MMTS, a New Subfamily of Tc1-like Transposons

  • Ahn, Sang Jung (Department of Biotechnology, Pukyong National University) ;
  • Kim, Moo-Sang (Department of Aquatic Life Medicine, Pukyong National University) ;
  • Jang, Jae Ho (Department of Biotechnology, Pukyong National University) ;
  • Lim, Sang Uk (Department of Biotechnology, Pukyong National University) ;
  • Lee, Hyung Ho (Department of Biotechnology, Pukyong National University)
  • Received : 2008.05.02
  • Accepted : 2008.07.01
  • Published : 2008.10.31

Abstract

A novel Tc1-like transposable element has been identified as a new DNA transposon in the mud loach, Misgurnus mizolepis. The M. mizolepis Tc1-like transposon (MMTS) is comprised of inverted terminal repeats and a single gene that codes Tc1-like transposase. The deduced amino acid sequence of the transposase-encoding region of MMTS transposon contains motifs including DDE motif, which was previously recognized in other Tc1-like transposons. However, putative MMTS transposase has only 34-37% identity with well-known Tc1, PPTN, and S elements at the amino acid level. In dot-hybridization analysis used to measure the copy numbers of the MMTS transposon in genomes of the mud loach, it was shown that the MMTS transposon is present at about $3.36{\times}10^4$ copies per $2{\times}10^9$ bp, and accounts for approximately 0.027% of the mud loach genome. Here, we also describe novel MMTS-like transposons from the genomes of carp-like fishes, flatfish species, and cichlid fishes, which bear conserved inverted repeats flanking an apparently intact transposase gene. Additionally, BLAST searches and phylogenetic analysis indicated that MMTS-like transposons evolved uniquely in fishes, and comprise a new subfamily of Tc1-like transposons, with only modest similarity to Drosophila melanogaster (foldback element FB4, HB2, HB1), Xenopus laevis, Xenopus tropicalis, and Anopheles gambiae (Frisky).

Keywords

Acknowledgement

Supported by : Ministry of Maritime Affairs and Fisheries

References

  1. Clements, K.D., Gray, R.D., and Howard Choat, J. (2003). Rapid evolutionary divergences in reef fishes of the family Acanthuridae (Perciformes: Teleostei). Mol. Phylogenet. Evol. 26, 190- 201 https://doi.org/10.1016/S1055-7903(02)00325-1
  2. Cui, Z., Geurts, A.M., Liu, G., Kaufman, C.D., and Hackett, P.B. (2002). Structure-function analysis of the inverted terminal repeats of the Sleeping Beauty transposon. J. Mol. Biol. 318, 1221-1235 https://doi.org/10.1016/S0022-2836(02)00237-1
  3. Doak, T.G., Doerder, F.P., Jahn, C.L., and 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
  4. Feschotte, C. (2004). Merlin a new superfamily of DNA transposons identified in diverse animal genomes and related to bacterial IS1016 insertion sequences. Mol. Biol. Evol. 21, 1769-1780 https://doi.org/10.1093/molbev/msh188
  5. Feschotte, C., and Pritham, E.J. (2007). DNA transposons and the evolution of eukaryotic genomes. Annu. Rev. Genet. 41, 331- 368 https://doi.org/10.1146/annurev.genet.40.110405.090448
  6. Goodier, J.L., and Davidson, W.S. (1994). Tc1 transposon-like sequences are widely distributed in salmonids. J. Mol. Biol. 241, 26-34 https://doi.org/10.1006/jmbi.1994.1470
  7. Hall, T.A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41, 95-98
  8. Harris, L.J., Baillie, D.L., and Rose, A.M. (1988). Sequence identity between an inverted repeat family of transposable elements in Drosophila and Caenorhabditis. Nucleic Acids Res. 16, 5991-5998 https://doi.org/10.1093/nar/16.13.5991
  9. Heierhorst, J., Lederis, K., and 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
  10. Henikoff, S. (1992). Detection of Caenorhabditis transposon homologs in diverse organisms. New Biol. 4, 382-388
  11. Hicks, G.R., and Raikhel, N.V. (1995). Protein import into the nucleus: an integrated view. Annu. Rev. Cell Dev. Biol. 11, 155- 188 https://doi.org/10.1146/annurev.cb.11.110195.001103
  12. Horton, P., and Nakai, K. (1997). Better prediction of protein cellular localization sites with the k nearest neighbors classifier. Proc. Int. Conf. Intell. Syst. Mol. Biol. 5, 147-152
  13. Hubbard, T., et al. (2005). Ensembl 2005. 33, D447-453 https://doi.org/10.1093/nar/gki378
  14. Ivics, Z., Izsvak, Z., Minter, A., and Hackett, P.B. (1996). Identification of functional domains and evolution of Tc1-like transposable elements. Proc. Natl. Acad. Sci. USA 93, 5008-5013
  15. Ivics, Z., Hackett, P.B., Plasterk, R.H., and Izsvak, Z. (1997). Molecular reconstruction of Sleeping Beauty, a Tc1-like transposon from fish, and its transposition in human cells. 91, 501-510 https://doi.org/10.1016/S0092-8674(00)80436-5
  16. Izsvak, Z., Ivics, Z., and Hackett, P.B. (1995). Characterization of a Tc1-like transposable element in zebrafish (Danio rerio). Mol. Gen. Genet. 247, 312-322 https://doi.org/10.1007/BF00293199
  17. Jacobson, J.W., Medhora, M.M., and Hartl, D.L. (1986). Molecular structure of a somatically unstable transposable element in Drosophila. Proc. Natl. Acad. Sci. USA 83, 8684-8688.
  18. Kapitonov, V.V., and Jurka, J. (1999). Molecular paleontology of transposable elements from Arabidopsis thaliana. Genetica 107, 27-37 https://doi.org/10.1023/A:1004030922447
  19. Kocher, T.D., Thomas, W.K., Meyer, A., Edwards, S.V., Paabo, S., Villablanca, F.X., and Wilson, A.C. (1989). Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc. Natl. Acad. Sci. USA 86, 6196-6200
  20. Kumar, S., Tamura, K., and Nei, M. (2004). MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform. 5, 150-163 https://doi.org/10.1093/bib/5.2.150
  21. Lam, W.L., Seo, P., Robison, K., Virk, S., and Gilbert, W. (1996). Discovery of amphibian Tc1-like transposon families. J. Mol. Biol. 257, 359-366 https://doi.org/10.1006/jmbi.1996.0168
  22. Leaver, M.J. (2001). A family of Tc1-like transposons from the genomes of fishes and frogs: evidence for horizontal transmission. Gene 271, 203-214 https://doi.org/10.1016/S0378-1119(01)00530-3
  23. Lim, H.S., Kim, M.S., Park, J.Y., Choi, K.E., Hwang, J.Y., Kim, D.S., and Lee, H.H. (2002). Molecular cloning and characterization of ARS elements from the mud loach (Misgurnus mizolepis). Mol. Cells 13, 185-193
  24. Lohe, A.R., Moriyama, E.N., Lidholm, D.A., and Hartl, D.L. (1995). Horizontal transmission, vertical inactivation, and stochastic loss of mariner-like transposable elements. Mol. Biol. Evol. 12, 62-72 https://doi.org/10.1093/oxfordjournals.molbev.a040191
  25. Nam, Y.K., Noh, C.H., and Kim, D.S. (1999). Transmission and expression of an integrated reporter construct up to three generations in transgenic mud loach, Misgurnus mizolepis. Aquaculture 172, 229-245 https://doi.org/10.1016/S0044-8486(98)00433-5
  26. Nam, Y.K., Cho, Y.S., Cho, H.J., and Kim, D.S. (2002). Accelerated growth performance and stable germ-line transmission in androgenetically derived homozygous transgenic mud loach, Misgurnus mizolepis. Aquaculture 209, 257-270 https://doi.org/10.1016/S0044-8486(01)00730-X
  27. Plasterk, R.H., Izsvak, Z., and Ivics, Z. (1999). Resident aliens: the Tc1/mariner superfamily of transposable elements. Trends Genet. 15, 326-332 https://doi.org/10.1016/S0168-9525(99)01777-1
  28. Radice, A.D., Bugaj, B., Fitch, D.H., and Emmons, S.W. (1994). Widespread occurrence of the Tc1 transposon family: Tc1-like transposons from teleost fish. Mol. Gen. Genet. 244, 606-612
  29. Robertson, H.M. (1995). The Tc1-mariner superfamily of transposons in animals. J. Insect Physiol. 41, 99-105 https://doi.org/10.1016/0022-1910(94)00082-R
  30. Saitou, N., and Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425
  31. Shao, H., and Tu, Z. (2001). Expanding the diversity of the IS630-Tc1-Mariner superfamily: discovery of a unique DD37E transposon and reclassification of the DD37D and DD39D transposons. Genetics 159, 1103-1115
  32. Tafalla, C., Estepa, A., and Coll, J.M. (2006). Fish transposons and their potential use in aquaculture. J. Biotechnol. 123, 397-412 https://doi.org/10.1016/j.jbiotec.2005.12.019
  33. Thompson, J.D., Higgins, D.G., and Gibson, T.J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680 https://doi.org/10.1093/nar/22.22.4673
  34. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., and Higgins, D.G. (1997). The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876-4882 https://doi.org/10.1093/nar/25.24.4876
  35. van Luenen, H.G., Colloms, S.D., and Plasterk, R.H. (1994). The mechanism of transposition Tc3 of C. elegans. Cell 79, 293-301 https://doi.org/10.1016/0092-8674(94)90198-8
  36. Vos, J.C., and Plasterk, R.H. (1994). Tc1 transposase of Caenorhabditis elegans is an endonuclease with a bipartite DNA binding domain. EMBO J. 13, 6125-6132