Academic journal article Genetics

The Evolution and Diversification of S-Locus Haplotypes in the Brassicaceae Family

Academic journal article Genetics

The Evolution and Diversification of S-Locus Haplotypes in the Brassicaceae Family

Article excerpt

ABSTRACT

Self-incompatibility (SI) in the Brassicaceae plant family is controlled by the SRK and SCR genes situated at the S locus. A large number of S haplotypes have been identified, mainly in cultivated species of the Brassica and Raphanus genera, but recently also in wild Arabidopsis species. Here, we used DNA sequences from the SRK and SCR genes of the wild Brassica species Brassica cretica, together with publicly available sequence data from other Brassicaceae species, to investigate the evolutionary relationships among S haplotypes in the Brassicaceae family. The results reveal that wild and cultivated Brassica species have similar levels of SRK diversity, indicating that domestication has had but a minor effect on S-locus diversity in Brassica. Our results also show that a common set of S haplotypes was present in the ancestor of the Brassica and Arabidopsis genera, that only a small number of haplotypes survived in the Brassica lineage after its separation from Arabidopsis, and that diversification within the two Brassica dominance classes occurred after the split between the two lineages. We also found indications that recombination may have occurred between the kinase domain of SRK and the SCR gene in Brassica.

TO avoid self-fertilization, different kinds of selfincompatibility (SI) mechanisms have evolved in many plant families (Richards 1997). In most cases, SI is controlled by a single locus, the S locus, which, even though it often contains several genes, is inherited as a single Mendelian locus (Silva and Goring 2001); for this reason, S alleles are often referred to as S haplotypes (Boyes and Nasrallah 1993). In the Brassicaceae, which has the sporophytic type of SI where the pollen SI phenotype is determined by the S-locus genotype of the diploid parent, two S-locus genes, SRK and SCR, encode the maternal (pistil) and paternal (pollen) specificities, respectively (Stein et al. 1991; Schopfer et al. 1999; Suzuki et al. 1999). The SRK receptor consists of three domains with different functions: an extracellular S domain (encoded by exon 1 in SRK), which is the center for recognition of SCR; a transmembrane domain (exon 2) that passes through the plasma membrane; and an intracellular kinase domain (exons 4-7), which initiates the signaling cascade in the stigma cells (see Takayama and Isogai 2005). The SCR gene product is a small soluble protein molecule present at the pollen surface where it interacts with the S domain of its cognate SRK protein (Takayama et al. 2001). 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 tensof kilobases beyondthe 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. For example, the Brassica S haplotypes can be divided into two distinct dominance classes with class I haplotypes being dominant over class II haplotypes in pollen but codominant in the stigma (Nasrallah et al. 1991). By contrast, dominance relationships among S haplotypes are more complex in Arabidopsis, where four distinct dominance classes have been identified to date (Prigoda et al. …

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