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Splice form variant and amino acid changes in MDR49 confers DDT resistance in transgenic Drosophila

Published on Mar 1, 2016in Scientific Reports4.01
· DOI :10.1038/srep23355
Keon Mook Seong5
Estimated H-index: 5
(UIUC: University of Illinois at Urbana–Champaign),
Weilin Sun13
Estimated H-index: 13
(UIUC: University of Illinois at Urbana–Champaign)
+ 1 AuthorsBarry Robert Pittendrigh25
Estimated H-index: 25
(UIUC: University of Illinois at Urbana–Champaign)
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Abstract
The ATP-binding cassette (ABC) transporters represent a superfamily of proteins that have important physiological roles in both prokaryotes and eukaryotes. In insects, ABC transporters have previously been implicated in insecticide resistance. The 91-R strain of Drosophila melanogaster has been intensely selected with DDT over six decades. A recent selective sweeps analysis of 91-R implicated the potential role of MDR49, an ABC transporter, in DDT resistance, however, to date the details of how MDR49 may play a role in resistance have not been elucidated. In this study, we investigated the impact of structural changes and an alternative splicing event in MDR49 on DDT-resistance in 91-R, as compared to the DDT susceptible strain 91-C. We observed three amino acid differences in MDR49 when 91-R was compared with 91-C, and only one isoform (MDR49B) was implicated in DDT resistance. A transgenic Drosophila strain containing the 91-R-MDR49B isoform had a significantly higher LD50 value as compared to the 91-C-MDR49B isoform at the early time points (6 h to 12 h) during DDT exposure. Our data support the hypothesis that the MDR49B isoform, with three amino acid mutations, plays a role in the early aspects of DDT resistance in 91-R.
  • References (41)
  • Citations (13)
Cite
References41
Newest
Published on Jun 1, 2015in Pesticide Biochemistry and Physiology2.87
Kyle J. Gellatly3
Estimated H-index: 3
(UMass: University of Massachusetts Amherst),
Kyong Sup Yoon24
Estimated H-index: 24
(SIU: Southern Illinois University Carbondale)
+ 3 AuthorsJ. Marshall Clark30
Estimated H-index: 30
(UMass: University of Massachusetts Amherst)
Abstract 4,4'-dichlorodiphenyltrichloroethane (DDT) has been re-recommended by the World Health Organization for malaria mosquito control. Previous DDT use has resulted in resistance, and with continued use resistance will increase in terms of level and extent. Drosophila melanogaster is a model dipteran that has many available genetic tools, numerous studies done on insecticide resistance mechanisms, and is related to malaria mosquitoes allowing for extrapolation. The 91-R strain of D. melanoga...
Published on May 1, 2015in Scientific Reports4.01
Sara Epis13
Estimated H-index: 13
,
Daniele Porretta13
Estimated H-index: 13
+ 8 AuthorsGuido Favia20
Estimated H-index: 20
In insects, ABC transporters have been shown to contribute to defence/resistance to insecticides by reducing toxic concentrations in cells/tissues. Despite the extensive studies about this detoxifying mechanism, the temporal patterns of ABC transporter activation have been poorly investigated. Using the malaria vector Anopheles stephensi as a study system, we investigated the expression profile of ABC genes belonging to different subfamilies in permethrin-treated larvae at different time points ...
Published on Mar 31, 2015in PLOS ONE2.78
Laura D. Steele5
Estimated H-index: 5
(UIUC: University of Illinois at Urbana–Champaign),
Brad S. Coates22
Estimated H-index: 22
(Iowa State University)
+ 5 AuthorsBarry Robert Pittendrigh25
Estimated H-index: 25
(UIUC: University of Illinois at Urbana–Champaign)
Adaptation of insect phenotypes for survival after exposure to xenobiotics can result from selection at multiple loci with additive genetic effects. To the authors’ knowledge, no selective sweep analysis has been performed to identify such loci in highly dichlorodiphenyltrichloroethane (DDT) resistant insects. Here we compared a highly DDT resistant phenotype in the Drosophila melanogaster (Drosophila) 91-R strain to the DDT susceptible 91-C strain, both of common origin. Whole genome re-sequenc...
Published on Nov 17, 2014in PLOS ONE2.78
J. Joe Hull17
Estimated H-index: 17
(ARS: Agricultural Research Service),
Kendrick Chaney1
Estimated H-index: 1
(ARS: Agricultural Research Service)
+ 4 AuthorsLaura Corley Lavine12
Estimated H-index: 12
(WSU: Washington State University)
ATP-binding cassette (ABC) transporters are a large superfamily of proteins that mediate diverse physiological functions by coupling ATP hydrolysis with substrate transport across lipid membranes. In insects, these proteins play roles in metabolism, development, eye pigmentation, and xenobiotic clearance. While ABC transporters have been extensively studied in vertebrates, less is known concerning this superfamily in insects, particularly hemipteran pests. We used RNA-Seq transcriptome sequencin...
Published on Feb 1, 2014in Insect Biochemistry and Molecular Biology3.62
Wannes Dermauw24
Estimated H-index: 24
(UGent: Ghent University),
Thomas Van Leeuwen34
Estimated H-index: 34
(UGent: Ghent University)
About a 100 years ago, the Drosophila white mutant marked the birth of Drosophila genetics. The white gene turned out to encode the first well studied ABC transporter in arthropods. The ABC gene family is now recognized as one of the largest transporter families in all kingdoms of life. The majority of ABC proteins function as primary-active transporters that bind and hydrolyze ATP while transporting a large diversity of substrates across lipid membranes. Although extremely well studied in verte...
Published on Dec 1, 2013in Scientific Reports4.01
Fang Zhu17
Estimated H-index: 17
(UK: University of Kentucky),
Hemant Gujar4
Estimated H-index: 4
(UK: University of Kentucky)
+ 3 AuthorsSubba Reddy Palli44
Estimated H-index: 44
(UK: University of Kentucky)
Recent advances in genomic and post-genomic technologies have facilitated a genome-wide analysis of the insecticide resistance-associated genes in insects. Through bed bug, Cimex lectularius transcriptome analysis, we identified 14 molecular markers associated with pyrethroid resistance. Our studies revealed that most of the resistance-associated genes functioning in diverse mechanisms are expressed in the epidermal layer of the integument, which could prevent or slow down the toxin from reachin...
Published on Oct 1, 2013in Pesticide Biochemistry and Physiology2.87
Joseph P. Strycharz12
Estimated H-index: 12
(UMass: University of Massachusetts Amherst),
Alice Lao1
Estimated H-index: 1
(UMass: University of Massachusetts Amherst)
+ 7 AuthorsJ. Marshall Clark30
Estimated H-index: 30
(UMass: University of Massachusetts Amherst)
Abstract Resistance to 4,4′-dichlorodiphenyltrichloroethane (DDT) in the 91-R strain of Drosophila melanogaster is extremely high compared to the susceptible Canton-S strain (>1500 times). In addition to enhanced oxidative detoxification, the 91-R strain also has a reduced rate of DDT penetration, increased levels of reductive and conjugative metabolism, and substantially more excretion than the Canton-S strain. Contact penetration of DDT was ∼30% less with 91-R flies, which also had significant...
Published on Aug 1, 2013in Pest Management Science3.25
Xinghui Qiu15
Estimated H-index: 15
,
Weilin Sun13
Estimated H-index: 13
(UIUC: University of Illinois at Urbana–Champaign)
+ 6 AuthorsBarry Robert Pittendrigh25
Estimated H-index: 25
(UIUC: University of Illinois at Urbana–Champaign)
BACKGROUND: Moderate to high DDT resistance in generally associated with overexpression of multiple genes and therefore has been considered to be polygenic. However, very little information is available about the molecular mechanisms that insect populationsemploywhenevolvingincreasedlevelsofresistance.Thepresenceofcommonregulatorymotifsamongresistanceassociated genes may help to explain how and why certain suites of genes are preferentially represented in genomic-scale analyses. RESULTS: A set o...
Published on Jan 1, 2013in BMC Genomics3.50
Gunnar Broehan5
Estimated H-index: 5
(University of Osnabrück),
Tobias Kroeger1
Estimated H-index: 1
(University of Osnabrück)
+ 1 AuthorsHans Merzendorfer26
Estimated H-index: 26
(University of Osnabrück)
Background The ATP-binding cassette (ABC) transporters belong to a large superfamily of proteins that have important physiological functions in all living organisms. Most are integral membrane proteins that transport a broad spectrum of substrates across lipid membranes. In insects, ABC transporters are of special interest because of their role in insecticide resistance.
Shogo Atsumi2
Estimated H-index: 2
,
Kazuhisa Miyamoto1
Estimated H-index: 1
+ 12 AuthorsKazuei Mita47
Estimated H-index: 47
Bt toxins derived from the arthropod bacterial pathogen Bacillus thuringiensis are widely used for insect control as insecticides or in transgenic crops. Bt resistance has been found in field populations of several lepidopteran pests and in laboratory strains selected with Bt toxin. Widespread planting of crops expressing Bt toxins has raised concerns about the potential increase of resistance mutations in targeted insects. By using Bombyx mori as a model, we identified a candidate gene for a re...
Cited By13
Newest
Published on Jun 1, 2019in Pesticide Biochemistry and Physiology2.87
Keon Mook Seong5
Estimated H-index: 5
(MSU: Michigan State University),
Brad S. Coates22
Estimated H-index: 22
(ARS: Agricultural Research Service),
Barry Robert Pittendrigh25
Estimated H-index: 25
(MSU: Michigan State University)
Abstract Cytochrome P450s are part of a super-gene family that has undergone gene duplication, divergence, over-expression and, in some cases, loss of function. One such case is the 91-R and 91-C strains of common origin, in Drosophila melanogaster , whereby 91-R (DDT resistant strain) overexpresses Cyp4p1 and Cyp4p2 and both genes are lost in 91-C (DDT susceptible strain). In this study, we used a comparative approach to demonstrate that transcription of Cyp4p1 and Cyp4p2 were constitutively up...
Published on Aug 1, 2019in Pesticide Biochemistry and Physiology2.87
Keon Mook Seong5
Estimated H-index: 5
(MSU: Michigan State University),
Omprakash Mittapalli19
Estimated H-index: 19
+ 1 AuthorsBarry Robert Pittendrigh25
Estimated H-index: 25
(MSU: Michigan State University)
Abstract While insecticide resistance presents a challenge for those intent on controlling insect populations, these challenges have also generated a set of tools that can be used to ask fundamental biological questions about that resistance. Numerous species of insects have evolved resistance to multiple classes of insecticides. Each one of these species and their respective resistant populations represent a potential tool for understanding the molecular basis of the evolution of resistance. Ho...
Published on Jun 10, 2019in International Journal of Molecular Sciences4.18
Chao Wu , Swapan Chakrabarty + 2 AuthorsYutao Xiao1
Estimated H-index: 1
ATP-binding cassette (ABC) transporters, a large class of transmembrane proteins, are widely found in organisms and play an important role in the transport of xenobiotics. Insect ABC transporters are involved in insecticide detoxification and Bacillus thuringiensis (Bt) toxin perforation. The complete ABC transporter is composed of two hydrophobic transmembrane domains (TMDs) and two nucleotide binding domains (NBDs). Conformational changes that are needed for their action are mediated by ATP hy...
Published on Feb 5, 2019in Frontiers in Genetics3.52
Keon Mook Seong5
Estimated H-index: 5
,
Brad S. Coates22
Estimated H-index: 22
,
Barry Robert Pittendrigh25
Estimated H-index: 25
Ten constitutively differentially expressed miRNAs were previously described between DDT-resistant 91-R and -susceptible control Drosophila melanogaster strains, and among their predicted target genes were those associated with metabolic DDT resistance mechanisms. The present study evaluated the inducibility of miRNA expression and putative downstream regulation of cytochrome P450s in response to DDT exposure in a time-dependent manner in 91-R and the susceptible Canton-S strain. Specifically, R...
Published on Dec 1, 2018in Insect Biochemistry and Molecular Biology3.62
Shane Denecke (FORTH: Foundation for Research & Technology – Hellas), Luc Swevers24
Estimated H-index: 24
+ 1 AuthorsJohn Vontas39
Estimated H-index: 39
(FORTH: Foundation for Research & Technology – Hellas)
Abstract The use of oral insecticidal molecules (small molecules, peptides, dsRNA) via spray or plant mediated applications represents an efficient way to manage damaging insect species. With the exception of Bt toxins that target the midgut epithelium itself, most of these compounds have targets that lie within the hemocoel (body) of the insect. Because of this, one of the greatest factors in determining the effectiveness of an oral insecticidal compound is its ability to traverse the gut epith...
Published on Nov 1, 2018in Journal of Insect Science1.45
Laura D. Steele5
Estimated H-index: 5
(UIUC: University of Illinois at Urbana–Champaign),
Brad S. Coates22
Estimated H-index: 22
(USDA: United States Department of Agriculture)
+ 5 AuthorsBarry Robert Pittendrigh25
Estimated H-index: 25
(MSU: Michigan State University)
Published on Nov 1, 2018in Pest Management Science3.25
Keon Mook Seong5
Estimated H-index: 5
(MSU: Michigan State University),
Brad S. Coates22
Estimated H-index: 22
(Iowa State University)
+ 2 AuthorsBarry Robert Pittendrigh25
Estimated H-index: 25
(MSU: Michigan State University)
Published on Jun 1, 2018in Current opinion in insect science3.78
Trent Perry11
Estimated H-index: 11
(University of Melbourne),
Philip Batterham31
Estimated H-index: 31
(University of Melbourne)
The vinegar fly, Drosophila melanogaster , has made an enormous contribution to our understanding of insecticide targets, metabolism and transport. This contribution has been enabled by the unmatched capacity to manipulate genes in D. melanogaster and the fact that lessons learn in this system have been applicable to pests, because of the evolutionary conservation of key genes, particularly those encoding targets. With the advent of the CRISPR-Cas9 gene editing technology, genes can now be manip...
Published on Apr 26, 2018in PLOS ONE2.78
Keon Mook Seong5
Estimated H-index: 5
(MSU: Michigan State University),
Brad S. Coates22
Estimated H-index: 22
(Iowa State University)
+ 2 AuthorsBarry Robert Pittendrigh25
Estimated H-index: 25
Published on Apr 1, 2018in Developmental and Comparative Immunology3.12
Guanyun Wei2
Estimated H-index: 2
(Nanjing Normal University),
Lianjie Sun2
Estimated H-index: 2
(Nanjing Normal University)
+ 3 AuthorsFei Ma12
Estimated H-index: 12
(Nanjing Normal University)
Abstract Pathogen bacteria infections can lead to dynamic changes of microRNA (miRNA) and mRNA expression profiles, which may control synergistically the outcome of immune responses. To reveal the role of dynamic miRNA-mRNA regulation in Drosophila innate immune responses, we have detailedly analyzed the paired miRNA and mRNA expression profiles at three time points during Drosophila adult males with Micrococcus luteus ( M. luteus ) infection using RNA- and small RNA-seq data. Our results demons...
View next paperResistance in the highly DDT-resistant 91-R strain of Drosophila melanogaster involves decreased penetration, increased metabolism, and direct excretion