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. 1996 Mar;142(3):681–691. doi: 10.1093/genetics/142.3.681

Opposing Roles of the Holliday Junction Processing Systems of Escherichia Coli in Recombination-Dependent Adaptive Mutation

R S Harris 1, K J Ross 1, S M Rosenberg 1
PMCID: PMC1207010  PMID: 8849879

Abstract

Aspects of the molecular mechanism of ``adaptive'' mutation are emerging from one experimental system: reversion of an Escherichia coli lac frameshift mutation carried on a conjugative plasmid. Homologous recombination is required and the mutations resemble polymerase errors. Reports implicating a role for conjugal transfer proteins suggested that the mutation mechanism is ordinary replication error occurring during transfer synthesis, followed by conjugation-like recombination, to capture the replicated fragment into an intact replicon. Whereas conjugational recombination uses either of two systems of Holliday junction resolution, we find that the adaptive lac reversions are inhibited by one resolution system and promoted by the other. Moreover, temporary absence of both resolution systems promotes mutation. These results imply that recombination intermediates themselves promote the mutations.

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Selected References

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  1. Asai T., Sommer S., Bailone A., Kogoma T. Homologous recombination-dependent initiation of DNA replication from DNA damage-inducible origins in Escherichia coli. EMBO J. 1993 Aug;12(8):3287–3295. doi: 10.1002/j.1460-2075.1993.tb05998.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Cairns J., Foster P. L. Adaptive reversion of a frameshift mutation in Escherichia coli. Genetics. 1991 Aug;128(4):695–701. doi: 10.1093/genetics/128.4.695. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Cairns J., Overbaugh J., Miller S. The origin of mutants. Nature. 1988 Sep 8;335(6186):142–145. doi: 10.1038/335142a0. [DOI] [PubMed] [Google Scholar]
  4. Cupples C. G., Cabrera M., Cruz C., Miller J. H. A set of lacZ mutations in Escherichia coli that allow rapid detection of specific frameshift mutations. Genetics. 1990 Jun;125(2):275–280. doi: 10.1093/genetics/125.2.275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Demerec M. "SELFERS"-ATTRIBUTED TO UNEQUAL CROSSOVERS IN SALMONELLA. Proc Natl Acad Sci U S A. 1962 Oct;48(10):1696–1704. doi: 10.1073/pnas.48.10.1696. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Drake J. W. Spontaneous mutation. Annu Rev Genet. 1991;25:125–146. doi: 10.1146/annurev.ge.25.120191.001013. [DOI] [PubMed] [Google Scholar]
  7. Dutreix M., Rao B. J., Radding C. M. The effects on strand exchange of 5' versus 3' ends of single-stranded DNA in RecA nucleoprotein filaments. J Mol Biol. 1991 Jun 20;219(4):645–654. doi: 10.1016/0022-2836(91)90661-o. [DOI] [PubMed] [Google Scholar]
  8. Esposito M. S., Bruschi C. V. Diploid yeast cells yield homozygous spontaneous mutations. Curr Genet. 1993 May-Jun;23(5-6):430–434. doi: 10.1007/BF00312630. [DOI] [PubMed] [Google Scholar]
  9. Foster P. L. Adaptive mutation: the uses of adversity. Annu Rev Microbiol. 1993;47:467–504. doi: 10.1146/annurev.mi.47.100193.002343. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Foster P. L., Gudmundsson G., Trimarchi J. M., Cai H., Goodman M. F. Proofreading-defective DNA polymerase II increases adaptive mutation in Escherichia coli. Proc Natl Acad Sci U S A. 1995 Aug 15;92(17):7951–7955. doi: 10.1073/pnas.92.17.7951. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Foster P. L., Trimarchi J. M. Adaptive reversion of a frameshift mutation in Escherichia coli by simple base deletions in homopolymeric runs. Science. 1994 Jul 15;265(5170):407–409. doi: 10.1126/science.8023164. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. François V., Louarn J., Patte J., Louaran J. M. A system for in vivo selection of genomic rearrangements with predetermined endpoints in Escherichia coli using modified Tn10 transposons. Gene. 1987;56(1):99–108. doi: 10.1016/0378-1119(87)90162-4. [DOI] [PubMed] [Google Scholar]
  13. Frost L. S., Ippen-Ihler K., Skurray R. A. Analysis of the sequence and gene products of the transfer region of the F sex factor. Microbiol Rev. 1994 Jun;58(2):162–210. doi: 10.1128/mr.58.2.162-210.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Galitski T., Roth J. R. Evidence that F plasmid transfer replication underlies apparent adaptive mutation. Science. 1995 Apr 21;268(5209):421–423. doi: 10.1126/science.7716546. [DOI] [PubMed] [Google Scholar]
  15. Hall B. G. Spontaneous point mutations that occur more often when advantageous than when neutral. Genetics. 1990 Sep;126(1):5–16. doi: 10.1093/genetics/126.1.5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Harris R. S., Longerich S., Rosenberg S. M. Recombination in adaptive mutation. Science. 1994 Apr 8;264(5156):258–260. doi: 10.1126/science.8146657. [DOI] [PubMed] [Google Scholar]
  17. Jensen R. B., Gerdes K. Programmed cell death in bacteria: proteic plasmid stabilization systems. Mol Microbiol. 1995 Jul;17(2):205–210. doi: 10.1111/j.1365-2958.1995.mmi_17020205.x. [DOI] [PubMed] [Google Scholar]
  18. Kowalczykowski S. C., Dixon D. A., Eggleston A. K., Lauder S. D., Rehrauer W. M. Biochemistry of homologous recombination in Escherichia coli. Microbiol Rev. 1994 Sep;58(3):401–465. doi: 10.1128/mr.58.3.401-465.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kuzminov A. Collapse and repair of replication forks in Escherichia coli. Mol Microbiol. 1995 May;16(3):373–384. doi: 10.1111/j.1365-2958.1995.tb02403.x. [DOI] [PubMed] [Google Scholar]
  20. Levinson G., Gutman G. A. High frequencies of short frameshifts in poly-CA/TG tandem repeats borne by bacteriophage M13 in Escherichia coli K-12. Nucleic Acids Res. 1987 Jul 10;15(13):5323–5338. doi: 10.1093/nar/15.13.5323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lloyd R. G. Conjugational recombination in resolvase-deficient ruvC mutants of Escherichia coli K-12 depends on recG. J Bacteriol. 1991 Sep;173(17):5414–5418. doi: 10.1128/jb.173.17.5414-5418.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Louarn J. M., Louarn J., François V., Patte J. Analysis and possible role of hyperrecombination in the termination region of the Escherichia coli chromosome. J Bacteriol. 1991 Aug;173(16):5097–5104. doi: 10.1128/jb.173.16.5097-5104.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Luisi-DeLuca C., Lovett S. T., Kolodner R. D. Genetic and physical analysis of plasmid recombination in recB recC sbcB and recB recC sbcA Escherichia coli K-12 mutants. Genetics. 1989 Jun;122(2):269–278. doi: 10.1093/genetics/122.2.269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Luria S. E., Delbrück M. Mutations of Bacteria from Virus Sensitivity to Virus Resistance. Genetics. 1943 Nov;28(6):491–511. doi: 10.1093/genetics/28.6.491. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Magni G E, Von Borstel R C. Different Rates of Spontaneous Mutation during Mitosis and Meiosis in Yeast. Genetics. 1962 Aug;47(8):1097–1108. doi: 10.1093/genetics/47.8.1097. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Mandal T. N., Mahdi A. A., Sharples G. J., Lloyd R. G. Resolution of Holliday intermediates in recombination and DNA repair: indirect suppression of ruvA, ruvB, and ruvC mutations. J Bacteriol. 1993 Jul;175(14):4325–4334. doi: 10.1128/jb.175.14.4325-4334.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Matic I., Rayssiguier C., Radman M. Interspecies gene exchange in bacteria: the role of SOS and mismatch repair systems in evolution of species. Cell. 1995 Feb 10;80(3):507–515. doi: 10.1016/0092-8674(95)90501-4. [DOI] [PubMed] [Google Scholar]
  28. Modrich P. Mismatch repair, genetic stability, and cancer. Science. 1994 Dec 23;266(5193):1959–1960. doi: 10.1126/science.7801122. [DOI] [PubMed] [Google Scholar]
  29. PASZEWSKI A., SURZYCKI S. 'SELFERS' AND HIGH MUTATION RATE DURING MEIOSIS IN ASCOBOLUS IMMERSUS. Nature. 1964 Nov 21;204:809–809. doi: 10.1038/204809a0. [DOI] [PubMed] [Google Scholar]
  30. Peters J. E., Benson S. A. Redundant transfer of F' plasmids occurs between Escherichia coli cells during nonlethal selections. J Bacteriol. 1995 Feb;177(3):847–850. doi: 10.1128/jb.177.3.847-850.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Priebe S. D., Westmoreland J., Nilsson-Tillgren T., Resnick M. A. Induction of recombination between homologous and diverged DNAs by double-strand gaps and breaks and role of mismatch repair. Mol Cell Biol. 1994 Jul;14(7):4802–4814. doi: 10.1128/mcb.14.7.4802. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Radicella J. P., Park P. U., Fox M. S. Adaptive mutation in Escherichia coli: a role for conjugation. Science. 1995 Apr 21;268(5209):418–420. doi: 10.1126/science.7716545. [DOI] [PubMed] [Google Scholar]
  33. Razavy H., Szigety S. K., Rosenberg S. M. Evidence for both 3' and 5' single-strand DNA ends in intermediates in chi-stimulated recombination in vivo. Genetics. 1996 Feb;142(2):333–339. doi: 10.1093/genetics/142.2.333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Rinken R., Thomas B., Wackernagel W. Evidence that recBC-dependent degradation of duplex DNA in Escherichia coli recD mutants involves DNA unwinding. J Bacteriol. 1992 Aug;174(16):5424–5429. doi: 10.1128/jb.174.16.5424-5429.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Ripley L. S. Frameshift mutation: determinants of specificity. Annu Rev Genet. 1990;24:189–213. doi: 10.1146/annurev.ge.24.120190.001201. [DOI] [PubMed] [Google Scholar]
  36. Rosenberg S. M., Harris R. S., Torkelson J. Molecular handles on adaptive mutation. Mol Microbiol. 1995 Oct;18(2):185–189. doi: 10.1111/j.1365-2958.1995.mmi_18020185.x. [DOI] [PubMed] [Google Scholar]
  37. Rosenberg S. M., Hastings P. J. The split-end model for homologous recombination at double-strand breaks and at Chi. Biochimie. 1991 Apr;73(4):385–397. doi: 10.1016/0300-9084(91)90105-a. [DOI] [PubMed] [Google Scholar]
  38. Rosenberg S. M. In pursuit of a molecular mechanism for adaptive mutation. Genome. 1994 Dec;37(6):893–899. doi: 10.1139/g94-127. [DOI] [PubMed] [Google Scholar]
  39. Ryan F. J. Spontaneous Mutation in Non-Dividing Bacteria. Genetics. 1955 Sep;40(5):726–738. doi: 10.1093/genetics/40.5.726. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Steele D. F., Jinks-Robertson S. An examination of adaptive reversion in Saccharomyces cerevisiae. Genetics. 1992 Sep;132(1):9–21. doi: 10.1093/genetics/132.1.9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Strand M., Prolla T. A., Liskay R. M., Petes T. D. Destabilization of tracts of simple repetitive DNA in yeast by mutations affecting DNA mismatch repair. Nature. 1993 Sep 16;365(6443):274–276. doi: 10.1038/365274a0. [DOI] [PubMed] [Google Scholar]
  42. Streisinger G., Okada Y., Emrich J., Newton J., Tsugita A., Terzaghi E., Inouye M. Frameshift mutations and the genetic code. This paper is dedicated to Professor Theodosius Dobzhansky on the occasion of his 66th birthday. Cold Spring Harb Symp Quant Biol. 1966;31:77–84. doi: 10.1101/sqb.1966.031.01.014. [DOI] [PubMed] [Google Scholar]
  43. West S. C. Enzymes and molecular mechanisms of genetic recombination. Annu Rev Biochem. 1992;61:603–640. doi: 10.1146/annurev.bi.61.070192.003131. [DOI] [PubMed] [Google Scholar]
  44. West S. C. The processing of recombination intermediates: mechanistic insights from studies of bacterial proteins. Cell. 1994 Jan 14;76(1):9–15. doi: 10.1016/0092-8674(94)90168-6. [DOI] [PubMed] [Google Scholar]
  45. Whitby M. C., Lloyd R. G. Branch migration of three-strand recombination intermediates by RecG, a possible pathway for securing exchanges initiated by 3'-tailed duplex DNA. EMBO J. 1995 Jul 17;14(14):3302–3310. doi: 10.1002/j.1460-2075.1995.tb07337.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Whitby M. C., Ryder L., Lloyd R. G. Reverse branch migration of Holliday junctions by RecG protein: a new mechanism for resolution of intermediates in recombination and DNA repair. Cell. 1993 Oct 22;75(2):341–350. doi: 10.1016/0092-8674(93)80075-p. [DOI] [PubMed] [Google Scholar]
  47. Whitby M. C., Vincent S. D., Lloyd R. G. Branch migration of Holliday junctions: identification of RecG protein as a junction specific DNA helicase. EMBO J. 1994 Nov 1;13(21):5220–5228. doi: 10.1002/j.1460-2075.1994.tb06853.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Wong K., Paranchych W. The preservation of the secondary structure of R17 RNA during penetration into host bacteria. Virology. 1976 Sep;73(2):476–488. doi: 10.1016/0042-6822(76)90409-8. [DOI] [PubMed] [Google Scholar]

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