Academic journal article Genetics

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

Academic journal article Genetics

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

Article excerpt

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 mating-type 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.

MATING 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 population genetic consequence of the bipolar vs. the tetrapolar mating system is a difference in the amount of interbreeding permitted between the haploid progeny from a single parent (siblings). Specifically, the potential for inbreeding is higher in the bipolar system because 50% of full-sib progeny are mating compatible, whereas only 25% are in the tetrapolar case. This trend in homobasidiomycetes toward the evolution of increased selfing is similar to the situation in Ascomycete fungi (e.g., YUN rf al. 1999) and plants (e.g., TAKEBAYASHI and MORRELL 2001) in which selfing is typically derived from a system of greater outcrossing.

Using the model tetrapolar species Schizophyllum commune and Coprinopsis cinema (Coprinus cinereus), the A mating-type loci of both species and the B mating-type locus of S. communeviere discovered to be composed of two tightly linked subloci, the a- and â-subunits (DAY 1960; RAPER et al. …

Search by... Author
Show... All Results Primary Sources Peer-reviewed

Oops!

An unknown error has occurred. Please click the button below to reload the page. If the problem persists, please try again in a little while.