Fungal mating-type loci

Fungi form one of the most ubiquitous and successful kingdoms of life on Earth. There are more than 100,000 known species of fungi, divided into four phyla — ascomycetes, basidiomycetes, zygomycetes and chytrids — and these have populated a vast array of biological niches, including those that are pathogens of animals (including humans and insects), plants and even other microorganisms. The morphological diversity among species is staggering, from the budding yeasts and filamentous fungi to the mushrooms and wood rotting organisms. Fungi also serve as powerful tools for our understanding of cell biology, and several have emerged as model systems, including most notably the budding yeast Saccharomyces cerevisiae. We shall review here our current understanding of the role of a specialized region of the fungal genome known as the matingtype locus, which plays a central role in the sexual cycle. The mating-type, or MAT, locus is a unique region of the fungal genome that governs the establishment of cell-type identity and orchestrates the sexual cycle. It is this region that differs in DNA sequence between cells of opposite mating-type. The MAT locus encodes global transcription factors, which establish cell-type identity by controlling the expression of developmental cascades, and this commonly involves homeodomain or other classes of transcriptional regulatory elements. Some fungi exist in only two mating-types (bipolar), whereas others occur in hundreds or thousands of matingtypes (tetrapolar). Some fungi are also endowed with the capacity to switch mating-type (homothallic), whereas others are not (heterothallic). The mechanisms that give rise to only two versus many mating-types, and those that enable mating-type switching are now understood in considerable molecular detail. The mating-type locus of fungi has evolved into two different organizational paradigms: the bipolar and tetrapolar systems. In organisms with a bipolar matingtype system, cells are of two opposite mating-types — commonly a and α or plus and minus — and cell identity is dictated by a single MAT locus that has two alternative alleles. For sexual reproduction to occur, mating partner cells must have different MAT alleles. Bipolar systems promote inbreeding, and can lead to the rapid homozygosis of recessive mutations in organisms that are predominantly diploid, such as S. cerevisiae. Fungi with a tetrapolar system, by contrast, arrange their matingtype information in two distinct unlinked regions of the genome, commonly known as the a and b loci. Both of these regions must differ for mating to occur. In many tetrapolar fungi, the mating-type loci are multiallelic, giving rise to thousands of mating-types in the most extreme examples. Tetrapolar systems promote outbreeding, as any given meiotic segregant can only interbreed with 25% of its siblings from a cross: a1 b1 can mate with a2 b2, but not with a1 b1, a1 b2 or a2 b1. The evolution of these paradigms in part reflects the evolution of different phyla of fungi, in that ascomycetous fungi have bipolar mating-type systems, whereas basidiomycetous fungi may be either bipolar or tetrapolar.