Orchestration of sexual reproduction and virulence by the fungal mating-type locus

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The mating-type locus (MAT) orchestrates sexual reproduction in fungi. Sexual reproduction is related not only to fitness of an organism, but also correlated with virulence in certain pathogens. In the dandruff-associated fungus Malassesia globosa, although the sexual cycle remains to be discovered, whole genome analysis has led to the hypothesis that mating may occur on host skin. Furthermore, the MAT locus of M. globosa and U. hordei provides evidence that transitions between tetrapolar and bipolar systems have independently occurred. These results, together with studies recapitulating the ancestral tetrapolar mating system in Cryptococcus and the structure of MAT in related smut fungi, have furthered understanding on transitions between different mating systems and the evolution of MAT in the Basidiomycota.

Introduction

Sexual reproduction is ubiquitous across kingdoms and important both to the origins and fitness of species. Fungi, in particular, serve as excellent models to study sexual reproduction and explore how sex is orchestrated. Sex is genetically determined in fungi, governed by a sex-specific region in the genome known as the mating-type locus (MAT). The molecular structure of MAT was first characterized in Saccharomyces cerevisiae, in which homeodomain or α-domain transcription factors are encoded by the a or α-idiomorph and are critical to establish cell-type identity [1]. With the wealth of fungal genome sequences now available, the structure, function, and evolution of MAT have been revealed in three major fungal lineages (Ascomycetes, Basidiomycetes, and Zygomycetes) [2, 3, 4]. Generally, MAT encodes transcription factors that have conserved homeodomain, α-domain, or HMG domain DNA-binding regions; these transcription factors then control the expression of cell-type-specific genes and genes that are required for mating. These advances provide insight into how the sexual cycle is orchestrated in fungi and how this sex-determining region evolves [4, 5]. In many fungal pathogens of both plants and animals, the sexual cycle has been associated with virulence. In this review, we discuss how sex is orchestrated and how it influences virulence with a focus on species in the Basidiomycota phylum that infect plants and animals.

Section snippets

Mating systems in Basidiomycetes

Fungi exhibit either of two mating patterns: self-fertile (homothallic) or self-sterile (heterothallic). In heterothallic fungi, mating occurs when cells of different mating types encounter each other. In homothallic fungi, sexual reproduction can occur in monoculture without the need for a mating partner but most homothallic fungi can also undergo outcrossing. Importantly, several species, including S. cerevisiae, encompass both heterothallic and homothallic members in their population. Mating

Structure and evolution of the MAT locus

As mentioned above, the molecular structure of MAT has been defined in many fungal species from three major lineages [2, 3, 4, 10]. Despite that conserved sex-determining transcription factors are ubiquitously present, MAT loci vary considerably in size and gene content. For example, MAT in the model yeast S. cerevisiae is less than 1 kb, and encodes only one or two genes. However, in another hemiascomycete yeast, Candida albicans, several additional genes (PAP, PIK, and OBP) have been

Sex and virulence

It is clear that sex has been favored by evolution since most organisms employ sexual reproduction as the mode to generate offspring. However, the roles that sex plays in the evolution of pathogenic species are debated. One can imagine that the virulence of a pathogen is a polygenic trait, and random chromosomal assortment and recombination during meiosis is likely to disrupt favorable gene combinations necessary for virulence. Nonetheless, one can also advance the counter argument that

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

We thank Jim Kronstad and Jana Klose for providing the images of U. maydis, Pat Pukkila for the image of Coprinopsis cinerea, and Banu Metin for assistance with the generation of Figure 1. This research is supported by NIH/NIAID grants AI39115 and AI50113.

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