Genome biology and evolution of mating-type loci in four cereal rust fungi

Permanent heterozygous loci, such as sex- or mating-compatibility regions, often display suppression of recombination and signals of genomic degeneration. In Basidiomycota, two distinct loci confer mating compatibility. These loci encode homeodomain (HD) transcription factors and pheromone receptor (Pra)-ligand allele pairs. To date, an analysis of genome level mating-type (MAT) loci is lacking for obligate biotrophic basidiomycetes in the Pucciniales, an order containing serious agricultural plant pathogens. Here, we focus on four species of Puccinia that infect oat and wheat, including P. coronata f. sp. avenae, P. graminis f. sp. tritici, P. triticina and P. striiformis f. sp. tritici. MAT loci are located on two separate chromosomes supporting previous hypotheses of a tetrapolar mating compatibility system in the Pucciniales. The HD genes are multiallelic in all four species while the PR locus appears biallelic, except for P. graminis f. sp. tritici, which potentially has multiple alleles. HD loci are largely conserved in their macrosynteny, both within and between species, without strong signals of recombination suppression. Regions proximal to the PR locus, however, displayed signs of recombination suppression and genomic degeneration in the three species with a biallelic PR locus. Our observations support a link between recombination suppression, genomic degeneration, and allele diversity of MAT loci that is consistent with recent mathematical modelling and simulations. Finally, we confirm that MAT genes are expressed during the asexual infection cycle, and we propose that this may support regulating nuclear maintenance and pairing during infection and spore formation. Our study provides insights into the evolution of MAT loci of key pathogenic Puccinia species. Understanding mating compatibility can help predict possible combinations of nuclear pairs, generated by sexual reproduction or somatic recombination, and the potential evolution of new virulent isolates of these important plant pathogens.