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. 1992 Aug;131(4):769–781. doi: 10.1093/genetics/131.4.769

Genetic Recombination in Bacteriophage T4: Single-Burst Analysis of Cosegregants and Evidence in Favor of a Splice/Patch Coupling Model

V P Shcherbakov 1, L A Plugina 1, M A Nesheva 1
PMCID: PMC1205090  PMID: 1516814

Abstract

To reveal the structure of penultimate DNA intermediates in T4 bacteriophage recombination, resolution of which produces free recombinant molecules, a single-burst analysis of the recombinant progeny was made in multifactor crosses, enabling one to determine quantitatively the different recombinants generated by one or two exchanges within the same chromosome segment. It was found that double and single exchanges are highly correlated in T4 recombination. These results were interpreted as evidence for simultaneous formation of a splice/patch pair as the primary recombination products. A recombination model called here the ``splice/patch coupling model'' is presented according to which resolution of a single DNA intermediate results in two linear heterozygous molecules containing a patch and a splice, respectively, in homologous positions.

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Selected References

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  1. Berger H. Genetic analysis of T4D phage heterozygotes produced in the presence of 5-fluorodeoxyuridine. Genetics. 1965 Oct;52(4):729–746. doi: 10.1093/genetics/52.4.729. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Campbell D. A. Analysis of multiplicty reactivation in x-irradiated bacteriophage T4D. Virology. 1971 Apr;44(1):188–199. doi: 10.1016/0042-6822(71)90164-4. [DOI] [PubMed] [Google Scholar]
  3. Curtis M. J., Alberts B. Studies on the structure of intracellular bacteriophage T4 DNA. J Mol Biol. 1976 Apr 25;102(4):793–816. doi: 10.1016/0022-2836(76)90292-8. [DOI] [PubMed] [Google Scholar]
  4. DOERMANN A. H., BOEHNER L. AN EXPERIMENTAL ANALYSIS OF BACTERIOPHAGE T4 HETEROZYGOTES. I. MOTTLED PLAQUES FROM CROSSES INVOLVING SIX RII LOCI. Virology. 1963 Dec;21:551–567. doi: 10.1016/0042-6822(63)90227-7. [DOI] [PubMed] [Google Scholar]
  5. Dannenberg R., Mosig G. Early intermediates in bacteriophage T4 DNA replication and recombination. J Virol. 1983 Feb;45(2):813–831. doi: 10.1128/jvi.45.2.813-831.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Doermann A. H., Parma D. H. Recombination in bacteriophage T4. J Cell Physiol. 1967 Oct;70(2 Suppl):147–164. doi: 10.1002/jcp.1040700411. [DOI] [PubMed] [Google Scholar]
  7. Doermann A. H. T4 and the rolling circle model of replication. Annu Rev Genet. 1973;7:325–341. doi: 10.1146/annurev.ge.07.120173.001545. [DOI] [PubMed] [Google Scholar]
  8. EPSTEIN R. H. A study of multiplicity-reactivation in the bacteriophage T4. I. Genetic and functional analysis of T4D-K12(lambda) complexes. Virology. 1958 Oct;6(2):382–404. doi: 10.1016/0042-6822(58)90090-4. [DOI] [PubMed] [Google Scholar]
  9. Ebisuzaki K., Campbell L. On the role of ligase in genetic recombination in bacteriophage T4. Virology. 1969 Aug;38(4):701–703. doi: 10.1016/0042-6822(69)90190-1. [DOI] [PubMed] [Google Scholar]
  10. Englund P. T. The initial step of in vitro synthesis of deoxyribonucleic acid by the T4 deoxyribonucleic acid polymerase. J Biol Chem. 1971 Sep 25;246(18):5684–5687. [PubMed] [Google Scholar]
  11. Formosa T., Alberts B. M. DNA synthesis dependent on genetic recombination: characterization of a reaction catalyzed by purified bacteriophage T4 proteins. Cell. 1986 Dec 5;47(5):793–806. doi: 10.1016/0092-8674(86)90522-2. [DOI] [PubMed] [Google Scholar]
  12. Formosa T., Alberts B. M. Purification and characterization of the T4 bacteriophage uvsX protein. J Biol Chem. 1986 May 5;261(13):6107–6118. [PubMed] [Google Scholar]
  13. Fry S. E. Stimulation of recombination in phage T4 by nitrous acid-induced lesions. J Gen Virol. 1979 Jun;43(3):719–722. doi: 10.1099/0022-1317-43-3-719. [DOI] [PubMed] [Google Scholar]
  14. GAREN A. Physiological effects of rII mutations in bacteriophage T4. Virology. 1961 Jun;14:151–163. doi: 10.1016/0042-6822(61)90190-8. [DOI] [PubMed] [Google Scholar]
  15. Griffith J., Formosa T. The uvsX protein of bacteriophage T4 arranges single-stranded and double-stranded DNA into similar helical nucleoprotein filaments. J Biol Chem. 1985 Apr 10;260(7):4484–4491. [PubMed] [Google Scholar]
  16. Hamilton S., Pettijohn D. E. Properties of condensed bacteriophage T4 DNA isolated from Escherichia coli infected with bacteriophage T4. J Virol. 1976 Sep;19(3):1012–1027. doi: 10.1128/jvi.19.3.1012-1027.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Harris L. D., Griffith J. Visualization of the homologous pairing of DNA catalyzed by the bacteriophage T4 UvsX protein. J Biol Chem. 1987 Jul 5;262(19):9285–9292. [PubMed] [Google Scholar]
  18. Hershey A. D., Rotman R. Genetic Recombination between Host-Range and Plaque-Type Mutants of Bacteriophage in Single Bacterial Cells. Genetics. 1949 Jan;34(1):44–71. doi: 10.1093/genetics/34.1.44. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hinton D. M., Nossal N. G. Cloning of the bacteriophage T4 uvsX gene and purification and characterization of the T4 uvsX recombination protein. J Biol Chem. 1986 Apr 25;261(12):5663–5673. [PubMed] [Google Scholar]
  20. Jensch F., Kemper B. Endonuclease VII resolves Y-junctions in branched DNA in vitro. EMBO J. 1986 Jan;5(1):181–189. doi: 10.1002/j.1460-2075.1986.tb04194.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kemper B., Janz E. Function of gene 49 of bacteriophage T4. I. Isolation and biochemical characterization of very fast-sedimenting DNA. J Virol. 1976 Jun;18(3):992–999. doi: 10.1128/jvi.18.3.992-999.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kodadek T., Wong M. L. Homologous pairing in vitro initiated by DNA synthesis. Biochem Biophys Res Commun. 1990 May 31;169(1):302–309. doi: 10.1016/0006-291x(90)91468-8. [DOI] [PubMed] [Google Scholar]
  23. Kozinski A. W., Kosturko L. D. Late events in T4 bacteriophage production. II. Giant bacteriophages contain concatemers generated by recombination. J Virol. 1976 Mar;17(3):801–804. doi: 10.1128/jvi.17.3.801-804.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Krisch H. M., Shah D. B., Berger H. Replication and recombination in ligase-deficient rII bacteriophage T4D. J Virol. 1971 Apr;7(4):491–498. doi: 10.1128/jvi.7.4.491-498.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Luder A., Mosig G. Two alternative mechanisms for initiation of DNA replication forks in bacteriophage T4: priming by RNA polymerase and by recombination. Proc Natl Acad Sci U S A. 1982 Feb;79(4):1101–1105. doi: 10.1073/pnas.79.4.1101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Meselson M. S., Radding C. M. A general model for genetic recombination. Proc Natl Acad Sci U S A. 1975 Jan;72(1):358–361. doi: 10.1073/pnas.72.1.358. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Minagawa T., Murakami A., Ryo Y., Yamagishi H. Structural features of very fast sedimenting DNA formed by gene 49 defective T4. Virology. 1983 Apr 15;126(1):183–193. doi: 10.1016/0042-6822(83)90470-1. [DOI] [PubMed] [Google Scholar]
  28. Mizuuchi K., Kemper B., Hays J., Weisberg R. A. T4 endonuclease VII cleaves holliday structures. Cell. 1982 Jun;29(2):357–365. doi: 10.1016/0092-8674(82)90152-0. [DOI] [PubMed] [Google Scholar]
  29. Mosig G., Ehring R., Schliewen W., Bock S. The patterns of recombination and segregation in terminal regions of T4DNA molecules. Mol Gen Genet. 1971;113(1):51–91. doi: 10.1007/BF00335007. [DOI] [PubMed] [Google Scholar]
  30. Mosig G., Ghosal D., Bock S. Interactions between the maturation protein gp17 and the single-stranded DNA binding protein gp32 initiate DNA packaging and compete with initiation of secondary DNA replication forks in phage T4. Prog Clin Biol Res. 1981;64:139–150. [PubMed] [Google Scholar]
  31. Mosig G., Luder A., Garcia G., Dannenberg R., Bock S. In vivo interactions of genes and proteins in DNA replication and recombination of phage T4. Cold Spring Harb Symp Quant Biol. 1979;43(Pt 1):501–515. doi: 10.1101/sqb.1979.043.01.056. [DOI] [PubMed] [Google Scholar]
  32. Mosig G. Recombination in bacteriophage T4. Adv Genet. 1970;15:1–53. doi: 10.1016/s0065-2660(08)60070-x. [DOI] [PubMed] [Google Scholar]
  33. Mueller J. E., Kemper B., Cunningham R. P., Kallenbach N. R., Seeman N. C. T4 endonuclease VII cleaves the crossover strands of Holliday junction analogs. Proc Natl Acad Sci U S A. 1988 Dec;85(24):9441–9445. doi: 10.1073/pnas.85.24.9441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Muzyczka N., Poland R. L., Bessman M. J. Studies on the biochemical basis of spontaneous mutation. I. A comparison of the deoxyribonucleic acid polymerases of mutator, antimutator, and wild type strains of bacteriophage T4. J Biol Chem. 1972 Nov 25;247(22):7116–7122. [PubMed] [Google Scholar]
  35. Shah D. B., Berger H. Replication of gene 46-47 amber mutants of bacteriophage T4D. J Mol Biol. 1971 Apr 14;57(1):17–34. doi: 10.1016/0022-2836(71)90117-3. [DOI] [PubMed] [Google Scholar]
  36. Shah D. B., DeLorenzo L. Suppression of gene 49 mutations of bacteriophage T4 by a second mutation in gene X: structure of pseudorevertant DNA. J Virol. 1977 Dec;24(3):794–804. doi: 10.1128/jvi.24.3.794-804.1977. [DOI] [PMC free article] [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. Shibata T., DasGupta C., Cunningham R. P., Radding C. M. Homologous pairing in genetic recombination: formation of D loops by combined action of recA protein and a helix-destabilizing protein. Proc Natl Acad Sci U S A. 1980 May;77(5):2606–2610. doi: 10.1073/pnas.77.5.2606. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Sigal N., Alberts B. Genetic recombination: the nature of a crossed strand-exchange between two homologous DNA molecules. J Mol Biol. 1972 Nov 28;71(3):789–793. doi: 10.1016/s0022-2836(72)80039-1. [DOI] [PubMed] [Google Scholar]
  40. Uhlenhopp E. L., Zimm B. H., Cummings D. J. Structural aberrations in T-even bacteriophage. VI. Molecular weight of DNA from giant heads. J Mol Biol. 1974 Nov 15;89(4):689–702. doi: 10.1016/0022-2836(74)90045-x. [DOI] [PubMed] [Google Scholar]
  41. WOMACK F. C. AN ANALYSIS OF SINGLE-BURST PROGENY OF BACTERIA SINGLY INFECTED WITH A BACTERIOPHAGE HETEROZYGOTE. Virology. 1963 Oct;21:232–241. doi: 10.1016/0042-6822(63)90262-9. [DOI] [PubMed] [Google Scholar]
  42. Watson J. D. Origin of concatemeric T7 DNA. Nat New Biol. 1972 Oct 18;239(94):197–201. doi: 10.1038/newbio239197a0. [DOI] [PubMed] [Google Scholar]
  43. Yonesaki T., Ryo Y., Minagawa T., Takahashi H. Purification and some of the functions of the products of bacteriophage T4 recombination genes, uvsX and uvsY. Eur J Biochem. 1985 Apr 1;148(1):127–134. doi: 10.1111/j.1432-1033.1985.tb08816.x. [DOI] [PubMed] [Google Scholar]

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