Evolutionary changes in gene expression, coding sequence and copy-number at the Cyp6g1 locus contribute to resistance to multiple insecticides in Drosophila.

Widespread use of insecticides has led to insecticide resistance in many populations of insects. In some populations, resistance has evolved to multiple pesticides. In Drosophila melanogaster, resistance to multiple classes of insecticide is due to the overexpression of a single cytochrome P450 gene...

Full description

Bibliographic Details
Main Authors: Thomas W R Harrop, Tamar Sztal, Christopher Lumb, Robert T Good, Phillip J Daborn, Philip Batterham, Henry Chung
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2014-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC3885650?pdf=render
id doaj-26fbaca04d5645c8a60566123d147738
record_format Article
spelling doaj-26fbaca04d5645c8a60566123d1477382020-11-25T00:47:15ZengPublic Library of Science (PLoS)PLoS ONE1932-62032014-01-0191e8487910.1371/journal.pone.0084879Evolutionary changes in gene expression, coding sequence and copy-number at the Cyp6g1 locus contribute to resistance to multiple insecticides in Drosophila.Thomas W R HarropTamar SztalChristopher LumbRobert T GoodPhillip J DabornPhilip BatterhamHenry ChungWidespread use of insecticides has led to insecticide resistance in many populations of insects. In some populations, resistance has evolved to multiple pesticides. In Drosophila melanogaster, resistance to multiple classes of insecticide is due to the overexpression of a single cytochrome P450 gene, Cyp6g1. Overexpression of Cyp6g1 appears to have evolved in parallel in Drosophila simulans, a sibling species of D. melanogaster, where it is also associated with insecticide resistance. However, it is not known whether the ability of the CYP6G1 enzyme to provide resistance to multiple insecticides evolved recently in D. melanogaster or if this function is present in all Drosophila species. Here we show that duplication of the Cyp6g1 gene occurred at least four times during the evolution of different Drosophila species, and the ability of CYP6G1 to confer resistance to multiple insecticides exists in D. melanogaster and D. simulans but not in Drosophila willistoni or Drosophila virilis. In D. virilis, which has multiple copies of Cyp6g1, one copy confers resistance to DDT and another to nitenpyram, suggesting that the divergence of protein sequence between copies subsequent to the duplication affected the activity of the enzyme. All orthologs tested conferred resistance to one or more insecticides, suggesting that CYP6G1 had the capacity to provide resistance to anthropogenic chemicals before they existed. Finally, we show that expression of Cyp6g1 in the Malpighian tubules, which contributes to DDT resistance in D. melanogaster, is specific to the D. melanogaster-D. simulans lineage. Our results suggest that a combination of gene duplication, regulatory changes and protein coding changes has taken place at the Cyp6g1 locus during evolution and this locus may play a role in providing resistance to different environmental toxins in different Drosophila species.http://europepmc.org/articles/PMC3885650?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Thomas W R Harrop
Tamar Sztal
Christopher Lumb
Robert T Good
Phillip J Daborn
Philip Batterham
Henry Chung
spellingShingle Thomas W R Harrop
Tamar Sztal
Christopher Lumb
Robert T Good
Phillip J Daborn
Philip Batterham
Henry Chung
Evolutionary changes in gene expression, coding sequence and copy-number at the Cyp6g1 locus contribute to resistance to multiple insecticides in Drosophila.
PLoS ONE
author_facet Thomas W R Harrop
Tamar Sztal
Christopher Lumb
Robert T Good
Phillip J Daborn
Philip Batterham
Henry Chung
author_sort Thomas W R Harrop
title Evolutionary changes in gene expression, coding sequence and copy-number at the Cyp6g1 locus contribute to resistance to multiple insecticides in Drosophila.
title_short Evolutionary changes in gene expression, coding sequence and copy-number at the Cyp6g1 locus contribute to resistance to multiple insecticides in Drosophila.
title_full Evolutionary changes in gene expression, coding sequence and copy-number at the Cyp6g1 locus contribute to resistance to multiple insecticides in Drosophila.
title_fullStr Evolutionary changes in gene expression, coding sequence and copy-number at the Cyp6g1 locus contribute to resistance to multiple insecticides in Drosophila.
title_full_unstemmed Evolutionary changes in gene expression, coding sequence and copy-number at the Cyp6g1 locus contribute to resistance to multiple insecticides in Drosophila.
title_sort evolutionary changes in gene expression, coding sequence and copy-number at the cyp6g1 locus contribute to resistance to multiple insecticides in drosophila.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2014-01-01
description Widespread use of insecticides has led to insecticide resistance in many populations of insects. In some populations, resistance has evolved to multiple pesticides. In Drosophila melanogaster, resistance to multiple classes of insecticide is due to the overexpression of a single cytochrome P450 gene, Cyp6g1. Overexpression of Cyp6g1 appears to have evolved in parallel in Drosophila simulans, a sibling species of D. melanogaster, where it is also associated with insecticide resistance. However, it is not known whether the ability of the CYP6G1 enzyme to provide resistance to multiple insecticides evolved recently in D. melanogaster or if this function is present in all Drosophila species. Here we show that duplication of the Cyp6g1 gene occurred at least four times during the evolution of different Drosophila species, and the ability of CYP6G1 to confer resistance to multiple insecticides exists in D. melanogaster and D. simulans but not in Drosophila willistoni or Drosophila virilis. In D. virilis, which has multiple copies of Cyp6g1, one copy confers resistance to DDT and another to nitenpyram, suggesting that the divergence of protein sequence between copies subsequent to the duplication affected the activity of the enzyme. All orthologs tested conferred resistance to one or more insecticides, suggesting that CYP6G1 had the capacity to provide resistance to anthropogenic chemicals before they existed. Finally, we show that expression of Cyp6g1 in the Malpighian tubules, which contributes to DDT resistance in D. melanogaster, is specific to the D. melanogaster-D. simulans lineage. Our results suggest that a combination of gene duplication, regulatory changes and protein coding changes has taken place at the Cyp6g1 locus during evolution and this locus may play a role in providing resistance to different environmental toxins in different Drosophila species.
url http://europepmc.org/articles/PMC3885650?pdf=render
work_keys_str_mv AT thomaswrharrop evolutionarychangesingeneexpressioncodingsequenceandcopynumberatthecyp6g1locuscontributetoresistancetomultipleinsecticidesindrosophila
AT tamarsztal evolutionarychangesingeneexpressioncodingsequenceandcopynumberatthecyp6g1locuscontributetoresistancetomultipleinsecticidesindrosophila
AT christopherlumb evolutionarychangesingeneexpressioncodingsequenceandcopynumberatthecyp6g1locuscontributetoresistancetomultipleinsecticidesindrosophila
AT roberttgood evolutionarychangesingeneexpressioncodingsequenceandcopynumberatthecyp6g1locuscontributetoresistancetomultipleinsecticidesindrosophila
AT phillipjdaborn evolutionarychangesingeneexpressioncodingsequenceandcopynumberatthecyp6g1locuscontributetoresistancetomultipleinsecticidesindrosophila
AT philipbatterham evolutionarychangesingeneexpressioncodingsequenceandcopynumberatthecyp6g1locuscontributetoresistancetomultipleinsecticidesindrosophila
AT henrychung evolutionarychangesingeneexpressioncodingsequenceandcopynumberatthecyp6g1locuscontributetoresistancetomultipleinsecticidesindrosophila
_version_ 1725260954430603264