Unconventional Recombination in the Mating Type Locus of Heterothallic Apple Canker Pathogen <i>Valsa mali</i>

Abstract

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