Unconventional Recombination in the Mating Type Locus of Heterothallic Apple Canker Pathogen Valsa mali

Sexual reproduction in filamentous ascomycetes is controlled by the mating type (MAT) locus, including two idiomorphs MAT1-1 and MAT1-2. Understanding the MAT locus can provide clues for unveiling the sexual development and virulence factors for fungal pathogens. The genus Valsa (Sordariomycetes, Diaporthales) contains many tree pathogens responsible for destructive canker diseases. The sexual stage of these ascomycetes is occasionally observed in nature, and no MAT locus has been reported to date. Here, we identified the MAT locus of the apple canker pathogen Valsa mali, which causes extensive damage, and even death, to trees. V. mali is heterothallic in that each isolate carries either the MAT1-1 or MAT1-2 idiomorph. However, the MAT structure is distinct from that of many other heterothallic fungi in the Sordariomycetes. Two flanking genes, COX13 and APN2, were coopted into the MAT locus, possibly by intrachromosomal rearrangement. After the acquisition of foreign genes, unequal recombination occurred between MAT1-1/2 idiomorphs, resulting in a reverse insertion in the MAT1-2 idiomorph. Evolutionary analysis showed that the three complete MAT1-1-2, COX13, and APN2 genes in this region diverged independently due to different selection pressure. Null hypothesis tests of a 1:1 MAT ratio of 86 V. mali isolates from four different provinces showed a relatively balanced distribution of the two idiomorphs in the fields. These results provide insights into the evolution of the mating systems in Sordariomycetes.