• 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.
Pan et al. (Sun,) studied this question.