Breakdown of self-incompatibility due to genetic interaction between a specific S-allele and an unlinked modifier

Abstract

Breakdown of self-incompatibility has frequently been attributed to loss-of-function mutations of alleles at the locus responsible for recognition of self-pollen (i.e. the S-locus). However, other potential causes have rarely been tested. Here, we show that self-compatibility of S1S1-homozygotes in selfing populations of the otherwise self-incompatible Arabidopsis lyrata is not due to S-locus mutation. Between-breeding-system cross-progeny are self-compatible if they combine S1 from the self-compatible cross-partner with recessive S1 from the self-incompatible cross-partner, but self-incompatible with dominant S-alleles. Because S1S1 homozygotes in outcrossing populations are self-incompatible, mutation of S1 cannot explain self-compatibility in S1S1 cross-progeny. This supports the hypothesis that an S1-specific modifier unlinked to the S-locus causes self-compatibility by functionally disrupting S1. Self-compatibility in S19S19 homozygotes may also be caused by an S19-specific modifier, but we cannot rule out a loss-of-function mutation of S19. Taken together, our findings indicate that breakdown of self-incompatibility is possible without disruptive mutations at the S-locus.

Dominance in self-compatibility between subgenomes of allopolyploid Arabidopsis kamchatica shown by transgenic restoration of self-incompatibility

“…The co-dominance of S -haplogroups B and D was observed in pistils 18 , and a previous report pointed out that S -haplogroup D belongs to the most dominant “phylogenetic class“ 51 based on phylogenetic analysis of SRK sequences 32 . However, our crossing experiment showed the male dominance of B over D. Furthermore, the evolutionary reversal experiment of SCR-B showed that the mutation in SCR was responsible for the evolution of self-compatibility, not that in other known or unknown genes such as an S -unlinked modifier gene recently reported from a self-compatible population of A. lyrata 56 . In this study, we focused on the transgenic experiments of SCR but did not manipulate sRNA.…”

“…Such transgenic restoration by introducing a single gene shows that the mutation in the gene is responsible for self-compatibility and that all other genes for self-incompatibility are functional. The self-incompatibility system of Brassicaceae involves many genes other than SCR and SRK , and therefore self-compatibility may be attributed to so-called modifier genes such as M- locus protein kinase gene that are not linked to S -locus 35 , or to an unknown locus in the self-compatible populations of A. lyrata 50 , 56 . Because the sRNAs regulating male dominance are located at the S -locus 28 , 30 , the self-compatibility mutation must be located at the S -locus for dominance to be linked.…”

Resynthesizing Brassica napus with race specific resistance genes and race non-specific QTLs to multiple races of Plasmodiophora brassicae

“…Resynthesized rapeseed lines exhibit self-incompatibility in the early generations, since they inherit functional S-alleles from both parent species, resulting in self-incompatibility in the offspring generations. The breakdown of self-incompatibility can occur due to not only loss-of-function mutations of alleles at the S-locus but also genetic interactions between specific S-alleles and unlinked modifiers 47 . In this study, although both parents of A and C genome used to produce the resynthesized lines were self-incompatible, self-compatible plants were selected during subsequent generations' selection processes and the self-compatibility trait improved in the advanced generations of the resynthesized lines.…”

Uncovering genes involved in pollinator‐driven mating system shifts and selfing syndrome evolution in Brassica rapa

“…This effort was essential to understand some of the evolutionary processes involved in the frequent transition of outcrossing to selfing mating systems in angiosperms (Barrett, 2002; Shimizu & Tsuchimatsu, 2015). It was also of value to breeders engaged in producing homozygous lines where SI is an undesired trait (Li et al ., 2023). However, the transition to selfing is also associated with changes in a combination of phenotypic traits, known as the selfing syndrome, and only a handful of studies have unraveled their genetic basis (Tsuchimatsu & Fujii, 2022).…”