Abstract
The mating compatibility in fungi is generally governed by genes located within a single or two unlinked mating type (MAT) loci. Hypsizygus marmoreus is an edible mushroom in the order Agaricales with a tetrapolar system, which contains two unlinked MAT loci-homeodomain (HD) transcription factor genes and pheromone/pheromone receptor genes (P/R). In this study, we analyzed the genetic structure and diversity of MAT loci in tetrapolar system of H. marmoreus through sequencing of 54 heterokaryon and 8 homokaryon strains. Although within the HD loci, the gene order was conserved, the gene contents were variable, and the HD loci haplotypes were further classified into four types. By analyzing the structure, phylogeny, and the HD transmissibility based on the progeny of these four HD mating-type loci types, we found that they were heritable and tightly linked at the HD loci. The P/R loci genes were found to comprise three pheromone receptors, three pheromones, and two pheromone receptor-like genes. Intra- and inter-specific phylogenetic analyses of pheromone receptors revealed that the STE3 genes were divided into three groups, and we thus theorize that they diverged before speciation. Comparative analysis of the MAT regions among 73 Basidiomycete species indicated that the diversity of HD and P/R loci in Agaricales and Boletales may contribute to mating compatibility. The number of HD genes were not correlated with the tetrapolar or bipolar systems. In H. marmoreus, the expression levels of these genes at HD and P/R loci of compatible strains were found higher than in those of homonuclear/homokaryotic strains, indicating that these mating genes acted as switches for mating processes. Further collinear analysis of HD loci in interspecific species found that HD loci contains conserved recombination hotspots showing major rearrangements in Coprinopsis cinerea and Schizophyllum commune, suggesting different mechanisms for evolution of physically linked MAT loci in these groups. It seems likely that gene rearrangements are common in Agaricales fungi around HD loci. Together, our study provides insights into the genomic basis of mating compatibility in H. marmoreus.
Highlights
Sexual reproduction plays a pivotal role in the biology of many eukaryotes (Dacks and Roger 1999)
The number of mating types can be greatly influenced by the recombination and suppression around mating type loci, and previous studies had showed that linkage of loci involved in gamete recognition and post syngamy compatibility is responsible for derivation of a bipolar mating-type segregation from a tetrapolar system that has two independently segregating traits (Petit et al 2012)
The mitochondrial intermediate peptidase (Mip) gene was closely linked to HD1.1 genes, whereas the beta-flanking gene (Bfg) gene was closely linked to HD2.2 at the other end, similar to other fungi in Agaricomycetes (James et al 2004a), excluding S. commune and L. edodes (Ohm et al 2010)
Summary
Sexual reproduction plays a pivotal role in the biology of many eukaryotes (Dacks and Roger 1999). The tetrapolar system comprises two unlinked matingtype loci (Xiong et al 2014); the HD loci, encoding two homeodomain-type transcription factors controlling post-mating growth, and the P/R loci, usually containing tightly linked pheromone and pheromone receptor genes that are involved in premating recognition (Xiong et al 2014; Sun et al 2019). These genes encode pre-mating lipopeptide pheromones and their cognate receptors (P/R), which mediate recognition of mating partners and cell fusion. The number of mating types can be greatly influenced by the recombination and suppression around mating type loci, and previous studies had showed that linkage of loci involved in gamete recognition and post syngamy compatibility is responsible for derivation of a bipolar mating-type segregation from a tetrapolar system that has two independently segregating traits (Petit et al 2012)
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