Dual mutations in the whitefly nicotinic acetylcholine receptor β1 subunit confer target-site resistance to multiple neonicotinoid insecticides.
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 ne...
| Main Authors: | , , , , , , , , , , , , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2024-02-01
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| Series: | PLoS Genetics |
| Online Access: | https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1011163&type=printable |
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| author | 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 Lu Wen Xie Dong Chu Xu-Guo Zhou Ralf Nauen Lian-You Gui Chris Bass Xin Yang You-Jun Zhang |
| author_facet | 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 Lu Wen Xie Dong Chu Xu-Guo Zhou Ralf Nauen Lian-You Gui Chris Bass Xin Yang You-Jun Zhang |
| author_sort | Cheng Yin |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-04-25T00:59:54Z |
| format | Article |
| id | doaj.art-dc4e72d26db840548c1d2cdc83524807 |
| institution | Directory Open Access Journal |
| issn | 1553-7390 1553-7404 |
| language | English |
| last_indexed | 2024-04-25T00:59:54Z |
| publishDate | 2024-02-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Genetics |
| spelling | doaj.art-dc4e72d26db840548c1d2cdc835248072024-03-11T05:31:54ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042024-02-01202e101116310.1371/journal.pgen.1011163Dual mutations in the whitefly nicotinic acetylcholine receptor β1 subunit confer target-site resistance to multiple neonicotinoid insecticides.Cheng YinAndrias O O'ReillyShao-Nan LiuTian-Hua DuPei-Pan GongCheng-Jia ZhangXue-Gao WeiJing YangMing-Jiao HuangBu-Li FuJin-Jin LiangHu XueJin-Yu HuYao JiChao HeHe DuChao WangRong ZhangQi-Mei TanHan-Tang LuWen XieDong ChuXu-Guo ZhouRalf NauenLian-You GuiChris BassXin YangYou-Jun ZhangNeonicotinoid 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.https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1011163&type=printable |
| spellingShingle | 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 Lu Wen Xie Dong Chu Xu-Guo Zhou Ralf Nauen Lian-You Gui Chris Bass Xin Yang You-Jun Zhang Dual mutations in the whitefly nicotinic acetylcholine receptor β1 subunit confer target-site resistance to multiple neonicotinoid insecticides. PLoS Genetics |
| title | Dual mutations in the whitefly nicotinic acetylcholine receptor β1 subunit confer target-site resistance to multiple neonicotinoid insecticides. |
| title_full | Dual mutations in the whitefly nicotinic acetylcholine receptor β1 subunit confer target-site resistance to multiple neonicotinoid insecticides. |
| title_fullStr | Dual mutations in the whitefly nicotinic acetylcholine receptor β1 subunit confer target-site resistance to multiple neonicotinoid insecticides. |
| title_full_unstemmed | Dual mutations in the whitefly nicotinic acetylcholine receptor β1 subunit confer target-site resistance to multiple neonicotinoid insecticides. |
| title_short | Dual mutations in the whitefly nicotinic acetylcholine receptor β1 subunit confer target-site resistance to multiple neonicotinoid insecticides. |
| title_sort | dual mutations in the whitefly nicotinic acetylcholine receptor β1 subunit confer target site resistance to multiple neonicotinoid insecticides |
| url | https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1011163&type=printable |
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