Host-Induced Gene Silencing of SmDSR32 Enhances Wheat Defense Against Sitobion miscanthi

The grain aphid, Sitobion miscanthi, poses a serious threat to cereal crops worldwide, leading to considerable yield losses and demanding annual insecticide applications during the grain-filling stage. As a sustainable alternative, we explored host-induced gene silencing (HIGS) targeting an aphid-specific gene. In this study, we identified SmDSR32, a novel gene encoding a salivary peptide in S. miscanthi, and validated its suitability for RNAi. Transgenic wheat lines expressing SmDSR32-dsRNA were generated. Aphids feeding on these lines showed a 20-fold reduction in SmDSR32 transcript levels compared with controls. This silencing disrupted normal feeding behavior in electropenetrography (EPG) analyses, characterized by a 1.94-fold prolongation of intercellular probing and a 61% shortening of phloem ingestion. Consequently, aphid performance was severely compromised, with at least a 56.7% decrease in survival, a shortening of 5 days in lifespan, and a reduction of 9–10 individuals in aphid progeny production. Impressively, upon being transferred to wild-type plants, both the surviving aphids and their progeny sustained fitness deficits, with a 30% reduction in survival still observed in the first generation. These findings validate SmDSR32 as a potent RNAi target and establish HIGS targeting essential salivary genes as a promising strategy for sustainable aphid management in wheat.