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.

Keywords: evolution; gametophyte; genomics; ovule; pollen; selection.

Figure 1

Two Key Questions Should Guide Future Research on Gametophytic Selection. Three approaches can be used to determine the prevalence of gametophytic selection: (A) Investigate gene-expression overlap between the gametophyte and sporophyte. (B) Reverse genetics: evaluate the impact of genetic knockouts on gametophytes. (C) Forward genetics: scan genome-wide for associations between alleles and gametophyte phenotypes (GWAS). To evaluate the effects of gametophytic selection on sporophytes, the following studies will be useful: (D) Use the allele frequency spectrum (AFS) to compare the frequency of alleles with effects on gametophyte fitness to neutral expectations. (E) Conduct artificial selection on gametophytes to evaluate the impact on the sporophyte (see, e.g. Domínguez et al., 2005 on selection for cold tolerance in tomatoes). (F) Use linked neutral genetic diversity to infer signals of past selection.

Figure 2

Gene Expression Overlap between Gametophyte and Sporophyte The observed overlap in gene expression between the sporophyte and female and male gametophytes in (A)Arabidopsis thaliana (data from Borges et al., 2008 and Wuest et al., 2010) and (B)Zea mays (data from Chettoor et al., 2014). See Supplemental Table 1 for numerical values.

Figure 3

Ploidy and Mating-System Comparisons Offer Insight into the Influence of Selection on Pollen Competition. (A) Increased ploidy affects dominance expectations in both the sporophyte and the gametophyte because ploidies greater than 2N can mask deleterious alleles even in the gametophyte stage. (B) The comparison between outcrossing and selfing mating systems highlights that selfers should experience increased purging in the sporophyte, resulting in more similar selection on recessive alleles between gametophytes and sporophytes. Reduced competition may also decrease investment in pollen compared with ovules. (C) In dioecious plants, the linkage of pollen-beneficial alleles to the Y chromosome may increase Y-bearing pollen competitive ability and skew sex ratios to male (XY) bias. However, the long-term impact of large linked regions of suppressed recombination can lead to degeneration of Y-linked pollen genes and to an increased competitive ability of X-bearing pollen, resulting in a skew to female-biased (XX) sex ratios.

Figure 4

Pleiotropic Effects of Gametophytic Selection on Sporophyte. Summary of the population genetic effects of negative/antagonistic and positive or neutral effects of gametophytic selection on sporophyte fitness. Positive covariances can accelerate evolution and give signals of elevated rates of adaptive evolution, and are expected to reduce the amount of standing variation in natural populations. In contrast, negative covariances can have a variety of effects, and may lead to balancing selection, showing population genetic signals of high diversity and an excess of common alleles, or positive and purifying selection, if the conditions for the maintenance of variation are not met.