Institute of Cell and Molecular Biology, Darwin Building, Mayfield Road, Edinburgh EH9 3JR, Scotland, UK1
Tel: +44 131 650 5374. Fax: +44 131 650 8650. e-mail: noreen.murray{at}ed.ac.uk
Keywords: Restriction and modification, control by proteolysis, DNA transfer, DNA modification, selfish genes
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Background and aims |
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It is often stated, though difficult to prove, that restriction systems exist to defend bacteria against invading phages. Recently, however, it has been argued that R-M systems are selfish elements. This hypothesis emanates from the finding that bacterial cells die if they lose the genes that specify their R-M system (Naito et al., 1995 ). It has been shown that the bacterial chromosome becomes susceptible to restriction as cell growth dilutes the modification enzyme (Handa et al., 2000
). However, while the loss of genes that specify some simple R-M systems leads to cell death, the loss of genes that specify other, more complex, R-M systems causes no detectable viability problem (ONeill et al., 1997
; Kulik & Bickle, 1996
; Makovets et al., 1998
). In this review I wish to emphasize the different behaviour of E. coli strains dependent upon the nature, or type, of their R-M system (see also Murray, 2000
). Some data will challenge our long-established belief that modification of DNA is essential to distinguish whether the DNA is self or foreign. Experiments show that while modification of DNA is sufficient, it is not always essential to identify resident DNA as self (Makovets et al., 1999
; Doronina & Murray, 2001
).
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Types of R-M systems |
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Genes encoding repressor-like proteins, referred to as C proteins for control, have been identified for some type II R-M systems (Ives et al., 1992 ; Tao et al., 1991
; Tao & Blumenthal, 1992
). The C-protein for the BamHI system has been shown to activate efficient expression of the restriction gene (Ives et al., 1992
, 1995
). Consequently, when R-M genes are transferred to a new environment in which there is no C protein, there will be preferential expression of the modification gene, and only after the production of C protein will transcription of the restriction gene be activated.
Type I R-M systems are heterooligomeric complexes that catalyse both restriction and modification (for reviews see Murray, 2000 ; Rao et al., 2000
; Dryden et al., 2001
). AdoMet is the methyl donor for modification but, importantly, endonuclease activity requires both AdoMet and ATP, in addition to Mg2+. The restriction activity of type I R-M systems is associated with the hydrolysis of ATP, an activity that correlates with the bizarre characteristic of these enzymes, that of translocating DNA before they cut it at nonspecific sequences considerable distances from the target sequence (Davies et al., 1999b
). The nucleotide sequences recognized by type I enzymes are asymmetric and comprise two components, one of 3 or 4 bp and the other of 4 or 5 bp, separated by a non-specific spacer of 68 bp. The type I R-M enzyme binds to its target sequence in the presence of cofactors and the alternative activities of restriction or modification are determined by the methylation state of the target sequence. Hemimethylated target sequences are the substrate for modification but, if the target sequence is unmodified, the enzyme, while bound to its target sequence, translocates the DNA from both sides towards itself in an ATP-dependent manner. DNA cleavage occurs when translocation is impeded (Studier & Bandyopadhyay, 1988
; Janscak et al., 1999a
).
The three subunits of a type I R-M system are encoded by closely linked genes: hsdR, hsdM and hsdS. The acronym hsd denotes host specificity of DNA. hsdM and hsdS are transcribed from the same promoter; hsdR is from a separate one (Loenen et al., 1987 ). The two subunits encoded by hsdM and hsdS, colloquially referred to as M and S, are both necessary and sufficient for methyltransferase activity. The third subunit, HsdR or R, is essential only for restriction. The specificity subunit, S, includes two target recognition domains (TRDs) that impart target-sequence specificity to the restriction and modification activities of the complex; the M subunits include the active site for DNA methylation and the R subunits that for nuclease activity. Two complexes are functional in bacterial cells: one comprises all three subunits (R2M2S1) and is an R-M system, and the other lacks R (M2S1) and has only methyltransferase activity (Lautenberger & Linn, 1972
; Suri & Bickle, 1985
; Taylor et al., 1992
).
A separate promoter from which hsdR is transcribed suggests a means for regulating restriction activity, but experiments provide no evidence for the transcriptional regulation of any of those type I R-M systems for which data are available (Kulik & Bickle, 1996 ; Loenen et al., 1987
; Prakash-Cheng et al., 1993
). Evidence is accumulating for the role of post-translational regulation of restriction activity (see section on the mechanism by which restriction activity of EcoKI is controlled).
Type III R-M systems are less complex than type I systems but nevertheless share some similarities with them (see Rao et al., 2000 ). A single heterooligomeric complex catalyses both restriction and modification activities. Modification requires the cofactor AdoMet, and restriction requires Mg2+ and ATP. Recent evidence indicates that type III restriction enzymes can translocate DNA. DNA cleavage is stimulated by collision of the translocating complexes and occurs close to, but on the 3' side of, the target sequence (Meisel et al., 1995
).
The foci of this review lecture are type I R-M systems, their extraordinary capacity for diversification and the acutely sensitive mechanisms for the control of their restriction activity: these mechanisms of control protect unmodified self DNA from attack.
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Distribution of R-M systems |
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Diversification of sequence specificity |
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Long repeated nucleotide sequences remain in the specificity genes of some type I R-M systems as evidence of gene duplication, providing an explanation for the origin of current specificity genes encoding two TRDs (Kannan et al., 1989 ). Early type I R-M systems with the subunit composition R2M2S2 are likely to have recognized hyphenated symmetrical sequences, dictated by the symmetrical arrangement of two specificity subunits. Enzymes of this sort have been generated by deletions that truncate a specificity gene leading to an active enzyme comprising two symmetrically arranged truncated subunits (Abadjieva et al., 1993
; Meister et al., 1993
). Diversification of TRDs has led to the recognition of a variety of target sequences comprising 35 bp but always sequences within which an adenine residue is the substrate for methylation.
The evolution of a type I R-M system with a different specificity (see Fig. 3) was first witnessed by chance in the laboratory (Bullas et al., 1976
) and later shown to be the result of recombination generating a hybrid S gene encoding a new combination of TRDs (Fuller-Pace et al., 1984
). Similarly, a minor change in the length of the spacer sequence connecting the two TRDs was shown to alter the length of the spacer sequence separating the two components of the target sequence (Price et al., 1989
). New combinations of TRDs can be generated experimentally quite readily, but attempts to generate new specificities as the result of changes within a TRD have been unsuccessful. The majority of many amino acid substitutions made within a TRD of EcoKI do not impair specificity (ONeill et al., 2001
). It seems likely that more than one amino acid substitution is necessary to change the specificity of a TRD. Even for type II R-M systems for which the structures of enzymes bound to their target sequences have been determined, it has not been possible to predict amino acid changes that lead to a new specificity. To date, BamHI has been changed so that it prefers a methylated substrate (Dorner et al., 1999
) and EcoRV has been engineered so that its preferred target sequence is 8 rather than 6 bp (Lanio et al., 2000
).
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The immigration control region and the family concept |
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It seems likely that all type I R-M systems derive from a common ancestor (Sharp et al., 1992 ), but systems allocated to different families are now so dissimilar that little evidence of homology remains at the level of gene sequences. One interesting exception is the 5' part of the specificity genes of StyLTIII (type IA) and EcoAI or EcoEI (type IB); these specify a TRD that recognizes the same trinucleotide target sequence (Table 2
). An examination of the target sequences of the type I R-M systems (see Table 2
) indicates that the evolution of different families of enzymes has enhanced the scope for diversification by varying the distance between those adenine residues within the target sequences that are the substrates for methylation. In the target sequences for members of the IB family, the adenine residues are separated by 9 bp, in the IA family by 8 bp, in the IC family by 7 or 8 bp and in type ID by only 6 bp; the variability in the IC family is dependent on whether a tetrapeptide sequence (TAEL) within the central conserved region is present in duplicate or in triplicate. The importance of the correct spacing between the adenine residues is illustrated by the target sequences for EcoRI24I
and EcoDXXI
(see Table 2
). These are the systems that comprise symmetrically arranged truncated S polypeptides and their target sequences require an additional base pair in the spacer to maintain the distance between the adenine residues.
In summary, diversity of specificity in type I systems, where two TRDs are present within the specificity subunit, not only depends on diversification of TRDs but is enhanced by different spacing between the TRDs and new combinations of TRDs.
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Is restriction an effective barrier to the acquisition of foreign DNA? |
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The modification of DNA by glucosylation, as in T-even phages, is effective against most restriction systems, while proteins that interfere with the activity of the enzyme may be specific to one enzyme, or one type of system. Phage T5 can inhibit the activity of EcoRI (Davison & Brunel, 1979 ) and a variety of host enzymes that modify DNA (see McCorquodale & Warner, 1988
), but most of the anti-restriction functions currently identified are directed against type I systems. It seems unlikely that this bias towards functions that protect against type I systems simply reflects the fact that most work has been done with E. coli K-12 and E. coli B; E. coli strains specifying EcoRI have been in common laboratory use for 30 years. The bias could reflect the prevalence of type I systems in natural strains of E. coli enhanced by the fact that some feature common to type I R-M systems, or the conformation of their DNA substrates, permits the evolution of anti-restriction proteins that are able to combat all members of one family or even the members of different families of type I R-M systems.
The 0.3 gene products of phages T3 and T7 are the only anti-restriction functions available in significant quantities for detailed molecular analyses. These proteins, sometimes referred to as Ocr (overcoming classical restriction), bind to type I restriction complexes, both the R-M complex and the modification enzyme, and prevent them from binding to DNA (Atanasiu et al., 2001 ). The T3 product also destroys the cofactor AdoMet. It has been suggested that the 0.3 gene product, or Ocr, mimics the DNA substrate, thereby neutralizing the R-M complexes (Bandyopadhyay et al., 1985
). Recent evidence based on the structure of Ocr supports this model: the protein is an elongated dimer that reflects both the size and shape of a bent DNA molecule (Atanasiu et al., 2001
; M. Walkinshaw & D. Dryden, personal communication). An alternative proposal for the Ard (alleviation of restriction of DNA) proteins of conjugative plasmids, based on their acidic nature, is that an acidic surface mimics sequences of the specificity subunits of type I systems and the Ard proteins can displace the specificity subunit from the active R-M complex (Belogurov & Delver, 1995
). Both the 0.3 gene product (C. Atanasiu & D. Dryden, personal communication) and ArdA (Read et al., 1992
) are active against members of different families of type I R-M enzymes.
The efficacy of anti-restriction functions poses the critical question of how a protein specified by the unmodified DNA of a transmissible agent is able to act before the sequence that encodes it is attacked by the restriction enzyme. Bacteriophage P1 solves the problem by co-transfer of the protein with its DNA. In contrast, the 0.3 genes of T3 and T7 are transcribed early, prior to the internalization of the remainder of the genome. The ard genes of transmissible plasmids, like the 0.3 gene of T3 or T7, are located in the leading end of the DNA, but for conjugative plasmids it is single-stranded DNA that is transferred (5' to 3'). Current evidence for IncI1 and ColIb supports a regulatory model in which the genes in the leading region of the DNA are transcribed from special promoters recognized within secondary structures of single-stranded DNA (Bates et al., 1999 ). This allows transcription of ard genes and the accumulation of anti-restriction protein before the transferred strand is converted into duplex DNA (see Fig. 5
).
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Conserved sequences and active sites in type I R-M systems |
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The R subunits are essential for restriction but not modification. A type I R subunit includes motifs characteristic of ATP-binding proteins (Loenen et al., 1987 ), consistent with the ATP-dependence of restriction. In addition, they include conserved sequences indicating the presence of motifs characteristic of ATP-dependent helicases (Gorbalenya & Koonin, 1991
; Murray et al., 1993
; Titheradge et al., 1996
). It has been suggested that these motifs, the DEAD-box motifs, define an engine that powers DNA translocation (Hall & Matson, 1999
). Analyses of mutations in the hsdR gene of E. coli K-12 (Fig. 6
) demonstrated that each of the seven DEAD-box motifs of EcoKI is essential for a restriction-proficient phenotype and for the DNA-dependent ATPase activity of the enzyme (Davies et al., 1998
, 1999a
). Of special relevance was the finding that these restriction-deficient mutants lack DNA translocation activity (Davies et al., 1999a
). This activity was assayed by monitoring the EcoKI-dependent transfer of the T7 genome from the phage capsid to the bacterial cell (Fig. 7
), an assay that relies on the inhibition of RNA polymerase activity, the normal means of DNA transfer, and the presence within the leading region of the T7 genome of a single target for EcoKI (Garcia & Molineux, 1999
). The EcoKI complex bound to the unmodified EcoKI target can mobilize the 39 kb of T7 DNA at the rate of
100 bp s-1.
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Mechanism of action of type I restriction enzymes |
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The in vivo and in vitro consequences of mutations in the hsdR gene of E. coli K-12 separate the restriction pathway into a series of steps in which AdoMet and ATP are required as cofactors for specific binding to the target sequence, while ATP hydrolysis is essential for the DNA translocation that precedes the eventual breakage of phosphodiester bonds in a Mg2+-dependent reaction (Fig. 9). Known mutations in hsdR apparently fail to prevent the binding of ATP and they block either the second or the third step in the pathway. AdoMet binds to the M rather than the R subunit; a substitution in motif I of the M subunit of EcoKI, which prevents the binding of AdoMet (Willcock et al., 1994
), results in an enzyme incapable of either modification or restriction (Doronina & Murray, 2001
). This defect is consistent with the predicted block in the first step of the restriction pathway. In contrast, a substitution in motif IV, which blocks methyltransferase activity but has little effect on the binding of AdoMet, leaves a complex able to translocate and break DNA. The expected consequence of this mutation in vivo would be fragmentation of the bacterial chromosome. However, recent experiments contradict this expectation (Makovets et al., 1999
; Doronina & Murray, 2001
; Cromie & Leach, 2001
). It would appear that when modification fails, the bacterial cell is endowed with the means of causing the restriction pathway to abort before the enzymes break the DNA. This effective control of the restriction activity of type I complexes is in stark contrast to the cell death that follows the concomitant loss of the genes that encode type II R-M system.
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Guarding the bacterial chromosome against DNA breakage |
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The early experiments of Bertani & Weigle (1953) showed that the restriction proficiency of E. coli K-12 was alleviated following UV irradiation. Many experiments now document this phenomenon for type I systems, but not, so far, for any type II system. A similar response has been demonstrated for a variety of agents that damage DNA, including mutagens such as the base analogue 2-aminopurine (2-AP), and defects in some genes that affect DNA metabolism, e.g. dam, topA and mutD (dnaQ) (Efimova et al., 1988a
, b
; Thoms & Wackernagel, 1984
; Makovets et al., 1999
). DNA damage may generate unmodified target sequences as a consequence of the repair of double-strand breaks by homologous recombination (see Fig. 10
), or directly by mutations that create target sequences. The original genetic evidence for the creation of vulnerable target sequences by mutation (Makovets et al., 1999
) is now supported by the demonstration of breaks in the bacterial chromosome when E. coli K-12 is treated with 2-AP. The breaks are dependent on EcoKI and, as predicted if they arise by base substitutions, their generation requires two rounds of replication (Cromie & Leach, 2001
).
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Finally, in the context of the generation of new specificities, it seems likely that the evolution of a TRD that recognizes a different nucleotide sequence will require a series of amino acid changes, some of which may initially impair the efficiency of modification. Our recent experiments show that even a modest drop in modification activity, one so small that the mutant strain still scores as modification proficient, elicits the modulation of restriction activity and this modulation is essential for the bacterium to survive (ONeill et al., 2001 ). In this case a mutation in hsdS is associated with a restriction-deficient, modification-proficient phenotype!
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ClpX and ClpP are needed to modulate the restriction activity of some type I R-M systems |
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The mechanism by which the restriction activity of EcoKI is controlled |
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The role of ClpXP in the alleviation of restriction has been demonstrated for EcoAI (type IB) as well as for EcoKI (type IA). Members of the IC and ID families are also susceptible to restriction alleviation, but this may be dependent on an alternative mechanism (Makovets & Murray, unpublished observations).
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The effect of restriction on the acquisition of foreign DNA |
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DNA molecules with ends are notoriously sensitive to degradation in E. coli; linear DNA fragments are degraded by a process dependent upon the ExoV activity of RecBCD (Simmon & Lederberg, 1972 ; see Telander-Muskavitch & Linn, 1981
, for a review), the enzyme that catalyses an essential step in the major pathway of recombination in this bacterium. The degradation of
fragments by ExoV prevents detectable expression of those genes that are normally transcribed immediately after infection (Pilarski & Egan, 1973
; Brammar et al., 1974
). This implies an apparent conflict, or competition, between the alternative roles of RecBCD of either degrading the DNA fragments produced by a restriction system or rescuing them by recombination. Many experiments have shown that the DNA ends generated by cutting with EcoRI can serve to stimulate recombination, but these experiments often rely on recombination by alternative pathways under conditions in which DNA breakdown by the RecBCD nuclease is prevented (see, for example, Thaler et al., 1987
; Eddy & Gold, 1992
). Of more general relevance are experiments in which it was shown that DNA breakage by a type II restriction enzyme can stimulate RecBCD-mediated recombination in the presence of the nucleolytic activity of the wild-type enzyme (Stahl et al., 1983
). In these experiments the recombination activity of RecBCD was assayed with a substrate that includes Chi, a specific nucleotide sequence of eight bases shown to be a hot-spot for RecBCD-dependent recombination (see, for example, Kowalczykowski et al., 1994
; Myers & Stahl, 1994
; Smith et al., 1995
; Kuzminov, 1999
; Smith, 2001
, for reviews). RecBCD enters a DNA molecule at an end. Genetic (Stahl et al., 1980
) and biochemical (Taylor et al., 1985
) evidence indicate that the Chi sequence must be oriented in the appropriate direction with respect to the approaching RecBCD enzyme, if it is to stimulate recombination. In vitro, the degradative behaviour of RecBCD prior to an encounter with a Chi sequence is dependent upon the relative concentrations of Mg2+ and ATP (Ponticelli et al., 1985
; Dixon & Kowalzcykowski, 1993
). Hence, models for the mode of action of RecBCD in vivo differ; in one model both strands of DNA are degraded in the absence of a Chi sequence (see Myers & Stahl, 1994
; Smith, 2001
, for discussions of the models). It is, however, generally agreed that the presence of Chi sites can impair the exonuclease activity of RecBCD and that this protective effect can be revealed in trans (Dabert et al., 1992
; Kuzminov et al., 1994
; Myers et al., 1995
; Köppen et al., 1995
; Taylor & Smith, 1999
). A loss of ExoV activity in E. coli following the fragmentation of DNA that contains frequent Chi sites is consistent with the inactivation, or sequestration, of the RecD subunit (Köppen et al., 1995
). In vitro, the RecBCD enzyme can disassemble into subunits following its encounter with a Chi sequence (Taylor & Smith, 1999
).
In the chromosome of E. coli K-12, there is one Chi sequence per 4·6 kb (Blattner et al., 1997 ), roughly seven times more often than expected from a random association of nucleotides within the genome and 4- to 14-fold higher than in the DNA of seven non-enteric bacteria whose complete nucleotide sequences were analysed (Colbert et al., 1998
). The frequency of Chi sequences is influenced by codon usage (Biaudet et al., 1998
; Colbert et al., 1998
). Chi sequences are predominantly within ORFs and predominantly oriented so that they will protect DNA from degradation should this proceed towards the origin of replication (Burland et al., 1993
; Kuzminov et al., 1994
; Blattner et al., 1997
). The RecBCD enzyme of all enteric bacteria that have been tested uses the Chi sequence of E. coli K-12 (see Colbert et al., 1998
). Other groups of related bacteria may have a functionally equivalent system in which the enzyme recognizes a different nucleotide sequence (Chedin et al., 2000
). Chi, or an analogue, is likely to enhance the rescue of DNA from closely related bacteria. Even so, sequence divergence between members of close genera, e.g. Escherichia and Salmonella, can be sufficient to significantly limit genetic exchange (Matic et al., 1996
). DNA fragments provoked by the R-M systems found within the same bacterial species are likely to be salvaged more efficiently than those generated within a bacterium from another genus, primarily because of sequence similarity, but aided perhaps by high frequencies of Chi sequences. These sequences, or their equivalents, should serve to stimulate recombination and, if present in abundance within the fragmented DNA, could convert a cell into an ExoV-deficient phenocopy that remains recombination proficient.
Some phages (e.g. T7 and P1) and many conjugative plasmids, as already mentioned, encode proteins that antagonize R-M systems. The F factor of E. coli, however, appears to lack an anti-restriction gene, and chromosomal DNA acquired by courtesy of an F factor is susceptible to restriction. DNA breakage reduces the linkage between markers transferred during conjugation (Pittard, 1964 ).
R-M systems seem likely to affect the flux of genetic information. DNA breakage followed by exonuclease activity may enhance the opportunity for the acquisition, and retention, of advantageous coding sequences in the absence of neighbouring deleterious ones (Milkman et al., 1999 ). This modulation of DNA transfer seems unlikely to provide the selective force for the allelic diversity detected for type I R-M systems in one species of enteric bacteria.
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Questions concerning the biological relevance of R-M systems |
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Two obvious questions arise about the mechanism and relevance of the alleviation of restriction by type I R-M systems. First, how are unmodified sequences in the resident bacterial chromosome distinguished from those in DNA that has recently entered the bacterial cell? Second, why do some, perhaps all, type I R-M systems have such elegant and sensitive mechanisms to control their activity and prevent cell death, while the genes for type II systems are apparently maintained by their failure to control endonuclease activity?
The translocation step in the complex restriction pathway of a type I system extends the opportunity for the bacterial proteins to counter-attack an R-M complex active on the resident chromosome. Perhaps the answer to the first question is simply that the translocation process on the resident chromosome is hindered by the nature of the bacterial nucleoid and this in turn increases the opportunity for recognition by the ClpXP protease, or any alternative control system.
Experiments in vivo, using phage DNA substrates for restriction by EcoKI (Brammar et al., 1974 ; Garcia & Molineux, 1999
), support the model (Studier & Bandyopadhyay, 1988
) in which cutting occurs between two target sequences when the translocating complexes collide. It is not known whether any feature of the structure or organization of the nucleoid, or any process such as DNA replication, would either reduce the speed of DNA translocation, or alternatively halt translocation and stimulate endonuclease activity. EcoKI is very effective at displacing a repressor bound to its target sequence (Dreier et al., 1996
). Therefore, collision with a protein that has a high affinity for its target sequence neither prevents translocation nor stimulates DNA breakage. In vitro, a fixed Holliday junction has been shown to stimulate cutting. Therefore one protein complex is sufficient to break the phosphodiester bonds in both strands of the duplex (Taylor & Smith 1990
; Janscak et al., 1999a
).
It is difficult to speculate about the fragmentation of the bacterial chromosome by type I R-M systems without knowing whether any events in vivo, other than the collision between translocating complexes, trigger DNA breakage. The spacing between unmodified target sequences is not obviously relevant. In some instances, as in response to treatment with 2-AP, ClpXP-dependent alleviation of restriction occurs when relatively few targets are unmodified while in others, such as the acquisition of R-M genes or the presence of a modification-deficient EcoKI complex, all or most of the genomic target sequences will be exposed. The only modification-deficient complex studied in vitro does, however, act more slowly than the wild-type enzyme (Doronina & Murray, 2001 ).
The behaviour of recipient bacteria following conjugation could be interpreted as support for a distinction between the nucleoid and other DNA. Unmodified DNA entering the cell by conjugation is recognized as foreign and attacked, but within 40 min of the time of entry restriction, assessed by infection with unmodified , is alleviated (Glover & Colson, 1965
). This alleviation of restriction was found to be ClpXP-dependent, and was not detected in a recA recipient (Doronina & Murray, unpublished observations). These observations are explained if fragmented donor DNA must be incorporated into the resident chromosome by recombination before unmodified DNA is identified as self, and can evoke the ClpXP-dependent alleviation of restriction. Alternatively, RecA protein itself could be necessary for activation of the alleviation pathway. RecA is necessary for the alleviation of restriction in response to UV irradiation (Thoms & Wackernagel, 1984
; Salaj-
mic et al., 1997
) but it is not necessary for the alleviation of restriction in response to treatment with 2-AP (Makovets et al., 1999
).
The mechanism of distinction between unmodified self and unmodified foreign DNA should be susceptible to analysis. However, the biological relevance of the distinctly different behaviours of type I and type II R-M systems may be more difficult to determine: the differences caution against generalized speculations for the evolutionary strategies of R-M systems.
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ACKNOWLEDGEMENTS |
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2001 Fred Griffith Review Lecture (Delivered at the 148th Meeting of the Society for General Microbiology, 27 March 2001)
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