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Rotation of Multiple Single-Gene Transgenic Crops Did Not Slow the Evolution of Resistance to Cry1F or Cry1Ie in Ostrinia furnacalis

SIMPLE SUMMARY: Delaying or preventing the evolution of resistance to Bacillus thuringiensis (Bt) toxins produced by transgenic crops in insect pests is a major challenge for agriculture. A simulation model suggested that the rotation of different single-gene crops planted in subsequent seasons has...

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Autores principales: Wang, Yueqin, Quan, Yudong, Wang, Zhenying, He, Kanglai
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9866647/
https://www.ncbi.nlm.nih.gov/pubmed/36662002
http://dx.doi.org/10.3390/insects14010074
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author Wang, Yueqin
Quan, Yudong
Wang, Zhenying
He, Kanglai
author_facet Wang, Yueqin
Quan, Yudong
Wang, Zhenying
He, Kanglai
author_sort Wang, Yueqin
collection PubMed
description SIMPLE SUMMARY: Delaying or preventing the evolution of resistance to Bacillus thuringiensis (Bt) toxins produced by transgenic crops in insect pests is a major challenge for agriculture. A simulation model suggested that the rotation of different single-gene crops planted in subsequent seasons has the potential to delay resistance. To test this prediction, we set out laboratory selection experiments under the alternation of multi-toxins by mixing individual toxins (Cry1Ab, Cry1F, and Cry1Ie) in an artificial diet to emulate single-gene Bt maize plants. Two (Cry1Ab-Cry1F, Cry1Ab-Cry1Ie) or three (Cry1Ab–Cry1F–Cry1Ie) toxin alternation regimes were tested to imitate two or three single-gene crops in a rotation fashion. The species tested was the Asian corn borer, Ostrinia furnacalis (Guenée), the most economically important species of maize pest in Asia. The present study suggested that rotation of multiple toxins did not slow the evolution of resistance to Cry1F or Cry1Ie. Data generated from the study will assist in the development of sustainable resistance-management strategies. ABSTRACT: A common strategy for delaying the evolution of resistance to transgenic crops that produce insecticidal proteins from Bacillus thuringiensis is to ensure that insect pests are exposed to multiple toxins with different mechanisms of action (MoAs). This can take the form of planting crops in a rotation pattern when different crops expressing single toxins are available on the market. The efficacy of a rotation strategy is reliant on mathematical models based on biological assumptions. Here, we designed laboratory evolution experiments to test whether Bt-based insecticidal proteins with different MoAs used in rotation could delay resistance from developing in Asian corn borer (ACB), Ostrinia furnacalis. We investigated the proteins Cry1Ab, Cry1F, and Cry1Ie, which are widely utilized for commercial insect control. We found that rotation of multiple toxins did not slow the evolution of resistance to Cry1F or Cry1Ie. Furthermore, the evolution of ACB to the Cry1Ab toxin develops faster when Cry1F or Cry1Ie is present, as compared to Cry1Ab exposure only. Our results suggest that toxins used in a rotation fashion do not work as an effective strategy in delaying ACB resistance evolution to Cry toxins over one-toxin exposure. Our result highlights the need to better understand the biological factors leading to insecticidal protein resistance and to develop IRM strategies against target insects.
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spelling pubmed-98666472023-01-22 Rotation of Multiple Single-Gene Transgenic Crops Did Not Slow the Evolution of Resistance to Cry1F or Cry1Ie in Ostrinia furnacalis Wang, Yueqin Quan, Yudong Wang, Zhenying He, Kanglai Insects Article SIMPLE SUMMARY: Delaying or preventing the evolution of resistance to Bacillus thuringiensis (Bt) toxins produced by transgenic crops in insect pests is a major challenge for agriculture. A simulation model suggested that the rotation of different single-gene crops planted in subsequent seasons has the potential to delay resistance. To test this prediction, we set out laboratory selection experiments under the alternation of multi-toxins by mixing individual toxins (Cry1Ab, Cry1F, and Cry1Ie) in an artificial diet to emulate single-gene Bt maize plants. Two (Cry1Ab-Cry1F, Cry1Ab-Cry1Ie) or three (Cry1Ab–Cry1F–Cry1Ie) toxin alternation regimes were tested to imitate two or three single-gene crops in a rotation fashion. The species tested was the Asian corn borer, Ostrinia furnacalis (Guenée), the most economically important species of maize pest in Asia. The present study suggested that rotation of multiple toxins did not slow the evolution of resistance to Cry1F or Cry1Ie. Data generated from the study will assist in the development of sustainable resistance-management strategies. ABSTRACT: A common strategy for delaying the evolution of resistance to transgenic crops that produce insecticidal proteins from Bacillus thuringiensis is to ensure that insect pests are exposed to multiple toxins with different mechanisms of action (MoAs). This can take the form of planting crops in a rotation pattern when different crops expressing single toxins are available on the market. The efficacy of a rotation strategy is reliant on mathematical models based on biological assumptions. Here, we designed laboratory evolution experiments to test whether Bt-based insecticidal proteins with different MoAs used in rotation could delay resistance from developing in Asian corn borer (ACB), Ostrinia furnacalis. We investigated the proteins Cry1Ab, Cry1F, and Cry1Ie, which are widely utilized for commercial insect control. We found that rotation of multiple toxins did not slow the evolution of resistance to Cry1F or Cry1Ie. Furthermore, the evolution of ACB to the Cry1Ab toxin develops faster when Cry1F or Cry1Ie is present, as compared to Cry1Ab exposure only. Our results suggest that toxins used in a rotation fashion do not work as an effective strategy in delaying ACB resistance evolution to Cry toxins over one-toxin exposure. Our result highlights the need to better understand the biological factors leading to insecticidal protein resistance and to develop IRM strategies against target insects. MDPI 2023-01-12 /pmc/articles/PMC9866647/ /pubmed/36662002 http://dx.doi.org/10.3390/insects14010074 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Wang, Yueqin
Quan, Yudong
Wang, Zhenying
He, Kanglai
Rotation of Multiple Single-Gene Transgenic Crops Did Not Slow the Evolution of Resistance to Cry1F or Cry1Ie in Ostrinia furnacalis
title Rotation of Multiple Single-Gene Transgenic Crops Did Not Slow the Evolution of Resistance to Cry1F or Cry1Ie in Ostrinia furnacalis
title_full Rotation of Multiple Single-Gene Transgenic Crops Did Not Slow the Evolution of Resistance to Cry1F or Cry1Ie in Ostrinia furnacalis
title_fullStr Rotation of Multiple Single-Gene Transgenic Crops Did Not Slow the Evolution of Resistance to Cry1F or Cry1Ie in Ostrinia furnacalis
title_full_unstemmed Rotation of Multiple Single-Gene Transgenic Crops Did Not Slow the Evolution of Resistance to Cry1F or Cry1Ie in Ostrinia furnacalis
title_short Rotation of Multiple Single-Gene Transgenic Crops Did Not Slow the Evolution of Resistance to Cry1F or Cry1Ie in Ostrinia furnacalis
title_sort rotation of multiple single-gene transgenic crops did not slow the evolution of resistance to cry1f or cry1ie in ostrinia furnacalis
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9866647/
https://www.ncbi.nlm.nih.gov/pubmed/36662002
http://dx.doi.org/10.3390/insects14010074
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