Multiple Reinventions of Mating-type Switching during Budding Yeast Evolution

Abstract

Summary 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 α), 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 , 4 , 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.

The yeast mating-type switching endonuclease HO is a domesticated member of an unorthodox homing genetic element family

“…Yeast spores are survival capsules, and mating-type switching enables the microcolony formed from a newly-germinated spore to sporulate again after just a few cell divisions if necessary, preventing its extinction (Herskowitz, 1988). Across the phylogenetic tree of budding yeasts, mating-type switching has arisen independently at least 11 times, indicating strong natural selection in favor of switching (Krassowski et al, 2019).…”

“…An outgroup species, Kluyveromyces lactis , also has a three-locus system but has no HO gene, and employs alternative mechanisms to create a double-strand break at the MAT locus to initiate switching (Barsoum et al, 2010; Rajaei et al, 2014). More distantly related budding yeasts switch mating types using ‘two-locus’ flip/flop inversion systems, and again do not have an HO gene (Hanson and Wolfe, 2017; Krassowski et al, 2019).…”

Genome editing in the yeast Nakaseomyces delphensis and description of its complete sexual cycle

“…Depending on their phylogenetic position, other yeasts exhibit switching (Krassowski et al, 2019), relying on Ho, or other mechanisms, such as what happens in Kluyveromyces lactis , which contains three mating‐type‐like (MTL) loci but no HO gene, relying instead on the machinery of transposable elements for switching (Rajaei, Chiruvella, Lin, & Åström, 2014). In the Nakaseomyces , the mating‐type switching genome elements that are known to function in S. cerevisiae are also present.…”

Identification of a novel gene controlling homothallism in the yeast Kazachstania naganishii isolated in Japan

“…In Saccharomyces cerevisiae , the precise mechanism of mating‐type determination and mating‐type interconversion has been clarified at the molecular level (for reviews, see Haber, 2012; Herskowitz, Rine, & Strathern, 1992; Lee & Haber, 2015; Sprague & Thorner, 1992). Wolfe's group has been intensively investigating evolution of genes concerning life cycles in the yeast family Saccharomycetaceae (Butler et al, 2004; Gordon et al, 2011; Hanson & Wolfe, 2017; Krassowski et al, 2019; Ortiz‐Merino et al, 2017; Wolfe et al, 2015; Wolfe & Butler, 2017). The whole genome sequence of K .…”