Differential pathogenicity of heterologous nucleopolyhedroviruses on Spodoptera frugiperda corresponds to modulated expression of immune-response-related genes

Abstract

The fall armyworm Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) is a notorious invasive pest wreaking havoc on various crops globally. Nucleopolyhedroviruses (NPVs) are viral pathogens that specially target lepidopteran pests. However, the homologous virus, Spodoptera frugiperda multiple nucleopolyhedrovirus (SfMNPV), has not been commercialized in China. Therefore, understanding the molecular mechanisms underlying heterologous virus-host interactions can inform the design of virus-based insecticides for controlling S. frugiperda. The pathogenicity of the four heterologous NPVs on S. frugiperda varied greatly. Mamestra brassicae multiple nucleopolyhedrovirus (MbMNPV) exhibited the most potent virulence on larvae and induced the most robust sublethal effects on adults. Spodoptera exigua multiple nucleopolyhedrovirus (SeMNPV) infection was characterized by more moderate pathogenicity, and larvae were relatively resistant to Helicoverpa armigera single nucleopolyhedrovirus (HaSNPV) and Spodoptera litura multiple nucleopolyhedrovirus (SlMNPV). Larval mortality was virus-concentration and larval stage dependent. Specifically, the corrected mortality rate of third instar larvae after treatment with 1 × 10⁶, 1 × 10⁷, and 1 × 10⁸ OBs/mL MbMNPV was 88.9 %, 100.0 %, and 100.0 %, respectively. All four NPVs negatively affected the longevity and fecundity of S. frugiperda adults. Female adults surviving treatment with MbMNPV and SeMNPV were unable to lay eggs. Transcriptomic analysis revealed that MbMNPV infection might suppress the antiviral immune response, and dysregulate biological pathways of S. frugiperda larvae to facilitate systemic infection. However, the overall transcript profiles remain unchanged after SlMNPV infection. The results reinforce the potential of NPVs, specifically MbMNPV, as potent biocontrol agents for S. frugiperda. These findings yield valuable insights into the complex arms race between S. frugiperda and NPVs that may advance the development of virus-based strategies to mitigate the destructive impact of this pest.