Abstract

BACKGROUND: MicroRNAs (miRNAs) regulate gene expression at the post-transcriptional level and play critical roles in diverse cellular processes. However, the functional significance of miRNA pathway core genes in the white-backed planthopper ( Sogatella furcifera , WBPH), a major rice pest in Asia, remains poorly understood. RESULTS: Here, we identified eight core miRNA pathway genes ( SfDicer-1 , SfArgonaute-1 , SfArgonaute-2 , SfArgonaute-3 , SfPasha , SfDrosha , SfLoquacious , and SfExportin-5 ) in WBPH and evaluated their functions using microinjection-based RNA interference (RNAi). To enhance field relevance, a spray-induced, nanocarrier-delivered gene silencing system (SI-NDGS) was applied, confirming lethal and developmental defects, particularly molting and cuticle abnormalities. Transcriptome analysis of five genes with high lethality ( SfArgonaute-1 , SfDrosha , SfLoquacious , SfExportin-5 , and SfPasha ) revealed extensive dysregulation of hundreds of genes, including key cuticle-related genes ( Cuticular Protein and Chitinase-N-acetylglucosaminidase ), perturbation of ecdysone signaling, and activation of the apoptotic gene Caspase-1 , collectively explaining ecdysis failure, wing deformities, melanization and high mortality. CONCLUSIONS: These findings demonstrate that miRNA core pathway genes are essential for WBPH ecdysis and survival, highlighting their potential as RNAi targets for precise, eco-friendly pest management. This work provides a mechanistic framework linking miRNA pathway disruption to lethal phenotypes in a major agricultural pest and introduces SI-NDGS as an innovative delivery strategy for RNAi-based crop protection. © 2026 Society of Chemical Industry.