Abstract
Heat shock protein gene (Hsp) families are thought to be important in thermal adaptation, but their expression patterns under various thermal stresses have still been poorly characterized outside of model systems. We have therefore characterized Hsp genes and their stress responses in the oriental fruit moth (OFM), Grapholita molesta, a widespread global orchard pest, and compared patterns of expression in this species to that of other insects. Genes from four Hsp families showed variable expression levels among tissues and developmental stages. Members of the Hsp40, 70, and 90 families were highly expressed under short exposures to heat and cold. Expression of Hsp40, 70, and Hsc70 family members increased in OFM undergoing diapause, while Hsp90 was downregulated. We found that there was strong sequence conservation of members of large Hsp families (Hsp40, Hsp60, Hsp70, Hsc70) across taxa, but this was not always matched by conservation of expression patterns. When the large Hsps as well as small Hsps from OFM were compared under acute and ramping heat stress, two groups of sHsps expression patterns were apparent, depending on whether expression increased or decreased immediately after stress exposure. These results highlight potential differences in conservation of function as opposed to sequence in this gene family and also point to Hsp genes potentially useful as bioindicators of diapause and thermal stress in OFM.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Angilletta MJ (2009) Looking for answers to questions about heat stress: researchers are getting warmer. Funct Ecol 23:231–232. doi:10.1111/j.1365-2435.2009.01548.x
Arbeitman MN, Hogness DS (2000) Molecular chaperones activate the Drosophila ecdysone receptor, an RXR heterodimer. Cell 101:67–77. doi:10.1016/S0092-8674(00)80624-8
Arrigo AP (2013) Human small heat shock proteins: protein interactomes of homo- and hetero-oligomeric complexes: an update. Febs Lett 587:1959–1969. doi:10.1016/j.febslet.2013.05.011
Ashok Kumar K, Somasundram P, RadhaKrishnan R et al (2014) A review on heat shock protein gene expressions and its association with thermo tolerance in the silkworm of Bombyx mori (L). J Entomol Zool Stud 2:170–176
Basha E, O’Neill H, Vierling E (2012) Small heat shock proteins and alpha-crystallins: dynamic proteins with flexible functions. Trends Biochem Sci 37:106–117. doi:10.1016/j.tibs.2011.11.005
Bedulina DS, Evgen’ev MB, Timofeyev MA et al (2013) Expression patterns and organization of the hsp70 genes correlate with thermotolerance in two congener endemic amphipod species (Eulimnogammarus cyaneus and E. verrucosus) from Lake Baikal. Mol Ecol 22:1416–1430. doi:10.1111/Mec.12136
Bettencourt BR, Hogan CC, Nimali M, Drohan BW (2008) Inducible and constitutive heat shock gene expression responds to modification of Hsp70 copy number in Drosophila melanogaster but does not compensate for loss of thermotolerance in Hsp70 null flies. BMC Biol 6:5. doi:10.1186/1741-7007-6-5
Chen H, Xu XL, Li YP, Wu JX (2014) Characterization of heat shock protein 90, 70 and their transcriptional expression patterns on high temperature in adult of Grapholita molesta (Busck). Insect Sci 21:439–448. doi:10.1111/1744-7917.12057
Chen SF, Kang ML, Chen YC et al (2012) Autophagy-related gene 7 is downstream of heat shock protein 27 in the regulation of eye morphology, polyglutamine toxicity, and lifespan in Drosophila. J Biomed Sci 19:52. doi:10.1186/1423-0127-19-52
Choi BG, Hepat R, Kim Y (2014) RNA interference of a heat shock protein, Hsp70, loses, its protection role in indirect chilling injury to the beet armyworm, Spodoptera exigua. Comp Biochem Phys A 168:90–95. doi:10.1016/j.cbpa.2013.11.011
Colinet H, Hoffmann AA (2012) Comparing phenotypic effects and molecular correlates of developmental, gradual and rapid cold acclimation responses in Drosophila melanogaster. Funct Ecol 26:84–93. doi:10.1111/j.1365-2435.2011.01898.x
Colinet H, Lee SF, Hoffmann AA (2010) Temporal expression of heat shock genes during cold stress and recovery from chill coma in adult Drosophila melanogaster. FEBS J 277:174–185. doi:10.1111/j.1742-4658.2009.07470.x
Colinet H, Siaussat D, Bozzolan F, Bowler K (2013) Rapid decline of cold tolerance at young age is associated with expression of stress genes in Drosophila melanogaster. J Exp Biol 216:253–259. doi:10.1242/jeb.076216
Dickson R (1949) Factors govering the induction of diapause in the oriental fruit moth. Ann Entomol Soc Am 42:511–537
Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95:14863–14868
Fischer K, Karl I (2010) Exploring plastic and genetic responses to temperature variation using copper butterflies. Climate Res 43:17–30. doi:10.3354/Cr00892
Fu XM, Chang ZY, Shi XD et al (2014) Multilevel structural characteristics for the natural substrate proteins of bacterial small heat shock proteins. Protein Sci 23:229–237. doi:10.1002/pro.2404
Gao J, Zhang W, Dang W et al (2014) Heat shock protein expression enhances heat tolerance of reptile embryos. Proc Biol Sci 281:20141135. doi:10.1098/rspb.2014.1135
Gillespie DR, Nasreen A, Moffat CE et al (2012) Effects of simulated heat waves on an experimental community of pepper plants, green peach aphids and two parasitoid species. Oikos 121:149–159. doi:10.1111/j.1600-0706.2011.19512.x
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. doi:10.1016/j.jinsphys.2008.08.009
Heckmann LH, Sorensen PB, Krogh PH, Sorensen JG (2011) NORMA-Gene: A simple and robust method for qPCR normalization based on target gene data. BMC Bioinformatics 12:250. doi:10.1186/1471-2105-12-250
Hoffmann AA, Blacket MJ, McKechnie SW et al (2012) A proline repeat polymorphism of the Frost gene of Drosophila melanogaster showing clinal variation but not associated with cold resistance. Insect Mol Biol 21:437–445. doi:10.1111/j.1365-2583.2012.01149.x
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. doi:10.1111/j.1365-2583.2007.00744.x
Jones MM (2010) Susceptibility of oriental fruit moth, (Grapholita molesta (Busck)) to selected insecticides and mixtures. PhD thesis. University of Illinois at Urbana-Champaign
Jones MM, Robertson JL, Weinzierl RA (2010) Susceptibility of oriental fruit moth (Lepidoptera: Tortricidae) larvae to selected reduced-risk insecticides. J Econ Entomol 103:1815–1820. doi:10.1603/Ec10029
Kampinga HH, Craig EA (2010) The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nat Rev Mol Cell Biol 11:579–592. doi:10.1038/nrm2941
Kim BM, Rhee JS, Jeong CB et al (2014) Heavy metals induce oxidative stress and trigger oxidative stress-mediated heat shock protein (hsp) modulation in the intertidal copepod Tigriopus japonicus. Comp Biochem Phys C 166:65–74. doi:10.1016/j.cbpc.2014.07.005
King AM, MacRae TH (2015) Insect heat shock proteins during stress and diapause. Ann Rev Entomol 60:59–75. doi:10.1146/annurev-ento-011613-162107
Kirk H, Dorn S, Mazzi D (2013) Worldwide population genetic structure of the oriental fruit moth (Grapholita molesta), a globally invasive pest. BMC Ecol 13:12. doi:10.1186/1472-6785-13-12
Krebs RA, Feder ME (1998) Hsp70 and larval thermotolerance in Drosophila melanogaster: how much is enough and when is more too much? J Insect Physiol 44:1091–1101
Kregel KC (2002) Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. J Appl Physiol 92:2177–2186. doi:10.1152/japplphysiol.01267.2001
Kvist J, Wheat CW, Kallioniemi E et al (2013) Temperature treatments during larval development reveal extensive heritable and plastic variation in gene expression and life history traits. Mol Ecol 22:602–619. doi:10.1111/j.1365-294X.2012.05521.x
Ma G, Rudolf VH, Ma CS (2015) Extreme temperature events alter demographic rates, relative fitness, and community structure. Glob Chang Biol 21:1794–1808. doi:10.1111/gcb.12654
Michels AA, Kanon B, Bensaude O, Kampinga HH (1999) Heat shock protein (Hsp) 40 mutants inhibit Hsp70 in mammalian cells. J Biol Chem 274:36757–36763
Mitchell KA, Hoffmann AA (2010) Thermal ramping rate influences evolutionary potential and species differences for upper thermal limits in Drosophila. Funct Ecol 24:694–700. doi:10.1111/j.1365-2435.2009.01666.x
Moribe Y, Oka K, Niimi T et al (2010) Expression of heat shock protein 70a mRNA in Bombyx mori diapause eggs. J Insect Physiol 56:1246–1252. doi:10.1016/j.jinsphys.2010.03.023
Morrow G, Tanguay RM (2012) Small heat shock protein expression and functions during development. Int J Biochem Cell Biol 44:1613–1621. doi:10.1016/j.biocel.2012.03.009
Morrow G, Tanguay RM (2015) Drosophila small heat shock proteins: an update on their features and functions. In: Hightower LE (ed) Tanguay RM. Springer International Publishing Switzerland, The big book on small heat shock proteins, pp 579–606
Peterson LB, Blagg BS (2009) To fold or not to fold: modulation and consequences of Hsp90 inhibition. Future Med Chem 1:267–283. doi:10.4155/fmc.09.17
Pratt WB, Toft DO (1997) Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr Rev 18:306–360. doi:10.1210/edrv.18.3.0303
Pratt WB, Toft DO (2003) Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery. Exp Biol Med 228:111–133
Rezende EL, Tejedo M, Santos M (2011) Estimating the adaptive potential of critical thermal limits: methodological problems and evolutionary implications. Funct Ecol 25:111–121. doi:10.1111/j.1365-2435.2010.01778.x
Rinehart JP, Li A, Yocum GD et al (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. doi:10.1073/pnas.0703538104
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. doi:10.1093/bioinformatics/btg180
Russell DA (1986) Ecology of the oriental fruit moth, Grapholita molesta (Busck) in New Zealand. PhD thesis. University of Auckland
Saldanha AJ (2004) Java Treeview—extensible visualization of microarray data. Bioinformatics 20:3246–3248. doi:10.1093/bioinformatics/bth349
Shatilina ZM, Riss HW, Protopopova MV et al (2011) The role of the heat shock proteins (HSP70 and sHSP) in the thermotolerance of freshwater amphipods from contrasting habitats. J Therm Biol 36:142–149. doi:10.1016/j.jtherbio.2010.12.008
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 Phys A 158:102–110. doi:10.1016/j.cbpa.2010.09.006
Sonoda S, Fukumoto K, Izumi Y et al (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 Physiol 63:36–47. doi:10.1002/arch.20138
Sørensen JG (2010) Application of heat shock protein expression for detecting natural adaptation and exposure to stress in natural populations. Curr Zool 56:703–713
Tachibana S, 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. doi:10.1016/j.jinsphys.2004.11.012
Takahashi KH, Rako L, Takano-Shimizu T et al (2010) Effects of small Hsp genes on developmental stability and microenvironmental canalization. BMC Evol Biol 10:284. doi:10.1186/1471-2148-10-284
Tamura K, Peterson D, Peterson N et al (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. doi:10.1093/molbev/msr121
Tower J (2011) Heat shock proteins and Drosophila aging. Exp Gerontol 46:355–362. doi:10.1016/j.exger.2010.09.002
Tungjitwitayakul J, Singtripop T, Nettagul A et al (2008) Identification, characterization, and developmental regulation of two storage proteins in the bamboo borer Omphisa fuscidentalis. J Insect Physiol 54:62–76. doi:10.1016/j.jinsphys.2007.08.003
Vabulas RM, Raychaudhuri S, Hayer-Hartl M, Hartl FU (2010) Protein folding in the cytoplasm and the heat shock response. Cold Spring HarbPerspect Biol 2:a004390. doi:10.1101/cshperspect.a004390
Wang XH, Kang L (2005) Differences in egg thermotolerance between tropical and temperate populations of the migratory locust Locusta migratoria (Orthoptera : Acridiidae). J Insect Physiol 51:1277–1285. doi:10.1016/j.jinsphys.2005.07.010
Xu Q, Zou Q, Zheng H et al (2011) Three heat shock proteins from Spodoptera exigua: Gene cloning, characterization and comparative stress response during heat and cold shocks. Comp Biochem Physiol B 159:92–102. doi:10.1016/j.cbpb.2011.02.005
Yocum GD, Joplin KH, Denlinger DL (1998) Upregulation of a 23 kDa small heat shock protein transcript during pupal diapause in the flesh fly, Sarcophaga crassipalpis. Insect Biochem Mol Biol 28:677–682
Zhang B, Zheng JC, Peng Y et al (2015) Stress responses of small heat shock protein genes in Lepidoptera point to limited conservation of function across phylogeny. Plos One 10:e0132700. doi:10.1371/journal.pone.0132700
Zhang Q, Denlinger DL (2010) Molecular characterization of heat shock protein 90, 70 and 70 cognate cDNAs and their expression patterns during thermal stress and pupal diapause in the corn earworm. J Insect Physiol 56:138–150. doi:10.1016/j.jinsphys.2009.09.013
Zhao L, Jones WA (2012) Expression of heat shock protein genes in insect stress responses. Invertebr Surviv J 9:93–101
Acknowledgments
We thank for Dr. Wei Zhang for assistance with experiments and topic discussion. This research was supported by the National Natural Science Foundation of China (31400323) and the National Special Fund for Agro-scientific Research in the Public Interest (201103024) as well as an ARC Fellowship to AAH.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(DOCX 133 kb).
Rights and permissions
About this article
Cite this article
Zhang, B., Peng, Y., Zheng, J. et al. Response of heat shock protein genes of the oriental fruit moth under diapause and thermal stress reveals multiple patterns dependent on the nature of stress exposure. Cell Stress and Chaperones 21, 653–663 (2016). https://doi.org/10.1007/s12192-016-0690-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12192-016-0690-8