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

Abstract

AbstractObligate 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 orderPucciniales, which contains many economically important plant pathogens.Here, we focus on fourPucciniacereal rust species, includingP. coronataf. sp.avenae,Puccinia graminisf. sp.tritici,P. triticinaandP. striiformisf. sp.tritici, which infect oat and wheat.MATloci are located on two separate chromosomes supporting previous hypotheses of tetrapolar mating types in thePucciniales. TheHDlocus is multiallelic in all four species while thePRlocus appears to be biallelic except forP. graminisf. sp.triticiwhich displays genetic features of more than two alleles.HDloci were largely conserved in their macrosynteny within and between species without strong signals of recombination suppression.PRloci proximate regions, however, displayed extensive signs of recombination suppression and genomic degeneration in the three species with a clear biallelicPRlocus. These observations suggest a correlation between recombination suppression, genomic degeneration and allele status ofMATloci which is consistent with recent mathematical modelling and simulations. Finally, we confirm the evolutionary conservation ofMATgene 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 ofMATloci of key pathogenicPucciniaspecies. 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 theMATloci in fungal pathogens from the orderPuccinialesthat can cause rust diseases on many economically important plants including wheat and oat. We show that one of theMATloci 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 ofMATloci 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.