Analysis of the multispecific B alpha mating‐type locus of Schizophyllum commune provided evidence that pheromones and pheromone receptors govern recognition of self versus non‐self and sexual development in this homobasidiomycetous fungus. Four subclones of an 8.2 kb genomic fragment carrying B alpha 1 specificity induced B‐regulated sexual morphogenesis when introduced into a strain with one of the eight compatible B alpha specificities that are known to exist in nature. One of these clones, which activated all other B alpha specificities, contains a gene termed bar1. The predicted protein product of bar1, as well as that of bar2, a homologous gene isolated from a B alpha 2 strain, has significant homology to known fungal pheromone receptor proteins in the rhodopsin‐like superfamily of G protein‐linked receptors. The other three active B alpha 1 clones were subcloned further to identify the minimal active element in each clone. Every active subclone contains a putative pheromone gene ending in a signal for possible isoprenylation. A message of approximately 600 bp was observed for one of these genes, bap1(1). This paper presents the first evidence for a system of multiple pheromones and pheromone receptors as a basis for multispecific mating types in a fungus.
The mushroom-producing fungus Schizophyllum commune has thousands of mating types defined, in part, by numerous lipopeptide pheromones and their G protein-linked receptors. Compatible combinations of pheromones and receptors encoded by different mating types regulate a pathway of sexual development leading to mushroom formation and meiosis. A complex set of pheromone-receptor interactions maximizes the likelihood of outbreeding; for example, a single pheromone can activate more than one receptor and a single receptor can be activated by more than one pheromone. The current study demonstrates that the sex pheromones and receptors of Schizophyllum, when expressed in Saccharomyces cerevisiae, can substitute for endogenous pheromone and receptor and induce the yeast pheromone response pathway through the yeast G protein. Secretion of active Schizophyllum pheromone requires some, but not all, of the biosynthetic machinery used by the yeast lipopeptide pheromone a-factor. The specificity of interaction among pheromone-receptor pairs in Schizophyllum was reproduced in yeast, thus providing a powerful system for exploring molecular aspects of pheromone-receptor interactions for a class of seven-transmembrane-domain receptors common to a wide range of organisms.
Mating competence in a majority of the higher Basidiomycetes, typified by Schizophyllum commune, is determined by a bifactorial incompatibility system.1' 2 The determination of mating competence, however, is only one result of a more inclusive role played by the incompatibility factors in the determination of internuclear relationships in four distinctive types of heterokaryons that may be formed whenever two haploid, homokaryotic strains interact. Only one of the four heterokaryons, the dikaryon, normally leads to sexual fertility and the completion of the life cycle.' -6The genetic basis of incompatibility in these forms resides in two independently assorting and segregating factors, A and B, each of which is constituted of two distinct, linked loci having multiple alleles.7-9 In S. commune, 9 and 26 alleles have been identified at Aa and AA, respectively, and series of 9 A a and 50 A: alleles have been projected for the total world-wide population. Each unique combination of A a and AS alleles determines a specific A factor phenotype, which is reflected in its compatibility with all 350-450 other A factors.10 11 The B factor is similarly constituted of two (or possibly three") component loci, each having a less extensive series of multiple alleles to yield ca. 65 factor-phenotypes.11The heterokaryons formed in interactions between homokaryons, each carrying a specific A factor and a specific B factor, are related to the incompatibility system as follows 3-6 (1) AH B$, e.g., Al Bi X A2 B2, yields the dikaryon, a specialized heterokaryon having a nuclear ratio of 1:1 maintained by synchronous nuclear-division, and leads to the conmpletion of the sexual cycle.(2) Other combinations, A = B., e.g., Al BL X Al B2, A B=, e.g., Al Bi X
) S U M M A R YFive collections from nature, originally identified as representing the three species Agaricus campestris, A. edulis and A . bitorquis, have been shown to be interfertile and are therefore designated A . bitorquis (QuClet) Saccardo. All stocks can be fruited, and analysis of the life-cycle has revealed heterothallism with sexuality controlled by a single incompatibility locus with multiple alleles : monosporous siblings are self-sterile and cross-fertile in a bipolar pattern. The fertile interaction in compatible matings is morphologically distinguishable in the formation of a differentiated dikaryotic mycelium without the clamp connexions common in the dikaryons of other Hymenomycetes. The segregation pattern of incompatibility alleles and nutritional markers indicates haploidy of vegetative nuclei. Six parental and four rare, non-parental incompatibility types were identified in the sample studied. Heterokaryotic interactions -dikaryons with homokaryons and di karyons with di karyons to establish new dikaryons -have been shown t o occur. A remote kinship to the cultivated mushroom was demonstrated in the formation of transitory heterokaryons between A . bitorquis and A. bisporus, but these could not be fruited. The life-cycles and patterns of sexuality in the two species are compared and the possibility that A. bitorquis could be an alternative to A . bisporus for mass cultivation and consumption, with emphasis on the advantage in breeding A . bitorquis, is mentioned. I N T R O D U C T I O NThe functional relationships among members of the genus Agaricus have not been explored. The origin of the commonly cultivated bisporic mushroom remains a mystery, and its relationship to the predominating tetrasporic forms found in nature is unknown. A knowledge of life-cycles and interfertility patterns within the genus is requisite to an understanding of species and their possible kinships.The life-cycle and sexual nature of the cultivated Agaricus bisporus have recently been described (Miller, 1971;Raper, Raper & Miller, 1972; Miller & Kananen, 1972; Raper & Raper, I 972; Elliott, 1972). The first comprehensive biological characterization of a wild, tetrasporic species of Agaricus is reported here. Life-cycles and sexual interactions were analysed in five collections, and the relationship between these collections and A . bisporus was examined. Although the five collections were originally designated as representing three species, all have been found to comprise a single species, presently designated Agaricus bitorquis (QuClet) Saccardo. The species is edible, tasty, cultivatable and of possible interest to commercial mushroom growers. M E T H O D SStocks. The five collections of Agaricus from nature that were examined in this study are listed here as stocks I to 5, with the species identification as originally designated.
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