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Dual mutations in the whitefly nicotinic acetylcholine receptor β1 subunit confer target-site resistance to multiple neonicotinoid insecticides

Yin, C, O'Reilly, AO, Liu, S-N, Du, T-H, Gong, P-P, Zhang, C-J, Wei, X-G, Yang, J, Huang, M-J, Fu, B-L, Liang, J-J, Xue, H, Hu, J-Y, Ji, Y, He, C, Du, H, Wang, C, Zhang, R, Tan, Q-M, Lu, H-T , Xie, W, Chu, D, Zhou, X-G, Nauen, R, Gui, L-Y, Bass, C, Yang, X and Zhang, Y-J (2024) Dual mutations in the whitefly nicotinic acetylcholine receptor β1 subunit confer target-site resistance to multiple neonicotinoid insecticides. PLoS Genetics, 20 (2). e1011163. ISSN 1553-7404

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Abstract

Neonicotinoid insecticides, which target insect nicotinic acetylcholine receptors (nAChRs), have been widely and intensively used to control the whitefly, Bemisia tabaci, a highly damaging, globally distributed, crop pest. This has inevitably led to the emergence of populations with resistance to neonicotinoids. However, to date, there have been no reports of target-site resistance involving mutation of B. tabaci nAChR genes. Here we characterize the nAChR subunit gene family of B. tabaci and identify dual mutations (A58T&R79E) in one of these genes (BTβ1) that confer resistance to multiple neonicotinoids. Transgenic D. melanogaster, where the native nAChR Dβ1 was replaced with BTβ1A58T&R79E, were significantly more resistant to neonicotinoids than flies where Dβ1 were replaced with the wildtype BTβ1 sequence, demonstrating the causal role of the mutations in resistance. The two mutations identified in this study replace two amino acids that are highly conserved in >200 insect species. Three-dimensional modelling suggests a molecular mechanism for this resistance, whereby A58T forms a hydrogen bond with the R79E side chain, which positions its negatively-charged carboxylate group to electrostatically repulse a neonicotinoid at the orthosteric site. Together these findings describe the first case of target-site resistance to neonicotinoids in B. tabaci and provide insight into the molecular determinants of neonicotinoid binding and selectivity.

Item Type: Article
Uncontrolled Keywords: 0604 Genetics; Developmental Biology
Subjects: G Geography. Anthropology. Recreation > GE Environmental Sciences
Q Science > QH Natural history > QH301 Biology
Q Science > QH Natural history > QH426 Genetics
Divisions: Biological & Environmental Sciences (from Sep 19)
Publisher: Public Library of Science
SWORD Depositor: A Symplectic
Date Deposited: 26 Feb 2024 13:54
Last Modified: 04 Mar 2024 12:45
DOI or ID number: 10.1371/journal.pgen.1011163
Editors: Copenhaver, GP
URI: https://researchonline.ljmu.ac.uk/id/eprint/22687
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