A plant virus-derived siRNA modulates wing dimorphism and fertility of vector insects to enhance virus spread

INTRODUCTION: The infection of plant viruses alters the wing dimorphism and reproductive development of vector insects, thereby enhancing viral dissemination. Notably, a fundamental trade-off inherently exists between wing development and reproductive development in insects. However, the regulatory mechanisms through which plant viruses balance these developmental processes remain poorly characterized. Elucidating such mechanisms is crucial for understanding viral transmission strategies. OBJECTIVES: This study aims to elucidate the molecular mechanism by which southern rice black-streaked dwarf virus (SRBSDV) regulates the wing dimorphism and reproductive development in white-backed planthopper (WBPH, Sogatella furcifera). METHODS: Gene expression patterns and flight muscle development were analyzed using qPCR and TEM, while juvenile hormone (JH) titers were quantified by HPLC-MS/MS. RNAi was applied for gene knockdown. Small RNA-seq was screened for virus-derived small interfering RNAs (vsiRNAs). Subsequently, the interaction between vsiRNAs and target gene was determined using northern blotting, RNA dot blotting, fusion protein construction, RIP-qPCR, RNA pull down, Western blot and Polysome profiling analysis. The regulatory effect was verified by injecting vsiRNA mimic or inhibitor. RESULTS: The infection of SRBSDV induces long-winged morphs and reduces the fertility of WBPH by inhibiting JH biosynthesis. Knocking down the methyl farnesoate epoxidase (MFE) reduces JH titer in WBPH and causes symptoms similar to those of SRBSDV infection. SRBSDV-derived siRNAs repress the translation of MFE by binding to the 5'UTR of MFE. Injecting vsiRNA mimics or inhibitors can promote or counteract the production of SRBSDV infection phenotypes. Our results suggest that SRBSDV inhibits the translation of MFE through vsiRNA, thereby reducing the JH titer of WBPH to regulate the wing dimorphism and reproductive development of WBPH. CONCLUSION: These research results have clarified the molecular mechanism by which SRBSDV regulates the wing dimorphism and reproductive development in WBPHs and provide new evidence for the regulation of vector insects by vsiRNAs.