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Domain 4:

Synthesis and Processing of Macromolecules

Homologous Recombination—Experimental Systems, Analysis, and Significance

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  • Author: Andrei Kuzminov1
  • Editors: Susan T. Lovett2, Andrei Kuzminov3
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Microbiology, University of Illinois at Urbana-Champaign, Urbana, IL 61801; 2: Brandeis University, Waltham, MA; 3: The Schoold of Molecular and Cellular Biology, University of Illinois at Urbana-Champaign, Urbana, IL
  • Received 12 May 2011 Accepted 15 August 2011 Published 01 December 2011
  • Address correspondence to Andrei Kuzminov kuzminov@life.uiuc.edu
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  • Abstract:

    Homologous recombination is the most complex of all recombination events that shape genomes and produce material for evolution. Homologous recombination events are exchanges between DNA molecules in the lengthy regions of shared identity, catalyzed by a group of dedicated enzymes. There is a variety of experimental systems in and to detect homologous recombination events of several different kinds. Genetic analysis of homologous recombination reveals three separate phases of this process: pre-synapsis (the early phase), synapsis (homologous strand exchange), and post-synapsis (the late phase). In , there are at least two independent pathway of the early phase and at least two independent pathways of the late phase. All this complexity is incongruent with the originally ascribed role of homologous recombination as accelerator of genome evolution: there is simply not enough duplication and repetition in enterobacterial genomes for homologous recombination to have a detectable evolutionary role and therefore not enough selection to maintain such a complexity. At the same time, the mechanisms of homologous recombination are uniquely suited for repair of complex DNA lesions called chromosomal lesions. In fact, the two major classes of chromosomal lesions are recognized and processed by the two individual pathways at the early phase of homologous recombination. It follows, therefore, that homologous recombination events are occasional reflections of the continual recombinational repair, made possible in cases of natural or artificial genome redundancy.

  • Citation: Kuzminov A. 2011. Homologous Recombination—Experimental Systems, Analysis, and Significance, EcoSal Plus 2011; doi:10.1128/ecosalplus.7.2.6

Key Concept Ranking

DNA Synthesis
0.60104156
Genetic Recombination
0.5993177
Genetic Elements
0.5712247
DNA Polymerase I
0.4883891
0.60104156

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/content/journal/ecosalplus/10.1128/ecosalplus.7.2.6
2011-12-01
2017-05-29

Abstract:

Homologous recombination is the most complex of all recombination events that shape genomes and produce material for evolution. Homologous recombination events are exchanges between DNA molecules in the lengthy regions of shared identity, catalyzed by a group of dedicated enzymes. There is a variety of experimental systems in and to detect homologous recombination events of several different kinds. Genetic analysis of homologous recombination reveals three separate phases of this process: pre-synapsis (the early phase), synapsis (homologous strand exchange), and post-synapsis (the late phase). In , there are at least two independent pathway of the early phase and at least two independent pathways of the late phase. All this complexity is incongruent with the originally ascribed role of homologous recombination as accelerator of genome evolution: there is simply not enough duplication and repetition in enterobacterial genomes for homologous recombination to have a detectable evolutionary role and therefore not enough selection to maintain such a complexity. At the same time, the mechanisms of homologous recombination are uniquely suited for repair of complex DNA lesions called chromosomal lesions. In fact, the two major classes of chromosomal lesions are recognized and processed by the two individual pathways at the early phase of homologous recombination. It follows, therefore, that homologous recombination events are occasional reflections of the continual recombinational repair, made possible in cases of natural or artificial genome redundancy.

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Figures

Image of Figure 1
Figure 1

DNA duplex is shown as a single line. The straight lines (whether open or filled) represent homologous DNA, and the wavy opposite straight lines represent heterologous DNAs. Within the diagram, the letters A and B, a and b, and Y and Z represent “markers”—DNA sequences that confer distinct phenotypes. Uppercase “A” and lowercase “a” represent alleles of the same gene. Explanations are in the text.

Citation: Kuzminov A. 2011. Homologous Recombination—Experimental Systems, Analysis, and Significance, EcoSal Plus 2011; doi:10.1128/ecosalplus.7.2.6
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Figure 2

Citation: Kuzminov A. 2011. Homologous Recombination—Experimental Systems, Analysis, and Significance, EcoSal Plus 2011; doi:10.1128/ecosalplus.7.2.6
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Figure 3

Citation: Kuzminov A. 2011. Homologous Recombination—Experimental Systems, Analysis, and Significance, EcoSal Plus 2011; doi:10.1128/ecosalplus.7.2.6
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Figure 4

Each diagonal pair of resolution cuts is numbered either “1” or “2” for each junction. If the two junctions freely isomerize and are resolved independently of each other, four outcomes of the resolution are expected. In two of the outcomes, the chromosome arms will be exchanged, resulting in recombinant chromosomes. (A) A joint molecule with two junctions as shown in Fig. 2, right . (B) The same joint molecule isomerized to show both junctions in the open planar configuration ( 18 ). (C) The four resolution outcomes, numbered according to the resolution options realized at the left and the right junctions. Note that two outcomes (1–1 and 2–2) produce chromosomes with recombinant shoulders, while the other two outcomes (1–2 and 2–1) produce chromosomes with parental shoulders.

Citation: Kuzminov A. 2011. Homologous Recombination—Experimental Systems, Analysis, and Significance, EcoSal Plus 2011; doi:10.1128/ecosalplus.7.2.6
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Figure 5

(A) Recombination between circular and linear chromosomes by the region of shared homology inserts the circular chromosome into the linear one. (B) Recombination between two directly oriented regions of homology on the same chromosome leads to the loss of genetic information (deletion) in the form of a circle.

Citation: Kuzminov A. 2011. Homologous Recombination—Experimental Systems, Analysis, and Significance, EcoSal Plus 2011; doi:10.1128/ecosalplus.7.2.6
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Image of Figure 6
Figure 6

(A) Recombination between inverted repeats within the same chromosome generates an inversion. (B) Recombination between sister chromatids carrying direct repeats can lead to unequal sister chromatid exchange (deletion in one chromatid, duplication in the other). (C) Recombination between sister chromatids carrying inverted repeats generates dysfunctional chromosomes and most of the time will result in cell death.

Citation: Kuzminov A. 2011. Homologous Recombination—Experimental Systems, Analysis, and Significance, EcoSal Plus 2011; doi:10.1128/ecosalplus.7.2.6
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Image of Figure 7
Figure 7

The two parental chromosomes are shown at the top. Alternatively, these could be two repeated sequences within the same chromosome. Although the two chromosomes (or repeats) are essentially homologous over their entire length, they are assumed to have enough markers (genetically scorable disagreements in their primary DNA sequences) to facilitate fine mapping of the recombination events and conversion tracts. The four major types of recombination events, all results of alternative processing of a single recombination intermediate as in Fig. 2 (right) and Fig. 4A , are presented.

Citation: Kuzminov A. 2011. Homologous Recombination—Experimental Systems, Analysis, and Significance, EcoSal Plus 2011; doi:10.1128/ecosalplus.7.2.6
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Figure 8

Explanations are given in the text. (A) Mapping based on segregation frequencies in eukaryotes. (B) Growth of a unicellular eukaryote with periodic sexual events: either syngamy or meiosis. Circles denote gametes (1n cells), and ovals denote zygotes (2n cells). (C) Strictly clonal growth in the majority of bacteria. (D) Mapping based on coinheritance frequencies in bacteria.

Citation: Kuzminov A. 2011. Homologous Recombination—Experimental Systems, Analysis, and Significance, EcoSal Plus 2011; doi:10.1128/ecosalplus.7.2.6
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Figure 9

(A) A single exchange with a linear subchromosomal fragment introduces unprotected ends into the chromosome, leading to chromosome degradation. The chromosome is shown linear, with telomere-protected ends, which does not change the argument. (B) The same situation as in panel A, but with two exchanges, which leave the chromosome physically intact, even though genetically different. (C) A single exchange between two circular chromosomes creates a chromosomal dimer, which will kill the cell if left unresolved. (D) The same situation as in panel C, but again with two exchanges that keep the two recombining chromosomes monomeric and, therefore, functional. (E) The double exchange from panel B is shown with markers to illustrate a better applicability of coinheritance, rather than segregation, to quantify crosses in systems in which only double exchanges survive.

Citation: Kuzminov A. 2011. Homologous Recombination—Experimental Systems, Analysis, and Significance, EcoSal Plus 2011; doi:10.1128/ecosalplus.7.2.6
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Figure 10

In this case, both strands of participating DNA duplexes are shown. One homologous duplex has open strands; the other homolog has filled strands.

Citation: Kuzminov A. 2011. Homologous Recombination—Experimental Systems, Analysis, and Significance, EcoSal Plus 2011; doi:10.1128/ecosalplus.7.2.6
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Figure 11

Despite the argument of Fig. 9 , for the sake of clarity, a single crossover is shown in all cases.

Citation: Kuzminov A. 2011. Homologous Recombination—Experimental Systems, Analysis, and Significance, EcoSal Plus 2011; doi:10.1128/ecosalplus.7.2.6
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Figure 12

This is, basically, a full-chromosome version of Fig. 6C .

Citation: Kuzminov A. 2011. Homologous Recombination—Experimental Systems, Analysis, and Significance, EcoSal Plus 2011; doi:10.1128/ecosalplus.7.2.6
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Image of Figure 13
Figure 13

The scheme is based on the results of the substrate analysis and the epistatic analysis. The chromosomal duplex DNA is shown as a single line, with the exception of the double Holliday junction, which is shown double-stranded. See the explanations in the text.

Citation: Kuzminov A. 2011. Homologous Recombination—Experimental Systems, Analysis, and Significance, EcoSal Plus 2011; doi:10.1128/ecosalplus.7.2.6
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Figure 14

(A) A DNA molecule with a two-strand lesion (small open rectangles in the filled duplex) is shown homologously aligned with an intact homolog (open duplex). (B) The two sequences have exchanged strands, converting the two-strand lesion into a pair of one-strand lesions. (C) Holliday junction resolution (the nicking of strands is shown in panel B) separates the chromosomes from each other. (D) Excision repair removes the one-strand lesions, completing the overall repair reaction. Note that if the black and white “parental” DNAs are homologs (carry genetically scorable differences), rather than identical sisters, the resulting chromosomes may be detectably recombinant.

Citation: Kuzminov A. 2011. Homologous Recombination—Experimental Systems, Analysis, and Significance, EcoSal Plus 2011; doi:10.1128/ecosalplus.7.2.6
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Image of Figure 15
Figure 15

The chromosome is shown by a double-line square. Yellow highlights in red frames are either double-strand breaks or their consequences. Brown circles with black arrows nearby are centromeres and the direction they are going. Blue arrows are normal cellular processes (chromosomal replication and segregation). Magenta arrows are chromosomal fragmentation. Red arrows show the consequences of chromosomal fragmentation. (A) Chromosome. (B) Initiation of chromosomal replication. (C) Initiation of sister chromosome segregation. (D) Fragmentation of nonreplicating chromosome. (E) Fragmentation of replicating chromosome. (F) Fragmentation of segregating chromosome. (G) Gene loss due to DNA degradation form unprotected ends. (H) Inability to replicate the chromosomal segment, separated from by double-strand breaks. (I) Inability to segregate chromosomal segment, separated from centromere by double-strand breaks.

Citation: Kuzminov A. 2011. Homologous Recombination—Experimental Systems, Analysis, and Significance, EcoSal Plus 2011; doi:10.1128/ecosalplus.7.2.6
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Image of Figure 16
Figure 16

A replication fork is moving from left to right along the template DNA with unrepaired one-strand lesions. The template on the left contains a noncoding lesion (T=T, thymine dimer), while the template on the right has a single-strand interruption. A replication fork encounter with a noncoding lesion generates a daughter-strand gap (left), while a replication fork encounter with a nick generates a one-ended double-strand break (= double-strand end, right).

Citation: Kuzminov A. 2011. Homologous Recombination—Experimental Systems, Analysis, and Significance, EcoSal Plus 2011; doi:10.1128/ecosalplus.7.2.6
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Image of Figure 17
Figure 17

This classification is based, on one hand, on whether formation of these lesions depends on DNA replication (“direct” versus “replication-dependent”) and, on the other hand, on the number of DNA strands interrupted in the final format of the lesion. In , the repair of chromosomal lesions with either one or two strands interrupted completely depends on recombinational repair. Chromosomal dimers are resolved by the FtsK-XerCD/ resolution system (site-specific recombination). Locked replication fork is still a hypothetical lesion, consistent with certain gross chromosomal rearrangements, and whose (hypothetical) repair is likely to depend on HR.

Citation: Kuzminov A. 2011. Homologous Recombination—Experimental Systems, Analysis, and Significance, EcoSal Plus 2011; doi:10.1128/ecosalplus.7.2.6
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Image of Figure 18
Figure 18

On the left, the daughter-strand gap repair pathway is shown, while the double-strand end repair pathway is shown on the right. Stages are marked with enzymes that catalyze them.

Citation: Kuzminov A. 2011. Homologous Recombination—Experimental Systems, Analysis, and Significance, EcoSal Plus 2011; doi:10.1128/ecosalplus.7.2.6
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Tables

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Table 1

Comparison of various types of genetic recombination with respect to frequency, DNA requirements, and the enzymes that catalyze these events

Citation: Kuzminov A. 2011. Homologous Recombination—Experimental Systems, Analysis, and Significance, EcoSal Plus 2011; doi:10.1128/ecosalplus.7.2.6
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Table 2

Conjugation recombination deficiency indices for various mutants in HR in wild-type, as well as in and , backgrounds

Citation: Kuzminov A. 2011. Homologous Recombination—Experimental Systems, Analysis, and Significance, EcoSal Plus 2011; doi:10.1128/ecosalplus.7.2.6
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Table 3

Quantitative illustration of substrate analysis: conjugational (linear x circular) versus plasmid (circular x circular) recombination deficiency indices for various single mutants in HR

Citation: Kuzminov A. 2011. Homologous Recombination—Experimental Systems, Analysis, and Significance, EcoSal Plus 2011; doi:10.1128/ecosalplus.7.2.6
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Table 4

Quantitative illustration of epistatic analysis using resistance to UV-irradiation as a read-out

Citation: Kuzminov A. 2011. Homologous Recombination—Experimental Systems, Analysis, and Significance, EcoSal Plus 2011; doi:10.1128/ecosalplus.7.2.6
Generic image for table
Table 5

Viability of HR mutants and their sensitivity to different kinds of DNA-damaging treatments

Citation: Kuzminov A. 2011. Homologous Recombination—Experimental Systems, Analysis, and Significance, EcoSal Plus 2011; doi:10.1128/ecosalplus.7.2.6

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