*Corresponding authors. Mailing address for Bénédicte Michel: CNRS, Centre de Génétique Moléculaire, UPR3404, Gif-sur-Yvette F-91198, France. Phone: 33 1 69 82 32 29, Fax: 33 1 69 82 31 40, E-mail:
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. Mailing address for David Leach: Institute of Cell Biology, School of Biological Sciences, University of Edinburgh, King's Buildings, Edinburgh EH9 3JR, United Kingdom. Phone: 44 131 650 8650, Fax: 44 131 650 6556, E-mail:
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.
The study of genetics has three requirements: first, the existence of mutants; second, a method to segregate (and eventually to map) mutations; and third, a method to combine multiple mutations in individuals. These requirements for the study of genetics imply mechanisms for bringing genomes of individuals together in single cells and recombination to segregate and combine mutations. These are features readily available in eukaryotic organisms with a sexual life cycle. Initially, Gregor Mendel established the rules of genetic segregation, using peas, and Bateson realized that there were two types of “re-combination”: the “re-combination” that occurs through independent assortment of alleles on different chromosomes and the occasional recombination of alleles in “genetic coupling,” or linkage, as we would now call it (26). Bacteria lagged a long way behind. It was not until auxotrophic mutations were discovered (137) and it was shown that different strains of bacteria could “mate” and produce recombinant offspring (220) that the genetics of bacteria can truly be said to have started. Lederberg's observation of bacterial mating is now understood in terms of integration of the F plasmid at sites of IS sequences in the Escherichia coli chromosome and using its conjugational transfer machinery to transfer sections of the host chromosome. Following his discovery of conjugation, Lederberg went on to show that gene transfer could also be mediated by bacteriophages via the mechanism known as generalized transduction (482). In addition to these two mechanisms, some bacteria are naturally competent for the uptake of DNA and can accomplish gene transfer by transformation (139).
The mechanisms of gene transfer in bacteria are different from the sexual life cycles of eukaryotes in that the genetic contributions of the two parents in a cross are unequal in bacteria. The donor provides a short region of DNA, whereas the recipient provides an entire chromosome. Furthermore, the chromosomes of bacteria such as E. coli and Salmonella enterica serovar Typhimurium are circular. This means that linear DNA introduced from a donor is required to undergo at least two crossover events with a recipient chromosome to be incorporated into a viable product (Fig. 1).
Recombination provides the very important role in evolution of “shuffling the pack” of genes in a species. Beneficial genes can be combined and deleterious genes separated by recombination, generating fitter genomes upon which natural selection can operate. Furthermore, recombinational events between the genomes of different bacterial “species” can contribute to the horizontal transfer of genes and genomic regions. However, barriers to genetic exchange between species have evolved to limit this mixing, and genetic divergence itself provides one important such barrier through the action of mismatch repair, as exemplified by its inhibition of recombination between the genomes of species such as Escherichia coli and S. enterica serovar Typhimurium (328).
Conjugation provided the assay for isolation of the first recombination-defective mutant of bacteria and thus opened up the study of the genes and proteins implicated in mediating recombination (60). The gene identified by this first recombination-defective mutant was denoted recA and has proved to encode the prototype recombinase centrally implicated in homologous recombination in organisms as diverse as bacteriophage T4 and humans. Interestingly, the recA mutant was shown to be not only defective in genetic recombination but also highly sensitive to UV irradiation, establishing a central connection between recombination and DNA repair. This led to isolation of two more UV-sensitive mutants in genes that were also centrally implicated in recombination, recB and recC (107, 108, 458).
The observation of gene conversion in fungi led to early proposals that recombination might be mediated by copying first one chromosome and then another (copy choice). However, understanding that replication was semiconservative made copy choice models of recombination difficult to understand from a mechanistic perspective, and models of break-join recombination, spearheaded by the Holliday model (165), came to dominate thinking. In a set of classic experiments, it was demonstrated that bacteriophage λ recombination could be accomplished either by break-join or break-copy mechanisms (396). However, the importance of meiotic recombination in the development of recombination models further reinforced the idea that recombination was primarily a break-join reaction. Despite this, it was clear that recombination was intimately associated with replication in the life cycles of bacteriophages lambda and T4 (219, 396). The intimate association of recombination with replication, even for the bacterial chromosome, became clear when it was observed that conjugational and transductional recombination required the function of PriA, a gene product implicated in the reestablishment of DNA replication by loading the replicative helicase DnaB to replication forks (193, 353). It is now generally accepted that DNA end-mediated recombination in E. coli proceeds via the setting up of replication forks as shown in Fig. 2. In this figure, we distinguish between ends-in, ends-out, and one-ended recombination events initiated at DNA breaks. Ends-out recombination is exemplified by conjugation and transduction, while ends-in recombination occurs at sites of DNA double-strand breaks (DSBs), and one-ended recombination occurs when replication forks break, for example by running into nicks, or are reversed (see "Roles of RecBCD in DNA replication," below).
The concept of recombination pathways was premature at the time it was proposed. However, it is beginning to make more sense now as progress is made in understanding the biochemical activities of the proteins involved. The first pathway to be investigated was that requiring the recA, recB, and recC genes that operate at DNA ends (see "RecBCD and the initiation of recombination at DNA double-strand ends," below).
It became clear that there was more than one way to mediate recombination when suppressors of the recombination deficiency of recBC mutants were isolated. The first of these suppressors was denoted sbcA (24), a mutation in the cryptic rac prophage activating the recE and recT genes analogous to the redα and redβ genes of bacteriophage λ (62, 150, 211). These phage-encoded systems are now widely used for recombineering in bacteria; for recent reviews, see reference 359 and Chapter Bacteriophage λ Recombination and Recombineering. The second suppressor was denoted sbcB; the corresponding gene encodes the enzyme exonuclease I (168, 210). However, the story is more complicated in that a recBC sbcB mutant is barely alive and accumulates mutations in the sbcC gene that significantly improve viability (230). This gene encodes one of the subunits of the SbcCD nuclease (65, 134). Recombination in a recBC sbcB sbcC mutant is mediated by a set of genes including recA, recJ, recF, recN, recO, recQ, and recR (reviewed in reference 61). Subsequently, the recA, recF, recO, recR, and recJ genes were found to be defective for recombination between circular plasmids and define a pathway of recombination that can operate at single-strand gaps (63, 195).
Robin Holliday proposed that recombination would proceed via the formation and resolution by cleavage of a 4-way junction now known as the Holliday junction (165). It was satisfying to discover that E. coli did indeed encode a protein complex capable of resolving Holliday junctions by cleavage. This complex of three enzymes, denoted RuvABC, is capable of branch migrating and cleaving 4-way junctions as predicted (reviewed in reference 450). However, in many recombination assays (e.g., conjugation and transduction) ruvA, ruvB, or ruvC mutants are only modestly recombination defective because another protein, RecG, permits resolution of Holliday junctions in the absence of RuvABC (238). recG encodes a helicase that can also migrate Holliday junctions but is not known to work with a nuclease except in the unusual situation of a rusA mutant where a bacteriophage enzyme capable of cleaving Holliday junctions is activated (reviewed in reference 49). Thus, RuvABC and RecG define alternative mechanisms for the resolution of Holliday junctions (see "RuvABC—branch migration, resolution of Holliday junctions, and replication fork reversal" and "RecG, a helicase implicated in resolving recombination intermediates," below).
In summary we can define two general pathways of recombination that are intrinsically bacterial (i.e., are not of bacteriophage origin). One pathway operates at DNA DSBs and utilizes RecBCD followed by RecA and either RuvABC or RecG (Fig. 2). The other operates at single-stranded regions not associated with DSBs and utilizes RecF, RecO, and RecR, followed by RecA and either RuvABC or RecG (Fig. 3). This is an oversimplified summary, and in the following sections we will explore these pathways in more detail. However, it provides a useful conceptual framework within which to place further details of mechanism.
RecA is central to all homologous recombination reactions (excluding those of bacteriophage origin). It is highly conserved in bacteria and has homologues in all kingdoms of life: Rad51 and Dmc1 in eukaryotes and RadA in archaea. The active form of RecA is a filament of proteins bound to single-strand DNA (ssDNA) (Fig. 4). During homologous recombination, the RecA filament catalyzes homology search, strand exchange, and branch migration of the resulting strand exchange point. The second main role of the RecA-ssDNA filament is its action as a regulator. It interacts with various proteins and promotes their proteolysis, which activates or inactivates them (UmuD, one of the two subunits of the bypass polymerase Pol V, is activated by cleavage, whereas the repressor of the SOS response LexA and phage repressors are inactivated). Finally, the RecA filament directly facilitates replication across lesions by interacting with the UmuD′2C (Pol V) polymerase at the site of lesion, and it is essential for the recovery of replication in UV-irradiated cells. Several proteins control RecA activity, either by promoting or by limiting it (Table 1). For recent reviews on RecA, see references 28, 74, 75, 102, 128, 208, 215, and 272.
RecA protein is a 352-amino-acid polypeptide with a molecular mass of about 38 kDa. Under certain incubation conditions, RecA assembles as hexameric rings (476), but the active form is the RecA-ssDNA filament. In vitro, RecA protomers preferentially assemble at the 3′ ends of filaments and disassemble from the 5′ ends; a higher rate of binding results in increased filament size (180, 227). The simplest reaction catalyzed by RecA filaments in vitro is D-loop formation or strand invasion (Fig. 5A). The strand exchange reaction is reconstituted in vitro by incubating RecA-coated ssDNA in the presence of homologous double-stranded DNA (dsDNA), and it can be quantified by measuring the formation of intermediate molecules and products (Fig. 5B). In addition to this three-strand reaction, RecA can catalyze a four-strand reaction initiated at a single-strand gap (Fig. 5C). These reactions require SSB (single-stranded DNA [ssDNA] binding protein) to undo secondary structures in ssDNA. A first set of information on the structure of the RecA filament was deduced from electron microscopy (100, 101). RecA forms a right-handed helical filament on ssDNA with three nucleotides per RecA protomer and six RecA protomers per helical turn. In the active form of the filament, the ssDNA is inside the filament and is 50% extended compared to the B-form dsDNA. Electron microscopy showed the existence of two kinds of filaments, i.e., one that is inactive in the absence of nucleotide cofactor or in the presence of ADP and one that is active in the presence of ATP. These two types of filament differ by the pitch, i.e., the distance between helical turns (68 Å versus 92 Å). More recent methods for imaging electron micrographs have provided insight into the conversion of inactive to active form of the RecA filament (426). The RecA protein was crystallized in 1992 in the inactive form, allowing the recognition of several important domains (402). The N-terminal domain of RecA interacts with the neighboring subunit in the filament. The central region (residues 34 to 269) is the nucleotide- and DNA-binding core. It comprises a central Beta-sheet and associated alpha-helices, which turned out to be conserved beyond RecA homologues in many ATP-binding proteins including helicases (99). The core domain contains the binding sites for ATP and ADP and the catalytic elements used for ATP hydrolysis. Two loops, which were disordered in the original structure, were identified by mutagenesis as important for strand exchange: loop 1 (L1, amino acids 157 to 164) and loop 2 (L2, amino acids 195 to 209). Two different DNA binding sites were defined in RecA: the “primary” site, which binds ssDNA, and the “secondary” DNA-binding site, which interacts with the incoming dsDNA. Results of biochemical studies were not always consistent in the attribution of L1 and L2 to these primary and secondary binding sites, but all concluded that these loops are crucial for RecA-DNA interactions (262, 286, 445). The C-terminal domain is located on the outer surface of the filament, and the very last residues (residues 329 to 352) form a disordered, negatively charged, C-terminal tail, which is an important element of control of RecA filament activities (103, 249, 251).
The question of precisely how strand exchange is achieved remained unanswered until recently, when Chen et al. determined the structure of the substrate (RecA filament on ssDNA) and of the product (RecA filament on dsDNA) of the reaction (57; see also comment in reference 208). The key point is the observation that the DNA is not uniformly extended within the filament. Sets of three nucleotides distant by 3.5 to 4.2 Å (as in normal B-form DNA) are separated by long internucleotide stretches of 7.8 Å. Pairing between a nucleotide triplet in the RecA filament and a complementary triplet in the dsDNA is facilitated by the fact that they both have approximately the same B-form dimensions. Each nucleotide triplet mainly interacts with one RecA molecule and also with the following and the previous RecA protomers in the filament. Conversely, each RecA protomer binds a nucleotide triplet and one nucleotide of each of the adjacent triplets. The L1 and L2 loops are now ordered, and both interact with ssDNA. Each ssDNA triplet is sandwiched between two L2 hairpins and also interacts with L1, in agreement with previous data showing that both loops are a crucial component of the primary DNA binding site. In the dsDNA-RecA complex, a structure made of B-form base pair triplets separated by stretched regions is maintained. Some amino acids in the L1 loop stabilize the intertriplet interactions, in agreement with L1 being an important component of the secondary (dsDNA) binding site. Nevertheless, the incoming DNA strand makes few contacts with the protein, ensuring that Watson-Crick base pairing is the key determinant of the stability of interaction between the filament and the strand coming from the dsDNA.
Single-molecule experiments were used to study the formation of RecA filaments in vitro (124, 129, 180; for a review, see reference 102). ssDNA-RecA and dsDNA-RecA filaments are initiated by several independent events of nucleation of five RecA molecules, followed by a binding of additional protomers on both sides. The initial protofilament grows at both ends, but binding is more efficient and cooperative on the 3′ side, resulting in a directional bias of RecA polymerization in the 5′-to-3′ direction on DNA. In vivo, RecA binds to SSB-covered ssDNA, with the help of presynaptic mediator proteins. Single-molecule studies of SSB in the presence of RecA showed that SSB protein diffuses on ssDNA, which stimulates RecA filament elongation by transiently removing DNA secondary structures, and that RecA filament elongation in turn directionally biases SSB diffusion (341, 480).
Nonhydrolyzable ATP analogues and RecA mutants impaired for ATP hydrolysis were used to investigate the role of ATP hydrolysis in RecA action. ATP binding but not ATP hydrolysis is required for initial RecA binding to DNA, for filament extension, for strand invasion (D-loop formation), and for nondirectional strand exchange. ATP hydrolysis is required for filament disassembly, for strand exchange to be unidirectional in the 5′-to-3′ direction relative the strand first bound by RecA, and for strand exchange to travel through DNA lesions and nonhomologous DNA (178, 191, 366); it also strongly improves the efficiency of long strand exchange reactions (see references 178 and 338 and references therein). Finally, ATP hydrolysis allows four-strand exchange reactions: when strand exchange is initiated at an ssDNA gap, it allows the reaction to proceed into the dsDNA that flanks the gap (190, 365) (Fig. 5). The mode of action of ATP in the strand exchange reaction has been the subject of numerous studies and is still debated. In the RecA-DNA structure, ATP binds at the RecA-RecA interface, accounting for the observation that ATP hydrolysis destabilizes the RecA-RecA interface. It was proposed that the functions that require ATP hydrolysis are all related to this destabilization, which promotes the recycling of RecA molecules within the filament (278, 331). An alternative model, in which ATP hydrolysis is a driving force that promotes strand exchange by fueling a rotation of DNA relative to RecA in the filament, has been proposed (73, 75, 364).
From 8,000 to 10,000 RecA molecules are present per cell, increasing to about 72,000 after SOS induction (46, 356). RecA can assemble in vivo on ssDNA only with the help of presynaptic proteins, required to destabilize SSB bound to DNA. The resulting RecA filament encounters a homologous sequence and is channeled to recombination, or it persists, lengthens, and induces the SOS response. In vivo, the minimal homology required for RecA-mediated recombination or MEPS (minimum efficient processing segment) is 20 to 30 base pairs (376, 447), whereas longer filaments are required for SOS induction (144). A recA null mutant is hypersensitive to all DNA-damaging agents tested so far and is killed by only one chromosome DSB (117, 209, 302, 303, 390). Because of spontaneously occurring DNA damage in otherwise wild-type cells, the recA mutant has a decreased viability compared to the wild type (about 50% of cells in a growing cultures are unable to form a colony, i.e., to propagate for about 20 generations [56]). recA null mutants suffer extensive DNA degradation because unrepaired broken chromosomes are degraded by the exonuclease V action of RecBCD (see section 3) (383).
Mutants that require RecA for viability belong to several classes. Notably, all require RecBC and RuvABC, the enzymes responsible for the pre- and postsynaptic steps of DNA DSB repair, respectively, indicating that RecA is needed essentially for DSB repair. This observation is in agreement with the idea that DNA single-strand gaps can be repaired by means other than homologous recombination, such as gap filling by DNA synthesis, whereas DNA DSBs can be repaired only by homologous recombination. The first E. coli mutants shown to require RecA for viability were mutants that accumulate DNA single-strand interruptions (nicks or gaps) during growth. In these mutants, DNA single-strand breaks are converted into DNA double-strand ends by replication runoff (replication fork collapse, Fig. 6D). This model accounts for the RecA requirement of mutants deficient for Okazaki fragment maturation (ligase [lig] and polymerase I [polA]) (reviewed in reference 213). It is also proposed in mutant cells deficient for the sanitizing of the nucleotide pools: actually, abnormal nucleotides in excess incorporate into the chromosome, and their excision leads to the production of nicks that are then converted by replication into DNA double-stranded ends. The best characterized are the rdgB mutant, deficient for a dITPase (48, 248), and the dut mutant deficient for a dUTPase (202, 203, 204). Double-stranded ends are also formed by replication runoff when a second round of replication runs into downstream forks. This reaction was first observed when the downstream replication fork was stopped by a replication terminator site (39, 40, 109) (replication fork collision [Fig. 6E]), and it also occurs upon overinitiation at the replication origin (301). Finally, certain classes of recombination-dependent mutants suffer DSBs formed independently of replication. RecA is thus essential in mutants deficient for the repair or the prevention of oxidative damage (205), in certain metabolic mutants (378), when chromosome segregation is affected (205, 340), and in cells lacking the Dam protein, which directs mismatch repair to the newly synthesized strand (264).
RecA plays at least four roles in UV-irradiated cells. First, by catalyzing RecFOR-dependent homologous recombination, it converts lesions present on ssDNA gaps into dsDNA, which renders them accessible to the nucleotide excision repair complex UvrABC (NER). Second, RecA is essential for the induction of the SOS response and hence for increased production of NER enzymes and all bypass polymerases. The third and fourth roles of RecA correspond to its action at replication blockage sites to promote replication of UV-irradiated cells.
As mentioned above, the RecA filament contacts the LexA repressor and promotes its autocleavage, which induces the SOS response. The site of interaction with LexA within the RecA filament has been deduced from numerous genetic studies (reviewed in reference 272). In addition, electron microscopy analyses of RecA/DNA/LexA complexes have defined two regions of the RecA filament important for LexA cleavage, one within the helical filament groove and one around L1 (427, 475). Genes that belong to the SOS regulon carry one or several LexA-binding boxes in their promoter regions (68, 112, 189, 437). There are more than 40 SOS-induced genes, most of them encoding functions required for lesion repair (see Chapter The SOS Regulatory Network and Chapter The SOS Response). Several SOS-induced proteins are still of unknown function. The number of LexA boxes and the sequence of these boxes vary between different SOS genes, so that certain genes with few or weak boxes are derepressed more rapidly after SOS induction (for example NER genes), while others like umuC and umuD, which encode the components of the bypass polymerase Pol V, are fully induced at a later time (68). In addition, cytological techniques revealed that in vivo SOS induction in response to UV irradiation is an oscillatory process in individual cells (119). SOS induction is dependent on RecFOR when the lesion is an ssDNA gap, as for example after UV irradiation or in replication mutants (186, 224, 411, 452). It is dependent on RecBC when the SOS-inducing lesion is a dsDNA break, as for example after treatment with a topoisomerase inhibitor or with a restriction enzyme (160, 192, 266, 294, 316, 317). SOS is induced by several conditions other than the exposure to DNA-damaging agents. Actually, it is constitutively induced in several null mutants, where either the level of spontaneous DNA lesions is increased or DNA repair is delayed (307). SOS is also induced when replication is perturbed by growing conditional mutants that affect an essential replication function at a semipermissive temperature (64, 224). Finally, SOS is induced by the exposure to certain antibiotics (285).
In addition to homologous recombination and SOS induction, a third role of RecA in UV-irradiated cells is defined by its requirement for SOS-induced mutagenesis, even in cells constitutively induced for the SOS response (lexADef [defective] mutants). This third role corresponds to two different RecA actions: (i) RecA filaments promote the proteolysis of UmuD to UmuD′, the active component of the bypass polymerase Pol V, and (ii) the tip of the RecA filament directly interacts with Pol V (UmuD′2 C) at the 3′ end of a DNA strand whose synthesis is blocked by a lesion (98, 121, 360). SOS-induced mutagenesis that occurs at gaps is RecFOR-dependent in vivo and in vitro (120, 229). In stationary phase, SOS-induced mutagenesis can be RecBC dependent (52, 116). Finally, an additional function of RecA in the replication of UV-irradiated cells is its role in “replisome reactivation.” UV irradiation causes a transient decrease in the rate of DNA synthesis (as measured by incorporation of labeled thymidine), and the recovery of a normal rate of DNA synthesis is an entirely RecA-dependent phenomenon called “replisome reactivation” (188, 461). Replisome reactivation is also dependent on RecFOR, and in recFOR or recA mutants DNA ends are degraded by the combined action of RecQ helicase and RecJ nuclease (58, 71). Although one of the consequences of the presence of RecFOR and RecA is the protection of DNA ends from exonuclease degradation, the main function of RecA during replisome reactivation is thought to be the promotion of replication resumption. Conflicting results have been reported on the role of bypass polymerases in this process. It is established that inactivation of only UmuCD does not prevent replisome reactivation (460); however, in one study (67) replisome reactivation was abolished when NER and the three bypass polymerases Pol II (polB gene), Pol IV (dinB gene), and Pol V (umuCD operon) were all inactive, whereas in another study (327), it was affected by the inactivation of only Pol II and UmuCD in NER+ cells. Replisome reactivation and the action of the proteins involved are also discussed below in the RecFOR section.
The first antirecombination protein to be described was the UvrD helicase. UvrD is an abundant helicase in E. coli (about 500 copies per cell in uninduced conditions) (133); it is a multifunctional enzyme essential for nucleotide excision repair and for mismatch repair (reviewed in references 416 and 417). In addition to being fully deficient for these two important repair processes, uvrD mutants exhibit an increased level of homologous recombination in all assays (42, 313, 481). The antirecombination action of UvrD in vivo correlates with a capacity to remove RecA from ssDNA and to undo a recombination intermediate in vitro (289, 428). The action of UvrD against bona fide recombination intermediates could be important to prevent too high a level of recombinational exchanges in growing cells. It could also result from a crucial role of UvrD against the nonrecombinogenic and deleterious binding of RecA to blocked replication forks (114). Actually, UvrD is essential for the viability of several replication mutants, where it acts either by preventing the formation of a deleterious RecA filament or by removing RecA from DNA, at gaps or at forks (224, 225, 428). Finally, the constitutive expression of the SOS response conferred by certain recA mutations can be suppressed by an intragenic suppressor. In certain cases, the intragenic suppressor acts in the double mutant by facilitating the anti-RecA action of UvrD (241).
DinI is a positive SOS-inducible regulator of RecA, at least in vitro: in contrast with RecX, purified DinI protein stabilizes the RecA filament (126, 250, 253). Although DinI overexpression confers severe UV sensitivity and results in the inhibition of LexA and UmuD processing, the dinI mutant confers only a slight increase in a specific recombination assay (23) and a slight increase in SOS-induced mutagenesis (471, 472). It was proposed that DinI interaction with the RecA filament limits SOS induction, and particularly UmuD2′C (Pol V)-dependent mutagenesis, by limiting UmuD, and to a much lower extent LexA, proteolysis (471, 472).
Another putative regulator of RecA is the RdgC protein. In vitro, RdgC competes with RecA for DNA binding sites, and DinI improves the capacity of RecA to compete against RdgC (94). However, the competition between RdgC and RecA for DNA could be nonspecific (50) and does not provide an explanation for the deleterious phenotype conferred by rdgC mutation in various recombination mutants (288, 348). Recently, the DinD protein was identified as an additional RecA regulator, which as for UvrD, RecX, and DinI is upregulated during SOS induction. DinD acts postsynaptically, by inhibiting RecA-mediated strand exchange, therefore at a later step than the other regulators (423). Finally, Psi is a RecA regulator expressed from the F plasmid. Its role is to prevent SOS induction by the ssDNA of F during conjugation. PsiB acts earlier in homologous recombination than the other regulators, as it is the only RecA regulator protein that interacts with free RecA protein, rather than with DNA-bound RecA molecules (314).
Homeologous recombination, which corresponds to strand exchange between diverged sequences, is antagonized by the mismatch repair proteins and facilitated by the induction of the SOS response (267). Homeologous recombination allows exchanges of DNA material between closely related but diverged bacterial species. The facilitation of this reaction in stress conditions is an important phenomenon for bacterial evolution (324). The inhibition of recombination between diverged sequences (463) and between damaged DNAs (54, 55) by mismatch repair proteins (MutL/MutS) has also been observed in vitro.
The RecBCD protein complex is responsible for recombination at DNA double-strand ends and for the degradation of unwanted linear DNA including foreign DNA that may have entered the cell. In order to carry out these two roles, it is required to be both an effective recombinase and a powerful DNA exonuclease. Furthermore, it needs to be able to distinguish self from foreign DNA and modulate its activities in relation to this information. For reviews of RecBCD action, see references 87, 106, 207, 215, 282, 292, 384, 386, and 387. There are several potential sources of DNA double-strand ends available to RecBCD that are shown in Fig. 6. A first important source of ends is DSBs induced by DNA damage. Repair of these breaks in E. coli relies on recombination with an intact sister chromosome, as the bacterium does not encode a nonhomologous end-joining pathway of DNA repair. A second source of ends is the transfer of DNA from another bacterium (e.g., by conjugation or transduction). Here, recombination will accomplish the integration of the foreign fragment. A third source of DNA ends is fork reversal during DNA replication. Here, the two newly replicated strands at a replication fork are paired, and replication cannot continue until they are either degraded or recombined to resolve the structure. A fourth source of DNA ends is replication fork collapse when copying a DNA template containing single-strand gaps or other single-strand interruptions. A fifth source of DNA ends is replication fork collision, where a replication fork has been blocked by a bound protein (Fig. 6E). Finally a sixth source of DNA ends is postreplication cleavage (Fig. 6F). These different situations present DNA ends in different configurations and have different requirements with respect to the recombination and degradation capabilities of the protein. Critical in converting the enzyme from a potent DNA exonuclease to a recombinase is the sequence known as chi, originally discovered as a hot spot for recombination in red gam mutant lambda bacteriophages (79, 163, 212, 216). chi has been shown to be the DNA sequence 5′GCTGGTGG3′ (36, 385, 395) and to act as an orientation-dependent and directional initiator of recombination requiring RecBCD (111, 399, 467). It would appear that RecBCD has evolved the ability to recognize chi as a means to distinguish self from foreign DNA. chi is the most overrepresented octameric DNA sequence in the E. coli chromosome, and there is a significant bias in the orientation of the sequence with respect to the direction of replication of the chromosome, consistent with its utilization to repair reversed and/or broken replication forks (15, 421, 422).
Significant advance in our understanding of the mode of action of RecBCD has come about via determination of the crystal structure of the complex bound to DNA (381). This crystal structure (Fig. 9) has revealed that the dsDNA enters the protein via an interaction with RecB and RecC and is split over a pin in RecC. The two separated strands pass down channels where the 3′-ended strand can interact with the helicase motor of RecB and the 5′-ended strand with the helicase motor of RecD. This makes sense, as RecB has been shown to possess 3′-to-5′ helicase activity and RecD has been shown to have 5′-to-3′ helicase activity (88, 409). The RecC subunit is placed appropriately to interact with the chi sequence in a region where mutations are known to alter chi recognition. As the separated strands pass through the protein, they emerge in the proximity of the single nuclease domain located in RecB. The existence of a single nuclease domain with access to either the 3′-ended or the 5′-ended strand explains the observation that one or the other strand is preferentially cleaved. The proposed mechanism of action of RecBCD nuclease involves preferential interaction of the 3′-ended strand with the nuclease domain of RecB until that strand is retained in the complex, by RecC binding chi, allowing preferential access of the 5′ end to the nuclease (Fig. 10). Finally the nuclease domain of RecB interacts with RecA and facilitates loading of RecA on the ssDNA generated by degradation of the 5′-ended strand following chi recognition (59, 247, 391). The RecD subunit must also play a role in the nuclease activity of the complex, although it does not contain the nuclease active site, as the RecBC enzyme has very little nuclease activity (13, 198, 199).
The other major advance in our understanding of RecBCD action has come about via the development of single-molecule assays for RecBCD action (37, 91, 154, 312, 392, 394). In the first such assay, DNA bound with the fluorescent dye YOYO1 is attached to a surface via one end and can be visualized as it interacts with RecBCD at the other end in an apparatus where fluid flow stretches out the DNA molecule. Here it was seen that RecBCD unwinds DNA at a rate of 1 to 2 kb/s until it reaches a chi sequence where its rate of unwinding is reduced by approximately a factor of 2. This is explained by a switch from the faster RecD motor acting up to the point of interaction with chi, whereupon the RecD motor becomes disengaged, leaving the slower RecB motor to drive further unwinding. This results in the formation of a single-strand loop terminating at the bound chi site. It is interesting that there is a wide range of translocation velocities of individual enzymes, both prior to and after chi recognition. Furthermore, there is no correlation between the velocity of one molecule before and after chi recognition, implying that some unknown variable is affecting the individual translocation rates.
It has also been possible to visualize the tracking of a single RecBCD complex on DNA by labeling the protein rather than the DNA. Here, a fluorescent nanoparticle has been attached to the RecD subunit of the enzyme (392). In this way it has been possible to address the hypothesis that interaction with chi leads to the loss of the RecD subunit from the complex. Clearly, this does not occur, as the fluorescent particle is seen to travel up to chi and then to continue at approximately one-half the velocity after chi.
DNA ends can be produced during replication and are acted upon by RecBCD. One source of DNA ends is the reversal of blocked replication forks (281). This reaction involves the formation at blocked forks of a dsDNA end by annealing of leading and lagging-strand ends (Fig. 6C). It was first characterized in rep mutants, which are not viable in the absence of RecBCD and where linear DNA accumulates, in a RuvAB-dependent reaction, following the shift of a rep recBCts mutant to the nonpermissive temperature (363). Viability in the absence of rep recA mutants indicated that RecBCD/RecA-mediated recombination was not essential for survival. This was consistent with a primary role for RecBCD-mediated DNA degradation following fork reversal. However, a rep recD mutant was shown to be viable, indicating that in the absence of RecBCD nuclease activity, there remains a pathway to survival. That this pathway is recombination is indicated by the loss of viability of a rep recD recA triple mutant (363, 424). In a RecBC+ context, the dsDNA end at reversed forks is processed by RecBCD, either by degrading the dsDNA end or by promoting its reincorporation into the intact chromosome by homologous recombination, both of which restore a structure from which replication can restart. However, in the absence of RecBCD, RuvABC-mediated resolution of the Holliday junction formed by fork reversal leads to fork breakage (reviewed in references 281 and 282). Replication fork reversal has been shown to occur following interference with the proper action of several different replication proteins, including the replicative helicase DnaB (363), polymerase III subunits (HolD, DnaE, and DnaN) (113, 142), and the replication restart protein PriA (141). Replication fork reversal was also observed in an nrdA101 mutant, where the enzyme ribonucleotide reductase has been affected, or when the enzyme is inactivated by hydroxyurea (HU) treatment (145, 146, 351). In all of these different situations, the action of RecBCD appears to be similar to that originally observed in the rep mutant.
Another source of DNA ends is the encounter of a replication fork with a gap or nick in its template. This reaction (Fig. 6D) has been called replication fork collapse, and mutants that are predicted to accumulate template breaks that can lead to collapse (such as polA) are not viable in conjunction with recB or recC mutations (213, 214). Replication fork collapse has been directly demonstrated in dut mutants that have increased incorporation of uracil into DNA (203, 204). In addition to replication fork collapse, the formation of some replication-dependent two-ended breaks has recently been observed in a dut mutant, indicating some postreplication breaks (204).
A third source of replication-dependent DNA ends is replication fork collision, where one replication fork runs into a previous fork that has been blocked by proteins bound to DNA (Fig. 6E). This has been demonstrated by insertion of ectopic Ter sites to block partially replicated chromosomes in the presence of the protein Tus (40). Here, new DNA ends are generated by collision of new forks with the blocked forks. RecBCD and RecA are required to repair the broken forks, and it is interesting that the fork generated by recombination is capable of proceeding through the barrier aided by UvrD (39). The outcome of this reaction seems to be dependent on the nature of the protein-mediated block, as the binding of the TetR repressor at an array of 250 copies of the tetO operator site does not lead to repair by RecBCD-mediated recombination (319).
Finally, replication can generate a break behind the fork, a postreplication break that also requires RecBCD and RecA for repair (Fig. 6F). An example of postreplication breakage is DNA palindrome cleavage by the SbcCD nuclease (78, 218). Here, a hairpin formed on the lagging-strand template is cleaved in a replication-dependent manner to generate a two-ended DNA break (110). In a reaction perhaps analogous to the passage of the Ter-Tus block, repair can be accomplished without recleavage of the palindrome.
RecA promotes strand exchange at DNA double-strand ends and DNA single-strand gaps. Genetic and in vitro evidence have now established that the presynaptic RecF, RecO, and RecR proteins (called RecFOR) act in concert to allow the action of RecA on ssDNA gaps (Fig. 11). Actually, ssDNA is covered in vivo with the ssDNA binding protein SSB, and the role of RecFOR is to allow RecA to bypass the SSB barrier (255, 420). The crucial role of RecFOR in gap repair was first proposed when it was observed that recF mutants accumulate gaps after UV irradiation (130, 439). RecFOR was then recognized as promoting RecA binding when it was observed that recA mutants that bypass the need for RecFOR encode RecA proteins that have an increased affinity for ssDNA in vitro (217, 444). That RecFOR acts by allowing RecA to bypass the SSB barrier at ssDNA gaps is now supported by direct in vitro evidence (290, 350).
Although its main role in a wild-type context is homologous recombination at ssDNA gaps, the so-called RecFOR recombinational repair pathway was first identified through its essential role in DNA DSB break repair in a recBC sbcB sbcC mutant. This mutant lacks the bona fide double-strand break repair complex RecBC and two nucleases encoded by the sbcB gene and sbcCD operon (168, 195, 259). In a recBC sbcB sbcC mutant, DSB repair via the RecFOR pathway requires three additional presynaptic proteins: RecN, RecQ, and RecJ (243, 293, 315). RecQ and RecJ act in concert to provide a 3′ extension substrate for RecFOR-promoted RecA binding (Fig. 12).
The RecO protein is characterized by the presence of an oligonucleotide/oligosaccharide-binding domain (OB fold region) (222, 261). OB fold domains are typical of ssDNA binding proteins such as SSB or the eukaryotic SSB homolog RPA. RecO is present in most bacteria and is encoded by either of two classes of genes. E. coli RecO is homologous to the crystallized D. radiodurans protein, whereas RecO from Helicobacter pylori defines a family of structurally related, but not sequence-related, RecO proteins (265). As do RecQ and RecJ (see below), E. coli RecO interacts functionally with the C-terminal tail of the SSB protein, and the three-dimensional crystal structure of the RecO protein bound to a SSB C-terminal peptide has been reported (see reference 349 and references therein).
The crystal structure of RecF revealed a strong structural homology with the eukaryotic Rad50 and SMC proteins (200). The Rad50 and the SMC families of proteins include substantial coiled-coil regions and are involved in DSB repair and chromosome cohesion, respectively; their head domains are sites of protein-protein interactions. RecF is the only one of the three RecFOR proteins that shows a DNA-dependent ATP binding and ATPase activity (256, 449). It forms ATP-dependent dimers, with a semiclamp or symmetrical crab claw shape. The inside surface of the dimer has been proposed to bind DNA (200).
The RecQ helicase unwinds duplex DNA by translocating on one DNA strand in the 3′-to-5′ direction. Its activity is stimulated by the presence of SSB (377, 418). The crystal structure of the catalytic core was determined (34). The two N-terminal domains contain all the helicase motifs. The third domain is called RecQ-conserved (RecQ-Ct) and contains Zn2+-binding and winged-helix motifs. The C-terminal domain called Helicase-and-RNaseD-C-terminal (HRDC) was deleted to facilitate crystallization, but its structure was determined independently. This domain forms a globular bundle of helices, similar to the DNA binding domain of several other proteins, and acts as a structure-specific DNA binding determinant (32, 33).
Finally, the last protein required for the RecFOR pathway of DNA DSB repair in vivo is RecN, a poorly characterized coiled-coil protein difficult to purify (276, 441). The RecN protein from Deinococcus radiodurans and from other bacteria was characterized (see reference 335 and references therein). RecN is a weak ATPase that acts as a multimer. It stimulates the intermolecular ligation of linear duplex DNA molecules, presumably by increasing the local concentration of DNA ends. RecN, which is highly SOS induced but rapidly degraded, was thus proposed to have a cohesin-like function, tethering DNA ends together.
The only activities detected for the purified RecF and RecO proteins are the DNA-dependent ATPase activity of RecF and the strand-annealing property of RecO (182, 449). The purified RecR protein has no activity alone; instead, it is part of two complexes formed in vitro by the RecF, RecO, and RecR proteins: RecFR and RecOR (419, 448). These two complexes are now thought to be the active forms for the RecFOR pathway. The RecO-RecR complex comprises two RecO monomers per RecR tetramer (222). RecOR is proposed to be responsible for rendering SSB-coated ssDNA accessible to RecA (44, 164, 350). The RecF-RecR complex of Thermus thermophilus consists of a RecR ring-like tetramer with two RecF monomers located near the center (166). RecFR binds dsDNA preferentially and is proposed to act at the ssDNA-dsDNA junction (44, 290, 365, 448). The three recF, recO, and recR single mutants are similarly impaired for homologous recombination, implying that the lack of any of the three partners prevents the action of the two others. This observation suggests that in vivo the RecOR and RecFR complexes act in concert. Actually, RecF improves RecOR-promoted loading of RecA onto SSB-covered ssDNA under certain conditions in vitro (156, 350). RecQ, RecJ, RecFOR, RecA, and SSB-dependent DSB repair was reconstituted in vitro (156). In this reaction, RecJ acts on a linear dsDNA substrate to provide, via its 5′ dsDNA exonuclease activity, the 3′ protruding end onto which RecFOR promotes RecA loading. This RecA filament invades a homologous supercoiled molecule. RecJ, RecFOR, and RecA are all absolutely required for the reaction, and SSB strongly stimulates it, whereas RecQ only acts as a stimulator of the RecJ dsDNA exonuclease action.
RecFOR is essential for gap repair in UV-irradiated cells because homologous recombination provides an efficient way of converting an ssDNA UV lesion into a double-stranded form, accessible to nucleotide excision repair. Actually, DNA strands were shown to be exchanged following UV irradiation (345; reviewed in reference 347), and recombinational repair involves the formation and the resolution of Holliday junctions (Fig. 13, gap repair) (347). However, inactivation of ruvA or ruvC or recG did not affect the conversion of low-molecular-weight to high-molecular-weight DNA after UV irradiation (415). Since ruvABC mutants are hypersensitive to UV irradiation, this observation could simply reflect the fact that resolution of Holliday junctions is not needed for the conversion of gapped DNA into sealed DNA molecules, i.e., Holliday junction-linked but gap-free DNA of high molecular weight. Actually, UV irradiation prevents proper segregation of chromosomes in ruvABC mutants, suggesting the presence of unresolved Holliday junctions that link daughter chromatids (172), and ruvAB and ruvC mutants accumulate unresolved Holliday junctions following replication after UV-induced damage in plasmid DNA (93).
RecFOR-initiated homologous recombination repairs gaps formed in replication mutants, for example, when a temperature-sensitive mutant of Pol III is propagated at semipermissive temperature (224). Similarly to gaps formed in UV-irradiated cells, gaps resulting from a replication defect induce the SOS response. They translate behind replication forks and can be distinguished from gaps formed at forks because they render the Holliday junction resolution complex RuvABC essential for viability in recombination-proficient backgrounds (21). Gap recombinational repair is not essential for viability in replication mutants, presumably because these gaps can be efficiently filled in by a polymerase, since the DNA is intact (82).
The first assay used to quantify homologous recombination was Hfr conjugation. Because this process relies mainly on recombination initiated at dsDNA ends, recA and recBC were the first recombination genes discovered. Mutations that suppress the defect of recBC mutants in Hfr recombination were isolated and named sbc for suppressors of recBC. Two suppressor genes were identified, named sbcA and sbcB (see the "Introduction" to this section, above). The sbcA mutation activates a cryptic prophage-encoded recombination process that requires RecE and RecT proteins (300). sbcB, a gene also identified independently under the name of xonA, encodes a 3′-to-5′ exonuclease, Exo I. The original suppressor mutation, sbcB15, is a better suppressor of recBC defects than a null sbcB (xonA) mutation because the sbcB15 allele encodes a defective Exo I that has retained DNA-binding activity and interferes with other nucleases (38, 329, 413, 477, 478). recBC sbcB mutants were later found to lack another nuclease, the SbcCD complex (134). It is generally believed that the inactivation of these nucleases allows recombination to proceed by a RecBCD-independent pathway by preventing the degradation of the ssDNA recombination substrate with a 3′ end. The structural homology between RecF and SbcCD head domain later led to the speculation that RecF and SbcCD might compete for DNA, rendering SbcCD inactivation essential for RecF DNA-binding (200). As explained above, the genes that are required for Hfr recombination in a recBC sbcB sbcC background defined what is called the “RecF pathway” of homologous recombination (reviewed in reference 61); these genes are recN, recQ, recJ, recF, recO, recR, and ruvABC (Fig. 12). RecN is a coiled-coil protein proposed to bind DNA ends and bring them in close proximity, which could be required in vivo because dsDNA end recombination is less efficient when it is catalyzed by the combined action of RecQ, RecJ, and RecFOR proteins than by the highly specialized and efficient RecBCD complex. Confirming a role for RecN in DSB repair, RecN was shown to be required for the repair of I-Sce1 DSBs specifically when the number of DSBs is higher than one per chromosome (276). The action of RecQJFOR at a double-strand end was reconstituted in vitro (155) (see above). RecG and RuvABC are Holliday junction branch migration and resolution enzymes and are described below.
Plasmid recombination was shown to require RecF, RecO, and RecJ (as the plasmids used lacked chi sites, they were committed to RecFOR-initiated recombination) (63, 195). recQ was not tested; recN inactivation had no effect in agreement with the role of this protein in joining DNA ends. Inactivation of either or both ruvAB and recG also had no effect (195, 231, 246). It was proposed that the replication of recombination intermediates through unresolved Holliday junctions generates viable recombinant molecules.
In addition to postreplicative gap repair (the recombinational repair of gaps formed by replication across DNA lesions), RecFOR participates, with RecA, in the other known UV repair processes: SOS induction, UV-induced mutagenesis, and replisome reactivation (71, 229, 411, 439, 452).
After UV irradiation, the rate of DNA replication (as measured by the incorporation of tritiated thymidine) is depressed for about 20 min. The recovery of a normal replication rate (replisome reactivation) implies replication restart from blocked forks and replication initiation from oriC, the chromosome origin, since it is delayed in the absence of PriA and partly dependent on DnaA (327, 342, 343). Replisome reactivation is abolished in several recombination mutants: recA, recF, recO, and recR, (58, 71, 327) (Fig. 13). Importantly, replisome reactivation is not affected by ruvAB or recG inactivation or by the simultaneous inactivation of ruvAB and recG, suggesting that it does not involve Holliday junctions (92, 344). In spite of 20 years of research, the precise molecular role of recombination proteins in replisome reactivation is still unclear. RecFOR-dependent replication resumption is important at early times following UV irradiation and prevents the degradation of nascent DNA ends at blocked forks (69, 343). Both DnaA-dependent and RecFOR-dependent replication resumption requires functional nucleotide excision repair proteins (72, 342). The accumulation of gaps after UV irradiation has led to the proposal of models in which replication continues beyond the lesions on both strands in a discontinuous fashion (reviewed in references 347 and 443). Replication fork block and residual synthesis of short DNA fragments from oriC and the alternative (and not exclusive) model of discontinuous DNA synthesis on both strands could both account for the slow rate of replication and the synthesis of chromosomes as fragments following UV irradiation. The demonstration that priming could occur on the leading as well as on the lagging strand in vitro brings biochemical support to the discontinuous synthesis model (161). However, the delay in replisome reactivation in a priA mutant suggests that the reloading of a DnaB helicase and, in turn, a novel replisome is required for the recovery of a continuous mode of leading-strand synthesis. Interestingly, in addition to their classical roles (homologous recombination, SOS induction, and stimulation of bypass polymerases), it was also proposed that RecFOR-RecA proteins facilitate replisome reactivation by clearing the blocked 3′ ends of replicating DNA, based on the observation that in vitro RecFOR and RecA displace a stalled DNA polymerase from a DNA template lesion (273).
RecFOR-dependent RecA filamentation can be toxic, as observed at blocked replication forks in replication mutants (114, 428). It requires RecFOR, RecJ, and RecQ, in contrast with RecA binding at gaps, which requires RecFOR but not RecQ (114, 224, 225). The deleterious action of RecQJFORA proteins was observed only in cells that lack UvrD, and it was proposed that this helicase prevents RecA binding or removes DNA-bound RecA molecules. It was proposed that either strand invasion is prevented at replication forks or a strand exchange reaction occurs, a reaction which is not reciprocal because SSB-stimulated exonucleases are present at forks and degrade the displaced ssDNA ends. The resulting ssDNA or dsDNA RecA-filaments do not lead to the formation of a Holliday junction (224). If after homologous recombination RecA is normally displaced from DNA by Holliday junction branch migration enzymes, then these RecA-ssDNA or RecA-dsDNA filaments that are not associated with a Holliday junction may require UvrD for removal.
An analog of RecFOR able to substitute for RecFOR in lambda crosses was identified as the product of the lambda orf gene. The Orf protein was purified and crystallized (269). It interacts with SSB and was proposed to act by promoting RecA binding to SSB-coated ssDNA. However, Orf does not substitute for RecFOR in vivo in conjugational recombination or for the repair of UV lesions and seems to be specifically active in the presence of the lambda presynaptic Exo and Beta proteins (357, 358).
The product of a reciprocal strand exchange between two homologous DNA molecules is the structure called a Holliday junction (Fig. 14). Movement of the junction along DNA provides a simple way to extend the length of the heteroduplex, by a process known as “branch migration” (Fig. 15A). Although the process has theoretically little or no energy cost, it is catalyzed by enzymes that consume ATP. In E. coli, branch migration is mainly catalyzed by a complex of RuvA and RuvB proteins. In this complex, RuvA plays a structural role and also stimulates RuvB activity. RuvB is an ATPase, the motor that drives branch migration. Holliday junction resolution is catalyzed by the RuvABC complex; RuvC is an endonuclease that acts as a dimer to catalyze a symmetrical cleavage of two opposite strands within a RuvABC-Holliday junction complex (Fig. 15B). Resolution is coupled with branch migration, and nicked strands are exchanged when they are rejoined by DNA ligase. For previous reviews on RuvABC, see references 372, 450, and 468.
The crystal structures of RuvAB complexes from several bacteria have been reported. Structures are highly similar, owing to the strong conservation of the proteins. E. coli RuvA was crystallized as a symmetrical tetramer (325) and later as a tetramer bound to a Holliday junction (18, 157) (Fig. 16). RuvA is a small protein of about 22 kDa. It forms a square planar tetramer with a convex negatively charged side and a concave positively charged side that interacts with DNA. The symmetrical structure of the RuvA tetramer imposes a square planar configuration to the Holliday junction. RuvA also binds Holliday junctions as an octamer, in which two tetramers sandwich the junction. The structure of a Holliday junction-bound RuvA octamer was determined (Mycobacterium leprae RuvA [337]), as was, later, the structure of a RuvAB complex composed of two RuvA tetramers flanked by two RuvB hexamers (Thermus thermophilus RuvAB [469]) (reviewed in reference 468). Each RuvA monomer is composed of three domains (Fig. 16). The N-terminal domains of the tetramer (domain I; residues 1 to 64) are at the center of the Holliday junction; they interact by hydrogen bonds that stabilize the tetrameric configuration. Two residues, Glu55 and Asp56, form an acidic pin that maintains the Holliday junction in an open configuration and facilitates branch migration by RuvB (169). Domain II of RuvA contains two helix-turn-helix structures that interact with DNA (18); each domain II in the tetramer is bound to a dsDNA arm of the Holliday junction. In addition, the octameric form is stabilized by interactions between two antiparallel alpha helices in domain II, residues 117 to 129 (122, 322). The C-terminal domain of RuvA (domain III) is flexible and separated from domain II by a nonstructured linker. Domain III interacts with RuvB and stimulates its action (295, 296); interactions between domain III and RuvB are essential for branch migration.
The RuvB polypeptide has a molecular mass of about 37 kDa. In the RuvA-RuvB complex, two RuvB hexameric rings assemble on two opposite dsDNA arms, on each side of the RuvA-Holliday junction complex, and promote branch migration by pumping the dsDNA away from RuvA (Fig. 15A). RuvB is an ATPase, which presents similarities with other proteins of the AAA+ family of proteins (WalkerA, WalkerB, and sensor 1 and sensor 2 motifs) (177, 304). The RuvB monomer has a crescent-like structure composed of three domains, and the two N-terminal domains contain all the motifs regarded as the signature of a DNA helicase. Its homology with other ATPases is interrupted in the N-terminal domain by a Beta-hairpin that interacts with the C-terminal domain of RuvA (152, 305). In single-molecule experiments the RuvAB complex was found to be a processive enzyme with a migration rate of about 40 bp/s, accompanied with DNA rotation (80, 153). These experiments also established that the six RuvB monomers in the hexamer are not functionally homogeneous, as suspected from previous analysis (279). Several mutational analyses of ruvB have identified residues that are important for its activity (132, 177, 279, 305, 323).
RuvC is a small protein of about 19 kDa. Although purified RuvC protein catalyzes Holliday junction resolution in vitro (29, 30), RuvC has no activity in vivo in the absence of RuvA or RuvB. The active resolution complex is a RuvC dimer bound to RuvAB to form a RuvABC complex; it resolves Holliday junctions by nicking two opposite strands (Fig. 15B). The nicks in the products of resolution are then re-joined by DNA ligase (reviewed in reference 450). RuvC binds Holliday junctions independently of the DNA sequence but preferentially cleaves at a/t T T↓g/c sequences. The three-dimensional structure of a RuvC dimer showed a striking similarity with E. coli RNaseH1, with a catalytic center composed of acidic residues (D7, G66, D138, and D141) (17). Other residues critical for RuvC activity were also identified (17, 149, 368). Resolution is prevented in vitro by an excess of RuvA protein, presumably because the octameric complex prevents RuvC action (454). In the RuvABC complex, RuvAB-mediated branch migration and RuvC-mediated Holliday junction resolution are intrinsically linked (479). The acidic pin in RuvA that maintains the Holliday junction in an open square configuration favors resolution (169). Notably, the outcome of the recombination reaction depends on the pair of strands cleaved by RuvC in the Holliday junction-RuvABC complex, and, interestingly, this pair of strands is determined by the direction of RuvAB branch migration, in vitro and in vivo (77, 280, 425) The RuvC paradigm (symmetrical cleavage that leaves ligatable nicks) was used to purify one of the human resolvases (170, 451).
As described above, UV irradiation renders cell viability dependent on RecFOR (indicating the formation of ssDNA gaps) and on RecBC (indicating the formation of dsDNA ends). In a recBC mutant, survival after UV irradiation (which entirely depends on RecFOR) is independent of RuvABC while it largely relies on RecG (138, 231, 236). In contrast, in recFOR mutants, survival after UV irradiation (which is entirely dependent on RecBC) is more dependent on RuvABC than on RecG (20, 231). All together, these observations suggest that, at least in UV-irradiated cells, Holliday junction resolution is not entirely independent of the type of recombination substrate and presynaptic proteins at the onset of the recombination reaction. RuvABC is important for one-ended (or ends-in) DSB repair, while it can be replaced by RecG in ends-out recombination and during gap repair (see "RecG, a helicase implicated in resolving recombination intermediates," below).
Studies of the mechanism responsible for the replication fork reversal reaction in various replication mutants showed that it is catalyzed by different pathways depending on the cause of replication arrest. Replication fork reversal requires RecA in the replicative helicase mutant dnaB but not in any other replication mutant (362). In two polymerase III mutants (dnaE and holD) and partly in the rep helicase mutant, the conversion of the fork into a Holliday junction requires RuvAB (21). This observation suggests that RuvAB plays two different roles in E. coli: resolution of Holliday junctions and fork reversal by the conversion of inactivated replication forks into Holliday junctions. RuvAB is required for replication fork reversal only in certain cases of replication arrest, which reinforces the notion that the accessibility of inactivated replication forks to recombination/repair/replication restart proteins may depend on the origin of replication arrest.
The idea that RuvAB plays a direct role in the remodeling of inactivated replication forks was further supported by the isolation of ruvA and ruvB separation-of-function mutants that have lost the capacity to reverse forks but are recombination proficient and therefore still resolve Holliday junctions. Two ruvA mutants were characterized both in vitro and in vivo, and although they were as efficient as wild-type ruvA for homologous recombination in vivo, they were defective for several in vitro activities (20). Four single ruvA and four single ruvB mutants were characterized in vivo only (223). The ruvA mutants were mutated in DNA binding domains, or in the RuvB-binding domain, or in the helix involved in octamerization and were defective for replication fork reversal only when RuvB was present in a limiting amount, suggesting a defect in RuvB helicase stimulation. Of the four ruvB separation-of-function mutants isolated, three lie in the ATP binding pocket, suggesting that they impair the action of the RuvB motor. Interestingly, preventing specific interactions between the two RuvA tetramers that sandwich the Holliday junction induces a separation of function phenotype, suggesting that RuvA octamerization is important for its action at replication forks (47). Altogether, the characterization of separation-of-function ruvA and ruvB mutants reveals that the RuvAB complex is stronger than needed for Holliday junction branch migration and resolution in vivo, so that mutants with reduced in vitro activity lose replication fork reversal while keeping Holliday junction resolution. In addition to replication fork reversal, the strength of RuvAB may be useful during Holliday junction branch migration for protein removal (2, 140, 375) and branch migration through heterologies (1, 310) and through certain DNA lesions (223). RuvA was also shown to be able to function in vitro with an alternative hexameric helicase, the replicative helicase DnaB (183). Although the physiological significance of this reaction is unclear, it correlates with the action of RuvAB at replication forks. Furthermore, several authors underlined a strong homology of RuvB with proteins that belong to the replication fork machinery, such as components of the gamma complex (25, 147, 177).
The enzymes that catalyze Holliday junction resolution were originally discovered in bacteria infected with phage T4 (187). Actually, several bacteriophages encode their own resolvases and the best-studied enzymes are T4 endonuclease VII, T7 endonuclease I, lambda Rap, and RusA (369; reviewed in references 81, 297, and 374). The expression of resolvases from phage genomes has increased their propensity of transmission by lateral exchange. However, with the exception of RusA, which specifically cleaves Holliday junctions, all phage resolvases fundamentally differ from RuvABC by their capacity to cleave a variety of branched structures, a reaction essential to eliminate any remaining branches from phage DNA prior to packaging (83, 179, 287, 321, 369, 370, 373). Phylogenetic analyses have shown that resolvases belong to different classes of enzymes. Several have an RNase H fold, like RuvC, while others, like T7 endo 1, are structurally related to restriction nucleases and T4 endo VII and RusA are in classes of their own (16). RusA, T4 endo VII, and T7 endo I were all recently crystallized in complexes with Holliday junctions (43, 148, 254). They all distort the Holliday junctions upon binding, although they exhibit different modes of binding.
The other important synthetic defect (initially observed for conjugation, P1 transduction, and UV sensitivity) occurs between recG and ruvABC, suggesting that RecG and RuvABC provide alternative pathways for resolving Holliday junctions (238). The involvement of RecG in conjugation and P1 transduction suggested a role in DSB repair. Recent studies have confirmed that RecG does indeed play a role in DSB repair. recG mutants are sensitive to breaks made by the endonuclease EcoKI (446) and to cleavage of a 246-bp palindrome by SbcCD (110) and are synthetically sensitive to breaks generated by I-SceI in the absence of RuvABC (275). Furthermore, repair of EcoKI, and I-SceI DSBs, and gamma irradiation damage, in the absence of RuvABC, and therefore relying on RecG, leads to a significant fraction of crossover products (143, 275, 446). These observations indicate that in addition to any role that RecG might play in resolving recombination intermediates to noncrossover products, e.g., at gaps repaired by RecFOR, it plays a role in generating crossover products in DSB repair. A cleavage-dependent (275) and a cleavage-independent (446) model for RecG-mediated DSB repair have been proposed and are summarized in Fig. 18.
While the precise role of RecG in recombination remains unclear, and there may indeed be several reactions that contribute to this role, an observation relating to the suppression of ruv mutants is pertinent. When suppressors of a ruvA mutant were isolated, they were found to activate the expression of rusA, a cryptic gene encoding a nuclease capable of resolving Holliday junctions (260, 263). It is relevant here that suppression of ruvA was found to be dependent on RecG, arguing strongly that RecG can migrate Holliday junctions in vivo to positions where they can be resolved by cleavage with RusA.
In conclusion, the inhibitory roles of RecG in adaptive mutagenesis, UV-induced SDR and RecA-mediated strand exchange, would seem to imply a regulatory role for the protein in the early stages of DSB repair, when it would be working with RecBCD and RecA. This regulatory role seems to be required because of a potentially damaging consequence of PriA helicase activity, at least in the case of SDR. However, there seems also to be a role for RecG in promoting the resolution of recombination intermediates in DSB repair, and this surprisingly often leads to crossing-over. Finally, there remains an activity of RecG that is detected in a recB mutant and could represent the dissolution of an intermediate in RecFOR-mediated gap repair following UV damage.
Although the molecular processes that lead to the formation of recombination products is generally well understood, and sometimes in exquisite details, several questions remain unanswered. The central and key step of homology searching is still a mystery. How does the RecA filament find a homologous dsDNA in the complexity of the whole genome? Although recombination between sister chromatids might be facilitated by the proximity of the two homologous DNA molecules behind replication forks, it is more difficult to visualize how following γ-irradiation, RecA can repair tens of DNA DSBs, none of which may originally be close to its homologous intact sequence. Another mystery is the precise role of the long and still-growing list of enzymes that control RecA actions. Of all the RecA regulator mutants, only uvrD clearly exhibits a hyperrecombination phenotype. Are RecX, DinI, and DinD proteins crucial under conditions other than those studied in the laboratory? Do they stimulate or counteract each other? Their biological roles are still elusive. RecBCD is, with RuvABC and RecA, the best -understood of all recombination enzymes, yet its model of action as a potent exonuclease, and as a chi-stimulated recombinase, is still not fully reconciled with the phenotypes of all recBCD mutants and the biochemical properties of the mutant enzymes. Although it is known that RecB, RecC, and RecD are all expressed at low levels, the precise stoichiometry of these three proteins in vivo is still unknown, leaving open the possibility that a significant fraction of RecBC enzyme coexists with RecBCD. Several questions are also still unanswered concerning RecF. In vitro, RecF is not needed for the promotion of RecA action on DNA gaps, and it weakly accelerates a reaction that is already efficiently catalyzed by RecO and RecR. Therefore, why does the inactivation of recF, recO, or recR confer a similar phenotype? Is the action of RecF, as a suppressor of the anti-RecA protein RecX, significant in vivo, and if so, under which conditions? Among presynaptic enzymes, the function of RecN remains a mystery, even though structural and biochemical data are now available. Is it because this protein does not exert a defined enzymatic activity, but rather plays a structural role of holding DNA molecules together? Then, RecN would become crucial only when recombination initiation is slowed down for some reason as exemplified by the use of a secondary recombination pathway. Along with RecN, RecG is one of the less understood recombination proteins. Decades of studies have failed to identify a cognate resolvase enzyme, indicating that it is unlikely that RecG acts in concert with a Holliday junction endonuclease. Therefore, how does a protein that catalyzes only branch migration resolve a Holliday junction? To date, the variety of weak defects of the recG mutant and the multiple substrates of the RecG proteins have been confusing. Which of recG mutant phenotypes are directly related to RecG action on Holliday junctions, and which are related to RecG action on D loops and R loops? The development of new powerful technologies such as single-molecule techniques in vitro and high spatial and temporal resolution microscopy in vivo might help to answer these questions.
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Module7.2.7
