Ben‐JNK signaling is required for host mortality during Periplaneta fuliginosa densovirus infection

BACKGROUND Cockroaches are widely acknowledged as significant vectors of pathogenic microorganisms. The Periplaneta fuliginosa densovirus (PfDNV) infects the smoky‐brown cockroach P. fuliginosa and causes host mortality, which identifies the PfDNV as a species‐specific and environmentally friendly biopesticide. However, although the biochemical characterization of PfDNV has been extensively studied, the immune response against PfDNV remains largely unclear. RESULTS Here, we investigated the replication of PfDNV and its associated pathological phenotype in the foregut and hindgut. Consequently, we dissected and performed transcriptome sequencing on the foregut, midgut, and hindgut separately. We revealed the up‐regulation of immune response signaling pathway c‐Jun N‐terminal kinase (JNK) and apoptosis in response to viral infection. Furthermore, knockdown of the JNK upstream gene Ben resulted in a decrease in virus titer and delayed host mortality. CONCLUSION Taken together, our findings provide evidence that the Ben‐JNK signaling plays a crucial role in PfDNV infection, leading to excessive apoptosis in intestinal tissues and ultimately resulting in the death of the host. Our results indicated that the host response to PfDNV fosters viral infection, thereby increasing host lethality. This underscores the potential of PfDNV as a viable, environmentally friendly biopesticide. © 2024 Society of Chemical Industry. Periplaneta fuliginosa densovirus (PfDNV) activates the Ben‐JNK signaling pathway and promotes viral replication. This positive feedback process leads to the death of P. fuliginosa, demonstrating significant potential of PfDNV as a bioinsecticide.