Skip to main content
The EMBO Journal logoLink to The EMBO Journal
. 1984 Jun;3(6):1417–1421. doi: 10.1002/j.1460-2075.1984.tb01986.x

A family of dispersed repetitive extragenic palindromic DNA sequences in E. coli.

E Gilson, J M Clément, D Brutlag, M Hofnung
PMCID: PMC557532  PMID: 6378622

Abstract

We report the properties of 67 members of a family of dispersed repetitive palindromic extragenic bacterial DNA sequences. These sequences, called palindromic units, appear to be present at least several hundred times outside structural genes on the Escherichia coli chromosome. They are found either in clusters - as in a previously described intercistronic element - or in single occurrences. They are not only found within an operon but also between different operons, including between convergent ones. The palindromic units could yield a stem and loop structure at the level of DNA or RNA. The base of the stem is made of eight remarkably conserved base pairs while the rest varies somewhat in length and sequence. We analyse the data available on the palindromic units and we speculate on their possible roles with emphasis on transcription and mRNA stability or processing, as well as on their possible relation to transposition elements and the modular evolution of the genome.

Full text

PDF
1420

Selected References

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

  1. Abarbanel R. M., Wieneke P. R., Mansfield E., Jaffe D. A., Brutlag D. L. Rapid searches for complex patterns in biological molecules. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):263–280. doi: 10.1093/nar/12.1part1.263. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bachmann B. J., Low K. B. Linkage map of Escherichia coli K-12, edition 6. Microbiol Rev. 1980 Mar;44(1):1–56. doi: 10.1128/mr.44.1.1-56.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barry G., Squires C., Squires C. L. Attenuation and processing of RNA from the rplJL--rpoBC transcription unit of Escherichia coli. Proc Natl Acad Sci U S A. 1980 Jun;77(6):3331–3335. doi: 10.1073/pnas.77.6.3331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Boyd A., Kendall K., Simon M. I. Structure of the serine chemoreceptor in Escherichia coli. Nature. 1983 Feb 17;301(5901):623–626. doi: 10.1038/301623a0. [DOI] [PubMed] [Google Scholar]
  5. Brosius J., Dull T. J., Sleeter D. D., Noller H. F. Gene organization and primary structure of a ribosomal RNA operon from Escherichia coli. J Mol Biol. 1981 May 15;148(2):107–127. doi: 10.1016/0022-2836(81)90508-8. [DOI] [PubMed] [Google Scholar]
  6. Burton Z. F., Gross C. A., Watanabe K. K., Burgess R. R. The operon that encodes the sigma subunit of RNA polymerase also encodes ribosomal protein S21 and DNA primase in E. coli K12. Cell. 1983 Feb;32(2):335–349. doi: 10.1016/0092-8674(83)90453-1. [DOI] [PubMed] [Google Scholar]
  7. Büchel D. E., Gronenborn B., Müller-Hill B. Sequence of the lactose permease gene. Nature. 1980 Feb 7;283(5747):541–545. doi: 10.1038/283541a0. [DOI] [PubMed] [Google Scholar]
  8. Clément J. M., Hofnung M. Gene sequence of the lambda receptor, an outer membrane protein of E. coli K12. Cell. 1981 Dec;27(3 Pt 2):507–514. doi: 10.1016/0092-8674(81)90392-5. [DOI] [PubMed] [Google Scholar]
  9. Danner D. B., Deich R. A., Sisco K. L., Smith H. O. An eleven-base-pair sequence determines the specificity of DNA uptake in Haemophilus transformation. Gene. 1980 Nov;11(3-4):311–318. doi: 10.1016/0378-1119(80)90071-2. [DOI] [PubMed] [Google Scholar]
  10. Davies W. D., Davidson B. E. The nucleotide sequence of aroG, the gene for 3-deoxy-D-arabinoheptulosonate-7-phosphate synthetase (phe) in Escherichia coli K12. Nucleic Acids Res. 1982 Jul 10;10(13):4045–4058. doi: 10.1093/nar/10.13.4045. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Deeley M. C., Yanofsky C. Nucleotide sequence of the structural gene for tryptophanase of Escherichia coli K-12. J Bacteriol. 1981 Sep;147(3):787–796. doi: 10.1128/jb.147.3.787-796.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Deutch A. H., Smith C. J., Rushlow K. E., Kretschmer P. J. Escherichia coli delta 1-pyrroline-5-carboxylate reductase: gene sequence, protein overproduction and purification. Nucleic Acids Res. 1982 Dec 11;10(23):7701–7714. doi: 10.1093/nar/10.23.7701. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Duchange N., Zakin M. M., Ferrara P., Saint-Girons I., Park I., Tran S. V., Py M. C., Cohen G. N. Structure of the metJBLF cluster in Escherichia coli K12. Sequence of the metB structural gene and of the 5'- and 3'-flanking regions of the metBL operon. J Biol Chem. 1983 Dec 25;258(24):14868–14871. [PubMed] [Google Scholar]
  14. Dunn J. J., Studier F. W. Complete nucleotide sequence of bacteriophage T7 DNA and the locations of T7 genetic elements. J Mol Biol. 1983 Jun 5;166(4):477–535. doi: 10.1016/s0022-2836(83)80282-4. [DOI] [PubMed] [Google Scholar]
  15. Erdei S., Boros I., Szabó G., Venetianer P. A novel type of bacterial transcription unit, specifying mRNA, rRNA, and tRNA. Mol Gen Genet. 1983;191(1):162–164. doi: 10.1007/BF00330905. [DOI] [PubMed] [Google Scholar]
  16. Higgins C. F., Ames G. F., Barnes W. M., Clement J. M., Hofnung M. A novel intercistronic regulatory element of prokaryotic operons. Nature. 1982 Aug 19;298(5876):760–762. doi: 10.1038/298760a0. [DOI] [PubMed] [Google Scholar]
  17. Higgins C. F., Haag P. D., Nikaido K., Ardeshir F., Garcia G., Ames G. F. Complete nucleotide sequence and identification of membrane components of the histidine transport operon of S. typhimurium. Nature. 1982 Aug 19;298(5876):723–727. doi: 10.1038/298723a0. [DOI] [PubMed] [Google Scholar]
  18. Inokuchi Y., Hirashima A., Watanabe I. Comparison of the nucleotide sequences at the 3'-terminal region of RNAs from RNA coliphages. J Mol Biol. 1982 Jul 15;158(4):711–730. doi: 10.1016/0022-2836(82)90256-x. [DOI] [PubMed] [Google Scholar]
  19. Joyce C. M., Kelley W. S., Grindley N. D. Nucleotide sequence of the Escherichia coli polA gene and primary structure of DNA polymerase I. J Biol Chem. 1982 Feb 25;257(4):1958–1964. [PubMed] [Google Scholar]
  20. Kingston R. E., Chamberlin M. J. Pausing and attenuation of in vitro transcription in the rrnB operon of E. coli. Cell. 1981 Dec;27(3 Pt 2):523–531. doi: 10.1016/0092-8674(81)90394-9. [DOI] [PubMed] [Google Scholar]
  21. Kleckner N. Transposable elements in prokaryotes. Annu Rev Genet. 1981;15:341–404. doi: 10.1146/annurev.ge.15.120181.002013. [DOI] [PubMed] [Google Scholar]
  22. Kopecko D. J., Brevet J., Cohen S. N. Involvement of multiple translocating DNA segments and recombinational hotspots in the structural evolution of bacterial plasmids. J Mol Biol. 1976 Dec;108(2):333–360. doi: 10.1016/s0022-2836(76)80124-6. [DOI] [PubMed] [Google Scholar]
  23. Lee C. A., Saier M. H., Jr Mannitol-specific enzyme II of the bacterial phosphotransferase system. III. The nucleotide sequence of the permease gene. J Biol Chem. 1983 Sep 10;258(17):10761–10767. [PubMed] [Google Scholar]
  24. Lightner V. A., Bell R. M., Modrich P. The DNA sequences encoding plsB and dgk loci of Escherichia coli. J Biol Chem. 1983 Sep 25;258(18):10856–10861. [PubMed] [Google Scholar]
  25. Lundberg L. G., Thoresson H. O., Karlström O. H., Nyman P. O. Nucleotide sequence of the structural gene for dUTPase of Escherichia coli K-12. EMBO J. 1983;2(6):967–971. doi: 10.1002/j.1460-2075.1983.tb01529.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. McPherson M. J., Wootton J. C. Complete nucleotide sequence of the Escherichia coli gdhA gene. Nucleic Acids Res. 1983 Aug 11;11(15):5257–5266. doi: 10.1093/nar/11.15.5257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Nakajima N., Ozeki H., Shimura Y. In vitro transcription of the supB-E tRNA operon of Escherichia coli. Characterization of transcription products. J Biol Chem. 1982 Sep 25;257(18):11113–11120. [PubMed] [Google Scholar]
  28. Nakajima N., Ozeki H., Shimura Y. Organization and structure of an E. coli tRNA operon containing seven tRNA genes. Cell. 1981 Jan;23(1):239–249. doi: 10.1016/0092-8674(81)90288-9. [DOI] [PubMed] [Google Scholar]
  29. Overbeeke N., Bergmans H., van Mansfeld F., Lugtenberg B. Complete nucleotide sequence of phoE, the structural gene for the phosphate limitation inducible outer membrane pore protein of Escherichia coli K12. J Mol Biol. 1983 Feb 5;163(4):513–532. doi: 10.1016/0022-2836(83)90110-9. [DOI] [PubMed] [Google Scholar]
  30. Parsot C., Cossart P., Saint-Girons I., Cohen G. N. Nucleotide sequence of thrC and of the transcription termination region of the threonine operon in Escherichia coli K12. Nucleic Acids Res. 1983 Nov 11;11(21):7331–7345. doi: 10.1093/nar/11.21.7331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Plamann M. D., Stauffer L. T., Urbanowski M. L., Stauffer G. V. Complete nucleotide sequence of the E. coli glyA gene. Nucleic Acids Res. 1983 Apr 11;11(7):2065–2075. doi: 10.1093/nar/11.7.2065. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Poulsen P., Jensen K. F., Valentin-Hansen P., Carlsson P., Lundberg L. G. Nucleotide sequence of the Escherichia coli pyrE gene and of the DNA in front of the protein-coding region. Eur J Biochem. 1983 Sep 15;135(2):223–229. doi: 10.1111/j.1432-1033.1983.tb07641.x. [DOI] [PubMed] [Google Scholar]
  33. Proudfoot N. The end of the message and beyond. Nature. 1984 Feb 2;307(5950):412–413. doi: 10.1038/307412a0. [DOI] [PubMed] [Google Scholar]
  34. Reed R. E., Altman S. Repeated sequences and open reading frames in the 3' flanking region of the gene for the RNA subunit of Escherichia coli ribonuclease P. Proc Natl Acad Sci U S A. 1983 Sep;80(17):5359–5363. doi: 10.1073/pnas.80.17.5359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Rice P. W., Dahlberg J. E. A gene between polA and glnA retards growth of Escherichia coli when present in multiple copies: physiological effects of the gene for spot 42 RNA. J Bacteriol. 1982 Dec;152(3):1196–1210. doi: 10.1128/jb.152.3.1196-1210.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Saint-Girons I., Duchange N., Zakin M. M., Park I., Margarita D., Ferrara P., Cohen G. N. Nucleotide sequence of metF, the E. coli structural gene for 5-10 methylene tetrahydrofolate reductase and of its control region. Nucleic Acids Res. 1983 Oct 11;11(19):6723–6732. doi: 10.1093/nar/11.19.6723. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Sanger F., Coulson A. R., Hong G. F., Hill D. F., Petersen G. B. Nucleotide sequence of bacteriophage lambda DNA. J Mol Biol. 1982 Dec 25;162(4):729–773. doi: 10.1016/0022-2836(82)90546-0. [DOI] [PubMed] [Google Scholar]
  38. Schwartz I., Klotsky R. A., Elseviers D., Gallagher P. J., Krauskopf M., Siddiqui M. A., Wong J. F., Roe B. A. Molecular cloning and sequencing of pheU, a gene for Escherichia coli tRNAPhe. Nucleic Acids Res. 1983 Jul 11;11(13):4379–4389. doi: 10.1093/nar/11.13.4379. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Shen W. F., Squires C., Squires C. L. Nucleotide sequence of the rrnG ribosomal RNA promoter region of Escherichia coli. Nucleic Acids Res. 1982 May 25;10(10):3303–3313. doi: 10.1093/nar/10.10.3303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Singleton C. K., Roeder W. D., Bogosian G., Somerville R. L., Weith H. L. DNA sequence of the E. coli trpR gene and prediction of the amino acid sequence of Trp repressor. Nucleic Acids Res. 1980 Apr 11;8(7):1551–1560. doi: 10.1093/nar/8.7.1551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Smith D. R., Calvo J. M. Nucleotide sequence of the E coli gene coding for dihydrofolate reductase. Nucleic Acids Res. 1980 May 24;8(10):2255–2274. doi: 10.1093/nar/8.10.2255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Stragier P., Patte J. C. Regulation of diaminopimelate decarboxylase synthesis in Escherichia coli. III. Nucleotide sequence and regulation of the lysR gene. J Mol Biol. 1983 Aug 5;168(2):333–350. doi: 10.1016/s0022-2836(83)80022-9. [DOI] [PubMed] [Google Scholar]
  43. Tinoco I., Jr, Borer P. N., Dengler B., Levin M. D., Uhlenbeck O. C., Crothers D. M., Bralla J. Improved estimation of secondary structure in ribonucleic acids. Nat New Biol. 1973 Nov 14;246(150):40–41. doi: 10.1038/newbio246040a0. [DOI] [PubMed] [Google Scholar]
  44. Valentin-Hansen P., Hammer-Jespersen K., Boetius F., Svendsen I. Structure and function of the intercistronic regulatory deoC-deoA element of Escherichia coli K-12. EMBO J. 1984 Jan;3(1):179–183. doi: 10.1002/j.1460-2075.1984.tb01781.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Wu A. M., Christie G. E., Platt T. Tandem termination sites in the tryptophan operon of Escherichia coli. Proc Natl Acad Sci U S A. 1981 May;78(5):2913–2917. doi: 10.1073/pnas.78.5.2913. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Yamao F., Inokuchi H., Cheung A., Ozeki H., Söll D. Escherichia coli glutaminyl-tRNA synthetase. I. Isolation and DNA sequence of the glnS gene. J Biol Chem. 1982 Oct 10;257(19):11639–11643. [PubMed] [Google Scholar]
  47. Young I. G., Rogers B. L., Campbell H. D., Jaworowski A., Shaw D. C. Nucleotide sequence coding for the respiratory NADH dehydrogenase of Escherichia coli. UUG initiation codon. Eur J Biochem. 1981 May;116(1):165–170. doi: 10.1111/j.1432-1033.1981.tb05314.x. [DOI] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES