Zhongxiang Sun, Yibin Lin, Rumeng Wang, Qilin Li, Qi Shi,Scott R. Baerson, Li Chen, Rensen Zeng and Yuanyuan Song
Co-evolution of complex plant-insect interactions plays a vital role in structuring terrestrial ecosystems. Volatile chemicals emitted by plants play key roles in signaling between plants and other organisms. Upon herbivore attack, plants increase emission of herbivore-induced plant volatiles (HIPVs) that protect plants by eliciting both direct defenses against herbivores and indirect defenses by attracting natural enemies such as parasites and predators. However, whether herbivorous insects, in particular insect larvae, can develop specialized counter-defenses in response to HIPVs is largely unexplored. In this study, we demonstrate that caterpillars of the tobacco cutworm, one of the most important insect pests of agricultural crops in the Asian tropics, can perceive volatile signals emitted from herbivore-challenged tomato plants. Counter-defense responses elicited by the volatiles include induction of eight genes encoding cuticle proteins, and seven genes encoding cytochrome P450s, an important class of detoxification enzymes. Caterpillars consequently improved their performance on both herbivore-pretreated host plants and when fed diets containing a toxin that interferes with the caterpillars’ ability to digest proteins. We also identify three specific volatiles emitted by host plants (α-pinene, ocimene and α-humulene) that are involved in improving larval performance. Given that most terrestrial plants release HIPVs in response to insect herbivory, and insects are frequently exposed to HIPVs, the ability of herbivore insects to utilize these HIPVs to mount counter-defenses could play a pivotal role in their adaptation to the chemical defenses of specific host plant species.