Mediation of JA signalling in glandular trichomes by thewoolly/SlMYC1regulatory module improves pest resistance in tomato

Almost all plants form trichomes, which protect them against insect herbivores by forming a physical barrier and releasing chemical repellents. Glandular trichomes produce a variety of specialized defensive metabolites, including volatile terpenes. Previous studies have shown that the defence hormone jasmonic acid (JA) affects trichome development and induces terpene synthases (TPSs) but the underlying molecular mechanisms remain unclear. Here, we characterized a loss-of-function allele of the HD-ZIP IV transcription factorwoolly(wo) and analysed its role in mediating JA signalling in tomato. We showed that knockout ofwoled to extensive trichome defects, including structural and functional changes in type VI glandular trichomes, and a dramatic reduction in terpene levels. We further found that wo directly binds to TPS gene promoters to recruit SlMYC1, a JA signalling modulator, and that together these transcription factors promote terpene biosynthesis in tomato trichomes. The wo/SlMYC1 regulatory module is inhibited by SlJAZ2 through a competitive binding mechanism, resulting in a fine-tuned JA response in tomato trichomes. Enhanced expression ofSlMYC1substantially increased terpene levels and improved tomato resistance to spider mites. Interestingly, we also found thatSlMYC1plays an additional role in glandular cell division and expansion in type VI trichomes, independent of JA. Together, our results reveal a novel, JA-mediated regulatory mechanism that promotes insect resistance in tomato.