4.7 Article

Phytochemical Flavone Confers Broad-Spectrum Tolerance to Insecticides in Spodoptera litura by Activating ROS/CncC-Mediated Xenobiotic Detoxification Pathways

期刊

JOURNAL OF AGRICULTURAL AND FOOD CHEMISTRY
卷 69, 期 26, 页码 7429-7445

出版社

AMER CHEMICAL SOC
DOI: 10.1021/acs.jafc.1c02695

关键词

Spodoptera litura; detoxification enzyme; insecticide tolerance; phytochemical; transcriptional regulation

资金

  1. National Natural Science Foundation of China [31601634, 31770474, 31870361, 31971833, U2005208]
  2. Natural Science Foundation of Fujian Province [2020J02030]

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The study revealed that pre-exposure to the flavonoid phytochemical flavone enhances larval tolerance to multiple synthetic insecticides and activates detoxification enzyme activities through the ROS/CncC pathway. The findings suggest a key role of the ROS/CncC pathway in driving detoxification gene expression responsible for insecticide tolerance after exposure to flavone.
Tolerance to chemical insecticides can be driven by the necessity of herbivorous insects to defend against host plant-produced phytochemicals. However, how the phytochemicals are sensed and further transduced into a defense response associated with insecticide tolerance is poorly understood. Herein, we show that pre-exposure to flavone, a flavonoid phytochemical, effectively enhanced larval tolerance to multiple synthetic insecticides and elevated detoxification enzyme activities in Spodoptera litura. RNASeq analysis revealed that flavone induced a spectrum of genes spanning phase I and II detoxification enzyme families, as well as two transcription factors Cap n collar isoform C (CncC) and its partner small muscle aponeurosis fibromatosis (MafK). Knocking down of CncC by RNA interference suppressed flavone-induced detoxification gene expression and rendered the larvae more sensitive to the insecticides. Flavone exposure elicited a reactive oxygen species (ROS) burst, while scavenging of ROS inhibited CncC-mediated detoxification gene expression and suppressed flavone-induced detoxification enzyme activation. Metabolome analysis showed that the ingested flavone was mainly converted into three flavonoid metabolites, and only 3-hydroxyflavone was found to affect the ROS/CncC pathway-mediated metabolic detoxification. These results indicate that the ROS/CncC pathway is an important route driving detoxification gene expression responsible for insecticide tolerance after exposure to the phytochemical flavone.

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