Skip to main content
Journal of Virology logoLink to Journal of Virology
. 1984 Apr;50(1):191–201. doi: 10.1128/jvi.50.1.191-201.1984

T4-induced antipolarity: temporal heterogeneity in response of early transcription units.

C Thermes, E Brody
PMCID: PMC255599  PMID: 6699944

Abstract

When T4 infects Escherichia coli in the absence of protein synthesis, rho-mediated termination takes place on early polycistronic transcription units. During the early period of development, the appearance of delayed early transcripts becomes insensitive to the inhibition of protein synthesis. In the absence of the T4 gene product mot, an inducer for the middle mode of transcription, only the early polycistronic messengers are synthesized. In mot- -infected cells, the synthesis of the distal transcripts still becomes completely insensitive to the polar effect of chloramphenicol. This happens because potential rho-sensitive termination sites are not used in these cells. In this respect, overcoming polarity induced by chloramphenicol can be called a process of antitermination. The mot-independent antitermination can be studied by addition of chloramphenicol during infections with mot- bacteriophage. The effect is stable; it allows a constant percentage of rho-sensitive termination sites in the cell to be traversed by RNA polymerase for at least 10 min at 42 degrees C. By examining six different transcription units on the T4 genome, we find that each transcription unit has a cis-acting component (or components) which determines when its rho-sensitive termination site stops functioning. In extreme cases, rho acts with 100% efficiency in some transcription units, whereas it is almost inactive in others.

Full text

PDF
191

Selected References

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

  1. Adhya S., Gottesman M. Control of transcription termination. Annu Rev Biochem. 1978;47:967–996. doi: 10.1146/annurev.bi.47.070178.004535. [DOI] [PubMed] [Google Scholar]
  2. Black L. W. Bacteriophage T4 internal protein mutants: isolation and properties. Virology. 1974 Jul;60(1):166–179. doi: 10.1016/0042-6822(74)90374-2. [DOI] [PubMed] [Google Scholar]
  3. Black L. W., Gold L. M. Pre-replicative development of the bacteriophage T4: RNA and protein synthesis in vivo and in vitro. J Mol Biol. 1971 Sep 14;60(2):365–388. doi: 10.1016/0022-2836(71)90300-7. [DOI] [PubMed] [Google Scholar]
  4. Bolle A., Epstein R. H., Salser W., Geiduschek E. P. Transcription during bacteriophage T4 development: synthesis and relative stability of early and late RNA. J Mol Biol. 1968 Feb 14;31(3):325–348. doi: 10.1016/0022-2836(68)90413-0. [DOI] [PubMed] [Google Scholar]
  5. Brody E. N., Geiduschek E. P. Transcription of the bacteriophage T4 template. Detailed comparison of in vitro and in vivo transcripts. Biochemistry. 1970 Mar 17;9(6):1300–1309. doi: 10.1021/bi00808a002. [DOI] [PubMed] [Google Scholar]
  6. Brody E. N., Gold L. M., Black L. W. Transcription and translation of sheared bacteriophage T4 DNA in vitro. J Mol Biol. 1971 Sep 14;60(2):389–393. doi: 10.1016/0022-2836(71)90301-9. [DOI] [PubMed] [Google Scholar]
  7. Caruso M., Coppo A., Manzi A., Pulitzer J. F. Host--virus interactions in the control of T4 prereplicative transcription. I. tabC (rho) mutants. J Mol Biol. 1979 Dec 25;135(4):959–977. doi: 10.1016/0022-2836(79)90522-9. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Daegelen P., D'Aubenton-Carafa Y., Brody E. The role of rho in bacteriophage T4 development. I. Control of growth and polarity. Virology. 1982 Feb;117(1):105–120. doi: 10.1016/0042-6822(82)90511-6. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Fukada K., Gossens L., Abelson J. The cloning of a T4 transfer RNA gene cluster. J Mol Biol. 1980 Feb 25;137(2):213–234. doi: 10.1016/0022-2836(80)90326-5. [DOI] [PubMed] [Google Scholar]
  12. Fukada K., Otsuka A., Abelson J. A restriction map of the T4 transfer RNA gene cluster. J Mol Biol. 1980 Feb 25;137(2):191–211. doi: 10.1016/0022-2836(80)90325-3. [DOI] [PubMed] [Google Scholar]
  13. Goldfarb A., Daniel V. Mapping of transcription units in the bacteriophage T4 tRNA gene cluster. J Mol Biol. 1981 Mar 15;146(4):393–412. doi: 10.1016/0022-2836(81)90039-5. [DOI] [PubMed] [Google Scholar]
  14. Goldfarb A., Daniel V. Transcriptional control of two gene subclusters in the tRNA operon of bacteriophage T4. Nature. 1980 Jul 24;286(5771):418–420. doi: 10.1038/286418a0. [DOI] [PubMed] [Google Scholar]
  15. Goldfarb A. IN vitro transcription of bacteriophage T4 tRNA gene cluster from two different promoters. Nucleic Acids Res. 1981 Feb 11;9(3):519–527. doi: 10.1093/nar/9.3.519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Greenblatt J. Regulation of transcription termination by the N gene protein of bacteriophage lambda. Cell. 1981 Apr;24(1):8–9. doi: 10.1016/0092-8674(81)90495-5. [DOI] [PubMed] [Google Scholar]
  17. Guha A., Szybalski W., Salser W., Geiduschek E. P., Pulitzer J. F., Bolle A. Controls and polarity of transcription during bacteriophage T4 development. J Mol Biol. 1971 Jul 28;59(2):329–349. doi: 10.1016/0022-2836(71)90054-4. [DOI] [PubMed] [Google Scholar]
  18. Hercules K., Sauerbier W. Two modes of in vivo transcription for genes 43 and 45 of phage T4. J Virol. 1974 Aug;14(2):341–348. doi: 10.1128/jvi.14.2.341-348.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kasai T., Bautz E. K. Regulation of gene-specific RNA synthesis in bacteriophage T4. J Mol Biol. 1969 May 14;41(3):401–417. doi: 10.1016/0022-2836(69)90284-8. [DOI] [PubMed] [Google Scholar]
  20. Kassavetis G. A., Chamberlin M. J. Pausing and termination of transcription within the early region of bacteriophage T7 DNA in vitro. J Biol Chem. 1981 Mar 25;256(6):2777–2786. [PubMed] [Google Scholar]
  21. Mattson T., Van Houwe G., Bolle A., Selzer G., Epstein R. Genetic identification of cloned fragments of bacteriophage T4 DNA and complementation by some clones containing early T4 genes. Mol Gen Genet. 1977 Sep 9;154(3):319–326. doi: 10.1007/BF00571289. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. O'Farrell P. H., Kutter E., Nakanishi M. A restriction map of the bacteriophage T4 genome. Mol Gen Genet. 1980;179(2):421–435. doi: 10.1007/BF00425473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. O'Farrell P. Z., Gold L. M. Bacteriophage T4 gene expression. Evidence for two classes of prereplicative cistrons. J Biol Chem. 1973 Aug 10;248(15):5502–5511. [PubMed] [Google Scholar]
  25. Owen J. E., Schultz D. W., Taylor A., Smith G. R. Nucleotide sequence of the lysozyme gene of bacteriophage T4. Analysis of mutations involving repeated sequences. J Mol Biol. 1983 Apr 5;165(2):229–248. doi: 10.1016/s0022-2836(83)80255-1. [DOI] [PubMed] [Google Scholar]
  26. Pribnow D., Sigurdson D. C., Gold L., Singer B. S., Napoli C., Brosius J., Dull T. J., Noller H. F. rII cistrons of bacteriophage T4. DNA sequence around the intercistronic divide and positions of genetic landmarks. J Mol Biol. 1981 Jul 5;149(3):337–376. doi: 10.1016/0022-2836(81)90477-0. [DOI] [PubMed] [Google Scholar]
  27. Pulitzer J. F., Coppo A., Caruso M. Host--virus interactions in the control of T4 prereplicative transcription. II. Interaction between tabC (rho) mutants and T4 mot mutants. J Mol Biol. 1979 Dec 25;135(4):979–997. doi: 10.1016/0022-2836(79)90523-0. [DOI] [PubMed] [Google Scholar]
  28. Rosenberg M., Court D. Regulatory sequences involved in the promotion and termination of RNA transcription. Annu Rev Genet. 1979;13:319–353. doi: 10.1146/annurev.ge.13.120179.001535. [DOI] [PubMed] [Google Scholar]
  29. Salser W., Bolle A., Epstein R. Transcription during bacteriophage T4 development: a demonstration that distinct subclasses of the "early" RNA appear at different times and that some are "turned off" at late times. J Mol Biol. 1970 Apr 28;49(2):271–295. doi: 10.1016/0022-2836(70)90246-9. [DOI] [PubMed] [Google Scholar]
  30. Sauer B., Ow D., Ling L., Calendar R. Mutants of satellite bacteriophage P4 that are defective in the suppression of transcriptional polarity. J Mol Biol. 1981 Jan 5;145(1):29–46. doi: 10.1016/0022-2836(81)90333-8. [DOI] [PubMed] [Google Scholar]
  31. Schechtman M. G., Alegre J. N., Roberts J. W. Assay and characterization of late gene regulators of bacteriophages lambda82 and phi.. J Mol Biol. 1980 Sep 25;142(3):269–288. doi: 10.1016/0022-2836(80)90273-9. [DOI] [PubMed] [Google Scholar]
  32. Schmidt D. A., Mazaitis A. J., Kasai T., Bautz E. K. Involvement of a phage T4 sigma factor and an anti-terminator protein in the transcription of early T4 genes in vivo. Nature. 1970 Mar 14;225(5237):1012–1016. doi: 10.1038/2251012a0. [DOI] [PubMed] [Google Scholar]
  33. Sederoff R., Bolle A., Epstein R. H. A method for the detection of specific T4 messenger RNAs by hybridization competition. Virology. 1971 Aug;45(2):440–455. doi: 10.1016/0042-6822(71)90344-8. [DOI] [PubMed] [Google Scholar]
  34. Selzer G., Belin D., Bolle A., Van Houwe G., Mattson T., Epstein R. In vivo expression of the rII region of bacteriophage T4 present in chimeric plasmids. Mol Gen Genet. 1981;183(3):505–513. doi: 10.1007/BF00268772. [DOI] [PubMed] [Google Scholar]
  35. Selzer G., Bolle A., Krisch B., Epstein R. Construction and properties of recombinant plasmids containing the rII genes of bacteriophage T4. Mol Gen Genet. 1978 Feb 27;159(3):301–309. doi: 10.1007/BF00268267. [DOI] [PubMed] [Google Scholar]
  36. Young E. T. Analysis of bacteriophage T4 chloramphenicol RNA by DNA-RNA hybridization and by cell-free protein synthesis, and the effect of Escherichia coli polarity-suppressing alleles on its synthesis. J Mol Biol. 1975 Aug 15;96(3):393–424. doi: 10.1016/0022-2836(75)90168-0. [DOI] [PubMed] [Google Scholar]
  37. Young E. T., Mattson T., Selzer G., Van Houwe G., Bolle A., Epstein R. Bacteriophage T4 gene transcription studied by hybridization to cloned restriction fragments. J Mol Biol. 1980 Apr 15;138(3):423–445. doi: 10.1016/s0022-2836(80)80011-8. [DOI] [PubMed] [Google Scholar]
  38. Young E. T., Menard R. C. Sizes of bacteriophage T4 early mRNA's separated by preparative polyacrylamide gel electrophoresis and identified by in vitro translation and by hybridization to recombinant T4 plasmids. J Virol. 1981 Dec;40(3):772–789. doi: 10.1128/jvi.40.3.772-789.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES