Journal of Biosciences

, Volume 32, Issue 3, pp 489–499 | Cite as

Molecular mechanisms underlying thermal adaptation of xeric animals

  • M B Evgen’evEmail author
  • D G Garbuz
  • V Y Shilova
  • O G Zatsepina


For many years, we and our collaborators have investigated the adaptive role of heat shock proteins in different animals, including the representatives of homothermic and poikilothermic species that inhabit regions with contrasting thermal conditions. Adaptive evolution of the response to hyperthermia has led to different results depending upon the species. The thermal threshold of induction of heat shock proteins in desert thermophylic species is, as a rule, higher than in the species from less extreme climates. In addition, thermoresistant poikilothermic species often exhibit a certain level of heat shock proteins in cells even at a physiologically normal temperature. Furthermore, there is often a positive correlation between the characteristic temperature of the ecological niche of a given species and the amount of Hsp70-like proteins in the cells at normal temperature. Although in most cases adaptation to hyperthermia occurs without changes in the number of heat shock genes, these genes can be amplified in some xeric species. It was shown that mobile genetic elements may play an important role in the evolution and fine-tuning of the heat shock response system, and can be used for direct introduction of mutations in the promoter regions of these genes.


Adaptation heat shock genes Hsp mobile elements promoters thermoresistance 


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  1. Belikov S V and Karpov V L 1996 Mapping Protein-DNA Interaction with CIS-DDP: Chromatine Structure of Promoter Region of Hsp70 Gene; Biochem. Mol. Biol. Int. 38 997–1002PubMedGoogle Scholar
  2. Bettencourt B R and Feder M E 2002 Rapid concerted evolution via gene conversion at the Hsp70 genes; J. Mol. Evol. 54 569–586PubMedCrossRefGoogle Scholar
  3. Buckley B A and Hofmann G E 2002 Thermal acclimation changes DNA-binding activity of heat shock factor 1 (HSF1) in the goby: implications for plasticity in the heat-shock response in natural populations; J. Exp. Biol. 205 3231–3240PubMedGoogle Scholar
  4. Diamant S, Eliahu N, Rosenthal D and Goloubinoff P 2001 Chemical chaperones regulate molecular chaperones in vitro and in cells under combined salt and heat sresses; J. Biol. Chem. 276 39586–39591PubMedCrossRefGoogle Scholar
  5. Duncan R F 2005 Inhibition of Hsp90 function delays and impairs recovery from heat shock; FEBS J. 272 5244–5256PubMedCrossRefGoogle Scholar
  6. Evgen’ev M B, Kolchinski A, Levin A, Preobrazhenskaya A L and Sarkisova E 1978 Heat-shock DNA homology in distantly related species of Drosophila; Chromosoma 68 357–365PubMedCrossRefGoogle Scholar
  7. Evgen’ev M B, Sheinker V S and Levin A V, et al 1987 Molecular Mechanisms of Adaptation to Hyperthermia in Higher Organisms. Synthesis of Heat-Shock Proteins in Cell Cultures and Larvae of Certain Silkworm Species; Mol. Biol. 21 484–494Google Scholar
  8. Evgen’ev M B, Zatsepina O G, Garbuz D G, Lerman D, Velikodvorskaya V, Zelentsova E and Feder M E 2004 Evolution and arrangement of the Hsp70 gene cluster in two closely related species of the virilis group of Drosophila; Chromosoma 113 223–232PubMedCrossRefGoogle Scholar
  9. Evgen’ev M B, Garbuz D G, Zatsepina O G 2005 Heat shock proteins: functions and role in adaptation to hyperthermia; Ontogenez (Rus.) 36 265–273Google Scholar
  10. Feder M E and Hofmann G E 1998 Evolutionary and ecological physiology of heat-shock proteins and the heat-shock response: A comprehensive bibliography; Suppl. Annu. Rev. Physiol. 61 http://www.annurev.arg/sup/material.htm
  11. Feder M E and Hofmann G E 1999 Heat-Shock Proteins, Molecular Chaperones, and the Stress Response, Evolutionary and Ecological Phisiology; Annu. Rev. Physiol. 61 243–282PubMedCrossRefGoogle Scholar
  12. Fujikake N, Nagai Y, Popiel H A, Kano H, Yamaguchi M and Toda T 2005 Alternative splicing regulates the transcriptional activity of heat shock factor in response to heat/cold stress; FEBS Lett. 579 3842–3848PubMedCrossRefGoogle Scholar
  13. Garbuz D G, Molodtsov V B, Velikodvorskaya V V, Evgen’ev M B and Zatsepina O G 2002 Evolution of the response to heat shock in genus; Genetika (Rus.) 38 1097–1109Google Scholar
  14. Garbuz D G, Evgenev M B, Feder M E and Zatsepina O G 2003 Evolution of thermotolerance and the heat-shock response: evidence from inter/intraspecific comparison and interspecific hybridization in the species group of I. Thermal phenotype; J. Exp. Biol. 206 2399–2408PubMedCrossRefGoogle Scholar
  15. Gehring W J and Wehner R 1995 Heat shock protein synthesis and thermotolerance in, an ant from the Sahara desert; Proc. Natl. Acad. Sci. USA 92 2994–2998PubMedCrossRefGoogle Scholar
  16. Gong W J and Golic K G 2006 Loss of Hsp70 in is pleiotropic, with effects on thermotolerance, recovery from heat shock and neurodegeneration; Proc. Natl. Acad. Sci. USA 172 275–286Google Scholar
  17. Ish-Horowicz D S, Pinchin J, Gausz H, Gyurkovics G and Bencze G et al 1979 Deletion mapping of two loci that code for the 70,000 dalton heat-induced protein; Cell 17 565–571PubMedCrossRefGoogle Scholar
  18. Krebs RA and Feder M E 1997 Deleterious consequences of Hsp70 overexpression in larvae; Cell Stress Chaperones 2 60–71PubMedCrossRefGoogle Scholar
  19. Lakhotia S C and Prasanth K V 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. 205 345–358PubMedGoogle Scholar
  20. Lebedeva L A, Nabirochkina E N, Kurshakova M M, Flavie R, Krasnov A N, Evgen’ev M B, Kadonaga J T, Georgieva S G and La’szlo’ Tora 2005 Occupancy of the Hsp70 promoter by a subset of basal transcription factors diminishes upon transcriptional activation; Proc. Natl. Acad. Sci. USA 102 18087–18092PubMedCrossRefGoogle Scholar
  21. Leigh Brown A J and Ish-Horowicz D 1981 Evolution of the 87A and 87C heat-shock loci in Drosophila; Nature (London) 290 677–682CrossRefGoogle Scholar
  22. Lerman D N, Michalak P, Helin A B, Bettencourt B R and Feder M E 2003 Modification of Heat-Shock Gene Expression in Populations via Transposable Elements; Mol. Biol. Evol. 20 135–144PubMedCrossRefGoogle Scholar
  23. Lewis M J, Helmsing P and Ashburner M 1975 Parallel changes in puffing activity and patterns of protein synthesis in salivary glands of Drosophila; Proc. Natl. Acad. Sci. USA 72 3604–36608PubMedCrossRefGoogle Scholar
  24. Lindquist S 1986 The heat-shock response; Annu. Rev. Biochem. 55 1151–1191PubMedCrossRefGoogle Scholar
  25. Lindquist S and Kim G 1996 Heat-shock protein 104 expression is sufficient for thermotolerance in yeast; Proc. Natl. Acad. Sci. USA 93 5301–5306PubMedCrossRefGoogle Scholar
  26. Lozovskaya E R and Evgen’ev M B 1984 Heat Shock in and Regulation of Genome Activity; Mol. Bio. (Russian) 20 142–185Google Scholar
  27. Lyashko V N, Vikulova V K, Chernicov V G, Ivanov V I, Ulmasov K A, Zatsepina O G and Evgen’ev M B 1994 Comparison of the heat shock response in ethnically and ecologically different human populations; Proc. Natl. Acad. Sci. USA 91 12492–12495PubMedCrossRefGoogle Scholar
  28. Margulis B A and Guzhova I V 2000 Stress Proteins in Eukaryotic Cell; Cytology (Russian) 42 323–342Google Scholar
  29. Morimoto R J, Jolly C, Satyal S, Mathew A, Shi Y and Kitagawa K 1999 Molecular chaperones and the heat shock response; Br. J. Cancer 80 S19Google Scholar
  30. Morrow G, Heikkila J J and Tanguay RM 2006 Differences in the chaperone-like activities of the four main small heat shock proteins of; Cell Stress Chaperones 11 51–60PubMedCrossRefGoogle Scholar
  31. Neal S J, Karunanithy S, Best A, Ken-Choy-So A, Tanguay R M, Atwood H L and Westwood J T 2005 Thermoprotection of synaptic transmission in a heat shock factor mutant is accompanied by increased expression of Hsp83 and DnaJ-1; Physiol. Genomics 25 493–501Google Scholar
  32. Norris C E, diTorio P J, Schultz R J and Hightower L 1995 Variation in heat shock proteins within tropical and desert species of poeciliid fishes; Mol. Biol. Evol. 12 1048–1062PubMedGoogle Scholar
  33. Podrabsky J E and Somero G N 2004 Changes in gene expression associated with acclimation to constant temperatures and fluctuating daily temperatures in an annual killifish; J. Exp. Biol. 207 2237–2254PubMedCrossRefGoogle Scholar
  34. Rinehart J P, Hayward S A, Elnitsky M A, Sandro L H, Lee R E Jr and Denlinger D L. 2006 Continuous up-regulation of heat shock proteins in larvae, but not adults, of a polar insect; Proc. Natl. Acad. Sci. USA 38 14223–14227CrossRefGoogle Scholar
  35. Schlesinger M J et al (eds) 1982 Heat Shock: from bacteria to man; (New York: Cold Spring Harbor Lab) pp 440Google Scholar
  36. Shilova V Y, Garbuz D G, Myasyankina E N, Chen B, Evgen’ev M B, Feder M E and Zatsepina O G 2006 Remarkable site specificity of local transposition into the Hsp70 promoter of Drosophila melanogaster; Genetics 173 809–820PubMedCrossRefGoogle Scholar
  37. Sorensen J G, Dahlgaard J and Loeschke 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. 15 289–296CrossRefGoogle Scholar
  38. Sorensen J G, Kristensen T N and Loeschke V 2003 The evolutionary and ecological role of heat shock proteins; Ecol. Lett. 6 1025–1037CrossRefGoogle Scholar
  39. Tissieres A, Mitchel H K and Tracy U 1974 Protein synthesis in salivary glands of relation to chromosome puffs; J. Mol. Biol. 84 389–398PubMedCrossRefGoogle Scholar
  40. Timakov B, Liu X, Turgut I and Zhang P 2002 Timing and Targeting of P-Element Local Transposition in the Male Germline Cells of Drosophila melanogaster; Genetics 160 1011–1022PubMedGoogle Scholar
  41. Tomanek L 2005 Two-dimensional gel analysis of the heat-shock response in marine snails (genus): interspecific variation in protein expression and acclimation ability; J. Exp. Biol. 208 3133–3143PubMedCrossRefGoogle Scholar
  42. Tomanek L and Somero G N 1999 Evolutionary and acclimation-induced variation in the heat-shock responses of congeneric marine snails (genus) from different thermal habitats: implications for limits of thermotolerance and biogeography; J. Exp. Biol. 202 2925–2936PubMedGoogle Scholar
  43. Tomanek L and Somero G N 2002 Interspecific-and acclimation-induced variation in levels of heat-shock proteins 70 (Hsp70) and 90 (Hsp90) and heat-shock transcription factor-1 (HSF1) in congeneric marine snails (genus): implications for regulations of Hsp gene expression; J. Exp. Biol. 205 677–685PubMedGoogle Scholar
  44. Udvardy A, Maine E and Schedl P 1985 The 87A7 chromomere. Identification of novel chromatin structures flanking the heat shock locus that may define the boundaries of higher order domains; J. Mol. Biol. 185 341–358PubMedCrossRefGoogle Scholar
  45. Ulmasov K A, Ovezmukhammedov A, Karaev K K and Evgen’ev M B 1988 Molecular Mechanisms of Adaptation to Hypothermia in Higher Organisms. 3. Induction of Heat Shock Proteins in Two Species; Mol. Biol. (Russian) 22 1583–1589Google Scholar
  46. Ulmasov KA, Shammakov S, Karavaev K and Evgen’ev M B 1992 Heat shock proteins and thermoresistance in lizards; Proc. Natl. Acad. Sci. USA 89 1666–1670PubMedCrossRefGoogle Scholar
  47. Ulmasov H A, Karaev K K, Lyashko V N and Evgen’ev M B 1993 Heat-shock response in camel 0 blood cells and adaptation to hyperthermia; Comp. Biochem. Physiol. 106 867–872CrossRefGoogle Scholar
  48. Ulmasov K A, Zatsepina O G, Molodtsov V B and Evgen’ev M B 1999 Natural body temperature and kinetics of heat shock protein synthesis in the toad-heated agamid lizard; Amphibia-Reptilia 20 1–9CrossRefGoogle Scholar
  49. Walser J C, Chen B and Feder M E 2006 Heat-Shock Promoters: Targets for Evolution by P Transposable Elements in; PLoS Genet 2 (in press)Google Scholar
  50. Wu C 1995 Heat Shock Transcription Factors: Structure and Regulation; Annu. Rev. Cell. Dev. Biol. 11 441–469PubMedCrossRefGoogle Scholar
  51. Zatsepina O G, Ulmasov K A, Beresten S F et al 2000 Thermotolerant desert lizards characteristically differ in terms of heat-shock system regulation; J. Exp. Biol. 203 1017–1025PubMedGoogle Scholar
  52. Zatsepina O G, Velikodvorskaia V V, Molodtsov V B, Garbuz D G, Lerman D N, Bettencourt B R, Feder M E and Evgenev M B 2001 A strain from sub-equatorial Africa has exceptional thermotolerance but decreased Hsp70 expression; J. Exp. Biol. 204 1869–1881PubMedGoogle Scholar
  53. Zatsepina O G, Karavanov A A, Garbuz D G, Shilova V, Tornatore P and Evgen’ev M B 2005 Use of surface-enhanced laser desorption ionization-time-of-flight to identify heat shock protein 70 isoforms in closely related species of the virilis group of Drosophila; Cell Stress Chaperones 10 12–16PubMedCrossRefGoogle Scholar

Copyright information

© Indian Academy of Sciences 2007

Authors and Affiliations

  • M B Evgen’ev
    • 1
    • 2
    Email author
  • D G Garbuz
    • 1
  • V Y Shilova
    • 1
  • O G Zatsepina
    • 1
  1. 1.Engelhardt Institute of Molecular BiologyRussian Academy of SciencesMoscowRussia
  2. 2.Institute of Cell BiophysicsRussian Academy of SciencesPushchino, Moscow RegionRussia

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