Evolution of the Bipolar Mating System of the Mushroom Coprinellus disseminatus From Its Tetrapolar Ancestors Involves Loss of Mating-Type-Specific Pheromone Receptor Function

Abstract

Mating incompatibility in mushroom fungi is controlled by the mating-type loci. In tetrapolar species, two unlinked mating-type loci exist (A and B), whereas in bipolar species there is only one locus. The A and B mating-type loci encode homeodomain transcription factors and pheromones and pheromone receptors, respectively. Most mushroom species have a tetrapolar mating system, but numerous transitions to bipolar mating systems have occurred. Here we determined the genes controlling mating type in the bipolar mushroom Coprinellus disseminatus. Through positional cloning and degenerate PCR, we sequenced both the transcription factor and pheromone receptor mating-type gene homologs from C. disseminatus. Only the transcription factor genes segregate with mating type, discounting the hypothesis of genetic linkage between the A and B mating-type loci as the causal origin of bipolar mating behavior. The mating-type locus of C. disseminatus is similar to the A mating-type locus of the model species Coprinopsis cinerea and encodes two tightly linked pairs of homeodomain transcription factor genes. When transformed into C. cinerea, the C. disseminatus A and B homologs elicited sexual reactions like native matingtype genes. Although mating type in C. disseminatus is controlled by only the transcription factor genes, cellular functions appear to be conserved for both groups of genes. M ATING in fungi is controlled by the loci that determine the mating type of an individual, and only individuals with differing mating types can mate. Basidiomycete fungi have evolved a unique mating system, termed tetrapolar or bifactorial incompatibility, in which mating type is determined by two unlinked loci; compatibility at both loci is required for mating to occur. The origin of the tetrapolar mating system in the basidiomycetes is likely to be ancient since it is observed in at least two of the three major lineages, the Ustilaginomycetes, or smut fungi, and the Hymenomycetes, primarily the mushroom fungi (Burnett 1975). Also unique to the basidiomycetes is the presence of multiple alleles at the mating-type loci that allows most individuals within a population to be mating compatible with one another. Only the mushroom-forming homobasidiomycetes possess large allelic series at both loci, typically termed the A and B mating-type loci (Whitehouse 1949;Raper 1966).The multiallelic tetrapolar mating system is considered to be a novel innovation that could have only evolved once (Raper 1966;Raper and Flexer 1971). For this reason, the ancestor of the homobasidiomycetes is accepted as having a tetrapolar mating system. Although most (65%) of the homobasidiomycetes possess a tetrapolar mating system, many species (25%) instead have a bipolar system controlled by a single locus with multiple alleles (Raper 1966). The distribution of bipolar species is scattered throughout the homobasidiomycete phylogeny, and bipolar species appear to have multiple independent origins from tetrapolar mating systems (Hibbett and Donoghue 2001). The popul...

Basidiomycete Mating Type Genes and Pheromone Signaling

“…For the tremellomycete Cryptococcus neoformans, the development of a sex chromosome, linking not only the mating type genes but also genes involved in downstream signaling, was proposed (53,57). However, bipolar mating type systems of agaricomycetes like Coprinellus disseminatus or Pholiota nameko appear to have followed a different evolutionary path, in which the B locus has lost its self/nonself discrimination ability and thus specificity, although not its other regulatory functions in development, perhaps as a consequence of a mutation or recombination event (41). This evolutionary route is substantiated by identification of self-recognizing B loci due to mutagenesis (80) as well as introduction of recombinant genes (28), leading to functionally bipolar mutant strains for S. commune and C. cinerea.…”

“…Only one pair of homeodomain genes was also detected in the tetrapolar oyster mushroom, Pleurotus djamor (40), and in the A mating type locus of bipolar Pholiota nameko (122). Another bipolar species, Coprinellus disseminatus, contains multiallelic A␣ and A␤ loci, each locus with an HD1 and an HD2 protein-encoding gene (41).…”

“…In P. placenta, the genes mip1 and ␤-fg, known from previous work to flank the A mating type loci in other basidiomycetes (39,41), were used to identify one pair of HD1-and HD2-encoding genes in both of the two putative A loci located on different scaffolds in the sequenced dikaryotic genome (62). The HD protein sequences show 40 to 50% similarity to other basidiomycete mating type proteins.…”

“…chrysosporium and P. placenta are assumed to represent bipolar mating type systems (62,70), and therefore the role of the B mating type genes in these fungi is still unclear. Perhaps they share the reason for bipolar behavior with Coprinellus disseminatus, where the B factor receptors Ste3.1 and Ste3.2 are not linked to mating type determination but still to function in clamp formation and fruiting (41). On the other hand, in the bipolar basidiomycete Cr.…”

Evolution of Mating Systems in Basidiomycetes and the Genetic Architecture Underlying Mating-Type Determination in the YeastLeucosporidium scottii

“…However, much of what is known about bipolarity in these species emphasizes that these bipolar states have most likely arisen from a tetrapolar configuration. This can be attained either by (i) loss of function of the P/R locus as an incompatibility factor (as, e.g., in Coprinus disseminatus, Pholiota microspore, and Phanerochaete chrysosporium) (Raper 1966;James et al 2006James et al , 2011Yi et al 2009) or (ii) coalescence of unlinked P/R and HD loci into a contiguous inheritable unit, with both MAT genes remaining functional in mating-type determination. This last scenario was shown to be at the basis of extant bipolar species belonging to two of the three major Basidiomycota lineages, namely Cryptococcus neoformans (subphylum Agaricomycotina) Findley et al 2012) and Ustilago hordei (subphylum Ustilaginomycotina) (Bakkeren et al 2006).…”