Skip to main content
SpringerLink
Log in

First evidence of miniature transposable elements in sponges (Porifera)

  • SPONGE RESEARCH DEVELOPMENTS
  • Chapter
  • First Online:
Ancient Animals, New Challenges

Part of the book series: Developments in Hydrobiology ((DIHY,volume 219))

  • 714 Accesses

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.

Guest editors: M. Maldonado, X. Turon, M. A. Becerro & M. J. Uriz / Ancient animals, new challenges: developments in sponge research

Dirk Erpenbeck and Jürgen Schmitz have contributed equally to the paper.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • 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.

    Article  CAS  Google Scholar 

  • Arkhipova, I. R., 2001. Transposable elements in the animal kingdom. Molecular Biology 35: 157–167.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Batzer, M. A. & P. L. Deininger, 2002. Alu repeats and human genomic diversity. Nature Reviews Genetics 3: 370–379.

    Article  CAS  Google Scholar 

  • 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 

  • Brosius, J., 1999. Transmutation of tRNA over time. Nature Genetics 22: 8–9.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Deininger, P. L. & M. A. Batzer, 1999. Alu repeats and human disease. Molecular Genetics and Metabolism 67: 183–193.

    Article  CAS  Google Scholar 

  • Feschotte, C., 2008. Opinion – transposable elements and the evolution of regulatory networks. Nature Reviews Genetics 9: 397–405.

    Article  CAS  Google Scholar 

  • Feschotte, C. & E. J. Pritham, 2007. DNA transposons and the evolution of eukaryotic genomes. Annual Review of Genetics 41: 331–368.

    Article  CAS  Google Scholar 

  • Feschotte, C., N. Jiang & S. R. Wessler, 2002. Plant transposable elements: where genetics meets genomics. Nature Reviews Genetics 3: 329–341.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Kazazian, H. H., 2004. Mobile elements: drivers of genome evolution. Science 303: 1626–1632.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Lim, J. K. & M. J. Simmons, 1994. Gross chromosome rearrangements mediated by transposable elements in Drosophila melanogaster. Bioessays 16: 269–275.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Tordai, H., A. Nagy, K. Farkas, L. Banyai & L. Patthy, 2005. Modules, multidomain proteins and organismic complexity. FEBS Journal 272: 5064–5078.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Zhang, J. B. & T. Peterson, 2004. Transposition of reversed Ac element ends generates chromosome rearrangements in maize. Genetics 167: 1929–1937.

    Article  CAS  Google Scholar 

  • 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 

Download references

Author information

Authors and Affiliations

  1. Department of Earth- and Environmental Sciences & GeoBio-CenterLMU, Ludwig-Maximilians Universität, Richard-Wagner-Str. 10, 80333, München, Germany

    Dirk Erpenbeck & Gert Wörheide

  2. School of Biological Sciences, University of Queensland, Brisbane, 4072, Australia

    Dirk Erpenbeck & Bernard M. Degnan

  3. Institute of Experimental Pathology, ZMBE, University of Münster, Von-Esmarch-Str. 56, 48149, Münster, Germany

    Jürgen Schmitz & Gennady Churakov

  4. Department of Zoology, George S. Wise Faculty of Life Sciences, Tel-Aviv University, Tel-Aviv, 69978, Israel

    Dorothée Huchon

  5. National Evolutionary Synthesis Center, 2024 W. Main St., Suite A200, Durham, NC, 27705, USA

    Dorothée Huchon

Authors
  1. Dirk Erpenbeck
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jürgen Schmitz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gennady Churakov
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dorothée Huchon
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gert Wörheide
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Bernard M. Degnan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Jürgen Schmitz or Bernard M. Degnan .

Editor information

Editors and Affiliations

  1. Department of Marine Ecology, Center for Advanced Studies of Blanes CEAB-CSIC, Accés Cala St. Francesc 14, 17300, Blanes Gerona, Spain

    Manuel Maldonado

  2. Deparment of Aquatic Ecology, Center for Advanced Studies of Blanes, Access a la Cala S. Francesc 14, 17300, Blanes Gerona, Spain

    Xavier Turon , Mikel Becerro  & Maria Jesús Uriz ,  & 

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 34 kb)

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Erpenbeck, D., Schmitz, J., Churakov, G., Huchon, D., Wörheide, G., Degnan, B.M. (2011). First evidence of miniature transposable elements in sponges (Porifera). In: Maldonado, M., Turon, X., Becerro, M., Jesús Uriz, M. (eds) Ancient Animals, New Challenges. Developments in Hydrobiology, vol 219. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-4688-6_5

Download citation

Publish with us

Policies and ethics

Search

Navigation