Phenylacetate Hydroxylase SsPhacA Modulates p ‐Coumaric Acid Accumulation to Regulate the Mating/Filamentation of Sporisorium scitamineum

Sugarcane smut, caused by Sporisorium scitamineum , is one of the most severe sugarcane diseases. A key pathogenic step is dikaryotic mycelium formation via sexual reproduction, but its regulatory mechanism is unclear. In this study, we identified a phenylacetate hydroxylase gene, SsPHACA , that is highly expressed during the sexual mating/filamentation of S. scitamineum and enriched within the phenylalanine metabolic pathway. SsPHACA deletion mutants presented significantly reduced sexual mating/filamentation and pathogenicity. Additionally, deletion of SsPHACA resulted in marked downregulation of the pheromone‐responsive transcription factor gene SsPRF1, a critical regulator of sexual mating/filamentation in S. scitamineum , as well as its downstream genes at the a‐ and b‐ locus genes. Constitutive expression of SsPRF1 restored the sexual mating/filamentation of the SsPHACA deletion mutant. Metabolomic analyses revealed that SsPhacA mediates phenylalanine metabolism in S. scitamineum and modulates the accumulation of p ‐coumaric acid, an intermediate in phenylalanine metabolism. Exogenous supplementation with p ‐coumaric acid increased the transcriptional level of SsPRF1 and partially restored sexual mating/filamentation in SsPHACA deletion mutants. In summary, our results demonstrate that SsPhacA mediates the phenylalanine metabolic pathway to modulate p ‐coumaric acid accumulation, which increases the transcriptional level of SsPRF1 , thereby regulating sexual reproduction in S. scitamineum . These findings not only identify a new regulatory factor involved in the sexual mating/filamentation of S. scitamineum, but also provide a new theoretical foundation for the development of disease control strategies targeting metabolic pathways.