Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-18T12:20:08.779Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  20 June 2019

H. Su ,
Y. Gao ,
Y. Liu ,
X. Li ,
Y. Liang ,
X. Dai ,
Y. Xu ,
Y. Zhou  and
H. Wang Open the ORCID record for H. Wang [Opens in a new window]
H. Su
Affiliation:
College of Animal Sciences, Zhejiang University, Hangzhou 310058, China
Y. Gao
Affiliation:
College of Animal Sciences, Zhejiang University, Hangzhou 310058, China
Y. Liu
Affiliation:
College of Animal Sciences, Zhejiang University, Hangzhou 310058, China
X. Li
Affiliation:
College of Animal Sciences, Zhejiang University, Hangzhou 310058, China
Y. Liang
Affiliation:
College of Animal Sciences, Zhejiang University, Hangzhou 310058, China
X. Dai
Affiliation:
College of Animal Sciences, Zhejiang University, Hangzhou 310058, China
Y. Xu
Affiliation:
College of Animal Sciences, Zhejiang University, Hangzhou 310058, China
Y. Zhou
Affiliation:
College of Animal Sciences, Zhejiang University, Hangzhou 310058, China
H. Wang*
Affiliation:
College of Animal Sciences, Zhejiang University, Hangzhou 310058, China
*
*Author for correspondence Phone: +86-571-88982523 Fax: +86-571-88982723 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

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.

Keywords

Glyphodes pyloalisinsecticide resistantmidgutdetoxification gene
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 110 , Issue 1 , February 2020 , pp. 57 - 67
Check for updates
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

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), 256–260.Google Scholar
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), 675–686.Google Scholar
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), 615–636.Google Scholar
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), 3584–3591.Google Scholar
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, 89–110.Google Scholar
Enayati, A.A., Ranson, H. & Hemingway, J. (2005) Insect glutathione transferases and insecticide resistance. Insect Molecular Biology 14(1), 3–8.Google Scholar
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.Google Scholar
Feyereisen, R. (2011) Arthropod CYPomes illustrate the tempo and mode in P450 evolution. Biochimica Et Biophysica Acta 1814(1), 19–28.Google Scholar
Ffrench-Constant, R.H. (2007) Which came first: insecticides or resistance? Trends in Genetics 23(1), 1–4.Google Scholar
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), 169–173.Google Scholar
Georghiou, G.P. (1972) The Evolution of Resistance to Pesticides. Annual Review of Ecology & Systematics 3(1), 133–168.Google Scholar
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, 33–38.Google Scholar
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), 169–177.Google Scholar
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), 651–658.Google Scholar
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), 5241–5250.Google Scholar
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), 4223–4236.Google Scholar
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.Google Scholar
Kim, D., Langmead, B. & Salzberg, S.L. (2015) HISAT: a fast spliced aligner with low memory requirements. Nature Methods 12(4), 357–360.Google Scholar
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), 180–187.Google Scholar
Li, X., Schuler, M.A. & Berenbaum, M.R. (2007) Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annual Review of Entomology 52, 231–253.Google Scholar
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.Google Scholar
Liu, N. (2015) Insecticide resistance in mosquitoes: impact, mechanisms, and research directions. Annual Review of Entomology 60(1), 537–559.Google Scholar
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.Google Scholar
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), 402–408.Google Scholar
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.Google Scholar
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), 1297–1303.Google Scholar
ME, H. (2008) Sequencing breakthroughs for genomic ecology and evolutionary biology. Molecular ecology resources 8(1), 3–17.Google Scholar
Motoyama, N. & Dauterman, W.C. (1980) Glutathione S-transferases: their role in the metabolism of organophosphorus insecticides. Rev. Biochem. Toxicol 20, 49–70.Google Scholar
Narahashi, T. (1996) Neuronal ion channels as the target sites of insecticides. Pharmacology & Toxicology 79(1), 1–14.Google Scholar
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.Google Scholar
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), 244–253.Google Scholar
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, 309–381.Google Scholar
Perry, T., Batterham, P. & Daborn, P.J. (2011) The biology of insecticidal activity and resistance. Insect Biochemistry and Molecular Biology 41(7), 411–422.Google Scholar
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), 203–214.Google Scholar
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), 507–512.Google Scholar
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.Google Scholar
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), 295–304.Google Scholar
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), 179–181.Google Scholar
Satoh, T. & Hosokawa, M. (1998) The mammalian carboxylesterases: from molecules to functions. Annual Review of Pharmacology & Toxicology 38(38), 257–288.Google Scholar
Scott, J.G. (1999) Cytochromes P450 and insecticide resistance. Insect Biochemistry and Molecular Biology 29(9), 757–777.Google Scholar
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.Google Scholar
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), 2725–2729.Google Scholar
Tang, A.H. & Tu, C.P. (1994) Biochemical characterization of Drosophila glutathione S-transferases D1 and D21. Journal of Biological Chemistry 269(45), 27876–27884.Google Scholar
Tompkins, L.M. & Wallace, A.D. (2007) Mechanisms of cytochrome P450 induction. Journal of Biochemical & Molecular Toxicology 21(4), 176–181.Google Scholar
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), 65–72.Google Scholar
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), 329–337.Google Scholar
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), 401–408.Google Scholar
Wu, K., Liang, G. & Guo, Y. (1997) Phoxim resistance in Helicoverpa armigera (Lepidoptera: Noctuidae) in China. Journal of Economic Entomology 90(4), 868–872.Google Scholar
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), 452–459.Google Scholar
Yamamoto, K., Ichinose, H., Aso, Y. & Fujii, H. (2010) Expression analysis of cytochrome P450s in the silkmoth, Bombyx mori. Pesticide Biochemistry Physiology 97(1), 1–6.Google Scholar
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), 1784–1789.Google Scholar
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), 180–187.Google Scholar
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), 250–257.Google Scholar
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), 1158–1164.Google Scholar
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.Google Scholar
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), 1–8.Google Scholar
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.Google Scholar
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), 8557–8562.Google Scholar
Supplementary material: File

Su et al. supplementary material

Tables S1-S6 and Figures S1-S2

Download Su et al. supplementary material(File)
File 511.5 KB