Genome biology and evolution of mating type loci in four cereal rust fungi
Obligate heterozygous loci such as sex- or mating-compatibility regions often display suppression of recombination and signals of genomic degeneration. In Basidiomycota, two distinct gene loci confer mating compatibility. These encode for homeodomain (HD) transcription factors and pheromone receptor (Pra)-ligand pairs. To date genome level mating type (MAT) loci analysis is lacking for obligate biotrophic basidiomycetes in the order Pucciniales, which contains many economically important plant pathogens. Here, we focus on four Puccinia cereal rust species, including P. coronata f. sp. avenae, Puccinia graminis f. sp. tritici, P. triticina and P. striiformis f. sp. tritici, which infect oat and wheat. MAT loci are located on two separate chromosomes supporting previous hypotheses of tetrapolar mating types in the Pucciniales. The HD locus is multiallelic in all four species while the PR locus appears to be biallelic except for P. graminis f. sp. tritici which displays genetic features of more than two alleles. HD loci were largely conserved in their macrosynteny within and between species without strong signals of recombination suppression. PR loci proximate regions, however, displayed extensive signs of recombination suppression and genomic degeneration in the three species with a clear biallelic PR locus. These observations suggest a correlation between recombination suppression, genomic degeneration and allele status of MAT loci which is consistent with recent mathematical modelling and simulations. Finally, we confirm the evolutionary conservation of MAT gene expression during the asexual infection cycle of the cereal host which we propose is related to correct nuclear pairing during spore formation. Together, our study provides insights into the evolution of MAT loci of key pathogenic Puccinia species. This detailed understanding is important to predict possible combinations of nuclear pairs that can arise via sexual reproduction or somatic recombination to enable the evolution of newly virulent isolates of these important plant pathogens. Author summarySex of animals and some plants is determined by sex chromosomes. In fungi, mate compatibility is determined by mating type (MAT) loci, which share some features with sex chromosomes including recombination suppression around heterozygous loci. Here, we study the MAT loci in fungal pathogens from the order Pucciniales that can cause rust diseases on many economically important plants including wheat and oat. We show that one of the MAT loci is multiallelic, while the other is biallelic. The biallelic locus shows strong signs of recombination suppression and genetic deterioration with an increase in transposable elements and gene deserts surrounding the locus. Our findings on the genome biology of MAT loci in four economically important pathogens will lead to a better understanding and prediction of evolution of novel virulent isolates that can lead to large scale pandemics in agriculture.