Fungal Sex: The Basidiomycota

Abstract

SUMMARY Fungi of the Basidiomycota, representing major pathogen lineages and mushroom-forming species, exhibit diverse means to achieve sexual reproduction, with particularly varied mechanisms to determine compatibilities of haploid mating partners. For species that require mating between distinct genotypes, discrimination is usually based on both the reciprocal exchange of diffusible mating pheromones, rather than sexes, and the interactions of homeodomain protein signals after cell fusion. Both compatibility factors must be heterozygous in the product of mating, and genetic linkage relationships of the mating pheromone/receptor and homeodomain genes largely determine the complex patterns of mating-type variation. Independent segregation of the two compatibility factors can create four haploid mating genotypes from meiosis, referred to as tetrapolarity. This condition is thought to be ancestral to the basidiomycetes. Alternatively, co-segregation by linkage of the two mating factors, or in some cases the absence of the pheromone-based discrimination, yields only two mating types from meiosis, referred to as bipolarity. Several species are now known to have large and highly rearranged chromosomal regions linked to mating-type genes. At the population level, polymorphism of the mating-type genes is an exceptional aspect of some basidiomycete fungi, where selection under outcrossing for rare, intercompatible allelic variants is thought to be responsible for mating types that may number several thousand. Advances in genome sequencing and assembly are yielding new insights by comparative approaches among and within basidiomycete species, with the promise to resolve the evolutionary origins and dynamics of mating compatibility genetics in this major eukaryotic lineage.

Evolutionary strata on young mating-type chromosomes despite the lack of sexual antagonism

“…In basidiomycetes, mating type is typically controlled by two loci: (i) the pheromone receptor (PR) locus, which carries one gene encoding a mating-type-specific PR and one to several genes encoding pheromones, and (ii) the homeodomain gene (HD) locus, encoding two homeodomaintype transcription factors controlling postmating growth. Recombination suppression ensures full linkage of the mating-type genes within each of these two loci, which is required for correct mating-type determination (11), and typically does not extend beyond the mating-type genes (12,13). Recombination suppression…”

Protein‐facilitated transport of hydrophobic molecules across the yeast plasma membrane

“…Yet, knowledge about export of pheromones from the Basidiomycetes class is scarce and somewhat contradictory. Though all pheromones of this class are stated to be diffusible [122], radiolabeling of tremerogen A-10, the mating factor of the heterobasidiomycetous yeast Tremella mesenterica, showed that it initially appeared in a membranebound form and subsequently converted into a more soluble form prior to secretion, suggesting a more complex form of transport [123]. Furthermore, basidiomycete pheromones all carry CaaX motifs for Cterminal farnesylation, which in turn aids membrane localization, guiding the pheromone to a transmembrane transporter protein [124,125].…”

Convergent evolution of linked mating-type loci in basidiomycete fungi

“…Among the Tremellomycetes, pathogenic Cryptococci are so far the only species for which fused MAT loci have been described [17,23]. In a previous study, we analyzed the genome sequence of Cutaneotrichosporon oleaginosum strain IBC0246 (formerly Trichosporon oleaginosus), which belongs to the Trichosporonales, a sister order to the Tremellales within the Tremellomycetes class.…”

“…One MAT locus usually contains tightly linked pheromone and pheromone receptor genes (P/R locus) involved in premating recognition, and the other encodes homeodomain transcription factor genes encoding homeodomain (HD) proteins of class 1 and class 2 (HD locus) determining viability after syngamy. Importantly, alleles at both loci must differ between mating partners for completion of the sexual cycle [17].…”

“…In the majority of basidiomycetes, each MAT allele at the HD locus carries both the HD1 and the HD2 transcription factor genes, whereas in C. neoformans, the MAT locus contains only the HD1 gene SXI1, and MATa contains only the HD2 gene SXI2a. Except for a gene conversion hotspot, the C. neoformans MAT locus displays suppressed meiotic recombination [23,34,35].Among the Tremellomycetes, pathogenic Cryptococci are so far the only species for which fused MAT loci have been described [17,23]. In a previous study, we analyzed the genome sequence of Cutaneotrichosporon oleaginosum strain IBC0246 (formerly Trichosporon oleaginosus), which belongs to the Trichosporonales, a sister order to the Tremellales within the Tremellomycetes class.…”