Mating-Type Switching in Budding Yeasts, from Flip/Flop Inversion to Cassette Mechanisms

Mating-type switching is a natural but unusual genetic control process that regulates cell identity in ascomycete yeasts. It involves physically replacing one small piece of genomic DNA by another, resulting in replacement of the master regulatory genes in the mating pathway and hence a switch of cell type and mating behavior. In this review, we concentrate on recent progress that has been made on understanding the origins and evolution of mating-type switching systems in budding yeasts (subphylum Saccharomycotina). Mating-type switching is a natural but unusual genetic control process that regulates cell identity in ascomycete yeasts. It involves physically replacing one small piece of genomic DNA by another, resulting in replacement of the master regulatory genes in the mating pathway and hence a switch of cell type and mating behavior. In this review, we concentrate on recent progress that has been made on understanding the origins and evolution of mating-type switching systems in budding yeasts (subphylum Saccharomycotina). Because of the unusual nature and the complexity of the mechanism in Saccharomyces cerevisiae, mating-type switching was assumed until recently to have originated only once or twice during yeast evolution. However, comparative genomics analysis now shows that switching mechanisms arose many times independently-at least 11 times in budding yeasts and once in fission yeasts-a dramatic example of convergent evolution. Most of these lineages switch mating types by a flip/flop mechanism that inverts a section of a chromosome and is simpler than the well-characterized 3-locus cassette mechanism (MAT/HML/HMR) used by S. cerevisiae. Mating-type switching (secondary homothallism) is one of the two possible mechanisms by which a yeast species can become self-fertile. The other mechanism (primary homothallism) has also emerged independently in multiple evolutionary lineages of budding yeasts, indicating that homothallism has been favored strongly by natural selection. Recent work shows that HO endonuclease, which makes the double-strand DNA break that initiates switching at the S. cerevisiae MAT locus, evolved from an unusual mobile genetic element that originally targeted a glycolytic gene, FBA1.

Automated summary

This review focuses on recent progress in understanding the origins and evolution of mating-type switching systems in budding yeasts, highlighting the multiple independent occurrences and convergent evolution of these mechanisms, as well as the diversity of self-fertilization mechanisms.