Pathogen infection alters the behavior and physiology of the host to maximize progeny production. Heliothis virescens ascovirus 3h (HvAV-3h) is an insect virus that infects the larvae of various pests belonging to the Noctuidae (Lepidoptera) with typical syndromes of almost ceased feeding behavior. Here, we showed that after infection with HvAV-3h, the content of glucose and trehalose in the hemolymph and fat bodies of Spodoptera exigua decreased. Meanwhile, the content of triglycerides (TAG) in both the hemolymph and fat bodies increased. The increased TAG in fat bodies, which are the preferred tissue for ascovirus infection, may provide an energy source for viral infection or as a storage site for the produced ascoviral virions. Three myristoylation site-containing proteins, namely, 3H-11, 3H-48, and 3H-62, were predicted from the 185 open reading frames of HvAV-3h. After applying IMP-1088, which was used as a myristoylation inhibitor in this study, the deformed virions of HvAV-3h were found to be surrounded by lipid inclusions of fat bodies. These were quite different from those stored in the lipid inclusions of the inhibitor-free S. exigua larval fat bodies. The application of perhexiline, that is, an inhibitor of fatty acid metabolism, shortened the survival time of HvAV-3h infected S. exigua larvae. Meanwhile, the application of IMP-1088 prolonged the survival time of HvAV-3h infected S. exigua larvae. However, both inhibited the viral DNA replication of HvAV-3h. Further, qPCR detection showed that the infection of HvAV-3h minimizes the impact on key genes involved in host lipid metabolism. This could supply sufficient acyl-CoA, acetyl-CoA, and fatty acids for the generation of any lipid modifications. We showed that the ascovirus depends on lipid metabolism and myristoylation of host larvae, broadening our understanding of the interaction between viral replication and assembly and host physiological changes.
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