Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1984 Sep;159(3):863–869. doi: 10.1128/jb.159.3.863-869.1984

Transcription of ribosomal component genes and lac in a relA+/relA pair of Escherichia coli strains.

R Little, H Bremer
PMCID: PMC215738  PMID: 6090395

Abstract

To determine the stringent response, a repression of gene activity during amino acid starvation assumed to be mediated by the effector necleotide guanosine tetraphosphate (ppGpp), of metabolically regulated constitutive genes, we measured the transcription of ribosomal protein genes, the constitutive lac operon, and stable RNA genes in a variety of growth media and after amino acid starvation in a relA+/relA pair of Escherichia coli B/r strains. For rRNA and tRNA (stable RNA) it has previously been shown that the distinction between stringent control and growth rate control is unfounded, as the function describing the stable RNA gene activities at different concentrations of guanosine tetraphosphate is independent of growth conditions (exponential growth or amino acid starvation) and of the relA allele present. Here, the results indicated that the stringent responses of ribosomal protein genes and lac differ from their metabolic control during exponential growth in different media. This can be explained by polarity and RNA polymerase sink effects during amino acid starvation which are irrelevant for stable RNA genes but which are superimposed on mRNA gene activities.

Full text

PDF
863

Selected References

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

  1. Blumenthal R. M., Lemaux P. G., Neidhardt F. C., Dennis P. P. The effects of the relA gene on the synthesis of aminoacyl-tRNA synthetases and other transcription and translation proteins in Escherichia coli A. Mol Gen Genet. 1976 Dec 22;149(3):291–296. doi: 10.1007/BF00268530. [DOI] [PubMed] [Google Scholar]
  2. Churchward G., Bremer H., Young R. Macromolecular composition of bacteria. J Theor Biol. 1982 Feb 7;94(3):651–670. doi: 10.1016/0022-5193(82)90305-8. [DOI] [PubMed] [Google Scholar]
  3. Churchward G., Bremer H., Young R. Transcription in bacteria at different DNA concentrations. J Bacteriol. 1982 May;150(2):572–581. doi: 10.1128/jb.150.2.572-581.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Dalbow D. G., Bremer H. Metabolic regulation of beta-galactosidase synthesis in Escherichia coli. A test for constitutive ribosome synthesis. Biochem J. 1975 Jul;150(1):1–8. doi: 10.1042/bj1500001b. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Dennis P. P., Bremer H. Macromolecular composition during steady-state growth of Escherichia coli B-r. J Bacteriol. 1974 Jul;119(1):270–281. doi: 10.1128/jb.119.1.270-281.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dennis P. P. Influence of the stringent control system on the transcription of ribosomal ribonucleic acid and ribosomal protein genes in Escherichia coli. J Bacteriol. 1977 Feb;129(2):580–588. doi: 10.1128/jb.129.2.580-588.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dennis P. P., Nomura M. Regulation of the expression of ribosomal protein genes in Escherichia coli. J Mol Biol. 1975 Sep 5;97(1):61–76. doi: 10.1016/s0022-2836(75)80022-2. [DOI] [PubMed] [Google Scholar]
  8. Dennis P. P., Nomura M. Stringent control of ribosomal protein gene expression in Escherichia coli. Proc Natl Acad Sci U S A. 1974 Oct;71(10):3819–3823. doi: 10.1073/pnas.71.10.3819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dennis P. P., Nomura M. Stringent control of the transcriptional activities of ribosomal protein genes in E. coli. Nature. 1975 Jun 5;255(5508):460–465. doi: 10.1038/255460a0. [DOI] [PubMed] [Google Scholar]
  10. Dennis P. P., Nordan D. H. Characterization of the hybridization between purified 16S and 23S ribosomal ribonucleic acid and ribosomal deoxyribonucleic acid from Escherichia coli. J Bacteriol. 1976 Oct;128(1):28–34. doi: 10.1128/jb.128.1.28-34.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dennis P. P. Transcription patterns of adjacent segments on the chromosome of Escherichia coli containing genes coding for four 50S ribosomal proteins and the beta and beta' subunits of RNA polymerase. J Mol Biol. 1977 Oct 5;115(4):603–625. doi: 10.1016/0022-2836(77)90105-x. [DOI] [PubMed] [Google Scholar]
  12. Gallant J. A. Stringent control in E. coli. Annu Rev Genet. 1979;13:393–415. doi: 10.1146/annurev.ge.13.120179.002141. [DOI] [PubMed] [Google Scholar]
  13. Gausing K. Regulation of ribosome production in Escherichia coli: synthesis and stability of ribosomal RNA and of ribosomal protein messenger RNA at different growth rates. J Mol Biol. 1977 Sep 25;115(3):335–354. doi: 10.1016/0022-2836(77)90158-9. [DOI] [PubMed] [Google Scholar]
  14. Haseltine W. A., Block R. Synthesis of guanosine tetra- and pentaphosphate requires the presence of a codon-specific, uncharged transfer ribonucleic acid in the acceptor site of ribosomes. Proc Natl Acad Sci U S A. 1973 May;70(5):1564–1568. doi: 10.1073/pnas.70.5.1564. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Imamoto F., Kano Y. Inhibition of transcription of the tryptophan operon in Escherichia coli by a block in initiation of translation. Nat New Biol. 1971 Aug 11;232(2):169–173. doi: 10.1038/newbio232169a0. [DOI] [PubMed] [Google Scholar]
  16. Jinks-Robertson S., Gourse R. L., Nomura M. Expression of rRNA and tRNA genes in Escherichia coli: evidence for feedback regulation by products of rRNA operons. Cell. 1983 Jul;33(3):865–876. doi: 10.1016/0092-8674(83)90029-6. [DOI] [PubMed] [Google Scholar]
  17. Lazzarini R. A., Cashel M., Gallant J. On the regulation of guanosine tetraphosphate levels in stringent and relaxed strains of Escherichia coli. J Biol Chem. 1971 Jul 25;246(14):4381–4385. [PubMed] [Google Scholar]
  18. Lindahl L., Post L., Zengel J., Gilbert S. F., Strycharz W. A., Nomura M. Mapping of ribosomal protein genes by in vitro protein synthesis using DNA fragments of lambdafus3 transducing phage DNA as templates. J Biol Chem. 1977 Oct 25;252(20):7365–7383. [PubMed] [Google Scholar]
  19. Lindahl L., Zengel J. M. Expression of ribosomal genes in bacteria. Adv Genet. 1982;21:53–121. doi: 10.1016/s0065-2660(08)60297-7. [DOI] [PubMed] [Google Scholar]
  20. Little R., Dennis P. P. Expression of RNA polymerase and ribosome component genes in Escherichia coli mutants having conditionally defective RNA polymerases. J Bacteriol. 1979 Jan;137(1):115–123. doi: 10.1128/jb.137.1.115-123.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Little R., Ryals J., Bremer H. Physiological characterization of Escherichia coli rpoB mutants with abnormal control of ribosome synthesis. J Bacteriol. 1983 Sep;155(3):1162–1170. doi: 10.1128/jb.155.3.1162-1170.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Little R., Ryals J., Bremer H. rpoB mutation in Escherichia coli alters control of ribosome synthesis by guanosine tetraphosphate. J Bacteriol. 1983 May;154(2):787–792. doi: 10.1128/jb.154.2.787-792.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Maher D. L., Dennis P. P. In vivo transcription of E. coli genes coding for rRNA, ribosomal proteins and subunits of RNA polymerase: influence of the stringent control system. Mol Gen Genet. 1977 Oct 20;155(2):203–211. doi: 10.1007/BF00393161. [DOI] [PubMed] [Google Scholar]
  24. Morse D. E., Guertin M. Regulation of mRNA utilization and degradation by amino-acid starvation. Nat New Biol. 1971 Aug 11;232(2):165–169. doi: 10.1038/newbio232165a0. [DOI] [PubMed] [Google Scholar]
  25. Nomura M., Gourse R., Baughman G. Regulation of the synthesis of ribosomes and ribosomal components. Annu Rev Biochem. 1984;53:75–117. doi: 10.1146/annurev.bi.53.070184.000451. [DOI] [PubMed] [Google Scholar]
  26. Primakoff P., Artz S. W. Positive control of lac operon expression in vitro by guanosine 5'-diphosphate 3'-diphosphate. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1726–1730. doi: 10.1073/pnas.76.4.1726. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Rose J. K., Yanofsky C. Metabolic regulation of the tryptophan operon of Escherichia coli: repressor-independent regulation of transcription initiation frequency. J Mol Biol. 1972 Aug 14;69(1):103–118. doi: 10.1016/0022-2836(72)90026-5. [DOI] [PubMed] [Google Scholar]
  28. Ryals J., Bremer H. relA-dependent RNA polymerase activity in Escherichia coli. J Bacteriol. 1982 Apr;150(1):168–179. doi: 10.1128/jb.150.1.168-179.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Ryals J., Little R., Bremer H. Control of RNA synthesis in Escherichia coli after a shift to higher temperature. J Bacteriol. 1982 Sep;151(3):1425–1432. doi: 10.1128/jb.151.3.1425-1432.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Ryals J., Little R., Bremer H. Control of rRNA and tRNA syntheses in Escherichia coli by guanosine tetraphosphate. J Bacteriol. 1982 Sep;151(3):1261–1268. doi: 10.1128/jb.151.3.1261-1268.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Ryals J., Little R., Bremer H. Temperature dependence of RNA synthesis parameters in Escherichia coli. J Bacteriol. 1982 Aug;151(2):879–887. doi: 10.1128/jb.151.2.879-887.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sarmientos P., Sylvester J. E., Contente S., Cashel M. Differential stringent control of the tandem E. coli ribosomal RNA promoters from the rrnA operon expressed in vivo in multicopy plasmids. Cell. 1983 Apr;32(4):1337–1346. doi: 10.1016/0092-8674(83)90314-8. [DOI] [PubMed] [Google Scholar]
  33. Seeburg P. H., Nüsslein C., Schaller H. Interaction of RNA polymerase with promoters from bacteriophage fd. Eur J Biochem. 1977 Mar 15;74(1):107–113. doi: 10.1111/j.1432-1033.1977.tb11372.x. [DOI] [PubMed] [Google Scholar]
  34. Shepherd N. S., Churchward G., Bremer H. Synthesis and activity of ribonucleic acid polymerase in Escherichia coli. J Bacteriol. 1980 Mar;141(3):1098–1108. doi: 10.1128/jb.141.3.1098-1108.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Travers A. A. Conserved features of coordinately regulated E. coli promoters. Nucleic Acids Res. 1984 Mar 26;12(6):2605–2618. doi: 10.1093/nar/12.6.2605. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Travers A. A., Lamond A. I., Mace H. A. PpGpp regulates the binding of two RNA polymerase molecules to the tyrT promoter. Nucleic Acids Res. 1982 Aug 25;10(16):5043–5057. doi: 10.1093/nar/10.16.5043. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Wanner B. L., Kodaira R., Neidhardt F. C. Physiological regulation of a decontrolled lac operon. J Bacteriol. 1977 Apr;130(1):212–222. doi: 10.1128/jb.130.1.212-222.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. van Ooyen A. J., de Boer H. A., Ab G., Gruber M. Specific inhibition of ribosomal RNA synthesis in vitro by guanosine 3' diphosphate, 5' diphosphate. Nature. 1975 Apr 10;254(5500):530–531. doi: 10.1038/254530a0. [DOI] [PubMed] [Google Scholar]

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

RESOURCES