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      Is Open Access

      Analysis of Differentially Expressed Genes Related to Resistance in Spinosad- and Neonicotinoid-Resistant Musca domestica L. (Diptera: Muscidae) Strains

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      PLoS ONE

      Public Library of Science

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          Abstract

          Background

          The housefly is a global pest that has developed resistance to most insecticides applied against it. Resistance of the spinosad-resistant strain 791spin and the neonicotinoid-resistant 766b strain is believed to be due to metabolism. We investigate differentially expressed genes in these two resistant strains related to metabolism in comparison with an insecticide-susceptible reference strain.

          Results

          Genes involved in metabolism of xenobiotics were primarily up-regulated in resistant flies with some differences between resistant strains. The cyp4g98 and cyp6g4 genes proved interesting in terms of neonicotinoid resistance, while cyp4d9 was overexpressed in 791spin compared to spinosad-susceptible strains. GSTs, ESTs and UGTs were mostly overexpressed, but not to the same degree as P450s. We present a comprehensive and comparative picture of gene expression in three housefly strains differing significantly in their response to insecticides. High differential expression of P450s and genes coding for cuticle protein indicates a combination of factors involved in metabolic neonicotinoid and spinosad resistance.

          Conclusion

          Resistance in these strains is apparently not linked to the alteration of a single gene but is composed of several changes including differential expression of genes encoding metabolic detoxification enzymes.

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          Most cited references 39

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          Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics.

          Xenobiotic resistance in insects has evolved predominantly by increasing the metabolic capability of detoxificative systems and/or reducing xenobiotic target site sensitivity. In contrast to the limited range of nucleotide changes that lead to target site insensitivity, many molecular mechanisms lead to enhancements in xenobiotic metabolism. The genomic changes that lead to amplification, overexpression, and coding sequence variation in the three major groups of genes encoding metabolic enzymes, i.e., cytochrome P450 monooxygenases (P450s), esterases, and glutathione-S-transferases (GSTs), are the focus of this review. A substantial number of the adaptive genomic changes associated with insecticide resistance that have been characterized to date are transposon mediated. Several lines of evidence suggest that P450 genes involved in insecticide resistance, and perhaps insecticide detoxification genes in general, may share an evolutionary association with genes involved in allelochemical metabolism. Differences in the selective regime imposed by allelochemicals and insecticides may account for the relative importance of regulatory or structural mutations in conferring resistance.
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            Insect glutathione transferases and insecticide resistance.

            Glutathione transferases (GSTs) are a diverse family of enzymes found ubiquitously in aerobic organisms. They play a central role in the detoxification of both endogenous and xenobiotic compounds and are also involved in intracellular transport, biosynthesis of hormones and protection against oxidative stress. Interest in insect GSTs has primarily focused on their role in insecticide resistance. GSTs can metabolize insecticides by facilitating their reductive dehydrochlorination or by conjugation reactions with reduced glutathione, to produce water-soluble metabolites that are more readily excreted. In addition, they contribute to the removal of toxic oxygen free radical species produced through the action of pesticides. Annotation of the Anopheles gambiae and Drosophila melanogaster genomes has revealed the full extent of this enzyme family in insects. This mini review describes the insect GST enzyme family, focusing specifically on their role in conferring insecticide resistance.
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              Cytochromes P450 and insecticide resistance.

              The cytochrome P450-dependent monooxygenases (monooxygenases) are an extremely important metabolic system involved in the catabolism and anabolism of xenobiotics and endogenous compounds. Monooxygenase-mediated metabolism is a common mechanism by which insects become resistant to insecticides as evidenced by the numerous insect species and insecticides affected. This review begins by presenting background information about P450s, the role of monooxygenases in insects, and the different techniques that have been used to isolate individual insect P450s. Next, insecticide resistance is briefly described, and then historical information about monooxygenase-mediated insecticide resistance is reviewed. For any case of monooxygenase-mediated resistance, identification of the P450(s) involved, out of the dozens that are present in an insect, has proven very challenging. Therefore, the next section of the review focuses on the minimal criteria for establishing that a P450 is involved in resistance. This is followed by a comprehensive examination of the literature concerning the individual P450s that have been isolated from insecticide resistant strains. In each case, the history of the strain and the evidence for monooxygenase-mediated resistance are reviewed. The isolation and characterization of the P450(s) from the strain are then described, and the evidence of whether or not the isolated P450(s) is involved in resistance is summarized. The remainder of the review summarizes our current knowledge of the molecular basis of monooxygenase-mediated resistance and the implications for the future. The importance of these studies for development of effective insecticide resistance management strategies is discussed.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                26 January 2017
                2017
                : 12
                : 1
                Affiliations
                Department of Agroecology, Aarhus University, Slagelse, Denmark
                Institute of Zoology Chinese Academy of Sciences, CHINA
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                • Conceptualization: DHH MK.

                • Data curation: MK.

                • Formal analysis: DHH MK.

                • Funding acquisition: MK.

                • Investigation: DHH.

                • Methodology: DHH MK.

                • Project administration: MK.

                • Resources: MK.

                • Supervision: MK.

                • Visualization: DHH.

                • Writing – original draft: DHH MK.

                • Writing – review & editing: DHH MK.

                Article
                PONE-D-16-38994
                10.1371/journal.pone.0170935
                5268453
                28125739
                © 2017 Højland, Kristensen

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                Page count
                Figures: 2, Tables: 2, Pages: 18
                Product
                Funding
                Funded by: Innovation Fund Denmark
                Award ID: 0603-00516B
                Award Recipient :
                This work was supported by the Innovation Fund Denmark. Grant 0603-00516B. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Animals
                Invertebrates
                Arthropoda
                Insects
                Diptera
                Musca Domestica
                Biology and Life Sciences
                Genetics
                Gene Expression
                Biology and Life Sciences
                Agriculture
                Agrochemicals
                Insecticides
                Biology and Life Sciences
                Biochemistry
                Enzymology
                Enzymes
                Hydrolases
                Esterases
                Biology and Life Sciences
                Biochemistry
                Proteins
                Enzymes
                Hydrolases
                Esterases
                Biology and Life Sciences
                Biochemistry
                Enzymology
                Enzyme Chemistry
                Enzyme Metabolism
                Biology and Life Sciences
                Biochemistry
                Metabolism
                Metabolic Pathways
                Xenobiotic Metabolism
                Biology and life sciences
                Molecular biology
                Molecular biology techniques
                Sequencing techniques
                RNA sequencing
                Research and analysis methods
                Molecular biology techniques
                Sequencing techniques
                RNA sequencing
                Research and Analysis Methods
                Database and Informatics Methods
                Biological Databases
                Sequence Databases
                Research and Analysis Methods
                Database and Informatics Methods
                Bioinformatics
                Sequence Analysis
                Sequence Databases
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

                Uncategorized

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