Amplification of a metabolic shunt for elicitor detoxification: a jasmonate‐exploited insect counter‐defense strategy

BACKGROUND: Chemical elicitors offer a promising strategy for sustainable pest control by activating plant defense responses. The elicitor 4-fluorophenoxyacetic acid (4-FPA) induces resistance in rice against the white-backed planthopper (WBPH; Sogatella furcifera) by triggering deposition of phenolic polymers that form a physical feeding barrier. However, whether piercing-sucking insects possess counter-defense strategies against such elicitor-induced resistance remains unknown. RESULTS: We found that infestation by gravid WBPH females (WBPH-GF) systemically suppressed 4-FPA-induced phenolic polymer deposition without degrading pre-formed deposits, thereby restoring nymph survival. Metabolomic analysis revealed that WBPH-GF reprogrammed 4-FPA metabolism from side-chain cleavage to 4-fluorophenol toward conjugation with l-aspartic acid and l-glutamic acid, with the 4-FPA-aspartate conjugate increasing approximately 56-fold. This shift correlated with up-regulation of the amide synthetase gene OsGH3.8 and maintenance of aspartate and glutamate levels. Crucially, this process requires jasmonate (JA) signaling, as demonstrated by JA-deficient mutants and exogenous methyl jasmonate application. CONCLUSION: Our findings reveal that WBPH-GF overcomes 4-FPA-induced resistance by hijacking the host JA pathway to amplify a latent metabolic shunt that diverts the elicitor into inert amino acid conjugates, thereby depleting the substrate for defensive polymer formation. This work uncovers a previously uncharacterized counter-defense strategy wherein a herbivore co-opts plant hormone signaling to metabolically disarm an exogenous elicitor, providing important insights for designing next-generation plant chemical elicitors with metabolic stability.