Abstract
Bacteriophage lambda with mutations in genes that control prohead assembly and other head precursors cannot mature their DNA. In this paper we present evidence that the failure of these phage mutants to mature DNA is a reflection of a mechanism that modulates terminase nicking activity during normal phage development. We have constructed plasmids that contain the lambda-cohesive end site (cos) and the genes that code for DNA terminase, the enzyme that matures DNA by cutting at cos. The DNA terminase genes are under control of a thermosensitive cI repressor. These plasmids lack most of the genes involved in prohead morphogenesis and other head precursors. However, when repression is lifted by destruction of the thermosensitive repressor, the terminase synthesized is able to cut almost 100% of the plasmids. Therefore, these plasmids can mature in the absence of proheads and other head gene products. The plasmids are also able to complement mutants of lambda deficient in terminase and DNA maturation. However, in these complementation experiments, if the phage carry mutations in prohead genes E or B, not only is phage DNA maturation blocked, but the plasmid also fails to mature. These experiments show that, in the absence of proheads, phage lambda produces a trans-acting inhibitor of maturation. The genetic determinant of this inhibitor maps in a region extending from the middle of gene B to the end of gene C. A model is proposed in which the nicking activity of DNA-bound terminase is inhibited by the trans-acting inhibitor. Prohead (and other factors) binding to this complex would release the block to allow DNA cleavage and packaging.
MeSH Terms
Bacteriophage lambda/genetics,growth & development,metabolism
Chromosome Mapping
DNA, Viral/genetics,metabolism
Endodeoxyribonucleases/antagonists & inhibitors,genetics,metabolism
Genes, Viral
Models, Biological
Models, Genetic
Mutation
Plasmids
Chemicals
DNA, Viral
Endodeoxyribonucleases
terminase
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Murialdo H
Fife W L
References (25)
25 references, click to expand
-
Action of the lambda chromosome. I. Control of functions late in bacteriophage development.
J Mol Biol. 1966 Aug;19(1):187-201
PMID: 5967283
-
New mutations in the S cistron of bacteriophage lambda affecting host cell lysis.
Virology. 1969 May;38(1):200-2
PMID: 4891223
-
DNA replication in head mutants of bacteriophage lambda.
J Mol Biol. 1969 Feb 14;39(3):679-83
PMID: 5357220
-
Isolation and structure of phage lambda head-mutant DNA.
J Mol Biol. 1972 Mar 14;64(3):519-40
PMID: 5022188
-
Head assembly steps controlled by genes F and W in bacteriophage lambda.
J Mol Biol. 1972 Mar 14;64(3):551-63
PMID: 5022189
-
Intermediates in the maturation of bacteriophage lambda DNA.
Virology. 1973 Jul;54(1):19-27
PMID: 4576745
-
Host participation in bacteriophage lambda head assembly.
J Mol Biol. 1973 May 5;76(1):45-60
PMID: 4578100
-
On maturation of the bacteriophage lambda chromosome.
Mol Gen Genet. 1973 Dec 31;127(4):285-95
PMID: 4594001
-
Bacteriophage lambda derivatives carrying two copies of the cohesive end site.
J Mol Biol. 1974 Mar 15;83(4):511-25
PMID: 4598361
-
Phage lambda DNA packaging, in vitro.
J Supramol Struct. 1974;2(2-4):302-17
PMID: 4437178
-
Role of genes O and P in the replication of bacteriophage lambda DNA.
J Mol Biol. 1975 May 25;94(3):385-96
PMID: 1177302
-
Petit lambda, a family of particles from coliphage lambda infected cells.
J Mol Biol. 1975 Oct 15;98(1):107-20
PMID: 1104865
-
Detection of specific sequences among DNA fragments separated by gel electrophoresis.
J Mol Biol. 1975 Nov 5;98(3):503-17
PMID: 1195397
-
Assembly of biologically active proheads of bacteriophage lambda in vitro.
Proc Natl Acad Sci U S A. 1977 Mar;74(3):906-10
PMID: 265585
-
Packaging of coliphage lambda DNA. II. The role of the gene D protein.
J Mol Biol. 1977 Dec 15;117(3):733-59
PMID: 609100
-
Genetic and physiological characterization of the J gene of bacteriophage lambda.
Virology. 1978 Jun 15;87(2):437-58
PMID: 664261
-
A genetic analysis of bacteriophage lambda prohead assembly in vitro.
J Mol Biol. 1978 Oct 15;125(1):57-74
PMID: 712857
-
Outer surface protein of bacteriophage lambda.
J Mol Biol. 1980 May 25;139(3):277-95
PMID: 6449595
-
Bacteriophage lambda DNA maturation. The functional relationships among the products of genes Nul, A and FI.
J Mol Biol. 1981 Jan 15;145(2):375-404
PMID: 6455531
-
Maturation cleavage of bacteriophage P22 DNA in the absence of DNA packaging.
J Mol Biol. 1982 Feb 5;154(4):565-79
PMID: 6283090
-
Nucleotide sequence of bacteriophage lambda DNA.
J Mol Biol. 1982 Dec 25;162(4):729-73
PMID: 6221115
-
A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity.
Anal Biochem. 1983 Jul 1;132(1):6-13
PMID: 6312838
-
The maturation of coliphage lambda DNA in the absence of its packaging.
Gene. 1984 Oct;30(1-3):183-94
PMID: 6096213
-
Analysis of cosmids using linearization by phage lambda terminase.
Gene. 1985;40(2-3):259-66
PMID: 3007292
-
THE AMOUNT OF GALACTOSE GENETIC MATERIAL IN LAMBDA-DG BACTERIOPHAGE WITH DIFFERENT DENSITIES.
J Mol Biol. 1963 Dec;7:710-20
PMID: 14102203