Contrasted Patterns of Molecular Evolution in Dominant and Recessive Self-Incompatibility Haplotypes in Arabidopsis

Abstract

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.

Gene duplication and genetic exchange drive the evolution of S-RNase-based self-incompatibility in Petunia

“…4c) 14,15 . These Solanaceae SLFs are distributed within 17.9 Mb in tomato and 14.6 Mb in potato, suggesting that the S-loci of the Solanaceae are very large, about two to three orders of magnitude larger than the Brassicaceae S-locus (28-110 kb) 16 .…”

Adding Complexity to Complexity: Gene Family Evolution in Polyploids

“…Consistent with theory (Billiard et al, 2007), recessive alleles in diploids have been demonstrated to occur at higher frequency, to show shallower branch lengths in phylogenetic analyses, and more extensive polymorphism within specificities than dominant alleles (Llaurens et al, 2008(Llaurens et al, , 2009Castric et al, 2010;Vekemans et al, 2011;Goubet et al, 2012). In our study, Class B alleles (recessive to A2 and A3 classes) showed lower intraclass polymorphism (13% average pairwise sequence divergence, compared to 25% for Class A2 and 15% for Class A3) but more haplotypes per allele than the two dominant classes (2.56 ± 1.33 compared to 1.59 ± 0.75 in Class A2 and 1.56 ± 0.89 in Class A3, Table 2) and there was high divergence between classes (26-29%; Table 3).…”

“…SRK alleles have been grouped into four different dominance classes (A1, A2, A3, B; Prigoda et al, 2005). Polymorphisms within specificities/alleles (which we will refer to as "haplotypes") are more apparent for recessive than dominant alleles because the former are expected to occur at higher frequency and show more sharing between populations (Bechsgaard et al, 2006;Castric and Vekemans, 2007;Castric et al, 2008Castric et al, , 2010Stoeckel et al, 2008;Llaurens et al, 2009;Goubet et al, 2012). There is a single most recessive allele (S1, Class A1; Prigoda et al, 2005) that is found globally and in multiple species in the genus Arabidopsis (Mable et al, 2003;Dart et al, 2004;Prigoda et al, 2005;Mable and Adam, 2007;Castric et al, 2010;Foxe et al, 2010).…”

“…Final contigs were then sorted into putative "types": known SRK alleles, putatively new SRK-like variants, or known paralogs. Contigs assigned to SRK alleles whose dominance had been established previously (Prigoda et al, 2005;Goubet et al, 2012) were further sorted into the following classes: (1) A1, consisting of a single most recessive allelic specificity that has been found globally in Arabidopsis species (SRK01); (2) A2, dominant to all other classes; (3) A3, recessive only to class A2; and (4) B, recessive to all except A1 and showing high similarity to unlinked loci (Aly13-2 and Aly13-7). Contigs were also inspected for clustering of more than one named SRK allele from the database.…”

“…The strict 7% threshold would have excluded some alleles that amplified in multiple individuals but were only present at low read numbers within individuals. A striking example was SRK01: it was fragmented across multiple contigs but when reassembled, it tended to be found at very low read numbers within individuals but was found across a wide range of individuals and showed population-and species-specific variants, as expected for a recessive allele (Billiard et al, 2007;Goubet et al, 2012). Many individuals showed <20 reads but the individuals that showed high read numbers (>100) tended not to show amplification of any other alleles, suggesting competition in the PCR when other alleles were present.…”