Characterization of a Tc1-like transposable element in zebrafish (Danio rerio) (original) (raw)
Abstract
We have characterized Tdr1, a family of _Tc1_-like transposable elements found in the genome of zebrafish (Danio rerio). The copy number and distribution of the sequence in the zebrafish genome have been determined, and by these criteria Tdr1 can be classified as a moderately repetitive, interspersed element. Examination of the sequences and structures of several copies of Tdr1 revealed that a particular deletion derivative, 1250 by long, of the transposon has been amplified to become the dominant form of Tdr1. The deletion in these elements encompasses sequences encoding the N-terminal portion of the putative Tdr1 transposase. Sequences corresponding to the deleted region were also detected, and thus allowed prediction of the nucleotide sequence of a hypothetical full-length element. Well conserved segments of _Tc1_-like transposons were found in the flanking regions of known fish genes, suggesting that these elements have a long evolutionary history in piscine genomes. Tdr1 elements have long, 208 by inverted repeats, with a short DNA motif repeated four times at the termini of the inverted repeats. Although different from that of the prototype C. elegans transposon Tc1, this inverted repeat structure is shared by transposable elements from salmonid fish species and two Drosophila species. We propose that these transposons form a subgroup within the _Tc1_-like family. Comparison of _Tc1_-like transposons supports the hypothesis that the transposase genes and their flanking sequences have been shaped by independent evolutionary constraints. Although _Tc1_-like sequences are present in the genomes of several strains of zebrafish and in salmonid fishes, these sequences are not conserved in the genus Danio, thus raising the possibility that these elements can be exploited for gene tagging and genome mapping.
Access this article
Subscribe and save
- Get 10 units per month
- Download Article/Chapter or eBook
- 1 Unit = 1 Article or 1 Chapter
- Cancel anytime Subscribe now
Buy Now
Price excludes VAT (USA)
Tax calculation will be finalised during checkout.
Instant access to the full article PDF.
Similar content being viewed by others
References
- Bernardi G, D'Onofrio G, Caccio S, Bernardi G (1993) Molecular phylogeny of bony fishes, based on the amino acid sequence of the growth hormone. J Mol Evol 37:644–649
Google Scholar - Brezinsky L, Wang GV, Humphreys T, Hunt J (1990) The transposable element Uhu from Hawaiian Drosophila — member of the widely dispersed class of _Tc1_-like elements. Nucleic Acids Res 18:2053–2059
Google Scholar - Bureau TE, Wessler SR (1992) Tourist: a large family of small inverted repeat elements frequently associated with maize genes. Plant Cell 4:1283–1294
Google Scholar - Caizzi R, Caggese C, Pimpinelli S (1993) Bari-1, a new transposon-like family in Drosophila melanogaster with a unique heterochromatic organization. Genetics 133:335–345
Google Scholar - Collins J, Forbes E, Anderson P (1989) The Tc3 family of transposable genetic elements in Caenorhabditis elegans. Genetics 121:47–55
Google Scholar - Daboussi MJ, Langin T, Brygoo Y (1992) For1, a new family of fungal transposable elements. Mol Gen Genet 232:12–16
Google Scholar - Datta U, Dutta P, Mandal RK (1988) Cloning and characterization of a highly repetitive fish nucleotide sequence. Gene 62:331–336
Google Scholar - Doak TG, Doerder FP, Jahn CL, Herrick G (1994) A proposed superfamily of transposase genes: transposon-like elements in ciliated protozoa and a common “D35E” motif. Proc Natl Acad Sci USA 91:942–946
Google Scholar - Driever W, Stemple D, Schier A, Solnica-Krezel L (1994) Zebrafish: genetic tools for studying vertebrate development. Trends Genet 10:152–159
Google Scholar - Ekker M, Fritz A, Westerfield M (1992) Identification of two families of satellite-like repetitive DNA sequences from the zebrafish (Brachydanio rerio). Genomics 13:1169–1173
Google Scholar - Emmons SW, Yesner L, Ruan KS, Katzenberg D (1983) Evidence for a transposon in Caenorhabditis elegans. Cell 32:55–65
Google Scholar - Ferris SD, Whitt GS (1977) The evolution of duplicate gene expression in the carp (Cyprinus carpio). Experientia 33:1299–1301
Google Scholar - Finnegan DJ (1989) Eukaryotic transposable elements and genome evolution. Trends Genet 5:103–107
Google Scholar - Franz G, Savakis C (1991) Minos, a new transposable element from Drosophila hydei, is a member of the _Tc1_-like family of transposons. Nucleic Acids Res 19:6646
Google Scholar - Franz G, Loukeris TG, Dialektaki G, Thompson CRL, Savakis C (1994) Mobile Minos elements from Drosophila hydei encode a two-exon transposase with similarity to the paired DNA-binding domain. Proc Natl Acad Sci USA 91:4746–4750
Google Scholar - Gierl SR, Lutticke S, Saedler H (1988) TnpA product encoded by the transposable element En-1 of Zea mays is a binding protein. EMBO 17:4045–4053
Google Scholar - Goodier JL, Davidson WS (1994) Tc1 transposon-like sequences are widely distributed in salmonids. J Mol Biol 241:26–34
Google Scholar - Handler AM, Gomez SP, O'Brochta DA (1993) Negative regulation of P element excision by the somatic product and terminal sequences of P in Drosophila melanogaster. Mol Gen Genet 237:145–151
Google Scholar - Harris LJ, Baillie DL, Rose AM (1988) Sequence identity between an inverted repeat family of transposable elements in Drosophila and Caenorhabditis. Nucleic Acids Res 16:5991–5997
Google Scholar - Hartl DL, Lozovskaya ER, Lawrence JG (1992) Nonautonomous transposable elements in prokaryotes and eukaryotes. Genetica 86:47–53
Google Scholar - He L, Zhu Z, Faras AJ, Guise KS, Hackett PB, Kapuscinski AR (1992) Characterization of _Alu_I repeats of zebrafish (Brachydanio rerio). Mol Marine Biol Biotech 1:125–135
Google Scholar - Heierhorst J, Lederis K, Richter D (1992) Presence of a member of the _Tc1_-like transposon family from nematodes and Drosophila within the vasotocin gene of a primitive vertebrate, the Pacific hagfish Eptatretus stouti. Proc Natl Acad Sci USA 89:6798–6802
Google Scholar - Henikoff S (1992) Detection of Caenorhabditis transposon homologs in diverse organisms. New Biol 4:382–388
Google Scholar - Ivics Z, Izsvák Zs, Hackett PB (1993) Enhanced incorporation of transgenic DNA into zebrafish chromosomes by a retroviral integration protein. Mol Marine Biol Biotech 2:162–173
Google Scholar - Kido Y, Aono M, Yamaki T, Matsumoto K, Murata S, Saneyoshi M, Okada N (1991) Shaping and reshaping of salmonid genomes by amplification of tRNA-derived retroposons during evolution. Proc Natl Acad Sci USA 88:2326–2330
Google Scholar - Kunze R, Starlinger P (1989) The putative transposase of transposable element Ac from Zea mays L. interacts with subterminal sequences of Ac. EMBO J 8:3177–3185
Google Scholar - MacRae AF, Clegg MT (1992) Evolution of Ac and Ds1 elements in selected grasses (Poaceae). Genetica 86:55–66
Google Scholar - Maruyama K, Hartl DL (1991) Evidence for interspecific transfer of the transposable element mariner between Drosophila and Zaprionus. J Mol Evol 33:514–524
Google Scholar - Meyer A, Biermann CH, Orti G (1993) The phylogenetic position of the zebrafish (Danio rerio), a model system in developmental biology: An invitation to the comparative method. Proc R Soc Lond 252:231–236
Google Scholar - Naruse K, Mitani H, Shima A (1992) A highly repetitive interspersed sequence isolated from genomic DNA of the medaka, Oryzias latipes, is conserved in three other related species within the genus Oryzias. J Exp Zool 262:81–86
Google Scholar - Nüsslein-Volhard C (1994) Of flies and fishes. Science 266:572–574
Google Scholar - Prasad SS, Harris LJ, Baillie DL, Rose AM (1991) Evolutionarily conserved regions in Caenorhabditis transposable elements deduced by sequence comparison. Genome 34:6–12
Google Scholar - Radice AD, Bugaj B, Fitch DHA, Emmons SW (1994) Widespread occurrence of the Tc1 transposon family: _Tc1_-like transposons from teleost fish. Mol Gen Genet 244:606–612
Google Scholar - Rio DC (1991) Regulation of Drosophila P element transposition. Trends Genet 7:282–287
Google Scholar - Rossant J, Hopkins N (1992) Of fin and fur: mutational analysis of vertebrate embryonic development. Genes Dev 6:1–13
Google Scholar - Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
Google Scholar - Simmons M, Merriman P (1994) The S element: a Drosophila member of the Tc1-mariner superfamily of transposable elements. Abstracts of the 35th Annual Drosophila Res Conference, Chicago, Illinois, p 221
- Schulte-Merker S, van Eeden FJM, Halpern ME, Kimmel CB, Nüsslein-Volhard C (1994) no tail (ntl) is the zebrafish homologue of the mouse T (Brachyury) gene. Development 120:1009–1015
Google Scholar - Vos JC, van Luenen HG, Plasterk RH (1993) Characterization of the Caenorhabditis elegans Tc1 transposase in vivo and in vitro. Genes Dev 7:1244–1253
Google Scholar - Wilson MR, Marcuz A, van Ginkel F, Miller NW, Clem LW, Middleton D, Warr GW (1990) The immunoglobulin M heavy chain constant region gene of the channel catfish, Ictalurus punctatus: an unusual mRNA splice pattern produces the membrane form of the molecule. Nucleic Acids Res 18:5227–5233
Google Scholar - Winkfein RJ, Moir RD, Krawetz DA, Blanco J, States C, Dixon GH (1988) A new family of repetitive, retroposon-like sequences in the genome of the rainbow trout. Eur J Biochem 176:255–264
Google Scholar - Wright JM (1989) Nucleotide sequence, genomic organization and evolution of a major repetitive DNA family in tilapia (Oreochromis mossambicus/hornorum). Nucleic Acids Res 17:5071–5079
Google Scholar
Author information
Author notes
- Zsuzsanna Izsvák
Present address: Institute of Biochemistry, Biological Research Center of Hungarian Academy of Sciences, Szeged, Hungary
Authors and Affiliations
- Department of Genetics and Cell Biology, University of Minnesota, 1445 Gortner Ave., 55108, St. Paul, MN, USA
Zsuzsanna Izsvák, Zoltán Ivics & Perry B. Hackett - Institute of Human Genetics, University of Minnesota, St. Paul, 55108, MN, USA
Perry B. Hackett
Authors
- Zsuzsanna Izsvák
You can also search for this author inPubMed Google Scholar - Zoltán Ivics
You can also search for this author inPubMed Google Scholar - Perry B. Hackett
You can also search for this author inPubMed Google Scholar
Additional information
Communicated by J. A. Campos-Ortega
Rights and permissions
About this article
Cite this article
Izsvák, Z., Ivics, Z. & Hackett, P.B. Characterization of a _Tc1_-like transposable element in zebrafish (Danio rerio).Molec. Gen. Genet. 247, 312–322 (1995). https://doi.org/10.1007/BF00293199
- Received: 07 September 1994
- Accepted: 13 December 1994
- Issue Date: May 1995
- DOI: https://doi.org/10.1007/BF00293199