Skip to main content
Log in

Geographic variation in thermal tolerance and strategies of heat shock protein expression in the land snail Theba pisana in relation to genetic structure

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

Abstract

Land snails are exposed to conditions of high ambient temperature and low humidity, and their survival depends on a suite of morphological, behavioral, physiological, and molecular adaptations to the specific microhabitat. We tested in six populations of the land snail Theba pisana whether adaptations to different habitats affect their ability to cope with thermal stress and their strategies of heat shock protein (HSP) expression. Levels of Hsp70 and Hsp90 in the foot tissue were measured in field-collected snails and after acclimation to laboratory conditions. Snails were also exposed to various temperatures (32 up to 54 °C) for 2 h and HSP messenger RNA (mRNA) levels were measured in the foot tissue and survival was determined. To test whether the physiological and molecular data are related to genetic parameters, we analyzed T. pisana populations using partial sequences of nuclear and mitochondrial DNA ribosomal RNA genes. We show that populations collected from warmer habitats were more thermotolerant and had higher constitutive levels of Hsp70 isoforms in the foot tissue. Quantitative real-time polymerase chain reaction (PCR) analysis indicated that hsp70 and hsp90 mRNA levels increased significantly in response to thermal stress, although the increase in hsp70 mRNA was larger compared to hsp90 and its induction continued up to higher temperatures. Generally, warm-adapted populations had higher temperatures of maximal induction of hsp70 mRNA synthesis and higher upper thermal limits to HSP mRNA synthesis. Our study suggests that Hsp70 in the foot tissue of T. pisana snails may have important roles in determining stress resistance, while Hsp90 is more likely implicated in signal transduction processes that are activated by stress. In the phylogenetic analysis, T. pisana haplotypes were principally divided into two major clades largely corresponding to the physiological ability to withstand stress, thus pointing to genetically fixed tolerance.

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

Access this article

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

Similar content being viewed by others

References

  • Arad Z (2009) Resistance to desiccation and heat. In: Heller J (ed) Landsnails of the land of Israel. Pensoft, Sofia and Moscow, pp 74–93

    Google Scholar 

  • Arad Z, Goldenberg S, Heller J (1989) Resistance to desiccation and distribution patterns in the land snail Sphincterochila. J Zool (Lond) 218:353–364

    Article  Google Scholar 

  • Arad Z, Goldenberg S, Heller J (1992) Intraspecific variation in resistance to desiccation and climatic gradients in the distribution of the land snail Xeropicta vestalis. J Zool (Lond) 226:643–656

    Article  Google Scholar 

  • Arad Z, Goldenberg S, Heller J (1993) Intraspecific variation in resistance to desiccation and climatic gradients in the distribution of the bush-dwelling land snail Trochoidea simulata. J Zool (Lond) 229:249–265

    Article  Google Scholar 

  • Arad Z, Mizrahi T, Goldenberg S, Heller J (2010) Natural annual cycle of heat shock proteins expression in land snails: desert vs. Mediterranean species of Sphincterochila. J Exp Biol 213:3487–3495

    Article  CAS  PubMed  Google Scholar 

  • Bahrndorff S, Marien J, Loeschcke V, Ellers J (2009) Dynamics of heat-induced thermal stress resistance and Hsp70 expression in the springtail, Orchesella cincta. Funct Ecol 23:233–239

    Article  Google Scholar 

  • Bedulina DS 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

    Article  CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Brooks SP, Storey KB (1995) Evidence for aestivation specific proteins in Otala lactea. Mol Cell Biochem 143:15–20

    Article  CAS  PubMed  Google Scholar 

  • Cameron RAD (1970) The survival, weight-loss and behaviour of three species of land snail in conditions of low humidity. J Zool (Lond) 160:143–157

    Article  Google Scholar 

  • Chapple JP, Smerdon GR, Hawkins AJS (1997) Stress-70 protein induction in Mytilus edulis: tissue-specific responses to elevated temperature reflect relative vulnerability and physiological function. J Exp Mar Biol Ecol 217:225–235

    Article  CAS  Google Scholar 

  • Chu ND, Kaluziak ST, Trussell GC, Vollmer SV (2014) Phylogenomic analyses reveal latitudinal population structure and polymorphisms in heat stress genes in the North Atlantic snail Nucella lapillus. Mol Ecol 23:1863–1873. doi:10.1111/mec.12681

    Article  PubMed  Google Scholar 

  • Csermely P, Schnaider T, Soti C, Prohaszka Z, Nardai G (1998) The 90-kDa molecular chaperone family: structure, function, and clinical applications. A comprehensive review. Pharmacol Ther 79:129–168

    Article  CAS  PubMed  Google Scholar 

  • Daumer C, Greve C, Hutterer R, Misof B, Haase M (2012) Phylogeography of an invasive land snail: natural range expansion versus anthropogenic dispersal in Theba pisana pisana. Biol Invasions 14:1665–1682

    Article  Google Scholar 

  • Davison A (2002) Land snails as a model to understand the role of history and selection in the origins of biodiversity. Popul Ecol 44:129–136

    Article  Google Scholar 

  • Deng W et al (2010) DIVEIN: a web server to analyze phylogenies, sequence divergence, diversity, and informative sites. Biotechniques 48:405–408. doi:10.2144/000113370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dereeper A et al (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36:W465–W469. doi:10.1093/nar/gkn180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dieterich A et al (2013) Daily and seasonal changes in heat exposure and the Hsp70 level of individuals from a field population of Xeropicta derbentina (Krynicki 1836) (Pulmonata, Hygromiidae) in Southern France. Cell Stress Chaperones 18:405–414. doi:10.1007/s12192-012-0393-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Diller KR (2006) Stress protein expression kinetics. Annu Rev Biomed Eng 8:403–424

    Article  CAS  PubMed  Google Scholar 

  • Dittbrenner N, Lazzara R, Köhler HR, Mazzia C, Capowiez Y, Triebskorn R (2009) Heat tolerance in Mediterranean land snails: histopathology after exposure to different temperature regimes. J Molluscan Stud 75:9–18

    Article  Google Scholar 

  • Dong Y, Dong S (2008) Induced thermotolerance and expression of heat shock protein 70 in sea cucumber Apostichopus japonicus. Fish Sci 74:573–578

    Article  CAS  Google Scholar 

  • Dong Y, Miller LP, Sanders JG, Somero GN (2008) Heat-shock protein 70 (Hsp70) expression in four limpets of the genus Lottia: interspecific variation in constitutive and inducible synthesis correlates with in situ exposure to heat stress. Biol Bull 215:173–181

    Article  PubMed  Google Scholar 

  • Evgen’ev MB, Garbuz DG, Shilova VY, Zatsepina OG (2007) Molecular mechanisms underlying thermal adaptation of xeric animals. J Biosci 32:489–499

    Article  PubMed  Google Scholar 

  • Fabbri E, Valbonesi P, Franzellitti S (2008) HSP expression in bivalves. Invertebr Surviv J 5:135–161

    Google Scholar 

  • Feder ME (1999) Organismal, ecological, and evolutionary aspects of heat-shock proteins and the stress response: established conclusions and unresolved issues. Am Zool 39:857–864

    Article  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 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giokas S, Pafilis P, Valakos E (2005) Ecological and physiological adaptations of the land snail Albinaria caerulea (pulmonata: Clausiliidae). J Molluscan Stud 71:15–23

    Article  Google Scholar 

  • Gittenberger E, Ripken TEJ (1987) The genus Theba (Mollusca: Gastropoda: Helicidae), systematics and distribution. Zool Verh 241:3–59

    Google Scholar 

  • Greve C, Gimnich F, Hutterer R, Misof B, Haase M (2012) Radiating on oceanic islands: patterns and processes of speciation in the land snail genus Theba (Risso 1826). PLoS One 7, e34339. doi:10.1371/journal.pone.0034339

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Greve C, Hutterer R, Groh K, Haase M, Misof B (2010) Evolutionary diversification of the genus Theba (Gastropoda: Helicidae) in space and time: a land snail conquering islands and continents. Mol Phylogenet Evol 57:572–584. doi:10.1016/j.ympev.2010.08.021

    Article  CAS  PubMed  Google Scholar 

  • Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321

    Article  CAS  PubMed  Google Scholar 

  • Heller J (1988) The biogeography of the land snails of Israel. In: Yom-Tov Y, Tchernov E (eds) The zoogeography of Israel. Dr. W. Junk Publishers, Dordrecht, pp 325–353

    Google Scholar 

  • Heller J (2009) Activity. In: Heller J (ed) Land snails of the land of Israel. Pensoft, Sofia and Moscow, pp 60–73

    Google Scholar 

  • Heller J, Kadmon R (2004) The use of GIS mapping techniques in assessing biodiversity. J Conchol 3:123–132

    Google Scholar 

  • Hoffmann AA, Chown SL, Clusella-Trullas S (2013) Upper thermal limits in terrestrial ectotherms: how constrained are they. Funct Ecol 27:934–949

    Article  Google Scholar 

  • IPCC (2007) Intergovernmental panel on climate change. Cambridge, UK

  • Jaffe S (1988) Climate of Israel. In: Yom-Tov Y, Tchernov E (eds) The zoogeography of Israel. Dr. W. Junk Publishers, Dordrecht, pp 79–94

    Google Scholar 

  • Kadmon R, Heller J (1998) Modelling faunal responses to climatic gradients with GIS: land snails as a case study. J Biogeog 25:527–539

    Article  Google Scholar 

  • Keller I, Seehausen O (2012) Thermal adaptation and ecological speciation. Mol Ecol 21:782–799

    Article  CAS  PubMed  Google Scholar 

  • Köhler HR, Lazzara R, Dittbrenner N, Capowiez Y, Mazzia C, Triebskorn R (2009) Snail phenotypic variation and stress proteins: do different heat response strategies contribute to Waddington’s widget in field populations? J Exp Zool B Mol Dev Evol 312:136–147

    Article  PubMed  Google Scholar 

  • Kotsakiozi P, Parmakelis A, Aggeli IK, Gaitanaki C, Giokas S, Valakos ED (2015) Water balance and expression of heat-shock protein 70 in Codringtonia species: a study within a phylogenetic framework. J Molluscan Stud 81:24–36

    Article  Google Scholar 

  • Kourtidis A, Drosopoulou E, Nikolaidis N, Hatzi VI, Chintiroglou CC, Scouras ZG (2006) Identification of several cytoplasmic HSP70 genes from the Mediterranean mussel (Mytilus galloprovincialis) and their long-term evolution in Mollusca and Metazoa. J Mol Evol 62:446–459. doi:10.1007/s00239-005-0121-4

    Article  CAS  PubMed  Google Scholar 

  • Krebs RA, Bettencourt BR (1999) Evolution of thermotolerance and variation in the heat shock protein, Hsp70. Am Zool 39:910–919

    Article  CAS  Google Scholar 

  • Krebs RA, Feder ME (1997) Deleterious consequences of Hsp70 overexpression in Drosophila melanogaster larvae. Cell Stress Chaperones 2:60–71

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kregel KC (2002) Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. J Appl Physiol 92:2177–2186

    Article  CAS  PubMed  Google Scholar 

  • Landry J, Bernier D, Chretien P, Nicole LM, Tanguay RM, Marceau N (1982) Synthesis and degradation of heat shock proteins during development and decay of thermotolerance. Cancer Res 42:2457–2461

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Lindquist S, Craig EA (1988) The heat-shock proteins. Annu Rev Genet 22:631–677

    Article  CAS  PubMed  Google Scholar 

  • Machin J (1967) Structural adaptation for reducing water-loss in three species of terrestrial snails. J Zool (Lond) 152:55–65

    Article  Google Scholar 

  • Mayer MP, Bukau B (1999) Molecular chaperones: the busy life of Hsp90. Curr Biol 9:R322–R325

    Article  CAS  PubMed  Google Scholar 

  • Mayer MP, Bukau B (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol Life Sci 62:670–684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McMillan DM, Irschick DJ, Rees BB (2011) Geographic variation in the effects of heat exposure on maximum sprint speed and Hsp70 expression in the western fence lizard Sceloporus occidentalis. Physiol Biochem Zool 84:573–582. doi:10.1086/662385

    Article  CAS  PubMed  Google Scholar 

  • Mizrahi T, Goldenberg S, Heller J, Arad Z (2015) Natural variation in resistance to desiccation and heat shock protein expression in the land snail Theba pisana along a climatic gradient. Physiol Biochem Zool 88:66–80. doi:10.1086/679485

    Article  PubMed  Google Scholar 

  • Mizrahi T, Heller J, Goldenberg S, Arad Z (2010) Heat shock proteins and resistance to desiccation in congeneric land snails. Cell Stress Chaperones 15:351–363. doi:10.1007/s12192-009-0150-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mizrahi T, Heller J, Goldenberg S, Arad Z (2012a) Heat shock proteins and survival strategies in congeneric land snails (Sphincterochila) from different habitats. Cell Stress Chaperones 17:523–527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mizrahi T, Heller J, Goldenberg S, Arad Z (2012b) The heat shock response in congeneric land snails (Sphincterochila) from different habitats. Cell Stress Chaperones 17:639–645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakano K, Iwama G (2002) The 70-kDa heat shock protein response in two intertidal sculpins, Oligocottus maculosus and O. snyderi: relationship of hsp70 and thermal tolerance. Comp Biochem Physiol A Mol Integr Physiol 133:79–94

    Article  PubMed  Google Scholar 

  • Narum SR, Campbell NR, Meyer KA, Miller MR, Hardy RW (2013) Thermal adaptation and acclimation of ectotherms from differing aquatic climates. Mol Ecol 22:3090–3097

    Article  PubMed  Google Scholar 

  • Nollen EA, Morimoto RI (2002) Chaperoning signaling pathways: molecular chaperones as stress-sensing ‘heat shock’ proteins. J Cell Sci 115:2809–2816

    CAS  PubMed  Google Scholar 

  • Pantzartzi CN, Kourtidis A, Drosopoulou E, Yiangou M, Scouras ZG (2009) Isolation and characterization of two cytoplasmic hsp90s from Mytilus galloprovincialis (Mollusca: Bivalvia) that contain a complex promoter with a p53 binding site. Gene 431:47–54. doi:10.1016/j.gene.2008.10.028

    Article  CAS  PubMed  Google Scholar 

  • Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669

    Article  Google Scholar 

  • Parmesan C et al (1999) Poleward shifts in geographical ranges of butterfly species associated with regional warming. Nature 399:579–583

    Article  CAS  Google Scholar 

  • Pfenninger M, Eppenstein A, Magnin F (2003) Evidence for ecological speciation in the sister species Candidula unifasciata (Poiret, 1801) and C. rugosiuscula (Michaud, 1831) (Helicellinae, Gastropoda). Biol J Linn Soc 79:611–628

    Article  Google Scholar 

  • Portner HO (2002) Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals. Comp Biochem Physiol A Mol Integr Physiol 132:739–761

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Ramnanan CJ, Allan ME, Groom AG, Storey KB (2009) Regulation of global protein translation and protein degradation in aerobic dormancy. Mol Cell Biochem 323:9–20

    Article  CAS  PubMed  Google Scholar 

  • Reuner A, Brümmer F, Schill RO (2008) Heat shock proteins (Hsp70) and water content in the estivating Mediterranean Grunt Snail (Cantareus apertus). Comp Biochem Physiol B 151:28–31

    Article  PubMed  Google Scholar 

  • Riddle WA (1983) Physiological ecology of land snails and slugs. In: Russell-Hunter WD (ed) The Mollusca, vol 6. Academic, London, pp 431–461

    Google Scholar 

  • Sanders BM, Hope C, Pascoe VM, Martin LS (1991) Characterization of the stress protein response in two species of Collisella limpets with different temperature tolerances. Physiol Zool 64:1471–1489

    Article  CAS  Google Scholar 

  • Scheil AE, Kohler HR, Triebskorn R (2011) Heat tolerance and recovery in Mediterranean land snails after pre-exposure in the field. J Molluscan Stud 77:165–174

    Article  Google Scholar 

  • Somero GN (1995) Proteins and temperature. Annu Rev Physiol 57:43–68

    Article  CAS  PubMed  Google Scholar 

  • Somero GN (2005) Linking biogeography to physiology: evolutionary and acclimatory adjustments of thermal limits. Front Zool 2:1–9

    Article  PubMed  PubMed Central  Google Scholar 

  • Sørensen JG, Dahlgaard J, Loeschcke V (2001) Genetic variation in thermal tolerance among natural populations of Drosophila buzzatii: down regulation of Hsp70 expression and variation in heat stress resistance traits. Funct Ecol 15:289–296

    Article  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, Michalak P, Justesen J, Loeschcke V (1999) Expression of the heat-shock protein HSP70 in Drosophila buzzatii lines selected for thermal resistance. Hereditas 131:155–164

    Article  PubMed  Google Scholar 

  • Sorte CJB, Hofmann GE (2005) Thermotolerance and heat-shock protein expression in Northeastern Pacific Nucella species with different biogeographical ranges. Mar Biol 146:985–993

    Article  CAS  Google Scholar 

  • Stillman JH, Somero GN (2000) A comparative analysis of the upper thermal tolerance limits of eastern Pacific porcelain crabs, genus Petrolisthes: influences of latitude, vertical zonation, acclimation, and phylogeny. Physiol Biochem Zool 73:200–208. doi:10.1086/316738

    Article  CAS  PubMed  Google Scholar 

  • Storey KB (2002) Life in the slow lane: molecular mechanisms of estivation. Comp Biochem Physiol A Mol Integr Physiol 133:733–754

    Article  PubMed  Google Scholar 

  • Teshima H et al (2003) The evolution of extreme shell shape variation in the land snail Ainohelix editha: a phylogeny and hybrid zone analysis. Mol Ecol 12:1869–1878

    Article  PubMed  Google Scholar 

  • Todgham AE, Iwama GK, Schulte PM (2006) Effects of the natural tidal cycle and artificial temperature cycling on Hsp levels in the tidepool sculpin Oligocottus maculosus. Physiol Biochem Zool 79:1033–1045. doi:10.1086/507664

    Article  CAS  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 

  • Troschinski S, Di Lellis MA, Sereda S, Hauffe T, Wilke T, Triebskorn R, Kohler HR (2014) Intraspecific variation in cellular and biochemical heat response strategies of Mediterranean Xeropicta derbentina [Pulmonata, Hygromiidae]. PLoS One 9, e86613. doi:10.1371/journal.pone.0086613

    Article  PubMed  PubMed Central  Google Scholar 

  • Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3, RESEARCH0034

    Article  PubMed  PubMed Central  Google Scholar 

  • Visser ME (2008) Keeping up with a warming world; assessing the rate of adaptation to climate change. Proc Biol Sci 275:649–659. doi:10.1098/rspb.2007.0997

    Article  PubMed  PubMed Central  Google Scholar 

  • Wade CM, Mordan PB (2000) Evolution within the gastropod molluscs; using the ribosomal RNA gene-cluster as an indicator of phylogenetic relationships. J Molluscan Stud 66:565–570

    Article  Google Scholar 

  • Watanabe Y, Chiba S (2001) High within-population mitochondrial DNA variation due to microvicariance and population mixing in the land snail Euhadra quaesita (Pulmonata: Bradybaenidae). Mol Ecol 10:2635–2645

    Article  CAS  PubMed  Google Scholar 

  • Young JC, Moarefi I, Hartl FU (2001) Hsp90: a specialized but essential protein-folding tool. J Cell Biol 154:267–273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zatsepina OG et al (2001) A Drosophila melanogaster strain from sub-equatorial Africa has exceptional thermotolerance but decreased Hsp70 expression. J Exp Biol 204:1869–1881

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We wish to express our gratitude to Dr. Carola Greve (KOENIG museum, Bonn, Germany) for providing research material, to Ido Izhaki for his help with the statistical analysis, and to the Life Sciences and Engineering Infrastructure Center for their help with the qPCR analysis. This work was supported by the Israel Science Foundation grant no. 537/11 and the Russell Berrie Nanotechnology Institute.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zeev Arad.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Table 1

Amplicon sequences (5′-3′) for T. pisana hsp70, hsp90, actin and Elongation factor 1α (PPTM 40 kb)

Supplementary Table 2

Analysis of the effect of acclimation to laboratory conditions on HSP levels. (a) Independent T-test comparisons within each population of HSP levels between field collected snails and acclimated snails. P values are reported for each population. (b-d) Post hoc comparisons between populations of HSP levels. P values are reported for each state: upper p values for field collected snails; lower p values for acclimated snails (PPTM 51 kb)

Supplementary Table 3

Analysis of the intensities of induction of hsp70 and hsp90 mRNAs in response to heat stress in T. pisana populations. (a) Peak values for hsp70 and hsp90 mRNA induction (n = 5) (relative to control, means ± SE). (b) Post hoc comparisons between populations of peak values of hsp70 mRNA induction. (c) Post hoc comparisons between populations of peak values of hsp90 mRNA induction (PPTM 49 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mizrahi, T., Goldenberg, S., Heller, J. et al. Geographic variation in thermal tolerance and strategies of heat shock protein expression in the land snail Theba pisana in relation to genetic structure. Cell Stress and Chaperones 21, 219–238 (2016). https://doi.org/10.1007/s12192-015-0652-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12192-015-0652-6

Keywords

Navigation