Experimental evolution of Hsp70 expression and thermotolerance in Drosophila melanogaster

Evolution

Volumn 53, Issue 2, 1999, Pages 484-492

  Bettencourt, Brian R ^a   Feder, Martin E ^a,b   Cavicchi, Sandro ^c  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

Acclimation; Drosophila; Experimental evolution; Heat shock proteins; Hsp70; Thermotolerance

Indexed keywords

EVOLUTION; TEMPERATURE TOLERANCE;

DIPTERA; DROSOPHILA MELANOGASTER; DROSOPHILIDAE;

EID: 0033044243     PISSN: 00143820     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1558-5646.1999.tb03783.x     Document Type: Article

References (52)

1. BENEDICT, M. Q., A. F. COCKBURN, AND J. A. SEAWRIGHT. 1993. The Hsp70 heat-shock gene family of the mosquito Anopheles albimanus. Insect Mol. Biol. 2:93-102.
2. BENNETT, A. E, AND R. E. LENSKI. 1996. Evolutionary adaptation to temperature. V. Adaptive mechanisms and correlated responses in experimental lines of Escherichia coli. Evolution 50:493-503.
3. BOON-NIERMEIJER, E. K., M. TUYL, AND H. VAN DE SCHEUR. 1986. Evidence for two states of thermotolerance. Int. J. Hyperthermia 2:93-106.
4. CAVICCHI, S., D. GUERRA, G. GIORGI, AND C. PEZZOLI. 1985. Temperature-related divergence in experimental populations of Drosophila melanogaster. I. Genetic and developmental basis of wing size and shape variation. Genetics 109:665-689.
5. CAVICCHI, S., D. GUERRA, V. NATALI, C. PEZZOLI, AND G. GIORGI. 1989. Temperature-related divergene in experimental populations of Drosophila melanogaster. II. Correlation between fitness and body dimensions. J. Evol. Biol. 2:235-251.
6. CAVICCHI, S., G. GIORGI, V. NATALI, AND D. GUERRA. 1991. Temperature-related divergence in experimental populations of Drosophila melanogaster. III. Fourier and centroid analysis of wing shape and relationship between shape variation and fitness. J. Evol. Biol. 4:141-159.
7. CAVICCHI, S., D. GUERRA, V. LA TORRE, AND R. B. HUEY. 1995. Chromosomal analysis of heat-shock tolerance in Drosophila melanogaster evolving at different temperatures in the laboratory. Evolution 49:676-684.
8. CHIPPINDALE, A. K., T. J. F. CHU, AND M. R. ROSE. 1996. Complex trade-offs and the evolution of starvation resistance in Drosophila melanogaster. Evolution 50:753-766.
9. COLOMBO, S. J., V. R. TIMMER, M. L. COLCLOUGH, AND E. BLUMWALD. 1995. Diurnal variation in heat tolerance and heat shock protein expression in black spruce (Picea mariana). Can. J. Forest Res. 25:369-375.
10. DIETZ, T. J. 1994. Acclimation of the threshold induction temperatures for 70-kDa and 90-kDa heat shock proteins in the fish Gillichthys mirabilis. J. Exp. Biol. 188:333-338.
11. DIIORIO, P. J., K. HOLSINGER, R. J. SCHULTZ, AND L. E. HIGHTOWER. 1996. Quantitative evidence that both Hsc70 and Hsp70 contribute to thermal adaptation in hybrids of the livebearing fishes Poeciliopsis. [published erratum appears in Cell Stress Chaperones 1:207]. Cell Stress Chaperones 1:139-147.
12. DJAWDAN, M., T. T. SUGIYAMA, L. K. SCHLAEGER, T. J. BRADLEY, AND M. R. ROSE. 1996. Metabolic aspects of the trade-off between fecundity and longevity in Drosophila melanogaster. Physiol. Zool. 69:1176-1195.
13. FADER, S. C., Z. YU, AND J. R. SPOTILA. 1994. Seasonal variation in heat shock proteins (hsp70) in stream fish under natural conditions. J. Therm. Biol. 19:335-341.
14. FEDER, J. H., J. M. ROSSI, J. SOLOMON, N. SOLOMON, AND S. LINDQUIST. 1992. The consequences of expressing Hsp70 in Drosophila cells at normal temperatures. Genes Dev. 6:1402-1413.
15. FEDER, M. E. 1996. Ecological and evolutionary physiology of stress proteins and the stress response: the Drosophila melanogaster model. Pp. 79-102 in I. A. Johnston and A. F. Bennett, eds. Animals and temperature: phenotypic and evolutionary adaptation. Cambridge Univ. Press, Cambridge, U.K.
16. FEDER, M. E., AND G. E. HOFMANN. 1999. Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu. Rev. Physiol. 61:243-282.
17. FEDER, M. E., N. V. CARTAÑO, L. MILOS, R. A. KREBS, AND S. L. LINDQUIST. 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.
18. FEDER, M. E., N. BLAIR, AND H. FIGUERAS. 1997. Natural thermal stress and heat-shock protein expression in Drosophila larvae and pupae. Funct. Ecol. 11:90-100.
19. FERNANDES, M., T. O'BRIEN, AND J. T. LIS. 1994. Structure and regulation of heat shock gene promoters. Pp. 375-394 in R. I. Morimoto, A. Tissieres, and C. Georgopoulos, eds. The biology of heat shock proteins and molecular chaperones. Cold Spring Harbor Laboratory Press, New York.
20. GLOOR, G. B., C. R. PRESTON, D. M. JOHNSON-SCHLITZ, N. A. NASSIF, R. W. PHILLIS, W. K. BENZ, H. M. ROBERTSON, AND W. R. ENGELS. 1993. Type I repressors of P element mobility. Genetics 135:81-95.
21. GUPTA, R. S., AND B. SINGH. 1994. Phylogenetic analysis of 70 kD heat shock protein sequences suggests a chimeric origin for the eukaryotic cell nucleus. Curr. Biol. 4:1104-1114.
22. HAZEL, J. R., AND C. L. PROSSER. 1974. Molecular mechanisms of temperature compensation in poikilotherms. Physiol. Rev. 54: 620-677.
23. HESS, M. A., AND R. F. DUNCAN. 1996. Sequence and structure determinants of Drosophila Hsp70 mRNA translation: 5′-UTR secondary structure specifically inhibits heat shock protein mRNA translation. Nucleic Acids Res. 24:2441-2449.
24. HOLMGREN, R., K. LIVAK, R. MORIMOTO, R. FREUND, AND M. MESELSON. 1979. Studies of cloned sequences from four Drosophila heat shock loci. Cell 18:1359-1370.
25. HOTTIGER, T., V. C. DE, W. BELL, T. BOLLER, AND A. WIEMKEN. 1992. The 70-kilodalton heat-shock proteins of the SSA subfamily negatively modulate heat-shock-induced accumulation of trehalose and promote recovery from heat stress in the yeast, Saccharomyces cerevisiae. Eur. J. Biochem. 210:125-132.
26. HUEY, R. B., T. WAKEFIELD, W. D. CRILL, AND G. W. GILCHRIST. 1995. Within- and between-generation effects of temperature on early fecundity of Drosophila melanogaster. Heredity 74:216-223.
27. ISH-HOROWICZ, D., S. M. PINCHIN, P. SCHEDL, T. S. ARTAVANIS, AND M. E. MIRAULT. 1979a. Genetic and molecular analysis of the 87A7 and 87C1 heat-inducible loci of D. melanogaster. Cell 18: 1351-1358.
28. ISH-HOROWICZ, D., S. M. PINCHIN, J. GAUSZ, H. GYURKOVICS, G. BENCZE, M. GOLDSCHMIDT-CLERMONT, AND J. J. HOLDEN. 1979b. Deletion mapping of two D. melanogaster loci that code for the 70,000 dalton heat-induced protein. Cell 17:565-571.
29. KOBAN, M., A. A. YUP, L. B. AGELLON, AND D. A. POWERS. 1991. Molecular adaptation to environmental temperature: Heat-shock response of the eurythermal teleost Fundulus heteroclitus. Mol. Mar. Biol. Biotech. 1:1-17.
30. KREBS, R. A., AND M. E. FEDER. 1997a. Natural variation in the expression of the heat-shock protein Hsp70 in a population of Drosophila melanogaster, and its correlation with tolerance of ecologically relevant thermal stress. Evolution 51:173-179.
31. _. 1997b. Deleterious consequences of Hsp70 overexpression in Drosophila melanogaster larvae. Cell Stress Chaperones 2: 60-71.
32. _. 1997c. Tissue-specific variation in Hsp70 expression and thermal damage in Drosophila melanogaster larvae. J. Exp. Biol. 200:2007-2015.
33. _. 1998. Experimental manipulation of the cost of thermal acclimation in Drosophila melanogaster. Biol. J. Linn. Soc. 63: 593-601.
34. LEE, J. H., AND F. SCHOFFL. 1996. An Hsp70 antisense gene affects the expression of HSP70/HSC70, the regulation of HSF, and the acquisition of thermotolerance in transgenic Arabidopsis thaliana. Mol. Gen. Gen. 252:11-19.
35. LEIGH BROWN, A. J., AND D. ISH-HOROWICZ. 1981. Evolution of the 87A and 87C heat-shock loci in Drosophila. Nature 290: 677-682.
36. LI, G. C., N. F. MIVECHI, AND G. WEITZEL. 1995. Heat shock proteins, thermotolerance, and their relevance to clinical hyperthermia. Int. J. Hyperthermia 11:459-488.
37. LINDQUIST, S. L. 1984. Heat shock - a comparison of Drosophila and yeast. J. Embryol Exp. Morphol. 83 (Suppl.):147-161.
38. _. 1993. Autoregulation of the heat-shock response. Pp. 279-320 in J. Ilan, Eds. Translational Regulation of Gene Expression 2. Plenum Press, New York.
39. LOESCHCKE, V., AND R. A. KREBS. 1996. Selection for heat-shock resistance in larval and adult Drosophila buzzatii: comparing direct and indirect responses on viability and development. Evolution 50:2354-2359.
40. MCCOLL, G., A. A. HOFFMANN, AND S. W. MCKECHNIE. 1996. Response of two heat shock genes to selection for knockdown heat resistance in Drosophila melanogaster. Genetics 143:1615-1627.
41. MCGARRY, T. J., AND S. LINDQUIST. 1986. Inhibition of heat shock protein synthesis by heat-inducible antisense RNA. Proc. Natl. Acad. Sci. USA 83:399-403.
42. MOSELEY, P. L. 1994. Mechanisms of heat adaptation: thermotolerance and acclimatization. J. Lab. Clin. Med. 123:48-52.
43. O'BRIEN, T., AND J. T. LIS. 1991. RNA polymerase II pauses at the 5′ end of the transcriptionally induced Drosophila hsp70 gene. Mol. Cell. Biol. 11:5285-5290.
44. PETERSEN, R. B., AND S. LINDQUIST. 1989. Regulation of HSP70 synthesis by messenger RNA degradation. Cell Regul. 1:135-149.
45. ROBERTS, D. A., G. E. HOFMANN, AND G. N. SOMERO. 1997. Heat-shock protein expression in Mytilus californianus: Acclimatization (seasonal and tidal-height comparisons) and acclimation effects. Biol. Bull. 192:309-320.
46. ROSE, M. R., T. J. NUSBAUM, AND A. K. CHIPPINDALE. 1996. Laboratory evolution: the experimental wonderland and the Cheshire cat syndrome. Pp. 221-241 in M. R. Rose and G. V. Lauder, eds. Adaptation. Academic Press, San Diego, CA.
47. SOLOMON, J. M., J. M. ROSSI, K. GOLIC, T. MCGARRY, AND S. LINDQUIST. 1991. Changes in Hsp70 alter thermotolerance and heat-shock regulation in Drosophila. New Biol. 3:1106-1120.
48. UDVARDY, A., J. SUMEGI, E. CSORDAS TOTH, J. GAUSZ, H. GYURKOVICS, P. SCHEDL, AND D. ISH-HOROWICZ. 1982. Genomic organization and functional analysis of a deletion variant of the 87A7 heat shock locus of Drosophila melanogaster. J. Mol. Biol. 155:267-280.
49. VELAZQUEZ, J. M., S. SONODA, G. BUGAISKY, AND S. LINDQUIST. 1983. Is the major Drosophila heat shock protein present in cells that have not been heat shocked? J. Cell Biol. 96:286-290.
50. WELTE, M. A., J. M. TETRAULT, R. P. DELLAVALLE, AND S. L. LINDQUIST. 1993. A new method for manipulating transgenes: engineering heat tolerance in a complex multicellular organism. Curr. Biol. 3:842-853.
51. WHEELER, J. C., E. T. BIESCHKE, AND J. TOWER. 1995. Muscle-specific expression of Drosophila Hsp70 in response to aging and oxidative stress. Proc. Natl. Acad. Sci. USA 92:10408-10412.
52. WU, C. 1995. Heat shock transcription factors: structure and regulation. Annu. Rev. Cell Dev. Biol. 11:441-469.