Plant defense metabolites influence the interaction between an insect herbivore and an entomovirus

Abstract

The tri-trophic interaction of plants, insect herbivores, and entomoviruses is an important topic in ecology and pest control. The susceptibility of insect herbivores to entomoviruses (e.g., nucleopolyhedroviruses) is influenced by host plants; however, the role of plant secondary metabolites in determining such susceptibility is poorly understood. Metabolomic analyses of Brassica oleracea, Glycine max, and Ipomoea aquatica plants, which differ in how they affect the susceptibility of Spodoptera exigua to nucleopolyhedroviruses among 14 plants, suggested that the plant secondary metabolites genistein, kaempferol, quercitrin, and coumarin play a role in influencing nucleopolyhedroviruses susceptibility. Subsequently, transcriptomic analysis of caterpillars, treated with nucleopolyhedroviruses alone or with one of these four phenolics, identified four genes (CYP340K4, CXE18, GSTe, and GSTe1) that were significantly downregulated by the phenolics. Functional characterization of these genes suggested that their downregulation significantly increased larval sensitivity to nucleopolyhedroviruses and altered aspects of the immune response. Our findings provide new insight into the role of plant defense metabolites in influencing the interactions between insect herbivores and entomopathogens and identify plant secondary metabolites as potential synergists of viral agents for the control of agricultural pests.