Skip to main content
SpringerLink
Log in

The Tc1/mariner DNA transposons in the genome of mollusk Littorina saxatilis

  • Animal Genetics
  • Published:
Russian Journal of Genetics Aims and scope Submit manuscript

Abstract

The Tc1/mariner superfamily is one of the most widely distributed among the DNA transposons in both terrestrial and aquatic organisms. We studied the abundance of the Tc1/mariner elements in the genome of the gastropod Littorina saxatilis Olivi, 1792 (Gastropoda: Littorinimorpha). For this purpose, nucleotide sequences with a total length of 358877 bp were analyzed. Six sequences were found to be similar to the Tc1/mariner DNA transposons. These sequences were studied for structure, the presence of functional transposase, and the systematic position within the superfamily. In addition, the loci with high homology to the DNA transposons of the hAT, Sola, Ginger, EnSpm/CACTA, ISL2EU, Kolobok, Novosib, Zisupton, and Helitron superfamilies were identified.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Guo, B., Zou, M., Gan, X., and He, S., Genome size evolution in pufferfish: an insight from BAC clonebased Diodon holocanthus genome sequencing, BMC Genomics, 2010, vol. 11, p. 396.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Sergeeva, E.M. and Salina, E.A., Transposable elements and plant genome evolution, Russ. J. Genet.: Appl. Res., 2011, vol. 1, no. 6, pp. 565–576. https://doi.org/10.1134/S2079059711060086.

    Article  Google Scholar 

  3. McClintock, B., Chromosome organization and genetic expression, Cold Spring Harbor Symp. Quant. Biol., 1951, vol. 16, pp. 13–47.

    Article  CAS  PubMed  Google Scholar 

  4. McClintock, B., Controlling elements and the gene, Cold Spring Harbor Symp. Quant. Biol., 1956, vol. 21, pp. 197–216.

    Article  CAS  PubMed  Google Scholar 

  5. Mobile DNA, Berg, D.E. and Howe, M.M., Eds., Washington D.C.: Amer. Soc. Microbiol., 1989.

  6. Mobile DNA, Craig, N.L., Craigie, R., Gellert, M., and Lambowitz, A.M., Eds., Washington. D.C.: Amer. Soc. Microbiol., 2002.

  7. Mikkelsen, T.S., Wakefield, M.J., Aken, B., et al., Genome of the marsupial Monodelphis domestica reveals innovation in non-coding sequences, Nature, 2007, vol. 447, pp. 167–177.

    Article  CAS  PubMed  Google Scholar 

  8. Chow, K.C. and Tung, W.L., Magnetic field exposure stimulates transposition through the induction of DnaK/J synthesis, Biochem. Biophys. Res. Commun., 2000, vol. 270, no. 3, pp. 745–748.

    Article  CAS  PubMed  Google Scholar 

  9. Bubenshchikova, E.V., Antonenko, O.V., Vasil’eva, L.V., and Ratner, V.A., Induction of MGE 412 transpositions in spermatogenesis of Drosophila males separately by heat and cold shock, Russ. J. Genet., 2002, vol. 38, no. 1, pp. 36–43. https://doi.org/10.1023/A:1013759626857.

    Article  CAS  Google Scholar 

  10. Del Re, B., Garoia, F., Mesirca, P., et al., Extremely low frequency magnetic fields affect transposition activity in Escherichia coli, Radiat. Environ. Biophys., 2003, vol. 42, no. 2, pp. 113–118.

    Article  PubMed  Google Scholar 

  11. Zakharenko, L.P., Kovalenko, L.V., Perepelkina, M.P., and Zakharov, I.K., The effect of γ-radiation on induction of the hobo element transposition in Drosophila melanogaster, Russ. J. Genet., 2006, vol. 42, no. 6, pp. 612–622. https://doi.org/10.1134/S10227954060-60056.

    Article  Google Scholar 

  12. Vasil’eva, L.A., Vykhristyuk, O.V., Antonenko, O.V., and Zakharov, I.K., The induction of transpositions of mobile genetic elements in the genome of Drosophila melanogaster by various stress factors, Inf. Vestn. Vavilovskogo O-va Genet. Sel., 2007, vol. 11, nos. 3–4, pp. 662–671.

    Google Scholar 

  13. Cheresiz, S.V., Yurchenko, N.N., Ivannikov, A.V., and Zakharov, I.K., Transposable elements and the stress, Inf. Vestn. Vavilovskogo O-va Genet. Sel., 2008, vol. 12, no. 1–2, pp. 217–242.

    Google Scholar 

  14. Piacentini, L., Fanti, L., Specchia, V., et al., Transposons, environmental changes, and heritable induced phenotypic variability, Chromosoma, 2014, vol. 123, pp. 345–354.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Kapitonov, V.V. and Jurka, J., A universal classification of eukaryotic transposable elements implemented in Repbase, Nat. Rev. Genet., 2008, vol. 9, no. 5, pp. 411–412. doi 10.1038/nrg2165-c1

    Article  PubMed  Google Scholar 

  16. Nefedova, L.N. and Kim, A.I., Molecular phylogeny and systematics of Drosophila retrotransposons and retroviruses, Mol. Biol. (Moscow), 2009, vol. 43:747. https://doi.org/10.1134/S0026893309050069.

    Article  CAS  Google Scholar 

  17. Biemont, C., A brief history of the status of transposable elements: from junk DNA to major players in evolution, Genetics, 2010, vol. 186, pp. 1085–1093. doi 10.1534/genetics.110.124180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Wicker, T., Sabot, F., Hua-Van, A., et al. A unified classification system for eukaryotic transposable elements, Nat. Rev. Genet., 2007, vol. 8, pp. 973–982. doi 10.1038/nrg2165

    Article  CAS  PubMed  Google Scholar 

  19. Haymer, D.S. and Marsh, J.L., Germ line and somatic instability of a white mutation in Drosophila mauritiana due to a transposable genetic element, Dev. Genet., 1986, vol. 6, pp. 281–291.

    Article  CAS  PubMed  Google Scholar 

  20. Jacobson, J.W., Medhora, M.M., and Hartl, D.L., Molecular structure of a somatically unstable transposable element in Drosophila, Proc. Natl. Acad. Sci. U.S.A., 1986, vol. 83, pp. 8684–8688.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Feschotte, C. and Pritham, E.J., DNA transposons and the evolution of eukaryotic genomes, Annu. Rev. Genet., 2007, vol. 41, pp. 331–368.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Liu, Y. and Yang, G., Tc1-like transposable elements in plant genomes, Mobile DNA, 2014, vol. 5, p. 17.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Lohe, A., Sullivan, D., and Hartl, D., Genetic evidence for subunit interactions in the transposase of the transposable element mariner, Genetics, 1996, vol. 144, pp. 1087–1095.

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Pietrokovski, S. and Henikoff, S., A helix-turn-helix DNA-binding motif predicted for transposases of DNA transposons, Mol. Gen. Genet., 1997, vol. 254, pp. 689–695.

    Article  CAS  PubMed  Google Scholar 

  25. Puzakov, M.V., Puzakova, L.V., and Zakharov, I.K., Diversity and distribution of mobile genetic elements in marine invertebrate genomes, Vavilovskii Zh. Genet. Sel., 2016. doi 10.18699/VJ16.16-o

    Google Scholar 

  26. Kohany, O., Gentles, A.J., Hankus, L., and Jurka, J., Annotation, submission and screening of repetitive elements in Repbase: Repbase Submitter and Censor, BMC Bioinf., 2006, vol. 25, no. 7, p. 474.

    Article  Google Scholar 

  27. Jurka, J., Repeats in genomic DNA: mining and meaning, Curr. Opin. Struct. Biol., 1998, vol. 8, pp. 333–337.

    Article  CAS  PubMed  Google Scholar 

  28. Zhang, Z., Schwartz, S., Wagner, L., and Miller, W., A greedy algorithm for aligning DNA sequences, J. Comput. Biol., 2000, vol. 7, nos. 1–2, pp. 203–214.

    Article  CAS  PubMed  Google Scholar 

  29. Altschul S.F., Madden T.L., Schäffer A.A., et al., Gapped BLAST and PSI-BLAST: a new generation of protein database search programs, Nucleic Acids Res., 1997, vol. 25, pp. 3389–3402.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Tamura, K., Stecher, G., Peterson, D., et al., MEGA6: molecular evolutionary genetics analysis version 6.0, Mol. Biol. Evol., 2013, vol. 30, pp. 2725–2729. doi 10.1093/molbev/mst197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Edgar, R.C., MUSCLE: multiple sequence alignment with high accuracy and high throughput, Nucleic Acids Res., 2004, vol. 32, pp. 1792–1797.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Saitou, N. and Nei, M., The Neighbor-Joining method: a new method for reconstructing phylogenetic trees, Mol. Biol. Evol., 1987, vol. 4, pp. 406–425.

    CAS  PubMed  Google Scholar 

  33. Nei, M. and Kumar, S., Molecular Evolution and Phylogenetics, New York: Oxford Univ., 2000.

    Google Scholar 

  34. Bao, W., Kapitonov, V.V., and Ginger, J.J., DNA transposons in eukaryotes and their evolutionary relationships with long terminal repeat retrotransposons, Mobile DNA, 2010, vol. 1, pp. 3–13.

    Article  PubMed  PubMed Central  Google Scholar 

  35. McInerney, C.E., Allcock, A.L., Johnson, M.P., et al., Comparative genomic analysis reveals species dependent complexities that explain difficulties with microsatellite marker development in mollusks, Heredity, 2011, vol. 106, pp. 78–87. doi 10.1038/hdy.2010.36

    Article  CAS  PubMed  Google Scholar 

  36. Henikoff, S., Detection of Caenorhabditis transposon homologs in diverse organisms, New Biol., 1992, vol. 4, pp. 382–388.

    CAS  PubMed  Google Scholar 

  37. Capy P., Vitalis R., Langin T. et al. Relationships between transposable elements based upon the integrase-transposase domains: is there a common ancestor?, J. Mol. Evol., 1996, vol. 42, pp. 359–368.

    Article  CAS  PubMed  Google Scholar 

  38. Robertson, H., The Tc1-mariner superfamily of transposons in animals, J. Insect. Physiol., 1995, vol. 41, pp. 99–105.

    Article  CAS  Google Scholar 

  39. Smit A.F.A., Riggs A.D. Tiggers and other DNA transposon fossils in the human genome, Proc. Natl. Acad. Sci. U.S.A., 1996, vol. 93, pp. 1443–1448.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Capy, P., Langin, T., Higuet, D., et al., Do the integrases of LTR-retrotransposons and class II element transposases have a common ancestor?, Genetica, 1997, vol. 100, pp. 63–72.

    Article  CAS  PubMed  Google Scholar 

  41. Shao, H. and Tu, Z., Expanding the diversity of the IS630-Tc1-mariner superfamily: discovery of a unique DD37E transposon and reclassification of the DD37D and DD39D transposons, Genetics, 2001, vol. 159, no. 3, pp. 1103–1115.

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Claudianos, C., Brownlie, J., Russell, R., et al., maT: a clade of transposons intermediate between mariner and Tc1, Mol. Biol. Evol., 2002, vol. 19, pp. 2101–2109.

    Article  CAS  PubMed  Google Scholar 

  43. Jarvik, T. and Lark, K.G., Characterization of Soymar1, a mariner element in soybean, Genetics, 1998, vol. 149, pp. 1569–1574.

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Gomulski, L.M., Torti, C., Bonizzoni, M., et al., A new basal subfamily of mariner elements in Ceratitis rosa and other tephritid flies, J. Mol. Evol., 2001, vol. 53, pp. 597–606.

    Article  CAS  PubMed  Google Scholar 

  45. Zhang H.H., Shen Y.H., Xiong X.M. et al. Identification and evolutionary history of the DD41D transposons in insects, Genes Genome, 2016, vol. 38, pp. 109–117. doi 10.1007/s13258-015-0356-4

    Article  CAS  Google Scholar 

  46. Collins, J., Forbes, E., and Anderson, P., The Tc3 family of transposable genetic elements in Caenorhabditis elegans, Genetics, 1989, vol. 121, pp. 47–55.

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Emmons, S.W., Yesner, L., Ruan, K., and Katzenberg, D., Evidence for a transposon in Caenorhabditis elegans, Cell, 1983, vol. 32, pp. 55–65.

    Article  CAS  PubMed  Google Scholar 

  48. Bryan, G., Garza, D., and Hartl, D., Insertion and excision of the transposable element mariner in Drosophila, Genetics, 1990, vol. 125, pp. 103–114.

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Franz, G. and Savakis, C., Minos, a new transposable element from Drosophila hydei, is a member of the Tc1-like family of transposons, Nucleic Acids Res., 1991, vol. 19, p. 6646.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Robertson, H.M. and Lampe, D.J., Recent horizontal transfer of a mariner transposable element among and between Diptera and Neuroptera, Mol. Biol. Evol., 1995, vol. 12, pp. 850–862.

    CAS  PubMed  Google Scholar 

  51. Daboussi, M.J., Langin, T., and Brygoo, Y., Fot1, a new family of fungal transposable elements, Mol. Gen. Genet., 1992, vol. 232, pp. 12–16.

    Article  CAS  PubMed  Google Scholar 

  52. Langin, T., Capy, P., and Daboussi, M.J., The transposable element impala, a fungal member of the Tc1-mariner superfamily, Mol. Gen. Genet., 1995, vol. 246, pp. 19–28.

    Article  CAS  PubMed  Google Scholar 

  53. Clark, K.J., Carlson, D.F., Leaver, M.J., et al., Passport, a native Tc1 transposon from flatfish, is functionally active in vertebrate cells, Nucleic Acids Res., 2009, vol. 37, pp. 1239–1247.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Munoz-Lopez, M., Siddique, A., Bischerour, J., et al., Transposition of Mboumar-9: identification of a new naturally active mariner-family transposon, J. Mol. Evol., 2008, vol. 382, pp. 567–572.

    CAS  Google Scholar 

  55. Schaack, S., Gilbert, C., and Feschotte, C., Promiscuous DNA: horizontal transfer of transposable elements and why it matters for eukaryotic evolution, Trends Ecol. Evol., 2010, vol. 25, pp. 537–546.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Kowalevsky Institute of Marine Biology Research, Russian Academy of Sciences, Sevastopol, 299011, Russia

    L. V. Puzakova & M. V. Puzakov

Authors
  1. L. V. Puzakova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. V. Puzakov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. V. Puzakov.

Additional information

Original Russian Text © L.V. Puzakova, M.V. Puzakov, 2017, published in Genetika, 2017, Vol. 53, No. 12, pp. 1436–1443.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Puzakova, L.V., Puzakov, M.V. The Tc1/mariner DNA transposons in the genome of mollusk Littorina saxatilis . Russ J Genet 53, 1358–1365 (2017). https://doi.org/10.1134/S1022795417120110

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1022795417120110

Keywords

Search

Navigation