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Diamide insecticide resistance in transgenic Drosophila and Sf9-cells expressing a full-length diamondback moth ryanodine receptor carrying an I4790M mutation

Ewan Richardson, Rafael A Homem, Bartlomiej J Troczka, Christopher George Orcid Logo, Ulrich Ebbinghaus‐Kintscher, Martin S Williamson, Ralf Nauen Orcid Logo, TG Emyr Davies Orcid Logo

Pest Management Science, Volume: 78, Issue: 3, Pages: 869 - 880

Swansea University Author: Christopher George Orcid Logo

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DOI (Published version): 10.1002/ps.6730

Abstract

BACKGROUNDResistance to diamide insecticides in Lepidoptera is known to be caused primarily by amino acid changes on the ryanodine receptor (RyR). Recently, two new target site mutations, G4946V and I4790M, have emerged in populations of diamondback moth, Plutella xylostella, as well as in other lep...

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Published in: Pest Management Science
ISSN: 1526-498X 1526-4998
Published: Wiley 2022
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URI: https://cronfa.swan.ac.uk/Record/cronfa58748
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Recently, two new target site mutations, G4946V and I4790M, have emerged in populations of diamondback moth, Plutella xylostella, as well as in other lepidopteran species, and both mutations have been shown empirically to decrease diamide efficacy. Here, we quantify the impact of the I4790M mutation on diamide activation of the receptor, as compared to alterations at the G4946 locus.RESULTSI4790M when introduced into P. xylostella RyR expressed in an insect-derived Sf9 cell line was found to mediate just a ten-fold reduction in chlorantraniliprole efficacy (compared to 104- and 146-fold reductions for the G4946E and G4946V variants, respectively), whilst in the field its presence is associated with a &#x2265;150-fold reduction. I4790M-mediated resistance to flubendiamide was estimated to be &gt;24-fold. When the entire coding sequence of P. xylostella RyR was integrated into Drosophila melanogaster, the I4790M variant conferred ~4.4-fold resistance to chlorantraniliprole and 22-fold resistance to flubendiamide in the 3rd instar larvae, confirming that it imparts only a moderate level of resistance to diamide insecticides. Although the I4790M substitution appears to bear no fitness costs in terms of the flies' reproductive capacity, when assessed in a noncompetitive environment, it does, however, have potentially major impacts on mobility at both the larval and adult stages.CONCLUSIONSI4790M imparts only a moderate level of resistance to diamide insecticides and potentially confers significant fitness costs to the insect.</abstract><type>Journal Article</type><journal>Pest Management Science</journal><volume>78</volume><journalNumber>3</journalNumber><paginationStart>869</paginationStart><paginationEnd>880</paginationEnd><publisher>Wiley</publisher><placeOfPublication/><isbnPrint/><isbnElectronic/><issnPrint>1526-498X</issnPrint><issnElectronic>1526-4998</issnElectronic><keywords>diamide insecticides; chlorantraniliprole; flubendiamide; Plutella xylostella; diamondback moth; insecticide resistance</keywords><publishedDay>1</publishedDay><publishedMonth>3</publishedMonth><publishedYear>2022</publishedYear><publishedDate>2022-03-01</publishedDate><doi>10.1002/ps.6730</doi><url/><notes/><college>COLLEGE NANME</college><department>Biomedical Sciences</department><CollegeCode>COLLEGE CODE</CollegeCode><DepartmentCode>BMS</DepartmentCode><institution>Swansea University</institution><apcterm>Another institution paid the OA fee</apcterm><funders>Biotechnology and Biological Sciences Research Council. Grant Number: BB/N504075/1; Bayer CropScience</funders><lastEdited>2022-03-16T12:26:14.9612185</lastEdited><Created>2021-11-22T14:35:41.7398317</Created><path><level id="1">Faculty of Medicine, Health and Life Sciences</level><level id="2">Swansea University Medical School - Medicine</level></path><authors><author><firstname>Ewan</firstname><surname>Richardson</surname><order>1</order></author><author><firstname>Rafael A</firstname><surname>Homem</surname><order>2</order></author><author><firstname>Bartlomiej J</firstname><surname>Troczka</surname><order>3</order></author><author><firstname>Christopher</firstname><surname>George</surname><orcid>0000-0001-9852-1135</orcid><order>4</order></author><author><firstname>Ulrich</firstname><surname>Ebbinghaus&#x2010;Kintscher</surname><order>5</order></author><author><firstname>Martin S</firstname><surname>Williamson</surname><order>6</order></author><author><firstname>Ralf</firstname><surname>Nauen</surname><orcid>0000-0002-7525-8589</orcid><order>7</order></author><author><firstname>TG Emyr</firstname><surname>Davies</surname><orcid>0000-0002-9452-2947</orcid><order>8</order></author></authors><documents><document><filename>58748__21784__4e0f2bf7e2f645b2b1d2284dbe083b0b.pdf</filename><originalFilename>58748.pdf</originalFilename><uploaded>2021-12-03T17:30:06.6684013</uploaded><type>Output</type><contentLength>1279563</contentLength><contentType>application/pdf</contentType><version>Version of Record</version><cronfaStatus>true</cronfaStatus><documentNotes>&#xA9; 2021 The Authors. This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License</documentNotes><copyrightCorrect>true</copyrightCorrect><language>eng</language><licence>http://creativecommons.org/licenses/by-nc/4.0/</licence></document></documents><OutputDurs/></rfc1807>
spelling 2022-03-16T12:26:14.9612185 v2 58748 2021-11-22 Diamide insecticide resistance in transgenic Drosophila and Sf9-cells expressing a full-length diamondback moth ryanodine receptor carrying an I4790M mutation a2e211f7bd379c81e9c393637803a0a0 0000-0001-9852-1135 Christopher George Christopher George true false 2021-11-22 BMS BACKGROUNDResistance to diamide insecticides in Lepidoptera is known to be caused primarily by amino acid changes on the ryanodine receptor (RyR). Recently, two new target site mutations, G4946V and I4790M, have emerged in populations of diamondback moth, Plutella xylostella, as well as in other lepidopteran species, and both mutations have been shown empirically to decrease diamide efficacy. Here, we quantify the impact of the I4790M mutation on diamide activation of the receptor, as compared to alterations at the G4946 locus.RESULTSI4790M when introduced into P. xylostella RyR expressed in an insect-derived Sf9 cell line was found to mediate just a ten-fold reduction in chlorantraniliprole efficacy (compared to 104- and 146-fold reductions for the G4946E and G4946V variants, respectively), whilst in the field its presence is associated with a ≥150-fold reduction. I4790M-mediated resistance to flubendiamide was estimated to be >24-fold. When the entire coding sequence of P. xylostella RyR was integrated into Drosophila melanogaster, the I4790M variant conferred ~4.4-fold resistance to chlorantraniliprole and 22-fold resistance to flubendiamide in the 3rd instar larvae, confirming that it imparts only a moderate level of resistance to diamide insecticides. Although the I4790M substitution appears to bear no fitness costs in terms of the flies' reproductive capacity, when assessed in a noncompetitive environment, it does, however, have potentially major impacts on mobility at both the larval and adult stages.CONCLUSIONSI4790M imparts only a moderate level of resistance to diamide insecticides and potentially confers significant fitness costs to the insect. Journal Article Pest Management Science 78 3 869 880 Wiley 1526-498X 1526-4998 diamide insecticides; chlorantraniliprole; flubendiamide; Plutella xylostella; diamondback moth; insecticide resistance 1 3 2022 2022-03-01 10.1002/ps.6730 COLLEGE NANME Biomedical Sciences COLLEGE CODE BMS Swansea University Another institution paid the OA fee Biotechnology and Biological Sciences Research Council. Grant Number: BB/N504075/1; Bayer CropScience 2022-03-16T12:26:14.9612185 2021-11-22T14:35:41.7398317 Faculty of Medicine, Health and Life Sciences Swansea University Medical School - Medicine Ewan Richardson 1 Rafael A Homem 2 Bartlomiej J Troczka 3 Christopher George 0000-0001-9852-1135 4 Ulrich Ebbinghaus‐Kintscher 5 Martin S Williamson 6 Ralf Nauen 0000-0002-7525-8589 7 TG Emyr Davies 0000-0002-9452-2947 8 58748__21784__4e0f2bf7e2f645b2b1d2284dbe083b0b.pdf 58748.pdf 2021-12-03T17:30:06.6684013 Output 1279563 application/pdf Version of Record true © 2021 The Authors. This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License true eng http://creativecommons.org/licenses/by-nc/4.0/
title Diamide insecticide resistance in transgenic Drosophila and Sf9-cells expressing a full-length diamondback moth ryanodine receptor carrying an I4790M mutation
spellingShingle Diamide insecticide resistance in transgenic Drosophila and Sf9-cells expressing a full-length diamondback moth ryanodine receptor carrying an I4790M mutation
Christopher George
title_short Diamide insecticide resistance in transgenic Drosophila and Sf9-cells expressing a full-length diamondback moth ryanodine receptor carrying an I4790M mutation
title_full Diamide insecticide resistance in transgenic Drosophila and Sf9-cells expressing a full-length diamondback moth ryanodine receptor carrying an I4790M mutation
title_fullStr Diamide insecticide resistance in transgenic Drosophila and Sf9-cells expressing a full-length diamondback moth ryanodine receptor carrying an I4790M mutation
title_full_unstemmed Diamide insecticide resistance in transgenic Drosophila and Sf9-cells expressing a full-length diamondback moth ryanodine receptor carrying an I4790M mutation
title_sort Diamide insecticide resistance in transgenic Drosophila and Sf9-cells expressing a full-length diamondback moth ryanodine receptor carrying an I4790M mutation
author_id_str_mv a2e211f7bd379c81e9c393637803a0a0
author_id_fullname_str_mv a2e211f7bd379c81e9c393637803a0a0_***_Christopher George
author Christopher George
author2 Ewan Richardson
Rafael A Homem
Bartlomiej J Troczka
Christopher George
Ulrich Ebbinghaus‐Kintscher
Martin S Williamson
Ralf Nauen
TG Emyr Davies
format Journal article
container_title Pest Management Science
container_volume 78
container_issue 3
container_start_page 869
publishDate 2022
institution Swansea University
issn 1526-498X
1526-4998
doi_str_mv 10.1002/ps.6730
publisher Wiley
college_str Faculty of Medicine, Health and Life Sciences
hierarchytype
hierarchy_top_id facultyofmedicinehealthandlifesciences
hierarchy_top_title Faculty of Medicine, Health and Life Sciences
hierarchy_parent_id facultyofmedicinehealthandlifesciences
hierarchy_parent_title Faculty of Medicine, Health and Life Sciences
department_str Swansea University Medical School - Medicine{{{_:::_}}}Faculty of Medicine, Health and Life Sciences{{{_:::_}}}Swansea University Medical School - Medicine
document_store_str 1
active_str 0
description BACKGROUNDResistance to diamide insecticides in Lepidoptera is known to be caused primarily by amino acid changes on the ryanodine receptor (RyR). Recently, two new target site mutations, G4946V and I4790M, have emerged in populations of diamondback moth, Plutella xylostella, as well as in other lepidopteran species, and both mutations have been shown empirically to decrease diamide efficacy. Here, we quantify the impact of the I4790M mutation on diamide activation of the receptor, as compared to alterations at the G4946 locus.RESULTSI4790M when introduced into P. xylostella RyR expressed in an insect-derived Sf9 cell line was found to mediate just a ten-fold reduction in chlorantraniliprole efficacy (compared to 104- and 146-fold reductions for the G4946E and G4946V variants, respectively), whilst in the field its presence is associated with a ≥150-fold reduction. I4790M-mediated resistance to flubendiamide was estimated to be >24-fold. When the entire coding sequence of P. xylostella RyR was integrated into Drosophila melanogaster, the I4790M variant conferred ~4.4-fold resistance to chlorantraniliprole and 22-fold resistance to flubendiamide in the 3rd instar larvae, confirming that it imparts only a moderate level of resistance to diamide insecticides. Although the I4790M substitution appears to bear no fitness costs in terms of the flies' reproductive capacity, when assessed in a noncompetitive environment, it does, however, have potentially major impacts on mobility at both the larval and adult stages.CONCLUSIONSI4790M imparts only a moderate level of resistance to diamide insecticides and potentially confers significant fitness costs to the insect.
published_date 2022-03-01T04:15:31Z
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