Continuous exchange of sequence information between dispersed Tc1 transposons in the Caenorhabditis elegans genome (original) (raw)
Abstract
In a genome-wide analysis of the active transposons in Caenorhabditis elegans we determined the localization and sequence of all copies of each of the six active transposon families. Most copies of the most active transposons, Tc1 and Tc3, are intact but individually have a unique sequence, because of unique patterns of single-nucleotide polymorphisms. The sequence of each of the 32 Tc1 elements is invariant in the C. elegans strain N2, which has no germline transposition. However, at the same 32 Tc1 loci in strains with germline transposition, Tc1 elements can acquire the sequence of Tc1 elements elsewhere in the N2 genome or a chimeric sequence derived from two dispersed Tc1 elements. We hypothesize that during double-strand-break repair after Tc1 excision, the template for repair can switch from the Tc1 element on the sister chromatid or homologous chromosome to a Tc1 copy elsewhere in the genome. Thus, the population of active transposable elements in C. elegans is highly dynamic because of a continuous exchange of sequence information between individual copies, potentially allowing a higher evolution rate than that found in endogenous genes.
Full Text
The Full Text of this article is available as a PDF (215.8 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
- Altschul S. F., Madden T. L., Schäffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997 Sep 1;25(17):3389–3402. doi: 10.1093/nar/25.17.3389. [DOI] [PMC free article] [PubMed] [Google Scholar]
- C. elegans Sequencing Consortium Genome sequence of the nematode C. elegans: a platform for investigating biology. Science. 1998 Dec 11;282(5396):2012–2018. doi: 10.1126/science.282.5396.2012. [DOI] [PubMed] [Google Scholar]
- Collins J. J., Anderson P. The Tc5 family of transposable elements in Caenorhabditis elegans. Genetics. 1994 Jul;137(3):771–781. doi: 10.1093/genetics/137.3.771. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Collins J., Forbes E., Anderson P. The Tc3 family of transposable genetic elements in Caenorhabditis elegans. Genetics. 1989 Jan;121(1):47–55. doi: 10.1093/genetics/121.1.47. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Collins J., Saari B., Anderson P. Activation of a transposable element in the germ line but not the soma of Caenorhabditis elegans. Nature. 1987 Aug 20;328(6132):726–728. doi: 10.1038/328726a0. [DOI] [PubMed] [Google Scholar]
- Daniels G. R., Deininger P. L. Repeat sequence families derived from mammalian tRNA genes. 1985 Oct 31-Nov 6Nature. 317(6040):819–822. doi: 10.1038/317819a0. [DOI] [PubMed] [Google Scholar]
- Doak T. G., Doerder F. P., Jahn C. L., Herrick G. A proposed superfamily of transposase genes: transposon-like elements in ciliated protozoa and a common "D35E" motif. Proc Natl Acad Sci U S A. 1994 Feb 1;91(3):942–946. doi: 10.1073/pnas.91.3.942. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dreyfus D. H., Emmons S. W. A transposon-related palindromic repetitive sequence from C. elegans. Nucleic Acids Res. 1991 Apr 25;19(8):1871–1877. doi: 10.1093/nar/19.8.1871. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dupuy A. J., Fritz S., Largaespada D. A. Transposition and gene disruption in the male germline of the mouse. Genesis. 2001 Jun;30(2):82–88. doi: 10.1002/gene.1037. [DOI] [PubMed] [Google Scholar]
- Eide D., Anderson P. Transposition of Tc1 in the nematode Caenorhabditis elegans. Proc Natl Acad Sci U S A. 1985 Mar;82(6):1756–1760. doi: 10.1073/pnas.82.6.1756. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Emmons S. W., Yesner L. High-frequency excision of transposable element Tc 1 in the nematode Caenorhabditis elegans is limited to somatic cells. Cell. 1984 Mar;36(3):599–605. doi: 10.1016/0092-8674(84)90339-8. [DOI] [PubMed] [Google Scholar]
- Engels W. R., Johnson-Schlitz D. M., Eggleston W. B., Sved J. High-frequency P element loss in Drosophila is homolog dependent. Cell. 1990 Aug 10;62(3):515–525. doi: 10.1016/0092-8674(90)90016-8. [DOI] [PubMed] [Google Scholar]
- Engels W. R., Preston C. R., Johnson-Schlitz D. M. Long-range cis preference in DNA homology search over the length of a Drosophila chromosome. Science. 1994 Mar 18;263(5153):1623–1625. doi: 10.1126/science.8128250. [DOI] [PubMed] [Google Scholar]
- Fadool J. M., Hartl D. L., Dowling J. E. Transposition of the mariner element from Drosophila mauritiana in zebrafish. Proc Natl Acad Sci U S A. 1998 Apr 28;95(9):5182–5186. doi: 10.1073/pnas.95.9.5182. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Feschotte Cédric, Wessler Susan R. Mariner-like transposases are widespread and diverse in flowering plants. Proc Natl Acad Sci U S A. 2001 Dec 26;99(1):280–285. doi: 10.1073/pnas.022626699. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fischer S. E., Wienholds E., Plasterk R. H. Regulated transposition of a fish transposon in the mouse germ line. Proc Natl Acad Sci U S A. 2001 May 29;98(12):6759–6764. doi: 10.1073/pnas.121569298. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Frame I. G., Cutfield J. F., Poulter R. T. New BEL-like LTR-retrotransposons in Fugu rubripes, Caenorhabditis elegans, and Drosophila melanogaster. Gene. 2001 Jan 24;263(1-2):219–230. doi: 10.1016/s0378-1119(00)00567-9. [DOI] [PubMed] [Google Scholar]
- Ganko E. W., Fielman K. T., McDonald J. F. Evolutionary history of Cer elements and their impact on the C. elegans genome. Genome Res. 2001 Dec;11(12):2066–2074. doi: 10.1101/gr.196201. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Harris L. J., Rose A. M. Somatic excision of transposable element Tc1 from the Bristol genome of Caenorhabditis elegans. Mol Cell Biol. 1986 May;6(5):1782–1786. doi: 10.1128/mcb.6.5.1782. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hartl D. L., Lozovskaya E. R., Nurminsky D. I., Lohe A. R. What restricts the activity of mariner-like transposable elements. Trends Genet. 1997 May;13(5):197–201. doi: 10.1016/s0168-9525(97)01087-1. [DOI] [PubMed] [Google Scholar]
- Horie K., Kuroiwa A., Ikawa M., Okabe M., Kondoh G., Matsuda Y., Takeda J. Efficient chromosomal transposition of a Tc1/mariner- like transposon Sleeping Beauty in mice. Proc Natl Acad Sci U S A. 2001 Jul 31;98(16):9191–9196. doi: 10.1073/pnas.161071798. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ketting R. F., Haverkamp T. H., van Luenen H. G., Plasterk R. H. Mut-7 of C. elegans, required for transposon silencing and RNA interference, is a homolog of Werner syndrome helicase and RNaseD. Cell. 1999 Oct 15;99(2):133–141. doi: 10.1016/s0092-8674(00)81645-1. [DOI] [PubMed] [Google Scholar]
- Lampe D. J., Walden K. K., Robertson H. M. Loss of transposase-DNA interaction may underlie the divergence of mariner family transposable elements and the ability of more than one mariner to occupy the same genome. Mol Biol Evol. 2001 Jun;18(6):954–961. doi: 10.1093/oxfordjournals.molbev.a003896. [DOI] [PubMed] [Google Scholar]
- Lander E. S., Linton L. M., Birren B., Nusbaum C., Zody M. C., Baldwin J., Devon K., Dewar K., Doyle M., FitzHugh W. Initial sequencing and analysis of the human genome. Nature. 2001 Feb 15;409(6822):860–921. doi: 10.1038/35057062. [DOI] [PubMed] [Google Scholar]
- Lankenau D. H., Gloor G. B. In vivo gap repair in Drosophila: a one-way street with many destinations. Bioessays. 1998 Apr;20(4):317–327. doi: 10.1002/(SICI)1521-1878(199804)20:4<317::AID-BIES8>3.0.CO;2-M. [DOI] [PubMed] [Google Scholar]
- Le Q. H., Turcotte K., Bureau T. Tc8, a Tourist-like transposon in Caenorhabditis elegans. Genetics. 2001 Jul;158(3):1081–1088. doi: 10.1093/genetics/158.3.1081. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Li W., Shaw J. E. A variant Tc4 transposable element in the nematode C. elegans could encode a novel protein. Nucleic Acids Res. 1993 Jan 11;21(1):59–67. doi: 10.1093/nar/21.1.59. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lohe A. R., De Aguiar D., Hartl D. L. Mutations in the mariner transposase: the D,D(35)E consensus sequence is nonfunctional. Proc Natl Acad Sci U S A. 1997 Feb 18;94(4):1293–1297. doi: 10.1073/pnas.94.4.1293. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lohe A. R., Timmons C., Beerman I., Lozovskaya E. R., Hartl D. L. Self-inflicted wounds, template-directed gap repair and a recombination hotspot. Effects of the mariner transposase. Genetics. 2000 Feb;154(2):647–656. doi: 10.1093/genetics/154.2.647. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Machida C., Onouchi H., Koizumi J., Hamada S., Semiarti E., Torikai S., Machida Y. Characterization of the transposition pattern of the Ac element in Arabidopsis thaliana using endonuclease I-SceI. Proc Natl Acad Sci U S A. 1997 Aug 5;94(16):8675–8680. doi: 10.1073/pnas.94.16.8675. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Moerman D. G., Benian G. M., Waterston R. H. Molecular cloning of the muscle gene unc-22 in Caenorhabditis elegans by Tc1 transposon tagging. Proc Natl Acad Sci U S A. 1986 Apr;83(8):2579–2583. doi: 10.1073/pnas.83.8.2579. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Moerman D. G., Waterston R. H. Spontaneous unstable unc-22 IV mutations in C. elegans var. Bergerac. Genetics. 1984 Dec;108(4):859–877. doi: 10.1093/genetics/108.4.859. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mori I., Moerman D. G., Waterston R. H. Analysis of a mutator activity necessary for germline transposition and excision of Tc1 transposable elements in Caenorhabditis elegans. Genetics. 1988 Oct;120(2):397–407. doi: 10.1093/genetics/120.2.397. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nassif N., Penney J., Pal S., Engels W. R., Gloor G. B. Efficient copying of nonhomologous sequences from ectopic sites via P-element-induced gap repair. Mol Cell Biol. 1994 Mar;14(3):1613–1625. doi: 10.1128/mcb.14.3.1613. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Plasterk R. H., Groenen J. T. Targeted alterations of the Caenorhabditis elegans genome by transgene instructed DNA double strand break repair following Tc1 excision. EMBO J. 1992 Jan;11(1):287–290. doi: 10.1002/j.1460-2075.1992.tb05051.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Plasterk R. H., Izsvák Z., Ivics Z. Resident aliens: the Tc1/mariner superfamily of transposable elements. Trends Genet. 1999 Aug;15(8):326–332. doi: 10.1016/s0168-9525(99)01777-1. [DOI] [PubMed] [Google Scholar]
- Raz E., van Luenen H. G., Schaerringer B., Plasterk R. H., Driever W. Transposition of the nematode Caenorhabditis elegans Tc3 element in the zebrafish Danio rerio. Curr Biol. 1998 Jan 15;8(2):82–88. doi: 10.1016/s0960-9822(98)70038-7. [DOI] [PubMed] [Google Scholar]
- Rezsohazy R., van Luenen H. G., Durbin R. M., Plasterk R. H. Tc7, a Tc1-hitch hiking transposon in Caenorhabditis elegans. Nucleic Acids Res. 1997 Oct 15;25(20):4048–4054. doi: 10.1093/nar/25.20.4048. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ruvolo V., Hill J. E., Levitt A. The Tc2 transposon of Caenorhabditis elegans has the structure of a self-regulated element. DNA Cell Biol. 1992 Mar;11(2):111–122. doi: 10.1089/dna.1992.11.111. [DOI] [PubMed] [Google Scholar]
- Sedensky M. M., Hudson S. J., Everson B., Morgan P. G. Identification of a mariner-like repetitive sequence in C. elegans. Nucleic Acids Res. 1994 May 11;22(9):1719–1723. doi: 10.1093/nar/22.9.1719. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Smit A. F., Riggs A. D. Tiggers and DNA transposon fossils in the human genome. Proc Natl Acad Sci U S A. 1996 Feb 20;93(4):1443–1448. doi: 10.1073/pnas.93.4.1443. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Surzycki S. A., Belknap W. R. Repetitive-DNA elements are similarly distributed on Caenorhabditis elegans autosomes. Proc Natl Acad Sci U S A. 2000 Jan 4;97(1):245–249. doi: 10.1073/pnas.97.1.245. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Szostak J. W., Orr-Weaver T. L., Rothstein R. J., Stahl F. W. The double-strand-break repair model for recombination. Cell. 1983 May;33(1):25–35. doi: 10.1016/0092-8674(83)90331-8. [DOI] [PubMed] [Google Scholar]
- Thompson J. D., Higgins D. G., Gibson T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994 Nov 11;22(22):4673–4680. doi: 10.1093/nar/22.22.4673. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tower J., Karpen G. H., Craig N., Spradling A. C. Preferential transposition of Drosophila P elements to nearby chromosomal sites. Genetics. 1993 Feb;133(2):347–359. doi: 10.1093/genetics/133.2.347. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tu Zhijian, Shao Hongguang. Intra- and inter-specific diversity of Tc3-like transposons in nematodes and insects and implications for their evolution and transposition. Gene. 2002 Jan 9;282(1-2):133–142. doi: 10.1016/s0378-1119(01)00841-1. [DOI] [PubMed] [Google Scholar]
- Vos J. C., De Baere I., Plasterk R. H. Transposase is the only nematode protein required for in vitro transposition of Tc1. Genes Dev. 1996 Mar 15;10(6):755–761. doi: 10.1101/gad.10.6.755. [DOI] [PubMed] [Google Scholar]
- Wicks S. R., de Vries C. J., van Luenen H. G., Plasterk R. H. CHE-3, a cytosolic dynein heavy chain, is required for sensory cilia structure and function in Caenorhabditis elegans. Dev Biol. 2000 May 15;221(2):295–307. doi: 10.1006/dbio.2000.9686. [DOI] [PubMed] [Google Scholar]
- van Luenen H. G., Colloms S. D., Plasterk R. H. The mechanism of transposition of Tc3 in C. elegans. Cell. 1994 Oct 21;79(2):293–301. doi: 10.1016/0092-8674(94)90198-8. [DOI] [PubMed] [Google Scholar]