Genetic basis and timing of a major mating system shift inCapsella

Abstract

Summary A crucial step in the transition from outcrossing to self‐fertilization is the loss of genetic self‐incompatibility (SI). In the Brassicaceae, SI involves the interaction of female and male specificity components, encoded by the genes SRK and SCR at the self‐incompatibility locus (S‐locus). Theory predicts that S‐linked mutations, and especially dominant mutations in SCR, are likely to contribute to loss of SI. However, few studies have investigated the contribution of dominant mutations to loss of SI in wild plant species. Here, we investigate the genetic basis of loss of SI in the self‐fertilizing crucifer species Capsella orientalis, by combining genetic mapping, long‐read sequencing of complete S‐haplotypes, gene expression analyses and controlled crosses. We show that loss of SI in C. orientalis occurred < 2.6 Mya and maps as a dominant trait to the S‐locus. We identify a fixed frameshift deletion in the male specificity gene SCR and confirm loss of male SI specificity. We further identify an S‐linked small RNA that is predicted to cause dominance of self‐compatibility. Our results agree with predictions on the contribution of dominant S‐linked mutations to loss of SI, and thus provide new insights into the molecular basis of mating system transitions.

Population Genomics of the “Arcanum” Species Group in Wild Tomatoes: Evidence for Separate Origins of Two Self-Compatible Lineages

“…Overall, both the observed patterns of diversity and raw divergence, as well as our demographic modeling that used other aspects of the genome-wide data, agree with a larger drop in N e concomitant with divergence of CHMI compared to divergence of NEOR. If these inferences prove correct, the morphological changes characterizing NEOR (i.e., tiny flowers, no stigma exsertion; Figure 1B and Supplementary Figure 1) have been quite rapid, here inferred to be within 78,000 generations (Figure 4), which would be similar to or even faster than the rapid evolution of a morphological selfing syndrome in Capsella, dated at between 70,000 and 2.6 million generations (or years) ago using a mutation rate similar to our study (Sicard and Lenhard, 2011;Bachmann et al, 2019).…”

“…The latter aspect has been thoroughly investigated in the genus Capsella, where the recently diverged self-compatible Capsella rubella was shown to be derived from the obligately outcrossing Capsella grandiflora (Foxe et al, 2009;Guo et al, 2009;Brandvain et al, 2013;Bachmann et al, 2019). With such transitions to self-fertilization concomitant with rapid speciation, demographic bottlenecks resulting in low levels of nucleotide diversity are plausible and have been documented in Capsella (Foxe et al, 2009;Guo et al, 2009) as well as in Mimulus (Brandvain et al, 2014).…”

Long-term balancing selection drives evolution of immunity genes in Capsella

“…The genus Capsella offers a unique opportunity to test the longevity of balancing selection, because selfing has evolved independently in C. orientalis , which diverged from C. grandiflora and C. rubella more than one million years ago and whose modern range no longer overlaps with the two other species, preventing ongoing introgression ( Hurka et al, 2012 ; Douglas et al, 2015 ). We expected the evolution of selfing to have generated a similar bottleneck as in C. rubella ( Douglas et al, 2015 ; Bachmann et al, 2018 ), and we therefore resequenced 16 C. orientalis genomes, to test whether there is evidence of balancing selection at similar types of loci.…”

“…In this study we sought to assess how strongly selection acts to maintain genetic diversity in the context of repeated transitions to self fertilisation in the flowering plant genus Capsella . Like many plant lineages, the ancestral state of Capsella is outcrossing (found in the extant diploid species C. grandiflora ), but selfing has evolved independently in two diploid species, C. rubella and C. orientalis ( Figure 1A )( Foxe et al, 2009 ; Guo et al, 2009 ; Bachmann et al, 2018 ). The genomes of both species exhibit the drastic loss of genetic diversity typical for many selfers ( Figure 1B–C ) ( Guo et al, 2009 ; Foxe et al, 2009 ; St Onge et al, 2011 ; Slotte et al, 2013 ; Brandvain et al, 2013 ; Slotte et al, 2012 ).…”

Retracing the molecular basis and evolutionary history of the loss of benzaldehyde emission in the genus Capsella

“…10–14 million years ago (Ma), provides a promising model to study the genetics of the selfing syndrome, as the transition from outbreeding to selfing has occurred twice independently within this genus (Hurka et al ., ). Approximately 1–2 Ma the self‐compatible Capsella orientalis diverged from a self‐incompatible C. grandiflora ‐like ancestor (Hurka et al ., ; Bachmann et al ., ), and c . 100 000–200 000 yr ago the self‐compatible C. rubella was derived from C. grandiflora (Foxe et al ., ; Guo et al ., ; Koenig et al ., ).…”