Advertisement

Hydrobiologia

, Volume 687, Issue 1, pp 43–47 | Cite as

First evidence of miniature transposable elements in sponges (Porifera)

  • Dirk Erpenbeck
  • Jürgen Schmitz
  • Gennady Churakov
  • Dorothée Huchon
  • Gert Wörheide
  • Bernard M. Degnan
SPONGE RESEARCH DEVELOPMENTS Short Research Note

Abstract

Transposable elements play a vital role in genome evolution and may have been important for the formation of the early metazoan genome, but only little is known about transposons at this interface between unicellular opisthokonts and Metazoa. Here, we describe the first miniature transposable elements (MITEs, Queen1 and Queen2) in sponges. Queen1 and Queen2 are probably derived from Tc1/mariner-like MITE families and are represented in more than 3,800 and 1,700 copies, respectively, in the Amphimedon queenslandica genome. Queen elements are located in intergenic regions as well as in introns, providing the potential to induce new splicing sites and termination signals in the genes. Further possible impacts of MITEs on the evolution of the metazoan genome are discussed.

Keywords

Early diverging Metazoa Porifera Transposable element MITE Amphimedon queenslandica Queen elements 

Notes

Acknowledgments

DE acknowledges financial support of the EU under a Marie–Curie Outgoing International Fellowship (MOIF–CT–2004 No2882). JS, GC, and GW thank the Deutsche Forschungsgemeinschaft for financial support (SCHM1469/3-1; Wo896/6-2 within SPP1174 “Deep Metazoan Phylogeny”). DH is supported by the Israel Science Foundation (600/06) and the National Evolutionary Synthesis Center (NESCent, NSF #EF-0905606.) The research was supported by an Australia Research Council grant to BMD. We thank Robert Baertsch for a local version of the UCSC Genome Browser and the A. queenslandica sequence library, Jürgen Brosius, Oliver Piskurek and two anonymous reviewers for valuable comments on earlier versions of the manuscript and Marsha Bundman for editing services.

Supplementary material

10750_2011_775_MOESM1_ESM.doc (34 kb)
Supplementary material 1 (DOC 34 kb)

References

  1. Adamska, M., D. Matus, M. Adamski, K. Green, D. Rokhsar, M. Martindale & B. Degnan, 2007. The evolutionary origin of hedgehog proteins. Current Biology 17: R836–R837.PubMedCrossRefGoogle Scholar
  2. Arkhipova, I. R., 2001. Transposable elements in the animal kingdom. Molecular Biology 35: 157–167.CrossRefGoogle Scholar
  3. Bailey, J. A., G. Liu & E. E. Eichler, 2003. An Alu transposition model for the origin and expansion of human segmental duplications. American Journal of Human Genetics 73: 823–834.PubMedCrossRefGoogle Scholar
  4. Batzer, M. A. & P. L. Deininger, 2002. Alu repeats and human genomic diversity. Nature Reviews Genetics 3: 370–379.PubMedCrossRefGoogle Scholar
  5. Brosius, J. & S. Gould, 1992. On “genomenclature”: a comprehensive (and respectful) taxonomy for pseudogenes and other” junk DNA”. Proceedings of the National Academy of Sciences of the United States of America 89: 10706–10710.Google Scholar
  6. Brosius, J., 1999. Transmutation of tRNA over time. Nature Genetics 22: 8–9.PubMedCrossRefGoogle Scholar
  7. Bureau, T. E. & S. R. Wessler, 1992. Tourist – a large family of small inverted repeat elements frequently associated with maize genes. Plant Cell 4: 1283–1294.PubMedCrossRefGoogle Scholar
  8. Cam, H. P., K. Noma, H. Ebina, H. L. Levin & S. I. S. Grewal, 2008. Host genome surveillance for retrotransposons by transposon-derived proteins. Nature 451: 431. U2.PubMedCrossRefGoogle Scholar
  9. Deininger, P. L. & M. A. Batzer, 1999. Alu repeats and human disease. Molecular Genetics and Metabolism 67: 183–193.PubMedCrossRefGoogle Scholar
  10. Feschotte, C., 2008. Opinion – transposable elements and the evolution of regulatory networks. Nature Reviews Genetics 9: 397–405.PubMedCrossRefGoogle Scholar
  11. Feschotte, C. & E. J. Pritham, 2007. DNA transposons and the evolution of eukaryotic genomes. Annual Review of Genetics 41: 331–368.PubMedCrossRefGoogle Scholar
  12. Feschotte, C., N. Jiang & S. R. Wessler, 2002. Plant transposable elements: where genetics meets genomics. Nature Reviews Genetics 3: 329–341.PubMedCrossRefGoogle Scholar
  13. Hoenigsberg, H. F., M. H. Tijaro & C. Sanabria, 2008. From unicellularity to multicellularity – molecular speculations about early animal evolution. Genetics and Molecular Research 7: 50–59.PubMedCrossRefGoogle Scholar
  14. Kazazian, H. H., 2004. Mobile elements: drivers of genome evolution. Science 303: 1626–1632.PubMedCrossRefGoogle Scholar
  15. King, N., M. Westbrook, S. Young, A. Kuo, M. Abedin, J. Chapman, S. Fairclough, U. Hellsten, Y. Isogai, I. Letunic, M. Marr, D. Pincus, N. Putnam, A. Rokas, K. Wright, R. Zuzow, W. Dirks, M. Good, D. Goodstein, D. Lemons, W. Li, J. Lyons, A. Morris, S. Nichols, D. Richter, A. Salamov, J. Sequencing, P. Bork, W. Lim, G. Manning, W. Miller, W. Mcginnis, H. Shapiro, R. Tjian, I. Grigoriev & D. Rokhsar, 2008. The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451: 783–788.PubMedCrossRefGoogle Scholar
  16. Krull, M., M. Petrusma, W. Makalowski, J. Brosius & J. Schmitz, 2007. Functional persistence of exonized mammalian-wide interspersed repeat elements (MIRs). Genome Research 17: 1139–1145.PubMedCrossRefGoogle Scholar
  17. Kuang, H., C. Padmanabhan, F. Li, A. Kamei, P. B. Bhaskar, S. Ouyang, J. Jiang, C. R. Buell & B. Baker, 2008. Identification of miniature inverted-repeat transposable elements (MITEs) and biogenesis of their siRNAs in the Solanaceae: new functional implications for MITEs. Genome Research 19: 42–56.PubMedCrossRefGoogle Scholar
  18. Larroux, C., G. N. Luke, P. Koopman, D. S. Rokhsar, S. M. Shimeld & B. M. Degnan, 2008. Genesis and expansion of metazoan transcription factor gene classes. Molecular Biology and Evolution 25: 980–996.PubMedCrossRefGoogle Scholar
  19. Lim, J. K. & M. J. Simmons, 1994. Gross chromosome rearrangements mediated by transposable elements in Drosophila melanogaster. Bioessays 16: 269–275.PubMedCrossRefGoogle Scholar
  20. Nakazaki, T., Y. Okumoto, A. Horibata, S. Yamahira, M. Teraishi, H. Nishida, H. Inoue & T. Tanisaka, 2003. Mobilization of a transposon in the rice genome. Nature 421: 170–172.PubMedCrossRefGoogle Scholar
  21. Philippe, H., R. Derelle, P. Lopez, K. Pick, C. Borchiellini, N. Boury-Esnault, J. Vacelet, E. Deniel, E. Houliston, E. Quéinnec, C. Dasilva, P. Wincker, H. Le Guyader, S. Leys, D. J. Jackson, F. Schreiber, D. Erpenbeck, B. Morgenstern, G. Wörheide & M. Manuel, 2009. Phylogenomics restores traditional views on deep animal relationships. Current Biology 19: 706–712.PubMedCrossRefGoogle Scholar
  22. Putnam, N. H., M. Srivastava, U. Hellsten, B. Dirks, J. Chapman, A. Salamov, A. Terry, H. Shapiro, E. Lindquist, V. V. Kapitonov, J. Jurka, G. Genikhovich, I. V. Grigoriev, S. M. Lucas, R. E. Steele, J. R. Finnerty, U. Technau, M. Q. Martindale & D. S. Rokhsar, 2007. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317: 86–94.PubMedCrossRefGoogle Scholar
  23. Srivastava, M., O. Simakov, J. Chapman, B. Fahey, M. E. A. Gauthier, T. Mitros, G. S. Richards, C. Conaco, M. Dacre, U. Hellsten, C. Larroux, N. H. Putnam, M. Stanke, M. Adamska, A. Darling, S. M. Degnan, T. H. Oakley, D. C. Plachetzki, Y. Zhai, M. Adamski, A. Calcino, S. F. Cummins, D. M. Goodstein, C. Harris, D. J. Jackson, S. P. Leys, S. Shu, B. J. Woodcroft, M. Vervoort, K. S. Kosik, G. Manning, B. M. Degnan & D. S. Rokhsar, 2010. The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466: 720–726.PubMedCrossRefGoogle Scholar
  24. Tordai, H., A. Nagy, K. Farkas, L. Banyai & L. Patthy, 2005. Modules, multidomain proteins and organismic complexity. FEBS Journal 272: 5064–5078.PubMedCrossRefGoogle Scholar
  25. Wang, S., L. Zhang, E. Meyer & M. V. Matz, 2010a. Characterization of a group of MITEs with unusual features from two coral genomes. PLoS ONE 5: e10700.PubMedCrossRefGoogle Scholar
  26. Wang, S., L .L. Zhang, E. Meyer & Z. M. Bao, 2010b. Genome-wide analysis of transposable elements and tandem repeats in the compact placozoan genome. Biology Direct 5.Google Scholar
  27. Wiens, M., V. A. Grebenjuk, H. C. Schröder, I. M. Müller & W. E. G. Müller, 2009. Identification and isolation of a retrotransposon from the freshwater sponge Lubomirskia baicalensis: implication in rapid evolution of endemic sponges. Progress in Molecular and Subcellular Biology 47: 207–234.PubMedCrossRefGoogle Scholar
  28. Xu, L., L. J. Wang, T. Liu, W. Q. Qlan, Y. Gao & C. C. An, 2007. Triton, a novel family of miniature inverted-repeat transposable elements (MITEs) in Trichosanthes kirilowii Maximowicz and its effect on gene regulation. Biochemical and Biophysical Research Communications 364: 668–674.PubMedCrossRefGoogle Scholar
  29. Zhang, J. B. & T. Peterson, 2004. Transposition of reversed Ac element ends generates chromosome rearrangements in maize. Genetics 167: 1929–1937.PubMedCrossRefGoogle Scholar
  30. Zhang, Q., J. Arbuckle & S.R. Wessler, 2000. Recent, extensive, and preferential insertion of members of the miniature inverted-repeat transposable element family Heartbreaker into genic regions of maize. Proceedings of the National Academy of Sciences of the United States of America 97: 1160–1165.Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Dirk Erpenbeck
    • 1
    • 2
  • Jürgen Schmitz
    • 3
  • Gennady Churakov
    • 3
  • Dorothée Huchon
    • 4
    • 5
  • Gert Wörheide
    • 1
  • Bernard M. Degnan
    • 2
  1. 1.Department of Earth- and Environmental Sciences & GeoBio-CenterLMULudwig-Maximilians UniversitätMünchenGermany
  2. 2.School of Biological SciencesUniversity of QueenslandBrisbaneAustralia
  3. 3.Institute of Experimental Pathology, ZMBEUniversity of MünsterMünsterGermany
  4. 4.Department of Zoology, George S. Wise Faculty of Life SciencesTel-Aviv UniversityTel-AvivIsrael
  5. 5.National Evolutionary Synthesis CenterDurhamUSA

Personalised recommendations