A co-regulatory switch for immunity and yeast-like symbiont release: Pleiotropic mechanism of the JH-Met signaling pathway in Nilaparvata lugens (Stål).

Abstract

Hormonal signaling pleiotropically regulates insect physiological processes, including development, reproduction, and immunity. Juvenile hormone (JH) and its receptor Methoprene-tolerant (Met) modulate immune responses across many insect species. Our previous studies demonstrated that mating behavior in Nilaparvata lugens induces the expression of defensin genes NlDfA/B, enhancing resistance to pathogens. Furthermore, the abundance of yeast-like symbionts (YLS) is closely linked to the reproduction-immunity trade-off. However, the regulatory mechanism underlying the dynamic changes in NlDfA/B expression and YLS remains unclear. Here, ELISA assays revealed that JH titers in female brown planthoppers gradually increased after eclosion, whereas NlDfA/B genes expression showed the opposite trend, accompanied by the release of YLS from the fat body to hemolymph. Exogenous JH treatment significantly suppressed NlDfA/B expression and promoted YLS release. Conversely, RNAi-mediated knockdown of juvenile hormone acid methyltransferase (NlJHAMT) upregulated NlDfA/B expression and reduced YLS levels in hemolymph. Western blot results further confirmed the inhibitory effect of JH on NlDfA/B protein expression. Mechanistically, JH via its receptor Met directly suppressed NlDfA/B promoter activity. Our findings reveal a regulatory circuit: JH suppresses NlDfA/B-mediated immune defense, thereby facilitating YLS release from fat body into hemolymph. This establishes an intrinsic link among insect hormone, immunity, and symbiotic fungus release, providing insights for green pest control targeting key genes and symbionts.