Maize Herbivore-Induced Volatiles Enhance Xenobiotic Detoxification in Larvae of Spodoptera frugiperda and S. litura

The release of herbivore-induced plant volatiles (HIPVs) has been recognized to be an important strategy for plant adaptation to herbivore attack. However, whether these induced volatiles are beneficial to insect herbivores, particularly insect larvae, is largely unknown. We used the two important highly polyphagous lepidopteran pests <i>Spodoptera frugiperda</i> and <i>S. litura</i> to evaluate the benefit on xenobiotic detoxification of larval exposure to HIPVs released by the host plant maize (<i>Zea mays</i>). Larval exposure of the invasive alien species <i>S. frugiperda</i> to maize HIPVs significantly enhanced their tolerance to all three of the well-known defensive compounds 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA), chlorogenic acid, and tannic acid in maize and the two commonly used insecticides methomyl and chlorpyrifos. HIPV exposure also improved the larval tolerance of <i>S. litura</i> third instars to chlorogenic and tannic acids. Furthermore, larval exposure to either maize HIPVs or DIMBOA induced the activities of cytochrome P450 enzymes (P450s), glutathione-s-transferase (GST), and carboxylesterase (CarE) in the midguts and fat bodies of the two insects, while the induction was significantly higher by the two components together. In addition, the expression of four genes encoding uridine diphosphate (UDP)-glycosyltransferases (<i>UGT33F28</i>, <i>UGT40L8</i>) and P450s (<i>CYP4d8</i>, <i>CYP4V2</i>) showed similar induction patterns in <i>S. frugiperda.</i> Cis-3-hexen-1-ol, an important component in maize HIPVs, also showed the same functions as maize HIPVs, and its exposure increased larval xenobiotic tolerance and induced the detoxification enzymes and gene expression. Our findings demonstrate that HIPVs released by the pest-infested host plants are conductive to the xenobiotic tolerance of lepidopteran insect larvae. Hijacking the host plant HIPVs is an important strategy of the invasive alien polyphagous lepidopteran pest to counter-defend against the host plant's chemical defense.