The evolution of selfing from outcrossing ancestors in Brassicaceae: what have we learned from variation at the S‐locus?

Abstract

Evolutionary transitions between mating systems have occurred repetitively and independently in flowering plants. One of the most spectacular advances of the recent empirical literature in the field was the discovery of the underlying genetic machinery, which provides the opportunity to retrospectively document the scenario of the outcrossing to selfing transitions in a phylogenetic perspective. In this review, we explore the literature describing patterns of polymorphism and molecular evolution of the locus controlling self-incompatibility (S-locus) in selfing species of the Brassicaceae family in order to document the transition from outcrossing to selfing, a retrospective approach that we describe as the 'mating system genes approach'. The data point to strikingly contrasted scenarios of transition from outcrossing to selfing. We also perform original analyses of the fully sequenced genomes of four species showing self-compatibility, to compare the orthologous S-locus region with that of functional S-locus haplotypes. Phylogenetic analyses suggest that all species we investigated evolved independently towards loss of self-incompatibility, and in most cases almost intact sequences of either of the two S-locus genes suggest that these transitions occurred relatively recently. The S-locus region in Aethionema arabicum, representing the most basal lineage of Brassicaceae, showed unusual patterns so that our analysis could not determine whether self-incompatibility was lost secondarily, or evolved in the core Brassicaceae after the split with this basal lineage. Although the approach we detail can only be used when mating system genes have been identified in a clade, we suggest that its integration with phylogenetic and population genetic approaches should help determine the main routes of this predominant mating system shift in plants.

African genomes illuminate the early history and transition to selfing in Arabidopsis thaliana

“…This finding differs from previous assertions that these events likely happened separately in geographically distinct populations (15,16). Moreover, it allows for the possibility that the transition to selfing was aided by a shared precursor mutation, a shared climate, and the bottleneck that occurred during the migration away from the ancestral population (22). Our proposed model parallels observations in partially selfing populations of A. lyrata (50).…”

“…In A. thaliana, three S-haplogroups are found, and each contains mutations that obliterate function of the S-locus genes (15)(16)(17). Loss-of-function occurred independently in each S-haplogroup (18)(19)(20)(21), but because these three S-haplogroups were never found together in the same geographic region, self-compatibility is inferred to have evolved separately in multiple locations (16,21,22). However, the hypothesis of geographically distinct origins is difficult to reconcile with the major genomic and phenotypic changes that render A. thaliana incompatible with its out-crossing congeners (9-13).…”

Flowers and mycorrhizal roots – closer than we think?

“…The extracellular domain of SRK contains a highly conserved cysteine-rich stretch consisting of an EGF-like and a PAN_APPLE motive that are required for receptor dimerization [49], and comprises Nglycosylation sites that are essential for localization to the plasma membrane [50]. The genes encoding SCR protein and SRK are tightly linked in the S-locus, and occur in many allelic variants in natural plant populations [51], thus ensuring efficient cross-pollination. Interestingly, maize roots express a closely related homolog of SRK, referred to as ZmPK1 [52].…”

Adding Complexity to Complexity: Gene Family Evolution in Polyploids

“…From previous studies we anticipated that the single most recessive allele, SRK01, would be present at high frequency and would show a higher number of haplotypes than other specificities (Billiard et al, 2007;Castric and Vekemans, 2007;Llaurens et al, 2008;Castric et al, 2010;Goubet et al, 2012;Vekemans et al, 2014). In our 454 data, SRK01 was present in all populations surveyed and we identified 15 unique variants that were present in more than one individual; however, read numbers tended to be very low (often with <10 reads per individual) and fell well below the thresholds set for considering "real" presence of a given haplotype used for other loci for most individuals.…”

“…The other four paralogs tested were present in all accessions, except for one diploid A. lyrata that lacked ARK3 (Aly8). Since this latter locus is tightly linked to SRK in some specificities and shows high polymorphism (Kusaba et al, 2001;Charlesworth et al, 2003b;Guo et al, 2011;Vekemans et al, 2014), this could be due to divergence from the reference sequence. AL2G2623090 included sequences similar to both Aly10.1 (ARK1 in A. thaliana) and Aly10.2 (ARK2 in A. thaliana), which were detected in all individuals.…”