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. 1996 Aug;143(4):1615–1627. doi: 10.1093/genetics/143.4.1615

Response of Two Heat Shock Genes to Selection for Knockdown Heat Resistance in Drosophila Melanogaster

G McColl 1, A A Hoffmann 1, S W McKechnie 1
PMCID: PMC1207425  PMID: 8844150

Abstract

To identify genes involved in stress resistance and heat hardening, replicate lines of Drosophila melanogaster were selected for increased resistance to knockdown by a 39° heat stress. Two selective regimes were used, one with and one without prior hardening. Mean knockdown times were increased from ~5 min to >20 min after 18 generations. Initial realized heritabilities were as high as 10% for lines selected without hardening, and crosses between lines indicated simple additive gene effects for the selected phenotypes. To survey allelic variation and correlated selection responses in two candidate stress genes, hsr-omega and hsp68, we applied denaturing gradient gel electrophoresis to amplified DNA sequences from small regions of these genes. After eight generations of selection, allele frequencies at both loci showed correlated responses for selection following hardening, but not without hardening. The hardening process itself was associated with a hsp68 frequency change in the opposite direction to that associated with selection that followed hardening. These stress loci are closely linked on chromosome III, and the hardening selection established a disequilibrium, suggesting an epistatic effect on resistance. The data indicate that molecular variation in both hsr-omega and hsp68 contribute to natural heritable variation for hardened heat resistance.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bendena W. G., Ayme-Southgate A., Garbe J. C., Pardue M. L. Expression of heat-shock locus hsr-omega in nonstressed cells during development in Drosophila melanogaster. Dev Biol. 1991 Mar;144(1):65–77. doi: 10.1016/0012-1606(91)90479-m. [DOI] [PubMed] [Google Scholar]
  2. Bendena W. G., Garbe J. C., Traverse K. L., Lakhotia S. C., Pardue M. L. Multiple inducers of the Drosophila heat shock locus 93D (hsr omega): inducer-specific patterns of the three transcripts. J Cell Biol. 1989 Jun;108(6):2017–2028. doi: 10.1083/jcb.108.6.2017. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bosch T. C., Krylow S. M., Bode H. R., Steele R. E. Thermotolerance and synthesis of heat shock proteins: these responses are present in Hydra attenuata but absent in Hydra oligactis. Proc Natl Acad Sci U S A. 1988 Nov;85(21):7927–7931. doi: 10.1073/pnas.85.21.7927. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Clos J., Westwood J. T., Becker P. B., Wilson S., Lambert K., Wu C. Molecular cloning and expression of a hexameric Drosophila heat shock factor subject to negative regulation. Cell. 1990 Nov 30;63(5):1085–1097. doi: 10.1016/0092-8674(90)90511-c. [DOI] [PubMed] [Google Scholar]
  5. Cohan F. M., Hoffmann A. A. Genetic divergence under uniform selection. II. Different responses to selection for knockdown resistance to ethanol among Drosophila melanogaster populations and their replicate lines. Genetics. 1986 Sep;114(1):145–164. doi: 10.1093/genetics/114.1.145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Don R. H., Cox P. T., Wainwright B. J., Baker K., Mattick J. S. 'Touchdown' PCR to circumvent spurious priming during gene amplification. Nucleic Acids Res. 1991 Jul 25;19(14):4008–4008. doi: 10.1093/nar/19.14.4008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Feder J. H., Rossi J. M., Solomon J., Solomon N., Lindquist S. The consequences of expressing hsp70 in Drosophila cells at normal temperatures. Genes Dev. 1992 Aug;6(8):1402–1413. doi: 10.1101/gad.6.8.1402. [DOI] [PubMed] [Google Scholar]
  8. Fini M. E., Bendena W. G., Pardue M. L. Unusual behavior of the cytoplasmic transcript of hsr omega: an abundant, stress-inducible RNA that is translated but yields no detectable protein product. J Cell Biol. 1989 Jun;108(6):2045–2057. doi: 10.1083/jcb.108.6.2045. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Garbe J. C., Bendena W. G., Alfano M., Pardue M. L. A Drosophila heat shock locus with a rapidly diverging sequence but a conserved structure. J Biol Chem. 1986 Dec 25;261(36):16889–16894. [PubMed] [Google Scholar]
  10. Hoffmann A. A., Parsons P. A. Selection for increased desiccation resistance in Drosophila melanogaster: additive genetic control and correlated responses for other stresses. Genetics. 1989 Aug;122(4):837–845. doi: 10.1093/genetics/122.4.837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hogan N. C., Slot F., Traverse K. L., Garbe J. C., Bendena W. G., Pardue M. L. Stability of tandem repeats in the Drosophila melanogaster Hsr-omega nuclear RNA. Genetics. 1995 Apr;139(4):1611–1621. doi: 10.1093/genetics/139.4.1611. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Holmgren R., Corces V., Morimoto R., Blackman R., Meselson M. Sequence homologies in the 5' regions of four Drosophila heat-shock genes. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3775–3778. doi: 10.1073/pnas.78.6.3775. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Holmgren R., Livak K., Morimoto R., Freund R., Meselson M. Studies of cloned sequences from four Drosophila heat shock loci. Cell. 1979 Dec;18(4):1359–1370. doi: 10.1016/0092-8674(79)90246-0. [DOI] [PubMed] [Google Scholar]
  14. Jenkins N. L., Hoffmann A. A. Genetic and maternal variation for heat resistance in Drosophila from the field. Genetics. 1994 Jul;137(3):783–789. doi: 10.1093/genetics/137.3.783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Knibb W. R., Oakeshott J. G., Gibson J. B. Chromosome Inversion Polymorphisms in DROSOPHILA MELANOGASTER. I. Latitudinal Clines and Associations between Inversions in Australasian Populations. Genetics. 1981 Aug;98(4):833–847. doi: 10.1093/genetics/98.4.833. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lakhotia S. C. The 93D heat shock locus of Drosophila melanogaster: modulation by genetic and developmental factors. Genome. 1989;31(2):677–683. doi: 10.1139/g89-124. [DOI] [PubMed] [Google Scholar]
  17. Myers R. M., Maniatis T., Lerman L. S. Detection and localization of single base changes by denaturing gradient gel electrophoresis. Methods Enzymol. 1987;155:501–527. doi: 10.1016/0076-6879(87)55033-9. [DOI] [PubMed] [Google Scholar]
  18. Nagao R. T., Kimpel J. A., Key J. L. Molecular and cellular biology of the heat-shock response. Adv Genet. 1990;28:235–274. doi: 10.1016/s0065-2660(08)60528-3. [DOI] [PubMed] [Google Scholar]
  19. Palter K. B., Watanabe M., Stinson L., Mahowald A. P., Craig E. A. Expression and localization of Drosophila melanogaster hsp70 cognate proteins. Mol Cell Biol. 1986 Apr;6(4):1187–1203. doi: 10.1128/mcb.6.4.1187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Parsons P. A. Genetics of resistance to environmental stresses in Drosophila populations. Annu Rev Genet. 1973;7:239–265. doi: 10.1146/annurev.ge.07.120173.001323. [DOI] [PubMed] [Google Scholar]
  21. Ulmasov K. A., Shammakov S., Karaev K., Evgen'ev M. B. Heat shock proteins and thermoresistance in lizards. Proc Natl Acad Sci U S A. 1992 Mar 1;89(5):1666–1670. doi: 10.1073/pnas.89.5.1666. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Walsh P. S., Metzger D. A., Higuchi R. Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques. 1991 Apr;10(4):506–513. [PubMed] [Google Scholar]
  23. White C. N., Hightower L. E., Schultz R. J. Variation in heat-shock proteins among species of desert fishes (Poeciliidae, Poeciliopsis). Mol Biol Evol. 1994 Jan;11(1):106–119. doi: 10.1093/oxfordjournals.molbev.a040085. [DOI] [PubMed] [Google Scholar]

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