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. 1985 Oct;111(2):197–218. doi: 10.1093/genetics/111.2.197

ESCHERICHIA COLI Rho Factor Is Involved in Lysis of Bacteriophage T4-Infected Cells

Claës H Linder 1,2, Karin Carlson 1,2
PMCID: PMC1202638  PMID: 3902562

Abstract

A Rid (Rho interaction deficient) phenotype of bacteriophage T4 mutants was defined by cold-sensitive restriction (lack of plaque formation) on rho+ hosts carrying additional polar mutations in unrelated genes, coupled to suppression (plaque formation) in otherwise isogenic strains carrying either a polarity-suppressing rho or a multicopy plasmid expressing the rho+ allele. This suggests that the restriction may be due to lower levels of Rho than what is available to T4 in the suppressing strains.—Rid394x4 was isolated upon hydroxylamine mutagenesis and mapped in the t gene; other t mutants (and mot, as well as dda dexA double mutants) also showed a Rid phenotype. In liquid culture in strains that restricted plaque formation Rid394x4 showed strong lysis inhibition (a known t- phenotype) but no prolonged phage production (another well-known t- phenotype). This implies that when Rho is limiting the t mutant shuts off phage production at the normal time. Lysis inhibition was partially relieved, and phage production prolonged to varying extents depending on growth conditions in strains that allowed plaque formation. No significant effects on early gene expression were found. Apparently, both mutant (polarity-suppressing) and wild-type Rho can function in prolonging phage production and partially relieving lysis inhibition of Rid394x4 when present at a sufficiently high level, and Rho may play other role(s) in T4 development than in early gene regulation.

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Selected References

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  1. Christiansen L., Pedersen S. Cloning, restriction endonuclease mapping and post-transcriptional regulation of rpsA, the structural gene for ribosomal protein S1. Mol Gen Genet. 1981;181(4):548–551. doi: 10.1007/BF00428751. [DOI] [PubMed] [Google Scholar]
  2. Daegelen P., Brody E. Early bacteriophage T4 transcription. A diffusible product controls rIIA and rIIB RNA synthesis. J Mol Biol. 1976 May 5;103(1):127–142. doi: 10.1016/0022-2836(76)90055-3. [DOI] [PubMed] [Google Scholar]
  3. Daegelen P., D'Aubenton-Carafa Y., Brody E. The role of rho in bacteriophage T4 development. II. mot-dependent (middle mode) RNA synthesis. Virology. 1982 Feb;117(1):121–134. doi: 10.1016/0042-6822(82)90512-8. [DOI] [PubMed] [Google Scholar]
  4. Darlix J. L., Horaist M. Existence and possible roles of transcriptional barriers in T7 DNA early region as shown by electron microscopy. Nature. 1975 Jul 24;256(5515):288–292. doi: 10.1038/256288a0. [DOI] [PubMed] [Google Scholar]
  5. Das A., Court D., Adhya S. Isolation and characterization of conditional lethal mutants of Escherichia coli defective in transcription termination factor rho. Proc Natl Acad Sci U S A. 1976 Jun;73(6):1959–1963. doi: 10.1073/pnas.73.6.1959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Fuller R. S., Platt T. The attenuator of the tryptophan operon in E.coli: rho-mediated release of RNA polymerase from a transcription termination complex in vitro. Nucleic Acids Res. 1978 Dec;5(12):4613–4623. [PMC free article] [PubMed] [Google Scholar]
  7. Gauss P., Doherty D. H., Gold L. Bacterial and phage mutations that reveal helix-unwinding activities required for bacteriophage T4 DNA replication. Proc Natl Acad Sci U S A. 1983 Mar;80(6):1669–1673. doi: 10.1073/pnas.80.6.1669. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Goldfarb A., Malik S. Changed promoter specificity and antitermination properties displayed in vitro by bacteriophage T4-modified RNA polymerase. J Mol Biol. 1984 Jul 25;177(1):87–105. doi: 10.1016/0022-2836(84)90059-7. [DOI] [PubMed] [Google Scholar]
  9. Grasso R. J., Buchanan J. M. Synthesis of early RNA in bacteriophage T4-infected Escherichia coli B. Nature. 1969 Nov 29;224(5222):882–885. doi: 10.1038/224882a0. [DOI] [PubMed] [Google Scholar]
  10. Gray J. E., Patin D. W., Calhoun D. H. Identification of the protein products of the rrnC, ilv, rho region of the Escherichia coli K-12 chromosome. Mol Gen Genet. 1981;183(3):428–436. doi: 10.1007/BF00268761. [DOI] [PubMed] [Google Scholar]
  11. Guarente L. P., Mitchell D. H., Beckwith J. Transcription termination at the end of the tryptophan operon of Escherichia coli. J Mol Biol. 1977 May 25;112(3):423–436. doi: 10.1016/s0022-2836(77)80190-3. [DOI] [PubMed] [Google Scholar]
  12. Guarente L. Restoration of termination by RNA polymerase mutations is rho allele-specific. J Mol Biol. 1979 Apr 5;129(2):295–304. doi: 10.1016/0022-2836(79)90283-3. [DOI] [PubMed] [Google Scholar]
  13. Gulletta E., Das A., Adhya S. The pleiotropic ts15 mutation of E. coli is an IS1 insertion in the rho structural gene. Genetics. 1983 Oct;105(2):265–280. doi: 10.1093/genetics/105.2.265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Guterman S. K., Howitt C. L. Rho and ribosome mutation interaction: lethality of rho-15 in rpsL or rpsE strains, and rho-15 methionine auxotrophy in rps+ strains of Escherichia coli. Genetics. 1979 Oct;93(2):353–360. doi: 10.1093/genetics/93.2.353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Guterman S. K., Howitt C. L. Rifampicin supersensitivity of rho strains of E. coli, and suppression by sur mutation. Mol Gen Genet. 1979 Jan 16;169(1):27–34. doi: 10.1007/BF00267541. [DOI] [PubMed] [Google Scholar]
  16. Hall D. H., Sargent R. G., Trofatter K. F., Russell D. L. Suppressors of mutations in the bacteriophage T4 gene coding for both RNA ligase and tail fiber attachment activities. J Virol. 1980 Oct;36(1):103–108. doi: 10.1128/jvi.36.1.103-108.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hall D. H., Snyder R. D. Suppressors of mutations in the rII gene of bacteriophage T4 affect promoter utilization. Genetics. 1981 Jan;97(1):1–9. doi: 10.1093/genetics/97.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Homyk T., Jr, Weil J. Deletion analysis of two nonessential regions of the T4 genome. Virology. 1974 Oct;61(2):505–523. doi: 10.1016/0042-6822(74)90286-4. [DOI] [PubMed] [Google Scholar]
  19. Howard B. H., de Crombrugghe B. ATPase activity required for termination of transcription by the Escherichia coli protein factor rho. J Biol Chem. 1976 Apr 25;251(8):2520–2524. [PubMed] [Google Scholar]
  20. Imai M., Shigesada K. Studies on the altered rho factor in a nitA mutants of Escherichia coli defective in transcription termination. I. Characterization and quantitative determination of rho in cell extracts. J Mol Biol. 1978 Apr 25;120(4):451–466. doi: 10.1016/0022-2836(78)90348-0. [DOI] [PubMed] [Google Scholar]
  21. Jayaraman R. Transcription of bacteriophage T4 DNA by Escherichia coli RNA polymerase in vitro: identification of some immediate-early and delayed-early genes. J Mol Biol. 1972 Sep 28;70(2):253–263. doi: 10.1016/0022-2836(72)90537-2. [DOI] [PubMed] [Google Scholar]
  22. Johnson J. R., Hall D. H. Isolation and characterization of mutants of bacteriophage T4 resistant to folate analogs. Virology. 1973 Jun;53(2):413–426. doi: 10.1016/0042-6822(73)90221-3. [DOI] [PubMed] [Google Scholar]
  23. Josslin R. Physiological studies on the t gene defect in T4-infected Escherichia coli. Virology. 1971 Apr;44(1):101–107. doi: 10.1016/0042-6822(71)90157-7. [DOI] [PubMed] [Google Scholar]
  24. Kung H., Bekesi E., Guterman S. K., Gray J. E., Traub L., Calhoun D. H. Autoregulation of the rho gene of Escherichia coli K-12. Mol Gen Genet. 1984;193(2):210–213. doi: 10.1007/BF00330669. [DOI] [PubMed] [Google Scholar]
  25. Linder C. H., Sköld O. Control of early gene expression of bacteriophage T4: involvement of the host rho factor and the mot gene of the bacteriophage. J Virol. 1980 Feb;33(2):724–732. doi: 10.1128/jvi.33.2.724-732.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Linder C. H., Sköld O. Evidence for a diffusible T4 bacteriophage protein governing the initiation of delayed early RNA synthesis. J Virol. 1977 Jan;21(1):7–15. doi: 10.1128/jvi.21.1.7-15.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Mattson T., Richardson J., Goodin D. Mutant of bacteriophage T4D affecting expression of many early genes. Nature. 1974 Jul 5;250(461):48–50. doi: 10.1038/250048a0. [DOI] [PubMed] [Google Scholar]
  28. Mattson T., Van Houwe G., Epstein R. H. Isolation and characterization of conditional lethal mutations in the mot gene of bacteriophage T4. J Mol Biol. 1978 Dec 15;126(3):551–570. doi: 10.1016/0022-2836(78)90058-x. [DOI] [PubMed] [Google Scholar]
  29. Morse D. E., Guertin M. Amber suA mutations which relieve polarity. J Mol Biol. 1972 Feb 14;63(3):605–608. doi: 10.1016/0022-2836(72)90453-6. [DOI] [PubMed] [Google Scholar]
  30. Neville D. M., Jr Molecular weight determination of protein-dodecyl sulfate complexes by gel electrophoresis in a discontinuous buffer system. J Biol Chem. 1971 Oct 25;246(20):6328–6334. [PubMed] [Google Scholar]
  31. Ratner D. Evidence that mutations in the suA polarity suppressing gene directly affect termination factor rho. Nature. 1976 Jan 15;259(5539):151–153. doi: 10.1038/259151a0. [DOI] [PubMed] [Google Scholar]
  32. Revel H. R., Stitt B. L., Lielausis I., Wood W. B. Role of the host cell in bacteriophage T4 development. I. Characterization of host mutants that block T4 head assembly. J Virol. 1980 Jan;33(1):366–376. doi: 10.1128/jvi.33.1.366-376.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Sharp J. A., Platt T. Rho-dependent termination and concomitant NTPase activity requires a specific, intact RNA region. J Biol Chem. 1984 Feb 25;259(4):2268–2273. [PubMed] [Google Scholar]
  34. Shigesada K., Wu C. W. Studies of RNA release reaction catalyzed by E. coli transcription termination factor rho using isolated ternary transcription complexes. Nucleic Acids Res. 1980 Aug 11;8(15):3355–3369. doi: 10.1093/nar/8.15.3355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Simon L. D., Snover D., Doermann A. H. Bacterial mutation affecting T4 phage DNA synthesis and tail production. Nature. 1974 Dec 6;252(5483):451–455. doi: 10.1038/252451a0. [DOI] [PubMed] [Google Scholar]
  36. Stitt B. L., Revel H. R., Lielausis I., Wood W. B. Role of the host cell in bacteriophage T4 development. II. Characterization of host mutants that have pleiotropic effects on T4 growth. J Virol. 1980 Sep;35(3):775–789. doi: 10.1128/jvi.35.3.775-789.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Takahashi H. Genetic and physiological characterization of Escherichia coli K12 mutants (tabC) which induce the abortive infection of bacteriophage T4. Virology. 1978 Jun 15;87(2):256–265. doi: 10.1016/0042-6822(78)90131-9. [DOI] [PubMed] [Google Scholar]
  38. Takahashi H., Yoshikawa H. Genetic study of a new early gene, comC-alpha, of bacteriophage T4. Virology. 1979 May;95(1):215–217. doi: 10.1016/0042-6822(79)90417-3. [DOI] [PubMed] [Google Scholar]
  39. Tessman I. Mutagenic treatment of double- and single-stranded DNA phages T4 ans S13 with hydroxylamine. Virology. 1968 Jun;35(2):330–333. doi: 10.1016/0042-6822(68)90275-4. [DOI] [PubMed] [Google Scholar]
  40. Thermes C., Brody E. T4-induced antipolarity: temporal heterogeneity in response of early transcription units. J Virol. 1984 Apr;50(1):191–201. doi: 10.1128/jvi.50.1.191-201.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]

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