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EcoSal Plus

Domain 4:

Synthesis and Processing of Macromolecules

Homologous Recombination—Enzymes and Pathways

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
  • Authors: Bénédicte Michel1, and David Leach2
  • Editors: Susan T. Lovett3, Andrei Kuzminov4
    Affiliations: 1: CNRS, Centre de Génétique Moléculaire, FRE 3144, Gif-sur-Yvette F-91198, and Université Paris-Sud, Orsay F-91405, France; 2: Institute of Cell Biology, School of Biological Sciences, King's Buildings, University of Edinburgh, Edinburgh EH9 3JR, United Kingdom; 3: Brandeis University, Waltham, MA; 4: The Schoold of Molecular and Cellular Biology, University of Illinois at Urbana-Champaign, Urbana, IL
  • Received 04 August 2011 Accepted 23 November 2011 Published 11 September 2012
  • Address correspondence to Bénédicte Michel [email protected] and David Leach [email protected].
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  • Abstract:

    Homologous recombination is an ubiquitous process that shapes genomes and repairs DNA damage. The reaction is classically divided into three phases: presynaptic, synaptic, and postsynaptic. In , the presynaptic phase involves either RecBCD or RecFOR proteins, which act on DNA double-stranded ends and DNA single-stranded gaps, respectively; the central synaptic steps are catalyzed by the ubiquitous DNA-binding protein RecA; and the postsynaptic phase involves either RuvABC or RecG proteins, which catalyze branch-migration and, in the case of RuvABC, the cleavage of Holliday junctions. Here, we review the biochemical properties of these molecular machines and analyze how, in light of these properties, the phenotypes of null mutants allow us to define their biological function(s). The consequences of point mutations on the biochemical properties of recombination enzymes and on cell phenotypes help refine the molecular mechanisms of action and the biological roles of recombination proteins. Given the high level of conservation of key proteins like RecA and the conservation of the principles of action of all recombination proteins, the deep knowledge acquired during decades of studies of homologous recombination in bacteria is the foundation of our present understanding of the processes that govern genome stability and evolution in all living organisms.

  • Citation: Michel B, Leach D. 2012. Homologous Recombination—Enzymes and Pathways, EcoSal Plus 2012; doi:10.1128/ecosalplus.7.2.7


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Homologous recombination is an ubiquitous process that shapes genomes and repairs DNA damage. The reaction is classically divided into three phases: presynaptic, synaptic, and postsynaptic. In , the presynaptic phase involves either RecBCD or RecFOR proteins, which act on DNA double-stranded ends and DNA single-stranded gaps, respectively; the central synaptic steps are catalyzed by the ubiquitous DNA-binding protein RecA; and the postsynaptic phase involves either RuvABC or RecG proteins, which catalyze branch-migration and, in the case of RuvABC, the cleavage of Holliday junctions. Here, we review the biochemical properties of these molecular machines and analyze how, in light of these properties, the phenotypes of null mutants allow us to define their biological function(s). The consequences of point mutations on the biochemical properties of recombination enzymes and on cell phenotypes help refine the molecular mechanisms of action and the biological roles of recombination proteins. Given the high level of conservation of key proteins like RecA and the conservation of the principles of action of all recombination proteins, the deep knowledge acquired during decades of studies of homologous recombination in bacteria is the foundation of our present understanding of the processes that govern genome stability and evolution in all living organisms.

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Image of Figure 1
Figure 1

In order for viable recombinants to be formed, the linear fragment must be integrated by an even number of crossover events (normally expected to be two).

Citation: Michel B, Leach D. 2012. Homologous Recombination—Enzymes and Pathways, EcoSal Plus 2012; doi:10.1128/ecosalplus.7.2.7
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Image of Figure 2
Figure 2

(A) Ends-in recombination is the situation expected when a chromosome has a DSB. (B) Ends-out recombination occurs when a DNA fragment is transferred to a recipient cell. (C) One-ended recombination occurs when a replication fork is broken. In all three situations, RecBCD initiates recombination by resection of the DNA end, followed by loading RecA protein onto a 3′-ended single strand. This RecA-coated single strand invades an intact duplex and sets up a D loop, which can be converted to a replication fork by resolution of the Holliday junction associated with it by RuvABC and/or RecG. This resolution generates a replication fork, and PriA acts to load the replicative helicase, DnaB, in order for processive DNA replication to be carried out. The timing of Holliday junction resolution relative to the initiation of replication is not currently known.

Citation: Michel B, Leach D. 2012. Homologous Recombination—Enzymes and Pathways, EcoSal Plus 2012; doi:10.1128/ecosalplus.7.2.7
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Image of Figure 3
Figure 3

A persistent gap is coated by RecA protein through the action of the RecFOR complex. This invades an intact duplex and establishes a joint molecule containing one or more Holliday junctions. These are resolved by the action of RuvABC and/or RecG, and the gap is filled by DNA synthesis.

Citation: Michel B, Leach D. 2012. Homologous Recombination—Enzymes and Pathways, EcoSal Plus 2012; doi:10.1128/ecosalplus.7.2.7
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Figure 4

The ATP-binding core is shown in blue, and the C-terminal domain is shown in green. (Courtesy of Vitold Galkin and Edward Egelman, University of Virginia, Charlottesville.)

Citation: Michel B, Leach D. 2012. Homologous Recombination—Enzymes and Pathways, EcoSal Plus 2012; doi:10.1128/ecosalplus.7.2.7
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Image of Figure 5
Figure 5

(A) A strand invasion reaction. A RecA filament formed on a linear ssDNA molecule is incubated in the presence of a homologous circular dsDNA molecule. Invasion by the 3′ end of the RecA filament causes D-loop formation. (B) A three-strand reaction. The RecA filament forms on a circular ssDNA molecule, and incubation with a homologous linear dsDNA molecule produces a nicked circular duplex and a linear ssDNA molecule. (C) A four-strand reaction. The RecA filament forms in the single-stranded region of a gapped duplex and invades the end of a linear dsDNA homologous molecule. Recombination intermediates are detectable, and the full reaction produces a nicked circular dsDNA molecule and a linear dsDNA molecule.

Citation: Michel B, Leach D. 2012. Homologous Recombination—Enzymes and Pathways, EcoSal Plus 2012; doi:10.1128/ecosalplus.7.2.7
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Image of Figure 6
Figure 6

(A) A DNA DSB is generated by a damaging agent such as gamma irradiation. This can be repaired by an “ends-in” recombination reaction with an intact copy of the DNA, which would normally be a sister chromosome. (B) A DNA fragment is introduced into a cell (e.g., by conjugation, transduction, or transformation). This can recombine with the host genome in an “ends-out” reaction. (C) Replication fork reversal occurs following interruption of DNA replication. Here the newly replicated strands become annealed to form a DNA end. This end can be degraded, as shown in C(i), to regenerate a replication fork; or it can be recombined with the parental strands, as shown in C(ii), again regenerating a replication fork following the formation and resolution of Holliday junctions (not shown). (D) Replication fork collapse following the encounter of a replication fork with an interruption in a template stand, as shown in D(i). The recombination, indicated in D(ii), will regenerate a replication fork following the formation and resolution of a Holliday junction (not shown). (E) Replication fork collision when a fork is blocked by a protein such as Tus bound to a site as shown in E(i). Repair occurs by recombination, and the repair forks dislodge the bound Tus protein; see E(ii). (F) Postreplication breakage of one of the DNA strands to generate a DSB that is repaired by recombination with an intact DNA strand. A hairpin formed on the lagging-strand template is shown in F(i). This is cleaved to generate the DSB shown in F(ii). The DNA is colored to indicate the strands with DNA ends (red) and the strands without ends (blue). DNA degradation is indicated by a yellow symbol in C(i), Tus protein bound to is indicated by a red stop sign in panel E, and recombination is indicated by a multiplier (×).

Citation: Michel B, Leach D. 2012. Homologous Recombination—Enzymes and Pathways, EcoSal Plus 2012; doi:10.1128/ecosalplus.7.2.7
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Figure 7

The patterns of unwinding and cleavage of DNA are determined as a function of the free Mg and the Mg/ATP ratio. At low free Mg and low Mg/ATP ratio, RecBCD translocates faster on DNA and