Tandem duplication of a genomic region encoding glutathione S-transferase epsilon-2 and -4 genes in DDT-resistant Anopheles stephensi strain from India

Abstract The glutathione S-transferases (GST) genes are a multigene family of enzymes involved in the metabolism of endogenous and xenobiotic compounds by catalysing the conjugation of the reduced form of glutathione to the substrate. The epsilon class of GST (GSTe), unique to arthropods, is known t...

Full description

Bibliographic Details
Main Authors: Cherry L. Dykes, Gunjan Sharma, Abhisek K. Behera, Neera Kapoor, Mark J. I. Paine, Martin J. Donnelly, Om P. Singh
Format: Article
Language:English
Published: Nature Portfolio 2022-10-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-022-21522-8
_version_ 1811335120610656256
author Cherry L. Dykes
Gunjan Sharma
Abhisek K. Behera
Neera Kapoor
Mark J. I. Paine
Martin J. Donnelly
Om P. Singh
author_facet Cherry L. Dykes
Gunjan Sharma
Abhisek K. Behera
Neera Kapoor
Mark J. I. Paine
Martin J. Donnelly
Om P. Singh
author_sort Cherry L. Dykes
collection DOAJ
description Abstract The glutathione S-transferases (GST) genes are a multigene family of enzymes involved in the metabolism of endogenous and xenobiotic compounds by catalysing the conjugation of the reduced form of glutathione to the substrate. The epsilon class of GST (GSTe), unique to arthropods, is known to be involved in the detoxification process of several classes of insecticides, and GSTe2 in particular is known to have DDT dehydrochlorinase activity. This communication reports a tandem duplication of a genomic region encoding GSTe2 and GSTe4 genes in a laboratory-colonized DDT-resistant Anopheles stephensi. We identified duplication breakpoints and the organization of gene duplication through Sanger sequencing performed on long-PCR products. Manual annotation of sequences revealed a tandemly-arrayed duplication of a 3.62 kb segment of GST epsilon gene clusters comprised of five genes: a partial GSTe1, GSTe2, GSTe2-pseudogene, GSTe4 and partial GSTe5, interconnected by a conserved 2.42 kb DNA insert segment major part of which is homologous to a genomic region located on a different chromosome. The tandemly duplicated array contained a total of two GSTe2 and three GSTe4 functional paralog genes. Read-depth coverage and split-read analysis of Illumina-based whole-genome sequence reads confirmed the presence of duplication in the corresponding region of the genome. The increased gene dose in mosquitoes as a result of the GSTe gene-duplication may be an adaptive process to increase levels of detoxifying enzymes to counter insecticide pressure.
first_indexed 2024-04-13T17:19:24Z
format Article
id doaj.art-58f459c72cea447ca939332a24dea7f1
institution Directory Open Access Journal
issn 2045-2322
language English
last_indexed 2024-04-13T17:19:24Z
publishDate 2022-10-01
publisher Nature Portfolio
record_format Article
series Scientific Reports
spelling doaj.art-58f459c72cea447ca939332a24dea7f12022-12-22T02:38:01ZengNature PortfolioScientific Reports2045-23222022-10-0112111410.1038/s41598-022-21522-8Tandem duplication of a genomic region encoding glutathione S-transferase epsilon-2 and -4 genes in DDT-resistant Anopheles stephensi strain from IndiaCherry L. Dykes0Gunjan Sharma1Abhisek K. Behera2Neera Kapoor3Mark J. I. Paine4Martin J. Donnelly5Om P. Singh6National Institute of Malaria ResearchNational Institute of Malaria ResearchNational Institute of Malaria ResearchIndira Gandhi National Open UniversityDepartment of Vector Biology, Liverpool School of Tropical MedicineDepartment of Vector Biology, Liverpool School of Tropical MedicineNational Institute of Malaria ResearchAbstract The glutathione S-transferases (GST) genes are a multigene family of enzymes involved in the metabolism of endogenous and xenobiotic compounds by catalysing the conjugation of the reduced form of glutathione to the substrate. The epsilon class of GST (GSTe), unique to arthropods, is known to be involved in the detoxification process of several classes of insecticides, and GSTe2 in particular is known to have DDT dehydrochlorinase activity. This communication reports a tandem duplication of a genomic region encoding GSTe2 and GSTe4 genes in a laboratory-colonized DDT-resistant Anopheles stephensi. We identified duplication breakpoints and the organization of gene duplication through Sanger sequencing performed on long-PCR products. Manual annotation of sequences revealed a tandemly-arrayed duplication of a 3.62 kb segment of GST epsilon gene clusters comprised of five genes: a partial GSTe1, GSTe2, GSTe2-pseudogene, GSTe4 and partial GSTe5, interconnected by a conserved 2.42 kb DNA insert segment major part of which is homologous to a genomic region located on a different chromosome. The tandemly duplicated array contained a total of two GSTe2 and three GSTe4 functional paralog genes. Read-depth coverage and split-read analysis of Illumina-based whole-genome sequence reads confirmed the presence of duplication in the corresponding region of the genome. The increased gene dose in mosquitoes as a result of the GSTe gene-duplication may be an adaptive process to increase levels of detoxifying enzymes to counter insecticide pressure.https://doi.org/10.1038/s41598-022-21522-8
spellingShingle Cherry L. Dykes
Gunjan Sharma
Abhisek K. Behera
Neera Kapoor
Mark J. I. Paine
Martin J. Donnelly
Om P. Singh
Tandem duplication of a genomic region encoding glutathione S-transferase epsilon-2 and -4 genes in DDT-resistant Anopheles stephensi strain from India
Scientific Reports
title Tandem duplication of a genomic region encoding glutathione S-transferase epsilon-2 and -4 genes in DDT-resistant Anopheles stephensi strain from India
title_full Tandem duplication of a genomic region encoding glutathione S-transferase epsilon-2 and -4 genes in DDT-resistant Anopheles stephensi strain from India
title_fullStr Tandem duplication of a genomic region encoding glutathione S-transferase epsilon-2 and -4 genes in DDT-resistant Anopheles stephensi strain from India
title_full_unstemmed Tandem duplication of a genomic region encoding glutathione S-transferase epsilon-2 and -4 genes in DDT-resistant Anopheles stephensi strain from India
title_short Tandem duplication of a genomic region encoding glutathione S-transferase epsilon-2 and -4 genes in DDT-resistant Anopheles stephensi strain from India
title_sort tandem duplication of a genomic region encoding glutathione s transferase epsilon 2 and 4 genes in ddt resistant anopheles stephensi strain from india
url https://doi.org/10.1038/s41598-022-21522-8
work_keys_str_mv AT cherryldykes tandemduplicationofagenomicregionencodingglutathionestransferaseepsilon2and4genesinddtresistantanophelesstephensistrainfromindia
AT gunjansharma tandemduplicationofagenomicregionencodingglutathionestransferaseepsilon2and4genesinddtresistantanophelesstephensistrainfromindia
AT abhisekkbehera tandemduplicationofagenomicregionencodingglutathionestransferaseepsilon2and4genesinddtresistantanophelesstephensistrainfromindia
AT neerakapoor tandemduplicationofagenomicregionencodingglutathionestransferaseepsilon2and4genesinddtresistantanophelesstephensistrainfromindia
AT markjipaine tandemduplicationofagenomicregionencodingglutathionestransferaseepsilon2and4genesinddtresistantanophelesstephensistrainfromindia
AT martinjdonnelly tandemduplicationofagenomicregionencodingglutathionestransferaseepsilon2and4genesinddtresistantanophelesstephensistrainfromindia
AT ompsingh tandemduplicationofagenomicregionencodingglutathionestransferaseepsilon2and4genesinddtresistantanophelesstephensistrainfromindia