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Title: Olfactory perception of herbivore-induced plant volatiles elicits counter-defenses in larvae of tobacco cutworm, spodoptera litura

Author
item SUN, ZHONGXIANG - Fujian Agriculture And Forest University
item LI, QILIN - Fujian Agriculture And Forest University
item LIN, YIBIN - Fujian Agriculture And Forest University
item SHI, QI - Fujian Agriculture And Forest University
item Baerson, Scott
item XU, CUICUI - Fujian Agriculture And Forest University
item WANG, RUMENG - Fujian Agriculture And Forest University
item CHEN, LI - Chinese Academy Of Sciences
item ZENG, REN-SEN - Fujian Agriculture And Forest University
item SONG, YUANYUAN - Fujian Agriculture And Forest University

Submitted to: Functional Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/20/2020
Publication Date: 2/2/2021
Citation: Sun, Z., Li, Q., Lin, Y., Shi, Q., Baerson, S.R., Xu, C., Wang, R., Chen, L., Zeng, R., Song, Y. 2021. Olfactory perception of herbivore-induced plant volatiles elicits counter-defenses in larvae of tobacco cutworm, spodoptera litura. Functional Ecology. 2021;35:384–397. https://doi.org/10.1111/1365-2435.13716.
DOI: https://doi.org/10.1111/1365-2435.13716

Interpretive Summary: Land plants serve as the primary food source for insect herbivores, which represent one of the most diverse and abundant groups of organisms. In response, plants have evolved a broad range of strategies to defend themselves against insects. For example, plants produce a large diversity of defensive chemicals termed allelochemicals, that exert repellent, antinutritive, or toxic effects on insect herbivores. In response to herbivore attacks, plants also produce mixtures of volatile chemicals, termed HIPVs, which can serve as signals to recruit natural enemies of herbivorous insects. Herbivorous insects have in turn developed various sophisticated strategies to counteract host plant chemical defenses, however relatively little is known concerning the manner in which insect larvae respond to HIPVs. In this work, we examined the response of tobacco cutworm larvae to HIPVs produced from tomato plants. Using a directed airflow apparatus, we investigated the influence of exposure to HIPVs emitted from tobacco cutworm-infested tomato plants on larval growth when feeding on tomato leaves, or an artificial diet supplemented with a digestive enzyme inhibitor. The expression of defensive genes associated with allelochemical resistance in HIPV-exposed larvae were also monitored. The HIPVs emitted from tobacco cutworm-infested tomato plants were identified by chemical analyses, and three of the identified volatile components were shown to increase larval growth. Collectively, these results describe a novel mechanism in which olfactory perception of HIPVs by larvae elicits counter-defenses that reduce the effectiveness of host plant anti-herbivore defenses.

Technical Abstract: Herbivore attack leads to increased emission of herbivore-induced plant volatiles (HIPVs) that protect plants by eliciting direct defenses against herbivores and indirect defenses via attraction of natural enemy parasitoids and predators. However, whether herbivorous insects can develop a specialized counter-defense in response to HIPVs is largely unexplored. Using a directed airflow system, we investigated the influence of HIPVs emitted from tobacco cutworm (Spodoptera litura Fabricius, Lepidoptera: Noctuidae)-infested tomato plants on the performance of larvae fed on tomato plants and trypsin inhibitor-amended synthetic diets, as well as the transcriptional responses of HIPV-exposed larvae at different developmental stages. S. litura larval feeding on tomato plants caused increased emission of HIPVs, including several monoterpene and sesquiterpene compounds. The HIPV-exposed larvae showed significantly increased survival rates and weight gains on both tomato leaves and on an artificial diet supplemented with trypsin inhibitor. The increased larval performance on tomato leaf diets was further confirmed by larval exposure to the terpenes a-pinene, ocimene and a-humulene. Exposure to HIPVs emitted from suppressor of prosystemin-mediated responses8 (spr8) mutant tomato plants, however, did not improve larval performance under the same bioassay conditions. HIPV exposure in S. litura also led to enhanced transcript levels of eight genes encoding cuticle proteins, and nine genes encoding cytochrome P450s. Our studies revealed a novel mechanism by which larval olfactory perception of HIPVs such as a-pinene, ocimene and a-humulene elicits counter-defenses that enhance the ability of S. litura to withstand host plant chemical defenses.