Planthopper-induced volatiles suppress rice plant defense by targeting Os4CL5-dependent phenolamide biosynthesis

Plants typically respond to attacks by herbivorous arthropods by releasing specific blends of volatiles. A common effect of these herbivore-induced plant volatiles (HIPVs) is that they prime neighboring plants to become more resistant to the same herbivores. The brown planthopper (BPH) apparently has "turned the tables" on rice plants by inducing volatiles that make exposed plants more susceptible to BPH attack. Here, we uncover the molecular mechanism behind this counterintuitive response in rice plants. Exposure to BPH-induced volatiles was found to suppress jasmonic acid (JA) signaling in rice plants, impairing their chemical defenses and enhancing planthopper performance. Metabolomic analyses revealed a significant reduction in phenolamides, notably N-feruloylputrescine, a JA-regulated compound with strong anti-BPH activity. We identify Os4CL5, a key gene in the phenylpropanoid-polyamine conjugate pathway, as a central node in this suppression. HIPV exposure markedly reduced Os4CL5 expression and N-feruloylputrescine accumulation. Using a rice mutant, we confirmed that Os4CL5 is essential for both N-feruloylputrescine production and resistance to BPH. By identifying Os4CL5 as the molecular target of BPH-induced volatiles and linking its suppression to reduced N-feruloylputrescine biosynthesis, our study provides the first mechanistic insight into volatile-mediated defense disruption and opens a new avenue for enhancing rice pest resistance.