Skip to main content
SpringerLink
Log in

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

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

Abstract

Two full-length cDNAs of heat shock protein (HSP) genes (Se-hsp90 and Se-hsp70) were cloned from the beet armyworm, Spodoptera exigua, and their expression was investigated in relation to cold shock, heat shock, and development. The open reading frames of Se-hsp90 and Se-hsp70 are 2,154 and 2,004 bp in length, encoding polypeptides of 717 and 667 amino acids with a molecular mass of 82.6 and 72.5 kDa, respectively. Both genes showed high similarity to their counterparts in other species. Transcriptional expression profiles revealed that both genes were significantly up-regulated under thermal stress. However, the temperature at which expression level became significantly higher than that of controls varied between genes. Intensity of response to temperature was more intense for Se-hsp70 than for Se-hsp90, regardless of temperature or developmental stage. However, intensities of response to temperature of either Se-hsp90 or Se-hsp70 varied with developmental stage. The basal expression of both genes was highest in young larvae and decreased with age. Translational expression of Se-Hsp70 was observed by using Western blot, the expression profiles of Se-Hsp70 protein were in high agreement with those of Se-hsp70 RNA under heat or cold stress in larvae and pupae. However, it does not completely accord with that of Se-hsp70 RNA expression during development without thermal stress. These results indicated that, in addition to heat shock responses, both Se-hsp90 and Se-hsp70 might be involved in development.

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
Fig. 8

Similar content being viewed by others

References

  • Adamczyk JJ Jr, Williams MR, Reed JT, Hubbard DW, Hardee DD (2003) Spatial and temporal occurrence of beet armyworm (Lepidoptera: Noctuidae) moths in Mississippi. Fla Entomol 86:229–232

    Article  Google Scholar 

  • Burris E, Graves JB, Leonard BR, White CA (1994) Beet armyworms (Lepidoptera: Noctuidae) in northeast Louisiana: observations on an uncommon insect pest. Fla Entomol 77:454–459

    Article  Google Scholar 

  • Chen B, Kayukawa T, Monteiro A, Ishikawa Y (2006) Cloning and characterization of the HSP70 gene, and its expression in response to diapauses and thermal stress in the onion maggot, Delia antique. J Biochem Mol Biol 39:749–758

    Article  PubMed  CAS  Google Scholar 

  • Cheng YX, Luo LZ, Jiang XF, Zhang L, Niu CY (2010) Expression of pheromone biosynthesis activating neuropeptide and its receptor (PBANR) mRNA in adult female Spodoptera exigua (Lepidoptera: Noctuidae). Arch Insect Biochem Physiol 75:13–27

    Article  PubMed  CAS  Google Scholar 

  • Chu YI, Wu HT (1992) Studies on emergence, copulation and oviposition of adult beet armyworm (Spodoptera exigua Hübner). Chin J Entomol 12:91–99

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Feder JH, Rossi JM, Solomon J, Solomon N, Lindquist S (1992) The consequences of expressing hsp70 in Drosophila cells at normal temperatures. Gene Dev 6:1402–1413

    Article  PubMed  CAS  Google Scholar 

  • Feng HQ, Wu KM, Cheng DF, Guo YY (2003) Radar observation of the autumn migration of the beet armyworm, Spodoptera exigua, and other moths in northern. China Bull Entomol Res 93:115–124

    Google Scholar 

  • French RA (1968) Migration of Laphygma exigua to the British Isles in relation to Large-Seale Weather System. J Anim Ecol 38:199–210

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Fye RE, Carranza RL (1973) Cotton pest: overwintering of three Lepidopterous species in Arizona. J Econ Entomol 66:657–659

    Google Scholar 

  • Garbuz D, Evgenev MB, Feder ME, Zatsepina OG (2003) Evolution of the thermotolerance and heat-shock response: evidence from inter/intra-specific comparison and interspecific hybridization in the virilis species group of Drosophila: I. Thermal phenotype. J Exp Biol 206:2392–2408

    Article  Google Scholar 

  • Garbuz D, Zatsepina OG, Przhiboro AA, Yushenova I, Guzhova IV, Evgenev MB (2008) Lavae of related Diptera species from thermally contrasting habitats exhibit continuous up-regulation of heat shock proteins and high thermotolerance. Mol Ecol 17:4763–4777

    Article  PubMed  CAS  Google Scholar 

  • Gill KS (1987) Insect pests of linseed. In: Linseed. Indian Council of Agricultural Research, New Delhi, India, pp 342–355

  • Goto SG, Kimura MT (1998) Heat and cold shock responses and temperature adaptations in subtropical and temperate species of Drosophila. J Insect Physiol 44:1233–1239

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Gupta RS (1995) Phylogenetic analysis of the 90 kDa heat shock family of protein sequences and an examination of the relationship among animals, plants, and fungi species. Mol Biol Evol 12:1063–1073

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

    Article  PubMed  CAS  Google Scholar 

  • Huang LH, Wang HS, Kang L (2008) Different evolutionary lineages of large and small heat shock proteins in eukaryotes. Cell Res 18:1074–1076

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Jia BT, Liu YJ, Zhu YC, Liu XG, Gao CF, Shen JL (2009) Inheritance, fitness cost and mechanism of resistance to tebufenozide in Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae). Pest Manag Sci 65:996–1002

    Article  PubMed  CAS  Google Scholar 

  • Jiang XF, Luo LZ (1998a) Investigation on outbreak and control of the beet armyworm Spodoptera exigua (Hb.). Agrochem Sci Technol 6:8–10

    Google Scholar 

  • Jiang XF, Luo LZ (1998b) Influence of moth ages on flight capacity of the beet armyworm. In: Cheng DF (ed) 21st century advance of plant protection. China Scientific Technique Press, Beijing, pp 371–375

    Google Scholar 

  • Jiang XF, Luo LZ (1999) Outbreak of Spodoptera exigua (Hb.) and its control. Plant Prot 25:32–34

    Google Scholar 

  • Jiang XF, Luo LZ, Hu Y (1999) Influence of larval diets on development, fecundity and flight capacity of the beet armyworm, Spodoptera exigua. Acta Entomol Sin 42:270–276

    Google Scholar 

  • Jiang XF, Luo LZ, Hu Y (2000) The effect of compensatory nutrition condition on flight ability of the beet armyworm, Spodoptera exigua. Acta Phytophyl Sin 27:327–332

    Google Scholar 

  • Jiang XF, Luo LZ, Li KB, Zhao TC, Hu Y (2001) A study on the cold hardiness of the beet armyworm, Spodoptera exigua. Acta Ecol Sin 21:1575–1582

    Google Scholar 

  • Jiang XF, Luo LZ, Li KB, Cao YZ, Hu Y, Liu YQ (2002) Influence of temperature on flight capacity of the beet armyworm, Spodoptera exigua. Acta Entomol Sin 45:275–278

    Google Scholar 

  • Jiang XF, Luo LZ, Sappington TW (2010) Relationship of flight and reproduction in beet armyworm, Spodoptera exigua (Lepidoptera: Noctuidae), a migrant lacking the oogenesis-flight syndrome. J Insect Physiol 56:1631–1637

    Article  PubMed  CAS  Google Scholar 

  • Kalosaka K, Soumaka E, Politis N, Mintzas AC (2009) Thermotolerance and HSP70 expression in the Mediterranean fruit fly Ceratitis capitata. J Insect Physiol 55:568–573

    Article  PubMed  CAS  Google Scholar 

  • Kimura S (1991) Immigration of the beet armyworm, Spodoptera exigua (Hübner), to northern coastal area of Akita Prefecture, 1990, in relation to atmospheric conditions. Annu Rep Soc Plant Prot North Japan 42:148–151

    Google Scholar 

  • Knowlton AA, Salfity M (1996) Nuclear localization and the heat shock proteins. J Biosci 21:123–132

    Article  CAS  Google Scholar 

  • Krebs RA, Loeschcke V (1994) Costs and benefits of activation of the heat shock response in Drosophila melanogaster. Funct Ecol 8:730–737

    Article  Google Scholar 

  • Kurdov M (1986) Prognosis of massive multiplication of the small ground moth Spodoptera exigua Hbn. (Laphygmia exigua Hb.) in Turkmenia. Izvestiya Akademii Nauk Turkmenskoi SSR (Biologicheskikh Nauk) 1:25–28

    Google Scholar 

  • Lan YQ, Zhao SX (2010) Resistance mechanisms of Spodoptera exigua (Hübner) to fenvalerate and alpha-cypermethrin. Chin J Appl Entomol 1:206–211

    Google Scholar 

  • Li DQ (2006) Occurrence and control of the beet armyworm feeding on Chinese onion in Xingchenzi district Shenyang Liaoning Province. Chin Countryside Well-off Technol 2:41

    Google Scholar 

  • Lin ZF, Luo LZ, Pan XL (2007) Insecticide abuse is an important cause of beet armyworm outbreak. Chin Bull Entomol 44:327–332

    Google Scholar 

  • Lu ZP, Xie YG (1995) Study on the occurrence regularity and control of the beet armyworm, Spodoptea exigua. Prospect for Plant Protection in China, Beijing, Chinese Sciences and Technology Press

  • Ma J, Chen Y, Xiao SJ, Mo GZ (1999) Influence of temperature on the increase of laboratory population of Spodoptera exigua. J Hunan Agric Univ 25:308–311

    Google Scholar 

  • Mahroof R, Zhu KY, Neven L, Subramanyam B, Bai J (2005a) Expression patterns of three heat shock protein 70 genes among developmental stages of the red flour beetle, Tribolium castaneum (Coleoptera: Tenebrionidae). Comp Biochem Physiol B 141:247–256

    Article  Google Scholar 

  • Mahroof R, Zhu KY, Subramanyam B (2005b) Changes in expression of heat shock proteins in Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae) in relation to developmental stage, exposure time, and temperature. Ann Entomol Soc Am 98:100–107

    Article  CAS  Google Scholar 

  • Mikkola K (1970) The interpretation of long-range migration of Spodoptera exigua. J Anim Ecol 39:593–598

    Article  Google Scholar 

  • Mitchell ER (1979) Migration by Spodoptera exigua and S. frugiperda. In: Rabb RL, Kennedy JS (eds) Movement of high mobile insects: concepts and methodology in research. North Carolina State University, Raleigh, pp 386–393

    Google Scholar 

  • Niu CW, Zhang QW, Ye ZH, Luo LZ (2006) Analysis of genetic diversity in different geographic populations of the beet armyworm Spodoptera exigua (Lepidoptera: Noctuidae) with AFLP technique. Acta Entomol Sin 49:867–873

    CAS  Google Scholar 

  • Oku T, Kobayashi T (1978) Migratory behavior and life-cycle of noctuid moths (Insecta, Lepidoptera) with notes on the recent status of migrant species in northern Japan. Bull Tohoku Nat Agric Exp Stn 58:97–209

    Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:2002–2007

    Article  Google Scholar 

  • Ramsey AJ, Russell LC, Whitt SR, Chinkers M (2000) Overlapping sites of tetratricopeptide repeat protein binding and chaperone activity in heat shock protein 90. J Biol Chem 275:17857–17862

    Article  PubMed  CAS  Google Scholar 

  • Rasmussen R (2001) Quantification on the light cycler. In: Meuer S, Wittwer C, Nakagawara K (eds) Rapid cycle real-time PCR, methods and applications. Springer, Heidelberg, pp 21–34

    Chapter  Google Scholar 

  • Rinehart JP, Yocum GD, Denlinger DL (2000) Developmental up-regulation of inducible hsp70 transcripts, but not the cognate form, during pupal diapause in the flesh fly, Sarcophaga crassipalpis. Insect Biochem Mol Biol 30:515–521

    Article  PubMed  CAS  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 diapauses. Proc Natl Acad Sci USA 104:11130–11137

    Article  PubMed  CAS  Google Scholar 

  • Saraste M, Sibbald PR, Wittinghofer A (1990) The P-loop: a common motif in ATP-and GTP-binding proteins. Trends Biochem Sci 11:430–434

    Article  Google Scholar 

  • Scheufler C, Brinker A, Bourenkov G, Pegoraro S, Moroder L, Bartunik H, Hartl FU, Moarefi I (2000) Structure of TPR domain-peptide complexes: critical elements in the assembly of the HSP70-HSP90 multichaperone machine. Cell 101:199–210

    Article  PubMed  CAS  Google Scholar 

  • Schlesinger MJ (1990) Heat shock proteins. J Biol Chem 265:12111–12114

    PubMed  CAS  Google Scholar 

  • Sinclair BJ, Gibbs AG, Roberts SP (2007) Gene transcription during exposure to, and recovery from, cold and desiccation stress in Drosophila melanogaster. Insect Mol Biol 16:435–443

    Article  PubMed  CAS  Google Scholar 

  • Sonna LA, Fujita J, Gaffin SL, Lilly CM (2002) Invited review: effects of heat and cold stress on mammalian gene expression. J Appl Physiol 92:1725–1742

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  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 

  • Suenaga H, Tanaka A (1997) Occurrence of beet armyworm, Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae) on young growing stage of garden pea, Pisum sativum L. Jpn J Appl Entomol Zool 41:17–25

    Article  Google Scholar 

  • Tian HG, Peng H, Yao Q, Chen HX, Xie Q, Tang B, Zhang WQ (2009) Developmental control of a lepidopteran pest Spodoptera exigua by ingestion of bacteria expressing dsRNA of a non-midgut gene. PLoS One 4:e6225. doi:10.1371/journal.pone.0006225

    Article  PubMed  Google Scholar 

  • Tomanek L, Somero GN (1999) Evolutionary and acclimation-induced variation in the heat-shock responses of congeneric marine snails (genus Tegula) from different thermal habitats: implications for limits of thermotolerance and biogeography. J Exp Biol 202:2925–2936

    PubMed  Google Scholar 

  • Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76:4350–4353

    Article  PubMed  CAS  Google Scholar 

  • Velazquez JM, Sonoda S, Bugaisky G, Lindquist S (1983) Is the major Drosophila heat shock protein present in cells that have not been heat shocked? J Cell Biol 96:286–290

    Article  PubMed  CAS  Google Scholar 

  • Wang WC, Li L, Jin HF, Li SY (2002) Preliminary observation of serious damage of resistant cotton created by beet armyworm. China Cotton 10:27–28

    Google Scholar 

  • Wang J, Jiang XF, Wu DL, Luo LZ (2008) Effect of larval rearing density on development and fecundity of the beet armyworm, Spodoptera exigua (Lepidoptera: Noctuidae). Acta Entomol Sin 51:889–894

    Google Scholar 

  • Wu G, Harris MK, Guo JY, Wan FH (2008) Response of multiple generations of beet armyworm, Spodoptera exigua (Hübner), feeding on transgenic BT cotton. J Appl Entomol 132:1–11

    Article  Google Scholar 

  • Yathom S (1971) Distribution and flight period of Amphipyrinae (Noctuidae: Lepidoptera) species in Israel in 1959–1970. Isr J Entomol 6:107–132

    Google Scholar 

  • Yin RG, OuYang BY, Liu YY (1994) Studies on the biological characteristic of asparagus caterpillar. Entomol Knowl 31:7–10

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Zhang SM, Zhao YX (1996) Geographical distribution of agricultural and forest insects in China. China Agriculture Press, Beijing, pp 260–261

    Google Scholar 

  • Zhou CJ, Xu XQ (1993) Studies on the biological characteristic of asparagus caterpillar and its control. Sugar Crops China 1:24–27

    Google Scholar 

Download references

Acknowledgements

This work was funded by Projects under the National Department Public Benefit Research Foundation (200803007), National Department Transgenic Crops Cultivation Research Foundation (2009ZX08011-018B), the Major State Basic Research Development Program (Grant 2006CB102001), National Natural Science Foundation of China (30871641, 31071677), and Natural Science Foundation of Beijing (6072023).

Author information

Authors and Affiliations

  1. State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, 100193, China

    Xingfu Jiang, Huifang Zhai, Ling Wang, Lizhi Luo & Lei Zhang

  2. USDA-ARS Corn Insects & Crop Genetics Research Unit Genetics Laboratory, Ames, IA, 50011, USA

    Thomas W. Sappington

Authors
  1. Xingfu Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Huifang Zhai
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ling Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lizhi Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Thomas W. Sappington
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lei Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xingfu Jiang.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jiang, X., Zhai, H., Wang, L. et al. 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 and Chaperones 17, 67–80 (2012). https://doi.org/10.1007/s12192-011-0286-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12192-011-0286-2

Keywords

Search

Navigation