Effects of Recombination on Hitchhiking Diversity in the Brassica Self-incompatibility Locus Complex

Abstract

In self-incompatibility, a number of S haplotypes are maintained by frequency-dependent selection, which results in trans-specific S haplotypes. The region of several kilobases ($40-60 kb) from SP6 to SP2, including self-incompatibility-related genes and some adjacent genes in Brassica rapa, has high nucleotide diversity due to the hitchhiking effect, and therefore we call this region the ''S-locus complex.'' Recombination in the S-locus complex is considered to be suppressed. We sequenced regions of .50 kb of the S-locus complex of three S haplotypes in B. rapa and found higher nucleotide diversity in intergenic regions than in coding regions. Two highly similar regions of .10 kb were found between BrS-8 and BrS-46. Phylogenetic analysis using trans-specific S haplotypes (called interspecific pairs) of B. rapa and B. oleracea suggested that recombination reduced the nucleotide diversity in these two regions and that the genes not involved in self-incompatibility in the S-locus complex and the kinase domain, but not the S domain, of SRK have also experienced recombination. Recombination may reduce hitchhiking diversity in the S-locus complex, whereas the region from the S domain to SP11 would disfavor recombination.

The Evolution and Diversification ofS-Locus Haplotypes in the Brassicaceae Family

“…The presence of haplotypes from all three Brassica species in both class I and class II provides further evidence that previous observations of trans-specific polymorphisms at the S locus in cultivated Brassica species (Kusaba et al 1997;Shiba et al 2002;Takuno et al 2007) extend to the wild B. cretica. Moreover, SRK lineages from the cultivated B. oleracea and B. rapa are widely dispersed among lineages from the wild B. cretica.…”

“…In the SCR tree, and to a lesser extent in the SRK class II tree, three strongly supported clades were found, each of which included one of the three known B. oleracea/B. rapa class II haplotype pairs (BolSCR2 and BraSCR44, BolSCR5 and BraSCR40, and BolSCR15 and BraSCR60; Sato et al 2003;Takuno et al 2007). Each of the three clades also included either a single or two or three closely related B. cretica haplotypes.…”

“…Because of the strong frequency-dependent selection acting on the SI system, the S locus typically maintains a large number of haplotypes (Lawrence 2000), and levels of diversity at both synonymous and nonsynonymous sites are high in the S domain of SRK and in SCR (e.g., Awadalla and Charlesworth 1999;Charlesworth et al 2003;Takuno et al 2007). Furthermore, in both Brassica and Arabidopsis, synonymous diversity is elevated in a region encompassing several tens of kilobases beyond the actual targets of selection due to the low level of recombination at the S locus (Kamau and Charlesworth 2005;Castric and Vekemans 2007;Takuno et al 2007).There is now firm evidence that the structural elements of SI are homologous among cultivated Brassicaceae species (including Brassica oleracea, Brassica rapa, Brassica nigra, and Raphanus sativus) and the wild Arabidopsis lyrata, indicating that SI has a single origin within the Brassicaceae family (Kusaba et al 2001;Schierup et al 2001). Nevertheless, there are characteristic differences in the SI systems between the Brassica and Arabidopsis genera.…”

“…Because of the strong frequency-dependent selection acting on the SI system, the S locus typically maintains a large number of haplotypes (Lawrence 2000), and levels of diversity at both synonymous and nonsynonymous sites are high in the S domain of SRK and in SCR (e.g., Awadalla and Charlesworth 1999;Charlesworth et al 2003;Takuno et al 2007). Furthermore, in both Brassica and Arabidopsis, synonymous diversity is elevated in a region encompassing several tens of kilobases beyond the actual targets of selection due to the low level of recombination at the S locus (Kamau and Charlesworth 2005;Castric and Vekemans 2007;Takuno et al 2007).…”

“…FJ670452-FJ670503. 1 2006), there are indications that some form of recombination or gene conversion has occurred within Brassica (Awadalla and Charlesworth 1999;Takuno et al 2007).…”