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BACKGROUND Spodoptera frugiperda is one of the significant migratory pests in the Global Alert issued by the Food and Agriculture Organization of the United Nations. As an insect‐specific microbial insecticide, baculovirus has been used to control various pests. MicroRNA‐34‐5p (miR‐34‐5p) is involved in regulating growth, reproduction and innate immunity to pathogens in insects, playing an essential role in host–virus interactions. In this study, we explored the critical function of miR‐34‐5p encoded by S. frugiperda in the anti‐Autographa californica multiple nucleopolyhedrovirus (AcMNPV), providing a reference for the design of a miR‐34‐5p target biopesticide against S. frugiperda and a theoretical basis for the wide application of microRNAs (miRNAs) in green pest control technology. RESULTS We focused on miR‐34‐5p identified as downregulated in Sf9 cells and S. frugiperda larvae infected by AcMNPV. The regulatory function of miR‐34‐5p in AcMNPV–S. frugiperda interactions was studied by transfecting synthetic mimics and inhibitors, and constructing recombinant bacmids with miR‐34‐5p overexpression. miR‐34‐5p inhibited the production of infectious budded virions at the cellular and insect levels, inhibited the replication of the viral DNA and glucose metabolism, and increased the transcription of the antimicrobial peptide gloverin. Furthermore, the virus genes odv‐e66, ac78 and ie2 were shown to be direct targets. CONCLUSION We systematically revealed the mechanism by which miR‐34‐5p is involved in the insect antiviral process. miR‐34‐5p inhibited the replication and infection of AcMNPV by directly targeting AcMNPV genes, especially ac78 and ie2. Our study provides a new direction and thinking for the prevention and green control of lepidopteran pests. © 2022 Society of Chemical Industry.

Background: The immune system of insects exerts fundamentally different antiviral mechanisms than mammals. MicroRNAs (miRNAs) play vital roles in developing insect antiviral immunity. MiRNAs expression profiles of insects changed significantly during baculovirus infection. Methods: Differential expression profiles of miRNAs in Spodoptera frugiperda were monitored by next-generation sequencing (NGS) and RT-qPCR during Autographa californica multiple nucleopolyhedrovirus (AcMNPV) infection. The transcription levels of genes were detected by RT-qPCR. The 50% tissue culture infective dose (TCID 50 ) endpoint dilution assay was used to determine the proliferation of progeny virus. Results: NGS revealed that 49 miRNAs were differentially expressed in Sf9 cells, and 10 of them were significantly up-or down-regulated. Though RT-qPCR analysis, we observed the similar trends for the expression patterns of significantly differentially expressed miRNAs from NGS. Moreover, the transcription levels of core genes, Exportin5, Dicer1, and Argonaute1, in miRNA biogenesis pathways were significantly increased after AcMNPV infection. For five selected miRNAs, miR-34-5p could regulate the proliferation of baculovirus progeny virus and energy metabolism. Conclusion: The miRNAs biogenesis pathway in Sf9 cells plays an important role and may be stimulated to resist AcMNPV infection. This work provides evidence for the molecular mechanism of baculovirus-insect interaction and offers novel ideas and directions for green pest control technology.