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. 1991 Apr;127(4):637–647. doi: 10.1093/genetics/127.4.637

Fine Structure Genetic and Physical Map of the Gene 3 to 10 Region of the Bacteriophage P22 Chromosome

S Casjens 1, K Eppler 1, L Sampson 1, R Parr 1, E Wyckoff 1
PMCID: PMC1204392  PMID: 2029965

Abstract

The mechanism by which dsDNA is packaged by viruses is not yet understood in any system. Bacteriophage P22 has been a productive system in which to study the molecular genetics of virus particle assembly and DNA packaging. Only five phage encoded proteins, the products of genes 3, 2, 1, 8 and 5, are required for packaging the virus chromosome inside the coat protein shell. We report here the construction of a detailed genetic and physical map of these genes, the neighboring gene 4 and a portion of gene 10, in which 289 conditional lethal amber, opal, temperature sensitive and cold sensitive mutations are mapped into 44 small (several hundred base pair) intervals of known sequence. Knowledge of missense mutant phenotypes and information on the location of these mutations allows us to begin the assignment of partial protein functions to portions of these genes. The map and mapping strains will be of use in the further genetic dissection of the P22 DNA packaging and prohead assembly processes.

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Selected References

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  1. Adams M. B., Hayden M., Casjens S. On the sequential packaging of bacteriophage P22 DNA. J Virol. 1983 May;46(2):673–677. doi: 10.1128/jvi.46.2.673-677.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Backhaus H. DNA packaging initiation of Salmonella bacteriophage P22: determination of cut sites within the DNA sequence coding for gene 3. J Virol. 1985 Aug;55(2):458–465. doi: 10.1128/jvi.55.2.458-465.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barrett B. K., Berget P. B. Using transposon Tn5 insertions to sequence bacteriophage T4 gene 11. DNA. 1989 May;8(4):287–295. doi: 10.1089/dna.1.1989.8.287. [DOI] [PubMed] [Google Scholar]
  4. Bazinet C., Benbasat J., King J., Carazo J. M., Carrascosa J. L. Purification and organization of the gene 1 portal protein required for phage P22 DNA packaging. Biochemistry. 1988 Mar 22;27(6):1849–1856. doi: 10.1021/bi00406a009. [DOI] [PubMed] [Google Scholar]
  5. Bazinet C., King J. Initiation of P22 procapsid assembly in vivo. J Mol Biol. 1988 Jul 5;202(1):77–86. doi: 10.1016/0022-2836(88)90520-7. [DOI] [PubMed] [Google Scholar]
  6. Casadaban M. J., Chou J., Cohen S. N. In vitro gene fusions that join an enzymatically active beta-galactosidase segment to amino-terminal fragments of exogenous proteins: Escherichia coli plasmid vectors for the detection and cloning of translational initiation signals. J Bacteriol. 1980 Aug;143(2):971–980. doi: 10.1128/jb.143.2.971-980.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Casjens S., Eppler K., Parr R., Poteete A. R. Nucleotide sequence of the bacteriophage P22 gene 19 to 3 region: identification of a new gene required for lysis. Virology. 1989 Aug;171(2):588–598. doi: 10.1016/0042-6822(89)90628-4. [DOI] [PubMed] [Google Scholar]
  8. Casjens S., Hayden M. Analysis in vivo of the bacteriophage P22 headful nuclease. J Mol Biol. 1988 Feb 5;199(3):467–474. doi: 10.1016/0022-2836(88)90618-3. [DOI] [PubMed] [Google Scholar]
  9. Casjens S., Hayden M., Jackson E., Deans R. Additional restriction endonuclease cleavage sites on the bacteriophage P22 genome. J Virol. 1983 Feb;45(2):864–867. doi: 10.1128/jvi.45.2.864-867.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Casjens S., Huang W. M., Hayden M., Parr R. Initiation of bacteriophage P22 DNA packaging series. Analysis of a mutant that alters the DNA target specificity of the packaging apparatus. J Mol Biol. 1987 Apr 5;194(3):411–422. doi: 10.1016/0022-2836(87)90671-1. [DOI] [PubMed] [Google Scholar]
  11. Casjens S., Huang W. M. Initiation of sequential packaging of bacteriophage P22 DNA. J Mol Biol. 1982 May 15;157(2):287–298. doi: 10.1016/0022-2836(82)90235-2. [DOI] [PubMed] [Google Scholar]
  12. Chan R. K., Botstein D. Genetics of bacteriophage P22. I. Isolation of prophage deletions which affect immunity to superinfection. Virology. 1972 Jul;49(1):257–267. doi: 10.1016/s0042-6822(72)80027-8. [DOI] [PubMed] [Google Scholar]
  13. Duda R. L., Gingery M., Eiserling F. A. Potential length determiner and DNA injection protein is extruded from bacteriophage T4 tail tubes in vitro. Virology. 1986 Jun;151(2):296–314. doi: 10.1016/0042-6822(86)90051-6. [DOI] [PubMed] [Google Scholar]
  14. Earnshaw W., Casjens S., Harrison S. C. Assembly of the head of bacteriophage P22: x-ray diffraction from heads, proheads and related structures. J Mol Biol. 1976 Jun 25;104(2):387–410. doi: 10.1016/0022-2836(76)90278-3. [DOI] [PubMed] [Google Scholar]
  15. Fane B., King J. Identification of sites influencing the folding and subunit assembly of the P22 tailspike polypeptide chain using nonsense mutations. Genetics. 1987 Oct;117(2):157–171. doi: 10.1093/genetics/117.2.157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gough M., Levine M. The circularity of the phage P22 linkage map. Genetics. 1968 Feb;58(2):161–169. doi: 10.1093/genetics/58.2.161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hayden M., Adams M. B., Casjens S. Bacteriophage L: chromosome physical map and structural proteins. Virology. 1985 Dec;147(2):431–440. doi: 10.1016/0042-6822(85)90145-x. [DOI] [PubMed] [Google Scholar]
  18. Jackson E. N., Jackson D. A., Deans R. J. EcoRI analysis of bacteriophage P22 DNA packaging. J Mol Biol. 1978 Jan 25;118(3):365–388. doi: 10.1016/0022-2836(78)90234-6. [DOI] [PubMed] [Google Scholar]
  19. Jackson E. N., Laski F., Andres C. Bacteriophage P22 mutants that alter the specificity of DNA packaging. J Mol Biol. 1982 Feb 5;154(4):551–563. doi: 10.1016/s0022-2836(82)80014-4. [DOI] [PubMed] [Google Scholar]
  20. Jarvik J., Botstein D. A genetic method for determining the order of events in a biological pathway. Proc Natl Acad Sci U S A. 1973 Jul;70(7):2046–2050. doi: 10.1073/pnas.70.7.2046. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Jarvik J., Botstein D. Conditional-lethal mutations that suppress genetic defects in morphogenesis by altering structural proteins. Proc Natl Acad Sci U S A. 1975 Jul;72(7):2738–2742. doi: 10.1073/pnas.72.7.2738. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kikuchi Y., King J. Genetic control of bacteriophage T4 baseplate morphogenesis. II. Mutants unable to form the central part of the baseplate. J Mol Biol. 1975 Dec 25;99(4):673–694. doi: 10.1016/s0022-2836(75)80179-3. [DOI] [PubMed] [Google Scholar]
  23. King J., Casjens S. Catalytic head assembling protein in virus morphogenesis. Nature. 1974 Sep 13;251(5471):112–119. doi: 10.1038/251112a0. [DOI] [PubMed] [Google Scholar]
  24. King J., Hall C., Casjens S. Control of the synthesis of phage P22 scaffolding protein is coupled to capsid assembly. Cell. 1978 Oct;15(2):551–560. doi: 10.1016/0092-8674(78)90023-5. [DOI] [PubMed] [Google Scholar]
  25. King J., Lenk E. V., Botstein D. Mechanism of head assembly and DNA encapsulation in Salmonella phage P22. II. Morphogenetic pathway. J Mol Biol. 1973 Nov 15;80(4):697–731. doi: 10.1016/0022-2836(73)90205-2. [DOI] [PubMed] [Google Scholar]
  26. Kolstad R. A., Prell H. H. An amber map of Salmonella phage P22. Mol Gen Genet. 1969 Aug 15;104(4):339–350. doi: 10.1007/BF00334233. [DOI] [PubMed] [Google Scholar]
  27. Kufer B., Backhaus H., Schmieger H. The packaging initiation site of phage P22. Analysis of packaging events by transduction. Mol Gen Genet. 1982;187(3):510–515. doi: 10.1007/BF00332636. [DOI] [PubMed] [Google Scholar]
  28. Laski F., Jackson E. N. Maturation cleavage of bacteriophage P22 DNA in the absence of DNA packaging. J Mol Biol. 1982 Feb 5;154(4):565–579. doi: 10.1016/s0022-2836(82)80015-6. [DOI] [PubMed] [Google Scholar]
  29. Lew K. K., Roth J. R. Isolation of UGA and UAG nonsense mutants of bacteriophage P22. Virology. 1970 Apr;40(4):1059–1062. doi: 10.1016/0042-6822(70)90153-4. [DOI] [PubMed] [Google Scholar]
  30. Manley J. L. Synthesis and degradation of termination and premature-termination fragments of beta-galactosidase in vitro and in vivo. J Mol Biol. 1978 Nov 15;125(4):407–432. doi: 10.1016/0022-2836(78)90308-x. [DOI] [PubMed] [Google Scholar]
  31. Plishker M. F., Berget P. B. Isolation and characterization of precursors in bacteriophage T4 baseplate assembly. III. The carboxyl termini of protein P11 are required for assembly activity. J Mol Biol. 1984 Sep 25;178(3):699–709. doi: 10.1016/0022-2836(84)90247-x. [DOI] [PubMed] [Google Scholar]
  32. Poteete A. R., Botstein D. Purification and properties of proteins essential to DNA encapsulation by phage P22. Virology. 1979 Jun;95(2):565–573. doi: 10.1016/0042-6822(79)90509-9. [DOI] [PubMed] [Google Scholar]
  33. Poteete A. R., King J. Functions of two new genes in Salmonella phage P22 assembly. Virology. 1977 Feb;76(2):725–739. doi: 10.1016/0042-6822(77)90254-9. [DOI] [PubMed] [Google Scholar]
  34. Raleigh E. A., Murray N. E., Revel H., Blumenthal R. M., Westaway D., Reith A. D., Rigby P. W., Elhai J., Hanahan D. McrA and McrB restriction phenotypes of some E. coli strains and implications for gene cloning. Nucleic Acids Res. 1988 Feb 25;16(4):1563–1575. doi: 10.1093/nar/16.4.1563. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Riggs P. D., Botstein D. Fusions of bacteriophage P22 late genes to the Escherichia coli lacZ gene. J Virol. 1987 Nov;61(11):3621–3624. doi: 10.1128/jvi.61.11.3621-3624.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Rutila J. E., Jackson E. N. Physical map of the bacteriophage P22 genome. Virology. 1981 Sep;113(2):769–775. doi: 10.1016/0042-6822(81)90206-3. [DOI] [PubMed] [Google Scholar]
  37. Schwarz J. J., Berget P. B. The isolation and sequence of missense and nonsense mutations in the cloned bacteriophage P22 tailspike protein gene. Genetics. 1989 Apr;121(4):635–649. doi: 10.1093/genetics/121.4.635. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Smith D. H., Berget P. B., King J. Temperature-sensitive mutants blocked in the folding or subunit assembly of the bacteriophage P22 tail-spike protein. I. Fine-structure mapping. Genetics. 1980 Oct;96(2):331–352. doi: 10.1093/genetics/96.2.331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Strauss H., King J. Steps in the stabilization of newly packaged DNA during phage P22 morphogenesis. J Mol Biol. 1984 Feb 5;172(4):523–543. doi: 10.1016/s0022-2836(84)80021-2. [DOI] [PubMed] [Google Scholar]
  40. Susskind M. M., Botstein D. Molecular genetics of bacteriophage P22. Microbiol Rev. 1978 Jun;42(2):385–413. doi: 10.1128/mr.42.2.385-413.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Susskind M. M., Botstein D., Wright A. Superinfection exclusion by P22 prophage in lysogens of Salmonella typhimurium. III. Failure of superinfecting phage DNA to enter sieA+ lysogens. Virology. 1974 Dec;62(2):350–366. doi: 10.1016/0042-6822(74)90398-5. [DOI] [PubMed] [Google Scholar]
  42. TESSMAN I., ISHIWA H., KUMAR S. MUTAGENIC EFFECTS OF HYDROXYLAMINE IN VIVO. Science. 1965 Apr 23;148(3669):507–508. doi: 10.1126/science.148.3669.507. [DOI] [PubMed] [Google Scholar]
  43. Weaver S., Levine M. Replication in situ and DNA encapsulation following induction of an excision-defective lysogen of Salmonella bacteriophage P22. J Mol Biol. 1978 Jan 25;118(3):389–411. doi: 10.1016/0022-2836(78)90235-8. [DOI] [PubMed] [Google Scholar]
  44. Winston F., Botstein D., Miller J. H. Characterization of amber and ochre suppressors in Salmonella typhimurium. J Bacteriol. 1979 Jan;137(1):433–439. doi: 10.1128/jb.137.1.433-439.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Wyckoff E., Casjens S. Autoregulation of the bacteriophage P22 scaffolding protein gene. J Virol. 1985 Jan;53(1):192–197. doi: 10.1128/jvi.53.1.192-197.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Wyckoff E., Sampson L., Hayden M., Parr R., Huang W. M., Casjens S. Plasmid vectors useful in the study of translation initiation signals. Gene. 1986;43(3):281–286. doi: 10.1016/0378-1119(86)90217-9. [DOI] [PubMed] [Google Scholar]
  47. Yanisch-Perron C., Vieira J., Messing J. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene. 1985;33(1):103–119. doi: 10.1016/0378-1119(85)90120-9. [DOI] [PubMed] [Google Scholar]
  48. Youderian P., Susskind M. M. Identification of the products of bacteriophage P22 genes, including a new late gene. Virology. 1980 Nov;107(1):258–269. doi: 10.1016/0042-6822(80)90291-3. [DOI] [PubMed] [Google Scholar]

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