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Self-limiting fall armyworm: a new approach in development for sustainable crop protection and resistance management

BACKGROUND: The fall armyworm, Spodoptera frugiperda, is a significant and widespread pest of maize, sorghum, rice, and other economically important crops. Successful management of this caterpillar pest has historically relied upon application of synthetic insecticides and through cultivation of gen...

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Autores principales: Reavey, Catherine E., Walker, Adam S., Joyce, Stephen P., Broom, Lucy, Willse, Alan, Ercit, Kyla, Poletto, Mattia, Barnes, Zoe H., Marubbi, Thea, Troczka, Bartlomiej J., Treanor, David, Beadle, Katherine, Granville, Ben, de Mello, Vanessa, Teal, Joss, Sulston, Edward, Ashton, Anna, Akilan, Luxziyah, Naish, Neil, Stevens, Oliver, Humphreys-Jones, Nerys, Warner, Simon A. J., Spinner, Sian A. M., Rose, Nathan R., Head, Graham, Morrison, Neil I., Matzen, Kelly J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8793274/
https://www.ncbi.nlm.nih.gov/pubmed/35086540
http://dx.doi.org/10.1186/s12896-022-00735-9
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author Reavey, Catherine E.
Walker, Adam S.
Joyce, Stephen P.
Broom, Lucy
Willse, Alan
Ercit, Kyla
Poletto, Mattia
Barnes, Zoe H.
Marubbi, Thea
Troczka, Bartlomiej J.
Treanor, David
Beadle, Katherine
Granville, Ben
de Mello, Vanessa
Teal, Joss
Sulston, Edward
Ashton, Anna
Akilan, Luxziyah
Naish, Neil
Stevens, Oliver
Humphreys-Jones, Nerys
Warner, Simon A. J.
Spinner, Sian A. M.
Rose, Nathan R.
Head, Graham
Morrison, Neil I.
Matzen, Kelly J.
author_facet Reavey, Catherine E.
Walker, Adam S.
Joyce, Stephen P.
Broom, Lucy
Willse, Alan
Ercit, Kyla
Poletto, Mattia
Barnes, Zoe H.
Marubbi, Thea
Troczka, Bartlomiej J.
Treanor, David
Beadle, Katherine
Granville, Ben
de Mello, Vanessa
Teal, Joss
Sulston, Edward
Ashton, Anna
Akilan, Luxziyah
Naish, Neil
Stevens, Oliver
Humphreys-Jones, Nerys
Warner, Simon A. J.
Spinner, Sian A. M.
Rose, Nathan R.
Head, Graham
Morrison, Neil I.
Matzen, Kelly J.
author_sort Reavey, Catherine E.
collection PubMed
description BACKGROUND: The fall armyworm, Spodoptera frugiperda, is a significant and widespread pest of maize, sorghum, rice, and other economically important crops. Successful management of this caterpillar pest has historically relied upon application of synthetic insecticides and through cultivation of genetically engineered crops expressing insecticidal proteins (Bt crops). Fall armyworm has, however, developed resistance to both synthetic insecticides and Bt crops, which risks undermining the benefits delivered by these important crop protection tools. Previous modelling and empirical studies have demonstrated that releases of insecticide- or Bt-susceptible insects genetically modified to express conditional female mortality can both dilute insecticide resistance and suppress pest populations. RESULTS: Here, we describe the first germline transformation of the fall armyworm and the development of a genetically engineered male-selecting self-limiting strain, OX5382G, which exhibits complete female mortality in the absence of an additive in the larval diet. Laboratory experiments showed that males of this strain are competitive against wild-type males for copulations with wild-type females, and that the OX5382G self-limiting transgene declines rapidly to extinction in closed populations following the cessation of OX5382G male releases. Population models simulating the release of OX5382G males in tandem with Bt crops and non-Bt ‘refuge’ crops show that OX5382G releases can suppress fall armyworm populations and delay the spread of resistance to insecticidal proteins. CONCLUSIONS: This article describes the development of self-limiting fall armyworm designed to control this pest by suppressing pest populations, and population models that demonstrate its potential as a highly effective method of managing resistance to Bt crops in pest fall armyworm populations. Our results provide early promise for a potentially valuable future addition to integrated pest management strategies for fall armyworm and other pests for which resistance to existing crop protection measures results in damage to crops and impedes sustainable agriculture. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12896-022-00735-9.
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spelling pubmed-87932742022-02-03 Self-limiting fall armyworm: a new approach in development for sustainable crop protection and resistance management Reavey, Catherine E. Walker, Adam S. Joyce, Stephen P. Broom, Lucy Willse, Alan Ercit, Kyla Poletto, Mattia Barnes, Zoe H. Marubbi, Thea Troczka, Bartlomiej J. Treanor, David Beadle, Katherine Granville, Ben de Mello, Vanessa Teal, Joss Sulston, Edward Ashton, Anna Akilan, Luxziyah Naish, Neil Stevens, Oliver Humphreys-Jones, Nerys Warner, Simon A. J. Spinner, Sian A. M. Rose, Nathan R. Head, Graham Morrison, Neil I. Matzen, Kelly J. BMC Biotechnol Research Article BACKGROUND: The fall armyworm, Spodoptera frugiperda, is a significant and widespread pest of maize, sorghum, rice, and other economically important crops. Successful management of this caterpillar pest has historically relied upon application of synthetic insecticides and through cultivation of genetically engineered crops expressing insecticidal proteins (Bt crops). Fall armyworm has, however, developed resistance to both synthetic insecticides and Bt crops, which risks undermining the benefits delivered by these important crop protection tools. Previous modelling and empirical studies have demonstrated that releases of insecticide- or Bt-susceptible insects genetically modified to express conditional female mortality can both dilute insecticide resistance and suppress pest populations. RESULTS: Here, we describe the first germline transformation of the fall armyworm and the development of a genetically engineered male-selecting self-limiting strain, OX5382G, which exhibits complete female mortality in the absence of an additive in the larval diet. Laboratory experiments showed that males of this strain are competitive against wild-type males for copulations with wild-type females, and that the OX5382G self-limiting transgene declines rapidly to extinction in closed populations following the cessation of OX5382G male releases. Population models simulating the release of OX5382G males in tandem with Bt crops and non-Bt ‘refuge’ crops show that OX5382G releases can suppress fall armyworm populations and delay the spread of resistance to insecticidal proteins. CONCLUSIONS: This article describes the development of self-limiting fall armyworm designed to control this pest by suppressing pest populations, and population models that demonstrate its potential as a highly effective method of managing resistance to Bt crops in pest fall armyworm populations. Our results provide early promise for a potentially valuable future addition to integrated pest management strategies for fall armyworm and other pests for which resistance to existing crop protection measures results in damage to crops and impedes sustainable agriculture. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12896-022-00735-9. BioMed Central 2022-01-27 /pmc/articles/PMC8793274/ /pubmed/35086540 http://dx.doi.org/10.1186/s12896-022-00735-9 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Reavey, Catherine E.
Walker, Adam S.
Joyce, Stephen P.
Broom, Lucy
Willse, Alan
Ercit, Kyla
Poletto, Mattia
Barnes, Zoe H.
Marubbi, Thea
Troczka, Bartlomiej J.
Treanor, David
Beadle, Katherine
Granville, Ben
de Mello, Vanessa
Teal, Joss
Sulston, Edward
Ashton, Anna
Akilan, Luxziyah
Naish, Neil
Stevens, Oliver
Humphreys-Jones, Nerys
Warner, Simon A. J.
Spinner, Sian A. M.
Rose, Nathan R.
Head, Graham
Morrison, Neil I.
Matzen, Kelly J.
Self-limiting fall armyworm: a new approach in development for sustainable crop protection and resistance management
title Self-limiting fall armyworm: a new approach in development for sustainable crop protection and resistance management
title_full Self-limiting fall armyworm: a new approach in development for sustainable crop protection and resistance management
title_fullStr Self-limiting fall armyworm: a new approach in development for sustainable crop protection and resistance management
title_full_unstemmed Self-limiting fall armyworm: a new approach in development for sustainable crop protection and resistance management
title_short Self-limiting fall armyworm: a new approach in development for sustainable crop protection and resistance management
title_sort self-limiting fall armyworm: a new approach in development for sustainable crop protection and resistance management
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8793274/
https://www.ncbi.nlm.nih.gov/pubmed/35086540
http://dx.doi.org/10.1186/s12896-022-00735-9
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