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It Takes Two Transposons to Tango Transposable-Element-Mediated Chromosomal Rearrangements

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It Takes Two Transposons to Tango Transposable-Element-Mediated Chromosomal Rearrangements Personal view of the genome project Perspective 45 Goffeau, A. et al. (1997) The Yeast Genome Directory. Nature 48 Leversha, M.A. et al. (1999) A molecular cytogenetic clone to microarrays. Nat. Genet. 20, 207–211 387, 1–105 resource for chromosome 22. Chromosome Res. 7, 571–573 51 Lockhart, D.J. and Winzeler, E.A. (2000) Genomics, gene 46 The C. elegans Sequencing Consortium (1998) Genome 49 Kirsch, I.R. et al. (2000) A systematic, high-resolution expression and DNA arrays. Nature 405, 827–836 sequence of the nematode C. elegans: a platform for linkage of the cytogenetic and physical maps of the human 52 Pandey, A. and Mann, M. (2000) Proteomics to study genes investigating biology. Science 282, 2012–2018 genome. Nat. Genet. 24, 339–340 and genomes. Nature 405, 837–846 47 Adams, M.D. et al. (2000) The genome sequence of 50 Pinkel, D. et al. (1998) High resolution analysis of DNA copy 53 Risch, N.J. (2000) Searching for genetic determinants in the Drosophila melanogaster. Science 287, 2185–2195 number variation using comparative genomic hybridization new millennium. Nature 405, 847–856 It takes two transposons to tango transposable-element-mediated chromosomal rearrangements Transposable elements (TEs) promote various chromosomal rearrangements more efficiently, and often more specifically, than other cellular processes1–3. One explanation of such events is homologous recombination between multiple copies of a TE present in a genome. Although this does occur, strong evidence from a number of TE systems in bacteria, plants and animals suggests that another mechanism – alternative transposition – induces a large proportion of TE-associated chromosomal rearrangements. This paper reviews evidence for alternative transposition from a number of unrelated but structurally similar TEs. The similarities between alternative transposition and V(D)J recombination are also discussed, as is the use of alternative transposition as a genetic tool. ince the first description of mobile genetic elements4,5, are TEs that contain sequences encoding other genes in Stransposable elements (TEs) have been found to be addition to transposase, such as genes encoding enzymes associated with chromosomal rearrangements such as responsible for antibiotic resistance. In eukaryotes, all TEs deletions, duplications, inversions, the formation of acen- that transpose by a DNA intermediate are classified as tric fragments and dicentric chromosomes, translocations transposons. Some Class II TEs, such as IS10, IS50, Ac/Ds and recombination of host genomes. This aspect of trans- (Box 1), Tam3, P, hobo and mariner, encode a single posable element function has implications for evolution2,6 transposase gene. Other Class II TEs, such as Tn7, Phage and for understanding several human genomic disorders7,8 Mu, Mutator and En/Spm, encode multiple proteins that and, because of this, the mechanisms involved in trans- catalyse and regulate transposition. poson-mediated chromosomal rearrangements warrant Two possible mechanisms by which TE-associated thorough investigation. chromosomal rearrangements can occur are: (i) indirectly TEs are classified by their sequence structure and trans- by homologous recombination or (ii) directly by an alter- position mechanisms1,3,6. Class I TEs – retroposons and native transposition process. retrotransposons – transpose by an RNA intermediate. The indirect action of TEs promotes chromosomal Retroposons have a structure similar to mRNA; retro- rearrangements by presenting the genome with multiple transposons are structurally similar to retroviruses and are similar, if not identical, sequences between which strand Yasmine H.M. Gray bounded by long terminal repeats (LTR). Class II TEs – transfer can occur. This may occur by recombination of [email protected] insertion sequences (IS elements, Box 1) and transposons – the homologous sequences or by faulty repair of double- Molecular Genetics and transpose by a DNA intermediate catalysed by a trans- strand breaks formed during transposable element Evolution Group, posase enzyme. IS elements and transposons are bounded excision using ectopic homologous sequences as a repair Research School of 3 by terminal inverted repeats (TIR). In addition to the TIR, template . Biological Sciences, additional sequences differentiate the two ends and are Not all the rearrangements observed can be explained Australian National necessary for transposition. In prokaryotes, IS elements by homologous recombination between elements at differ- University, Canberra, contain sequences encoding transposase, and transposons ent locations. For instance, rearrangements have been ACT 2601, Australia. 0168-9525/00/$ – see front matter © 2000 Elsevier Science Ltd. All rights reserved. PII: S0168-9525(00)02104-1 TIG October 2000, volume 16, No. 10 461 Perspective Transposons and chromosomal rearrangements FIGURE 1. Chromosomal rearrangements caused by homologous recombination (a) (b) (c) (d) inversion trends in Genetics Homologous recombination between repetitive sequences, such as TEs, can result in chromosomal rearrangement such as deletions, duplications and inversions. Each line represents a DNA double helix. The two sister chromatids of each of the homologous chromosomes are shown. Black ovals denote the centromere. TEs are represented by the thick black line bounded by open and closed arrows, indicating relative orientation of the element. The TE insertion sites are illustrated by open circles or boxes, with each shape representing distinct insertion sites on the chromosome and the equivalent sites on the chromosome(s) without a TE at that site. Homologous recombination requires a minimum of two copies of the repetitive sequence, one at each breakpoint, and is denoted by an ‘X’ in this figure. (a) TEs in same relative orientation on homologous chromosomes result in the formation of chromosomes containing either a deletion or a duplication of the intervening sequence. Both rearrangements are associated with recombination between two homologues. (b) TEs in opposite relative orientation on homologous chromosomes result in the formation of a dicentric chromosome and an acentric fragment. (c) TEs in same relative orientation on one chromosome result in the formation of chromosomes containing either a deletion or a duplication of the intervening sequence, differing from events in A by the lack of recombination between homologues and the net increase or decrease of the TE number. (d) TEs in opposite relative orientation on one chromosome can result in the formation of an inversion between the two TEs. If caused by homologous recombination, deletions and duplications can only be formed by TEs in the same relative orientation and inversions can only be formed by TEs in opposite relative orientation. Another mechanism must be invoked to explain inversions between TEs in the same relative orientation, deletions and duplications between TEs in opposite relative orientations, and all chromosomal rearrangements when a TE is present at only one of the rearrangement breakpoints. described where an element was found at only one of repair of the double-strand breaks produced during the rearrangement breakpoints in the parental chromo- alternative transposition is analogous to V(D)J recombination some9,10. Some rearrangements described are inconsistent and provides additional evidence supporting the theory with the orientation of the elements present in the chro- that V(D)J recombination is derived from a so-called RAG mosome prior to rearrangement11, such as duplications transposon. between inverted copies of a TE or inversions between TEs in the same relative orientation (Fig. 1). Also, because TEs – a common resource for genome plasticity recombination does not normally occur in Drosophila In order to comprehend complex chromosomal rearrange- melanogaster males12, rearrangements mediated by TEs ments induced by alternative transposition of TEs, one such as P and hobo must occur by another mechanism in must first understand the basics of traditional transpos- the male germ line of Drosophila. ition. The TEs inducing rearrangements described in this The direct action of TEs in promoting chromosomal review are all Class II TEs encoding a single transposase rearrangements is one mechanism that can account for and include prokaryotic IS elements and both prokaryotic rearrangements not caused by homologous recombi- and eukaryotic transposons. Functionally, these TEs share nation. TEs induce chromosomal rearrangements directly a common conservative transposition mechanism, known by an alternative version of the traditional transposition as cut-and-paste, where the first step of transposition is reaction where the TE ends involved come from separate the synapsis of complementary left- and right-TE ends, elements rather than a single element (Fig. 2b). Evidence followed by excision of the ends, target site capture and for similar events has been described for several families of strand transfer1,3. Insertion of the TE into the target mol- TEs, including the IS10/Tn10 elements in bacteria13,14, ecule can occur in either orientation relative to the original Ac/Ds elements in maize and tobacco11,15,16, Tam3 in element, resulting in a simple insertion (Fig. 2a). Repair of Antirrhinum majus (snapdragon)9,10,17–20 and P elements in the double-strand break occurs and can result in for- Drosophila21–24. mation of an excision footprint, regeneration of the TE Rearrangements associated with different TE systems using the sister chromatid as a template,
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