A dicistrovirus increases pupal mortality in Spodoptera frugiperda by suppressing protease activity and inhibiting larval diet consumption

Sun, M. and Li, T. and Liu, Y. and Wilson, K. and Chen, X. and Graham, R.I. and Yang, X. and Ren, G. and Xu, P. (2024) A dicistrovirus increases pupal mortality in Spodoptera frugiperda by suppressing protease activity and inhibiting larval diet consumption. Journal of Integrative Agriculture, 23 (8). pp. 2723-2734. ISSN 2095-3119

Abstract

Understanding interactions between viruses and their hosts is conducive to enabling better application of viruses as biocontrol agents. Certain viruses carried by parasitic wasps enhance the parasitic efficiency of wasp-larvae by protecting them against the immune system of their Lepidopteran host. However, the relationship between prey pests and viruses found in predatory natural enemies remains unclear. Herein, we report the interaction between Arma chinensis virus-1 (AcV-1), originally isolated from a predatory natural enemy, Arma chinensis (Hemiptera: Pentatomidae), and one of its prey species, Spodoptera frugiperda (Lepidoptera: Noctuidae). The results showed that the AcV-1 virus appeared harmful to the novel host S. frugiperda by inhibiting larval diet consumption and increasing pupal mortality. Meanwhile, sequencing data indicated that the virus altered the gene expression profiles of S. frugiperda. KEGG analysis showed that the proteasome and phagosome pathways related to protein degradation and immune response were significantly enriched. Although the expression levels of digestive enzyme genes did not change significantly, the total protease activity of AcV-1 virus-positive individuals was significantly decreased, suggesting that the virus inhibited diet consumption of S. frugiperda via the down-regulation of digestive enzyme activities. These results indicate that a virus initially isolated in a predatory natural enemy can decrease the fitness of its prey species. The virus was found to impact the host proteasome and phagosome pathways related to protein degradation and immunity, providing a potential mechanism to enhance controlling efficiency.