Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1986 Jun;83(11):3885–3889. doi: 10.1073/pnas.83.11.3885

A phage P1 function that stimulates homologous recombination of the Escherichia coli chromosome.

B E Windle, J B Hays
PMCID: PMC323629  PMID: 3012538

Abstract

Recombination between two different defective lacZ genes in the Escherichia coli chromosome (lac- X lac- recombination) was stimulated 2- to 8-fold by prophage P1, depending on the nature of the phage c1 repressor. The P1 BamHI restriction fragment B8 in a lambda-P1:B8 hybrid phage, stimulated lac- X lac- recombination 90-fold in the absence of P1 repressor. A gene necessary for recombination enhancement, designated ref, was localized to one end of B8. Ref expression from lambda-P1:B8 was repressed in trans by a P1 c+ prophage. Two P1 regulatory mutations, bof and lxc, derepressed prophage expression of ref and depressed a prophage function that complemented an E. coli mutant (ssb) deficient in the single-stranded DNA binding protein. Ref stimulation was dependent on preexisting E. coli recombination functions (RecA-RecBC and RecA-RecF). However, other (phage and plasmid) recombination processes involving these functions were not stimulated. ref::Tn5 phages plated and formed lysogens normally. Thus ref appears to be an integral, but not essential, phage gene that stimulates recombination of the host chromosome specifically.

Full text

PDF
3885

Selected References

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

  1. Becker A., Gold M. Isolation of the bacteriophage lambda A-gene protein. Proc Natl Acad Sci U S A. 1975 Feb;72(2):581–585. doi: 10.1073/pnas.72.2.581. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bächi B., Arber W. Physical mapping of BglII, BamHI, EcoRI, HindIII and PstI restriction fragments of bacteriophage P1 DNA. Mol Gen Genet. 1977 Jun 24;153(3):311–324. doi: 10.1007/BF00431596. [DOI] [PubMed] [Google Scholar]
  3. Chesney R. H., Scott J. R., Vapnek D. Integration of the plasmid prophages P1 and P7 into the chromosome of Escherichia coli. J Mol Biol. 1979 May 15;130(2):161–173. doi: 10.1016/0022-2836(79)90424-8. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. D'Ari R., Jaffé-Brachet A., Touati-Schwartz D., Yarmolinsky M. B. A dnaB analog specified by bacteriophage P1. J Mol Biol. 1975 May 25;94(3):341–366. doi: 10.1016/0022-2836(75)90207-7. [DOI] [PubMed] [Google Scholar]
  6. Enquist L. W., Weisberg R. A. The red plaque test: a rapid method for identification of excision defective variants of bacteriophage lambda. Virology. 1976 Jul 1;72(1):147–153. doi: 10.1016/0042-6822(76)90319-6. [DOI] [PubMed] [Google Scholar]
  7. Hays J. B., Korba B. E., Konrad E. B. Novel mutations of Escherichia coli that produce recombinogenic lesions in DNA. I. Identification and mapping of arl mutations. J Mol Biol. 1980 May 25;139(3):455–472. doi: 10.1016/0022-2836(80)90141-2. [DOI] [PubMed] [Google Scholar]
  8. Hays J. B., Smith T. A., Friedman S. A., Lee E., Coffman G. L. RecF and RecBC function during recombination of nonreplicating, UV-irradiated phage lambda DNA and during other recombination processes. Cold Spring Harb Symp Quant Biol. 1984;49:475–483. doi: 10.1101/sqb.1984.049.01.054. [DOI] [PubMed] [Google Scholar]
  9. Horii Z., Clark A. J. Genetic analysis of the recF pathway to genetic recombination in Escherichia coli K12: isolation and characterization of mutants. J Mol Biol. 1973 Oct 25;80(2):327–344. doi: 10.1016/0022-2836(73)90176-9. [DOI] [PubMed] [Google Scholar]
  10. Iida S., Arber W. Plaque forming specialized transducing phage P1: isolation of P1CmSmSu, a precursor of P1Cm. Mol Gen Genet. 1977 Jun 24;153(3):259–269. doi: 10.1007/BF00431591. [DOI] [PubMed] [Google Scholar]
  11. Iida S., Meyer J., Arber W. The insertion element IS1 is a natural constituent of coliphage P1 DNA. Plasmid. 1978 Jun;1(3):357–365. doi: 10.1016/0147-619x(78)90051-3. [DOI] [PubMed] [Google Scholar]
  12. Johnson B. F. Suppression of the lexC (ssbA) mutation of Escherichia coli by a mutant of bacteriophage P1. Mol Gen Genet. 1982;186(1):122–126. doi: 10.1007/BF00422923. [DOI] [PubMed] [Google Scholar]
  13. Jorgensen R. A., Rothstein S. J., Reznikoff W. S. A restriction enzyme cleavage map of Tn5 and location of a region encoding neomycin resistance. Mol Gen Genet. 1979;177(1):65–72. doi: 10.1007/BF00267254. [DOI] [PubMed] [Google Scholar]
  14. KONDO E., MITSUHASHI S. DRUG RESISTANCE OF ENTERIC BACTERIA. IV. ACTIVE TRANSDUCING BACTERIOPHAGE P1 CM PRODUCED BY THE COMBINATION OF R FACTOR WITH BACTERIOPHAGE P1. J Bacteriol. 1964 Nov;88:1266–1276. doi: 10.1128/jb.88.5.1266-1276.1964. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Konrad E. B., Lehman I. R. A conditional lethal mutant of Escherichia coli K12 defective in the 5' leads to 3' exonuclease associated with DNA polymerase I. Proc Natl Acad Sci U S A. 1974 May;71(5):2048–2051. doi: 10.1073/pnas.71.5.2048. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Konrad E. B. Method for the isolation of Escherichia coli mutants with enhanced recombination between chromosomal duplications. J Bacteriol. 1977 Apr;130(1):167–172. doi: 10.1128/jb.130.1.167-172.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Konrad E. B., Modrich P., Lehman I. R. Genetic and enzymatic characterization of a conditional lethal mutant of Escherichia coli K12 with a temperature-sensitive DNA ligase. J Mol Biol. 1973 Jul 15;77(4):519–529. doi: 10.1016/0022-2836(73)90220-9. [DOI] [PubMed] [Google Scholar]
  18. Lundblad V., Taylor A. F., Smith G. R., Kleckner N. Unusual alleles of recB and recC stimulate excision of inverted repeat transposons Tn10 and Tn5. Proc Natl Acad Sci U S A. 1984 Feb;81(3):824–828. doi: 10.1073/pnas.81.3.824. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Meyer J., Iida S., Arber W. Physical analysis of the genomes of hybrid phages between phage P1 and plasmid p15B. J Mol Biol. 1983 Mar 25;165(1):191–195. doi: 10.1016/s0022-2836(83)80250-2. [DOI] [PubMed] [Google Scholar]
  20. Mizusawa S., Ward D. F. A bacteriophage lambda vector for cloning with BamHI and Sau3A. Gene. 1982 Dec;20(3):317–322. doi: 10.1016/0378-1119(82)90200-1. [DOI] [PubMed] [Google Scholar]
  21. Mural R. J., Chesney R. H., Vapnek D., Kropf M. M., Scott J. R. Isolation and characterization of cloned fragments of bacteriophage P1 DNA. Virology. 1979 Mar;93(2):387–397. doi: 10.1016/0042-6822(79)90243-5. [DOI] [PubMed] [Google Scholar]
  22. Oliver D. B., Goldberg E. B. Protection of parental T4 DNA from a restriction exonuclease by the product of gene 2. J Mol Biol. 1977 Nov;116(4):877–881. doi: 10.1016/0022-2836(77)90276-5. [DOI] [PubMed] [Google Scholar]
  23. Rae M. E., Stodolsky M. Chromosome breakage, fusion and reconstruction during P1dl transduction. Virology. 1974 Mar;58(1):32–54. doi: 10.1016/0042-6822(74)90139-1. [DOI] [PubMed] [Google Scholar]
  24. Rosner J. L. Formation, induction, and curing of bacteriophage P1 lysogens. Virology. 1972 Jun;48(3):679–689. doi: 10.1016/0042-6822(72)90152-3. [DOI] [PubMed] [Google Scholar]
  25. Sakaki Y. Inactivation of the ATP-dependent DNase of Escherichia coli after infection with double-stranded DNA phages. J Virol. 1974 Dec;14(6):1611–1612. doi: 10.1128/jvi.14.6.1611-1612.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Schultz D. W., Taylor A. F., Smith G. R. Escherichia coli RecBC pseudorevertants lacking chi recombinational hotspot activity. J Bacteriol. 1983 Aug;155(2):664–680. doi: 10.1128/jb.155.2.664-680.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Shapiro J. A., Brinkley P. M. Programming of DNA rearrangements involving mu prophages. Cold Spring Harb Symp Quant Biol. 1984;49:313–320. doi: 10.1101/sqb.1984.049.01.037. [DOI] [PubMed] [Google Scholar]
  28. Smith T. A., Hays J. B. Repair and recombination of nonreplicating UV-irradiated phage DNA in E. coli II. Stimulation of RecF-dependent recombination by excision repair of cyclobutane pyrimidine dimers and of other photoproducts. Mol Gen Genet. 1985;201(3):393–401. doi: 10.1007/BF00331329. [DOI] [PubMed] [Google Scholar]
  29. Stahl F. W., Stahl M. M. Recombination pathway specificity of Chi. Genetics. 1977 Aug;86(4):715–725. doi: 10.1093/genetics/86.4.715. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Sternberg N., Hoess R. The molecular genetics of bacteriophage P1. Annu Rev Genet. 1983;17:123–154. doi: 10.1146/annurev.ge.17.120183.001011. [DOI] [PubMed] [Google Scholar]
  31. Sternberg N., Sauer B., Hoess R., Abremski K. Bacteriophage P1 cre gene and its regulatory region. Evidence for multiple promoters and for regulation by DNA methylation. J Mol Biol. 1986 Jan 20;187(2):197–212. doi: 10.1016/0022-2836(86)90228-7. [DOI] [PubMed] [Google Scholar]
  32. Touati-Schwartz D. A new pleiotropic bacteriophage P1 mutation, bof, affecting c1 repression activity, the expression of plasmid incompatibility and the expression of certain constitutive prophage genes. Mol Gen Genet. 1979 Jul 13;174(2):189–202. doi: 10.1007/BF00268355. [DOI] [PubMed] [Google Scholar]
  33. Unger R. C., Echols H., Clark A. J. Interaction of the recombination pathways of bacteriophage lambda and host Escherichia coli: effects on lambda recombination. J Mol Biol. 1972 Oct 14;70(3):531–537. doi: 10.1016/0022-2836(72)90557-8. [DOI] [PubMed] [Google Scholar]
  34. Yun T., Vapnek D. Electron microscopic analysis of bacteriophages P1, P1Cm, and P7. Determination of genome sizes, sequence homology, and location of antibiotic-resistance determinants. Virology. 1977 Mar;77(1):376–385. doi: 10.1016/0042-6822(77)90434-2. [DOI] [PubMed] [Google Scholar]
  35. Zieg J., Kushner S. R. Analysis of genetic recombination between two partially deleted lactose operons of Escherichia coli K-12. J Bacteriol. 1977 Jul;131(1):123–132. doi: 10.1128/jb.131.1.123-132.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Zieg J., Maples V. F., Kushner S. R. Recombinant levels of Escherichia coli K-12 mutants deficient in various replication, recombination, or repair genes. J Bacteriol. 1978 Jun;134(3):958–966. doi: 10.1128/jb.134.3.958-966.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES