Skip to main content

Different Trends in the Evolution of Heat Shock Genes System

  • Chapter
  • First Online:
  • 763 Accesses

Abstract

In Chap. 4 we described characteristic differences in the thermoresistance and Hsp synthesis patterns in various organisms including vertebrates, insects, Crustacea etc. Striking differences observed in Hsp synthesis in response to HS in close and phylogenetically distant forms could be due to different molecular mechanisms. It is possible to suggest that thermoresistant species may contain higher copy numbers of Hsp70 genes as compared to related species from cold and temperate climates. However, this is an exception rather than a general rule. Thus, Southern blot analysis of genomic DNA has shown that lizard species sharply different in the constitutive level and kinetics of Hsp70 synthesis in response to temperature elevation (i.e. L. vivipara and P. interscapularis) not only preserved the same number of Hsp70 genes but also retained their practically identical structure and arrangement in the genome. It is noteworthy, that the species compared belong to different subfamilies that diverged millions years ago. On the other hand, the comparison of hsf1 genes in these two lizard species demonstrated striking differences in their structure (Zatsepina et al. 2000). These data suggest high conservatism for Hsp70 genes in the investigated lizard species. Therefore, it is plausible to conclude that the observed differences in the HSR resulted not from different copy number but may be due to peculiarities of the regulatory machinery of heat shock genes in various organisms.

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

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD   109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Archibald JM, Logsdon JM Jr, Doolittle WF (2000) Origin and evolution of eukaryotic chaperonins: phylogenetic evidence for ancient duplications in CCT genes. Mol Biol Evol 17:1456–1466

    Article  PubMed  CAS  Google Scholar 

  • Astakhova LN, Zatsepina OG, Przhiboro AA, Evgen’ev MB, Garbuz DG (2013) Novel arrangement and comparative analysis of hsp90 family genes in three thermotolerant species of Stratiomyidae (Diptera). Insect Mol Biol 22:284–296

    Article  PubMed  CAS  Google Scholar 

  • Ayme A, Tissieres A (1985) Locus 67B of Drosophila melanogaster contains seven, not four, closely related heat shock genes. EMBO J 4:2949–2954

    PubMed  CAS  PubMed Central  Google Scholar 

  • Benedict MQ, Cockburn AF, Seawright JA (1993) The Hsp70 heat-shock gene family of the mosquito Anopheles albimanus. Insect Mol Biol 2:93–102

    Article  PubMed  CAS  Google Scholar 

  • Benedict MQ, Levine BJ, Ke ZX, Cockburn AF, Seawright JA (1996) Precise limitation of concerted evolution to ORFs in mosquito Hsp82 genes. Insect Mol Biol 5:73–79

    Article  PubMed  CAS  Google Scholar 

  • Bettencourt BR, Feder ME (2001) Hsp70 duplication in the Drosophila melanogaster species group: how and when did two become five? Mol Biol Evol 18:1272–1282

    Article  PubMed  CAS  Google Scholar 

  • Bettencourt BR, Feder ME (2002) Rapid concerted evolution via gene conversion at the Drosophila hsp70 genes. J Mol Evol 54:569–586

    Article  PubMed  CAS  Google Scholar 

  • Bork P, Sander C, Valencia A (1992) An ATPase domain common to prokaryotic cell cycle proteins, sugar kinases, actin, and hsp70 heat shock proteins. Proc Natl Acad Sci U S A 89:7290–7294

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Cameron PU, Tabarias HA, Pulendran B, Robinson W, Dawkins RL (1990) Conservation of the central MHC genome: PFGE mapping and RFLP analysis of complement, HSP70, and TNF genes in the goat. Immunogenetics 31:253–264

    Article  PubMed  CAS  Google Scholar 

  • Campo D, Lehmann K, Fjeldsted C, Souaiaia T, Kao J, Nuzhdin SV (2013) Whole-genome sequencing of two North American Drosophila melanogaster populations reveals genetic differentiation and positive selection. Mol Ecol 22:5084–5097

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Chen B, Zhong D, Monteiro A (2006) Comparative genomics and evolution of the HSP90 family of genes across all kingdoms of organisms. BMC Genomics 7:156

    Article  PubMed  PubMed Central  Google Scholar 

  • Dragon E, Sias S, Kato E, Gabe J (1978) The genome of Trypanosoma cruzi contains a constitutively expressed, tandemly arranged multicopy gene homologous to a major heat shock protein. Mol Cell Biol 7:1271–1275

    Google Scholar 

  • Evgen’ev MB, Kolchinski A, Levin A, Preobrazhenskaya AL, Sarkisova E (1978) Heat-shock DNA homology in distantly related species of Drosophila. Chromosoma 68:357–365

    Article  PubMed  Google Scholar 

  • Evgen’ev MB, Zatsepina OG, Garbuz D, Lerman DN, Velikodvorskaya V et al (2004) Evolution and arrangement of the hsp70 gene cluster in two closely related species of the virilis group of Drosophila. Chromosoma 113:223–232

    Article  PubMed  Google Scholar 

  • Feder M (1997) Necrotic fruit: a novel model system for thermal ecologists. J Therm Biol 22:1–9

    Article  Google Scholar 

  • Feder ME, Cartano NV, Milos L, Krebs RA, Lindquist SL (1996) Effect of engineering hsp70 copy number on Hsp70 expression and tolerance of ecologically relevant heat shock in larvae and pupae of Drosophila melanogaster. J Exp Biol 199:1837–1844

    PubMed  CAS  Google Scholar 

  • Felts SJ, Owen BA, Nguyen P, Trepel J, Donner DB, Toft DO (2000) The hsp90-related protein TRAP1 is a mitochondrial protein with distinct functional properties. J Biol Chem 275:3305–3312

    Article  PubMed  CAS  Google Scholar 

  • Flajnik MF, Canel C, Kramer J, Kasahara M (1991) Which came first, MHC class I or class II? Immunogenetics 33:295–300

    Article  PubMed  CAS  Google Scholar 

  • Garbuz D, Evgenev MB, Feder ME, Zatsepina OG (2003) Evolution of thermotolerance and the heat-shock response: evidence from inter/intraspecific comparison and interspecific hybridization in the virilis species group of Drosophila. I. Thermal phenotype. J Exp Biol 206:2399–2408

    Article  PubMed  CAS  Google Scholar 

  • Garbuz DG, Zatsepina OG, Przhiboro AA, Yushenova I, Guzhova IV, Evgen’ev MB (2008) Larvae 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 

  • Garbuz DG, Astakhova LN, Zatsepina OG, Arkhipova IR, Nudler E, Evgen’ev MB (2011a) Functional organization of hsp70 cluster in camel (Camelus dromedarius) and other mammals. PLoS One 6:e27205

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Garbuz DG, Yushenova IA, Zatsepina OG, Przhiboro AA, Bettencourt BR, Evgen’ev MB (2011b) Organization and evolution of hsp70 clusters strikingly differ in two species of Stratiomyidae (Diptera) inhabiting thermally contrasting environments. BMC Evol Biol 11:74

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Glass D, Polvere RI, Van der Ploeg LHT (1986) Conserved sequences and transcription of the hsp70 gene family in Trypanosoma brucei. Mol Cell Biol 6:4657–4666

    PubMed  CAS  PubMed Central  Google Scholar 

  • Gupta RS, Singh B (1992) Cloning of the HSP70 gene from Halobacterium marismortui: relatedness of archaebacterial HSP70 to its eubacterial homologs and a model for the evolution of the HSP70 gene. J Bacteriol 174:4594–4605

    PubMed  CAS  PubMed Central  Google Scholar 

  • Hackett RW, Lis JT (1981) DNA sequence analysis reveals extensive homologies of regions preceding hsp70 and alphabeta heat shock genes in Drosophila melanogaster. Proc Natl Acad Sci U S A 78:6196–6200

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Hansen JJ, Bross P, Westergaard M, Nielsen MN, Eiberg H et al (2003) Genomic structure of the human mitochondrial chaperonin genes: HSP60 and HSP10 are localised head to head on chromosome 2 separated by a bidirectional promoter. Hum Genet 112:71–77

    Article  PubMed  CAS  Google Scholar 

  • Hart C, Zhao K, Laemmli U (1997) The scs’ boundary element: characterization of boundary element-associated factors. Mol Cell Biol 17:999–1009

    PubMed  CAS  PubMed Central  Google Scholar 

  • Heschl MF, Baillie DL (1989) Characterization of the hsp70 multigene family of Caenorhabditis elegans. DNA 8:233–243

    Article  PubMed  CAS  Google Scholar 

  • Heschl MF, Baillie DL (1990) The HSP70 multigene family of Caenorhabditis elegans. Comp Biochem Physiol B 96:633–637

    PubMed  CAS  Google Scholar 

  • Holmgren R, Livak K, Morimoto RI, Frend R, Meselson M (1979) Studies of cloned sequences from four Drosophila heat shock loci. Cell 18:1359–1370

    Article  PubMed  CAS  Google Scholar 

  • Hughes AL, Nei M (1993) Evolutionary relationships of the classes of major histocompatibility complex genes. Immunogenetics 37:337–346

    Article  PubMed  CAS  Google Scholar 

  • Hunt C, Morimoto RI (1985) Conserved features of eukaryotic hsp70 genes revealed by comparison with the nucleotide sequence of human hsp70. Proc Natl Acad Sci U S A 82:6455–6459

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Hunt CR, Gasser DL, Chaplin DD, Piers JC, Kozak CA (1993) Chromosomal localization of five murine HSP70 gene family members: Hsp70-1, Hsp70-2, Hsp70-3, Hsp70t and Grp78. Genomics 16:193–198

    Article  PubMed  CAS  Google Scholar 

  • Hurley JH (1996) The sugar kinase/heat shock protein 70/actin superfamily: implications of conserved structure for mechanism. Annu Rev Biophys Biomol Struct 25:137–162

    Article  PubMed  CAS  Google Scholar 

  • Kampinga HH, Hageman J, Vos MJ, Kubota H, Tanguay RM et al (2009) Guidelines for the nomenclature of the human heat shock proteins. Cell Stress Chaperones 14:105–111

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kellett M, McKechnie SW (2005) A cluster of diagnostic Hsp68 amino acid sites that are identified in Drosophila from the melanogaster species group are concentrated around beta-sheet residues involved with substrate binding. Genome 48:226–233

    Article  PubMed  CAS  Google Scholar 

  • Kim S, Willison KR, Horwich AL (1994) Cystosolic chaperonin subunits have a conserved ATPase domain but diverged polypeptide-binding domains. Trends Biochem Sci 19:543–548

    Article  PubMed  CAS  Google Scholar 

  • Konstantopoulou I, Nikolaidis N, Scouras ZG (1998) The hsp70 locus of Drosophila auraria (montium subgroup) is single and contains copies in a conserved arrangement. Chromosoma 107:577–586

    Article  PubMed  CAS  Google Scholar 

  • Krebs RA (1999) A comparison of Hsp70 expression and thermotolerance in adults and larvae of three Drosophila species. Cell Stress Chaperones 4:243–249

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Lakhotia SC, Prasanth KV (2002) Tissue- and development-specific induction and turnover of hsp70 transcripts from loci 87A and 87C after heat shock and during recovery in Drosophila melanogaster. J Exp Biol 205:345–358

    PubMed  CAS  Google Scholar 

  • Lee-Yoon D, Easton D, Murawski M, Burd R, Subjeck JR (1995) Identification of a major subfamily of large hsp70-like proteins through the cloning of the mammalian 110-kDa heat shock protein. J Biol Chem 270:15725–15733

    Article  PubMed  CAS  Google Scholar 

  • Leigh Brown AJ, Ish-Horowicz D (1981) Evolution of the 87A and 87C heat-shock loci in Drosophila. Nature 290:677–682

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Livak KJ, Freund R, Schweber M, Wensink PC, Meselson M (1978) Sequence organization and transcription at two heat shock loci in Drosophila. Proc Natl Acad Sci U S A 75:5613–5617

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Marzluff WF, Gongidi P, Woods KR, Jin J, Maltais LJ (2002) The human and mouse replication-dependent histone genes. Genomics 80:487–498

    Article  PubMed  CAS  Google Scholar 

  • Maside X, Bartolome C, Charlesworth B (2002) S-element insertions are associated with the evolution of the Hsp70 genes in Drosophila melanogaster. Curr Biol 12:1686–1691

    Article  PubMed  CAS  Google Scholar 

  • Maynard JC, Pham T, Zheng T, Jockheck-Clark A, Rankin HB et al (2010) Gp93, the Drosophila GRP94 ortholog, is required for gut epithelial homeostasis and nutrient assimilation-coupled growth control. Dev Biol 339:295–306

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Miller WJ, Nagel A, Bachmann J, Bachmann L (2000) Evolutionary dynamics of the SGM transposon family in the Drosophila obscura species group. Mol Biol Evol 17:1597–1609

    Article  PubMed  CAS  Google Scholar 

  • Milner CM, Campbell RD (1990) Structure and expression of the three MHC-linked HSP70 genes. Immunogenetics 32:242–251

    Article  PubMed  CAS  Google Scholar 

  • Milner CM, Campbell RD (1992) Polymorphic analysis of three MHC-linked HSP70 genes. Immunogenetics 36:357–362

    Article  PubMed  CAS  Google Scholar 

  • Muhich ML, Boothroyd JC (1989) Synthesis of Trypanosome hsp70 mRNA is resistant to disruption of trans-splicing by heat shock. J Biol Chem 264:7107–7110

    PubMed  CAS  Google Scholar 

  • Patterson JT, Stone WS (1952) Evolution in the genus Drosophila. The Macmillan Company, New York, p 610

    Google Scholar 

  • Petesch SJ, Lis JT (2008) Rapid, transcription-independent loss of nucleosomes over a large chromatin domain at Hsp70 loci. Cell 134:74–84

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Rippmann F, Taylor WR, Rothbard JB, Green NM (1991) A hypothetical model for the peptide binding domain of hsp70 based on the peptide binding domain of HLA. EMBO J 10:1053–1059

    PubMed  CAS  PubMed Central  Google Scholar 

  • Ryan MT, Herd SM, Sberna G, Samuel MM, Hoogenraad NJ, Høj PB (1997) The genes encoding mammalian chaperonin 60 and chaperonin 10 are linked head-to-head and share a bidirectional promoter. Gene 196:9–17

    Article  PubMed  CAS  Google Scholar 

  • Salter-Cid L, Kasahara M, Flajnik MF (1994) Hsp70 genes are linked to the Xenopus major histocompatibility complex. Immunogenetics 39:1–7

    Article  PubMed  CAS  Google Scholar 

  • Segal R, Ron EZ (1996) Regulation and organization of the groE and dnaK operons in Eubacteria. FEMS Microbiol Lett 138:1–10

    Article  PubMed  CAS  Google Scholar 

  • Shapira M, Pinelli E (1989) Heat-shock protein 83 of Leishmania mexicana amazonensis is an abundant cytoplasmic protein with a tandemly repeated genomic arrangement. Eur J Biochem 185:231–236

    Article  PubMed  CAS  Google Scholar 

  • Smith TM, Kirley TL (1999) Site-directed mutagenesis of a human brain ecto-apyrase: evidence that the E-type ATPases are related to the actin/heat shock 70/sugar kinase superfamily. Biochemistry 38:321–328

    Article  PubMed  CAS  Google Scholar 

  • Sørensen JG, Nielsen MM, Kruhøffer M, Justesen J, Loeschcke V (2005) Full genome gene expression analysis of the heat stress response in Drosophila melanogaster. Cell Stress Chaperones 10:312–328

    Article  PubMed  PubMed Central  Google Scholar 

  • Southgate R, Mirault M, Ayme A, Tissieres A (1985) Organization, sequences and induction of heat shock genes. In: Changes in eukaryotic gene expression in response to environmental stress. Academic, New York, pp 3–30

    Chapter  Google Scholar 

  • Spicer G, Bell C (2002) Molecular phylogeny of the Drosophila virilis species group (Diptera: Drosophilidae) inferred from mitochondrial 12S and 16S ribosomal RNA genes. Ann Entomol Soc Am 95:156–161

    Article  CAS  Google Scholar 

  • Throckmorton L (1982) The virilis species group, pp. 227–296 in The Genetics and Biology of Drosophila, 3b, edited by M. ASHBURNER and E. NOVITSKY. Academic Press, New York

    Google Scholar 

  • Velikodvorskaia VV, Lyozin GT, Feder ME, Evgen’ev MB (2005) Unusual arrangement of the hsp68 locus in the virilis species group of Drosophila implicates evolutionary loss of an hsp68 gene. Genome 48:234–240

    Article  PubMed  CAS  Google Scholar 

  • Walter L, Rauh F, Gunther E (1994) Comparative analysis of the three major histocompatibility complex-linked heat shock protein 70 (hsp70) genes of the rat. Immunogenetics 40:325–330

    Article  PubMed  CAS  Google Scholar 

  • Yang Y, Ye H, Huang H, Li S, Liu X, Zeng X, Gong J (2013a) Expression of Hsp70 in the mud crab, Scylla paramamosain in response to bacterial, osmotic, and thermal stress. Cell Stress Chaperones 18:475–482

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Yang Y, Ye H, Huang H, Li S, Zeng X, Gong J, Huang X (2013b) Characterization and expression of SpHsp60 in hemocytes after challenge to bacterial, osmotic and thermal stress from the mud crab Scylla paramamosain. Fish Shellfish Immunol 35:1185–1191

    Article  PubMed  CAS  Google Scholar 

  • Zatsepina OG, Ulmasov KA, Beresten SF, Molodtsov VB, Rybtsov SA, Evgen’ev MB (2000) Thermotolerant desert lizards characteristically differ in terms of heat-shock system regulation. J Exp Biol 203:1017–1025

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Evgen’ev, M.B., Garbuz, D.G., Zatsepina, O.G. (2014). Different Trends in the Evolution of Heat Shock Genes System. In: Heat Shock Proteins and Whole Body Adaptation to Extreme Environments. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-9235-6_5

Download citation

Publish with us

Policies and ethics