Skip to main content
SpringerLink
Log in

Characterization of an inducible HSP70 gene in Chilo suppressalis and expression in response to environmental and biological stress

  • Original Paper
  • Published:
Cell Stress and Chaperones Aims and scope

Abstract

The highly conserved heat shock protein 70 (HSP70) contributes to survival at a cellular level and greatly enhances stress tolerance in many organisms. In this study, we isolate and characterize Cshsp702, which encodes an inducible form of HSP70 in the rice stem borer, Chilo suppressalis. Cshsp702 does not contain introns; the translational product is comprised of 629 amino acids with an isoelectric point of 5.69. Real-time quantitative PCR revealed that Cshsp702 was expressed at maximal levels in hemocytes and was minimally expressed in the midgut. Expression of Cshsp702 in response to a range of temperatures (−11 to 43 °C) indicated significant induction by extreme cold and hot temperatures, with maximum expression after 2 h at 42 °C. The induction of Cshsp702 in response to the endoparasite Cotesia chilonis was also studied; interestingly, Cshsp702 expression in C. suppressalis was significantly induced at 24 h and 5 days, which correspond to predicted times of C. chilonis feeding and growth, respectively. The potential induction of Cshsp702 as an inflammatory response due to parasitic stress is discussed. In conclusion, Cshsp702 is induced in response to both environmental and biotic stress and plays an important role in the physiological adaptation of C. suppressalis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Abdel-Latif M, Sakran T, Badawi YK, Abdel-Hady DS (2018) Influence of Moringa oleifera, extract, vitamin C, and sodium bicarbonate on heat stress-induced HSP70 expression and cellular immune response in rabbits. Cell Stress Chaperon 23:975–984

    Article  CAS  Google Scholar 

  • Borges TJ, Wieten L, Van Herwijnen MJC, Broere F, Ruurd VDZ, Bonorino C, Van Eden W (2012) The anti-inflammatory mechanisms of Hsp70. Front Immunol 3:95

    Article  PubMed  PubMed Central  Google Scholar 

  • Boutet I, Tanguy A, Rousseau S, Auffret M, Moraga D (2003) Molecular identification and expression of heat shock cognate 70 (hsc70) and heat shock protein 70 (hsp70) genes in the Pacific oyster Crassostrea gigas. Cell Stress Chaperon 8:76–85

    Article  CAS  Google Scholar 

  • Buckley BA, Place SP, Hofmann GE (2004) Regulation of heat shock genes in isolated hepatocytes from an Antarctic fish, Trematomus bernacchii. J Exp Biol 207(21):3649–3656

    Article  CAS  PubMed  Google Scholar 

  • Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubisa M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55:611–622

    Article  CAS  PubMed  Google Scholar 

  • Castillo-Davis CI, Mekhedov SL, Hartl DL, Koonin EV, Kondrashov FA (2002) Selection for short introns in highly expressed genes. Nat Genet 31(4):415–419

    Article  CAS  PubMed  Google Scholar 

  • Comeron JM (2004) Selective and mutational patterns associated with gene expression in humans: influences on synonymous composition and intron presence. Genetics 167:1293–1304

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cui YD, Lu MX, Du YZ (2010) Cloning of the heat shock protein70 gene from Chilo suppressalis and the analysis of its expression characteristics under heat stress. Acta Ecol Sin 53(8):841–848 (In Chinese)

    CAS  Google Scholar 

  • Denlinger DL, Lee RE, Yocum GD, Kukal O (1992) Role of chilling in the acquisition of cold tolerance and the capacitation to express stress proteins in diapausing pharate larvae of the gypsy moth, Lymantria dispar. Arch Insect Biochem Physiol 21:271–280

    Article  CAS  Google Scholar 

  • Deane EE, Woo NYS (2005) Cloning and characterization of the hsp70 multigene family from silver sea bream: Modulated gene expression between warm and cold temperature acclimation. Biochem Biophys Res Commun 330:776–783

    Article  CAS  PubMed  Google Scholar 

  • Duan YF, Liu P, Li JT, Wang Y, Li J, Chen P (2014) A farnesoic acid O-methyltransferase (FAMeT) from Exopalaemon carinicauda is responsive to Vibrio anguillarum and WSSV challenge. Cell Stress Chaperon 19:367–377

    Article  CAS  Google Scholar 

  • Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282

    Article  CAS  PubMed  Google Scholar 

  • Feder ME, Krebs RA (1997) Ecological and evolutionary physiology of heat shock proteins and the stress response in Drosophila: complementary insights from genetic engineering and natural variation. EXS 83:155–173

    CAS  PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39:783–791

    Article  PubMed  Google Scholar 

  • Franzellitti S, Fabbri E (2005) Differential HSP70 gene expression in the Mediterranean mussel exposed to various stressors. Biochem Biophys Res Commun 336:1157–1163

    Article  CAS  PubMed  Google Scholar 

  • Gupta RS, Singh B (1994) Phylogenetic analysis of 70 kD heat shock protein sequences suggests a chimeric origin for the eukaryotic cell nucleus. Curr Biol 4:1104

    Article  CAS  PubMed  Google Scholar 

  • Gusev O, Cornette R, Kikawada T, Okuda T (2011) Expression of heat shock protein-coding genes associated with anhydrobiosis in an African chironomid Polypedilum vanderplanki. Cell Stress Chaperones 16:81–90

    Article  CAS  PubMed  Google Scholar 

  • He JH, Chen ZF, Xu JS (1979) Zhejiang rice pests natural enemies catalogue. Zhejiang Science Press

  • Hellmann JJ (2002) The effect of an environmental change on mobile butterfly larvae and the nutritional quality of their hosts. J Anim Ecol 71(6):925–936

    Article  Google Scholar 

  • Hoffmann AA, Parsons PA (1991) Evolutionary genetics and environmental stress. Oxford University Press, New York

    Google Scholar 

  • Hoffmann AA, Sørensen JG, Loeschcke V (2003) Adaptation of Drosophila to temperature extremes: bringing together quantitative and molecular approaches. J Therm Biol 28(3):175–216

    Article  Google Scholar 

  • Huang LH, Chen B, Kang L (2007) Impact of mild temperature hardening on thermotolerance, fecundity, and Hsp gene expression in Liriomyza huidobrensis. J Insect Physiol 53:1199–1205 (in Chinese)

    Article  CAS  PubMed  Google Scholar 

  • Iwanaga S, Lee BL (2005) Recent advances in the innate immunity of invertebrate animals. J Biochem Mol Biol 38:128–150

    CAS  PubMed  Google Scholar 

  • Johnston JA, Ward CL, Kopito RR (1998) Aggresomes: a cellular response to misfolded proteins. J Cell Biol 143(7):1883–1898

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jong PRD, Schadenberg AWL, Jansen NJG, Prakken BJ (2009) Hsp70 and cardiac surgery: molecular chaperone and inflammatory regulator with compartmentalized effects. Cell Stress Chaperon 14:117–131

    Article  CAS  Google Scholar 

  • Kazuo I, Yamazaki S, Machimura N (1974) Studies on the parasite, Apanteles chilonis Munakata, on the rice stem bore, Chilo suppressalis Waiker. II. Generations in a year and the parasitism. In: Proceedings of the Association for Plant Protection of Hokuriku, pp 43–47

    Google Scholar 

  • Kim KK, Kim R, Kim SH (1998) Crystal structure of a small heat shock protein. Nature 394:595–599

    Article  CAS  PubMed  Google Scholar 

  • Koštál V, Borovánsk MT (2009) The 70 kDa heat shock protein assists during the repair of chilling injury in the insect, Pyrrhocoris apterus. PLoS ONE 2(4):e4546

    Article  CAS  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lavine MD, Strand MR (2002) Insect hemocytes and their role in immunity. Insect Biochem Mol Biol 32:1295–1309

    Article  CAS  PubMed  Google Scholar 

  • Lee S, Söderhäll K (2002) Early events in crustacean innate immunity. Fish Shellfish Immunol 12:421–437

    Article  CAS  PubMed  Google Scholar 

  • Li HB, Du YZ (2013) Molecular cloning and characterization of an Hsp90/70 organizing protein gene from Frankliniella occidentalis (Insecta: Thysanoptera, Thripidae). Gene 520:148–155

    Article  CAS  PubMed  Google Scholar 

  • Lindquist S (1986) The heat-shock response. Annu Rev Biochem 55:1151–1191

    Article  CAS  PubMed  Google Scholar 

  • Liu AYC, Bian HJ, Huang LE, Lee YK (1994) Transient cold shock induces the heat-shock response upon recovery at 37- degrees-c in human-cells. J Biol Chem 269:14768–14775

    CAS  PubMed  Google Scholar 

  • Lu MX, Du YZ, Liu ZX, Hua J, Liu PY, Li JY (2013) Diapause, signal and molecular characteristics of overwintering Chilo suppressalis. Sci Rep 3:3211

    Article  PubMed  PubMed Central  Google Scholar 

  • Lu MX, Liu ZX, Wang X, Du YZ (2012) Seasonal cold tolerance of Chilo suppressalis (Walker) in Yangzhou, China. Ann Entomol Soc America 105:479–483

    Article  Google Scholar 

  • Mayer MP, Bukau B (2005) HSP70 Chaperones: Cellular functions and molecular mechanism. Cell Mol Life Sci 62(6):670–684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McMillan DM, Fearnley SL, Rank NE, Dahlhoff EP (2005) Natural temperature variation affects larval survival, development and Hsp70 expression in a leaf beetle. Funct Ecol 19(5):844–852

    Article  Google Scholar 

  • Nolan T, Hand RE, Bustin SA (2006) Quantification of mRNA using real-time RT-PCR. Nat Protoc 1:1559–1552

    Article  CAS  PubMed  Google Scholar 

  • Odashima M, Otaka M, Jin M, Konishi N, Sato T, Kato S, Matsuhashi T, Nakamura C, Watanabe S (2002) Induction of a 72-kDa heat shock protein in cultured rat gastric mucosal cells and rat gastric mucosa by zinc I-carnosine. Dig Dis Sci 47(12):2799–2804

    Article  CAS  PubMed  Google Scholar 

  • Oyake J, Otaka M, Matsuhashi T, Jin M, Odashima M, Komatsu K, Wada I, Horikawa Y, Ohba R, Hatakeyama N, Itoh H, Watanabe S (2006) Over-expression of 70-kda heat shock protein confers protection against monochloramine-induced gastric mucosal cell injury. Life Sci 79(3):300–305

    Article  CAS  PubMed  Google Scholar 

  • Pallant JF, Bailey CM (2005) Assessment of the structure of the hospital anxiety and depression scale in musculoskeletal patients. Health and quality life outcomes 3:82

    Article  Google Scholar 

  • Pan DD, Lu MX, Li QY, Du YZ (2018) Characteristics and expression of genes encoding two small heat shock protein genes lacking introns from Chilo suppressalis. Cell Stress Chaperon 23:55–64

    Article  CAS  Google Scholar 

  • Pardue ML, Scott MP, Storti RV, Lengyel JA (1980) The heat shock response: a model system for the study of gene regulation in Drosophila. Basic Life Sci 16:41–55

    CAS  PubMed  Google Scholar 

  • Place SP, Hofmann GE (2005) Constitutive expression of a stress-inducible heat shock protein gene, hsp70, in phylogenetically distant Antarctic fish. Polar Biol 28:261–267

    Article  Google Scholar 

  • Qin J, Zhang XX, Gao P, Lu MX, Du YZ (2017) Cloning and expression profile of a novel, thermal, inducible HSP70 gene in insects. Chin Bull Emtomol 54:380–391 (in Chinese)

    Google Scholar 

  • Queitsch C, Sangster TA, Lindquist S (2002) Hsp90 as a capacitor of phenotypic variation. Nature 417:618–624

    Article  CAS  PubMed  Google Scholar 

  • Robich RM, Rinehart JP, Denlinger DL (2006) Enhanced cold and desiccation tolerance in diapausing adults of Culex pipiens, and a role for Hsp70 in response to cold shock but not as a component of the diapause program. J Med Entomol 43(4):713–722

    Article  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Schmittgen TD, Tamura KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1101–1108

    Article  CAS  PubMed  Google Scholar 

  • Shang ZZ, Wang YS, Zhou YH (1979) Study on the feeding method of Chilo suppressalis. Acta Entomologica Sinica (02):164–168 + 239 (in Chinese)

  • Sonoda S, Fukumoto K, Izumi Y, Yoshida H, Tsumuki H (2006) Cloning of heat shock protein genes (hsp90 and hsc70) and their expression during larval diapause and cold tolerance acquisition in the rice stem borer, Chilo suppressalis Walker. Arch Insect Biochem 63:36–47

    Article  CAS  Google Scholar 

  • Sørensen JG, Kristensen TN, Loeschcke V (2003) The evolutionary and ecological role of heat shock proteins. Ecol Lett 6:1025–1037

    Article  Google Scholar 

  • Sørensen JG, Norry FM, Scannapieco AC, Loeschcke V (2005) Altitudinal variation for stress resistance traits and thermal adaptation in adult Drosophila buzzatii from the New World. J Evol Biol 18(4):829–837

    Article  PubMed  Google Scholar 

  • Vazquez L, Alpuche J, Maldonado G, Agundis C, Pereyra-Morales A, Zenteno E (2009) Immunity mechanisms in crustaceans. Innate Immunol 15:179–188

    Article  CAS  Google Scholar 

  • Wachstein J, Tischer S, Figueiredo C, Limbourg A, Falk C, Immenschuh S, Blasczyk R, Eiz-Vesper B (2012) HSP70 enhances immunosuppressive function of CD4 + CD25 + FoxP3+ T regulatory cells and cytotoxicity in CD4 + CD25- T cells. PLoS One 7(12):e51747

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Whittall T, McGowan E, Younson J, Kelly C, Bergmeier LA, Singh M, Lehner T (2005) Identification of stimulating and inhibitory epitopes within the heat shock protein 70 molecule that modulate cytokine production and maturation of dendritic cells. J Immunol 174:3306–3316

    Article  CAS  PubMed  Google Scholar 

  • Wei Y, Zhao X, Kariya Y, Fukata H, Teshigawara K, Uchida A (1996) Induction of autologous tumor killing by heat treatment of fresh human tumor cells: involvement of gamma delta T cells and heat shock protein 70. Cancer Res 56(5):1104–1110

    CAS  PubMed  Google Scholar 

  • Wu SF, Sun FD, Qi YX, Yao Y, Fang Q, Huang J, Stanley D, Ye GY (2013) Parasitization by Cotesia chilonis influences gene expression in fat body and hemocytes of Chilo suppressalis. PLoS ONE 8:e74309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu J, Lu MX, Cui YD, Du YZ (2017) Selection and evaluation of reference genes for expression analysis using qrt-pcr in Chilo suppressalis (Lepidoptera: Pyralidae). J Econ Entomol 110(2):683–691

    CAS  PubMed  Google Scholar 

  • Yin C, Liu Y, Liu J, Xiao H, Huang S, Lin Y, Han Z, Li F (2014) ChiloDB: a genomic and transcriptome database for an important rice insect pest Chilo suppressalis. Database 15:92–108

    Google Scholar 

  • Yocum GD (2001) Differential expression of two HSP70 transcripts in responses to cold shock, thermoperiod, and adult diapause in the Colorado potato beetle. J Insect Physiol 47(10):1139–1145

    Article  CAS  PubMed  Google Scholar 

  • Yocum GD, Joplin KH, Denlinger DL (1991) Expression of heat-shock proteins in response to high and low-temperature extremes in diapausing pharate larvae of the gypsy moth, Lymantria dispar. Arch Insect Biochem Physiol 18:239–249

    Article  CAS  Google Scholar 

  • Zuckerkandl E, Pauling L (1965) Evolutionary divergence and convergence in proteins. Academic Press, New York

    Book  Google Scholar 

Download references

Acknowledgments

This research was funded by the National Key R&D Program of China (2017YFD0200400) and the National Natural Science Foundation of China (31401733). We sincerely thank Dr. Carol L. Bender for editing and providing comments on the manuscript. We express our deep gratitude to the Testing Center of Yangzhou University.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Author information

Authors and Affiliations

  1. School of Horticulture and Plant Protection & Institute of Applied Entomology, Yangzhou University, Yangzhou, 225009, China

    Peng Gao, Ming-Xing Lu, Dan-Dan Pan & Yu-Zhou Du

  2. Jiangsu Key Laboratory of Crop Genetics and Physiology/Co-Innovation Center for Modern Production Technology of Grain Crops, Yangzhou University, Yangzhou, 225009, China

    Yu-Zhou Du

Authors
  1. Peng Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ming-Xing Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dan-Dan Pan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yu-Zhou Du
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Ming-Xing Lu or Yu-Zhou Du.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gao, P., Lu, MX., Pan, DD. et al. Characterization of an inducible HSP70 gene in Chilo suppressalis and expression in response to environmental and biological stress. Cell Stress and Chaperones 25, 65–72 (2020). https://doi.org/10.1007/s12192-019-01047-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12192-019-01047-2

Keywords

Search

Navigation