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Chapter 14 : The Movement of Tn-Like Elements: Transposition and Cointegrate Resolution

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Abstract:

This chapter discusses the organization of Tn3-family transposons and their transposition (the formation and resolution of the cointegrate intermediate). The bulk of the chapter, however, is concerned with the process of cointegrate resolution as performed by the resolvase (serine recombinase) class of site-specific recombinases, since this is both the most novel feature of Tn3-family transposons and the feature about which we know the most. While initial studies failed to identify the resolvase, they led to the proposal that cointegrates were an intermediate in the complete transposition pathway and that an internal site, deleted in this subset, was needed for the conversion of cointegrates to simple insertions. This proposal was subsequently proved correct, and it became apparent that Tn3 intermolecular transposition proceeded in two distinct and separable steps: formation of a cointegrate, involving the combined action of the transposase and the host cell replication machinery, followed by cointegrate resolution using the distinct site-specific recombination activity of resolvase. Taking a slightly different perspective (from that of the resolution systems), two transposons with very similar resolvases, Tn5501 and Tn(pTF5), have dramatically different transposases, suggesting that two different transposons capture the same resolvase system. Finally, despite their similar organization, two TnpI-encoding transposons, Tn4430 and Tn5401, have transposases and TnpI recombinases that are so diverged that independent origins seem highly likely.

Citation: Grindley N. 2002. The Movement of Tn-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. doi: 10.1128/9781555817954.ch14

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Image of Figure 1
Figure 1

Two stages of Tn3 transposition: the formation of the donor-target cointegrate and its subsequent resolution. Transposase, responsible for the first step, acts at the transposon ends. The site-specific recombinase, resolvase, acts at a site, res, shown as a stippled patch within the transposon.

Citation: Grindley N. 2002. The Movement of Tn-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. doi: 10.1128/9781555817954.ch14
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Image of Figure 2
Figure 2

Genetic organization of Tn3 family transposons. A selection of prototypical transposons is shown, divided into groups with distinctive patterns of tnpA and tnpR (or tnpI) placement and orientation. The crosshatched boxes are res sites; the striped boxes are IRSs (TnpI recombination sites). IS101 is a minimal, defective transposon of only 209 bp ( ). It consists of two terminal IRs flanking a res site and is activated by the transposon γδ. Note that Tn5502 and Tn1721 both have an extra, internal IR and are presumably derived from composite transposons. For more details, see the text.

Citation: Grindley N. 2002. The Movement of Tn-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. doi: 10.1128/9781555817954.ch14
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Image of Figure 3
Figure 3

The DDE motif of Tn3-family transposases. Sequences of selected TnpA proteins spanning the regions with the three conserved acidic side chains are aligned. The numbering is that for Tn3 transposase. The TnpA proteins are a selection of those listed in Table 1 , excluding those that show very little variation from a listed transposase (see Color Plate 26).

Citation: Grindley N. 2002. The Movement of Tn-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. doi: 10.1128/9781555817954.ch14
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Image of Figure 4
Figure 4

Shapiro model for replicative transposition ( ). Transposase binds to the transposon ends, pairs them, and then makes single-stranded breaks at both transposon 3ʹ ends (3ʹ processing). The complex captures a target DNA, and the 3ʹ OH transposon ends directly attack the target phosphate backbone, linking them to the target and leaving a free 3ʹ-OH end in each target strand (strand transfer). Following disassembly of the complex, replication complexes are loaded on each three-way junction, and the entire transposon is duplicated (the broken line indicates a newly synthesized strand), forming the cointegrate.

Citation: Grindley N. 2002. The Movement of Tn-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. doi: 10.1128/9781555817954.ch14
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Figure 5

res sites. (A) γδ res site ( ). The three resolvase binding sites are shown as boxes, with the arrowheads representing the 12-bp resolvase recognition sequence. The actual sequence of site I is shown below, indicating the position of DNA cleavage. The numbers beneath each of the three binding sites indicate the size of the spacer, the DNA segment separating the two 12-bp recognition sequences. PA and PR indicate the promoters for tnpA and tnpR, respectively; both are repressed by the binding of resolvase. (B) Schematics of generic res sites, showing the typical three-site organization (i) and the unusual two-subsite organization found in Tn1546 and the pXO1 gerX transposon (ii). (i) The left half of site III is shown shaded (rather than black) because this half-site in many transposons is very poorly defined. (ii) Note that site II contains two recognition sequences in the same orientation and is thought to bind two resolvase monomers (S. J. Rowland, M. R. Boocock, and W. M. Stark, personal communication).

Citation: Grindley N. 2002. The Movement of Tn-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. doi: 10.1128/9781555817954.ch14
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Figure 6

Conserved sequence motifs in resolvase ( ). The bar represents the amino acid sequence of γδ resolvase (183 residues). Residues that are totally conserved are shown as black bars; those that are highly conserved (≤10% divergence amongst the 29 recombinases compared) are crosshatched. The 29 recombinases (see Color Plate 30 for the full list) include 25 transposon-encoded cointegrate resolvases (all those listed in Table 1 plus three from the Mu-like transposons Tn552, Tn5053, and Tn5090), two DNA invertases (Gin and Hin), and two β-recombinases from pAMβ1 and pSM19035.

Citation: Grindley N. 2002. The Movement of Tn-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. doi: 10.1128/9781555817954.ch14
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Image of Figure 7
Figure 7

Topological consequences of resolvase recombination. Shown in the top row from left to right are relaxed forms of the resolvase substrate and, in order of increasing complexity, the various observed products of resolution. The res sites divide the substrate into two domains, shown as thick and thin lines. Note that the res sites alternate between the parental and recombinant configurations. The bottom row shows how the observed products can be formed by a succession of single-recombination events if (i) synapsis traps three (−) interdomainal nodes (crossings of thick and thin lines) and (ii) each recombination event introduces one (+) node. (Adapted from reference )

Citation: Grindley N. 2002. The Movement of Tn-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. doi: 10.1128/9781555817954.ch14
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Image of Figure 8
Figure 8

Synapsis and strand exchange. (A) Cartoon of the resolvase synaptic complex. The two substrate domains, separated by the two res sites, are shown as thick and thin lines. The only interdomainal DNA crossings are the three (−) nodes entrapped in the complex. One res (thick line) is bound by the stippled resolvase dimers; the other (thin line) is bound by the striped dimers. (B) Double-strand break–rotation model for strand exchange. Site I DNA segments (represented by planar ribbons) are aligned with either both major or both minor grooves facing one another. Double-strand breaks are made by resolvase (R) at both crossover points, and then one pair of duplexes is rotated by 180° in a right-hand direction about the twofold axis between the aligned sites. This rotation creates one () interdomainal node and adds half a turn for each duplex (relaxing one additional substrate supercoil). For further details, see the text.

Citation: Grindley N. 2002. The Movement of Tn-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. doi: 10.1128/9781555817954.ch14
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Image of Figure 9
Figure 9

Two-step model for res site synapsis and the topological filter ( ). (A) Two-step synapsis. Synapsis is initiated by antiparallel pairing of sites II and III, trapping three (−) nodes. This facilitates the productive pairing of both sites I. (B) Consequence of trapping two (−) interdomainal nodes at the initiation stage. To compensate for the wrapping of sites II and III around resolvase, three () intradomainal nodes must be introduced into one of the two substrate domains. (C) Consequence of pairing inverted res sites. To obtain antiparallel pairing of sites II and III, at least one interdomainal node must be formed. The subsequent interwrapping of the two res sites causes a further four interdomainal nodes to form. [Note that in panel C, nodes formed by the res interwrapping are (−) relative to the res site orientation but are () relative to the path of the DNA.]

Citation: Grindley N. 2002. The Movement of Tn-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. doi: 10.1128/9781555817954.ch14
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Image of Figure 10
Figure 10

Integrase-related cointegrate resolution systems. (A) Alignment of the portions of the TnpI amino acid sequences that contain the essential active-site residues (in boldface type and marked with an asterisk). (B) Structure of the Tn5041 resolution site (IRS). The TnpI binding sites are indicated by the boxed arrowheads. Numbers indicate the distances (in base pairs) between the binding sites and the tnpI gene.

Citation: Grindley N. 2002. The Movement of Tn-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. doi: 10.1128/9781555817954.ch14
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Tables

Generic image for table
Table 1

Tn family transposons

Citation: Grindley N. 2002. The Movement of Tn-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. doi: 10.1128/9781555817954.ch14
Generic image for table
Table 2

Site-specific recombination systems used for cointegrate resolution: a comparison

Citation: Grindley N. 2002. The Movement of Tn-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. doi: 10.1128/9781555817954.ch14
Generic image for table
Table 3

Site-specific recombinases of the resolvase (serine recombinase) family

Citation: Grindley N. 2002. The Movement of Tn-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. doi: 10.1128/9781555817954.ch14

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