Genomic regulation of plant mating systems: flexibility and adaptative potential. A commentary on: ‘A new genetic locus for self-compatibility in the outcrossing grass species perennial ryegrass (Lolium perenne)’

Abstract

This article comments on:

Lucy M. Slatter, Susanne Barth, Chloe Manzanares, Janaki Velmurugan, Iain Place and Daniel Thorogood A new genetic locus for self-compatibility in the outcrossing grass species perennial ryegrass (Lolium perenne), Annals of Botany, Volume 127, Issue 6, 7 May 2021, Pages 715–722, https://doi.org/10.1093/aob/mcaa140

The evolutionary dynamics of plant mating systems have fascinated theoretical and empirical population geneticists, ecologists and plant breeders since at least the time of Darwin. A shift from outcrossing to inbreeding is one of the most commonly observed evolutionary transitions but represents an intriguing paradox: since inbreeding reduces genetic variation and so theoretically should reduce adaptive potential, why is there a strong association between successful invasion of novel habitats and self-compatibility (SC)? Studies like that of Slatter et al. (2021) in this issue could provide important insights.

Although the focus of the study by Slatter et al. (2021) was in resolving the genetic basis of loss of SI to aid in genomic selection for crop breeding, their results could have implications for resolving mechanisms for rapid adaptation to changing ecological conditions in natural environments. They used a genotyping by sequencing approach to identify regions associated with loss of self-incompatibility (SI) in a normally outcrossing perennial grass (Lolium perenne), for which prevention of self-fertilization is controlled gametophytically (i.e. with specificity determined by the haploid genotype of the pollen grains) by two loci (S and Z) on separate linkage groups (LG1 and LG2). Unexpectedly, they identified the strongest association with SI phenotypes at a single quantitative trait locus (QTL) on a linkage group (LG6) not associated with the self-recognition reaction. What is intriguing is that although the authors had previously found a similarly strong unlinked candidate gene region using a different set of F₂ individuals segregating for an SC phenotype (Thorogood et al., 2005), this was not on the same linkage group as identified here and they also had identified a locus apparently linked to the S locus; neither of these QTLs was found in the present study. Importantly, this could suggest that there is more flexibility in the regulation of mating systems than previously considered; different loci on different chromosomes might have the ability to disrupt the SI system, even between individuals within a single species.

Although reversions to SI have been observed only rarely (if at all) in phylogenetic comparisons at the level of species, flexible regulation of plant mating systems could be beneficial within species exposed to variable environmental conditions (Slatter et al., 2021). It is tempting to draw parallels with ecological speciation and biological invasions in animals. In classic cases such as sticklebacks and salmonids, genomic approaches have revolutionized understanding of rapid phenotypic change without underlying genetic changes. Epigenetics, as defined as changes in gene expression rather than mutations in underlying coding sequences, is now known to play a critical role in efficient adaptation to changing environmental conditions, including during invasions (Carneiro and Lyko, 2020). Such changes in gene expression can confer a reversible phenotype (i.e. phenotypic plasticity) subject to selection, although eventually reproductive isolation resulting from differential resource utilization could lead to speciation (i.e. fixed mutational differences between lineages).

The same could be true of plant mating systems: reversible regulation of SI through the action of one or more potential modifiers that would allow rapid adaptation to changing environmental conditions (e.g. during postglacial range expansions), with eventual accumulation of non-functional mutations in S genes due to relaxation of selection during transitional periods. Newly SC plants (i.e. before evolution of the ‘selfing syndrome’ observed in highly selfing species of both plants and animals; Cutter, 2019) could preserve adaptive potential through outcrossing, thus experiencing the best of both worlds: reproductive assurance when invading new habitats and preservation of genetic diversity in the face of climatic change. If true, this scenario could resolve another paradox: the theoretical instability of mixed mating systems due to the challenges of maintaining coordinated control of SI in male and female components, contrasted with frequent observation of ‘leakiness’ or inclusion of both SI and SC individuals within populations of the same species. Such a scenario could also explain previous controversies over whether loss of SI is primarily due to modifiers that are linked or unlinked to the S locus or mutations in the S genes themselves (reviewed in Mable et al., 2017); perhaps it is all a matter of timescales.

For example, Kerbs et al. (2021) were surprised to find genome-wide signatures of extensive outcrossing within a small island population of a plant in the family Asteraceae (Tolpis succulenta; sporophytic SI) where they expected to see selection for self-fertilization due to low pollinator availability, particularly given findings from a previous study that plants on this island showed high levels of apparently heritable SC in a greenhouse setting. They explained this as indirect evidence for high inbreeding depression in selfed progeny. However, given that the loss of SI has not yet resulted in a shift in floral phenotypes compared with outcrossing populations, it would be difficult to distinguish SI from SC individuals in the field, if the population was actually mixed. The observations in this species are similar to what we have observed in populations of Arabidopsis lyrata (Brassicaceae; sporophytic SI) in the Great Lakes region of eastern North America: although the species is SI throughout most of its range, a shift to selfing has occurred in some populations, with high levels of outcrossing maintained in populations that include both SI and SC individuals (Mable et al., 2017). In contrast to previous comparisons between A. lyrata and A. thaliana suggesting that loss of SI was due to mutations at the S locus, a bulked segregant analysis suggested a single recessive modifier unlinked to the S locus could explain the loss of SC in one of these populations, although sample sizes were not large enough to identify a specific gene. Moreover, like Slatter et al. (2021), conclusions were based on progeny from a single cross, so it is also possible that the cause of the shift was not the same in all populations or among individuals within populations. This emphasizes that broad sampling of individuals from natural environments and genetics based on multiple crosses from such samples could be required to fully understand just how much variation might exist in the regulation of mating systems, even among populations of a single species.

The increasing number of genomic-scale approaches applied within rather than between species differing in mating system for a range of self-incompatibility types (e.g. sporophytic, gametophytic, heteromorphic), provides the exciting opportunity to readdress the long-standing question of whether selfing lineages should still be viewed as evolutionary dead ends or more stable strategies to allow rapid environmental responses. What is needed next is to explicitly test potential mechanisms for how ecological pressures could influence mating system transitions; for example, the role that environmental stress might play in the ability of selfing species to respond to environmental change (van Ginkel and Flipphi, 2020). There is also accumulating evidence from both plants and animals that we might need to reconsider our models of the critical importance of the role of mating system in conferring adaptation to variable environments. For example, increasing evidence from both theory (Clo et al., 2020) and conservation genomics research (reviewed in Mable, 2019) suggests that inbred populations can maintain higher levels of standing genetic variation than previously suspected. Particularly if shifts to selfing have the potential to be transient and reversible in their early stages, flexibility in mating systems could offer the greatest potential for exploiting rapidly changing environments.