Sex in fungi

Abstract

Sexual reproduction enables genetic exchange in eukaryotic organisms as diverse as fungi, animals, plants, and ciliates. Given its ubiquity, sex is thought to have evolved once, possibly concomitant with or shortly after the origin of eukaryotic organisms themselves. The basic principles of sex are conserved, including ploidy changes, the formation of gametes via meiosis, mate recognition, and cell-cell fusion leading to the production of a zygote. Although the basic tenants are shared, sex determination and sexual reproduction occur in myriad forms throughout nature, including outbreeding systems with more than two mating types or sexes, unisexual selfing, and even examples in which organisms switch mating type. As robust and diverse genetic models, fungi provide insights into the molecular nature of sex, sexual specification, and evolution to advance our understanding of sexual reproduction and its impact throughout the eukaryotic tree of life.

Figure 1

Modes of sexual reproduction in fungi. (a) Modes of heterothallism. Bipolar: one mating-type (MAT) locus regulates sexual development, and two isolates need to possess opposite MAT alleles to mate. Tetrapolar: two MAT loci regulate sexual development and are often multiallelic, and two isolates need to possess opposite alleles at both loci for sexual reproduction. (b) Modes of homothallism: mating-type switching in which an α daughter cell mates with an a mother cell; pseudohomothallism in which two nuclei of opposite mating types are packaged into one spore; two MATs in one nucleus in which the two opposite MAT loci are either fused in one locus or reside at different loci; and finally, there is only one MAT idiomorph present and cells reproduce via same sex mating.

Figure 2

Mating-type switching in Saccharomyces cerevisiae, Kluyveromyces lactis, and Schizosaccharomyces pombe. (a) In S. cerevisiae, the Ho endonuclease creates a double-strand break (DSB) in MAT that is repaired via homologous recombination with one of the silent cassettes as a donor, leading to gene conversion. (b) K. lactis utilizes the native α3 transposase or an unknown nuclease to induce a DSB in MAT directed by the binding of Mts1. Homologous recombination repairs the break via gene conversion. (c) In S. pombe, an unknown nuclease promotes a lesion at the imprint, which is repaired through homologous recombination. (d) Evolution of mating-type switching in S. cerevisiae, S. pombe, and K. lactis. Initially, the silent cassettes were independently acquired in S. cerevisiae and K. lactis, resulting in inefficient mating-type switching via mitotic recombination. The Saccharomycotina gained the HO gene, which increased switching efficiency. However, in the diverged lineage of K. lactis, the HO gene degenerated and the α3 transposase or an unknown nuclease was conscripted to promote mating-type switching.

Figure 3

Sexual development cycles and MAT loci in Neurospora crassa, Podospora anserina, and Sordaria macrospora. (a) Sexual development begins with the germination of ascospores, followed by the growth of vegetative mycelium with the formation of an ascogonium, which further develops into a perithecium. Inside the perithecium, two nuclei fuse to generate a diploid nucleus, which undergoes meiosis followed by a postmeiotic mitosis, resulting in the formation of eight haploid, linearly arranged ascospores in N. crassa and S. macrospora and four binucleate ascospores in P. anserina. Mating of heterothallic N. crassa occurs only between strains of MATA and MATa. Microconidia (male) of one MAT (A in figure; can also be a) are fertilized with ascogonia (female) of the other MAT (a in figure; can also be A). Sexual development of pseudohomothallic P. anserina initiates from the germination of binucleate ascospores (MAT+/−) to form self-fertile, heterokaryotic mycelia carrying nuclei of both mating types. The mycelia of each mating type develop into spermatia or ascogonia, and fertilization occurs between a spermatium and an ascogonium of opposite mating types. S. macrospora is homothallic, and its mycelia grow from the germination of uninucleate ascospores. Figures were modified from Figure 1 with permission from the author Patrick Shiu (132). (b) MAT in Aspergillus fumigatus, N. crassa, P. anserina, and S. macrospora. Abbreviations: HMG, high-mobility group domain; PPF, the domain containing conserved proline, proline, and phenylalanine residues.

Figure 4

Modes of sexual reproduction. Sex typically involves two genetically divergent partners of opposite sex or mating type. (a) Obligate sexual reproduction, e.g., human sexual cycle. Specialized cells (2n) in adult gonads undergo meiosis to form haploid (n) gametes (sperm or egg). Haploid gametes fuse to form the diploid zygote (2n), which undergoes repeated mitosis, differentiation, and growth to become multicellular organisms (juvenile, 2n). The mature organism is diploid; gametes are the only haploid cells. (b) Facultative sexual reproduction, e.g., yeast life cycle. Saccharomyces cerevisiae can grow as haploid yeasts by asexual budding. Mating occurs between strains of MATa and MATα to form diploid cells, which can undergo meiosis to generate haploid spores. The mature organism can be diploid or haploid; gametes are haploid cells. Many fungi maintain haploid life cycles, and only become diploid following fertilization.