Ancestral self-compatibility facilitates the establishment of allopolyploids in Brassicaceae

Abstract

Self-incompatibility systems based on self-recognition evolved in hermaphroditic plants to maintain genetic variation of offspring and mitigate inbreeding depression. Despite these benefits in diploid plants, for polyploids who often face a scarcity of mating partners, self-incompatibility can thwart reproduction. In contrast, self-compatibility provides an immediate advantage: a route to reproductive viability. Thus, diploid selfing lineages may facilitate the formation of new allopolyploid species. Here, we describe the mechanism of establishment of at least four allopolyploid species in Brassicaceae (Arabidopsis suecica, Arabidopsis kamchatica, Capsella bursa-pastoris, and Brassica napus), in a manner dependent on the prior loss of the self-incompatibility mechanism in one of the ancestors. In each case, the degraded S-locus from one parental lineage was dominant over the functional S-locus of the outcrossing parental lineage. Such dominant loss-of-function mutations promote an immediate transition to selfing in allopolyploids and may facilitate their establishment.

Dominance between self-incompatibility alleles determines the mating system of Capsella allopolyploids

“…In the specific case of allopolyploidy in Brassicaceae, our results formally establish that the mating system immediately upon hybridization depends on the relative dominance of the non-functional allele inherited from the selfer C. orientalis as compared to that of the functional S-allele(s) inherited from the outcrosser C. grandiflora, in line with the model proposed by Novikova et al (2022). This observation raises at least three intriguing questions.…”

“…Some factors affecting the fixation probability of SC mutations have been studied by Tsuchimatsu & Shimizu (2013), but to the best of our knowledge, the effect of dominance on the fixation probability of SC mutations in a sporophytic SI system remains to be investigated formally. A third interesting question is why most known examples of recent allotetraploids in Brassicaceae involve hybridization between a selfer and an outcrosser (Novikova et al 2022). A more general survey of recent allopolyploids would be needed to determine the generality of this pattern, but one tempting hypothesis is that, given an appropriate combination of S-haplotypes, this kind of crosses might instantaneously generate SC allotetraploid individuals avoiding minority cytotype exclusion (Novikova et al 2022).…”

“…The reason why these allopolyploid species originating from SIxSC are SC rather than SI is intriguing. An interesting possibility could be that the dominance interactions between Shaplotypes could have caused the instantaneous breakdown of SI in these species if the (non-functional) S-haplotype contributed by the SC species had retained the ability to suppress the expression of the (functional) SCR alleles contributed by the SI species in hybrid offspring (reviewed in Novikova et al 2022). Consistent with this hypothesis, the allotetraploid A. suecica, A. kamchatica, and C. bursa-pastoris all share the same nonfunctional S-allele as their respective SC parental species (Novikova et al 2017;Bachmann et al 2019Bachmann et al , 2021Kolesnikova et al 2022).…”

Inbreeding depression in polyploid species: a meta-analysis

“…Husband et al . [21] showed that autopolyploid species generally self-fertilize less than diploid ones, while allopolyploids showed the opposite pattern [21,63]. Since our dataset is mainly composed of autopolyploid species (table 1), our finding seems to be counterintuitive.…”

Inbreeding depression in polyploid species: a meta-analysis

“…Husband et al . [21] showed that autopolyploid species generally self-fertilize less than diploid ones, while allopolyploids showed the opposite pattern [21,37]. Since our dataset is mainly composed of autopolyploid species (Table 1), our finding seems to be counterintuitive.…”