Skip to main content
Genetics logoLink to Genetics
. 1989 Mar;121(3):433–443. doi: 10.1093/genetics/121.3.433

Role of Recbc Function in Formation of Chromosomal Rearrangements: A Two-Step Model for Recombination

M J Mahan 1, J R Roth 1
PMCID: PMC1203631  PMID: 2714635

Abstract

The role of recBC functions has been tested for three types of chromosomal recombination events: (1) recombination between direct repeats to generate a deletion, (2) recombination between a small circular fragment and the chromosome, and (3) recombination between inversely oriented repeats to form an inversion. Deletion formation by recombination between direct repeats, which does not require a fully reciprocal exchange, is independent of recBC function. Circle integration and inversion formation are both stimulated by the recBC function; these events require full reciprocality. The results suggest that half-reciprocal exchanges can occur without recBC, but recBC functions greatly stimulate completion of a fully reciprocal exchange. We propose that chromosomal recombination is a two-step process, and recBC functions are primarily required for the second step.

Full Text

The Full Text of this article is available as a PDF (1.1 MB).

Selected References

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

  1. Abstracts of papers presented at the 1980 meetings of the Genetic Society of America. Boulder, Colorado August 18-20, 1980. Genetics. 1980;94(4 Pt 2 Suppl):1–16. [PMC free article] [PubMed] [Google Scholar]
  2. Berkowitz D., Hushon J. M., Whitfield H. J., Jr, Roth J., Ames B. N. Procedure for identifying nonsense mutations. J Bacteriol. 1968 Jul;96(1):215–220. doi: 10.1128/jb.96.1.215-220.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Birge E. A., Low K. B. Detection of transcribable recombination products following conjugation in rec+, reCB- and recC-strains of Escherichia coli K12. J Mol Biol. 1974 Mar 15;83(4):447–457. doi: 10.1016/0022-2836(74)90506-3. [DOI] [PubMed] [Google Scholar]
  4. Chan R. K., Botstein D., Watanabe T., Ogata Y. Specialized transduction of tetracycline resistance by phage P22 in Salmonella typhimurium. II. Properties of a high-frequency-transducing lysate. Virology. 1972 Dec;50(3):883–898. doi: 10.1016/0042-6822(72)90442-4. [DOI] [PubMed] [Google Scholar]
  5. Chumley F. G., Menzel R., Roth J. R. Hfr formation directed by tn10. Genetics. 1979 Apr;91(4):639–655. doi: 10.1093/genetics/91.4.639. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Clark A. J. Recombination deficient mutants of E. coli and other bacteria. Annu Rev Genet. 1973;7:67–86. doi: 10.1146/annurev.ge.07.120173.000435. [DOI] [PubMed] [Google Scholar]
  7. Demerec M., Adelberg E. A., Clark A. J., Hartman P. E. A proposal for a uniform nomenclature in bacterial genetics. Genetics. 1966 Jul;54(1):61–76. doi: 10.1093/genetics/54.1.61. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dower N. A., Stahl F. W. Chi activity during transduction-associated recombination. Proc Natl Acad Sci U S A. 1981 Nov;78(11):7033–7037. doi: 10.1073/pnas.78.11.7033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Eisenstark A., Eisenstark R., van Dillewijn J., Rörsch A. Radiation--sensitive and recombinationless mutants of Salmonella typhimurium. Mutat Res. 1969 Nov-Dec;8(3):497–504. doi: 10.1016/0027-5107(69)90066-9. [DOI] [PubMed] [Google Scholar]
  10. Goldmark P. J., Linn S. Purification and properties of the recBC DNase of Escherichia coli K-12. J Biol Chem. 1972 Mar 25;247(6):1849–1860. [PubMed] [Google Scholar]
  11. James A. A., Morrison P. T., Kolodner R. Genetic recombination of bacterial plasmid DNA. Analysis of the effect of recombination-deficient mutations on plasmid recombination. J Mol Biol. 1982 Sep 25;160(3):411–430. doi: 10.1016/0022-2836(82)90305-9. [DOI] [PubMed] [Google Scholar]
  12. Karu A. E., MacKay V., Goldmark P. J., Linn S. The recBC deoxyribonuclease of Escherichia coli K-12. Substrate specificity and reaction intermediates. J Biol Chem. 1973 Jul 25;248(14):4874–4884. [PubMed] [Google Scholar]
  13. Kobayashi I., Stahl M. M., Fairfield F. R., Stahl F. W. Coupling with packaging explains apparent nonreciprocality of Chi-stimulated recombination of bacteriophage lambda by RecA and RecBC functions. Genetics. 1984 Dec;108(4):773–794. doi: 10.1093/genetics/108.4.773. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kobayashi I., Stahl M. M., Leach D., Stahl F. W. The interaction of cos with Chi is separable from DNA packaging in recA-recBC-mediated recombination of bacteriophage lambda. Genetics. 1983 Aug;104(4):549–570. doi: 10.1093/genetics/104.4.549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kobayashi I., Stahl M. M., Stahl F. W. The mechanism of the chi-cos interaction in RecA-RecBC-mediated recombination in phage lambda. Cold Spring Harb Symp Quant Biol. 1984;49:497–506. doi: 10.1101/sqb.1984.049.01.056. [DOI] [PubMed] [Google Scholar]
  16. Laban A., Cohen A. Interplasmidic and intraplasmidic recombination in Escherichia coli K-12. Mol Gen Genet. 1981;184(2):200–207. doi: 10.1007/BF00272905. [DOI] [PubMed] [Google Scholar]
  17. Lloyd R. G., Evans N. P., Buckman C. Formation of recombinant lacZ+ DNA in conjugational crosses with a recB mutant of Escherichia coli K12 depends on recF, recJ, and recO. Mol Gen Genet. 1987 Aug;209(1):135–141. doi: 10.1007/BF00329848. [DOI] [PubMed] [Google Scholar]
  18. Lloyd R. G., Thomas A. A molecular model for conjugational recombination in Escherichia coli K12. Mol Gen Genet. 1984;197(2):328–336. doi: 10.1007/BF00330981. [DOI] [PubMed] [Google Scholar]
  19. Mahan M. J., Roth J. R. Reciprocality of recombination events that rearrange the chromosome. Genetics. 1988 Sep;120(1):23–35. doi: 10.1093/genetics/120.1.23. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Mahan M. J., Roth J. R. recB and recC genes of Salmonella typhimurium. J Bacteriol. 1989 Jan;171(1):612–615. doi: 10.1128/jb.171.1.612-615.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Muskavitch K. M., Linn S. A unified mechanism for the nuclease and unwinding activities of the recBC enzyme of Escherichia coli. J Biol Chem. 1982 Mar 10;257(5):2641–2648. [PubMed] [Google Scholar]
  22. Orr-Weaver T. L., Szostak J. W. Fungal recombination. Microbiol Rev. 1985 Mar;49(1):33–58. doi: 10.1128/mr.49.1.33-58.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Ponticelli A. S., Schultz D. W., Taylor A. F., Smith G. R. Chi-dependent DNA strand cleavage by RecBC enzyme. Cell. 1985 May;41(1):145–151. doi: 10.1016/0092-8674(85)90069-8. [DOI] [PubMed] [Google Scholar]
  24. Sanderson K. E., Roth J. R. Linkage map of Salmonella typhimurium, Edition VI. Microbiol Rev. 1983 Sep;47(3):410–453. doi: 10.1128/mr.47.3.410-453.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Sandri R. M., Berger H. Bacteriophage P1-mediated generalized transduction in Escherichia coli: fate of transduced DNA in rec+ and recA- recipients. Virology. 1980 Oct 15;106(1):14–29. doi: 10.1016/0042-6822(80)90217-2. [DOI] [PubMed] [Google Scholar]
  26. Schmid M., Roth J. R. Circularization of transduced fragments: a mechanism for adding segments to the bacterial chromosome. Genetics. 1980 Jan;94(1):15–29. doi: 10.1093/genetics/94.1.15. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Schmieger H. Phage P22-mutants with increased or decreased transduction abilities. Mol Gen Genet. 1972;119(1):75–88. doi: 10.1007/BF00270447. [DOI] [PubMed] [Google Scholar]
  28. Sclafani R. A., Wechsler J. A. High frequency of genetic duplications in the dnaB region of the Escherichia coli K12 chromosome. Genetics. 1981 Aug;98(4):677–689. doi: 10.1093/genetics/98.4.677. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Smith G. R., Amundsen S. K., Chaudhury A. M., Cheng K. C., Ponticelli A. S., Roberts C. M., Schultz D. W., Taylor A. F. Roles of RecBC enzyme and chi sites in homologous recombination. Cold Spring Harb Symp Quant Biol. 1984;49:485–495. doi: 10.1101/sqb.1984.049.01.055. [DOI] [PubMed] [Google Scholar]
  30. 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]
  31. 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]
  32. Stahl M. M., Kobayashi I., Stahl F. W., Huntington S. K. Activation of Chi, a recombinator, by the action of an endonuclease at a distant site. Proc Natl Acad Sci U S A. 1983 Apr;80(8):2310–2313. doi: 10.1073/pnas.80.8.2310. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Taylor A. F., Schultz D. W., Ponticelli A. S., Smith G. R. RecBC enzyme nicking at Chi sites during DNA unwinding: location and orientation-dependence of the cutting. Cell. 1985 May;41(1):153–163. doi: 10.1016/0092-8674(85)90070-4. [DOI] [PubMed] [Google Scholar]
  34. Winans S. C., Elledge S. J., Krueger J. H., Walker G. C. Site-directed insertion and deletion mutagenesis with cloned fragments in Escherichia coli. J Bacteriol. 1985 Mar;161(3):1219–1221. doi: 10.1128/jb.161.3.1219-1221.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES