection, we compared the strength of purifying selection and extent of positive selection on gametophyte- and sporophyte-specific genes in the highly outcrossing plant Capsella grandiflora. We found that pollen-exclusive genes had a larger fraction of sites under strong purifying selection, a greater proportion of adaptive substitutions, and faster protein evolution compared with seedling-exclusive genes. In contrast, sperm cell-exclusive genes had a smaller fraction of sites under strong purifying selection, a lower proportion of adaptive substitutions, and slower protein evolution compared with seedling-exclusive genes. Observations of strong selection acting on pollen-expressed genes are likely explained by sexual selection resulting from pollen competition aided by the haploid nature of that tissue. The relaxation of selection in sperm might be due to the reduced influence of intrasexual competition, but reduced gene expression may also be playing an important role.

The Molecular Dialog between Flowering Plant Reproductive Partners Defined by SNP-Informed RNA-Sequencing

“…Molecules involved in gamete:gamete recognition have been shown to evolve rapidly and to be responsible for specieslevel discrimination in mating interactions (Metz et al, 1998;Clark et al, 2006). Interestingly, it was recently shown that the pollen tube expresses a larger fraction of species-limited genes than other tissues (Arunkumar et al, 2013;Gossmann et al, 2014), which is consistent with the idea that pollen tubes may express species-limited proteins that determine their species-level identity. To address whether groups of genes expressed in reproductive tissues maintain higher rates of sequence diversity, we calculated Col versus Cvi exonic SNP rates and compared them to control rates simulated using 100 sets of randomly selected genes of the same number.…”

Discovery of novel transcripts and gametophytic functions via RNA-seq analysis of maize gametophytic transcriptomes

“…Second, differentiating it from the female gametophyte (which did not show such preferential retention), in an outcrossing species such as maize, pollen and the pollen tube are potentially under more stringent selection than other phases of the life cycle, via intense competition as a haploid for efficient pollen tube germination, tip growth and fertilization processes. Consistent with this idea, pollen-specific genes in an outcrossing relative of Arabidopsis (Capsella grandiflora) are associated with stronger purifying selection and greater proportion of adaptive substitutions than sporophytespecific genes [78]. In this interpretation of gene balance, one would expect to see a larger percentage of pollencritical genes to be retained as duplicates in maize, and furthermore, that mutation of either copy should result in a deleterious phenotype.…”

Evolutionary Fates and Dynamic Functionalization of Young Duplicate Genes in Arabidopsis Genomes

“…Second, these tissues may experience fast evolutionary rates due to their haploid nature and the strong selection forces they undergo and are associated with sexual selection and sperm/pollen competition. Thus, these tissues may appear as evolutionarily accommodating, welcoming and tolerating genomic and functional innovations such as new genes (Bernasconi et al, 2004;Kaessmann, 2010;Arunkumar et al, 2013). More importantly, both methylation levels and the abundances of active histone modifications in promoter regions are significantly and temporally associated with the ages of duplicate genes.…”