Co-infestation by two major pests suppresses phenylpropanoid defense and reprograms volatiles to facilitate stable cohabitation on rice.

Abstract

Classical ecological theory predicts that herbivorous species are in competition when they share the same host plant, yet in agricultural systems certain pest insects can stably coexist on the same plant, and even perform better when they feed together than if they feed alone. As yet, the molecular mechanisms underlying such collaborative cohabitation have remained unclear. Here we unravel how two major rice pests, the brown planthopper (BPH, Nilaparvata lugens) and the rice leaf folder (RLF, Cnaphalocrocis medinalis), achieve stable cohabitation by jointly suppressing plant chemical defenses. Prior BPH feeding induced strong rice resistance that reduced RLF performance, whereas prior RLF feeding did not affect BPH. This asymmetric consequence of resistance induction was fully abolished when both pests initiated feeding simultaneously. Metabolomics and network analyses identified phenylpropanoid-derived chlorogenic acids and coniferin as key BPH-induced defense compounds detrimental to RLF but not BPH. Dual infestation suppressed the accumulation of these toxins by inhibiting the phenylpropanoid pathway through downregulation of the hub gene OsHCT4. Feeding assays with mutant and overexpression lines confirmed the key role of the phenylpropanoid pathway in determining if the interaction results in competition or coexistence. Moreover, plants with dual infestation were preferred by ovipositing females of both pests due to reduced emissions of decanal that repels RLF and BPH but enhanced release of DMNT and (E)-nerolidol that attract BPH females. These findings reveal how herbivores can jointly subvert host plant defenses to relax competition, providing a mechanistic extension of niche segregation and competition theory.