Odorant-Binding Proteins Contribute to the Defense of the Red Flour Beetle, Tribolium castaneum, Against Essential Oil of Artemisia vulgaris.

Yuan-chen Zhang,Jing-shun Wang,Bin Li,Shuang Xue,Shan-shan Gao,Kun-peng Zhang

doi:10.3389/fphys.2020.00819

Yuan-chen Zhang, Jing-shun Wang + Show 4 more

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https://doi.org/10.3389/fphys.2020.00819

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Abstract

The function of odorant-binding proteins (OBPs) in insect chemodetection has been extensively studied. However, the role of OBPs in the defense of insects against exogenous toxic substances remains elusive. The red flour beetle, Tribolium castaneum, a major pest of stored grains, causes serious economic losses for the agricultural grain and food processing industries. Here, biochemical analysis showed that essential oil (EO) from Artemisia vulgaris, a traditional Chinese medicine, has a strong contact killing effect against larvae of the red flour beetle. Furthermore, one OBP gene, TcOBPC11, was significantly induced after exposure to EO. RNA interference (RNAi) against TcOBPC11 led to higher mortality compared with the controls after EO treatment, suggesting that this OBP gene is associated with defense of the beetle against EO and leads to a decrease in sensitivity to the EO. Tissue expression profiling showed that expression of TcOBPC11 was higher in the fat body, Malpighian tubule, and hemolymph than in other larval tissues, and was mainly expressed in epidermis, fat body, and antennae from the early adult. The developmental expression profile revealed that expression of TcOBPC11 was higher in late larval stages and adult stages than in other developmental stages. These data indicate that TcOBPC11 may be involved in sequestration of exogenous toxicants in the larvae of T. castaneum. Our results provide a theoretical basis for the degradation mechanism of exogenous toxicants and identify potential novel targets for controlling the beetle.

Highlights

Insects have evolved a sensitive olfactory system to detect diverse odor molecules in their habitation environment
There were significant differences in the mortality of larvae of T. castaneum exposed to different concentrations of essential oil (EO)-AV when reared for the same length of time (Figure 1 and Table 2)
Mortality of T. castaneum larvae significantly increased following the extension of rearing time after exposure to essential oil from A. vulgaris (EO-AV) at concentrations of 10, 15, and 20% (10%: x2 = 24.366, df = 5, P < 0.001; 15%: x2 = 20.875, df = 5, P < 0.001; 20%: x2 = 16.071, df = 5, P = 0.007), but there was no significant effect at concentrations of 0, 2.5, and 5% (0%: x2 = 2.231, df = 5, P = 0.816; 2.5%: x2 = 3.295, df = 5, P = 0.655; 5%: x2 = 6.364, df = 5, P = 0.272)

Summary

Introduction

Insects have evolved a sensitive olfactory system to detect diverse odor molecules in their habitation environment. Insects are able to carry out various physiological and reproductive activities (Pelosi et al, 2018; Yan et al, 2020). Bound with some proteins in the sensillum lymph, are transported to odorant receptors across the sensillar lymph, and activate a series of signaling pathways (Pelosi et al, 2006; Leal, 2013). Proteins that bind odor chemicals include odorant binding proteins (OBPs) and chemosensory proteins (CSPs). Interactions between odorants and OBPs likely trigger the signal transduction process of odorant recognition in insects (Leal et al, 2005; Smith, 2007; Rong et al, 2015).

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