Evolution of the MAT locus and its Ho endonuclease in yeast species

Abstract

The genetics of the mating-type (MAT) locus have been studied extensively in Saccharomyces cerevisiae, but relatively little is known about how this complex system evolved. We compared the organization of MAT and mating-type-like (MTL) loci in nine species spanning the hemiascomycete phylogenetic tree. We inferred that the system evolved in a two-step process in which silent HMR/HML cassettes appeared, followed by acquisition of the Ho endonuclease from a mobile genetic element. Ho-mediated switching between an active MAT locus and silent cassettes exists only in the Saccharomyces sensu stricto group and their closest relatives: Candida glabrata, Kluyveromyces delphensis, and Saccharomyces castellii. We identified C. glabrata MTL1 as the ortholog of the MAT locus of K. delphensis and show that switching between C. glabrata MTL1a and MTL1alpha genotypes occurs in vivo. The more distantly related species Kluyveromyces lactis has silent cassettes but switches mating type without the aid of Ho endonuclease. Very distantly related species such as Candida albicans and Yarrowia lipolytica do not have silent cassettes. In Pichia angusta, a homothallic species, we found MATalpha2, MATalpha1, and MATa1 genes adjacent to each other on the same chromosome. Although some continuity in the chromosomal location of the MAT locus can be traced throughout hemiascomycete evolution and even to Neurospora, the gene content of the locus has changed with the loss of an HMG domain gene (MATa2) from the MATa idiomorph shortly after HO was recruited.

Fig. 1.

(a) Organization of the α and a idiomorphs of the C. glabrata MTL1 and K. delphensis MAT loci. The organization is identical in the two species. The a1 gene has three exons. Broken open arrows denote truncated copies of the 3′ ends of the α2 and α1 genes present in the a idiomorphs. W, X, Z1, and Z2 indicate regions shared with silent cassettes. (b) PCR amplification of idiomorph-specific products from C. glabrata strains CBS 138 and RND13. Shown are idiomorph-specific primer pair combinations as diagrammed in Upper (lanes CBS 138 a-d and RND13 a-d); lanes 2-fold overloaded compared with the others (lanes CBS 138 c and d and RND13 a and b); and a size standard (lane M).

Fig. 2.

Gene organization around the HO locus in yeast species. Homologous gene groups are aligned vertically. Triple vertical lines indicate duplicated gene pairs. The phylogenetic tree on the left shows the evolutionary relationships among sequences, with the genome duplication event (asterisk) resulting in two descendant lineages in some species. Green, lineages and genes orthologous to S. cerevisiae chromosome XIV; dark blue, orthologs of chromosome IV. The extent of sequence data available for each species is shown by black horizontal lines. Data for Saccharomyces castellii and Saccharomyces kluyveri are from ref. (GenBank accession nos. AACE01000158, AACE01000109, AACF01000039, and AACF01000107). K. marx., Kluyveromyces marxianus; S. kluy., S. kluyveri; Z. roux., Z. rouxii; S. cast., S. castellii; S. cer. XIV, S. cerevisiae chromosome XIV; S. cer. IV, S. cerevisiae chromosome IV; K. delph., K. delphensis; C. glab, C. glabrata.

Fig. 3.

Comparative organization of the MAT locus in nine yeast species and Neurospora. For each species, the main horizontal line shows the organization of the α idiomorph, and the a idiomorph is represented by the offset box below it. Vertical lines connect orthologous genes. The position of a Ho endonuclease site in MATα1 is marked when present. Coloring indicates conserved groups of genes: red, α idiomorph; green, a idiomorph; blue, homologs of S. cerevisiae chromosome III (YCR033W-YCR038W); orange, homologs of chromosome X (YJL201W-YJL210W); purple, homologs of chromosome XIV (YNL243W-YNL245C), pink, DIC1 (YLR348C); yellow, APN2 (YBL019W); white, homologs of chromosome III (YCR042C-YCR045C); gray, homologs of chromosome XII (YLR186W-YLR182W); and gray gradient, CAN1 (YEL063C). Gene names in parentheses are species-specific. Previously published data are from refs. , , , , , , , and . GenBank accession numbers are listed under species names.

Fig. 4.

Summary of events in MAT and HO locus evolution. The phylogenetic tree on the left (based on refs. , , and 51) is schematic and not drawn to scale. In the table on the right, blanks indicate missing data. Z. rouxii information is from Fig. 2 and low-coverage shotgun sequencing.