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Expression profiles of 14 small heat shock protein (sHSP) transcripts during larval diapause and under thermal stress in the spruce budworm, Choristoneura fumiferana (L.)

Cell Stress and Chaperones volume 23, pages 1247–1256 (2018)Cite this article

Abstract

Diapause is an important strategy for certain insect species to survive unfavorable environmental conditions, including low temperatures experienced when they overwinter in cold climate. Many studies have indicated that the increased expression of heat shock proteins during diapause improves the thermal tolerance of insects. However, the relationship between small heat shock proteins (sHSPs) and diapause is not clear or well-researched. In this study, we investigated the transcript levels of 14 sHSP genes in the spruce budworm, Choristoneura fumiferana, a major pest of spruce and fir in Canada, during pre-diapause, diapause, and post-diapause under normal rearing conditions and in response to a heat shock treatment. We found that sHSP expression profiles could be classified into five patterns under normal laboratory conditions: pattern I was upregulated only during pre-diapause, pattern II was upregulated only during diapause, pattern III was constantly expressed throughout diapause, pattern IV was upregulated in both pre-diapause and diapause, and pattern V was upregulated only during post-diapause. After heat shock, five different expression patterns were observed: pattern I responded weakly or not at all throughout diapause, pattern II responded weakly during the diapause stage but strongly at the onset of diapause and in the post-diapause period, pattern III was upregulated only during post-diapause, pattern IV was strongest during diapause, and pattern V was strongest only in early diapause. These complex expression profiles lead us to suggest that most of the sHSP genes are involved in the diapause process and that they may have multiple and important roles in different phases of this process.

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References

  • Arrigo AP (1998) Small stress proteins: chaperones that act as regulators of intracellular redox state and programmed cell death. Biol Chem 379:19–26

    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

    CAS  Article  Google Scholar 

  • Blais JR (1983) Trends in the frequency, extent, and severity of spruce budworm outbreaks in eastern Canada. Can J For Res 13:539–547

    Article  Google Scholar 

  • Boulanger Y, Arseneault D (2004) Spruce budworm outbreaks in eastern Quebec over the last 450 years. Can J For Res 34:1035–1043

    Article  Google Scholar 

  • Denlinger DL (2002) Regulation of diapause. Annu Rev Entoml 47:93–122

    CAS  Article  Google Scholar 

  • de Kort CAD (1996) Cosmic influences on the expression of a specific gene in the Colorado potato beetle: the diapause protein 1 gene. Arch Insect Biochem Physiol 32:567–573

    Article  Google Scholar 

  • Dubrovsky EB, Dretzen G, Berger EM (1996) The broad-complex gene is a tissue-specific modulator of the ecdysone response of the Drosophila hsp23 gene. Mol Cell Biol 16:6542–6552

    CAS  Article  Google Scholar 

  • Evgrafov OV, Mersiyanova I, Irobi J, Van Den Bosch L, Dierick I, Leung CL, Schagina O, Verpoorten N, Van Impe K, Fedotov V, Dadali E (2004) Mutant small heat-shock protein 27 causes axonal Charcot-Marie-tooth disease and distal hereditary motor neuropathy. Nat Genet 36:602–606

    CAS  Article  Google Scholar 

  • Feng QL, Davey KG, Pang ASD, Ladd TR, Retnakaran A (2001) Developmental expression and stress induction of glutathione S-transferase in the spruce budworm, Choristoneura fumiferana: developmental expression and the induction by various stresses. J Insect Physiol 47:1–10

    CAS  Article  Google Scholar 

  • Flannagan RD, Tammariello SP, Joplin KH, Cikra-Ireland RA, Yocum GD, Denlinger DL (1998) Diapause-specific gene expression in pupae of the flesh fly Sarcophaga crassipalpis. Proc Natl Acad Sci U S A 95:5616–5620

    CAS  Article  Google Scholar 

  • Fremdt H, Amendt J, Zehner R (2014) Diapause-specific gene expression in Calliphora vicina (Diptera: Calliphoridae)—a useful diagnostic tool for forensic entomology. Int J Legal Med 128:1001–1011

    Article  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

    CAS  Article  Google Scholar 

  • Godlewski J, Kludkiewicz B, Grzelak K, Cymborowski B (2001) Expression of larval hemolymph proteins (Lhp) genes and protein synthesis in the fat body of greater wax moth (Galleria mellonella) larvae during diapause. J Insect Physiol 47:759–766

    CAS  Article  Google Scholar 

  • Haass CH, Klein UL, Kloetzel PM (1990) Developmental expression of Drosophila melanogaster small heat-shock proteins. J Cell Sci 96:413–418

    CAS  PubMed  Google Scholar 

  • Han EN, Bauce E (1993) Physiological changes and cold hardiness of spruce budworm larvae, Choristoneura fumiferana (Clem.), during pre-diapause and diapause development under laboratory conditions. Can Ent 125:1043–1053

    Article  Google Scholar 

  • Hayward SA, 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

    CAS  Article  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

    CAS  Article  Google Scholar 

  • Huet F, Lage JD, Ruiz C, Richards G (1996) The role of ecdysone in the induction and maintenance of hsp27 transcripts during larval and prepupal development of Drosophila. Dev Genes Evol 206:326–332

    CAS  Article  Google Scholar 

  • Hwang JS, Go HJ, Goo TW, Yun EY, Choi KH (2005) The analysis of differentially expressed novel transcripts in diapausing and diapause-activated eggs of Bombyx mori. Arch Insect Biochem Physiol 59:197–201

    CAS  Article  Google Scholar 

  • Jaya N, Garcia V, Vierling E (2009) Substrate binding site flexibility of the small heat shock protein molecular chaperones. Proc Natl Acad Sci U S A 106:15604–15609

    CAS  Article  Google Scholar 

  • Joanisse DR, Michaud S, InagumaY TRM (1998) Small heat shock proteins of Drosophila: developmental expression and functions. J Biosci 23:369–376

    CAS  Article  Google Scholar 

  • King AM, MacRae TH (2015) Insect heat shock proteins during stress and diapause. Annu Rev Entomol 60:59–75

    CAS  Article  Google Scholar 

  • Kokolakis G, Tatari M, Zacharopoulou A, Mintzas AC (2008) The hsp27 gene of the Mediterranean fruit fly, Ceratitis capitata: structural characterization, regulation and developmental expression. Insect Mol Biol 17:699–710

    CAS  Article  Google Scholar 

  • Landry J, Chrétien P, Lambert H, Hickey E, Weber LA (1989) Heat shock resistance conferred by expression of the human HSP27 gene in rodent cells. J Cell Biol 109:7–15

    CAS  Article  Google Scholar 

  • Lee KY, Valaitis AP, Denlinger DL (1998) Activity of gut alkaline phosphatase, proteases and esterase in relation to diapause of pharate first instar larvae of the gypsy moth, Lymantria dispar. Arch Insect Biochem Physiol 37:197–205

    Article  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 9:1–14

    CAS  Article  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

    CAS  Article  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

    CAS  Article  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

    CAS  Article  Google Scholar 

  • Mackay DS, Andley UP, Shiels A (2003) Cell death triggered by a novel mutation in the alpha A-crystallin gene underlies autosomal dominant cataract linked to chromosome 21q. Eur J Hum Genet 11:784–793

    CAS  Article  Google Scholar 

  • MacRae TH (2010) Gene expression, metabolic regulation and stress tolerance during diapause. Cell Mol Life Sci 67:2405–2424

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  • McMorran A (1965) A synthetic diet for the spruce budworm, Choristoneura fumiferana (Clem.)(Lepidoptera: Tortricidae). Can Ent 97:58–62

    Article  Google Scholar 

  • Morrow G, Heikkila JJ, Tanguay RM (2006) Differences in the chaperone-like activities of the four main small heat shock proteins of Drosophila melanogaster. Cell Stress Chaperones 11:51–60

    CAS  Article  Google Scholar 

  • Mymrikov EV, Seit-Nebi AS, Gusev NB (2011) Large potentials of small heat shock proteins. Physiol Rev 91:1123–1159

    CAS  Article  Google Scholar 

  • Niimi T, Yamashita O, Yaginuma T (1993) A cold-inducible Bombyx gene encoding a protein similar to mammalian sorbitol dehydrogenase. FEBS J 213:1125–1131

    CAS  Google Scholar 

  • Palli SR, Kothapalli R, Feng Q, Ladd T, Perera SC, Zheng S-C, Gojtan K, Pang ASD, Primavera M, Tomkins W, Retnakaran A (2001) Molecular analysis of overwintering diapause. In: Denlinger DL, Giebultowicz JM, Saunders DS (eds) Insect Timing: Circadian Rhythmicity to Seasonality (133–144). Elsevier, Amsterdam

    Google Scholar 

  • Palli SR, Ladd TR, Ricci AR, Primavera M, Mungrue IN (1998) Synthesis of the same two proteins prior to larval diapause and pupation in the spruce budworm, Choristoneura fumiferana. J Insect Physiol 44:509–524

    CAS  Article  Google Scholar 

  • Poupardin R, Schöttner K, Korbelová J, Provazník J, Doležel D, Pavlinic D, Beneš V, Koštál V (2015) Early transcriptional events linked to induction of diapause revealed by RNAseq in larvae of drosophilid fly, Chymomyza costata. BMC Genomics 16:720

    Article  Google Scholar 

  • Quan G, Duan J, Ladd L, Krell PJ (2018) Identification and expression analysis of multiple small heat shock protein genes in spruce budworm, Choristoneura fumiferana (L.). Cell Stress Chaperones 23:141–154

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  • Rezende EL, Tejedo M, Santos M (2011) Estimating the adaptive potential of critical thermal limits: methodological problems and evolutionary implications. Fun Ecol 25:111–121

    Article  Google Scholar 

  • Régnière J (1987) Temperature-dependent development of eggs and larvae of Choristoneura fumiferana (Clem.) (Lepidoptera: Tortricidae) and simulation of its seasonal history. Can Entomol 119:717–728

    Article  Google Scholar 

  • Régnière J (1990) Diapause termination and changes in thermal responses during postdiapause development in larvae of the spruce budworm, Choristoneura fumiferana. J Insect Physiol 36:727–735

    Article  Google Scholar 

  • Régnière J, St-Amant R, Duval P (2012) Predicting insect distributions under climate change from physiological responses: spruce budworm as an example. Biol Invasions 14:1571–1586

    Article  Google Scholar 

  • Rinehart JP, Denlinger DL (2000) Heat shock protein 90 is downregulated during pupal diapause in the flesh fly, Sarcophaga crassipalpis, but remains responsive to thermal stress. Insect Mol Biol 9:641–645

    CAS  Article  Google Scholar 

  • Rinehart JP, Hayward SA, Elnitsky MA, Sandro LH, Lee RE, Denlinger DL (2006) Continuous up-regulation of heat shock proteins in larvae, but not adults, of a polar insect. Proc Natl Acad Sci U S A 103:14223–14227

    CAS  Article  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

    CAS  Article  Google Scholar 

  • Rinehart JP, Robich RM, Denlinger DL (2010) Isolation of diapause-regulated genes from the flesh fly, Sarcophaga crassipalpis by suppressive subtractive hybridization. J Insect Physiol 56:603–609

    CAS  Article  Google Scholar 

  • Royama TO (1984) Population dynamics of the spruce budworm Choristoneura fumiferana. Ecol Monogr 54:429–462

    Article  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

    CAS  Article  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 70:2443–2450

    CAS  Article  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

    CAS  Article  Google Scholar 

  • Stehr GW (1967) On coniferophagous species of Choristoneura (Lepidoptera: Tortricidae) in North America: II. Geographic distribution in accordance with forest regions. Can Entomol 99:456–463

    Article  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 10:1–11

    Article  Google Scholar 

  • Tammariello SP, Denlinger DL (1998) G0/G1 cell cycle arrest in the brain of Sarcophaga crassipalpis during pupal diapause and the expression pattern of the cell cycle regulator, proliferating cell nuclear antigen. Insect Biochem Mol Biol 28:83–89

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  • Tungjitwitayakul J, Tatun N, Singtripop T, Sakurai S (2008) Characteristic expression of three heat shock-responsive genes during larval diapause in the bamboo borer Omphisa fuscidentalis. Zool Sci 25:321–333

    CAS  Article  Google Scholar 

  • Uno T, Nakasuji A, Shimoda M, Aizono Y (2004) Expression of cytochrome c oxidase subunit 1 gene in the brain at an early stage in the termination of pupal diapause in the sweet potato hornworm, Agrius convolvuli. J Insect Physiol 50:35–42

    CAS  Article  Google Scholar 

  • Villeneuve TS, Ma X, Sun Y, Oulton MM, Oliver AE, MacRae TH (2006) Inhibition of apoptosis by p26: implications for small heat shock protein function during Artemia development. Cell Stress Chaperones 11:71–80

    CAS  Article  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

    CAS  Article  Google Scholar 

  • Waters ER (2013) The evolution, function, structure, and expression of the plant sHSPs. J Exp Bot 64:391–403

    CAS  Article  Google Scholar 

  • Wieske M, Benndorf R, Behlke J, Dölling R, Grelle G, Bielka H, Lutsch G (2001) Defined sequence segments of the small heat shock proteins HSP25 and αB-crystallin inhibit actin polymerization. FEBS J 268:2083–2090

    CAS  Google Scholar 

  • Wood KL, Voss OH, Huang Q, Parihar A, Mehta N, Batra S, Doseff AI (2010) The small heat shock protein 27 is a key regulator of CD8+ CD57+ lymphocyte survival. J Immunol 184:5582–5588

    CAS  Article  Google Scholar 

  • Yocum GD, Joplin KH, Denlinger DL (1998) Upregulation of a 23 kDa small heat shock protein transcript during diapause in the flesh fly, Sarcophaga crassipalpis. Insect Biochem Mol Biol 28:677–682

    CAS  Article  Google Scholar 

  • Zhang B, Zheng J, Peng Y, Liu X, Hoffmann AA, Ma CS (2015) Stress responses of small heat shock protein genes in Lepidoptera point to limited conservation of function across phylogeny. PLoS One 10:e0132700

    Article  Google Scholar 

  • Zhang G, Storey JM, Storey KB (2011) Chaperone proteins and winter survival by a freeze tolerant insect. J Insect Physiol 57:1115–1122

    CAS  Article  Google Scholar 

  • Zhao L, Jones WA (2012) Expression of heat shock protein genes in insect stress responses. Invertebrate Surviv J 90:93–101

    Google Scholar 

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Acknowledgments

We greatly thank Insect Production Services at the Great Lake Forestry Centre for providing insect materials. We thank two anonymous reviewers for their constructive comments.

Funding

This work was supported by grants from the Genomics Research and Development Initiative (GRDI) and the Canadian Forest Service, Natural Resources Canada.

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Affiliations

  1. Natural Resources Canada, Canadian Forest Service, Great Lakes Forestry Centre, Sault Ste. Marie, ON, P6A 2E5, Canada

    Guoxing Quan, Jun Duan, William Fick, George Kyei-Poku & Jean-Noël Candau

  2. Department of Pathology and Laboratory Medicine, University of British Columbia, Vancouver, V6T 1Z3, Canada

    Jun Duan

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  1. Guoxing Quan
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  2. Jun Duan
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  3. William Fick
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  4. George Kyei-Poku
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Correspondence to Guoxing Quan.

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Quan, G., Duan, J., Fick, W. et al. Expression profiles of 14 small heat shock protein (sHSP) transcripts during larval diapause and under thermal stress in the spruce budworm, Choristoneura fumiferana (L.). Cell Stress and Chaperones 23, 1247–1256 (2018). https://doi.org/10.1007/s12192-018-0931-0

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  • DOI: https://doi.org/10.1007/s12192-018-0931-0

Keywords

  • Diapause
  • Spruce budworm
  • sHSP
  • Chaperone
  • Overwinter
  • Gene expression