An Evolutionary Perspective on Yeast Mating-Type Switching

Abstract

Cell differentiation in yeast species is controlled by a reversible, programmed DNA-rearrangement process called mating-type switching. Switching is achieved by two functionally similar but structurally distinct processes in the budding yeast Saccharomyces cerevisiae and the fission yeast Schizosaccharomyces pombe In both species, haploid cells possess one active and two silent copies of the mating-type locus (a three-cassette structure), the active locus is cleaved, and synthesis-dependent strand annealing is used to replace it with a copy of a silent locus encoding the opposite mating-type information. Each species has its own set of components responsible for regulating these processes. In this review, we summarize knowledge about the function and evolution of mating-type switching components in these species, including mechanisms of heterochromatin formation, MAT locus cleavage, donor bias, lineage tracking, and environmental regulation of switching. We compare switching in these well-studied species to others such as Kluyveromyces lactis and the methylotrophic yeasts Ogataea polymorpha and Komagataella phaffii We focus on some key questions: Which cells switch mating type? What molecular apparatus is required for switching? Where did it come from? And what is the evolutionary purpose of switching?

Keywords: evolution; homothallism; mating-type switching; sporulation; yeast genetics.

Figure 1

Schematic life cycle of S. cerevisiae.

Figure 2

Gene organization in the MAT, HML, and HMR loci on S. cerevisiae chromosome III. Shading indicates genes whose transcription is repressed.

Figure 3

Logic of the cell type-specification circuits in Saccharomycetaceae species. Solid colors represent cell types (green, a; pink, α; brown, a/α), and outline colors represent gene sets. The genotype (1) of a cell’s MAT locus specifies the regulatory proteins present in that cell (2; checkboxes), which act at promoters (3) to generate appropriate transcription of the three gene sets (4; asg’s, αsg’s, and hsg’s) and determine the cell type (5). The yellow boxes describe the rewiring event that occurred when MATa2 was lost, coinciding with the WGD. The diagram summarizes information from the post-WGD species S. cerevisiae and the non-WGD species K. lactis, L. kluyveri, and C. albicans (Tsong et al. 2003, 2006; Booth et al. 2010; Baker et al. 2012; Sorrells et al. 2015).

Figure 4

Phylogenetic tree of phylum Ascomycota showing major clades, MAT-locus organization, and known or inferred mating-type switching mechanisms. Based on Riley et al. (2016), with placement of A. rubescens as in Shen et al. (2016). Mating-type switching does not occur in species with only one MAT-like locus or in Aspergillus nidulans, which is a primary homothallic species.

Figure 5

Organization of repeat sequences flanking the MAT loci in four species (Klar 2007; Hanson et al. 2014). In K. phaffii, the region that becomes inverted during mating-type switching is 138-kb long, and was recently discovered to contain a centromere at its approximate center (Coughlan et al. 2016). CEN, centromere; TEL, telomere.

Figure 6

Seven ways to organize a MAT locus in family Saccharomycetaceae. The X and Z repeats, which occur in three copies in the genome (at MAT, HML, and HMR), overlap with parts of different MAT genes in different species. Each cartoon illustrates how the MAT genes are arranged, relative to the X and Z regions, in a group of species. The horizontal lines in each cartoon represent sequence that is shared between the MATα and MATa alleles, while the bubbles represent the divergence between the Yα and Ya regions. Blue arrows represent the neighboring chromosomal genes, which also vary among species (Gordon et al. 2011).