Changes in Both Trans- and Cis-Regulatory Elements Mediate Insecticide Resistance in a Lepidopteron Pest, Spodoptera exigua

Authors

Bo Hu, Nanjing Agricultural University, China
He Huang, Nanjing Agricultural University, China
Songzhu Hu, Nanjing Agricultural University, China
Miaomiao Ren, Nanjing Agricultural University, China
Qi Wei, Nanjing Agricultural University, China
Xiangrui Tian, Nanjing Agricultural University, China
Mohammed Esmail Abdalla Elzaki, Fujian Agriculture and Forestry University, China
Chris Bass, University of Exeter, UK
Jianya Su, Nanjing Agricultural University, China
Subba Reddy Palli, University of KentuckyFollow

Abstract

The evolution of insect resistance to insecticides is frequently associated with overexpression of one or more cytochrome P450 enzyme genes. Although overexpression of CYP450 genes is a well-known mechanism of insecticide resistance, the underlying regulatory mechanisms are poorly understood. Here we uncovered the mechanisms of overexpression of the P450 gene, CYP321A8 in a major pest insect, Spodoptera exigua that is resistant to multiple insecticides. CYP321A8 confers resistance to organophosphate (chlorpyrifos) and pyrethroid (cypermethrin and deltamethrin) insecticides in this insect. Constitutive upregulation of transcription factors CncC/Maf are partially responsible for upregulated expression of CYP321A8 in the resistant strain. Reporter gene assays and site-directed mutagenesis analyses demonstrated that CncC/Maf enhanced the expression of CYP321A8 by binding to specific sites in the promoter. Additional cis-regulatory elements resulting from a mutation in the CYP321A8 promoter in the resistant strain facilitates the binding of the orphan nuclear receptor, Knirps, and enhances the promoter activity. These results demonstrate that two independent mechanisms; overexpression of transcription factors and mutations in the promoter region resulting in a new cis-regulatory element that facilitates binding of the orphan nuclear receptor are involved in overexpression of CYP321A8 in insecticide-resistant S. exigua.

Document Type

Article

Publication Date

3-9-2021

Notes/Citation Information

Published in PLOS Genetics, v. 17, issue 3, e1009403.

© 2021 Hu et al.

This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Digital Object Identifier (DOI)

https://doi.org/10.1371/journal.pgen.1009403

Funding Information

The work was funded by the National Natural Science Foundation of China (No.32000333) and China Postdoctoral Science Foundation (2020M671264) to BH. The work was supported by the National Natural Science Foundation of China (No.32072452) and Provincial Key Research and Development Program of Jiangsu (BE2019396) to JS. The project was funded by the European Research Council under the European Union's Horizon 2020 research and innovation program (n° 646625) to CB. The project was supported by National Institute of Food and Agriculture of US Department of Agriculture, HATCH Project 2351177000 and Agriculture and Food Research Initiative Competitive Grant no. 2019-67013-29351 to SRP.

Related Content

All gene accession numbers are available from the Gene Bank (accession number(s) MK327547 and MK327548).

Repository Citation

Hu, Bo; Huang, He; Hu, Songzhu; Ren, Miaomiao; Wei, Qi; Tian, Xiangrui; Esmail Abdalla Elzaki, Mohammed; Bass, Chris; Su, Jianya; and Palli, Subba Reddy, "Changes in Both Trans- and Cis-Regulatory Elements Mediate Insecticide Resistance in a Lepidopteron Pest, Spodoptera exigua" (2021). Entomology Faculty Publications. 213.
https://uknowledge.uky.edu/entomology_facpub/213