On the asymmetry of mating in natural populations of the mushroom fungus Schizophyllum commune

Before a mycelium of a mushroom-forming basidiomycete develops mushrooms, the monokaryotic mycelium needs to become fertilized. Although the mechanistic details of mating in mushrooms have been studied thoroughly in laboratory research, very little is known on mating patterns in nature. In this study, we performed fine-scale analyses of three populations of Schizophyllum commune from their natural substrate (i.e. dead beech branches). From the three branches, 24, 12, and 24 fruiting bodies were isolated and for each mushroom, the origins of its nuclei and cytoplasm were reconstructed using DNA markers. Nuclear genotypes were determined using sequencing data and mating types, and mitochondrial haplotypes using SNP markers. From these combined data we reconstructed colonization and mating patterns of the mycelia. On each branch, we found multiple dikaryons (3, 3, and 8, respectively); in two instances one nuclear haplotype was shared between two dikaryons and in two other cases a nuclear haplotype was shared between three dikaryons. Each dikaryon always had a single mitochondrial haplotype. These findings indicate that mating usually is not symmetrical and that a monokaryon is most likely fertilized by a small monokaryon, a spore or a dikaryon. Sharing of nuclear haplotype between different dikaryons resulted either from multiple fertilizations of a single monokaryon, if the dikaryons had identical mitochondrial haplotypes, or, if the dikaryons had different mitochondrial haplotypes, most likely from secondary matings between a monokaryon and a dikaryon (Buller phenomenon). We conclude that mating in S. commune between same-sized monokaryons with reciprocal migration, as generally described in textbooks, is rare in nature. We discuss the implications of non-symmetric mating for basidiomycete evolution.