Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1995 Feb;177(3):660–666. doi: 10.1128/jb.177.3.660-666.1995

Very short patch repair of T:G mismatches in vivo: importance of context and accessory proteins.

M Lieb 1, S Rehmat 1
PMCID: PMC176641  PMID: 7836300

Abstract

In Escherichia coli, T:G mismatches in specific contexts are corrected by a very short patch (VSP) repair system. Previous studies have shown that the product of gene vsr mediates correction of T:G to C:G in the 5'CTAGG/3'GGTCC context and in some related contexts. Amber mutations that arose in CAG sequences in gene cI of bacteriophage lambda were used to determine the effect of flanking bases on the repair of T:G mispairs arising during phage recombination. The experimental findings were combined with published data on mismatch repair of mutations in lambda gene P and E. coli gene lacI. While VSP repair was most efficient in the context 5'CTAGG, there was very significant correction when either the 5'C or the 3' G was replaced by another base. Some mismatch repair of TAG to CAG occurred in all contexts tested. Reduction in VSP repair caused by the lack of MutL or MutS was fully complemented by the addition of vsr+ plasmids when the T:G mispair was in the 5'CTAGG/3'GGTCC context. VSP repair was decreased in bacteria containing mutS+ on a multicopy plasmid. It is suggested that VSP repair maintains sequences such as the repetitive extragenic palindromic (REP) and Chi sequences, which have important roles in E. coli and closely related bacteria.

Full Text

The Full Text of this article is available as a PDF (257.2 KB).

Selected References

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

  1. Au K. G., Cabrera M., Miller J. H., Modrich P. Escherichia coli mutY gene product is required for specific A-G----C.G mismatch correction. Proc Natl Acad Sci U S A. 1988 Dec;85(23):9163–9166. doi: 10.1073/pnas.85.23.9163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bachmann B. J. Pedigrees of some mutant strains of Escherichia coli K-12. Bacteriol Rev. 1972 Dec;36(4):525–557. doi: 10.1128/br.36.4.525-557.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bale A., d'Alarcao M., Marinus M. G. Characterization of DNA adenine methylation mutants of Escherichia coli K12. Mutat Res. 1979 Feb;59(2):157–165. doi: 10.1016/0027-5107(79)90153-2. [DOI] [PubMed] [Google Scholar]
  4. Bhagwat A. S., McClelland M. DNA mismatch correction by Very Short Patch repair may have altered the abundance of oligonucleotides in the E. coli genome. Nucleic Acids Res. 1992 Apr 11;20(7):1663–1668. doi: 10.1093/nar/20.7.1663. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Blaisdell B. E., Rudd K. E., Matin A., Karlin S. Significant dispersed recurrent DNA sequences in the Escherichia coli genome. Several new groups. J Mol Biol. 1993 Feb 20;229(4):833–848. doi: 10.1006/jmbi.1993.1090. [DOI] [PubMed] [Google Scholar]
  6. Burge C., Campbell A. M., Karlin S. Over- and under-representation of short oligonucleotides in DNA sequences. Proc Natl Acad Sci U S A. 1992 Feb 15;89(4):1358–1362. doi: 10.1073/pnas.89.4.1358. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Burland V., Plunkett G., 3rd, Daniels D. L., Blattner F. R. DNA sequence and analysis of 136 kilobases of the Escherichia coli genome: organizational symmetry around the origin of replication. Genomics. 1993 Jun;16(3):551–561. doi: 10.1006/geno.1993.1230. [DOI] [PubMed] [Google Scholar]
  8. Cheng K. C., Smith G. R. Recombinational hotspot activity of Chi-like sequences. J Mol Biol. 1984 Dec 5;180(2):371–377. doi: 10.1016/s0022-2836(84)80009-1. [DOI] [PubMed] [Google Scholar]
  9. Coulondre C., Miller J. H., Farabaugh P. J., Gilbert W. Molecular basis of base substitution hotspots in Escherichia coli. Nature. 1978 Aug 24;274(5673):775–780. doi: 10.1038/274775a0. [DOI] [PubMed] [Google Scholar]
  10. Coulondre C., Miller J. H. Genetic studies of the lac repressor. III. Additional correlation of mutational sites with specific amino acid residues. J Mol Biol. 1977 Dec 15;117(3):525–567. doi: 10.1016/0022-2836(77)90056-0. [DOI] [PubMed] [Google Scholar]
  11. Daniels D. L., Plunkett G., 3rd, Burland V., Blattner F. R. Analysis of the Escherichia coli genome: DNA sequence of the region from 84.5 to 86.5 minutes. Science. 1992 Aug 7;257(5071):771–778. doi: 10.1126/science.1379743. [DOI] [PubMed] [Google Scholar]
  12. Dimri G. P., Rudd K. E., Morgan M. K., Bayat H., Ames G. F. Physical mapping of repetitive extragenic palindromic sequences in Escherichia coli and phylogenetic distribution among Escherichia coli strains and other enteric bacteria. J Bacteriol. 1992 Jul;174(14):4583–4593. doi: 10.1128/jb.174.14.4583-4593.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Dzidic S., Radman M. Genetic requirements for hyper-recombination by very short patch mismatch repair: involvement of Escherichia coli DNA polymerase I. Mol Gen Genet. 1989 Jun;217(2-3):254–256. doi: 10.1007/BF02464889. [DOI] [PubMed] [Google Scholar]
  14. Fisher C., Parks R. J., Lauzon M. L., Evans D. H. Heteroduplex DNA formation is associated with replication and recombination in poxvirus-infected cells. Genetics. 1991 Sep;129(1):7–18. doi: 10.1093/genetics/129.1.7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gabbara S., Wyszynski M., Bhagwat A. S. A DNA repair process in Escherichia coli corrects U:G and T:G mismatches to C:G at sites of cytosine methylation. Mol Gen Genet. 1994 Apr;243(2):244–248. doi: 10.1007/BF00280322. [DOI] [PubMed] [Google Scholar]
  16. Garcia P., Gasc A. M., Kyriakidis X., Baty D., Sicard M. DNA sequences required to induce localized conversion in Streptococcus pneumoniae transformation. Mol Gen Genet. 1988 Nov;214(3):509–513. doi: 10.1007/BF00330488. [DOI] [PubMed] [Google Scholar]
  17. Grilley M., Welsh K. M., Su S. S., Modrich P. Isolation and characterization of the Escherichia coli mutL gene product. J Biol Chem. 1989 Jan 15;264(2):1000–1004. [PubMed] [Google Scholar]
  18. Hennecke F., Kolmar H., Bründl K., Fritz H. J. The vsr gene product of E. coli K-12 is a strand- and sequence-specific DNA mismatch endonuclease. Nature. 1991 Oct 24;353(6346):776–778. doi: 10.1038/353776a0. [DOI] [PubMed] [Google Scholar]
  19. Jones M., Wagner R., Radman M. Mismatch repair and recombination in E. coli. Cell. 1987 Aug 14;50(4):621–626. doi: 10.1016/0092-8674(87)90035-3. [DOI] [PubMed] [Google Scholar]
  20. Jones M., Wagner R., Radman M. Mismatch repair of deaminated 5-methyl-cytosine. J Mol Biol. 1987 Mar 5;194(1):155–159. doi: 10.1016/0022-2836(87)90724-8. [DOI] [PubMed] [Google Scholar]
  21. Jones M., Wagner R., Radman M. Repair of a mismatch is influenced by the base composition of the surrounding nucleotide sequence. Genetics. 1987 Apr;115(4):605–610. doi: 10.1093/genetics/115.4.605. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lefèvre J. C., Gasc A. M., Burger A. C., Mostachfi P., Sicard A. M. Hyperrecombination at a specific DNA sequence in pneumococcal transformation. Proc Natl Acad Sci U S A. 1984 Aug;81(16):5184–5188. doi: 10.1073/pnas.81.16.5184. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lieb M., Allen E., Read D. Very short patch mismatch repair in phage lambda: repair sites and length of repair tracts. Genetics. 1986 Dec;114(4):1041–1060. doi: 10.1093/genetics/114.4.1041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Lieb M. Bacterial genes mutL, mutS, and dcm participate in repair of mismatches at 5-methylcytosine sites. J Bacteriol. 1987 Nov;169(11):5241–5246. doi: 10.1128/jb.169.11.5241-5246.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Lieb M. Mapping missense and nonsense mutation in gene cI of bacteriophage lambda: marker effects. Mol Gen Genet. 1976 Aug 2;146(3):285–290. doi: 10.1007/BF00701252. [DOI] [PubMed] [Google Scholar]
  26. Lieb M. Recombination in the lambda repressor gene: evidence that very short patch (VSP) mismatch correction restores a specific sequence. Mol Gen Genet. 1985;199(3):465–470. doi: 10.1007/BF00330759. [DOI] [PubMed] [Google Scholar]
  27. Lieb M. Specific mismatch correction in bacteriophage lambda crosses by very short patch repair. Mol Gen Genet. 1983;191(1):118–125. doi: 10.1007/BF00330898. [DOI] [PubMed] [Google Scholar]
  28. Lieb M. Spontaneous mutation at a 5-methylcytosine hotspot is prevented by very short patch (VSP) mismatch repair. Genetics. 1991 May;128(1):23–27. doi: 10.1093/genetics/128.1.23. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Lu A. L., Chang D. Y. Repair of single base-pair transversion mismatches of Escherichia coli in vitro: correction of certain A/G mismatches is independent of dam methylation and host mutHLS gene functions. Genetics. 1988 Apr;118(4):593–600. doi: 10.1093/genetics/118.4.593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Marinus M. G. Location of DNA methylation genes on the Escherichia coli K-12 genetic map. Mol Gen Genet. 1973 Dec 14;127(1):47–55. doi: 10.1007/BF00267782. [DOI] [PubMed] [Google Scholar]
  31. May M. S., Hattaman S. Deoxyribonucleic acid-cytosine methylation by host- and plasmid-controlled enzymes. J Bacteriol. 1975 Apr;122(1):129–138. doi: 10.1128/jb.122.1.129-138.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Merkl R., Kröger M., Rice P., Fritz H. J. Statistical evaluation and biological interpretation of non-random abundance in the E. coli K-12 genome of tetra- and pentanucleotide sequences related to VSP DNA mismatch repair. Nucleic Acids Res. 1992 Apr 11;20(7):1657–1662. doi: 10.1093/nar/20.7.1657. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Modrich P. Mechanisms and biological effects of mismatch repair. Annu Rev Genet. 1991;25:229–253. doi: 10.1146/annurev.ge.25.120191.001305. [DOI] [PubMed] [Google Scholar]
  34. Radicella J. P., Clark E. A., Fox M. S. Some mismatch repair activities in Escherichia coli. Proc Natl Acad Sci U S A. 1988 Dec;85(24):9674–9678. doi: 10.1073/pnas.85.24.9674. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Raposa S., Fox M. S. Some features of base pair mismatch and heterology repair in Escherichia coli. Genetics. 1987 Nov;117(3):381–390. doi: 10.1093/genetics/117.3.381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Schultz D. W., Smith G. R. Conservation of Chi cutting activity in terrestrial and marine enteric bacteria. J Mol Biol. 1986 Jun 20;189(4):585–595. doi: 10.1016/0022-2836(86)90489-4. [DOI] [PubMed] [Google Scholar]
  37. Shcherbakov V. P., Plugina L. A. Marker-dependent recombination in T4 bacteriophage. III. Structural prerequisites for marker discrimination. Genetics. 1991 Aug;128(4):673–685. doi: 10.1093/genetics/128.4.673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Smith G. R. Homologous recombination in procaryotes. Microbiol Rev. 1988 Mar;52(1):1–28. doi: 10.1128/mr.52.1.1-28.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Sohail A., Lieb M., Dar M., Bhagwat A. S. A gene required for very short patch repair in Escherichia coli is adjacent to the DNA cytosine methylase gene. J Bacteriol. 1990 Aug;172(8):4214–4221. doi: 10.1128/jb.172.8.4214-4221.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Stahl F. W. Special sites in generalized recombination. Annu Rev Genet. 1979;13:7–24. doi: 10.1146/annurev.ge.13.120179.000255. [DOI] [PubMed] [Google Scholar]
  41. Stern M. J., Ames G. F., Smith N. H., Robinson E. C., Higgins C. F. Repetitive extragenic palindromic sequences: a major component of the bacterial genome. Cell. 1984 Jul;37(3):1015–1026. doi: 10.1016/0092-8674(84)90436-7. [DOI] [PubMed] [Google Scholar]
  42. Su S. S., Modrich P. Escherichia coli mutS-encoded protein binds to mismatched DNA base pairs. Proc Natl Acad Sci U S A. 1986 Jul;83(14):5057–5061. doi: 10.1073/pnas.83.14.5057. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Yang Y., Ames G. F. DNA gyrase binds to the family of prokaryotic repetitive extragenic palindromic sequences. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8850–8854. doi: 10.1073/pnas.85.23.8850. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Yura T., Mori H., Nagai H., Nagata T., Ishihama A., Fujita N., Isono K., Mizobuchi K., Nakata A. Systematic sequencing of the Escherichia coli genome: analysis of the 0-2.4 min region. Nucleic Acids Res. 1992 Jul 11;20(13):3305–3308. doi: 10.1093/nar/20.13.3305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Zell R., Fritz H. J. DNA mismatch-repair in Escherichia coli counteracting the hydrolytic deamination of 5-methyl-cytosine residues. EMBO J. 1987 Jun;6(6):1809–1815. doi: 10.1002/j.1460-2075.1987.tb02435.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES