Clonal plants are interconnected to form clonal plant networks with physiological integration, enabling the reassignment as well as sharing of resources among the members. The systemic induction of antiherbivore resistance via clonal integration may frequently operate in the networks. Here, we used an important food crop rice (Oryza sativa), and its destructive pest rice leaffolder (LF; Cnaphalocrocis medinalis) as a model to examine defense communication between the main stem and clonal tillers. LF infestation and MeJA pretreatment on the main stem for two days reduced the weight gain of LF larvae fed on the corresponding primary tillers by 44.5% and 29.0%, respectively. LF infestation and MeJA pretreatment on the main stem also enhanced antiherbivore defense responses in primary tillers: increased levels of a trypsin protease inhibitor, putative defensive enzymes, and jasmonic acid (JA), a key signaling compound involved in antiherbivore induced defenses; strong induction of genes encoding JA biosynthesis and perception; and rapid activation of JA pathway. However, in a JA perception OsCOI RNAi line, LF infestation on main stem showed no or minor effects on antiherbivore defense responses in primary tillers. Our work demonstrates that systemic antiherbivore defense operate in the clonal network of rice plants and JA signaling plays a crucial role in mediating defense communication between main stem and tillers in rice plants. Our findings provide a theoretical basis for the ecological control of pests by using the systemic resistance of cloned plants themselves.

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 Spodoptera frugiperda and S. litura to evaluate the benefit on xenobiotic detoxification of larval exposure to HIPVs released by the host plant maize (Zea mays). Larval exposure of the invasive alien species S. frugiperda 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 S. litura 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 (UGT33F28, UGT40L8) and P450s (CYP4d8, CYP4V2) showed similar induction patterns in S. frugiperda. 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.

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 two important highly polyphagous lepidopteran pests Spodoptera frugiperda and S. litura to evaluate their benefit for xenobiotic detoxification from larval exposure to HIPVs released by the host plant maize (Zea mays). Larval exposure of the invasive alien species S. frugiperda to maize HIPVs significantly enhanced their tolerance to all three well-known defensive compounds 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA), chlorogenic and tannic acids in maize, and two commonly used insecticides methomyl and chlorpyrifos. The HIPVs exposure also improved larval tolerance of S. litura third instars to chlorogenic and tannic acids. Furthermore, larval exposure to either maize HIPVs or DIMBOA induced 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 two components together. In addition, expression of four genes encoding uridine diphosphate (UDP)-glycosyltransferases (UGT33F28, UGT40L8) and P450s (CYP4d8, CYP4V2) showed similar induction pattern in S. frugiperda. Cis-3-hexen-1-ol, an important component in maize HIPVs also showed the same functions as maize HIPVs, its exposure increased larval xenobiotic tolerance and induced detoxification enzymes and genes. Our findings demonstrate that HIPVs released by the pest-infested host plants are conductive to xenobiotic tolerance of lepidopteran insect larvae. Hijacking the host plant HIPVs is an important strategy of the invasive alien polyphagous lepidopteran pest to counter-defense host plant chemical defense.