Immunity and Repression in Bacteriophages P1 and P7

Scott, June R.

doi:10.1007/978-3-642-67717-5_3

Cited by 38 publications

(14 citation statements)

References 51 publications

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“…The cl gene is located in the immunity region immC, and the C1 repressor acts on at least 14 operators (Ops) which are widely distributed over the P1 genome (2,5,6,29). The c4 gene is located in the immI region, and the C4 repressor prevents expression of the closely linked antirepressor gene ant (21). The antirepressor antagonizes the effect of the C1 repressor by an as yet unknown mechanism.…”

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Cloning, expression, and characterization of the icd gene in the immI operon of bacteriophage P1

1993

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The immI operon of P1 contains the genes c4, ied (formerly called orf), and ant which are constitutively transcribed in that order from a single promoter, PSib. C4 is an antisense RNA which is processed from the precursor transcript. C4 RNA acts as a translational repressor oficd, thereby also inhibiting antirepressor (ant) synthesis. We have cloned the icd and the overlapping icd and ant genes. We show, by means of plasmid deletion analysis, that icd is translationally coupled to ant. An internal in-frame deletion of icd making up 65% of the codons still allows antirepressor synthesis at a reduced rate, indicating that a functionally active icd gene product is dispensable for ant expression. We identify the product of the icd gene as a 7.3-kDa protein which interferes with cell division. The results suggest that constitutive expression oficd, in the absence of a functionally active antirepressor, prevents P1 lysogen formation because of its detrimental effect on the host cell.The temperate bacteriophage P1 is maintained as a unitcopy plasmid in the bacterial host. Maintenance of lysogeny requires the continuous expression of two genes, cl and c4, that code for repressors of lytic growth (for a review, see reference 33). The cl gene is located in the immunity region immC, and the C1 repressor acts on at least 14 operators (Ops) which are widely distributed over the P1 genome (2,5,6,29). The c4 gene is located in the immI region, and the C4 repressor prevents expression of the closely linked antirepressor gene ant (21). The antirepressor antagonizes the effect of the C1 repressor by an as yet unknown mechanism. A third regulatory gene, bof, encoding a corepressor of C1 is located in the immT region (18,28,30).A detailed analysis of the P1 immI operon revealed the following organization (see Fig. 1 and 2). A C1i Bof-controlled operator-promoter element, Op51-P5ia; a non-regulated promoter, P5lb; and the genes c4, icd (formerly called orfx), and ant are arranged in that order in clockwise orientation of the P1 map (1,8,12). The ant gene encodes two antirepressor proteins, Antl and Ant2, the latter initiating at an in-frame start codon (9, 12). The product of the c4 repressor gene is a 77-base antisense RNA (4), acting on a target ant mRNA. Interaction depends on the complementarity of two pairs of short sequences, a'-a2 and b'-b2, respectively. The sequences a' and b' are contained within loops of a stem-loop secondary structure of C4; that of a2 and b2 are contained in the target RNA and encompass the virs mutation and the ribosome-binding site of icd, respectively (3).

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Cloning, expression, and characterization of the icd gene in the immI operon of bacteriophage P1

1993

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“…For example, P1 genes for both immunity control and morphogenesis are widely dispersed over the genome (50,62,63). The presence of at least 14 operator sites for the P1 cI repressor protein (8,15,16,28,29,59) and the tripartite immunity system of the phage (64) indicate the degree of complexity which P1 faces in regulating and expressing its genetic information.…”

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Bacteriophage P1 gene 10 encodes a trans-activating factor required for late gene expression

1991

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Amber mutants of bacteriophage P1 were used to identify functions involved in late regulation of the P1 lytic growth cycle. A single function has been genetically identified to be involved in activation of the phage-specific late promoter sequence P. In vivo, P1 gene 10 amber mutants fail to trans activate a lacZ operon fusion under the transcriptional control of promoter Ps. Several P1 segments, mapping around position 95 on the P1 chromosome, were cloned into multicopy plasmid vectors. Some of the cloned DNA segments had a deleterious effect on host cells unless they were propagated in a P1 lysogenic background. By deletion and sequence analysis, the harmful effect could be delimited to a 869-bp P1 fragment, containing a 453-bp open reading frame. This open reading frame was shown to be gene 10 by sequencing the amber mutation amlO.1 and by marker rescue experiments with a number of other gene 10 amber mutants. Gene 10 codes for an 18.1-kDa protein showing an unusually high density of charged amino acid residues. No significant homology to sequences present in the EMBL/GenBank data base was found, and the protein contained none of the currently known DNA-binding motifs. An in vivo trans activation assay system, consisting of gene 10 under the transcriptional control of an inducible promoter and a gene SllacZ fusion transcribed from Ps, was used to show that gene 10 is the only phage-encoded function required for late promoter activation.The temperate bacteriophage P1 propagates on several enterobacterial species, including Escherichia coli (64). The linear DNA molecule carried in a phage particle is about 100 kb in size and has a terminal redundancy of 8 to 12% (32, 65). As a prophage, P1 is a low-copy-number plasmid of about 90 kb (3, 33).The genome of P1 is organized in relatively short transcriptional units and in this respect resembles the virulent bacteriophage T4 (43) rather than the temperate lambdoid phages (57). For example, P1 genes for both immunity control and morphogenesis are widely dispersed over the genome (50,62,63). The presence of at least 14 operator sites for the P1 cI repressor protein (8,15,16,28,29,59) and the tripartite immunity system of the phage (64) indicate the degree of complexity which P1 faces in regulating and expressing its genetic information.While the lysogenic condition of P1 has been studied intensively (for a recent review, see reference 64), relatively little is known about the regulation of the lytic growth cycle. A few functions which are under transcriptional control of the P1 cI repressor have been identified (8,10). Among those is the repL function, which is essential for the lytic replication of the phage genome (9,25,52).Recently, a new class of P1 promoters, controlling the late genes encoded by the tail fiber and the dar operons, has been identified (21,22

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“…The virC mutation, which maps upstream from these elements and appears to make expression of at least one of the orf genes constitutive (10), might be considered part of immC. Overexpressed orfprotein is thought to cause the phenotype of P1 virC by acting at the level of Cl function (41) rather than at the level of cl gene expression (10,25).…”

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“…The immI region (coordinates 50 to 52) is responsible for the synthesis and control of a function or functions (ant [34], rebA,B [25]) that antagonize Cl and for P1-P7 heteroimmunity (27). Expression of ant and reb is regulated by the c4 gene.…”

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The bof gene of bacteriophage P1: DNA sequence and evidence for roles in regulation of phage c1 and ref genes

Schaefer

Hays

1990

J Bacteriol

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The C1 repressor of bacteriophage P1 acts via 14 or more distinct operators. This repressor represses its own synthesis as well as the synthesis of other gene products. Previously, mutation of an auxiliary regulatory gene, bof, has been shown to increase expression of some C1-regulated P1 genes (e.g., ref) but to decrease expression of others (e.g., ban). In this study the bof gene was isolated on the basis of its ability to depress stimulation of Escherichia coli chromosomal recombination by the P1 ref gene, if and only if a source of C1 was present. C1 alone, but not Bof alone, was partially effective. The bofDNA sequence encodes an 82-codon reading frame that begins with a TTG codon and includes the sites of the bof-1(Am) mutation and a bof::Tn5 null mutation. Expression of ref::lacZ and cl::lacZ fusion genes was partially repressed in trans by a P1 bof-1 prophage or by plasmid-encoded C1 alone, which was in agreement with effects on Ref-stimulated recombination and with previous indirect evidence for c1 autoregulation. Repression of both fusion genes by plasmid-encoded C1 plus Bof or by a P1 bof+ prophage was more complete. When the C1 source also included a 0.7-kilobase region upstream from C1 which encodes the coi gene, repression of both c1::lacZ and ref::lacZ by C1 alone or by C1 plus Bof was much less effective, as if Coi interfered with C1 repressor function.

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Immunity and Repression in Bacteriophages P1 and P7

Cited by 38 publications

References 51 publications

Cloning, expression, and characterization of the icd gene in the immI operon of bacteriophage P1

Cloning, expression, and characterization of the icd gene in the immI operon of bacteriophage P1

Bacteriophage P1 gene 10 encodes a trans-activating factor required for late gene expression

The bof gene of bacteriophage P1: DNA sequence and evidence for roles in regulation of phage c1 and ref genes

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