A fungal phosphate starvation regulator gates virulence to prioritize nutrient adaptation in response to host phosphate status

Abstract

Plant-associated microbes must constantly balance environmental adaptation with virulence to survive in fluctuating ecosystems, yet the molecular mechanisms coupling these processes remain poorly understood. Here, we identify NUTRIENT-DEPENDENT FACILITATOR OF COLONIZATION1 (NFC1), a virulence factor in a conditionally pathogenic Colletotrichum tofieldiae strain, whose expression is tightly regulated by both temperature and phosphate availability. Leveraging plant phosphate starvation response (PSR) mutants and direct phosphate supplementation to host plants, we demonstrate that NFC1 expression is driven by the internal phosphate status of the host rather than environmental availability alone. Notably, the fungal PSR regulator CtPHO4 represses NFC1 and virulence during phosphate starvation, while simultaneously activating canonical fungal PSR-related genes. Conversely, under phosphate sufficiency, NFC1 is strongly induced and promotes infection, potentially by modulating the host circadian clock system. This study uncovers a molecular link between metabolic adaptation and virulence programming, providing a conceptual framework for predicting disease dynamics under changing environments.