Modification of heat-shock gene expression in Drosophila melanogaster populations via transposable elements

Molecular Biology and Evolution

Volumn 20, Issue 1, 2003, Pages 135-144

  Lerman, Daniel N ^b   Michalak, Pawel ^a   Helin, Amanda B ^b   Bettencourt, Brian R ^b   Feder, Martin E ^b  

^a UNIVERSITY OF HAIFA   (Israel)

^b NONE

Author keywords

Drosophila melanogaster; Hsp70; heat shock proteins; Regulatory evolution; Transposable elements

Indexed keywords

CHAPERONE; HEAT SHOCK PROTEIN 70;

ARTICLE; BIOACCUMULATION; DROSOPHILA MELANOGASTER; GENE DISRUPTION; GENE EXPRESSION REGULATION; GENE INSERTION; GENE SEQUENCE; GENETIC VARIABILITY; HEAT TOLERANCE; NATURAL SELECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; POPULATION; PROMOTER REGION; PROTEIN EXPRESSION; REPRODUCTION; RIBONUCLEASE PROTECTION ASSAY; TRANSCRIPTION REGULATION; TRANSPOSON;

ANALYSIS OF VARIANCE; ANIMALS; DNA TRANSPOSABLE ELEMENTS; DROSOPHILA MELANOGASTER; FEMALE; GENE EXPRESSION REGULATION; HSP70 HEAT-SHOCK PROTEINS; PHENOTYPE; PROMOTER REGIONS (GENETICS); REPRODUCTION; TEMPERATURE;

ARACHNIDA; DROSOPHILA MELANOGASTER; HEXAPODA; ILEX COOKII; MELANOGASTER;

EID: 0037226830     PISSN: 07374038     EISSN: None     Source Type: Journal    
DOI: 10.1093/molbev/msg015     Document Type: Article

References (57)

1. Amin, J., M. Fernandez, J. Ananthan, J. T. Lis, and R. Voellmy. 1994. Cooperative binding of heat shock transcription factor to the hsp70 promoter in vivo and in vitro. J. Biol. Chem. 269:4804-4811.
2. Bettencourt, B. R., and M. E. Feder. 2001. hsp70 duplication in the Drosophila melanogaster species group: how and when did two become five? Mol. Biol. Evol. 18:1272-1282.
3. -. 2002. Rapid concerted evolution via gene conversion at the Drosophila hsp70 genes. J. Mol. Evol. 54:569-586.
4. Bettencourt, B. R., M. E. Feder, and S. Cavicchi. 1999. Experimental evolution of Hsp70 expression and thermotolerance in Drosophila melanogaster. Evolution 53:484-492.
5. Bettencourt, B. R., I. Kim, A. A. Hoffmann, and M. E. Feder. 2002. Response to natural and laboratory selection at the Drosophila hsp70 genes. Evolution 56:1796-1801.
6. Brosius, J. 1999a. RNAs from all categories generate retrosequences that may be exapted as novel genes or regulatory elements. Gene 238:115-134.
7. -. 1999b. Genomes were forged by massive bombardments with retroelements and retrosequences. Genetica 107:209-238.
8. Capy, P., G. Gasperi, C. Biemont, and C. Bazin. 2000. Stress and transposable elements: co-evolution or useful parasites? Heredity 85:101-106.
9. Charlesworth, B., and C. H. Langley. 1989. The population genetics of Drosophila transposable elements. Annu. Rev. Genet. 23:251-287.
10. Charlesworth, B., P. Sniegowski, and W. Stephan. 1994. The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371:215-220.
11. Costlow, N., and J. T. Lis. 1984. High-resolution mapping of DNase I-hypersensitive sites of Drosophila heat shock genes in Drosophila melanogaster and Saccharomyces cerevisiae. Mol. Cell. Biol. 4:1853-1863.
12. Craig, N. L. 1997. Target site selection in transposition. Annu. Rev. Biochem. 66:437-474.
13. Dahlgaard, J., V. Loeschcke, P. Michalak, and J. Justesen. 1998. Induced thermotolerance and associated expression of the heat-shock protein HSP70 in adult Drosophila melanogaster. Funct. Ecol. 12:786-793.
14. Dickinson, W. J., 1991. The evolution of regulatory genes and patterns in Drosophila. Evol. Biol. 25:127-173.
15. Dunn, R. C., and C. C. Laurie. 1995. Effects of a transposable element insertion on alcohol dehydrogenase expression in Drosophila melanogaster. Genetics 140:667-677.
16. Feder, M. E., T. B. C. Bedford, D. R. Albright, and P. Michalak. 2002. Evolvability of Hsp70 expression under artificial selection for inducible thermotolerance in independent populations of Drosophila melanogaster. Physiol. Biochem. Zool. 75:325-334.
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., and R. A. Krebs. 1998. Natural and genetic engineering of thermotolerance in Drosophila melanogaster. Am. Zool. 38:503-517.
19. Gabai, V. L., A. B. Meriin, D. D. Mosser, A. W. Caron, S. Rits, V. I. Shifrin, and M. Y. Sherman. 1997. Hsp70 prevents activation of stress kinases. A novel pathway of cellular thermotolerance. J. Biol. Chem. 272:18033-18037.
20. Gabai, V. L., and M. Y. Sherman. 2002. Interplay between molecular chaperones and signaling pathways in survival of heat shock. J. Appl. Physiol. 92:1743-1748.
21. 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.
22. Gray, Y. H. M. 2000. It takes two transposons to tango - transposable-element-mediated chromosomal rearrangements. Trends Genet. 16:461-468.
23. Kidwell, M. G., and D. R. Lisch. 2001. Perspective: transposable elements, parasitic DNA, and genome evolution. Evolution 55:1-24.
24. Krebs, R. A., and M. E. Feder. 1997. Deleterious consequences of Hsp70 overexpression in Drosophila melanogaster larvae. Cell Stress Chaperones 2:60-71.
25. -. 1998. Hsp70 and larval thermotolerance in Drosophila melanogaster: how much is enough and when is more too much? J. Insect Physiol. 44:1091-1101.
26. Krebs, R. A., M. E. Feder, and J. Lee. 1998. Heritability of expression of the 70-kD heat-shock protein in Drosophila melanogaster and its relevance to the evolution of thermotolerance. Evolution 52:841-847.
27. Lakhotia, S. C., and K. V. Prasanth. 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.
28. Lander, E. S., L. M. Linton, and B. Birren. 2001. Initial sequencing and analysis of the human genome. Nature 409:860-921.
29. Lansing, I., J. Justesen, and V. Loeschcke. 2000. Variation in the expression of HSP70, the major heat-shock protein, and thermotolerance in larval and adult selection lines of Drosophila melanogaster. J. Therm. Biol. 25:443-450.
30. Lee, H., K. W. Kraus, M. F. Wolfner, and J. T. Lis. 1992. DNA sequence requirements for generating paused polymerase at the start of hsp70. Genes. Dev. 6:284-295.
31. Lindquist, S. 1993. Autoregulation of the heat-shock response. Pp. 279-320 in J. Ilan, ed. Translational regulation of gene expression 2. Plenum Press, New York.
32. Maside, X., C. Bartolome, and B. Charlesworth. 2002. S-element insertions are associated with the evolution of the hsp70 genes in Drosophila melanogaster. Curr. Biol. 12:1686-1691.
33. Mason, P. I., I. Torok, I. Kiss, F. Karch, and A. Udvardy. 1982. Evolutionary implications of a complex pattern of DNA sequence homology extending far upstream of the hsp70 genes at loci 87A7 and 87C1 in Drosophila melanogaster. J. Mol. Biol. 156:21-35.
34. McCollum, A., E. Ganko, P. Barrass, J. Rodriguez, and J. McDonald. 2002. Evidence for the adaptive significance of an LTR retrotransposon sequence in a Drosophila heterochromatic gene. BMC Evol. Biol. 2:5.
35. McDonald, J. F. 1995. Transposable elements - possible catalysts of organismic evolution. Trends Ecol. Evol. 10:123-126.
36. Michalak, P., I. Minkov, A. Helin, D. N. Lerman, B. R. Bettencourt, M. E. Feder, A. B. Korol, and E. Nevo. 2001. Genetic evidence for adaptation-driven incipient speciation of Drosophila melanogaster along a microclimatic contrast in "Evolution Canyon," Israel. Proc. Natl. Acad. Sci. U.S.A. 98:13195-13200.
37. Moran, L., M. E. Mirault, A. Tissieres, J. Lis, P. Schedl, S. Artavanis-Tsakonas, and W. J. Gehring. 1979. Physical map of two D. melanogaster DNA segments containing sequences coding for the 70,000 dalton heat shock protein. Cell 17:1-8.
38. Mosser, D. D., A. W. Caron, L. Bourget, A. B. Merlin, M. Y. Sherman, R. I. Morimoto, and B. Massie. 2000. The chaperone function of Hsp70 is required for protection against stress-induced apoptosis. Mol. Cell Biol. 20:7146-7159.
39. Rizzon, C., G. Marais, M. Gouy, and C. Biemont. 2002. Recombination rate and the distribution of transposable elements in the Drosophila melanogaster genome. Genome Res. 12:400-407.
40. Roberts, S. P., and M. E. Feder. 2000. Changing fitness consequences of hsp70 copy number in transgenic Drosophila larvae undergoing natural thermal stress. Funct. Ecol. 14:353-357.
41. Shapiro, J. A. 1992. Natural genetic engineering in evolution. Genetica 86:99-111.
42. Shopland, L. S., K. Hirayoshi, M. Fernandes, and J. T. Lis. 1995. HSF access to heat-shock elements in vivo depends critically on promoter architecture defined by GAGA factor, TFIID and RNA polymerase II binding sites. Genes Dev. 9:2756-2769.
43. Silbermann, R., and M. Tatar. 2000. Reproductive costs of heat shock protein in transgenic Drosophila melanogaster. Evolution 54:2038-2045.
44. Sorensen, J. G., P. Michalak, J. Justesen, and V. Loeschcke. 1999. Expression of the heat-shock protein HSP70 in Drosophila buzzatii lines selected for thermal resistance. Hereditas 131:155-164.
45. Spradling, A. C., D. M. Stem, I. Kiss, J. Roote, T. Laverty, and G. M. Rubin. 1995. Gene disruptions using P transposable elements - an integral component of the Drosophila Genome Project. Proc. Natl. Acad. Sci. USA. 92:10824-10830.
46. Tang, D., Y. Xie, M. J. Zhao, M. A. Stevenson, and S. K. Calderwood. 2001. Repression of the HSP70B promoter by NFIL6, Ku70, and MAPK involves three complementary mechanisms. Biochem. Biophys. Res. Commun. 280:280-285.
47. Timakov, B., X. Liu, I. Turgut, and P. Zhang. 2002. Timing and targeting of P element local transposition in the male germline cells of Drosophila melanogaster. Genetics 160:1011-1022.
48. Velazquez, J. M., B. J. DiDomenico, and S. Lindquist. 1980. Intracellular localization of heat shock proteins in Drosophila. Cell 20:679-689.
49. Voelker, R. A., J. Graves, W. Gibson, and M. Eisenberg. 1990. Mobile element insertions causing mutations in the Drosophila suppressor of sable locus occur in DNase I hypersensitive subregions of 5′-transcribed nontranslated sequences. Genetics 126:1071-1082.
50. Weber, J. A., D. J. Taxman, Q. Lu, and D. S. Gilmour. 1997. Molecular architecture of the hsp70 promoter after deletion of the TATA box or the upstream regulation region. Mol. Cell Biol. 17:3799-3808.
51. Wendel, J. F., and S. R. Wessler. 2000. Retrotransposon-mediated genome evolution on a local ecological scale. Proc. Natl. Acad. Sci. USA. 97:6250-6252.
52. White, L. D., and J. W. Jacobson. 1996. Insertion of the retroposable element, jockey, near the Adh gene of Drosophila melanogaster is associated with altered gene expression. Genet. Res. 68:203-209.
53. Wilkins, R. C., and J. T. Lis. 1997. Dynamics of potentiation and activation: GAGA factor and its role in heat shock gene regulation. Nucleic Acids Res. 25:3963-3968.
54. Wilson, A. C., S. S. Carlson, and T. J. White. 1977. Biochemical evolution. Ann. Rev. Biochem. 46:573-639.
55. Wu, Y. H., A. V. Wilks, and J. B. Gibson. 1998. A KP element inserted between the two promoters of the alcohol dehydrogenase gene of Drosophila melanogaster differentially affects expression in larvae and adults. Biochem. Genet. 36:363-379.
56. Xiao, H., and J. T. Lis. 1988. Germline transformation used to define key features of heat-shock response elements. Science 239:1139-1142.
57. Zatsepina, O. G., V. V. Velikodvorskaia, V. B. Molodtsov, D. Garbuz, D. N. Lerman, B. R. Bettencourt, M. E. Feder, and M. B. Evgenev. 2001. A Drosophila melanogaster strain from sub-equatorial Africa has exceptional thermotolerance but decreased Hsp70 expression. J. Exp. Biol. 204:1869-1881.