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. 1976 Sep;19(3):915–924. doi: 10.1128/jvi.19.3.915-924.1976

Bacteriophage G4 DNA synthesis in temperature-sensitive dna mutants of Escherichia coli.

P L Derstine, L B Dumas, C A Miller
PMCID: PMC354932  PMID: 787559

Abstract

The synthesis of bacteriophage G4 DNA was examined in temperature-sensitive dna mutants under permissive and nonpermissive conditions. The infecting single-stranded G4 DNA was converted to the parental replicative form (RF) at the nonpermissive temperature in infected cells containing a temperature sensitive mutation in the dnaA, dnaB, dnaC, dnaE, or dnaG gene. The presence of 30 mug of chloramphenicol or 200 mug of rifampin per ml had no effect on parental RF synthesis in these mutants. Replication of G4 double-stranded RF DNA occurred at a normal rate in dnaAts cells at the nonpermissive temperature, but the rate was greatly reduced in cells containing a temperature-sensitive mutation in the dnaB, dnaC, dnaE, or dnaG gene. RF DNA replicated at normal rates in revertants of these dna temperature-sensitive host cells. The simplest interpretation of these observations is that none of the dna gene products tested is essential for the synthesis of the complementary DNA strand on the infecting single-stranded G4 DNA, whereas the dnaB, dnaC, dnaE, (DNA polymerase III), and dnaG gene products are all essential for replication of the double-stranded G4 RF DNA. The alternate possibility that one or more of the gene products are actually essential for G4 parental RF synthesis, even though this synthesis is not defective in the mutant hosts, is also discussed.

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Selected References

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

  1. Blau S., Mordoh J. A new element in the control of DNA initiation in Escherichia coli. Proc Natl Acad Sci U S A. 1972 Oct;69(10):2895–2898. doi: 10.1073/pnas.69.10.2895. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bouché J. P., Zechel K., Kornberg A. dnaG gene product, a rifampicin-resistant RNA polymerase, initiates the conversion of a single-stranded coliphage DNA to its duplex replicative form. J Biol Chem. 1975 Aug 10;250(15):5995–6001. [PubMed] [Google Scholar]
  3. Bowden D. W., Twersky R. S., Calendar R. Escherichia coli deoxyribonucleic acid synthesis mutants: their effect upon bacteriophage P2 and satellite bacteriophage P4 deoxyribonucleic acid synthesis. J Bacteriol. 1975 Oct;124(1):167–175. doi: 10.1128/jb.124.1.167-175.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brutlag D., Schekman R., Kornberg A. A possible role for RNA polymerase in the initiation of M13 DNA synthesis. Proc Natl Acad Sci U S A. 1971 Nov;68(11):2826–2829. doi: 10.1073/pnas.68.11.2826. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Burton A., Sinsheimer R. L. The process of infection with bacteriophage phi-X174 VII. Ultracentrifugal analysis of the replicative form. J Mol Biol. 1965 Dec;14(2):327–347. doi: 10.1016/s0022-2836(65)80185-1. [DOI] [PubMed] [Google Scholar]
  6. Carl P. L. Escherichia coli mutants with temperature-sensitive synthesis of DNA. Mol Gen Genet. 1970;109(2):107–122. doi: 10.1007/BF00269647. [DOI] [PubMed] [Google Scholar]
  7. Denhardt D. T., Sinsheimer R. L. The process of infection with bacteriophage phi-X174. 3. Phage maturation and lysis after synchronized infection. J Mol Biol. 1965 Jul;12(3):641–646. doi: 10.1016/s0022-2836(65)80318-7. [DOI] [PubMed] [Google Scholar]
  8. Dumas L. B., Darby G., Sinsheimer R. L. The replication of bacteriophage phi X174 DNA in vitro. Temperature effects on repair synthesis and displacement synthesis. Biochim Biophys Acta. 1971 Jan 28;228(2):407–422. [PubMed] [Google Scholar]
  9. Dumas L. B., Miller C. A. Bacteriophage phiX174 single-stranded viral DNA synthesis in temperature-sensitive dnaB and dna C mutants of Escherichia coli. J Virol. 1976 May;18(2):426–435. doi: 10.1128/jvi.18.2.426-435.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dumas L. B., Miller C. A., Bayne M. L. Rifampin inhibition of bacteriophage phiX174 parental replicative-form DNA synthesis in an Escherichia coli dnaC mutant. J Virol. 1975 Sep;16(3):575–580. doi: 10.1128/jvi.16.3.575-580.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dumas L. B., Miller C. A. Inhibition of bacteriophage phi chi 174 DNA replication in dnaB mutants of Escherichia coli C. J Virol. 1974 Dec;14(6):1369–1379. doi: 10.1128/jvi.14.6.1369-1379.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dumas L. B., Miller C. A. Replication of bacteriophage phiX174 DNA in a temperature-sensitive dnaE mutant of Escherichia coli C. J Virol. 1973 Jun;11(6):848–855. doi: 10.1128/jvi.11.6.848-855.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Francke B., Ray D. S. Formation of the parental replicative form DNA of bacteriophage phi-X174 and initial events in its replication. J Mol Biol. 1971 Nov 14;61(3):565–586. doi: 10.1016/0022-2836(71)90065-9. [DOI] [PubMed] [Google Scholar]
  14. Gefter M. L., Hirota Y., Kornberg T., Wechsler J. A., Barnoux C. Analysis of DNA polymerases II and 3 in mutants of Escherichia coli thermosensitive for DNA synthesis. Proc Natl Acad Sci U S A. 1971 Dec;68(12):3150–3153. doi: 10.1073/pnas.68.12.3150. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Geider K., Kornberg A. Conversion of the M13 viral single strand to the double-stranded replicative forms by purified proteins. J Biol Chem. 1974 Jul 10;249(13):3999–4005. [PubMed] [Google Scholar]
  16. Godson G. N. Evolution of phi chi 174. II. A cleavage map of the G4 phage genome and comparison with the cleavage map of phi chi 174. Virology. 1975 Feb;63(2):320–325. doi: 10.1016/0042-6822(75)90306-2. [DOI] [PubMed] [Google Scholar]
  17. Godson G. N. Evolution of phi-chi 174. Isolation of four new phi-chi-like phages and comparison with phi-chi 174. Virology. 1974 Mar;58(1):272–289. doi: 10.1016/0042-6822(74)90161-5. [DOI] [PubMed] [Google Scholar]
  18. Hirota Y., Mordoh J., Jacob F. On the process of cellular division in Escherichia coli. 3. Thermosensitive mutants of Escherichia coli altered in the process of DNA initiation. J Mol Biol. 1970 Nov 14;53(3):369–387. doi: 10.1016/0022-2836(70)90072-0. [DOI] [PubMed] [Google Scholar]
  19. Hirota Y., Ryter A., Jacob F. Thermosensitive mutants of E. coli affected in the processes of DNA synthesis and cellular division. Cold Spring Harb Symp Quant Biol. 1968;33:677–693. doi: 10.1101/sqb.1968.033.01.077. [DOI] [PubMed] [Google Scholar]
  20. Kranias E. G., Dumas L. B. Replication of bacteriophage phiX174 DNA in a temperature-sensitive dnaC mutant of escherichia coli C. J Virol. 1974 Jan;13(1):146–154. doi: 10.1128/jvi.13.1.146-154.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kranias E. G., Dumas L. B. Synthesis of complex forms of bacteriophage phiX174 double-stranded DNA in a temperature-sensitive dnaC mutant of Escherichia coli C. J Virol. 1975 Aug;16(2):412–419. doi: 10.1128/jvi.16.2.412-419.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lark K. G. Genetic control over the initiation of the synthesis of the short deoxynucleotide chains in E. coli. Nat New Biol. 1972 Dec 20;240(103):237–240. doi: 10.1038/newbio240237a0. [DOI] [PubMed] [Google Scholar]
  23. McFadden G., Denhardt D. T. Mechanism of replication of phi x174 single-stranded DNA. IX. Requirement for the Escherichia coli dnaG protein. J Virol. 1974 Nov;14(5):1070–1075. doi: 10.1128/jvi.14.5.1070-1075.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Mitra S., Stallions D. R. Role of dna genes of Escherichia coli in M13 phage replication. Virology. 1973 Apr;52(2):417–424. doi: 10.1016/0042-6822(73)90336-x. [DOI] [PubMed] [Google Scholar]
  25. Nüsslein V., Otto B., Bonhoeffer F., Schaller H. Function of DNA polymerase 3 in DNA replication. Nat New Biol. 1971 Dec 29;234(52):285–286. doi: 10.1038/newbio234285a0. [DOI] [PubMed] [Google Scholar]
  26. Olsen W. L., Staudenbauer W. L., Hofschneider P. H. Replication of bacteriophage M13: specificity of the Escherichia coli dnaB function for replication of double-stranded M13 DNA. Proc Natl Acad Sci U S A. 1972 Sep;69(9):2570–2573. doi: 10.1073/pnas.69.9.2570. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Ray D. S., Dueber J., Suggs S. Replication of bacteriophage M13 IX. Requirement of the Escherichia coli dnaG function for M13 duplex DNA replication. J Virol. 1975 Aug;16(2):348–355. doi: 10.1128/jvi.16.2.348-355.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. SINSHEIMER R. L., STARMAN B., NAGLER C., GUTHRIE S. The process of infection with bacteriophage phi-XI74. I. Evidence for a "replicative form". J Mol Biol. 1962 Mar;4:142–160. doi: 10.1016/s0022-2836(62)80047-3. [DOI] [PubMed] [Google Scholar]
  29. Schekman R., Weiner J. H., Weiner A., Kornberg A. Ten proteins required for conversion of phiX174 single-stranded DNA to duplex form in vitro. Resolution and reconstitution. J Biol Chem. 1975 Aug 10;250(15):5859–5865. [PubMed] [Google Scholar]
  30. Schubach W. H., Whitmer J. D., Davern C. I. Genetic control of DNA initiation in Escherichia coli. J Mol Biol. 1973 Feb 25;74(2):205–221. doi: 10.1016/0022-2836(73)90107-1. [DOI] [PubMed] [Google Scholar]
  31. Steinberg R. A., Denhardt D. T. Inhibition of synthesis of phiX174 DNA in a mutant host thermosensitive for DNA synthesis. J Mol Biol. 1968 Nov 14;37(3):525–528. doi: 10.1016/0022-2836(68)90120-4. [DOI] [PubMed] [Google Scholar]
  32. Truffaut N., Manheimer I. Development of bacteriophage Ha2, a phiX174 derivative, in Escherichia coli strains carrying a thermosensitive mutation in the dnaG gene. Biochimie. 1975;57(8):905–915. doi: 10.1016/s0300-9084(75)80213-6. [DOI] [PubMed] [Google Scholar]
  33. Wechsler J. A., Gross J. D. Escherichia coli mutants temperature-sensitive for DNA synthesis. Mol Gen Genet. 1971;113(3):273–284. doi: 10.1007/BF00339547. [DOI] [PubMed] [Google Scholar]
  34. Wehrli W., Nüesch J., Knüsel F., Staehelin M. Action of rifamycins on RNA polymerase. Biochim Biophys Acta. 1968 Mar 18;157(1):215–217. doi: 10.1016/0005-2787(68)90285-2. [DOI] [PubMed] [Google Scholar]
  35. Wickner R. B., Wright M., Wickner S., Hurwitz J. Conversion of phiX174 and fd single-stranded DNA to replicative forms in extracts of Escherichia coli. Proc Natl Acad Sci U S A. 1972 Nov;69(11):3233–3237. doi: 10.1073/pnas.69.11.3233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Wickner S., Wright M., Hurwitz J. Association of DNA-dependent and -independent ribonucleoside triphosphatase activities with dnaB gene product of Escherichia coli. Proc Natl Acad Sci U S A. 1974 Mar;71(3):783–787. doi: 10.1073/pnas.71.3.783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Zechel K., Bouché J. P., Kornberg A. Replication of phage G4. A novel and simple system for the initiation of deoxyribonucleic acid synthesis. J Biol Chem. 1975 Jun 25;250(12):4684–4689. [PubMed] [Google Scholar]

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