Unveiling the molecular mechanisms underlying the effects of beet curly top virus on beet leafhopper performance

Beet curly top virus (BCTV) is a major threat to sugar beets in the western US, spread exclusively by beet leafhoppers (BLHs, Circulifer tenellus). Despite progress in understanding virus-insect interactions, our understanding of the molecular interactions between BCTV and BLH remained unclear due to the limited omics resources for BLH. This study unveils the significant impact of BCTV on both the performance and transcriptome response of BLHs. Viruliferous BLHs had higher fecundity than non-viruliferous counterparts, which was evident by up-regulation of differentially expressed transcripts (DETs) associated with development, viability, and fertility of germline and embryos in viruliferous insects. Conversely, most DETs associated with muscle movement and locomotor activities were down-regulated in viruliferous insects, implying potential behavioral modifications by BCTV. Additionally, a great proportion of DETs related to innate immunity and detoxification was up-regulated in viruliferous insects. Viral infection also induced notable alterations in primary metabolisms, including energy metabolism namely glucosidases, lipid digestion and transport, and protein degradation, along with other cellular functions, particularly in chromatin remodeling and DNA repair. Our RNAi-mediated gene silencing in BLHs showed a significant silencing of gustavus and pumilio homolog 3 genes, paving the way for future functional analysis. This study represents the first comprehensive transcriptome analysis for BLH and confirms the feasibility of RNAi in BLHs for future functional analysis. Overall, the presented findings offer new understanding of BCTV's multifaceted effects on BLHs, providing a foundation for exploring the complex virus-vector relationship and developing potential management strategies for curly top disease.