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Chapter 7 : DNA Site-Specific Resolution Systems

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Abstract:

Resolution of multimeric forms of circular plasmids and chromosomes is mediated by site-specific recombination, an efficient and tightly controlled DNA breakage and joining reaction occurring at the level of determined DNA sequences. Site-specific recombinases, the enzymes that catalyze this type of reaction, fall into two families of proteins: the serine-recombinase and tyrosine-recombinase families. The chapter discusses the mechanisms that generate DNA multimers and their consequence on the segregational stability of bacterial replicons, and also provides an overview of the variety of site-specific resolution systems found on circular plasmids and chromosomes and their relationship to other recombination systems. It focuses on site-specific resolution systems of the serine-recombinase family, and plasmid and chromosome resolution systems of the tyrosine recombinase family. The topology of the recombination reaction catalyzed by other resolvases of the serine-recombinase family, such as the ParA protein of RP4/RK2, the resolvase of ISXc5, the Sin recombinase of , and the β recombinase of pSM19035, was found to be identical to that reported for the cointegrate resolution system of Tn3-family transposons. Studies on plasmid and transposon resolution systems provide fascinating examples of convergent evolution, in which structurally and biochemically unrelated molecular machines have been adapted to bring about functionally similar DNA rearrangements in an exquisitely controlled manner.

Citation: Hallet B, Vanhooff V, Cornet F. 2004. DNA Site-Specific Resolution Systems, p 145-180. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch7
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Image of Figure 1
Figure 1

Formation and resolution of circular replicon dimers. Homologous recombination (HR) occurring during or after replication of a circular plasmid or chromosome produces a dimeric DNA molecule in which the two copies of the replicon are fused in a head-to-tail configuration. The dimer is converted to monomers by site-specific recombination between the duplicated copies of the replicon resolution site (colored in black and gray). The core recombination sites where the recombinase catalyzes the strand-exchange reaction are represented by squares. The adjacent colored regions are regulatory sequences that are often associated with the recombination site to control the recombination reaction. Circles represent the plasmid or chromosome replication origin.

Citation: Hallet B, Vanhooff V, Cornet F. 2004. DNA Site-Specific Resolution Systems, p 145-180. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch7
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Image of Figure 2
Figure 2

Formation and resolution of chromosome dimers in E. coli. In 10 to 15% of dividing cells, recombinational repair of stalled replication forks (arrowheads) results in the formation of a chromosome dimer by HR between the sister chromatids (represented by solid and dotted black lines). When replication is completed, the chromosome dimer is resolved by XerCD-mediated recombination at (inverted arrows). Recombination takes place at the closing septum and is assisted by the cell division protein FtsK. is the chromosome replication origin.

Citation: Hallet B, Vanhooff V, Cornet F. 2004. DNA Site-Specific Resolution Systems, p 145-180. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch7
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Figure 3

The effect of multimerization on randomly inherited multicopy plasmids. The figure illustrates a theoretical situation in which the plasmid reaches four monomeric copies before cell division. The replication origin is shown as a black circle, and the plasmid resolution site is represented by a triangle. If segregation occurs at random, the probability of producing a plasmid- free cell is given by the relation =2, where n is the number of independently inheritable units ( ). For a plasmid that has four monomeric copies, this probability is 0.125. If a plasmid dimer forms (HR) and is not resolved by site-specific recombination (SSR), and if the number of replication origins per cell is kept constant, the number of segregation units falls to 2 and the probability of plasmid loss increases to 0.5.

Citation: Hallet B, Vanhooff V, Cornet F. 2004. DNA Site-Specific Resolution Systems, p 145-180. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch7
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Image of Figure 4
Figure 4

Phylogenetic tree of plasmid and transposon resolvases of the serine-recombinase family. Plasmid resolvases that have been characterized at a genetic or biochemical level are in bold. Asterisks indicate unusually large proteins of the family. Mu-like transposons are underlined. Accession numbers of the protein sequences are listed on the right.

Citation: Hallet B, Vanhooff V, Cornet F. 2004. DNA Site-Specific Resolution Systems, p 145-180. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch7
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Figure 5

Replicative transposition pathway of resolvase-encoding transposons. The transposon DNA strands are shown in bold, donor backbone sequences as dotted lines, and the target molecule as thin lines. L and R designate the transposon left and right ends, respectively. The resolution site is represented by a square. During intermolecular transposition, DNA strand transfer mediated by the transposase followed by replication by the host machinery results in the formation of a cointegrate in which the donor and target DNA molecules are fused by directly repeated copies of the transposon. The cointegrate is resolved by resolvase-mediated recombination between the duplicated copies of .

Citation: Hallet B, Vanhooff V, Cornet F. 2004. DNA Site-Specific Resolution Systems, p 145-180. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch7
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Figure 6

Recombination site organization of resolvases of the serine-recombinase family. Arrows represent 12-bp resolvase-binding motifs. Shaded arrows are for sequences that have a poorer match to the consensus. Cylinders show the end of the recombinase coding sequence. Boxed triangles indicate the position of the Hbsu binding sites in the resolution site of Sin. The organization ofTn and IS resolution sites was revised by Rowland et al. ( ).

Citation: Hallet B, Vanhooff V, Cornet F. 2004. DNA Site-Specific Resolution Systems, p 145-180. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch7
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Figure 7

Phylogenetic tree of selected chromosome, plasmid, and transposon resolvases from the tyrosine-rccombinase family. Plasmid recombinases for which functional data are available are in bold. Accession numbers of the protein sequences are listed on the right. The Tn resolvase sequence is according to that of De Mot et al. ( ). .

Citation: Hallet B, Vanhooff V, Cornet F. 2004. DNA Site-Specific Resolution Systems, p 145-180. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch7
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Figure 8

Resolution site organization of tyrosine recombinases. Arrows and open boxes (in the case of ResD) indicate the position of recombinase-binding elements. The recombination core sites are aligned on the left. Shaded boxes represent additional motifs and accessory sequences that are bound by auxiliary proteins as indicated. Cylinders show the end of the recombinase gene when present in the same locus. The length and the distance (in base pairs) that separate the different sequence elements are indicated below each recombination site.

Citation: Hallet B, Vanhooff V, Cornet F. 2004. DNA Site-Specific Resolution Systems, p 145-180. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch7
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Figure 9

Structural diversity among serine recombinases. The conserved catalytic domain (∼120 amino acid residues) is colored in dark gray. Brackets show the position of five conserved motifs (a to e) in the protein sequence ( ). The position of residues thought to be directly involved in catalysis ( ) is indicated, and the active site serine is circled. DNA-binding domains are colored in medium gray. White cylinders indicate the presence of additional extensions of unknown function at the N or C terminus of the proteins.

Citation: Hallet B, Vanhooff V, Cornet F. 2004. DNA Site-Specific Resolution Systems, p 145-180. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch7
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Figure 10

Concerted DNA breakage and rejoining reactions catalyzed by serine recombinases. The DNA strands of the recombination partners are shown in black and gray. Inverted arrows represent the recombinase recognition motifs in the core recombination sites. Vertical bars are the central dinuclcotides that are exchanged between the two DNA duplexes during recombination. The core site-bound recombinase molecules (shaded ovals) cleave all four DNA strands, using their active site serine as a nucleophile. DNA strands are exchanged by 180° rotation of the cleaved half-sites. The 3′ OH of the cleaved DNA ends attack the phosphoseryl DNA-protein bond in the partner to reseal the DNA strands in the recombinant configuration.

Citation: Hallet B, Vanhooff V, Cornet F. 2004. DNA Site-Specific Resolution Systems, p 145-180. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch7
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Figure 11

Structure of the γδ resolvase dimer bound to core recombination site I ( ). Two orthogonal views of the complex are shown: a lateral view on the left, and a section view across the DNA on the right. The DNA strands are shown in a black and white space-fill representation. The scissile phosphates (P) are highlighted. The resolvase dimer is represented in ribbon diagrams, with one monomer colored in white and the other in dark gray. The active site serine side chains (S) are highlighted in a ball-and-stick configuration. The position of the kink in α-helix E of one resolvase monomer is indicated.

Citation: Hallet B, Vanhooff V, Cornet F. 2004. DNA Site-Specific Resolution Systems, p 145-180. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch7
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Figure 12

Current models for strand exchange by serine recombinases. Only the subunit rotation (A) and domain-swapping (B) models are shown. The half-site-bound recombinase is drawn based on gd resolvase crystal structure. The DNA is represented by cylinders. For both models, the complex containing the recombinase tetramer bound onto the two recombination core sites is shown after cleavage (left) and before rejoining (right) the four DNA strands. The recombinase catalytic domains lie inside the complex and the DNA-binding domains outside. In the subunit rotation model (A) the DNA strands are exchanged by 180° rotation of one pair of half-site-bound recombinase subunits with respect to the other. This requires the complete dissociation and reassociation of recombinase dimers within the complex. In the domain-swapping model (B), only the portions of the catalytic domain that are covalently linked to the DNA exchange position, leaving the initial dimer interface unchanged.

Citation: Hallet B, Vanhooff V, Cornet F. 2004. DNA Site-Specific Resolution Systems, p 145-180. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch7
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Figure 13

Domain structure of tyrosine recombinases and eukaryotic type IB topoisomerases. The C-terminal catalytic domain of the proteins is shaded in dark gray. Brackets show the position of three conserved regions of the catalytic domain: boxes I, II, and III. Residues of the catalytic signature of the family arc indicated, and the tyrosine nucleophile is circled. Other protein regions are colored in different shades of gray to indicate that they are structurally unrelated. Integrases, such as λ Int, have an additional DNA-binding domain at the C terminus to bind the arm-site sequences of the recombination site ( ). In the human type IB topoisomerasc core enzyme (Hum. Topo IB, residues 215 to 765), the catalytic domain is interrupted by a linker region spanning between the active-site histidine and the tyrosine nucleophile ( ). Vac. Topo IB, type IB topoisomerase of vaccinia virus.

Citation: Hallet B, Vanhooff V, Cornet F. 2004. DNA Site-Specific Resolution Systems, p 145-180. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch7
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Figure 14

The strand-swapping-isomerization model for the site-specific recombination reaction catalyzed by tyrosine recombinases. The different reaction intermediates are drawn based on the Cre/DNA complex structures. The catalytic domain of each recombinase molecule is represented by an oval. The stem-and-ball extensions depict the cyclical donor-acceptor interactions that interconnect the four active sites in the recombinase tetramer. The rccombining DNA segments are colored in black and gray, with inverted arrows representing the recombinase-binding motifs. In the initial synapse, the recombination sites are aligned antiparallel, and the DNA is bent to expose one specific strand of each duplex in the central cavity of the complex. In this configuration of the synapse the light gray subunits have an extended C-terminal tail, which orients the catalytic tyrosine (circled Y) and possibily other active-site residues for nucleophilic attack of the target phosphate (arrowhead). After cleavage, three to four nucleotides from the central region are swapped between the partner duplexes to orient the cleaved -OH ends for the rejoining step. Nucleophilic attack of the DNA-recombinase phosphotyrosyl bonds by the invading -OH DNA ends releases the protein and generates a twofold symmetric HJ junction intermediate in which one pair of DNA strands is exchanged. Coupled conformational changes in DNA and protein interfaces lead to synchronized inactivation of the light gray recombinase subunits and concomitant activation of the dark gray subunits for the exchange of the second pair of strands.

Citation: Hallet B, Vanhooff V, Cornet F. 2004. DNA Site-Specific Resolution Systems, p 145-180. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch7
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Figure 15

Structure of a Cre dimer hound to the site ( ). A space-filling model of the DNA shows one strand in white and the other in black. Scissile phosphates are circled. The Cre protein is shown in a ribbon-cylinder representation, with the active-site tyrosine highlighted in a ball-and-stick configuration. The white Cre monomer is activated for cleavage, and its C-terminal α-helix N (α-N) is donated to the acceptor pocket of the adjacent subunit. The linker peptide that connects α-helix N to α-helix M (α-M) is in an extended conformation, which positions the active-site tyrosine for nucleophilic attack of the phosphate.

Citation: Hallet B, Vanhooff V, Cornet F. 2004. DNA Site-Specific Resolution Systems, p 145-180. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch7
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Figure 16

Synapse topology of different site-specific resolution systems. The recombination complexes are shown before and after strand exchange (black arrow). The topology of the recombination products is shown to the right. The initial DNA substrates contain directly repeated copies of the recombination sites colored in white and gray. The two sites divide the substrate into two domains shown as thick and thin lines. Arrows represent the core recombination sites, whereas boxes and ribbons are regulatory recombinase-binding sites or accessory sequences. The Hbsu-binding site of the Sin resolution site is represented by a diamond. For further details on recombination site organization, see Fig. 6 and 8 .

Citation: Hallet B, Vanhooff V, Cornet F. 2004. DNA Site-Specific Resolution Systems, p 145-180. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch7
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Figure 17

Models for the structural organization of topologically defined synaptic complexes. Each complex is modeled based on the crystal structure of the participating proteins. DNA is represented by tubes, with one recombination site shaded and the other colored in white. (A) The Tn/γδ resolvase synaptosome ( ). DNA is wrapped around a pair of interlocked protein filaments constituted of the catalytic domains of the six resolvase dimers bound to the two sites. Adjacent dimers interact through the so-called 2–3′ interface (white double-arrow). Each resolvase dimer contacts its partner of the opposite site using the same synaptic interface (black double-arrow). The resolvase DNA-binding domains, represented as cup-like structures, grasp the DNA at the outer surface of the complex. (B) The synaptic complex of Sin and β recombinases ( ). Recombinase dimers form the same tetrameric arrangement as the resolvase dimers bound to sites I and III in the synaptosome. The DNA-bending activity of Hbsu replaces the architectural role of the site III-bound resolvase subunits. (C) Architecture of Xer recombination complex at ( ). The ArgR hexamer is sandwiched between two PepA hexamers. The accessory sequences wrap around the complex by running across three large grooves at the surface of PepA. The XerCD-core complex is represented with the recombinase C-terminal domains oriented toward the accessory proteins, in a configuration that activates XerC for the first strand exchange ( ).

Citation: Hallet B, Vanhooff V, Cornet F. 2004. DNA Site-Specific Resolution Systems, p 145-180. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch7
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Figure 18

The relocation model for Xer-mediated chromosome dimer resolution at The top panel represents a dividing cell with two monomeric sister chromosomes (shaded areas). Cylinders represent hypothetical nucleoid organizing elements. Each chromosome is shown with an Ori domain containing the replication origin oriC at the cell poles and a Ter domain located close to the septum ( ). The Ter domain contains the recombination site (black and white square) bound by the XerCD recombinase (open circles). An oligomer of FtsK forms as a pore through the septum. Chromosome segregation is completed and the sites do not interact with FtsK. The two lower panels represent enlargements of the central part of the dividing cell when a chromosome dimer has formed. Two DNA stretches link the sister chromosomes through the FtsK pore. FtsK (alone or with help of other factors) tracks along the DNA following hypothetical polar sequence elements of the Ter domain (black arrows). DNA tracking stops when FtsK raises the /XerCDcomplexes, or an oppositely polarized region. FtsK-dependent recombination between the sites resolves the chromosome dimer and segregation can proceed.

Citation: Hallet B, Vanhooff V, Cornet F. 2004. DNA Site-Specific Resolution Systems, p 145-180. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch7
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