Foregut prophenoloxidase in phytophagous insects detoxifies plant phenolics

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  As a group of important secondary metabolites,the majority of plant phenolics are toxic to insects.However,wild phytophagous insects can adapt to or tolerate plant phenolics through unknown mechanisms.Here,we use typical phytophagous insects(silkworm Bombyx mori,Helicoverpa armigera and Spodoptera litura)as models to study this mechanism.We show that the silkworm foregut can produce and release prophenoloxidase(PPO)into the lumen and bind mulberry leaf fragments.Similar to in vitro analysis,the activated foregut phenoloxidase(PO)oxidizes plant phenolics(such as tannic acid and gallic acid).Although tannic acid is toxic to most animals,it does not affect silkworm larvae after ingestion since it is catalyzed by foregut PO,but can damage the silkworm if injected directly into the hemocoel.In the normal larva,no obvious melanization is observed in the foregut even if the contents do have PO activity.During melanization,insect PO catalyzes substrates to produce intermediates at different stages.To avoid melanization induced by foregut PO,intermediates are required.H.armigera and S.litura larvae cannot excrete brown and/or melanized feces unless the pure artificial diets are supplemented with alkanility intolerable L-DOPA,which suggests that foregut PO catalyzes phenolics into intermediates without inducing melanization in the foregut and midgut.Intermediates are sequentially transferred to the hindgut with food,where hindgut PO continuously utilizes them as substrates to induce feces melanization.Thus,wild phytophagous insects utilize foregut PPO to detoxify food by catalyzing phenolics into intermediates.
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