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. 1977 May;22(2):489–499. doi: 10.1128/jvi.22.2.489-499.1977

Structural aberrations in T-even bacteriophage. IX. Effect of mixed infection on the production of giant bacteriophage.

D J Cummings, V A Chapman, S S DeLong
PMCID: PMC515739  PMID: 864836

Abstract

To date, the production of T-even bacteriophage with giant heads has been achieved in two ways: (i) by use of canavanine-arginine treatment of Escherichia coli B cultures infected by wild-type bacteriophage (Cummings and Bolin, Bacteriol. Rev. 40:314-359, 1976; Cummings et al., Virology 54:245-261, 1973), which give a size distribution of giants that is phage specific (Cummings et al., Virology 54:245-261, 1973); and (ii) by infection with certain missense mutants of T4D gene 23 (Doermann et al., J. Virol. 12:374-385, 1973; ICN-UCLA Symposium on Molecular Biology, p. 243-285, 1973) or temperature-sensitive mutants of gene 24 (Aebi et al., J. Supramol. Struct. 2:253-275, 1974; Biljenga et al., J. Mol. Biol. 103:469-498, 1976). We now report the effect of mixed infection with several mutants of T4D on both the production and the size of giant bacteriophage. We found that gene 24 mutant is a critical partner for the production of giants. Infection using T4.24 mutants together with either T4.23 mutants, T4B+ or T6+ led to the formation of giants with heads 10- to 14-fold longer than normal-length heads. Infection with amber 24-bypass 24 double mutants of T4D led to the production of giants when gene 23 mutant was used to co-infect. Addition of canavanine to the co-infected cultures could alter the size distribution of giants, depending on which phage were used to coinfect. Gene 22 mutants had a modifying effect on these results. In the absence of canavanine co-infection with gene 22 mutants prevented the production of giants, and in the presence of canavanine giants of 1.5 to 5 head lengths were found. We have interpreted these results to mean that critical concentrations of gene products 22, 23, and 24 interact to control head length in T-even bacteriophage.

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Selected References

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  1. Aebi U., Bijlenga R., v d Broek J., v d Broek H., Eiserling F., Kellenberger C., Kellenberger E., Mesyanzhinov V., Müller L., Showe M. The transformation of tau particles into T4 heads. II. Transformations of the surface lattice and related observations on form determination. J Supramol Struct. 1974;2(2-4):253–275. doi: 10.1002/jss.400020218. [DOI] [PubMed] [Google Scholar]
  2. BRENNER S., HORNE R. W. A negative staining method for high resolution electron microscopy of viruses. Biochim Biophys Acta. 1959 Jul;34:103–110. doi: 10.1016/0006-3002(59)90237-9. [DOI] [PubMed] [Google Scholar]
  3. Bijlenga R. K., Aebi U., Kellenberger E. Properties and structure of a gene 24-controlled T4 giant phage. J Mol Biol. 1976 May 25;103(3):469–498. doi: 10.1016/0022-2836(76)90213-8. [DOI] [PubMed] [Google Scholar]
  4. Bijlenga R. K., Scraba D., Kellenberger E. Studies on the morphopoiesis of the head of T-even phage. IX. Gamma-particles: their morphology, kinetics of appearance and possible precursor function. Virology. 1973 Nov;56(1):250–267. doi: 10.1016/0042-6822(73)90304-8. [DOI] [PubMed] [Google Scholar]
  5. Broker T. R., Lehman I. R. Branched DNA molecules: intermediates in T4 recombination. J Mol Biol. 1971 Aug 28;60(1):131–149. doi: 10.1016/0022-2836(71)90453-0. [DOI] [PubMed] [Google Scholar]
  6. Chao J., Chao L., Speyer J. F. Bacteriophage T4 head morphogenesis: host DNA enzymes affect frequency of petite forms. J Mol Biol. 1974 May 5;85(1):41–50. doi: 10.1016/0022-2836(74)90127-2. [DOI] [PubMed] [Google Scholar]
  7. Couse N. L., Cummings D. J., Chapman V. A., DeLong S. S. Structural aberrations in T-even bacteriophage. I. Specificity of induction of aberrations. Virology. 1970 Nov;42(3):590–602. doi: 10.1016/0042-6822(70)90305-3. [DOI] [PubMed] [Google Scholar]
  8. Cummings D. J., Bolin R. W. Head length control in T4 bacteriophage morphogenesis: effect of canavanine on assembly. Bacteriol Rev. 1976 Jun;40(2):314–359. doi: 10.1128/br.40.2.314-359.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cummings D. J., Chapman V. A., De Long S. S., Mondale L. Induced structural defects in T-even bacteriophage. J Virol. 1967 Feb;1(1):193–204. doi: 10.1128/jvi.1.1.193-204.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cummings D. J., Chapman V. A., DeLong S. S., Couse N. L. Structural aberrations in T-even bacteriophage. 3. Induction of "lollipops" and their partial characterization. Virology. 1973 Jul;54(1):245–261. doi: 10.1016/0042-6822(73)90134-7. [DOI] [PubMed] [Google Scholar]
  11. Cummings D. J., Couse N. L., Forrest G. L. Structural defects of T-even bacteriophages. Adv Virus Res. 1970;16:1–41. doi: 10.1016/s0065-3527(08)60020-2. [DOI] [PubMed] [Google Scholar]
  12. Doermann A. H., Eiserling F. A., Boehner L. Genetic control of capsid length in bacteriophage T4. I. Isolation and preliminary description of four new mutants. J Virol. 1973 Aug;12(2):374–385. doi: 10.1128/jvi.12.2.374-385.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Eiserling F. A., Geiduschek E. P., Epstein R. H., Metter E. J. Capsid size and deoxyribonucleic acid length: the petite variant of bacteriophage T4. J Virol. 1970 Dec;6(6):865–876. doi: 10.1128/jvi.6.6.865-876.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Ishii T., Yanagida M. Molecular organization of the shell of the Teven bacteriophage head. J Mol Biol. 1975 Oct 5;97(4):655–660. doi: 10.1016/s0022-2836(75)80065-9. [DOI] [PubMed] [Google Scholar]
  15. Kozinski A. W., Felgenhauer Z. Z. Molecular recombination in T4 bacteriophage deoxyribonucleic acid. II. Single-strand breaks and exposure of uncomplemented areas as a prerequisite for recombination. J Virol. 1967 Dec;1(6):1193–1202. doi: 10.1128/jvi.1.6.1193-1202.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  18. Laemmli U. K., Johnson R. A. Maturation of the head of bacteriophage T4. II. Head-related, aberrant tau-particles. J Mol Biol. 1973 Nov 15;80(4):601–611. doi: 10.1016/0022-2836(73)90199-x. [DOI] [PubMed] [Google Scholar]
  19. Laemmli U. K., Mölbert E., Showe M., Kellenberger E. Form-determining function of the genes required for the assembly of the head of bacteriophage T4. J Mol Biol. 1970 Apr 14;49(1):99–113. doi: 10.1016/0022-2836(70)90379-7. [DOI] [PubMed] [Google Scholar]
  20. Laemmli U. K., Paulson J. R., Hitchins V. Maturation of the head of bacteriophage T4. V. A possible DNA packaging mechanism: in vitro cleavage of the head proteins and the structure of the core of the polyhead. J Supramol Struct. 1974;2(2-4):276–301. doi: 10.1002/jss.400020219. [DOI] [PubMed] [Google Scholar]
  21. Mosig G., Carnighan J. R., Bibring J. B., Cole R., Bock H. G., Bock S. Coordinate variation in lengths of deoxyribonucleic acid molecules and head lengths in morphological variants of bacteriophage T4. J Virol. 1972 May;9(5):857–871. doi: 10.1128/jvi.9.5.857-871.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Paulson J. R., Lazaroff S., Laemmli U. K. Head length determination in bacteriophage T4: the role of the core protein P22. J Mol Biol. 1976 May 5;103(1):155–174. doi: 10.1016/0022-2836(76)90057-7. [DOI] [PubMed] [Google Scholar]
  24. SARABHAI A. S., STRETTON A. O., BRENNER S., BOLLE A. CO-LINEARITY OF THE GENE WITH THE POLYPEPTIDE CHAIN. Nature. 1964 Jan 4;201:13–17. doi: 10.1038/201013a0. [DOI] [PubMed] [Google Scholar]
  25. Sato K., Sekiguchi M. Studies on temperature-dependent ultraviolet light-sensitive mutants of bacteriophage T4: the structural gene for T4 endonuclease V. J Mol Biol. 1976 Mar 25;102(1):15–26. doi: 10.1016/0022-2836(76)90071-1. [DOI] [PubMed] [Google Scholar]
  26. Showe M. K., Black L. W. Assembly core of bacteriophage T4: an intermediate in head formation. Nat New Biol. 1973 Mar 21;242(116):70–75. doi: 10.1038/newbio242070a0. [DOI] [PubMed] [Google Scholar]
  27. Sigal N., Delius H., Kornberg T., Gefter M. L., Alberts B. A DNA-unwinding protein isolated from Escherichia coli: its interaction with DNA and with DNA polymerases. Proc Natl Acad Sci U S A. 1972 Dec;69(12):3537–3541. doi: 10.1073/pnas.69.12.3537. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Streisinger G., Emrich J., Stahl M. M. Chromosome structure in phage t4, iii. Terminal redundancy and length determination. Proc Natl Acad Sci U S A. 1967 Feb;57(2):292–295. doi: 10.1073/pnas.57.2.292. [DOI] [PMC free article] [PubMed] [Google Scholar]

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