Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1985 Jun;162(3):1083–1091. doi: 10.1128/jb.162.3.1083-1091.1985

Heat shock response of Neurospora crassa: protein synthesis and induced thermotolerance.

N Plesofsky-Vig, R Brambl
PMCID: PMC215887  PMID: 3158641

Abstract

At elevated temperatures, germinating conidiospores of Neurospora crassa discontinue synthesis of most proteins and initiate synthesis of three dominant heat shock proteins of 98,000, 83,000, and 67,000 Mr and one minor heat shock protein of 30,000 Mr. Postemergent spores produce, in addition to these, a fourth major heat shock protein of 38,000 Mr and a minor heat shock protein of 34,000 Mr. The three heat shock proteins of lower molecular weight are associated with mitochondria. This exclusive synthesis of heat shock proteins is transient, and after 60 min of exposure to high temperatures, restoration of the normal pattern of protein synthesis is initiated. Despite the transiency of the heat shock response, spores incubated continuously at 45 degrees C germinate very slowly and do not grow beyond the formation of a germ tube. The temperature optimum for heat shock protein synthesis is 45 degrees C, but spores incubated at other temperatures from 40 through 47 degrees C synthesize heat shock proteins at lower rates. Survival was high for germinating spores exposed to temperatures up to 47 degrees C, but viability declined markedly at higher temperatures. Germinating spores survived exposure to the lethal temperature of 50 degrees C when they had been preexposed to 45 degrees C; this thermal protection depends on the synthesis of heat shock proteins, since protection was abolished by cycloheximide. During the heat shock response mitochondria also discontinue normal protein synthesis; synthesis of the mitochondria-encoded subunits of cytochrome c oxidase was as depressed as that of the nucleus-encoded subunits.

Full text

PDF
1083

Images in this article

Selected References

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

  1. Arrigo A. P., Fakan S., Tissières A. Localization of the heat shock-induced proteins in Drosophila melanogaster tissue culture cells. Dev Biol. 1980 Jul;78(1):86–103. doi: 10.1016/0012-1606(80)90320-6. [DOI] [PubMed] [Google Scholar]
  2. Ashburner M., Bonner J. J. The induction of gene activity in drosophilia by heat shock. Cell. 1979 Jun;17(2):241–254. doi: 10.1016/0092-8674(79)90150-8. [DOI] [PubMed] [Google Scholar]
  3. Atkinson B. G. Synthesis of heat-shock proteins by cells undergoing myogenesis. J Cell Biol. 1981 Jun;89(3):666–673. doi: 10.1083/jcb.89.3.666. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Ballinger D. G., Pardue M. L. The control of protein synthesis during heat shock in Drosophila cells involves altered polypeptide elongation rates. Cell. 1983 May;33(1):103–113. doi: 10.1016/0092-8674(83)90339-2. [DOI] [PubMed] [Google Scholar]
  5. Bardwell J. C., Craig E. A. Major heat shock gene of Drosophila and the Escherichia coli heat-inducible dnaK gene are homologous. Proc Natl Acad Sci U S A. 1984 Feb;81(3):848–852. doi: 10.1073/pnas.81.3.848. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bienz M., Gurdon J. B. The heat-shock response in Xenopus oocytes is controlled at the translational level. Cell. 1982 Jul;29(3):811–819. doi: 10.1016/0092-8674(82)90443-3. [DOI] [PubMed] [Google Scholar]
  7. Brambl R. Mitochondrial biogenesis during fungal spore germination. Biosynthesis and assembly of cytochrome c oxidase in Botryodiplodia theobromae. J Biol Chem. 1980 Aug 25;255(16):7673–7680. [PubMed] [Google Scholar]
  8. Cosgrove J. W., Brown I. R. Heat shock protein in mammalian brain and other organs after a physiologically relevant increase in body temperature induced by D-lysergic acid diethylamide. Proc Natl Acad Sci U S A. 1983 Jan;80(2):569–573. doi: 10.1073/pnas.80.2.569. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. DiDomenico B. J., Bugaisky G. E., Lindquist S. Heat shock and recovery are mediated by different translational mechanisms. Proc Natl Acad Sci U S A. 1982 Oct;79(20):6181–6185. doi: 10.1073/pnas.79.20.6181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. DiDomenico B. J., Bugaisky G. E., Lindquist S. The heat shock response is self-regulated at both the transcriptional and posttranscriptional levels. Cell. 1982 Dec;31(3 Pt 2):593–603. doi: 10.1016/0092-8674(82)90315-4. [DOI] [PubMed] [Google Scholar]
  11. Farrelly F. W., Finkelstein D. B. Complete sequence of the heat shock-inducible HSP90 gene of Saccharomyces cerevisiae. J Biol Chem. 1984 May 10;259(9):5745–5751. [PubMed] [Google Scholar]
  12. Guttman S. D., Glover C. V., Allis C. D., Gorovsky M. A. Heat shock, deciliation and release from anoxia induce the synthesis of the same set of polypeptides in starved T. pyriformis. Cell. 1980 Nov;22(1 Pt 1):299–307. doi: 10.1016/0092-8674(80)90177-4. [DOI] [PubMed] [Google Scholar]
  13. Ingolia T. D., Slater M. R., Craig E. A. Saccharomyces cerevisiae contains a complex multigene family related to the major heat shock-inducible gene of Drosophila. Mol Cell Biol. 1982 Nov;2(11):1388–1398. doi: 10.1128/mcb.2.11.1388. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kapoor M. A study of the heat-shock response in Neurospora crassa. Int J Biochem. 1983;15(5):639–649. doi: 10.1016/0020-711x(83)90188-x. [DOI] [PubMed] [Google Scholar]
  15. Kelley P. M., Schlesinger M. J. Antibodies to two major chicken heat shock proteins cross-react with similar proteins in widely divergent species. Mol Cell Biol. 1982 Mar;2(3):267–274. doi: 10.1128/mcb.2.3.267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kloetzel P. M., Bautz E. K. Heat-shock proteins are associated with hnRNA in Drosophila melanogaster tissue culture cells. EMBO J. 1983;2(5):705–710. doi: 10.1002/j.1460-2075.1983.tb01488.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lai B. T., Chin N. W., Stanek A. E., Keh W., Lanks K. W. Quantitation and intracellular localization of the 85K heat shock protein by using monoclonal and polyclonal antibodies. Mol Cell Biol. 1984 Dec;4(12):2802–2810. doi: 10.1128/mcb.4.12.2802. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lambowitz A. M. Preparation and analysis of mitochondrial ribosomes. Methods Enzymol. 1979;59:421–433. doi: 10.1016/0076-6879(79)59103-4. [DOI] [PubMed] [Google Scholar]
  19. Lambowitz A. M., Slayman C. W. Cyanide-resistant respiration in Neurospora crassa. J Bacteriol. 1971 Dec;108(3):1087–1096. doi: 10.1128/jb.108.3.1087-1096.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Li G. C., Werb Z. Correlation between synthesis of heat shock proteins and development of thermotolerance in Chinese hamster fibroblasts. Proc Natl Acad Sci U S A. 1982 May;79(10):3218–3222. doi: 10.1073/pnas.79.10.3218. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lin C. Y., Roberts J. K., Key J. L. Acquisition of Thermotolerance in Soybean Seedlings : Synthesis and Accumulation of Heat Shock Proteins and their Cellular Localization. Plant Physiol. 1984 Jan;74(1):152–160. doi: 10.1104/pp.74.1.152. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lindquist S. Regulation of protein synthesis during heat shock. Nature. 1981 Sep 24;293(5830):311–314. doi: 10.1038/293311a0. [DOI] [PubMed] [Google Scholar]
  23. Lindquist S. Varying patterns of protein synthesis in Drosophila during heat shock: implications for regulation. Dev Biol. 1980 Jun 15;77(2):463–479. doi: 10.1016/0012-1606(80)90488-1. [DOI] [PubMed] [Google Scholar]
  24. Loomis W. F., Wheeler S. A. Chromatin-associated heat shock proteins of Dictyostelium. Dev Biol. 1982 Apr;90(2):412–418. doi: 10.1016/0012-1606(82)90390-6. [DOI] [PubMed] [Google Scholar]
  25. McAlister L., Finkelstein D. B. Alterations in translatable ribonucleic acid after heat shock of Saccharomyces cerevisiae. J Bacteriol. 1980 Aug;143(2):603–612. doi: 10.1128/jb.143.2.603-612.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. McAlister L., Finkelstein D. B. Heat shock proteins and thermal resistance in yeast. Biochem Biophys Res Commun. 1980 Apr 14;93(3):819–824. doi: 10.1016/0006-291x(80)91150-x. [DOI] [PubMed] [Google Scholar]
  27. Michéa-Hamzehpour M., Grange F., Ton That T. C., Turian G. Heat-induced changes in respiratory pathways and mitochondrial structure during microcycle conidiation of Neurospora crassa. Arch Microbiol. 1980 Mar;125(1-2):53–58. doi: 10.1007/BF00403197. [DOI] [PubMed] [Google Scholar]
  28. Miller M. J., Xuong N. H., Geiduschek E. P. A response of protein synthesis to temperature shift in the yeast Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1979 Oct;76(10):5222–5225. doi: 10.1073/pnas.76.10.5222. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Pelham H. R. Hsp70 accelerates the recovery of nucleolar morphology after heat shock. EMBO J. 1984 Dec 20;3(13):3095–3100. doi: 10.1002/j.1460-2075.1984.tb02264.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Petersen N. S., Mitchell H. K. Recovery of protein synthesis after heat shock: prior heat treatment affects the ability of cells to translate mRNA. Proc Natl Acad Sci U S A. 1981 Mar;78(3):1708–1711. doi: 10.1073/pnas.78.3.1708. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Spradling A., Pardue M. L., Penman S. Messenger RNA in heat-shocked Drosophila cells. J Mol Biol. 1977 Feb 5;109(4):559–587. doi: 10.1016/s0022-2836(77)80091-0. [DOI] [PubMed] [Google Scholar]
  32. Stade S., Brambl R. Mitochondrial biogenesis during fungal spore germination: respiration and cytochrome c oxidase in Neurospora crassa. J Bacteriol. 1981 Sep;147(3):757–767. doi: 10.1128/jb.147.3.757-767.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Storti R. V., Scott M. P., Rich A., Pardue M. L. Translational control of protein synthesis in response to heat shock in D. melanogaster cells. Cell. 1980 Dec;22(3):825–834. doi: 10.1016/0092-8674(80)90559-0. [DOI] [PubMed] [Google Scholar]
  34. Tilly K., McKittrick N., Zylicz M., Georgopoulos C. The dnaK protein modulates the heat-shock response of Escherichia coli. Cell. 1983 Sep;34(2):641–646. doi: 10.1016/0092-8674(83)90396-3. [DOI] [PubMed] [Google Scholar]
  35. Velazquez J. M., DiDomenico B. J., Lindquist S. Intracellular localization of heat shock proteins in Drosophila. Cell. 1980 Jul;20(3):679–689. doi: 10.1016/0092-8674(80)90314-1. [DOI] [PubMed] [Google Scholar]
  36. Velazquez J. M., Lindquist S. hsp70: nuclear concentration during environmental stress and cytoplasmic storage during recovery. Cell. 1984 Mar;36(3):655–662. doi: 10.1016/0092-8674(84)90345-3. [DOI] [PubMed] [Google Scholar]
  37. Welch W. J., Feramisco J. R. Nuclear and nucleolar localization of the 72,000-dalton heat shock protein in heat-shocked mammalian cells. J Biol Chem. 1984 Apr 10;259(7):4501–4513. [PubMed] [Google Scholar]
  38. Yamamori T., Ito K., Nakamura Y., Yura T. Transient regulation of protein synthesis in Escherichia coli upon shift-up of growth temperature. J Bacteriol. 1978 Jun;134(3):1133–1140. doi: 10.1128/jb.134.3.1133-1140.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Yamamori T., Yura T. Genetic control of heat-shock protein synthesis and its bearing on growth and thermal resistance in Escherichia coli K-12. Proc Natl Acad Sci U S A. 1982 Feb;79(3):860–864. doi: 10.1073/pnas.79.3.860. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES