Salivary elicitor disulfide isomerase from Nilaparvata lugens targets host rice UDP-glucose epimerase 2 to induce plant defenses

•NlPDI1 activates rice defense by inducing H2O2, JA, and JA-Ile production.•NlPDI1 interacts with OsUGE2, decreasing its protein levels and affecting immunity.•OsUGE2 negatively regulates BPH defense responses and performance.•NlPDI1 is crucial for BPH feeding, survival and reproduction.•NlPDI1′s role in insect growth prevents evolutionary adaptation to evade detection by plants. Elicitors in insect saliva enable plants to detect insect presence and activate their defense responses. However, the detailed mechanisms through which these elicitors induce host plant defense responses and interact with endogenous host plant proteins remain poorly understood. In this study, we identified a salivary elicitor, protein disulfide isomerase (NlPDI1), from the brown planthopper (Nilaparvata lugens, BPH). Overexpression of NlPDI1 in rice triggered the production of hydrogen peroxide (H2O2), jasmonate (JA), and JA-isoleucine (JA-Ile), thereby enhancing rice's resistance to BPH. Furthermore, NlPDI1 interacts with the immunity-related protein UDP-glucose epimerase 2 (OsUGE2), leading to a decrease in OsUGE2 protein abundance. BPH performance was negatively affected in uge2 mutants, which exhibited elevated levels of H2O2, JA, and JA-Ile, along with stunted growth. Conversely, BPH preferred the rice overexpressing OsUGE2, which displayed reduced levels of H2O2, JA, and JA-Ile. These findings elucidate the mechanism by which the salivary elicitor NlPDI1 induces defense responses in host rice by targeting the negative immune regulator OsUGE2. However, NlPDI1 is essential for the feeding, survival, and fecundity of BPH. The significance of NlPDI1 for insect growth makes it unlikely that the insect could evolve ways to evade perception by rice.