Mating-type (MAT) loci are traditionally considered vestigial remnants in asexual fungi, yet their widespread retention suggests additional, yet unrecognised functions. Here we show that in the asexual plant pathogen Fusarium oxysporum f.sp. lycopersici the two MAT loci function as master regulators of developmental processes through autocrine pheromone signalling. MAT1-1 and MAT1-2 exhibit opposing regulatory roles in density-dependent conidial germination, creating a bistable switch for population-level behavioural coordination. MAT1-1 promotes vegetative hyphal fusion and multicellular aggregation, whereas MAT1-2 inhibits these processes. These opposing effects are mediated in part by enhanced expression of the protease Bar1 in MAT1-2 isolates, which specifically cleaves α-pheromone thereby modulating signalling responses. Unexpectedly, MAT1-1 enhances virulence of F. oxysporum on tomato plants in a background-dependent manner, whereas MAT1-2 exhibits only a slight influence on pathogenicity. Together, our findings establish that MAT loci have undergone evolutionary repurposing to control essential developmental processes through autocrine communication networks, revealing novel targets for sustainable disease management approaches.
Keywords: Fusarium oxysporum; autocrine pheromone signalling; evolutionary co‐option; fungal pathogenicity; mating‐type loci; quorum sensing.
© 2026 The Author(s). Molecular Plant Pathology published by British Society for Plant Pathology and John Wiley & Sons Ltd.