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Comparative transcriptome profiling reveals candidate genes related to insecticide resistance of Glyphodes pyloalis

  • H. Su (a1), Y. Gao (a1), Y. Liu (a1), X. Li (a1), Y. Liang (a1), X. Dai (a1), Y. Xu (a1), Y. Zhou (a1) and H. Wang (a1)...


Glyphodes pyloalis Walker (Lepidoptera: Pyralididae) is a common pest in sericulture and has developed resistance to different insecticides. However, the mechanisms involved in insecticide resistance of G. pyloalis are poorly understood. Here, we present the first whole-transcriptome analysis of differential expression genes in insecticide-resistant and susceptible G. pyloalis. Clustering and enrichment analysis of DEGs revealed several biological pathways and enriched Gene Ontology terms were related to detoxification or insecticide resistance. Genes involved in insecticide metabolic processes, including cytochrome P450, glutathione S-transferases and carboxylesterase, were identified in the larval midgut of G. pyloalis. Among them, CYP324A19, CYP304F17, CYP6AW1, CYP6AB10, GSTs5, and AChE-like were significantly increased after propoxur treatment, while CYP324A19, CCE001c, and AChE-like were significantly induced by phoxim, suggesting that these genes were involved in insecticide metabolism. Furthermore, the sequence variation analysis identified 21 single nucleotide polymorphisms within CYP9A20, CYP6AB47, and CYP6AW1. Our findings reveal many candidate genes related to insecticide resistance of G. pyloalis. These results provide novel insights into insecticide resistance and facilitate the development of insecticides with greater specificity to G. pyloalis.


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Chelvanayagama, G., Parker, M.W. & Board, P.G. (2001) Fly fishing for GSTs: a unified nomenclature for mammalian and insect glutathione transferases. Chemico-Biological Interactions 133(1), 256260.
Claudianos, C., Russell, R.J. & Oakeshott, J.G. (1999) The same amino acid substitution in orthologous esterases confers organophosphate resistance on the house fly and a blowfly. Insect Biochemistry and Molecular Biology 29(8), 675686.
Claudianos, C., Ranson, H., Johnson, R.M., Biswas, S., Schuler, M.A., Berenbaum, M.R., Feyereisen, R. & Oakeshott, J.G. (2006) A deficit of detoxification enzymes: pesticide sensitivity and environmental response in the honeybee. Insect Molecular Biology 15(5), 615636.
Cui, F., Qu, H., Cong, J., Liu, X.L. & Qiao, C.L. (2007) Do mosquitoes acquire organophosphate resistance by functional changes in carboxylesterases? Faseb Journal 21(13), 35843591.
Dermauw, W. & Van Leeuwen, T. (2014) The ABC gene family in arthropods: Comparative genomics and role in insecticide transport and resistance. Insect Biochemistry and Molecular Biology 45, 89110.
Enayati, A.A., Ranson, H. & Hemingway, J. (2005) Insect glutathione transferases and insecticide resistance. Insect Molecular Biology 14(1), 38.
Epis, S., Porretta, D., Mastrantonio, V., Urbanelli, S., Sassera, D., Marco, L.D., Mereghetti, V., Montagna, M., Ricci, I. & Favia, G. (2014) Temporal dynamics of the ABC transporter response to insecticide treatment: insights from the malaria vector Anopheles stephensi. Scientific Reports 4(8), 7435.
Feyereisen, R. (2011) Arthropod CYPomes illustrate the tempo and mode in P450 evolution. Biochimica Et Biophysica Acta 1814(1), 1928.
Ffrench-Constant, R.H. (2007) Which came first: insecticides or resistance? Trends in Genetics 23(1), 14.
Field, L. & Devonshire, A. (1998) Evidence that the E4 and FE4 esterase genes responsible for insecticide resistance in the aphid Myzus persicae (Sulzer) are part of a gene family. Biochemical Journal 330 (Pt 1)(1), 169173.
Georghiou, G.P. (1972) The Evolution of Resistance to Pesticides. Annual Review of Ecology & Systematics 3(1), 133168.
Gu, Z., Zhou, Y., Xie, Y., Li, F., Ma, L., Sun, S., Wu, Y., Wang, B., Wang, J., Hong, F., Shen, W. & Li, B. (2014) The adverse effects of phoxim exposure in the midgut of silkworm, Bombyx mori. Chemosphere 96, 3338.
He, W., You, M., Vasseur, L., Yang, G., Xie, M., Cui, K., Bai, J., Liu, C., Li, X. & Xu, X. (2012) Developmental and insecticide-resistant insights from the de novo assembled transcriptome of the diamondback moth, Plutella xylostella. Genomics 99(3), 169177.
Huang, H.S., Hu, N.T., Yao, Y.E., Wu, C.Y., Chiang, S.W. & Sun, C.N. (1998) Molecular cloning and heterologous expression of a glutathione S-transferase involved in insecticide resistance from the diamondback moth, Plutella xylostella. Insect Biochemistry and Molecular Biology 28(9), 651658.
Huang, Y.Y., Shen, C., Chen, J.X., He, C.T., Zhou, Q., Tan, X., Yuan, J. & Yang, Z. (2016) Comparative transcriptome analysis of two Ipomoea aquatica Forsk. Cultivars targeted to explore possible mechanism of genotype dependent accumulation of cadmium. Journal of Agricultural & Food Chemistry 64(25), 52415250.
Huang, R., Huang, Y., Sun, Z., Huang, J. & Wang, Z. (2017) Transcriptome analysisof genes involved in lipid biosynthesis in the developing embryo of pecan (Carya illinoinensis). Journal of Agricultural & Food Chemistry 65(20), 42234236.
Jean-Philippe, D., Mahmoud, I.H., Alexia, C.P. & Ingraham, P.M.J. (2013) Role of cytochrome P450s in insecticide resistance: impact on the control of mosquito-borne diseases and use of insecticides on Earth. Philosophical Transactions of the Royal Society of London 368(1612), 20120429.
Kim, D., Langmead, B. & Salzberg, S.L. (2015) HISAT: a fast spliced aligner with low memory requirements. Nature Methods 12(4), 357360.
Lei, Y., Zhu, X., Xie, W., Wu, Q., Wang, S., Guo, Z., Xu, B., Li, X., Zhou, X. & Zhang, Y. (2014) Midgut transcriptome response to a Cry toxin in the diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae). Gene 533(1), 180187.
Li, X., Schuler, M.A. & Berenbaum, M.R. (2007) Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annual Review of Entomology 52, 231253.
Lin, Q., Jin, F., Hu, Z., Chen, H., Yin, F., Li, Z., Dong, X., Zhang, D., Ren, S. & Feng, X. (2013) Transcriptome analysis of chlorantraniliprole resistance development in the diamondback moth Plutella xylostella. PLOS ONE 8(8), e72314.
Liu, N. (2015) Insecticide resistance in mosquitoes: impact, mechanisms, and research directions. Annual Review of Entomology 60(1), 537559.
Liu, Y., Su, H., Li, R., Li, X., Xu, Y., Dai, X., Zhou, Y. & Wang, H. (2017) Comparative transcriptome analysis of Glyphodes pyloalis Walker (Lepidoptera: Pyralidae) reveals novel insights into heat stress tolerance in insects. BMC Genomics 18(1), 974.
Livak, K.J. & Schmittgen, T.D. (2012) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25(4), 402408.
Mahmood, K., Højland, D.H., Asp, T. & Kristensen, M. (2016) Transcriptome analysis of an insecticide resistant housefly strain: insights about SNPs and regulatory elements in cytochrome P450 genes. PLOS ONE 11(3), e151434.
McKenna, A., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., Garimella, K., Altshuler, D., Gabriel, S. & Daly, M. (2010) The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Research 20(9), 12971303.
ME, H. (2008) Sequencing breakthroughs for genomic ecology and evolutionary biology. Molecular ecology resources 8(1), 317.
Motoyama, N. & Dauterman, W.C. (1980) Glutathione S-transferases: their role in the metabolism of organophosphorus insecticides. Rev. Biochem. Toxicol 20, 4970.
Narahashi, T. (1996) Neuronal ion channels as the target sites of insecticides. Pharmacology & Toxicology 79(1), 114.
Nascimento, A.R.B.D., Fresia, P., Cônsoli, F.L. & Omoto, C. (2015) Comparative transcriptome analysis of lufenuron-resistant and susceptible strains of Spodoptera frugiperda (Lepidoptera: Noctuidae). BMC Genomics 16(1), 985.
Niu, G., Rupasinghe, S.G., Zangerl, A.R., Siegel, J.P., Schuler, M.A. & Berenbaum, M.R. (2011) A substrate-specific cytochrome P450 monooxygenase, CYP6AB11, from the polyphagous navel orangeworm (Amyelois transitella). Insect Biochemistry and Molecular Biology 41(4), 244253.
Oakeshott, J.G., Claudianos, C., Campbell, P. M., Newcomb, R. D. & Russell, R. J., (2005) Biochemical genetics and genomics of insect esterases. Comprehensive Molecular Insect Science 5, 309381.
Perry, T., Batterham, P. & Daborn, P.J. (2011) The biology of insecticidal activity and resistance. Insect Biochemistry and Molecular Biology 41(7), 411422.
Piri Aliabadi, F., Sahragard, A. & Ghadamyari, M. (2016) Lethal and sublethal effects of a chitin synthesis inhibitor, lufenuron, against Glyphodes pyloalis Walker (Lepidoptera: Pyralidae). Journal of Crop Protection 5(2), 203214.
Pittendrigh, B., Aronstein, K., Zinkovsky, E., Andreev, O., Campbell, B., Daly, J., Trowell, S. & Ffrench-Constant, R.H. (1997) Cytochrome P450 genes from Helicoverpa armigera: expression in a pyrethroid-susceptible and -resistant strain. Insect Biochemistry and Molecular Biology 27(6), 507512.
Preissner, S.C., Hoffmann, M.F., Preissner, R., Dunkel, M., Gewiess, A. & Preissner, S. (2013) Polymorphic cytochrome P450 enzymes (CYPs) and their role in personalized therapy. PLOS ONE 8(12), e82562.
Ranson, H., Rossiter, L., Ortelli, F., Jensen, B., Wang, X., Roth, C.W., Collins, F.H. & Hemingway, J. (2001) Identification of a novel class of insect glutathione S-transferases involved in resistance to DDT in the malaria vector Anopheles gambiae. Biochemical Journal 359(2), 295304.
Ranson, H., Claudianos, C., Ortelli, F., Abgrall, C., Hemingway, J., Sharakhova, M.V., Unger, M.F., Collins, F.H. & Feyereisen, R. (2002) Evolution of supergene families associated with insecticide resistance. Science 298(5591), 179181.
Satoh, T. & Hosokawa, M. (1998) The mammalian carboxylesterases: from molecules to functions. Annual Review of Pharmacology & Toxicology 38(38), 257288.
Scott, J.G. (1999) Cytochromes P450 and insecticide resistance. Insect Biochemistry and Molecular Biology 29(9), 757777.
Sparks, M.E., Blackburn, M.B., Kuhar, D. & Gundersen-Rindal, D.E. (2013) Transcriptome of the Lymantria dispar (gypsy moth) larval midgut in response to infection by Bacillus thuringiensis. PLOS ONE 8(5), e61190.
Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30(12), 27252729.
Tang, A.H. & Tu, C.P. (1994) Biochemical characterization of Drosophila glutathione S-transferases D1 and D21. Journal of Biological Chemistry 269(45), 2787627884.
Tompkins, L.M. & Wallace, A.D. (2007) Mechanisms of cytochrome P450 induction. Journal of Biochemical & Molecular Toxicology 21(4), 176181.
Vontas, J.G., Small, G.J. & Hemingway, J. (2001) Glutathione S-transferases as antioxidant defence agents confer pyrethroid resistance in Nilaparvata lugens. Biochemical Journal 357 (Pt 1), 6572.
Vontas, J.G., Small, G.J., Nikou, D.C., Ranson, H. & Hemingway, J. (2002) Purification, molecular cloning and heterologous expression of a glutathione S-transferase involved in insecticide resistance from the rice brown planthopper, Nilaparvata lugens. Biochemical Journal 362 (Pt 2), 329337.
Watanabe, H., Kurihara, Y., Wang, Y.X. & Shimizu, T. (1988) Mulberry pyralid, Glyphodes pyloalis: Habitual host of nonoccluded viruses pathogenic to the silkworm, Bombyx mori. Journal of Invertebrate Pathology 52(3), 401408.
Wu, K., Liang, G. & Guo, Y. (1997) Phoxim resistance in Helicoverpa armigera (Lepidoptera: Noctuidae) in China. Journal of Economic Entomology 90(4), 868872.
Wondji, C. S., Irving, H., Morgan, J., Lobo, N.F., Collins, F.H., Hunt, R.H., Coetzee, M., Hemingway, J. & Ranson, H. (2009). Two duplicated p450 genes are associated with pyrethroid resistance in Anopheles funestus, a major malaria vector. Genome Research 90(3), 452459.
Yamamoto, K., Ichinose, H., Aso, Y. & Fujii, H. (2010) Expression analysis of cytochrome P450s in the silkmoth, Bombyx mori. Pesticide Biochemistry Physiology 97(1), 16.
Yang, Y.H., Chen, S., Wu, S.W., Yue, L.N. & Wu, Y.D. (2006) Constitutive overexpression of multiple cytochrome P450 genes associated with pyrethroid resistance in Helicoverpa armigera. Journal of Economic Entomology 99(5), 17841789.
Yanyuan, L., Xun, Z., Wen, X., Qingjun, W., Shaoli, W., Zhaojiang, G., Baoyun, X., Xianchun, L., Xuguo, Z. & Youjun, Z. (2014) Midgut transcriptome response to a Cry toxin in the diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae). Gene 533(1), 180187.
Yazdani, E., Sendi, J.J., Aliakbar, A. & Senthil-Nathan, S. (2013) Effect of Lavandula angustifolia essential oil against lesser mulberry pyralid Glyphodes pyloalis Walker (Lep: Pyralidae) and identification of its major derivatives. Pesticide Biochemistry Physiology 107(2), 250257.
Yu, Q., Lu, C., Li, B., Fang, S., Zuo, W., Dai, F., Zhang, Z. & Xiang, Z. (2008) Identification, genomic organization and expression pattern of glutathione S-transferase in the silkworm, Bombyx mori. Insect Biochemistry and Molecular Biology 38(12), 11581164.
Yu, L., Tang, W., He, W., Ma, X., Vasseur, L., Baxter, S.W., Yang, G., Huang, S., Song, F. & You, M. (2015) Characterization and expression of the cytochrome P450 gene family in diamondback moth, Plutella xylostella (L.). Scientific Reports 5(1), 8952.
Yu, H., Xu, J., Wang, X., Ma, Y., Yu, D., Fei, D., Zhang, S. & Wang, W. (2017) Identification of four ATP-binding cassette transporter genes in cnaphalocrocis medinalis and their expression in response to insecticide treatment. Journal of Insect Science 17(2), 18.
Zhang, J., Zhang, Y., Li, J., Liu, M. & Liu, Z. (2016) Midgut transcriptome of the cockroach Periplaneta americana and its Microbiota: digestion, detoxification and oxidative stress response. PLOS ONE 11(5), e155254.
Zhu, F., Parthasarathy, R., Bai, H., Woithe, K., Kaussmann, M., Nauen, R., Harrison, D.A. & Palli, S.R. (2010) A brain-specific cytochrome P450 responsible for the majority of deltamethrin resistance in the QTC279 strain of Tribolium castaneum. Proceedings of the National Academy of Sciences 107(19), 85578562.


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Comparative transcriptome profiling reveals candidate genes related to insecticide resistance of Glyphodes pyloalis

  • H. Su (a1), Y. Gao (a1), Y. Liu (a1), X. Li (a1), Y. Liang (a1), X. Dai (a1), Y. Xu (a1), Y. Zhou (a1) and H. Wang (a1)...


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