An Overview of the Function and Maintenance of Sexual Reproduction in Dikaryotic Fungi

Abstract

Sexual reproduction likely evolved as protection from environmental stresses, specifically, to repair DNA damage, often via homologous recombination. In higher eukaryotes, meiosis and the production of gametes with allelic combinations different from parental type provides the side effect of increased genetic variation. In fungi it appears that while the maintenance of meiosis is paramount for success, outcrossing is not a driving force. In the subkingdom Dikarya, fungal members are characterized by existence of a dikaryon for extended stages within the life cycle. Such fungi possess functional or, in some cases, relictual, loci that govern sexual reproduction between members of their own species. All mating systems identified so far in the Dikarya employ a pheromone/receptor system for haploid organisms to recognize a compatible mating partner, although the paradigm in the Ascomycota, e.g., Saccharomyces cerevisiae, is that genes for the pheromone precursor and receptor are not found in the mating-type locus but rather are regulated by its products. Similarly, the mating systems in the Ascomycota are bipolar, with two non-allelic idiomorphs expressed in cells of opposite mating type. In contrast, for the Basidiomycota, both bipolar and tetrapolar mating systems have been well characterized; further, at least one locus directly encodes the pheromone precursor and the receptor for the pheromone of a different mating type, while a separate locus encodes proteins that may regulate the first locus and/or additional genes required for downstream events. Heterozygosity at both of two unlinked loci is required for cells to productively mate in tetrapolar systems, whereas in bipolar systems the two loci are tightly linked. Finally, a trade-off exists in wild fungal populations between sexual reproduction and the associated costs, with adverse conditions leading to mating. For fungal mammal pathogens, the products of sexual reproduction can be targets for the host immune system. The opposite appears true for phytopathogenic fungi, where mating and pathogenicity are inextricably linked. Here, we explore, compare, and contrast different strategies used among the Dikarya, both saprophytic and pathogenic fungi, and highlight differences between pathogens of mammals and pathogens of plants, providing context for selective pressures acting on this interesting group of fungi.

Keywords: Dikarya; bipolar mating; dimorphic fungi; homeodomain transcription factor; mating type; pheromone/receptor; tetrapolar mating.

FIGURE 1

Expression of haploid-specific genes in Saccharomyces cerevisiae leading to mating between haploid cells. (A) In the haploid a cells, a1, the homeodomain protein, is expressed constitutively from the mating type locus. While the genes for the pheromone and pheromone receptor are not located within the mating-type loci, in the haploid a cell, the a-factor and Ste2, the receptor for α-factor, are both expressed constitutively as well. In the haploid α cells, α1 and α2 are expressed from the mating type locus. α2 forms a homodimer to block transcription of a-specific genes. (B) The interaction of pheromone with its receptor on the cell of the opposite mating type results in the formation of a “shmoo” structure, a protrusion of the cytoplasm, toward each other. (C) Fusion of the cells and subsequently the nuclei. In the diploid a/α cell, α2 and a1 form a heterodimer to block expression of haploid-specific genes.

FIGURE 2

Representative mating type loci from the Ascomycota. (A) The organization of the mating-type loci of Saccharomyces cerevisiae serves as the model for the group, containing homeodomain proteins that regulate the expression of other mating type-specific genes. (B) Although not as well characterized as Sa. cerevisiae, Neurospora crassa exists as two haploid mating types, each of which contain genetic information at the mating type loci to govern expression of mating type specific genes. (C) Like Sa. cerevisiae, Schizosaccharomyces pombe contains homeodomain proteins at its mating type loci consisting of both expressed and donor regions. (D) Although most clinical isolates are diploid, Candida albicans does have two different mating type loci found in two haploid strains that can be cultivated in the laboratory setting. Boxes of the same color represent corresponding components in the different mating types.

FIGURE 3

Sample tetrapolar mating systems in basidiomycete fungi. While the number of homeodomain proteins may vary across this group, the composition of genetic material at the mating type loci is conserved. Boxes of the same color represent orthologous components in the different mating types and across species.

FIGURE 4

Sample bipolar mating systems in basidiomycete fungi. While the two mating type loci of these organisms have become physically linked by chromosomal arrangement, the composition of the mating type loci remains similar to that found in tetrapolar systems. Boxes of the same color represent orthologous components in the different mating types and across species.

FIGURE 5

Mating in Ustilago maydis. (A) An initial environmental cue, which may be from the plant or involve nutrient limitation, results in the initial phosphorylation of Prf1. (B) Prf1 binds to a response element in the a mating type loci, resulting in increased expression of the pheromone and pheromone receptor in both types of haploid cells. (C) Interaction of the pheromone with the receptor on the cell of opposite mating type results in additional phosphorylation of Prf1. Prf1 phosphorylated by both pathways then binds to response elements within the b mating type locus, leading to increased expression of the homeodomain proteins. Additionally, interaction of pheromone and receptor results in the growth of conjugation tubes from each cell toward each other. (D) Creation of a homeodomain heterodimer comprised of bE and bW from different allelles results in the formation of an infection dikaryon. (E) This dikaryon is able to establish infection within the host, although fusion of the nuclei does not occur during infection until teliospore formation, just prior to release from the infected plant galls.