Evolutionary Origins of the HO Gene and Other Components of the MAT Switching System

The evolutionary origin of HO is enigmatic because the gene has a very limited phylogenetic distribution. Apart from S. cerevisiae and its close relatives such as S. bayanus (the Saccharomyces sensu stricto group of species), the HO gene is present only in Candida glabrata, Saccharomyces castellii, and Zygosaccharomyces rouxii (Butler et al. 2004). In these species, mating-type switching probably occurs by HO-catalyzed switching between an active MAT

locus and silent HM cassettes, similar to the S. cerevisiae paradigm, although a direct demonstration of such switching has yet to be shown. A second group of yeasts, exemplified by Kluyveromyces lactis, have HM cassettes but do not have an ortholog of HO. K. lactis can switch mating types at a very low frequency (Herman and Roman 1966; Zonneveld and Steensma 2003), similar to HO-negative ho strains of S. cerevisiae. Other species with cassettes but lacking HO include K. waltii and A. gossypii. Switching in these species probably proceeds by homologous recombination between the cassettes and the MAT locus, without a specific endonuclease to initiate the recombination process. A third group of more distantly related species, such as Yarrowia lipolytica, do not have silent cassettes or an HO gene and do not switch mating type; they are heterothallic. The HO gene seems to have been gained by yeasts shortly before the whole genome duplication (WGD) that occurred in the shared ancestor of several yeast species (Wolfe and Shields 1997; Dietrich et al. 2004; Kellis et al. 2004), because all known species that are descended from the WGD event have HO (Butler et al. 2004). The origin of HO can be inferred to pre-date the WGD because HO is present in Z. rouxii, which is a representative of the lineage of yeasts that is sister to the WGD lineage (Kurtzman and Robnett 2003). Gene order at the HO locus in different yeast species is well conserved once the WGD event is taken into account (Butler et al. 2004), and does not provide much in the way of clues to HO's origins. The gene simply seems to materialize in the interval between the genes RI02 and SSB. This interval seems to have had an unusually dynamic history but the significance of this observation is unclear. In several species the interval contains a very rapidly evolving gene (YNL208W) with prion-like amino acid composition, and in Z. rouxii a gene for an endoribonuclease of the T2 family (distantly related to S. cerevisiae RNYl; Macintosh et al. 2001) is present.

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