A secreted GH12 endoglucanase from Fusarium graminearum promotes root colonization and activates defense in maize...

Fusarium graminearum, a major fungal pathogen of cereal crops, deploys an array of effectors to subvert plant immunity, causing substantial yield and quality losses. In this study, we performed transcriptomic analysis during maize root infection and identified a highly expressed secreted gene, FgCel4, which plays a critical role in pathogenesis. FgCel4 is a nuclear-localized glycoside hydrolase family 12 protein that exhibits endoglucanase activity. Loss of its function compromises pathogenicity on maize roots without significantly affecting fungal growth. We demonstrated that FgCel4 triggers cell death in N. benthamiana in a manner independent of light and its signal peptide. Furthermore, FgCel4 does not act as a typical pathogen-associated molecular pattern (PAMP) but requires its intact, enzymatically active structure to elicit this immunogenic response. This activity is partially suppressed by an uncharacterized plant LRR protein, RCel4, which is upregulated in infected maize roots and interacts with FgCel4 in the nucleus. Importantly, pretreatment of maize roots with FgCel4 conferred enhanced resistance, resulting in significantly reduced disease symptoms. Our findings thus unveil a novel pathogenicity-related hydrolase that is targeted by a host immune protein, and they highlight the potential of utilizing such effector proteins in developing induced resistance strategies.