A population mating investigation reveals that mating-type locus StMAT1-2 dominates field pathogenesis by directly regulating the expression of the pheromone receptor StSte2 in Setosphaeria turcica

Northern corn leaf blight, a globally significant maize disease, is caused by the heterothallic fungus Setosphaeria turcica, which relies on mating type for its sexual reproduction. The mating-type locus (MAT) genes StMAT1-1 and StMAT1-2 determine three mating types (A, a, and Aa) of S. turcica. The sexual cycle of S. turcica in natural ecosystems has garnered substantial research interest; however, the functional dynamics of its sexual reproduction-including regulatory mechanisms and adaptive significance-remain uncharacterized. From 2011 to 2023, a 13-year continuous monitoring of S. turcica in major Chinese corn-producing regions identified the a mating type (with StMAT1-2) as the field-dominant type. Laboratory analyses of artificially induced F1 populations confirmed that a mating-type strains exhibit superior fitness (enhanced sporulation, faster mycelial growth, stronger pathogenicity) compared with A mating-type strains (with StMAT1-1). Generation of mating-type gene mutants demonstrated that StMAT1-1 and StMAT1-2 are essential for sexual reproduction in S. turcica. Transcriptome analysis further revealed that StMAT1-2 regulates a larger set of genes involved in metabolism-related pathways. Mechanistically, StMAT1-2 directly binds to the promoter of pheromone receptor gene StSte2 to modulate its expression. Silencing StSte2 disrupted sexual reproduction and downregulated downstream MAPK pathway genes, while exogenous pheromone partially rescued these defects, verifying the pheromone pathway's role in S. turcica sexual reproduction. Notably, silencing of StMAT1-2 and StSte2 was associated with reduced sporulation and pathogenicity. Collectively, StMAT1-2 regulates sexual reproduction and pathogenicity by targeting StSte2, driving the field dominance of the a mating type. This study advances understanding of mating-type distribution bias in heterothallic fungi.