Mating system complexity and cryptic speciation in the seed bank pathogen Pyrenophora semeniperda

Abstract

Mating strategies contributing to a balance between inbreeding and outcrossing are understudied in all but a few model fungal pathogens. This study examined factors that influence the occurrence of the sexual state of Pyrenophora semeniperda. It was consistently found to have functional copies of the MAT1‐1 and MAT1‐2 idiomorphs essential for sexual reproduction, despite considerable polymorphism in both single nucleotide polymorphisms (SNPs) and number of 18‐base minisatellite repeats. The two idiomorphs occurred at approximately equal frequencies across 25 populations on Bromus tectorum seeds in the western United States, suggesting maintenance of sexual reproduction. The putative mating system is described as facultative pseudohomothallism, with only one of the two MAT1 idiomorphs found in a nucleus. Unikaryotic strains of opposite mating type can potentially mate, as can nuclei of opposite mating type in a thallus that results from anastomosis between vegetatively compatible unikaryotic strains. Strains shown to be dikaryotic using simple sequence repeat (SSR) markers may contain either or both MAT1 idiomorphs. Most populations consist of a mixture of MAT1‐1, MAT1‐2 and MAT1‐1/MAT1‐2 genotypes. A possible constraint on recombination is the presence of multiple strain groups characterized by ITS haplotype. These are apparently vegetatively incompatible, as even dikaryotic strains are invariably composed of a single ITS haplotype. Different ITS haplotypes also have unique combinations of MAT1‐1 and MAT1‐2 allelic variants, suggesting that perhaps these strain groups are also sexually incompatible. Phylogenetic analysis using both genome‐wide SNP/indel polymorphisms and SSR markers demonstrated genetic divergence among ITS haplotypes, supporting the hypothesis that these strain groups may represent cryptic species.