Dual mutations in the whitefly nicotinic Acetylcholine receptor β1 subunit confer Target-site resistance to multiple Neonicotinoid insecticides

Cheng Yin, Andrias O. O'Reilly, Shao Nan Liu, Tian Hua Du, Pei Pan Gong, Cheng Jia Zhang, Xue Gao Wei, Jing Yang, Ming Jiao Huang, Bu Li Fu, Jin Jin Liang, Hu Xue, Jin Yu Hu, Yao Ji, Chao He, He Du, Chao Wang, Rong Zhang, Qi Mei Tan, Han Tang LuWen Xie, Dong Chu, Xu Guo Zhou, Ralf Nauen, Lian You Gui, Chris Bass, Xin Yang, You Jun Zhang

Research output: Contribution to journalArticlepeer-review

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 targetsite 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.

Original languageEnglish (US)
Article numbere1011163
JournalPLoS genetics
Volume20
Issue number2
DOIs
StatePublished - Feb 20 2024
Externally publishedYes

ASJC Scopus subject areas

  • Genetics(clinical)
  • Genetics
  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Cancer Research

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