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. 1979 Jan;137(1):584–594. doi: 10.1128/jb.137.1.584-594.1979

Organization of genes for transcription and translation in the rif region of the Escherichia coli chromosome.

M Yamamoto, M Nomura
PMCID: PMC218486  PMID: 368032

Abstract

The lambdarifd18 transducing phage is known to carry several genes for components of transcriptional and translational machineries; these genes are clustered in the rif region at 88 min on the Escherichia coli genetic map. They include a set of genes for rRNA's (rrnB), a gene for spacer tRNA, tRNA2Glu (tgtB), one of the two genes for EF-Tu (tufB), genes for four ribosomal proteins (rplK, A, J, and L), genes for the beta and beta' subunits of RNA polymerase (rpoB and rpoC), and genes for three tRNA's (tyrU, gluT, and thrT). An additional tRNA gene (subsequently identified as thrU by Landy and his co-workers) and a gene for a protein (protein U) with unknown functions were found to be carried by lambdarif d18. We analyzed the organization of these genes by using various deletion and hybrid phages derived from lambdarif d18 and lambdarif d12, a phage related to lambdarif d18. The expression of various genes was examined in UV-irradiated cells infected with these transducing phages. Two main conclusions were obtained. First, the four tRNA genes are not cotranscribed with the genes in rrnB, even though these tRNA genes are located close to the distal end of rrnB. Second, the four ribosomal protein genes are organized into two separate transcriptional units; rplK and A are in one unit and rplJ and L are in the second unit. The first group of genes was shown to have a promoter separate from that for tufB or protein U. The second group of genes shares the promoter with rpoB and C, as described in a separate paper (M. Yamamoto and M. Nomura, Proc. Natl. Acad. Sci. U.S.A., 75:3891--3895). These and other results described in this paper show that the genes are organized in the following order: promoter, genes in rrnB; promoter, thrU, tyrU, (promoter?) glyT, thrT; (promoter?) tufB; promoter, a gene for protein U; promoter, rplK, rplA; promoter, rplJ, rplL, rpoB, rpoC.

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Selected References

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

  1. Apirion D., Lassar A. B. A conditional lethal mutant of Escherichia coli which affects the processing of ribosomal RNA. J Biol Chem. 1978 Mar 10;253(5):1738–1742. [PubMed] [Google Scholar]
  2. Blattner F. R., Williams B. G., Blechl A. E., Denniston-Thompson K., Faber H. E., Furlong L., Grunwald D. J., Kiefer D. O., Moore D. D., Schumm J. W. Charon phages: safer derivatives of bacteriophage lambda for DNA cloning. Science. 1977 Apr 8;196(4286):161–169. doi: 10.1126/science.847462. [DOI] [PubMed] [Google Scholar]
  3. Brody S., Yanofsky C. Mechanism studies of suppressor-gene action. J Bacteriol. 1965 Sep;90(3):687–695. doi: 10.1128/jb.90.3.687-695.1965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Carbon J., Berg P., Yanofsky C. Studies of missense suppression of the tryptophan synthetase A-protein mutant A36. Proc Natl Acad Sci U S A. 1966 Aug;56(2):764–771. doi: 10.1073/pnas.56.2.764. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chang S., Carbon J. The nucleotide sequence of a precursor to the glycine- and threonine-specific transfer ribonucleic acids of Escherichia coli. J Biol Chem. 1975 Jul 25;250(14):5542–5555. [PubMed] [Google Scholar]
  6. Clarke L., Carbon J. The nucleotide sequence of a threonine transfer ribonucleic acid from Escherichia coli. J Biol Chem. 1974 Nov 10;249(21):6874–6885. [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. Goodman H. M., Abelson J. N., Landy A., Zadrazil S., Smith J. D. The nucleotide sequences of tyrosine transfer RNAs of Escherichia coli. Eur J Biochem. 1970 Apr;13(3):461–483. doi: 10.1111/j.1432-1033.1970.tb00950.x. [DOI] [PubMed] [Google Scholar]
  9. Ikemura T., Nomura M. Expression of spacer tRNA genes in ribosomal RNA transcription units carried by hybrid Col E1 plasmids in E. coli. Cell. 1977 Aug;11(4):779–793. doi: 10.1016/0092-8674(77)90291-4. [DOI] [PubMed] [Google Scholar]
  10. Ilgen C., Kirk L. L., Carbon J. Isolation and characterization of large transfer ribonucleic acid precursors from Escherichia coli. J Biol Chem. 1976 Feb 25;251(4):922–929. [PubMed] [Google Scholar]
  11. Jaskunas S. R., Fallon A. M., Nomura M. Identification and organization of ribosomal protein genes of Escherichia coli carried by lambdafus2 transducing phage. J Biol Chem. 1977 Oct 25;252(20):7323–7336. [PubMed] [Google Scholar]
  12. Jaskunas S. R., Lindahl L., Nomura M. Identification of two copies of the gene for the elongation factor EF-Tu in E. coli. Nature. 1975 Oct 9;257(5526):458–462. doi: 10.1038/257458a0. [DOI] [PubMed] [Google Scholar]
  13. Kenerley M. E., Morgan E. A., Post L., Lindahl L., Nomura M. Characterization of hybrid plasmids carrying individual ribosomal ribonucleic acid transcription units of Escherichia coli. J Bacteriol. 1977 Dec;132(3):931–949. doi: 10.1128/jb.132.3.931-949.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kirschbaum J. B., Konrad E. B. Isolation of a specialized lambda transducing bacteriophage carrying the beta subunit gene for Escherichia coli ribonucleic acid polymerase. J Bacteriol. 1973 Nov;116(2):517–526. doi: 10.1128/jb.116.2.517-526.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  16. Lindahl L., Jaskunas S. R., Dennis P. P., Nomura M. Cluster of genes in Escherichia coli for ribosomal proteins, ribosomal RNA, and RNA polymerase subunits. Proc Natl Acad Sci U S A. 1975 Jul;72(7):2743–2747. doi: 10.1073/pnas.72.7.2743. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Lindahl S., Yamamoto M., Nomura M. Mapping of a cluster of genes for components of the transcriptional and translational machineries of Escherichia coli. J Mol Biol. 1977 Jan 5;109(1):23–47. doi: 10.1016/s0022-2836(77)80044-2. [DOI] [PubMed] [Google Scholar]
  19. Lund E., Dahlberg J. E., Lindahl L., Jaskunas S. R., Dennis P. P., Nomura M. Transfer RNA genes between 16S and 23S rRNA genes in rRNA transcription units of E. coli. Cell. 1976 Feb;7(2):165–177. doi: 10.1016/0092-8674(76)90016-7. [DOI] [PubMed] [Google Scholar]
  20. Morgan E. A., Ikemura T., Lindahl L., Fallon A. M., Nomura M. Some rRNA operons in E. coli have tRNA genes at their distal ends. Cell. 1978 Feb;13(2):335–344. doi: 10.1016/0092-8674(78)90202-7. [DOI] [PubMed] [Google Scholar]
  21. Morgan E. A., Ikemura T., Nomura M. Identification of spacer tRNA genes in individual ribosomal RNA transcription units of Escherichia coli. Proc Natl Acad Sci U S A. 1977 Jul;74(7):2710–2714. doi: 10.1073/pnas.74.7.2710. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Neidhardt F. C., Bloch P. L., Smith D. F. Culture medium for enterobacteria. J Bacteriol. 1974 Sep;119(3):736–747. doi: 10.1128/jb.119.3.736-747.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Nomura M., Morgan E. A. Genetics of bacterial ribosomes. Annu Rev Genet. 1977;11:297–347. doi: 10.1146/annurev.ge.11.120177.001501. [DOI] [PubMed] [Google Scholar]
  24. Nomura M. Organization of bacterial genes for ribosomal components: studies using novel approaches. Cell. 1976 Dec;9(4 Pt 2):633–644. doi: 10.1016/0092-8674(76)90127-6. [DOI] [PubMed] [Google Scholar]
  25. Orias E., Gartner T. K., Lannan J. E., Betlach M. Close linkage between ochre and missense suppressors in Escherichia coli. J Bacteriol. 1972 Mar;109(3):1125–1133. doi: 10.1128/jb.109.3.1125-1133.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Roberts J. W., Carbon J. Nucleotide sequence studies of normal and genetically altered glycine transfer ribonucleic acids from Escherichia coli. J Biol Chem. 1975 Jul 25;250(14):5530–5541. [PubMed] [Google Scholar]
  27. Roberts J. W., Roberts C. W. Proteolytic cleavage of bacteriophage lambda repressor in induction. Proc Natl Acad Sci U S A. 1975 Jan;72(1):147–151. doi: 10.1073/pnas.72.1.147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Sidikaro J., Masayasu N. In vitro synthesis of the E3 immunity protein directed by Col E3 plasmid deoxyribonucleic acid. J Biol Chem. 1975 Feb 10;250(3):1123–1131. [PubMed] [Google Scholar]
  29. Squires C., Carbon J., Hill C. W. Glycine transfer RNA of Escherichia coli. I. Structural genes for two glycine tRNA species. J Mol Biol. 1970 Sep 28;52(3):557–569. doi: 10.1016/0022-2836(70)90419-5. [DOI] [PubMed] [Google Scholar]
  30. Squires C., Konrad B., Kirschbaum J., Carbon J. Three adjacent transfer RNA genes in Escherichia coli. Proc Natl Acad Sci U S A. 1973 Feb;70(2):438–441. doi: 10.1073/pnas.70.2.438. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Tomizawa J., Ogawa T. Effect of ultraviolet irradiation on bacteriophage lambda immunity. J Mol Biol. 1967 Jan 28;23(2):247–263. doi: 10.1016/s0022-2836(67)80031-7. [DOI] [PubMed] [Google Scholar]
  32. Watson R. J., Parker J., Fiil N. P., Flaks J. G., Friesen J. D. New chromosomal location for structural genes of ribosomal proteins. Proc Natl Acad Sci U S A. 1975 Jul;72(7):2765–2769. doi: 10.1073/pnas.72.7.2765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Williams B. G., Blattner F. R., Jaskunas S. R., Nomura M. Insertion of DNA carrying ribosomal protein genes of Escherichia coli into Charon vector phages. J Biol Chem. 1977 Oct 25;252(20):7344–7354. [PubMed] [Google Scholar]
  34. Wu M., Davidson N., Carbon J. Physical mapping of the transfer RNA genes on lambda-h80dglytsu+36. J Mol Biol. 1973 Jun 25;78(1):23–34. doi: 10.1016/0022-2836(73)90425-7. [DOI] [PubMed] [Google Scholar]
  35. Yamamoto M., Lindahl L., Nomura M. Synthesis of ribosomal RNA in E. coli: analysis using deletion mutants of a lambda transducing phage carrying ribosomal RNA genes. Cell. 1976 Feb;7(2):179–190. doi: 10.1016/0092-8674(76)90017-9. [DOI] [PubMed] [Google Scholar]
  36. Yamamoto M., Nomura M. Contranscription of genes for RNA polymerase subunits beta and beta' with genes for ribosomal proteins in Escherichia coli. Proc Natl Acad Sci U S A. 1978 Aug;75(8):3891–3895. doi: 10.1073/pnas.75.8.3891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Yamamoto M., Nomura M. Isolation of lambda transducing phages carrying rRNA genes at the metA-purD region of the Escherichia coli chromosome. FEBS Lett. 1976 Dec 31;72(2):256–261. doi: 10.1016/0014-5793(76)80981-7. [DOI] [PubMed] [Google Scholar]
  38. Young R. A., Steitz J. A. Complementary sequences 1700 nucleotides apart form a ribonuclease III cleavage site in Escherichia coli ribosomal precursor RNA. Proc Natl Acad Sci U S A. 1978 Aug;75(8):3593–3597. doi: 10.1073/pnas.75.8.3593. [DOI] [PMC free article] [PubMed] [Google Scholar]

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