UvNTH-mediated trehalose metabolism is essential for rice false smut ball formation in Ustilaginoidea virens

• U. virens exploits host-derived trehalose by enhancing trehalose catabolism, uncovering a previously unrecognized pathogenic strategy in plant-fungal interactions. • UvNTH is essential for false smut ball formation, and its deletion decouples colonization from symptom development, highlighting its unique role in fungal pathogenicity. • UvNTH coordinately regulates virulence and chlamydospore reproduction, serving as a dual-action target for precise and sustainable rice false smut control. The fungal pathogen Ustilaginoidea virens , which causes the devastating rice false smut disease, relies on scavenging host nutrients for infection, yet the identity and exploitation mechanisms of these nutrients remain unclear. This study reveals a previously unrecognized virulence strategy in which U. virens hijacks host-derived trehalose, a disaccharide linked to plant stress responses, by enhancing its trehalose catabolic capacity. Central to this process are two functionally distinct trehalases, UvNTH (neutral trehalase) and UvATH (acid trehalase), which exhibit a clear division of labor. UvNTH drives extracellular trehalose utilization, vegetative growth, and asexual sporulation, while UvATH specifically regulated aerial hyphal development. Strikingly, the Δ UvNTH mutant colonizes host tissues normally but completely fails to produce mature false smut balls, uncoupling colonization from symptom formation and identifying UvNTH as a dedicated virulence switch essential for pathogenicity. In addition, UvNTH plays a critical regulatory role in the germination process of chlamydospores, the primary inoculum of the pathogen. Collectively, these findings demonstrate that UvNTH functions not only as a metabolic enzyme but also as a dual-functional regulator that coordinates virulence and the propagation of primary infection sources, thereby providing an ideal target for the sustainable management of rice false smut.