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Identification of multiple small heat-shock protein genes in Plutella xylostella (L.) and their expression profiles in response to abiotic stresses

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Cell Stress and Chaperones Aims and scope

Abstract

We identify and characterize 14 small heat-shock protein (sHSP) genes from the diamondback moth (DBM), Plutella xylostella (L.), a destructive pest. Phylogenetic analyses indicate that, except for sHSP18.8 and sHSP19.22, the other 12 DBM sHSPs belong to five known insect sHSP groups. Developmental expression analysis revealed that most sHSPs peaked in the pupal and adult stages. The transcripts of sHSPs display tissue specificity with two exhibiting constitutive expression in four tested tissues. Expression of sHSP18.8 in fourth instar larvae is not induced by the tested abiotic stressors, and unless sHSP21.8 is not sensitive to thermal stress, 12 sHSPs are significantly up-regulated. The messenger RNA (mRNA) levels of all sHSPs are reduced under oxidative stress. Food deprivation leads to significant down-regulation of three sHSPs. The majority of sHSPs show expression variation to various heavy metals, whereas mRNA abundances of sHSP22.1 and sHSP 28.9 are reduced by four heavy metals. The responses of sHSPs to indoxacarb and cantharidin are varied. Beta-cypermethrin and chlorfenapyr exposure results in an increase of 13 sHSP transcripts and a reduction of 12 sHSP transcripts, respectively. These results show that different sHSPs might play distinct roles in the development and regulation of physiological activities, as well as in response to various abiotic stresses of DBM.

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References

  • Aevermann BD, Waters ER (2008) A comparative genomic analysis of the small heat shock proteins in Caenorhabditis elegans and briggsae. Genetica 133:307–319

    Article  CAS  PubMed  Google Scholar 

  • Basha E, Friedrich KL, Vierling E (2006) The N-terminal arm of small heat shock proteins is important for both chaperone activity and substrate specificity. J Biol Chem 281:39943–39952

    Article  CAS  PubMed  Google Scholar 

  • Basha E, O’Neill H, Vierling E (2012) Small heat shock proteins and α-crystallins: dynamic proteins with flexible functions. Trends Biochem Sci 37:106–117

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Basha E, Jones C, Blackwell AE, Cheng G, Waters ER, Samsel KA, Siddique M, Pett V, Wysocki V, Vierling E (2013) An unusual dimeric small heat shock protein provides insight into the mechanism of this class of chaperones. J Mol Biol 425:1683–1696

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Colinet H, Lee SF, Hoffmann A (2010) Temporal expression of heat shock genes during cold stress and recovery from chill coma in adult Drosophila melanogaster. FEBS J 277:174–185

    Article  CAS  PubMed  Google Scholar 

  • Concha C, Edman RM, Belikoff EJ, Schiemann AH, Carey B, Scott MJ (2012) Organization and expression of the Australian sheep blowfly (Lucilia cuprina) hsp23, hsp24, hsp70 and hsp83 genes. Insect Mol Biol 21:169–180

    Article  CAS  PubMed  Google Scholar 

  • Franck E, Madsen O, van Rheede T, Ricard G, Huynen MA, de Jong WW (2004) Evolutionary diversity of vertebrate small heat shock proteins. J Mol Evol 59:792–805

    Article  CAS  PubMed  Google Scholar 

  • Garczynski SF, Unruh TR, Guédot C, Neven LG (2011) Characterization of three transcripts encoding small heat shock proteins expressed in the codling moth, Cydia pomonella (Lepidoptera: Tortricidae). Insect Sci 18:473–483

    Article  CAS  Google Scholar 

  • Gehring WJ, Wehner R (1995) Heat shock protein synthesis and thermotolerance in Cataglyphis, an ant from the Sahara desert. Proc Natl Acad Sci U S A 92:2994–2998

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gkouvitsas T, Kontogiannatos D, Kourti A (2008) Differential expression of two small Hsps during diapause in the corn stalk borer Sesamia nonagrioides (Lef.). J Insect Physiol 54:1503–1510

    Article  CAS  PubMed  Google Scholar 

  • Gu J, Huang LX, Shen Y, Huang LH, Feng QL (2012) Hsp70 and small Hsps are the major heat shock protein members involved in midgut metamorphosis in the common cutworm, Spodoptera litura. Insect Mol Biol 5:535–543

    Article  Google Scholar 

  • Haslbeck M (2002) sHsps and their role in the chaperone network. Cell Mol Life Sci 59:1649–1657

    Article  CAS  PubMed  Google Scholar 

  • Haslbeck M, Franzmann T, Weinfurtner D, Buchner J (2005) Some like it hot: the structure and function of small heat-shock proteins. Nat Struct Mol Biol 12:842–846

    Article  CAS  PubMed  Google Scholar 

  • Hayward SAL, Pavlides SC, Tammariello SP, Rinehart JP, Denlinger DL (2005) Temporal expression patterns of diapause-associated genes in flesh fly pupae from the onset of diapause through post-diapause quiescence. J Insect Physiol 51:631–640

    Article  CAS  PubMed  Google Scholar 

  • Huang LH, Kang L (2007) Cloning and interspecific altered expression of heat shock protein genes in two leafminer species in response to thermal stress. Insect Mol Biol 16:491–500

    Article  PubMed  Google Scholar 

  • 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 leafminer, Liriomyza sativa. J Insect Physiol 55:279–285

    Article  CAS  PubMed  Google Scholar 

  • Jouraku A, Yamamoto K, Kuwazaki S, Urio M, Suetsugu Y, Narukawa J, Miyamoto K, Kurita K, Kanamori H, Katayose Y, Matsumoto T, Noda H (2013) KONAGAbase: a genomic and transcriptomic database for the diamondback moth, Plutella xylostella. BMC Genomics 14:464

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kappé G, Franck E, Verschuure P, Boelens WC, Leunissen JA, de Jong WW (2003) The human genome encodes 10 α-crystalline-related small heat shock proteins: HspB1-10. Cell Stress Chaperones 8:53–61

    Article  PubMed Central  PubMed  Google Scholar 

  • Kokolakis G, Kritsidima M, Tkachenko T, Mintzas AC (2009) Two hsp23 genes in the Mediterranean fruit fly, Ceratitis capitata: structural characterization, heat shock regulation and developmental expression. Insect Mol Biol 18:171–181

    Article  CAS  PubMed  Google Scholar 

  • Kriehuber T, Rattei T, Weinmaier T, Bepperling A, Haslbeck M, Buchner J (2010) Independent evolution of the core domain and its flanking sequences in small heat shock proteins. FASEB J 24:3633–3642

    Article  CAS  PubMed  Google Scholar 

  • Li ZW, Li X, Yu QY, Xiang ZH, Kishino H, Zhang Z (2009) The small heat shock protein (sHSP) genes in the silkworm, Bombyx mori, and comparative analysis with other insect sHSP genes. BMC Evol Biol 9:215

    Article  PubMed Central  PubMed  Google Scholar 

  • Liu Z, Xi D, Kang M, Guo X, Xu B (2012) Molecular cloning and characterization of Hsp27. 6: the first reported small heat shock protein from Apis cerana cerana. Cell Stress Chaperones 17:539–551

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lu MX, Hua J, Cui YD, Du YZ (2014) Five small heat shock protein genes from Chilo suppressalis: characteristics of gene, genomic organization, structural analysis, and transcription profiles. Cell Stress Chaperones 19:91–104

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Martínez-Paz P, Morales M, Martín R, Martínez-Guitarte JL, Morcillo G (2013) Characterization of the small heat shock protein Hsp27 gene in Chironomus riparius (Diptera) and its expression profile in response to temperature changes and xenobiotic exposures. Cell Stress Chaperones. doi:10.1007/s12192-013-0479-y

    PubMed  Google Scholar 

  • Nguyen TTA, Michaud D, Cloutier C (2009) A proteomic analysis of the aphid Macrosiphum euphorbiae under heat and radiation stress. Insect Biochem Mol Biol 39:20–30

    Article  CAS  PubMed  Google Scholar 

  • Poulain P, Gelly JC, Flatters D (2010) Detection and architecture of small heat shock protein monomers. PLoS One 5:e9990

    Article  PubMed Central  PubMed  Google Scholar 

  • Quinlan R (2002) Cytoskeletal competence requires protein chaperones. Prog Mol Subcell Biol 28:219–234

    Article  CAS  PubMed  Google Scholar 

  • Rinehart JP, Li A, Yocum GD, Robich RM, Hayward SA, Denlinger DL (2007) Up-regulation of heat shock proteins is essential for cold survival during insect diapause. Proc Natl Acad Sci U S A 104:11130–11137

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sakano D, Li B, Xia Q, Yamamoto K, Fujii H, Aso Y (2006) Genes encoding small heat shock proteins of the silkworm, Bombyx mori. Biosci Biotechnol Biochem 70:2443

    Article  CAS  PubMed  Google Scholar 

  • Sang W, Ma WH, Qiu L, Zhu ZH, Lei CL (2012) The involvement of heat shock protein and cytochrome P450 genes in response to UV-A exposure in the beetle Tribolium castaneum. J Insect Physiol 58:830–836

    Article  CAS  PubMed  Google Scholar 

  • Saravanakumar R, Ponnuvel KM, Qadri SMH (2008) Expression of metabolic enzyme genes and heat-shock protein genes during embryonic development in diapause and non-diapause egg of multivoltine silkworm Bombyx mori. Biologia 63:737–744

    Article  CAS  Google Scholar 

  • Shen Y, Gu J, Huang LH, Zheng SC, Liu L, Xu WH, Feng QL, Kang L (2011) Cloning and expression analysis of six small heat shock protein genes in the common cutworm, Spodoptera litura. J Insect Physiol 57:908–914

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 65:210–222

    Article  CAS  Google Scholar 

  • Sun Y, MacRae TH (2005) Small heat shock proteins: molecular structure and chaperone function. Cell Mol Life Sci 62:2460–2476

    Article  CAS  PubMed  Google Scholar 

  • Takahashi KH, Rako L, Takano-Shimizu T, Hoffmann AA, Lee SF (2010) Effects of small Hsp genes on developmental stability and microenvironmental canalization. BMC Evol Biol 10:284

    Article  PubMed Central  PubMed  Google Scholar 

  • Trisyono A, Whalon ME (1997) Fitness costs of resistance to Bacillus thuringiensis in Colorado potato beetle (Coleoptera: Chrysomelidae). J Econ Entomol 90:267–271

    Google Scholar 

  • Tsvetkova NM, Horvath I, Torok Z, Wolkers WF, Balogi Z, Shigapova N, Crowe LM, Tablin F, Vierling E, Crowe JH, Vigh L (2002) Small heat shock proteins regulate membrane lipid polymorphism. Proc Natl Acad Sci U S A 99:13504–13509

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • van Montfort RL, Basha E, Friedrich KL, Slingsby C, Vierling E (2001) Crystal structure and assembly of a eukaryotic small heat shock protein. Nat Struct Mol Biol 8:1025–1030

    Article  Google Scholar 

  • van Montfort R, Slingsby C, Vierling E (2002) Structure and function of the small heat shock protein/alpha-crystallin family of molecular chaperones. Adv Protein Chem 59:105–156

    Article  Google Scholar 

  • 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 79:247–263

    Article  CAS  Google Scholar 

  • Waters ER, Rioflorido I (2007) Evolutionary analysis of the small heat shock proteins in five complete algal genomes. J Mol Evol 65:162–174

    Article  CAS  PubMed  Google Scholar 

  • Waters ER, Aevermann BD, Sanders-Reed Z (2008) Comparative analysis of the small heat shock proteins in three angiosperm genomes identifies new subfamilies and reveals diverse evolutionary patterns. Cell Stress Chaperones 13:127–142

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhao L, Jones WA (2012) Expression of heat shock protein genes in insect stress responses. Invertebr Surviv J 9:93–101

    Google Scholar 

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Acknowledgments

We sincerely thank Prof. John Richard Schrock (Emporia State University, USA) for revising the manuscript. This research is supported by the Special Fund for the Public Interest (Agriculture) (200903052) by The Ministry of Science and Technology and The Ministry of Agriculture of China and the ‘13115’ Sci-Tech Innovation Project of Shaanxi Province (2007ZDKG-14).

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  1. Key Laboratory of Plant Protection Resources and Pest Management, Ministry of Education, College of Plant Protection, Northwest A & F University, Yangling, Shaanxi, China

    Xi’en Chen & Yalin Zhang

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  1. Xi’en Chen
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  2. Yalin Zhang
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Correspondence to Yalin Zhang.

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Chen, X., Zhang, Y. Identification of multiple small heat-shock protein genes in Plutella xylostella (L.) and their expression profiles in response to abiotic stresses. Cell Stress and Chaperones 20, 23–35 (2015). https://doi.org/10.1007/s12192-014-0522-7

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  • DOI: https://doi.org/10.1007/s12192-014-0522-7

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