Abstract
In this study, we cloned a full-length cDNA of heat shock protein (HSP) gene of Apolygus lucorum (Meyer-Dür) [AlHSP90, KC109781] and investigated its expression in response to temperature and pesticide stresses. The open reading frame (ORF) of AlHSP90 is 2,169 bp in length, encoding a 722 amino acid polypeptide with a predicted molecular weight of 82.99 kDa. Transcriptional and translational expression profiles of AlHSP90 under extreme temperature or pesticide stresses were examined by fluorescent real-time quantitative PCR and Western blot. Results showed that the expression profiles of AlHSP90 protein were in high agreement with those of AlHSP90 RNA and indicated that AlHSP90 was not only an important gene for A. lucorum adults in response to extremely high temperature, but also involved in the resistance or tolerance to cyhalothrin, imidacloprid, chlorpyrifos, and emamectin benzoate, especially for female adults to emamectin benzoate and for male adults to cyhalothrin. Transcriptional results of AlHSP90 also confirmed that AlHSP90 was an important gene involved in the resistance or tolerance to both temperature and pesticide stresses. In addition, our study also revealed that ∼24 °C may be the suitable temperature range for A. lucorum survival, which is also confirmed by the results of the expression of AlHSP90, the nymph mortality, and the intrinsic rate of increase (r m) when A. lucorum is reared at six different temperatures. Therefore, these studies are significant in elucidating the AlHSP90 in response to temperature and pesticide stresses and would provide guidance for A. lucorum management with different pesticides or temperatures in fields.
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Benoit JB, Lopez-Martinez G, Teets NM, Phillips SA, Denlinger DL (2009) Responses of the bed bug, Cimex lectularius, to temperature extremes and dehydration: levels of tolerance, rapid cold hardening and expression of heat shock proteins. Med Vet Entomol 23:418–425
Buchner J (1999) Hsp90 & Co.—a holding for folding. Trends Biochem Sci 24:136–141
Byrd CA, Bornmann W, Erdjument-Bromage H, Tempst P, Pavletich N, Rosen N, Nathan CF, Ding A (1999) Heat shock protein 90 mediates macrophage activation by Taxol and bacterial lipopolysaccharide. Proc Natl Acad Sci U S A 96:5645–5650
Caplan AJ (1999) Hsp90’s secrets unfold: new insights from structural and functional studies. Trends Cell Biol 9:262–268
Chen CK, Li XF, Han ZJ (2000) Method for monitoring insecticide resistance in rice stem borer Chilo suppressalis Walker and relative susceptible baseline data. J Nanjing Agric Univ 23:25–28
Csemely P, Schnaider T, Soti C, Prohaszka Z, Nardai G (1998) The 90-kDa molecular chaperone family: structure, function, and clinical application. Compr Rev Pharmacol Ther 79:129–168
FAO (1980) Method for larvae of the rice stem borer (Chilo suppressalis Walker), FAO Method No. 3 [A], in: Pest resistance to pesticides and crop loss assessment-2[2]. FAO, Rome, pp. 25–28
Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282
Feng H, Wang L, Liu Y, He L, Li M, Lu W, Xue C (2010) Molecular characterization and expression of a heat shock protein gene (HSP90) from the carmine spider mite, Tetranychus cinnabarinus (Boisduval). J Insect Sci 10:112
Finney DJ (1971) Probit analysis, 3rd edn. Cambridge University Press, Cambridge
Fuertesa MA, Peŕezb JM, Sotoa M, Menéndezc M, Alonsoa C (2004) Thermodynamic stability of the C-terminal domain of the human inducible heat shock protein 70. Biochim Biophys Acta 1699:45–56
Goto SG, Yoshida KM, Kimura MT (1998) Accumulation of Hsp70 mRNA under environmental stresses in diapausing and nondiapausing adults of Drosophila triauraria. J Insect Physiol 44:1009–1015
Govindan K, Gunasekaran K, Kuttalam S (2012) Evaluation of Indian transgenic Bt cotton and non Bt cotton against Spodoptera litura Fab. (Noctuidae: Lepidoptera) fourth and fifth instar larvae. J Biol Pest 5:171–177
Graefe SE, Wiesgigl M, Gaworski I, Macdonald A, Clos J (2002) Inhibition of HSP90 in Trypanosoma cruzi induces a stress response but no stage differentiation. Eukaryotic Cell 1:936–943
Gupta RS (1995) Phylogenetic analysis of the 90 kD heat shock family of protein sequences and an examination of the relationship among animals, plants, and fungi species. Mol Biol Evol 12:1063–1073
Hao H, Naomoto Y, Bao X, Watanabe N, Sakurama K, Noma K, Motoki T, Tomono Y, Fukazawa T, Shirakawa Y, Yamatsuji T, Matsuoka J, Takaoka M (2010) HSP90 and its inhibitors. Oncol Rep 23:1483–1492
Huang LH, Kang L (2007) Cloning and inter-specific altered expression of heat shock protein genes in two leaf miner species in response to thermal stress. Insect Mol Biol 16:491–500
Huang LH, Wang CZ, Kang L (2009) Cloning and expression of five heat shock protein genes in relation to cold hardening and development in the leaf miner, Liriomyza sativa. J Insect Physiol 55:279–285
Jiang XF, Zhai HF, Wang L, Luo LZ, Sappington TW, Zhang L (2012) Cloning of the heat shock protein 90 and 70 genes from the beet armyworm, Spodoptera exigua, and expression characteristics in relation to thermal stress and development. Cell Stress Chaperones 17:67–80
Jones C, Anderson S, Singha UK, Chaudhuri M (2008) Protein phosphatase 5 is required for Hsp90 function during proteotoxic stresses in Trypanosoma brucei. Parasitol Res 102:835–844
Knorr E, Vilcinskas A (2011) Post-embryonic functions of HSP90 in Tribolium castaneum include the regulation of compound eye development. Dev Genes Evol 221:357–362
LeOra Software (1987) POLO-PC. A user’s guide to probit analysis or logit analysis. LeOra Software, Berkeley
Li HB, Du YZ (2013) Molecular cloning and characterization of an Hsp90/70 organizing protein gene from Frankliniella occidentalis (Insecta: Thysanoptera, Thripidae). Gene published online
Li Z, Srivastava P (2004) Heat-shock proteins. Curr Protoc Immunol Appendix 1: Appendix 1 T
Li GP, Feng HQ, McNeil JN, Liu B, Chen PY, Qiu F (2011) Impacts of transgenic Bt cotton on a non-target pest, Apolygus lucorum (Meyer-Dür) (Hemiptera: Miridae), in northern China. Crop Prot 30:1573–1578
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods 25:402–408
Lu YH, Wu KM (2008) Biology and control of the mirids. Golden Shield, Beijing
Lu YH, Liang GM, Wu KM (2007) Advances in integrated management of cotton mirids. Plant Prot 33:10–15
Lu YH, Wu KM, Jiang YY, Xia B, Li P, Feng HQ, Wyckhuys KAG, Guo YY (2010) Mirid bug outbreaks in multiple crops correlated with wide-scale adoption of Bt cotton in China. Science 328:1151–1154
Men XY, Yu Y, Zhang AS, Li LL, Zhang JT, Ge F (2008) Life table of the laboratory population of Lygus lucorum Meyer-Dür (Hemiptera: Miridae) at different temperatures. Acta Entomol Sin 51:1216–1219
Minami Y, Kimura Y, Kawasaki H, Suzuki K, Yahara I (1994) The carboxy-terminal region of mammalian HSP90 is required for its dimerization and function in vivo. Mol Cell Biol 14:1459–1464
Nemoto T, Ohara-Nemoto Y, Ota M, Takagi T, Yokoyama K (1995) Mechanism of dimer formation of the 90-kDa heat-shock protein. Eur J Biochem 233:1–8
Patil NS, Lole KS, Deobagkar DN (1996) Adaptive larval thermo-tolerance and induced cross-tolerance to propoxur insecticide in mosquitoes Anopheles stephensi and Aedes aefypti. Med Vet Entomol 10:277–282
Pisa V, Cozzolino M, Gargiulo S, Ottone C, Piccioni F, Monti M, Gigliotti S, Talamo F, Graziani F, Pucci P, Verrotti AC (2009) The molecular chaperone Hsp90 is a component of the capbinding complex and interacts with the translational repressor Cup during Drosophila oogenesis. Gene 432:67–74
Prodromou C, Pearl LH (2003) Structure and functional relationships of Hsp90. Curr Cancer Drug Targets 3:301–323
Shu YH, Du Y, Wang JW (2011) Molecular characterization and expression patterns of Spodoptera litura heat shock protein 70/90, and their response to zinc stress. Comp Biochem Physiol 158A:102–110
Song Y, Fee L, Lee TH, Wharton RP (2007) The molecular chaperone Hsp90 is required for mRNA localization in Drosophila melanogaster embryos. Genetics 176:2213–2222
Song NN, Ding WH, Chu SY, Zhao J, Dong X, Di BB, Tang CS (2012) Urotensin II stimulates vascular endothelial growth actor secretion from adventitial fibroblasts in synergy with angiotensin II. Vasc Med 76:1267–1273
Sonoda S, Tsumuki H (2007) Induction of heat shock protein genes by chlorfenapyr in cultured cells of the cabbage armyworm, Mamestra brassicae. Pestic Biochem Physiol 89:185–189
Sonoda S, Ashfaq M, Tsumuki H (2006) Cloning and nucleotide sequencing of three heat shock protein genes (hsp90, hsc70, and hsp19.5) from the diamondback moth, Plutella xylostella (L.) and their expression in relation to developmental stage and temperature. Arch Insect Biochem Physiol 62:80–90
Sonoda S, Ashfaq M, Tsumuki H (2007) A comparison of heat shock protein genes from cultured cells of the cabbage armyworm, Mamestra brassicae, in response to heavy metals. Arch Insect Biochem Physiol 65:210–222
Tachibana SI, Numata H, Goto SG (2005) Gene expression of heat-shock proteins (Hsp23, Hsp70 and Hsp90) during and after larval diapause in the blow fly Lucilia sericata. J Insect Physiol 51:641–647
Taipale M, Jarosz DF, Lindquist S (2010) Hsp90 at the hub of protein homeostasis: emerging mechanistic insights. Nat Rev Mol Cell Biol 11:515–528
Tsutsumi S, Neckers L (2007) Extracellular heat shock protein 90: a role for a molecular chaperone in cell motility and cancer metastasis. Cancer Sci 98:1536–1539
Wang H, Li K, Zhu JY, Fang Q, Ye GY (2012) Cloning and expression pattern of heat shock protein genes from the endoparasitoid wasp, Pteromalus puparum in response to environmental stresses. Arch Insect Biochem Physiol 79:247–263
Wright MK, Brandt SL, Coudron TA, Wagner RM, Habibi J, Backus EA, Huesinge JE (2006) Characterization of digestive proteolytic activity in Lygus hesperus Knight (Hemiptera: Miridae). J Insect Physiol 52:717–728
Wu KM, Lu YH, Feng HQ, Jiang YY, Zhao JZ (2008) Suppression of cotton bollworm in multiple crops in China in areas with Bt toxin containing cotton. Science 5896:1676–1678
Xu J, Shu J, Zhang Q (2010) Expression of the Tribolium castaneum (Coleoptera: Tenebrionidae) hsp83 gene and its relation to oogenesis during ovarian maturation. J Genet Genom 37:513–522
Young JC, Moarefi I, Hartl FU (2001) Hsp90: a specialized but essential protein-folding tool. J Cell Biol 154:267–273
Yue L, Karr TL, Nathan DF, Swift H, Srinivasan S, Lindquist S (1999) Genetic analysis of viable Hsp90 alleles reveals a critical role in Drosophila spermatogenesis. Genetics 151:1065–1079
Zhao HX, Tan YA, Xiao LB, Wu GQ, Bai LX (2012) Effects of different temperatures on the development and reproduction of Apolygus lucorum. Chin J Appl Entomol 49:585–590
Acknowledgments
This work was supported by the Open Fund in State Key Laboratory for Biology of Plant Diseases and Insect Pests (SKL2012OP03), the Natural Science Fund of Jiangsu Province (BK20130717), the Special Fund for Agro-scientific Research in the Public Interest of China (201103012-04), and the National Key Technology Research and Development Program of China (2012BAD19B05-003). We thank Professor G.U. Zhong Yan for providing the pesticide AI for this study.
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Yang Sun and Yang Sheng equally contributed to this paper.
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Sun, Y., Sheng, Y., Bai, L. et al. Characterizing heat shock protein 90 gene of Apolygus lucorum (Meyer-Dür) and its expression in response to different temperature and pesticide stresses. Cell Stress and Chaperones 19, 725–739 (2014). https://doi.org/10.1007/s12192-014-0500-0
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DOI: https://doi.org/10.1007/s12192-014-0500-0