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A genomic amplification affecting a carboxylesterase gene cluster confers organophosphate resistance in the mosquito Aedes aegypti: From genomic characterization to high‐throughput field detection

By altering gene expression and creating paralogs, genomic amplifications represent a key component of short‐term adaptive processes. In insects, the use of insecticides can select gene amplifications causing an increased expression of detoxification enzymes, supporting the usefulness of these DNA m...

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Autores principales: Cattel, Julien, Haberkorn, Chloé, Laporte, Fréderic, Gaude, Thierry, Cumer, Tristan, Renaud, Julien, Sutherland, Ian W., Hertz, Jeffrey C., Bonneville, Jean‐Marc, Arnaud, Victor, Fustec, Bénédicte, Boyer, Sébastien, Marcombe, Sébastien, David, Jean‐Philippe
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8061265/
https://www.ncbi.nlm.nih.gov/pubmed/33897817
http://dx.doi.org/10.1111/eva.13177
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author Cattel, Julien
Haberkorn, Chloé
Laporte, Fréderic
Gaude, Thierry
Cumer, Tristan
Renaud, Julien
Sutherland, Ian W.
Hertz, Jeffrey C.
Bonneville, Jean‐Marc
Arnaud, Victor
Fustec, Bénédicte
Boyer, Sébastien
Marcombe, Sébastien
David, Jean‐Philippe
author_facet Cattel, Julien
Haberkorn, Chloé
Laporte, Fréderic
Gaude, Thierry
Cumer, Tristan
Renaud, Julien
Sutherland, Ian W.
Hertz, Jeffrey C.
Bonneville, Jean‐Marc
Arnaud, Victor
Fustec, Bénédicte
Boyer, Sébastien
Marcombe, Sébastien
David, Jean‐Philippe
author_sort Cattel, Julien
collection PubMed
description By altering gene expression and creating paralogs, genomic amplifications represent a key component of short‐term adaptive processes. In insects, the use of insecticides can select gene amplifications causing an increased expression of detoxification enzymes, supporting the usefulness of these DNA markers for monitoring the dynamics of resistance alleles in the field. In this context, the present study aims to characterize a genomic amplification event associated with resistance to organophosphate insecticides in the mosquito Aedes aegypti and to develop a molecular assay to monitor the associated resistance alleles in the field. An experimental evolution experiment using a composite population from Laos supported the association between the over‐transcription of multiple contiguous carboxylesterase genes on chromosome 2 and resistance to multiple organophosphate insecticides. Combining whole genome sequencing and qPCR on specific genes confirmed the presence of a ~100‐Kb amplification spanning at least five carboxylesterase genes at this locus with the co‐existence of multiple structural duplication haplotypes. Field data confirmed their circulation in South‐East Asia and revealed high copy number polymorphism among and within populations suggesting a trade‐off between this resistance mechanism and associated fitness costs. A dual‐color multiplex TaqMan assay allowing the rapid detection and copy number quantification of this amplification event in Ae. aegypti was developed and validated on field populations. The routine use of this novel assay will improve the tracking of resistance alleles in this major arbovirus vector.
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spelling pubmed-80612652021-04-23 A genomic amplification affecting a carboxylesterase gene cluster confers organophosphate resistance in the mosquito Aedes aegypti: From genomic characterization to high‐throughput field detection Cattel, Julien Haberkorn, Chloé Laporte, Fréderic Gaude, Thierry Cumer, Tristan Renaud, Julien Sutherland, Ian W. Hertz, Jeffrey C. Bonneville, Jean‐Marc Arnaud, Victor Fustec, Bénédicte Boyer, Sébastien Marcombe, Sébastien David, Jean‐Philippe Evol Appl Original Articles By altering gene expression and creating paralogs, genomic amplifications represent a key component of short‐term adaptive processes. In insects, the use of insecticides can select gene amplifications causing an increased expression of detoxification enzymes, supporting the usefulness of these DNA markers for monitoring the dynamics of resistance alleles in the field. In this context, the present study aims to characterize a genomic amplification event associated with resistance to organophosphate insecticides in the mosquito Aedes aegypti and to develop a molecular assay to monitor the associated resistance alleles in the field. An experimental evolution experiment using a composite population from Laos supported the association between the over‐transcription of multiple contiguous carboxylesterase genes on chromosome 2 and resistance to multiple organophosphate insecticides. Combining whole genome sequencing and qPCR on specific genes confirmed the presence of a ~100‐Kb amplification spanning at least five carboxylesterase genes at this locus with the co‐existence of multiple structural duplication haplotypes. Field data confirmed their circulation in South‐East Asia and revealed high copy number polymorphism among and within populations suggesting a trade‐off between this resistance mechanism and associated fitness costs. A dual‐color multiplex TaqMan assay allowing the rapid detection and copy number quantification of this amplification event in Ae. aegypti was developed and validated on field populations. The routine use of this novel assay will improve the tracking of resistance alleles in this major arbovirus vector. John Wiley and Sons Inc. 2021-02-16 /pmc/articles/PMC8061265/ /pubmed/33897817 http://dx.doi.org/10.1111/eva.13177 Text en © 2020 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Articles
Cattel, Julien
Haberkorn, Chloé
Laporte, Fréderic
Gaude, Thierry
Cumer, Tristan
Renaud, Julien
Sutherland, Ian W.
Hertz, Jeffrey C.
Bonneville, Jean‐Marc
Arnaud, Victor
Fustec, Bénédicte
Boyer, Sébastien
Marcombe, Sébastien
David, Jean‐Philippe
A genomic amplification affecting a carboxylesterase gene cluster confers organophosphate resistance in the mosquito Aedes aegypti: From genomic characterization to high‐throughput field detection
title A genomic amplification affecting a carboxylesterase gene cluster confers organophosphate resistance in the mosquito Aedes aegypti: From genomic characterization to high‐throughput field detection
title_full A genomic amplification affecting a carboxylesterase gene cluster confers organophosphate resistance in the mosquito Aedes aegypti: From genomic characterization to high‐throughput field detection
title_fullStr A genomic amplification affecting a carboxylesterase gene cluster confers organophosphate resistance in the mosquito Aedes aegypti: From genomic characterization to high‐throughput field detection
title_full_unstemmed A genomic amplification affecting a carboxylesterase gene cluster confers organophosphate resistance in the mosquito Aedes aegypti: From genomic characterization to high‐throughput field detection
title_short A genomic amplification affecting a carboxylesterase gene cluster confers organophosphate resistance in the mosquito Aedes aegypti: From genomic characterization to high‐throughput field detection
title_sort genomic amplification affecting a carboxylesterase gene cluster confers organophosphate resistance in the mosquito aedes aegypti: from genomic characterization to high‐throughput field detection
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8061265/
https://www.ncbi.nlm.nih.gov/pubmed/33897817
http://dx.doi.org/10.1111/eva.13177
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