Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-20T00:24:10.710Z Has data issue: false hasContentIssue false
  • English
  • Français

Thermotolerance, oxidative stress, apoptosis, heat-shock proteins and damages to reproductive cells of insecticide-susceptible and -resistant strains of the diamondback moth Plutella xylostella

Published online by Cambridge University Press:  31 January 2017

L.J. Zhang ,
J.L. Chen ,
B.L. Yang ,
X.G. Kong ,
D. Bourguet  and
G. Wu
L.J. Zhang
Affiliation:
Key Laboratory of Biopesticide and Chemical Biology (Ministry of Education), Fujian Agriculture and Forestry University, Fuzhou 350002, China
J.L. Chen
Affiliation:
Key Laboratory of Biopesticide and Chemical Biology (Ministry of Education), Fujian Agriculture and Forestry University, Fuzhou 350002, China
B.L. Yang
Affiliation:
Key Laboratory of Biopesticide and Chemical Biology (Ministry of Education), Fujian Agriculture and Forestry University, Fuzhou 350002, China
X.G. Kong
Affiliation:
Key Laboratory of Biopesticide and Chemical Biology (Ministry of Education), Fujian Agriculture and Forestry University, Fuzhou 350002, China
D. Bourguet*
Affiliation:
Inra, UMR CBGP (Centre de Biologie pour la Gestion des Populations), Montferrier-sur-Lez, France
G. Wu*
Affiliation:
Key Laboratory of Biopesticide and Chemical Biology (Ministry of Education), Fujian Agriculture and Forestry University, Fuzhou 350002, China
*
*Author for correspondence Phone: +86 059183769631 Fax: +86 059183789460 E-mail: newugang@163com Phone: +33 499623366 Fax: +33 499623345 E-mail: [email protected]
*Author for correspondence Phone: +86 059183769631 Fax: +86 059183789460 E-mail: newugang@163com Phone: +33 499623366 Fax: +33 499623345 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

In this study, we investigated thermotolerance, several physiological responses and damage to reproductive cells in chlorpyrifos-resistant (Rc) and -susceptible (Sm) strains of the diamondback moth, Plutella xylostella subjected to heat stress. The chlorpyrifos resistance of these strains was mediated by a modified acetylcholinesterase encoded by an allele, ace1R, of the ace1 gene. Adults of the Rc strain were less heat resistant than those of the Sm strain; they also had lower levels of enzymatic activity against oxidative damage, higher reactive oxygen species contents, weaker upregulation of two heat shock protein (hsp) genes (hsp69s and hsp20), and stronger upregulation of two apoptotic genes (caspase-7 and -9). The damage to sperm and ovary cells was greater in Rc adults than in Sm adults and was temperature sensitive. The lower fitness of the resistant strain, compared with the susceptible strain, is probably due to higher levels of oxidative stress and apoptosis, which also have deleterious effects on several life history traits. The greater injury observed in conditions of heat stress may be due to both the stronger upregulation of caspase genes and weaker upregulation of hsp genes in resistant than in susceptible individuals.

Keywords

thermotolerancechlorpyrifossperm and ovary cellshsps genesapoptotic genesPlutella xylostellacost of resistanceinsecticide resistance
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 107 , Issue 4 , August 2017 , pp. 513 - 526
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

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.)

Footnotes

†

These authors contributed equally to this work.

References

Abrashev, R.I., Pashova, S.B., Stefanova, L.N., Vassilev, S.V., Dolashka-Angelova, P.A. & Angelova, M.B. (2008) Heat-shock-induced oxidative stress and antioxidant response in Aspergillus niger . Canadian Journal of Microbiology 54, 783–799.CrossRefGoogle ScholarPubMed
Agarwal, A., Saleh, R.A. & Bedaiwy, M.A. (2003) Role of reactive oxygen species in the pathophysiology of human reproduction. Fertility and Sterility 79, 829–843.CrossRefGoogle ScholarPubMed
An, M.I. & Choi, C.Y. (2010) Activity of antioxidant enzymes and physiological responses in ark shell, Scapharca broughtonii, exposed to thermal and osmotic stress: effects on hemolymph and biochemical parameters. Comparative Biochemistry and Physiology – Part B 155, 34–42.CrossRefGoogle ScholarPubMed
Atwal, A.S. (1955) Influence of temperature, photoperiod, and food on the speed of development, longevity, fecundity, and other qualities of the Diamond-Back moth Plutella maculipennis (Curtis) (Lepidoptera: Tineidae). Australian Journal of Zoology 3, 185–221.CrossRefGoogle Scholar
Bahrndorff, S., Mariën, J., Loeschcke, V. & Ellers, J. (2009) Dynamics of heat-induced thermal stress resistance and Hsp70 expression in the springtail, Orchesella cincta. Functional Ecology 23, 233–239.CrossRefGoogle Scholar
Barbehenn, R.V. (2002) Gut-based antioxidant enzymes in a polyphagous and a graminivorous grasshopper. Journal of Chemical Ecology 28, 1329–1347.CrossRefGoogle Scholar
Beere, H.M. (2004) “The stress of dying”: the role of heat shock proteins in the regulation of apoptosis. Journal of Cell Science 117, 2641–2651.CrossRefGoogle ScholarPubMed
Berticat, C., Bonnet, J., Duchon, S., Agnew, P., Weill, M. & Corbel, V. (2008) Costs and benefits of multiple resistance to insecticides for Culex quinquefasciatus mosquitoes. BMC Evolutionary Biology 8, 104.CrossRefGoogle ScholarPubMed
Bourguet, D., Guillemaud, T., Chevillon, C. & Raymond, M. (2004) Fitness cost of insecticide resistance in natural breeding sites of the mosquito Culex pipiens . Evolution 58, 128–135.Google ScholarPubMed
Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein unitizing the principle of protein dye binding. Annals of Biochemistry 72, 248–254.CrossRefGoogle Scholar
Calabria, G., Dolgova, O., Rego, C., Castañeda, L.E., Rezende, E.L., Balanyà, J., Pascual, M., Sørensen, J.G., Loeschcke, V. & Santos, M. (2012) Hsp70 protein levels and thermotolerance in Drosophila subobscura: a reassessment of the thermal co-adaptation hypothesis. Journal of Evolutionary Biology 25, 691–700.CrossRefGoogle ScholarPubMed
Castañeda, L., Baeeientos, K., Cortes, P.A., Figueroa, C., Fuentes-contreras, E., Luna-Rudloff, M., Silva, A.X. & Bacigalupe, L.D. (2011) Evaluating reproductive fitness and metabolic costs for insecticide resistance in Myzus persicae from Chile. Physiological Entomology 36, 253–260.CrossRefGoogle Scholar
Chang, H.Y. & Yang, X. (2000) Proteases for cell suicide: functions and regulation of caspases. Microbiology and Molecular Biology Reviews 64, 821–846.CrossRefGoogle ScholarPubMed
Chowdhury, I., Tharakan, B. & Bhat, G.K. (2006) Current concepts in apoptosis: the physiological suicide program revisited. Cellular and Molecular Biology Letters 11, 506–525.CrossRefGoogle ScholarPubMed
Circu, M.L. & Aw, T.Y. (2010) Reactive oxygen species, cellular redox systems, and apoptosis. Free Radical Biology and Medicine 48, 749–762.CrossRefGoogle ScholarPubMed
Colinet, H., Sinclair, B.J., Vernon, P. & Renault, D. (2015) Insects in fluctuating thermal environments. Annual Review of Entomology 60, 123–140.CrossRefGoogle ScholarPubMed
Cui, Y., Du, Y., Lu, M. & Qiang, C. (2011) Antioxidant responses of Chilo suppressalis (Lepidoptera: Pyralidae) larvae exposed to thermal stress. Journal of Thermal Biology 36, 292–297.CrossRefGoogle Scholar
Cullen, S.P. & Martin, S.J. (2009) Caspase activation pathways: some recent progress. Cell Death and Differentiation 16, 935–938.CrossRefGoogle ScholarPubMed
Daugaard, M., Rohde, M. & Jäättelä, M. (2007) The heat shock protein 70 family: highly homologous proteins with overlapping and distinct functions. FEBS Letter 581, 3702–3710.Google Scholar
DeJong, R.J., Miller, L.M., Molina-Cruz, A., Gupta, L., Kumar, S. & Barillas-Mury, C. (2007) Reactive oxygen species detoxification by catalase is a major determinant of fecundity in the mosquito Anopheles gambiae . Proceedings of the National Academy of Sciences of the United States of America 104, 2121–2126.CrossRefGoogle Scholar
Djogbénou, L., Noel, V. & Agnew, P. (2010) Costs of insensitive acetylcholinesterase insecticide resistance for the malaria vector. Anopheles gambiae homozygous for the G119S mutation. Malaria Journal l9, 12.CrossRefGoogle Scholar
Diaz-Albiter, H., Mitford, R., Genta, F., Mauricio, R.V., Anna, S., Rod, J. & Dillon, R.J. (2011) Reactive oxygen species scavenging by catalase is important for female Lutzomyia longipalpis fecundity and mortality. PLoS ONE 6, e17486.CrossRefGoogle ScholarPubMed
Fahmy, N.M. (2012) Impact of two insect growth regulators on the enhancement of oxidative stress and antioxidant efficiency of the cotton leaf worm, Spodoptera littoralis (Biosd.). Egyptian Academic Journal of Biological Science 5, 137–149.Google Scholar
Furlong, M.J., Wright, D.J. & Dosdall, L.M. (2013) Diamondback moth ecology and managements: problems, progress, and prospects. Annual Review of Entomology 58, 517–541.CrossRefGoogle ScholarPubMed
Garrido, C., Gurbuxani, S., Ravagnan, L. & Kroemer, G. (2001) Heat shock proteins: endogenous modulators of apoptotic cell death. Biochemical and Biophysical Research Communications 286, 433–442.CrossRefGoogle ScholarPubMed
Jia, F.X., Dou, W., Hu, F. & Wang, J.J. (2011) Effects of thermal stress on lipid peroxidation and antioxidant enzyme activity of oriental fruit fly, Bactrocera dorsalis (Diptera: Tephritidae). Florida Entomologist 94, 956–963.CrossRefGoogle Scholar
Kalmar, B. & Greensmith, L. (2009) Induction of heat shock proteins for protection against oxidative stress. Advanced Drug Delivery Reviews 61, 310–318.Google Scholar
Karlin, S. & Brocchieri, L. (1998) Heat shock protein family: multiple sequence comparisons, function and evolution. Journal of Molecular Evolution 47, 565–577.CrossRefGoogle ScholarPubMed
Kiang, J.G. & Tsokos, G.C. (1998) Heat shock protein 70 kDa: molecular biology, biochemistry, and physiology. Pharmacology & Therapeutics 80, 183–201.CrossRefGoogle ScholarPubMed
King, A.M. & Macrae, T.H. (2015) Insect heat shock proteins during stress and diapause. Annual Review of Entomology 60, 59–75.CrossRefGoogle ScholarPubMed
Kliot, A. & Ghanim, M. (2012) Fitness costs associated with insecticide resistance. Pest Management Science 68, 1431–1437.CrossRefGoogle ScholarPubMed
Konca, K., Lankoff, A., Banasik, A., Lisowska, H., Kuszewski, T., Gozdz, S., Kaza, Z. & Wojcik, A. (2003) A cross-platform public domain PC image-analysis program for the comet assay. Mutation Research 534, 15–20.CrossRefGoogle ScholarPubMed
Krebs, R.A. & Feder, M.E. (1997) Tissue special variation in Hsp70 expression and thermal damage in Drosophila melanogaster larvae. Journal of Experimental Biology 200, 2007–2015.Google Scholar
Kregel, K.C. (2002) Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. Journal of Applied Physiology 92, 2177–2186.CrossRefGoogle ScholarPubMed
Larionov, A., Krause, A. & Miller, W. (2005) A standard curve based method for relative real time PCR data processing. BMC Bioinformatics 6, 62.CrossRefGoogle ScholarPubMed
Li, Z.M., Liu, S.S., Liu, Y.Q. & Ye, G.Y. (2007) Temperature-related fitness costs of resistance to spinosad in the diamondback moth, Plutella xylostella (Lepidoptera: Plutelidae). Bulletin of Entomological Research 97, 627–635.CrossRefGoogle ScholarPubMed
Liu, Y.S. & Wu, J.Y. (2006) Hydrogen peroxide-induced astaxanthin biosynthesis and catalase activity in Xanthophyllomyces dendrorhous . Applied Microbiology and Biotechnology 73, 663–668.Google Scholar
Liu, X.L., Zhang, S.Z., Shan, X.Q., et al. (2007) Combined toxicity of cadmium and arsenate to wheat seedings and plant uptake and antioxidative enzyme responses to cadmium and arsenate contamination. Ecotoxicology and Environmental Safe 68, 305–313.CrossRefGoogle Scholar
Liu, F., Miyata, T., Wu, Z.J., Li, C.W., Wu, G., Zhao, S.X. & Xie, L.H. (2008) Effects of temperature on fitness costs, insecticide susceptibility and heat shock protein 70 in insecticide-resistant and susceptible Plutella xylostella . Pesticide Biochemistry and Physiology 91, 45–52.CrossRefGoogle Scholar
Mahroof, R., Zhu, K.Y., Neven, L., Sunramanyam, B. & Bai, J. (2005) Expression patterns of three heat shock protein 70 genes among developmental stages of the red flour beetle, Tribolium castaneum (Coleoptera: Tenebrionidae). Comparative Biochemistry and Physiology 141, 247–256.CrossRefGoogle ScholarPubMed
Marklund, D. & Marklund, G. (1974) Involvement of superoxide anion radical in auto-oxidation of pyrogallol. A convenient assay for superoxide dismutase. European Journal of Biochemistry 47, 469–474.CrossRefGoogle Scholar
Marsh, H.O. (1917) Life history of Plutella maculipennis, the diamondback moth. Journal of Agricultural Research 10, 1–10.Google Scholar
Martins, A.J., Ribeiro, C., Bellinato, D.F., Peixoto, A.A., Valle, D. & Lima, J.B.P. (2012) Effect of insecticide resistance on development, longevity and reproduction of field or laboratory selected Aedes aegypti populations. PLoS ONE 7, e31889.CrossRefGoogle ScholarPubMed
Monaghan, P., Metcalfe, N.B. & Torres, R. (2009) Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecology Letters 12, 75–92.CrossRefGoogle ScholarPubMed
Nover, L. & Scharf, K.D. (1997) Heat stress proteins and transcription factors. Cellular and Molecular Life Sciences 53, 80–103.CrossRefGoogle ScholarPubMed
Parsell, D.A. & Lindquist, S. (1993) The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annual Review of Genetics 27, 437–456.CrossRefGoogle ScholarPubMed
Ravagnan, L., Gurbuxani, S., Susin, S.A., Maisse, C., Daugas, E., Zamzami, N., Mak, T., Jäättelä, M., Penninger, J.M., Garrido, C. & Kroemer, G. (2001) Heat-shock protein 70 antagonizes apoptosis-inducing factor. Nature Cell Biology 3, 839–843.CrossRefGoogle ScholarPubMed
Rinehart, J.P., Yocum, G.D. & Denlinger, D.L. (2000) Developmental upregulation of inducible hsp70 transcripts, but not the cognate form, during pupal diapause in the flesh fly, Sarcophaga crassipalpis . Insect Biochemistry and Molecular Biology 30, 515–521.CrossRefGoogle ScholarPubMed
R Development Core Team. (2015) R: A language and environment for statistical computing (Version 3.2.2) [Computer software]. Available online at https://www.r-project.org/index.html Google Scholar
Schneider, K. & Schlegel, H.G. (1981) Production of superoxide radicals by soluble hydrogenase from Akcaligeneseutro phus H16. Biochemical Journal 193, 99–107.Google Scholar
Shen, Y., Gong, Y.J., Gu, J., Huang, L.H. & Feng, Q.L. (2014) Physiological effect of mild thermal stress and its induction of gene expression in the common cutworm, Spodoptera litura . Journal of Insect Physiology 61, 34–41.CrossRefGoogle ScholarPubMed
Shi, M.A., Lougarre, A., Alies, C., Fremaux, I., Tang, Z.H. & Fournier, D. (2004) Acetylcholinesterase alterations reveal the fitness cost of mutations conferring insecticide resistance. BMC Evolutionary Biology 4, 5.CrossRefGoogle ScholarPubMed
Shi, M., Wang, Y.N., Zhu, N. & Chen, X.X. (2013) Four heat shock protein genes of the endoparasitoid wasp, Cotesia vestalis, and their transcriptional profiles in relation to developmental stages and temperature. PLoS ONE 8, e59721.Google Scholar
Sim, C. & Denlinger, D.L. (2011) Catalase and superoxide dismutase-2 enhance survival and protect ovaries during overwintering diapause in the mosquito Culex pipiens . Journal of Insect Physiology 57, 628–634.CrossRefGoogle ScholarPubMed
Singh, N.P., McCoy, M.T., Tice, R.R. & Schneider, E.L. (1988) A simple technique for quantification of low levels of DNA damage in individual cells. Experimental Cell Research 17, 184–191.Google Scholar
Udaka, H., Ueda, C. & Goto, S.G. (2010) Survival rate and expression of Heat-shock protein 70 and Frost genes after temperature stress in Drosophila melanogaster lines that are selected for recovery time from temperature coma. Journal of Insect Physiology 56, 1889–1894.CrossRefGoogle ScholarPubMed
Xu, P., Xiao, J., Liu, L., Li, T. & Huang, D. (2010) Molecular cloning and characterization of four heat shock protein genes from Macrocentrus cingulum (Hymenoptera: Braconidae). Molecular Biology Reports 37, 2265–2272.CrossRefGoogle ScholarPubMed
Xu, Q., Zou, Q., Zheng, H., Zhang, F., Tang, B. & Wang, S. (2011) Three heat shock proteins from Spodoptera exigua: gene cloning, characterization and comparative stress response during heat and cold shocks. Comparative Biochemistry and Physiology – Part B 159, 92–102.Google Scholar
Yang, L.H., Huang, H. & Wang, J.J. (2010) Antioxidant responses of citrus red mite, Panonychus citri (McGregor) (Acari: Tetranychidae), exposed to thermal stress. Journal of Insect Physiology 56, 1871–1876.CrossRefGoogle ScholarPubMed
Yin, X., Wang, S., Tang, J., Hansen, D. & Lurie, S. (2006) Thermal conditioning of fifth-instar Cydia pomonella (Lepidoptera: Tortricidae) affects HSP70 accumulation and insect mortality. Physiological Entomology 31, 241–247.CrossRefGoogle Scholar
Yun, L., Chuanqing, R., Bo, L. & Yujing, Z. (2013) Effects of temperature on oviposition and longevity of adult diamondback moth (Plutella xylostella L.). Chinese Agricultural Science Bulletin 12, 035.Google Scholar
Zhang, Q. & Denlinger, D.L. (2010) Molecular characterization of heat shock protein 90, 70 and 70 cognate cDNAs and their expression patterns during thermal stress and pupal diapause in the corn earworm. Journal of Insect Physiology 56, 138–150.CrossRefGoogle Scholar
Zhang, L.J., Wang, K.F., Zhuang, H.M. & Wu, G. (2014) Identifications of cytochrome c and Apaf-1 and their mRNA expressions under heat stress in insecticide-susceptible and -resistant Plutella xylostella (Lepidoptera: Plutellidae). European Journal of Entomology 111, 457–468.CrossRefGoogle Scholar
Zhang, L.J., Jing, Y.P., Li, X.H., Li, C.W., Bourguet, D. & Wu, G. (2015 a) Temperature-sensitive fitness cost of insecticide resistance in Chinese populations of the diamondback moth Plutella xylostella . Molecular Ecology 24, 1611–1627.CrossRefGoogle ScholarPubMed
Zhang, L.J., Wu, Z.L., Wang, K.F., Liu, Q., Zhuang, H.M. & Wu, G. (2015 b) Trade-off between thermal tolerance and insecticide resistance in Plutella xylostella . Ecology & Evolution 5, 515–530.CrossRefGoogle ScholarPubMed
Zhang, L.J., Wang, K.F., Zhuang, H.M., Jing, Y.P. & Wu, G. (2015 c) Identifications of hsp70sand hsc70 and mRNA expressions under heat stress in insecticide-resistant and -susceptible Plutella xylostella (Lepidoptera: Plutellidae). European Journal of Entomology 112, 215–226.CrossRefGoogle Scholar
Zhu, K.Y., Lee, S.H. & Clark, M. (1996) A point mutation of acetylcholinesterase associated with azinphosmethyl resistance and reduced fitness in Colorado potato beetle. Pesticide Biochemistry and Physiology 55, 100–108.CrossRefGoogle ScholarPubMed
Zhuang, H.M., Wuang, K.F., Miyata, T., Wu, Z.J., Wu, G. & Xie, L.H. (2011) Identification and expression of caspase-1 gene under heat stress in insecticide-susceptible and -resistant Plutella xylostella (Lepidoptera: Plutellidae). Molecular Biology Reports 38, 2529–2539.CrossRefGoogle ScholarPubMed
Supplementary material: File

Zhang supplementary material

Tables S1-S3

Download Zhang supplementary material(File)
File 150 KB