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Multiple Reinventions of Mating-type Switching during Budding Yeast Evolution.

ABSTRACT: Cell type in budding yeasts is determined by the genotype at the mating-type (MAT) locus, but yeast species differ widely in their mating compatibility systems and life cycles. Among sexual yeasts, heterothallic species are those in which haploid strains fall into two distinct and stable mating types (MATa and MAT?), whereas homothallic species are those that can switch mating types or that appear not to have distinct mating types [1, 2]. The evolutionary history of these mating compatibility systems is uncertain, particularly regarding the number and direction of transitions between homothallism and heterothallism, and regarding whether the process of mating-type switching had a single origin [3-5]. Here, we inferred the mating compatibility systems of 332 budding yeast species from their genome sequences. By reference to a robust phylogenomic tree [6], we detected evolutionary transitions between heterothallism and homothallism, and among different forms of homothallism. We find that mating-type switching has arisen independently at least 11 times during yeast evolution and that transitions from heterothallism to homothallism greatly outnumber transitions in the opposite direction (31 versus 3). Although the 3-locus MAT-HML-HMR mechanism of mating-type switching as seen in Saccharomyces cerevisiae had a single evolutionary origin in budding yeasts, simpler "flip/flop" mechanisms of switching evolved separately in at least 10 other groups of yeasts. These results point to the adaptive value of homothallism and mating-type switching to unicellular fungi.

SUBMITTER: Krassowski T

PROVIDER: S-EPMC6692504 | biostudies-literature | 2019 Aug

REPOSITORIES: biostudies-literature

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Multiple Reinventions of Mating-type Switching during Budding Yeast Evolution.

Krassowski Tadeusz T Kominek Jacek J Shen Xing-Xing XX Opulente Dana A DA Zhou Xiaofan X Rokas Antonis A Hittinger Chris Todd CT Wolfe Kenneth H KH

Current biology : CB 20190725 15

Cell type in budding yeasts is determined by the genotype at the mating-type (MAT) locus, but yeast species differ widely in their mating compatibility systems and life cycles. Among sexual yeasts, heterothallic species are those in which haploid strains fall into two distinct and stable mating types (MATa and MATα), whereas homothallic species are those that can switch mating types or that appear not to have distinct mating types [1, 2]. The evolutionary history of these mating compatibility sy ...[more]

PMID: 31353182

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Project description:The Saccharomyces cerevisiae Fkh1 protein has roles in cell-cycle regulated transcription as well as a transcription-independent role in recombination donor preference during mating-type switching. The conserved FHA domain of Fkh1 regulates donor preference by juxtaposing two distant regions on chromosome III to promote their recombination. A model posits that this Fkh1-mediated long-range chromosomal juxtaposition requires an interaction between the FHA domain and a partner protein(s), but to date no relevant partner has been described. In this study, we used structural modeling, 2-hybrid assays, and mutational analyses to show that the predicted phosphothreonine-binding FHA domain of Fkh1 interacted with multiple partner proteins. The Fkh1 FHA domain was important for its role in cell-cycle regulation, but no single interaction partner could account for this role. In contrast, Fkh1's interaction with the Mph1 DNA repair helicase regulated donor preference during mating-type switching. Using 2-hybrid assays, co-immunoprecipitation, and fluorescence anisotropy, we mapped a discrete peptide within the regulatory Mph1 C-terminus required for this interaction and identified two threonines that were particularly important. In vitro binding experiments indicated that at least one of these threonines had to be phosphorylated for efficient Fkh1 binding. Substitution of these two threonines with alanines (mph1-2TA) specifically abolished the Fkh1-Mph1 interaction in vivo and altered donor preference during mating-type switching to the same degree as mph1?. Notably, the mph1-2TA allele maintained other functions of Mph1 in genome stability. Deletion of a second Fkh1-interacting protein encoded by YMR144W also resulted in a change in Fkh1-FHA-dependent donor preference. We have named this gene FDO1 for Forkhead one interacting protein involved in donor preference. We conclude that a phosphothreonine-mediated protein-protein interface between Fkh1-FHA and Mph1 contributes to a specific long-range chromosomal interaction required for mating-type switching, but that Fkh1-FHA must also interact with several other proteins to achieve full functionality in this process.

Dataset Information

Multiple Reinventions of Mating-type Switching during Budding Yeast Evolution.

Publications

Multiple Reinventions of Mating-type Switching during Budding Yeast Evolution.

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