Ascovirus suppresses feeding and growth in Spodoptera litura larvae by targeting the neuropeptide F

Abstract

Ascoviruses, a family of large, double-stranded circular DNA viruses, exhibit high host specificity and pathogenicity, suggesting their significant potential in biocontrol. A hallmark characteristic of ascovirus infection in larvae is reduced feeding and retarded growth. However, the mechanisms by which ascoviruses regulate these effects remain largely unknown. Given their crucial role in regulating larval feeding, insect neuropeptides have attracted our attention in the context of ascovirus infection. During HvAV-3h infection in S. litura, the expression levels of neuropeptide F (NPF), including NPF1 and NPF2, which are integral to feeding regulation, were significantly reduced. HvAV-3h infection impaired NPF regulation in larvae, leading to reduced food intake and larval weight gain across different physiological states. Concurrently, significant up-regulation of the NPF receptor (NPFR) was observed in the head tissue. The observed dysregulation of the NPF/NPFR signaling pathway was associated with elevated juvenile hormone (JH) titers. In contrast, the expression levels of short neuropeptide F (sNPF) and the molting hormone ecdysone remained unchanged. Moreover, histopathological analysis of the midgut revealed no epithelial cell damage. Furthermore, RNA interference of NPF1 or NPF2 significantly increased the expression of NPFR and juvenile hormone acid O-methyltransferase (JHAMT), and tended to further reduce food intake and weight gain, which consequently increased the mortality during HvAV-3h infection. HvAV-3h infection disrupts the NPF/NPFR signaling pathway in S. litura larvae, subsequently elevating JH titers, ultimately leading to reduced food intake and larval weight gain. This study enhances our understanding of the interaction between HvAV-3h and its host, and provides a theoretical basis for the development of innovative pest management strategies.