Cross-kingdom signaling manipulation by insect-associated microbial symbionts: Linking molecular mechanisms to pest management strategies.

Microbial symbionts associated with herbivorous insects can modulate plant hormone networks and reconfigure induced defenses during feeding. This review synthesizes current knowledge on how symbiont effectors converge on conserved jasmonic acid (JA)/salicylic acid (SA)/ethylene (ET) signaling hubs to suppress or reprogram plant immunity. These microbial partners secrete a diverse arsenal of bioactive molecules, including effector proteins (e.g., the histidine-rich Ca2+-binding protein ApHRC from Serratia symbiotica in pea aphids), enzymes (e.g., gut microbiome-derived proteases in Anticarsia gemmatalis larvae), and host metabolite mimics (e.g., cytokinin production induced by Wolbachia in the apple leaf-mining moth). Through these mechanisms, symbionts selectively manipulate plant hormonal pathways, a form of molecular interference that often enhances herbivore performance by increasing feeding efficiency, fecundity, and host plant range, thereby increasing plant susceptibility to biotic stress. These physiological alterations trigger cascading ecological effects, reshaping multitrophic interactions: symbiont-mediated changes in herbivore-induced plant volatiles (HIPVs) and secondary metabolites influence the behavior of natural enemies, alter competitive outcomes among herbivores, and disrupt plant-insect communication. Consequently, microbial symbionts act as hidden ecological engineers, driving community dynamics and evolutionary trajectories. By integrating molecular, ecological, and evolutionary perspectives, we propose a unified framework that explicitly links symbiont effector function to plant immune modulation and its ecosystem-level consequences. Ultimately, this synthesis underscores the potential of targeting insect-microbe partnerships through approaches such as effector blocking, microbiome augmentation, or symbiont disruption, for developing sustainable pest management strategies and advancing the field of plant defense ecology. © 2026 Society of Chemical Industry.