Silencing core miRNA pathway genes disrupts ecdysis and development in white‐backed planthopper ( Sogatella furcifera ) via RNAi and nanocarrier‐mediated delivery

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.