Self-incompatibility has been considered by geneticists a model system for reproductive biology and balancing selection, but our understanding of the genetic basis and evolution of this molecular lock-and-key system has remained limited by the extreme level of sequence divergence among haplotypes, resulting in a lack of appropriate genomic sequences. In this study, we report and analyze the full sequence of eleven distinct haplotypes of the self-incompatibility locus (S-locus) in two closely related Arabidopsis species, obtained from individual BAC libraries. We use this extensive dataset to highlight sharply contrasted patterns of molecular evolution of each of the two genes controlling self-incompatibility themselves, as well as of the genomic region surrounding them. We find strong collinearity of the flanking regions among haplotypes on each side of the S-locus together with high levels of sequence similarity. In contrast, the S-locus region itself shows spectacularly deep gene genealogies, high variability in size and gene organization, as well as complete absence of sequence similarity in intergenic sequences and striking accumulation of transposable elements. Of particular interest, we demonstrate that dominant and recessive S-haplotypes experience sharply contrasted patterns of molecular evolution. Indeed, dominant haplotypes exhibit larger size and a much higher density of transposable elements, being matched only by that in the centromere. Overall, these properties highlight that the S-locus presents many striking similarities with other regions involved in the determination of mating-types, such as sex chromosomes in animals or in plants, or the mating-type locus in fungi and green algae.
Self-incompatibility is a common genetic system preventing selfing through recognition and rejection of self-pollen in hermaphroditic flowering plants. In the Brassicaceae family, this system is controlled by a single genomic region, called the S-locus, where many distinct specificities segregate in natural populations. In this study, we obtained genomic sequences comprising the S-locus in two closely related Brassicaceae species, Arabidopsis lyrata and A. halleri, and analyzed their diversity and patterns of molecular evolution. We report compelling evidence that the S-locus presents many similar properties with other genomic regions involved in the determination of mating-types in mammals, insects, plants, or fungi. In particular, in spite of their diversity, these genomic regions all show absence of similarity in intergenic sequences, large depth of genealogies, highly divergent organization, and accumulation of transposable elements. Moreover, some of these features were found to vary according to dominance of the S-locus specificities, suggesting that dominance/recessivity interactions are key drivers of the evolution of this genomic region.