1887

Chapter 3 : The Serine Recombinases

Author: W. Marshall Stark1
VIEW AFFILIATIONS HIDE AFFILIATIONS
Affiliations: 1: Institute of Molecular, Cell and Systems Biology, University of Glasgow, Bower Building, Glasgow G12 8QQ, Scotland, United Kingdom
Content Type: Monograph
Publication Year: 2015

Category: Clinical Microbiology

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Preview Magnify
Zoom in
Zoomout

The Serine Recombinases, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555819217/9781555819200_Chap03-1.gif /docserver/preview/fulltext/10.1128/9781555819217/9781555819200_Chap03-2.gif

Abstract:

The term site-specific recombination encompasses a group of biological processes that, unlike homologous recombination, promote rearrangements of DNA by breaking and rejoining strands at precisely defined sequence positions. In a canonical site-specific recombination event, two discrete sites (sequences of DNA, typically a few tens of base pairs long) are broken, and the ends are reciprocally exchanged and rejoined, resulting in recombinant products ( Fig. 1 ). Site-specific recombination does not require extensive sequence homology; the sites are identified and brought together by protein–DNA and protein–protein interactions involving specialized recombinase proteins, unlike homologous recombination where DNA–DNA interactions define the loci of strand exchange. “Conservative” site-specific recombination systems form recombinants without any requirement for DNA synthesis or high-energy cofactors. Some other biological processes such as transposition are sometimes categorized with site-specific recombination because of common features including cleavage and rejoining of DNA strands at precise positions defined by protein–DNA interactions, but these processes may require DNA synthesis and/or ligase-mediated rejoining of DNA strands. The systems discussed in this chapter conform to the strict “conservative” definition. General aspects of site-specific recombination have been reviewed elsewhere ( ).

Citation: Stark W. 2015. The Serine Recombinases, p 73-89. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0046-2014
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

The Serine Recombinases
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555819217.chap3-1,webId=/content/author/10.1128/9781555819217.chap3-1,properties={foaf_givenname=W. Marshall, foaf_name=W. Marshall Stark, foaf_surname=Stark, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555819217.chap3-aff1]]}]]
Citation: Stark W. 2015. The Serine Recombinases, p 73-89. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0046-2014
/content/10.1128/9781555819217.chap3.fig3-1
Figure 1
Site-specific recombination. Two sites (pointed boxes) in double-helical DNA (shown as double lines) are recognized by a recombinase protein (not shown), and then cut and rejoined to form recombinants.
10.1128/9781555819217/fig3-1_thmb.gif
10.1128/9781555819217/fig3-1.gif
Image of Figure 1
Figure 1

Site-specific recombination. Two sites (pointed boxes) in double-helical DNA (shown as double lines) are recognized by a recombinase protein (not shown), and then cut and rejoined to form recombinants.

Citation: Stark W. 2015. The Serine Recombinases, p 73-89. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0046-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/10.1128/9781555819217.chap3.fig3-2
Figure 2
Site-specific recombination outcomes. (a) Recombination between two sites in separate linear DNA molecules results in two linear recombinant products. Usually, the sites have a polarity (indicated by the pointed boxes) such that the lower pathway (red arrow) is forbidden. (b) Recombination between two sites in separate DNA molecules, when one or both of the molecules is circular, results in a single product molecule containing two sites in direct repeat. This is called integration or fusion. The “reverse” reaction splits a molecule containing two sites into two product molecules, one or both of which are circular. This is called resolution, excision, or deletion (depending on the biological context). (c) Recombination between two sites in inverted repeat in a DNA molecule inverts the orientation of one segment of DNA relative to the other. This is called inversion.
10.1128/9781555819217/fig3-2_thmb.gif
10.1128/9781555819217/fig3-2.gif
Image of Figure 2
Figure 2

Site-specific recombination outcomes. (a) Recombination between two sites in separate linear DNA molecules results in two linear recombinant products. Usually, the sites have a polarity (indicated by the pointed boxes) such that the lower pathway (red arrow) is forbidden. (b) Recombination between two sites in separate DNA molecules, when one or both of the molecules is circular, results in a single product molecule containing two sites in direct repeat. This is called integration or fusion. The “reverse” reaction splits a molecule containing two sites into two product molecules, one or both of which are circular. This is called resolution, excision, or deletion (depending on the biological context). (c) Recombination between two sites in inverted repeat in a DNA molecule inverts the orientation of one segment of DNA relative to the other. This is called inversion.

Citation: Stark W. 2015. The Serine Recombinases, p 73-89. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0046-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/10.1128/9781555819217.chap3.fig3-3
Figure 3
Recombination sites. (a) A typical recombination site. The crossover site, where strand exchange takes place (at the position marked by the staggered red line), binds a recombinase dimer and typically has partial dyad symmetry (indicated by the blue arrows). “Accessory sites,” which may be adjacent on one side of the crossover site (as shown), on both sides or more distant, may bind additional recombinase subunits or other proteins, or may make looping interactions with recombinase bound at the crossover site. (b) Example of a real crossover site (, a site acted upon by Hin recombinase). The colors and symbols are as in part (a). Hin, like all serine recombinases characterized to date, cuts the DNA at the center of the crossover site with a 2 bp “stagger” as shown.
10.1128/9781555819217/fig3-3_thmb.gif
10.1128/9781555819217/fig3-3.gif
Image of Figure 3
Figure 3

Recombination sites. (a) A typical recombination site. The crossover site, where strand exchange takes place (at the position marked by the staggered red line), binds a recombinase dimer and typically has partial dyad symmetry (indicated by the blue arrows). “Accessory sites,” which may be adjacent on one side of the crossover site (as shown), on both sides or more distant, may bind additional recombinase subunits or other proteins, or may make looping interactions with recombinase bound at the crossover site. (b) Example of a real crossover site (, a site acted upon by Hin recombinase). The colors and symbols are as in part (a). Hin, like all serine recombinases characterized to date, cuts the DNA at the center of the crossover site with a 2 bp “stagger” as shown.

Citation: Stark W. 2015. The Serine Recombinases, p 73-89. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0046-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/10.1128/9781555819217.chap3.fig3-4
Figure 4
The serine recombinase strand-exchange mechanism. A synaptic complex of two crossover sites bridged by a recombinase tetramer (yellow ovals) is shown. The four subunits are spaced out, so that the catalytic steps can be seen clearly. The catalytic serine residues are indicated by S-OH. The scissile phosphodiesters are represented as circled Ps, and in the first and last panels the 2-bp overlap sequence is indicated by vertical lines. For further details, see text.
10.1128/9781555819217/fig3-4_thmb.gif
10.1128/9781555819217/fig3-4.gif
Image of Figure 4
Figure 4

The serine recombinase strand-exchange mechanism. A synaptic complex of two crossover sites bridged by a recombinase tetramer (yellow ovals) is shown. The four subunits are spaced out, so that the catalytic steps can be seen clearly. The catalytic serine residues are indicated by S-OH. The scissile phosphodiesters are represented as circled Ps, and in the first and last panels the 2-bp overlap sequence is indicated by vertical lines. For further details, see text.

Citation: Stark W. 2015. The Serine Recombinases, p 73-89. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0046-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/10.1128/9781555819217.chap3.fig3-5
Figure 5
Domain structures of serine recombinases ( ). The SR (catalytic) domain (shown in pink; typically ∼150 amino acids) is common to all serine recombinases and contains the active site (red star). Small serine recombinases (including resolvases and invertases) have a helix–turn–helix DNA-binding domain (blue; ∼40 amino acids) at the C terminus. Some related recombinases such as ISXc5 resolvase have additional C-terminal domains (orange) of unknown function. Serine transposases have a similar helix–turn–helix domain at the N terminus. Large serine recombinases have multiple domains at the C terminus of the SR domain ( ).
10.1128/9781555819217/fig3-5_thmb.gif
10.1128/9781555819217/fig3-5.gif
Image of Figure 5
Figure 5

Domain structures of serine recombinases ( ). The SR (catalytic) domain (shown in pink; typically ∼150 amino acids) is common to all serine recombinases and contains the active site (red star). Small serine recombinases (including resolvases and invertases) have a helix–turn–helix DNA-binding domain (blue; ∼40 amino acids) at the C terminus. Some related recombinases such as ISXc5 resolvase have additional C-terminal domains (orange) of unknown function. Serine transposases have a similar helix–turn–helix domain at the N terminus. Large serine recombinases have multiple domains at the C terminus of the SR domain ( ).

Citation: Stark W. 2015. The Serine Recombinases, p 73-89. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0046-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/10.1128/9781555819217.chap3.fig3-6
Figure 6
Crystal structures of γδ resolvase–NA complexes. (a) Wild-type γδ resolvase dimer bound to crossover-site DNA (PDB 1GDT; 40). The subunits are in cartoon representation (green and orange). The active site serine residues (α carbons) are indicated by magenta spheres. (b) Activated mutant γδ resolvase tetramer in a cleaved-DNA synaptic intermediate (PDB 1ZR4; 41). The resolvase is rendered as in (a). The active-site serines are covalently linked to DNA ends (see Fig. 4 ); only two are visible. This view emphasizes the flat interface (marked by a dashed red line) between “rotating pairs” of resolvase subunits. The red arrows indicate positions of double-strand breaks in the DNA. The structure corresponds to the intermediates cartooned in the two central panels of Fig. 4 .
10.1128/9781555819217/fig3-6_thmb.gif
10.1128/9781555819217/fig3-6.gif
Image of Figure 6
Figure 6

Crystal structures of γδ resolvase–NA complexes. (a) Wild-type γδ resolvase dimer bound to crossover-site DNA (PDB 1GDT; 40). The subunits are in cartoon representation (green and orange). The active site serine residues (α carbons) are indicated by magenta spheres. (b) Activated mutant γδ resolvase tetramer in a cleaved-DNA synaptic intermediate (PDB 1ZR4; 41). The resolvase is rendered as in (a). The active-site serines are covalently linked to DNA ends (see Fig. 4 ); only two are visible. This view emphasizes the flat interface (marked by a dashed red line) between “rotating pairs” of resolvase subunits. The red arrows indicate positions of double-strand breaks in the DNA. The structure corresponds to the intermediates cartooned in the two central panels of Fig. 4 .

Citation: Stark W. 2015. The Serine Recombinases, p 73-89. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0046-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/10.1128/9781555819217.chap3.fig3-7
Figure 7
Topologically selective recombination by Tn/γδ resolvase. (a) The reaction pathway of resolvase (lower row) is contrasted with that of a non-selective recombinase (upper row). Random collision of sites results in products with a variety of topologies (a 6-noded catenane is shown as an example here). Selective synapsis by resolvase results in a product with a specific topology (2-noded catenane). (b) Architecture of the synapse. The Tn/γδ site is diagrammed on the left. On the right, the arrangement of DNA in the synapse is shown. The catalytic tetramer bound to the crossover sites (the “catalytic module”) is represented as an orange oval, and the eight resolvase subunits bound at the accessory sites (the “regulatory module”) are collectively represented by the pink oval. Chapter 10, this volume, gives more details on the structures of this and other synaptic complexes.
10.1128/9781555819217/fig3-7_thmb.gif
10.1128/9781555819217/fig3-7.gif
Image of Figure 7
Figure 7

Topologically selective recombination by Tn/γδ resolvase. (a) The reaction pathway of resolvase (lower row) is contrasted with that of a non-selective recombinase (upper row). Random collision of sites results in products with a variety of topologies (a 6-noded catenane is shown as an example here). Selective synapsis by resolvase results in a product with a specific topology (2-noded catenane). (b) Architecture of the synapse. The Tn/γδ site is diagrammed on the left. On the right, the arrangement of DNA in the synapse is shown. The catalytic tetramer bound to the crossover sites (the “catalytic module”) is represented as an orange oval, and the eight resolvase subunits bound at the accessory sites (the “regulatory module”) are collectively represented by the pink oval. Chapter 10, this volume, gives more details on the structures of this and other synaptic complexes.

Citation: Stark W. 2015. The Serine Recombinases, p 73-89. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0046-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/10.1128/9781555819217.chap3.fig3-8
Figure 8
Subunit rotation mechanism of resolvase. (a) Topologies of first round and “iteration products” observed by Cozzarelli’s group ( ). The upper part shows the products predicted by a rotation mechanism in a resolvase synapse with topology as shown in Fig. 7 . The lower panels show the simplified topologies of these products. “Mismatched” substrates (see text) form only the nonrecombinant knot products, starting with the 4-noded knot. (b). Cartoon illustrating the proposed subunit rotation mechanism. DNA is represented as ribbons and recombinase subunits as ovals. The crystal structure of a proposed intermediate in subunit rotation is shown in Fig. 6b .
10.1128/9781555819217/fig3-8_thmb.gif
10.1128/9781555819217/fig3-8.gif
Image of Figure 8
Figure 8

Subunit rotation mechanism of resolvase. (a) Topologies of first round and “iteration products” observed by Cozzarelli’s group ( ). The upper part shows the products predicted by a rotation mechanism in a resolvase synapse with topology as shown in Fig. 7 . The lower panels show the simplified topologies of these products. “Mismatched” substrates (see text) form only the nonrecombinant knot products, starting with the 4-noded knot. (b). Cartoon illustrating the proposed subunit rotation mechanism. DNA is represented as ribbons and recombinase subunits as ovals. The crystal structure of a proposed intermediate in subunit rotation is shown in Fig. 6b .

Citation: Stark W. 2015. The Serine Recombinases, p 73-89. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0046-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/10.1128/9781555819217.chap3.fig3-9
Figure 9
Cartoon of proposed inversion synaptic complex. An invertase tetramer bridging the two crossover sites is shown as an orange oval, and contacts the enhancer DNA (brown) and a FIS dimer bound there (pink). The DNA in the complex is intertwined as shown. Supercoiled loops of DNA outside the complex are shown as dashed lines.
10.1128/9781555819217/fig3-9_thmb.gif
10.1128/9781555819217/fig3-9.gif
Image of Figure 9
Figure 9

Cartoon of proposed inversion synaptic complex. An invertase tetramer bridging the two crossover sites is shown as an orange oval, and contacts the enhancer DNA (brown) and a FIS dimer bound there (pink). The DNA in the complex is intertwined as shown. Supercoiled loops of DNA outside the complex are shown as dashed lines.

Citation: Stark W. 2015. The Serine Recombinases, p 73-89. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0046-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/10.1128/9781555819217.chap3.fig3-10
Figure 10
Recombination by serine integrases. In nature, integrase promotes recombination between a crossover site, , in the circular bacteriophage DNA and a different crossover site, , in the host bacterial genome (indicated by a squiggly line). Integrase alone does not promote any reaction between the product sites and . However, the presence of a bacteriophage-encoded recombination directionality factor (RDF) protein alters the properties of integrase so that it preferentially promotes × recombination (red arrow). See text for further details.
10.1128/9781555819217/fig3-10_thmb.gif
10.1128/9781555819217/fig3-10.gif
Image of Figure 10
Figure 10

Recombination by serine integrases. In nature, integrase promotes recombination between a crossover site, , in the circular bacteriophage DNA and a different crossover site, , in the host bacterial genome (indicated by a squiggly line). Integrase alone does not promote any reaction between the product sites and . However, the presence of a bacteriophage-encoded recombination directionality factor (RDF) protein alters the properties of integrase so that it preferentially promotes × recombination (red arrow). See text for further details.

Citation: Stark W. 2015. The Serine Recombinases, p 73-89. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0046-2014
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555819217.chap3
1. Jayaram M,, Grainge I, . 2005. Introduction to site-specific recombination, p 33– 81. In Mullany P (ed), The dynamic bacterial genome. Cambridge University Press, New York, NY. [CrossRef]
2. Nash HA, . 1996. Site-specific recombination: integration, excision, resolution and inversion of defined DNA segments, p 2363– 2376. In Neidhardt FC (ed), Escherichia coli and Salmonella typhimurium. ASM Press, Washington, DC.
3. Grindley ND,, Whiteson KL,, Rice PA . 2006. Mechanism of site-specific recombination. Ann Rev Biochem 75 : 567– 605.[PubMed] [CrossRef]
4. Hallet B,, Sherratt DJ . 1997. Transposition and site-specific recombination: adapting DNA cut-and-paste mechanisms to a variety of genetic rearrangements. FEMS Microbiol Rev 21 : 157– 178.[PubMed] [CrossRef]
5. Berg DE,, Howe MM (ed) . 1989. Mobile DNA. ASM Press, Washington DC [see Chapters 1, 5, 28, 29, and 33].
6. Craig N,, Craigie R,, Gellert M,, Lambowitz A (ed) . 2004. Mobile DNA II. ASM Press, Washington DC [see Chapters 6 to 14].
7. Brembu T,, Winge P,, Tooming-Klunderud A,, Nederbragt AJ,, Jakobsen KS,, Bones AM . 2013. The chloroplast genome of the diatom Seminavis robusta: new features introduced through multiple mechanisms of horizontal gene transfer. Mar Genomics 16 : 17– 7.[PubMed] [CrossRef]
8. Piednoël M,, Gonçalves IR,, Higuet D,, Bonnivard E . 2011. Eukaryote DIRS1-like retrotransposons: an overview. BMC Genomics 12 : 621. [PubMed] [CrossRef]
9. Heffron F,, Mccarthy BJ . 1979. DNA sequence analysis of the transposon Tn3: three genes and three sites involved in transposition of Tn3. Cell 18 : 1153– 1163.[PubMed] [CrossRef]
10. Arthur A,, Sherratt DJ . 1979. Dissection of the transposition process: a transposon-encoded site-specific recombination system. Mol Gen Genet 175 : 267– 274.[PubMed] [CrossRef]
11. Kostriken R,, Morita C,, Heffron F . 1981. Transposon Tn3 encodes a site-specific recombination system: identification of essential sequences, genes and actual site of recombination. Proc Natl Acad Sci U S A 78 : 4041– 4045.[PubMed] [CrossRef]
12. Grindley NDF,, Lauth MR,, Wells RG,, Wityk RJ,, Salvo JJ,, Reed RR . 1982. Transposon-mediated site-specific recombination: identification of three binding sites for resolvase at the res site of γδ and Tn 3 . Cell 30 : 19– 27.[CrossRef]
13. Kitts PA,, Symington LS,, Dyson P,, Sherratt DJ . 1983. Transposon-encoded site-specific recombination: nature of the Tn 3 DNA sequences which constitute the recombination site res . EMBO J 2 : 1055– 1060.[PubMed]
14. Plasterk RHA,, Brinkman A,, van de Putte P . 1983. DNA inversions in the chromosome of Escherichia coli and in bacteriophage Mu: relationship to other site-specific recombination systems. Proc Natl Acad Sci U S A 80 : 5355– 5358.[PubMed] [CrossRef]
15. Hatfull GF,, Grindley NDF, . 1988. Resolvases and DNA-invertases: a family of enzymes active in site-specific recombination, p 357– 396. In Kucherlapati R,, Smith GR (ed), Genetic recombination. ASM Press, Washington DC.
16. Reed RR . 1981. Transposon-mediated site-specific recombination: a defined in vitro system. Cell 25 : 713– 719.[PubMed] [CrossRef]
17. Reed RR . 1981. Resolution of cointegrates between transposons γδ and Tn 3 defines the recombination site. Proc Natl Acad Sci U S A 78 : 3428– 3432.[PubMed] [CrossRef]
18. Reed RR,, Grindley NDF . 1981. Transposon-mediated site-specific recombination in vitro: DNA cleavage and protein-DNA linkage at the recombination site. Cell 25 : 721– 728.[PubMed] [CrossRef]
19. Reed RR,, Moser CD . 1984. Resolvase-mediated recombination intermediates contain a serine residue covalently linked to DNA. Cold Spring Harbor Symp Quant Biol 49 : 245– 249.[PubMed] [CrossRef]
20. Klippel A,, Mertens G,, Patschinsky T,, Kahmann R . 1988. The DNA invertase Gin of phage Mu: formation of a covalent complex with DNA via a phosphoserine at amino acid position 9. EMBO J 7 : 1229– 1237.[PubMed]
21. Hatfull GF,, Grindley NDF . 1986. Analysis of γδ resolvase mutants in vitro: evidence for an interaction between serine-10 of resolvase and site I of res . Proc Natl Acad Sci U S A 83 : 5429– 5433.[PubMed] [CrossRef]
22. Leschziner A,, Boocock MR,, Grindley NDF . 1995. The tyrosine-6 hydroxyl of γδ resolvase is not required for the DNA cleavage and rejoining reactions. Mol Microbiol 15 : 865– 870.[PubMed] [CrossRef]
23. Esposito D,, Scocca JJ . 1997. The integrase family of tyrosine recombinases: evolution of a conserved active site domain. Nucleic Acids Res 25 : 3605– 3614.[PubMed] [CrossRef]
24. Kamali-Moghaddam M,, Sundstrom L . 2000. Transposon targeting determined by resolvase. FEMS Microbiol Lett 186 : 55– 59.[PubMed] [CrossRef]
25. Smith MCM,, Thorpe HM . 2002. Diversity in the serine recombinases. Mol Microbiol 44 : 299– 307.[PubMed] [CrossRef]
26. Rowland SJ,, Stark WM, . 2005. Site-specific recombination by the serine recombinases, p 121– 150. In Mullany P (ed), The dynamic bacterial genome. Cambridge University Press, New York, NY. [CrossRef]
27. Van Duyne GD,, Rutherford K . 2013. Large serine recombinase domain structure and attachment site binding. Crit Rev Biochem Mol Biol 48 : 476– 491.[PubMed] [CrossRef]
28. Thorpe HM,, Smith MCM . 1998. In vitro site-specific integration of bacteriophage DNA catalysed by a recombinase of the resolvase/invertase family. Proc Natl Acad Sci U S A, 95 : 5505– 5510.[PubMed] [CrossRef]
29. Kersulyte D,, Mukhopadhyay AK,, Shirai M,, Nakazawa T,, Berg DE . 2000. Functional organization and insertion specificity of IS 607: a chimeric element of Helicobacter pylori . J Bacteriol 182 : 5300– 5308.[PubMed] [CrossRef]
30. Boocock MR,, Rice PA . 2013. A proposed mechanism for IS607-family transposases. Mobile DNA 4 : 24. [PubMed] [CrossRef]
31. Grindley NDF, . 2002. The movement of Tn 3-like elements: transposition and cointegrate resolution, p 272– 302. In Craig N,, Craigie R,, Gellert M,, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington DC.
32. Sherratt D, . 1989. Tn 3 and related transposable elements: site-specific recombination and transposition, p 163– 184. In Berg DE,, Howe MM (ed), Mobile DNA. ASM Press, Washington DC.
33. Johnson RC, . 2002. Bacterial site-specific DNA inversion systems, p 230– 271. In Craig N,, Craigie R,, Gellert M,, Lambowitz A (ed) Mobile DNA II. ASM Press, Washington DC.
34. Groth AC,, Calos MP . 2004. Phage integrases: biology and applications. J Mol Biol 335 : 667– 678.[PubMed] [CrossRef]
35. Smith MCM,, Brown WRA,, McEwan AR,, Rowley PA . 2010. Site-specific recombination by ɸC31 integrase and other large serine recombinases. Biochem Soc Trans 38 : 388– 394.[PubMed] [CrossRef]
36. Askora A,, Kawasaki T,, Fujie M,, Yamada T . 2011. Resolvase-like serine recombinase mediates integration/excision in the bacteriophage ɸRSM. J Biosci Bioeng 111 : 109– 116.[PubMed] [CrossRef]
37. Sanderson MR,, Freemont PS,, Rice PA,, Goldman A,, Hatfull GF,, Grindley NDF,, Steitz TA . 1990. The crystal structure of the catalytic domain of the site-specific recombination enzyme γδ resolvase at 2.7 Å resolution. Cell 63 : 1323– 1329.[PubMed] [CrossRef]
38. Rice PA,, Steitz TA . 1994. Model for a DNA-mediated synaptic complex suggested by crystal packing of γδ resolvase subunits. EMBO J 13 : 1514– 1524.[PubMed]
39. Rice PA,, Steitz TA . 1994. Refinement of γδ resolvase reveals a strikingly flexible molecule. Structure 2 : 371– 384.[PubMed] [CrossRef]
40. Yang W,, Steitz TA . 1995. Crystal structure of the site-specific recombinase γδ resolvase complexed with a 34 bp cleavage site. Cell 82 : 193– 207.[PubMed] [CrossRef]
41. Li W,, Kamtekar S,, Xiong Y,, Sarkis GJ,, Grindley NDF,, Steitz TA . 2005. Structure of a synaptic γδ resolvase tetramer covalently linked to two cleaved DNAs. Science 309 : 1210– 125.[PubMed] [CrossRef]
42. Kamtekar S,, Ho RS,, Cocco MJ,, Li W,, Wenwieser SVCT,, Boocock MR,, Grindley NDF,, Steitz TA . 2006. Implications of structures of synaptic tetramers of γδ resolvase for the mechanism of recombination. Proc Natl Acad Sci U S A 103 : 10642– 10647.[PubMed] [CrossRef]
43. Mouw KW,, Rowland SJ,, Gajjar MM,, Boocock MR,, Stark WM,, Rice PA . 2008. Architecture of a serine recombinase-DNA regulatory complex. Mol Cell 30 : 145– 155.[PubMed] [CrossRef]
44. Keenholtz RA,, Rowland SJ,, Boocock MR,, Stark WM,, Rice PA . 2011. Structural basis for catalytic activation of a serine recombinase. Structure 19 : 799– 809.[PubMed] [CrossRef]
45. Pan B,, Maciejewski MW,, Marintchev A,, Mullen GP . 2001. Solution structure of the catalytic domain of γδ resolvase. Implications for the mechanism of catalysis. J Mol Biol 310 : 1089– 1107.[PubMed] [CrossRef]
46. Liu T,, DeRose EF,, Mullen GP . 1994. Determination of the structure of the DNA binding domain of γδ resolvase in solution. Protein Sci 3 : 1286– 1295.[PubMed] [CrossRef]
47. Feng JA,, Johnson RC,, Dickerson RE . 1994. Hin recombinase bound to DNA: the origin of specificity in major and minor groove interactions. Science 263 : 348– 355.[PubMed] [CrossRef]
48. Chiu TK,, Sohn C,, Dickerson RE,, Johnson RC . 2002. Testing water-mediated DNA recognition by the Hin recombinase. EMBO J 21 : 801– 814.[PubMed] [CrossRef]
49. Ritacco CJ,, Kamtekar S,, Wang J,, Steitz TA . 2012. Crystal structure of an intermediate of rotating dimers within the synaptic tetramer of the G-segment invertase. Nucleic Acids Res 41 : 2673– 2682.[PubMed] [CrossRef]
50. Ritacco CJ,, Steitz TA,, Wang J . 2014. Exploiting large non-isomorphous differences for phase determination of a G-segment invertase–DNA complex. Acta Cryst D70 : 685– 693.[PubMed] [CrossRef]
51. Rutherford K,, Yuan P,, Perry K,, Sharp R,, Van Duyne GD . 2013. Attachment site recognition and regulation of directionality by the serine integrases. Nucleic Acids Res 41 : 8341– 8356.[PubMed] [CrossRef]
52. Yuan P,, Gupta K,, Van Duyne GD . 2008. Tetrameric structure of a serine integrase catalytic domain. Structure 16 : 1275– 1286.[PubMed] [CrossRef]
53. Nöllmann M,, He J,, Byron O,, Stark WM . 2004. Solution structure of the Tn 3 resolvase-crossover site synaptic complex. Mol Cell 16 : 127– 137.[PubMed] [CrossRef]
54. Aravind L,, Landsman D . 1998. AT-hook motifs identified in a wide variety of DNA-binding proteins. Nucleic Acids Res 26 : 4413– 4421.[PubMed] [CrossRef]
55. Krasnow MA,, Cozzarelli NR . 1983. Site-specific relaxation and recombination by the Tn 3 resolvase: recognition of the DNA path between oriented res sites. Cell 32 : 1313– 1324.[PubMed] [CrossRef]
56. Stark WM,, Boocock MR,, Sherratt DJ . 1989. Site-specific recombination by Tn 3 resolvase. Trends Genet 5 : 304– 309.[PubMed] [CrossRef]
57. Stark WM,, Boocock MR, . 1995. Topological selectivity in site-specific recombination, p 101– 129. In Sherratt DJ (ed), Mobile genetic elements. Frontiers in Molecular Biology series. Oxford University Press, Oxford, UK.
58. Wasserman SA,, Cozzarelli NR . 1985. Determination of the stereostructure of the product of Tn 3 resolvase by a general method. Proc Natl Acad Sci U S A 82 : 1079– 1083.[PubMed] [CrossRef]
59. Wasserman SA,, Dungan JM,, Cozzarelli NR . 1985. Discovery of a predicted DNA knot substantiates a model for site-specific recombination. Science 229 : 171– 174.[PubMed] [CrossRef]
60. Wasserman SA,, Cozzarelli NR . 1986. Biochemical topology: applications to DNA recombination and replication. Science 232 : 951– 960.[PubMed] [CrossRef]
61. Stark WM,, Sherratt DJ,, Boocock MR . 1989. Site-specific recombination by Tn 3 resolvase: topological changes in the forward and reverse reactions. Cell 58 : 779– 790.[PubMed] [CrossRef]
62. Kanaar R,, Klippel A,, Shekhtman E,, Dungan JM,, Kahmann R,, Cozzarelli NR . 1990. Processive recombination by the phage Mu Gin system: implications for the mechanism of DNA exchange DNA site alignment, and enhancer action. Cell 62 : 353– 366.[PubMed] [CrossRef]
63. Heichman KA,, Moskowitz IPG,, Johnson RC . 1991. Configuration of DNA strands and mechanism of strand exchange in the Hin invertasome as revealed by analysis of recombinant knots. Genes Dev 5 : 1622– 1634.[PubMed] [CrossRef]
64. Moskowitz IP,, Heichman KA,, Johnson RC . 1991. Alignment of recombination sites in Hin-mediated site-specific recombination. Genes Dev 5 : 1635– 1645.[PubMed] [CrossRef]
65. Stark WM,, Grindley NDF,, Hatfull GF,, Boocock MR . 1991. Resolvase-catalysed reactions between res sites differing in the central dinucleotide of subsite I. EMBO J 10 : 3541– 3548.[PubMed]
66. Stark WM,, Boocock MR . 1994. The linkage change of a knotting reaction catalysed by Tn 3 resolvase. J Mol Biol 239 : 25– 36.[PubMed] [CrossRef]
67. McIlwraith MJ,, Boocock MR,, Stark WM . 1996. Site-specific recombination by Tn 3 resolvase, photocrosslinked to its supercoiled DNA substrate. J Mol Biol 260 : 299– 303.[PubMed] [CrossRef]
68. McIlwraith MJ,, Boocock MR,, Stark WM . 1997. Tn 3 resolvase catalyses multiple recombination events without intermediate rejoining of DNA ends. J Mol Biol 266 : 108– 121.[PubMed] [CrossRef]
69. Dhar G,, Sanders ER,, Johnson RC . 2004. Architecture of the Hin synaptic complex during recombination: the recombinase subunits translocate with the DNA strands. Cell 119 : 33– 45.[PubMed] [CrossRef]
70. Dhar G,, McLean MM,, Heiss JK,, Johnson RC . 2009. The Hin recombinase assembles a tetrameric protein swivel that exchanges DNA strands. Nucleic Acids Res 37 : 4743– 4756.[PubMed] [CrossRef]
71. Klippel A,, Cloppenborg K,, Kahmann R . 1988. Isolation and characterization of unusual gin mutants. EMBO J 7 : 3983– 3989.[PubMed]
72. Haffter P,, Bickle TA . 1988. Enhancer-independent mutants of the Cin recombinase have a relaxed topological specificity. EMBO J 7 : 3991– 3996.[PubMed]
73. Klippel A,, Kanaar R,, Kahmann R,, Cozzarelli NR . 1993. Analysis of strand exchange and DNA binding of enhancer-independent Gin recombinase mutants. EMBO J 12 : 1047– 1057.[PubMed]
74. Arnold PH,, Blake DG,, Grindley NDF,, Boocock MR,, Stark WM . 1999. Mutants of Tn 3 resolvase which do not require accessory binding sites for recombination activity. EMBO J 18 : 1407– 1414.[PubMed] [CrossRef]
75. Sarkis GJ,, Murley LL,, Leschziner AE,, Boocock MR,, Stark WM,, Grindley NDF . 2001. A model for the γδ resolvase synaptic complex. Mol Cell 8 : 623– 631.[PubMed] [CrossRef]
76. Leschziner AE,, Grindley NDF . 2003. The architecture of the γδ resolvase crossover site synaptic complex revealed by using constrained DNA substrates. Mol Cell 12 : 775– 781.[PubMed] [CrossRef]
77. Dhar G,, Heiss JK,, Johnson RC . 2009. Mechanical constraints on Hin subunit rotation imposed by the Fis/enhancer system and DNA supercoiling during site-specific recombination. Mol Cell 34 : 746– 759.[PubMed] [CrossRef]
78. Bai H,, Sun M,, Ghosh P,, Hatfull GF,, Grindley NDF,, Marko JF . 2011. Single-molecule analysis reveals the molecular bearing mechanism of DNA strand exchange by a serine recombinase. Proc Natl Acad Sci U S A 108 : 7419– 7424.[PubMed] [CrossRef]
79. Olorunniji FJ,, Buck DE,, Colloms SD,, McEwan AR,, Smith MCM,, Stark WM,, Rosser SJ . 2012. Gated rotation mechanism of site-specific recombination by ɸC31 integrase. Proc Natl Acad Sci U S A 109 : 19661– 19666.[PubMed] [CrossRef]
80. Olorunniji FJ,, Stark WM . 2009. The catalytic residues of Tn 3 resolvase. Nucleic Acids Res 37 : 7590– 7602.[PubMed] [CrossRef]
81. Keenholtz RA,, Mouw KW,, Boocock MR,, Li NS,, Piccirilli JA,, Rice PA . 2013. Arginine as a general acid catalyst in serine recombinase-mediated DNA cleavage. J Biol Chem 288 : 29206– 29214.[PubMed] [CrossRef]
82. Mizuuchi K,, Baker TA, . 2002. Chemical mechanisms for mobilizing DNA, 12– 23. In Craig N,, Craigie R,, Gellert M,, Lambowitz A (ed) Mobile DNA II. ASM Press, Washington DC.
83. Abdel-Meguid SS,, Grindley NDF,, Templeton NS,, Steitz TA . 1984. Cleavage of the site-specific recombination protein γδ resolvase: the smaller of the two fragments binds DNA specifically. Proc Natl Acad Sci U S A 81 : 2001– 2005.[PubMed] [CrossRef]
84. Rimphanitchayakit V,, Grindley NDF . 1990. Saturation mutagenesis of the DNA site bound by the small carboxy-terminal domain of γδ resolvase. EMBO J 9 : 719– 725.[PubMed]
85. Wells RG,, Grindley NDF . 1984. Analysis of the γδ res site: sites required for site-specific recombination and gene expression. J Mol Biol 179 : 667– 687.[PubMed] [CrossRef]
86. Proudfoot CM,, McPherson AL,, Kolb AF,, Stark WM . 2011. Zinc finger recombinases with adaptable DNA sequence specificity. PLoS ONE 6 : e19537. [PubMed] [CrossRef]
87. Olorunniji FJ,, He J,, Wenwieser SVCT,, Boocock MR,, Stark WM . 2008. Synapsis and catalysis by activated Tn 3 resolvase mutants. Nucleic Acids Res 36 : 7181– 7191.[PubMed] [CrossRef]
88. Rowland SJ,, Boocock MR,, McPherson AL,, Mouw KW,, Rice PA,, Stark WM . 2009. Regulatory mutations in Sin recombinase support a structure-based model of the synaptosome. Mol Microbiol 74 : 282– 298.[PubMed] [CrossRef]
89. Watson MA,, Boocock MR,, Stark WM . 1996. Rate and selectivity of synapsis of res recombination sites by Tn 3 resolvase. J Mol Biol 257 : 317– 329.[PubMed] [CrossRef]
90. Kilbride E,, Boocock MR,, Stark WM . 1999. Topological selectivity of a hybrid site-specific recombination system with elements from Tn 3 res/resolvase and bacteriophage P1 loxP/Cre. J Mol Biol 289 : 1219– 1230.[PubMed] [CrossRef]
91. Hughes RE,, Hatfull GF,, Rice PA,, Steitz TA,, Grindley NDF . 1990. Cooperativity mutants of the γδ resolvase identify an essential interdimer interaction. Cell 63 : 1331– 1338.[PubMed] [CrossRef]
92. Murley LL,, Grindley NDF . 1998. Architecture of the γδ resolvase synaptosome: oriented heterodimers identify interactions essential for synapsis and recombination. Cell 95 : 553– 562.[PubMed] [CrossRef]
93. Rowland SJ,, Stark WM,, Boocock MR . 2002. Sin recombinase from Staphylococcus aureus: synaptic complex architecture and transposon targeting. Mol Microbiol 44 : 607– 619.[PubMed] [CrossRef]
94. Huber HE,, Iida S,, Arber W,, Bickle TA . 1985. Site-specific DNA inversion is enhanced by a DNA sequence element in cis . Proc Natl Acad Sci U S A 82 : 3776– 3780.[PubMed] [CrossRef]
95. Hubner P,, Arber W . 1989. Mutational analysis of a prokaryotic recombinational enhancer with two functions. EMBO J 8 : 577– 585.[PubMed]
96. Johnson RC,, Simon MI . 1985. Hin-mediated site-specific recombination requires two 26 bp recombination sites and a 60 bp enhancer. Cell 41 : 781– 791.[PubMed] [CrossRef]
97. Kahmann R,, Rudt F,, Koch C,, Mertens G . 1985. G inversion in bacteriophage Mu DNA is stimulated by a site within the invertase gene and a host factor. Cell 41 : 771– 780.[PubMed] [CrossRef]
98. Bruist MF,, Glasgow AC,, Johnson RC,, Simon MI . 1987. Fis binding to the recombinational enhancer of the Hin DNA inversion system. Genes Dev 1 : 762– 772.[PubMed] [CrossRef]
99. Haykinson MJ,, Johnson RC . 1993. DNA looping and the helical repeat in vitro and in vivo: effect of HU protein and enhancer location on Hin invertasome assembly. EMBO J 12 : 2503– 2512.[PubMed]
100. McLean MM,, Chang Y,, Dhar G,, Heiss JK,, Johnson RC . 2013. Multiple interfaces between a serine recombinase and an enhancer control site-specific DNA inversion. eLife 2 : e01211.
101. Adams V,, Lucet IS,, Lyras D,, Rood JI . 2004. DNA binding properties of TnpX indicate that different synapses are formed in the excision and integration of the Tn 4451 family. Mol Microbiol 53 : 1195– 1207.[PubMed] [CrossRef]
102. Misiura A,, Pigli YZ,, Boyle-Vavra S,, Daum RS,, Boocock MR,, Rice PA . 2013. Roles of two large serine recombinases in mobilizing the methicillin-resistance cassette SCC mec . Mol Microbiol 88 : 1218– 1229.[PubMed] [CrossRef]
103. Ghosh P,, Kim AI,, Hatfull GF . 2003. The orientation of mycobacteriophage Bxb1 integration is solely dependent on the central dinucleotide of attP and attB . Mol Cell 12 : 1101– 1111.[PubMed] [CrossRef]
104. Smith MCA,, Till R,, Smith MCM . 2004. Switching the polarity of a bacteriophage integration system. Mol Microbiol 51 : 1719– 1728.[PubMed] [CrossRef]
105. Ghosh P,, Pannunzio NR,, Hatfull GF . 2005. Synapsis in phage Bxb1 integration: selection mechanism for the correct pair of recombination sites. J Mol Biol 349 : 331– 348.[PubMed] [CrossRef]
106. Smith MCA,, Till R,, Brady K,, Soultanas P,, Thorpe H,, Smith MCM . 2004. Synapsis and DNA cleavage in ɸC31 integrase-mediated site-specific recombination. Nucleic Acids Res 32 : 2607– 2617.[PubMed] [CrossRef]
107. Stark WM . 2011. Cutting out the ɸC31 prophage. Mol Microbiol 80 : 1417– 1419.[PubMed] [CrossRef]
108. Ghosh P,, Wasil LR,, Hatfull GF . 2006. Control of phage Bxb1 excision by a novel recombination directionality factor. PLoS Biol 4 : e186. [PubMed] [CrossRef]
109. Khaleel T,, Younger E,, McEwan AR,, Varghese AS,, Smith MCM . 2011. A phage protein that binds ɸC31 integrase to switch its directionality. Mol Microbiol 80 : 1450– 1463.[PubMed] [CrossRef]
110. Artymiuk P,, Ceska TA,, Suck D,, Sayers JR . 1997. Prokaryotic 5′-3′ exonucleases share a common core structure with gamma-delta resolvase. Nucleic Acids Res 25 : 4224– 4229.[PubMed] [CrossRef]
111. Yang W . 2010. Topoisomerases and site-specific recombinases: similarities in structure and mechanism. Crit Rev Biochem Mol Biol 45 : 520– 534.[PubMed] [CrossRef]
112. Bischof J,, Basler K . 2008. Recombinases and their uses in gene activation, gene inactivation, and transgenesis. Methods Mol Biol 420 : 175– 195.[PubMed] [CrossRef]
113. Fogg PCM,, Colloms SD,, Rosser SJ,, Stark WM,, Smith MCM . 2014. New applications for phage integrases. J Mol Biol 426 : 2703– 2716.[PubMed] [CrossRef]
114. Maranhao AC,, Ellington AD . 2013. Endowing cells with logic and memory. Nat Biotechnol 31 : 413– 415.[PubMed] [CrossRef]
115. Zhang L,, Zhao G,, Ding X . 2011. Tandem assembly of the epothilone biosynthetic gene cluster by in vitro site-specific recombination. Sci Rep 1 : 141. [PubMed] [CrossRef]
116. Colloms SD,, Merrick CA,, Olorunniji FJ,, Stark WM,, Smith MCM,, Osbourn A,, Keasling JD,, Rosser SJ . 2014. Rapid metabolic pathway assembly and modification using serine integrase site-specific recombination. Nucleic Acids Res 42 : e23. [PubMed] [CrossRef]
117. Burke ME,, Arnold PH,, He J,, Wenwieser SVCT,, Rowland SJ,, Boocock MR,, Stark WM . 2004. Activating mutations of Tn 3 resolvase marking interfaces important in recombination catalysis and its regulation. Mol Microbiol 51 : 937– 948.[PubMed] [CrossRef]
118. Grindley NDF . 1993. Analysis of a nucleoprotein complex: the synaptosome of γδ resolvase. Science 262 : 738– 740.[PubMed] [CrossRef]
119. Ackroyd AJ,, Avila P,, Parker CN,, Halford SE . 1990. Site-specific recombination by mutants of Tn 21 resolvase with DNA recognition functions from Tn 3 resolvase. J Mol Biol 216 : 633– 643.[PubMed] [CrossRef]
120. Schneider F,, Schwikardi M,, Muskhelishvili G,, Dröge P . 2000. A DNA-binding domain swap converts the invertase Gin into a resolvase. J Mol Biol 295 : 767– 775.[PubMed] [CrossRef]
121. Akopian A,, He J,, Boocock MR,, Stark WM . 2003. Chimeric site-specific recombinases with designed DNA sequence recognition. Proc Natl Acad Sci U S A 100 : 8688– 8691.[PubMed] [CrossRef]
122. Gordley RM,, Gersbach CA,, Barbas CF III . 2009. Synthesis of programmable integrases. Proc Natl Acad Sci U S A 106 : 5053– 5058.[PubMed] [CrossRef]
123. Sirk SJ,, Gaj T,, Jonsson A,, Mercer AC,, Barbas CF III . 2014. Expanding the zinc-finger recombinase repertoire: directed evolution and mutational analysis of serine recombinase specificity determinants. Nucleic Acids Res 42 : 4755– 4766.[PubMed] [CrossRef]
124. Akopian A,, Stark WM . 2005. Site-specific recombinases as instruments for genomic surgery. Adv Genet 55 : 1– 23.[PubMed] [CrossRef]
125. Gaj T,, Sirk SJ,, Barbas CF III . 2014. Expanding the scope of site-specific recombinases for genetic and metabolic engineering. Biotechnology and Bioengineering 111 : 1– 15.[PubMed] [CrossRef]
126. Mercer AC,, Gaj T,, Fuller RP,, Barbas CF III . 2012. Chimeric TALE recombinases with programmable DNA sequence specificity. Nucleic Acids Res 40 : 11163– 11172.[PubMed] [CrossRef]

Tables

The Serine Recombinases
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555819217.chap3-1,webId=/content/author/10.1128/9781555819217.chap3-1,properties={foaf_givenname=W. Marshall, foaf_name=W. Marshall Stark, foaf_surname=Stark, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555819217.chap3-aff1]]}]]
Citation: Stark W. 2015. The Serine Recombinases, p 73-89. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0046-2014
/content/10.1128/9781555819217.chap3.tab3-1
Table 1
Structural data for serine recombinases
Generic image for table
Table 1

Structural data for serine recombinases

Citation: Stark W. 2015. The Serine Recombinases, p 73-89. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0046-2014

Back to top
This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error