A universal classification of eukaryotic transposable elements implemented in Repbase (original) (raw)

In their Perspective (A unified classification system for eukaryotic transposable elements. Nature Rev. Genet. 8, 973–982 (2007))1, Wicker et al. attempt to introduce the 'first universal classification scheme'. Here, we would like to point out a similar universal hierarchical classification system that was developed earlier by us and implemented in Repbase2.

Repbase is a database of eukaryotic repetitive and transposable elements (TEs), developed since 1990. It was first published as a collection of the consensus sequences and sequence fragments of human TEs, as well as satellite DNA, that was available at the time3. Subsequently, repetitive and transposable sequences from other animal and plant species were added, and in the mid-1990s Repbase became available online for downloading and sequence analysis using the computer tools Censor server4 and RepeatMasker. At the same time, a systematic classification of repetitive elements based on their origin from different classes of TEs was developed and implemented in parallel in Repbase and RepeatMasker. Since 2001, Repbase has been routinely used in conjunction with RepeatMasker to analyze and annotate entire genomes. The resulting information is available through major international genome browsers, including the University of California, Santa Cruz (UCSC) browser and the Ensembl browser.

The current version of Repbase, known as Repbase Update, contains >7,600 sequences of TEs and other repeats, including those that are reported in the literature and those that are only reported in Repbase. Since 2001, all new information on TEs compiled in Repbase is first published in an electronic journal, Repbase Reports2,4.

In 2005, Repbase was converted to a relational database, which permitted us to implement our universal classification of TEs. According to this classification (Fig. 1), all eukaryotic TEs belong to two types (retrotransposons and DNA transposons) and are composed of five major classes: long terminal repeat (LTR) retrotransposons, non-LTR retrotransposons, cut-and-paste DNA transposons, rolling-circle DNA transposons (Helitrons) and self-synthesizing DNA transposons (Polintons). This classification is based on enzymology, structural similarities and sequence relationships5,6,7,8,9,10,11,12,13,14. Each class of TE is composed of a small number of superfamilies or clades5,6,8,9,10,11,15 (see the 40 superfamilies in Fig. 1). Each superfamily consists of numerous families of TEs. Ancient families are represented in Repbase by consensus sequences approximating active TEs from which these families were derived (consensus sequences of any two families are less than 75% identical to each other).

Figure 1: The universal classification and nomenclature of eukaryotic transposable elements.

figure 1

Different classes of transposable elements (TEs) are differently coloured. Penelope and DIRS can be viewed as two additional classes of retrotransposons. An asterisk indicates that the lengths of target-site duplications (TSDs) by short interspersed nuclear elements (SINEs) depend on non-LTR retrotransposons being involved in their transpositions. Alternative names for the superfamilies are shown in parentheses. LTR, long terminal repeat; TA, TpA dinucleotide.

Full size image

For instance, the class of LTR retrotransposons is composed of the Gypsy, Copia, BEL and DIRS superfamilies, plus the ERV1, ERV2 and ERV3 superfamilies of endogenous retroviruses6,13,15. The class of non-LTR retrotransposons is composed of the CR1, CRE, I, Jockey, L1, NeSL, Penelope, R2, R4, RandI, Rex1, RTE and Tx1 superfamilies (also known as clades)8,15. It also includes the SINE1, SINE2, and SINE3 superfamilies of short interspersed nuclear elements (SINEs), which are viewed as non-autonomous non-LTR retrotransposons7. The class of cut-and-paste DNA transposons consists of 15 superfamilies, including those described only in Repbase (Mirage, Rehavkus, Nobosib, Kolobok, ISL2EU and Chapaev). Autonomous TEs from each of these superfamilies encode superfamily-specific transposases when transposases from different superfamilies are not similar to each other (that is, when the E-value in BLASTP or PSI-BLAST is greater than 0.01).

Based on a system that was established over a decade ago by Smit and ourselves13,16, non-autonomous DNA transposons are routinely classified based on significant similarities of their terminal inverted repeats and target-site duplications to those in known autonomous DNA transposons. Analogously, structural and sequence similarities are used for the classification of non-autonomous LTR and non-LTR retrotransposons.

Although the Repbase interface does not directly display the hierarchical classification scheme, it reflects and corresponds to this scheme published in literature. According to the published information, eukaryotic DNA transposons identified so far in eukaryotes belong to three classes characterized by the so-called cut-and-paste, rolling-circle and self-synthesizing mechanisms of transposition, reflecting three different mechanisms of transposition11,15.

During the last 4 years, thousands of families of transposable elements in genomes of several eukaryotic species have been identified, classified and named based on the classification scheme and nomenclature shown in Fig. 1, including those from protozoans (diatom Thalassiosira pseudonana and green alga Chlamydomonas reinhardtii)17,18, fungi (Aspergillus nidulans, Aspergillus oryzae and Aspergillus fumigatus)19, cnidarians (starlet sea anemone Nematostella vectensis)20 and mammals (opossum Monodelphis domestica)21.

In April 2006, the above classification scheme was presented by us during the first international conference and workshop named Genomic Impact of Eukaryotic Transposable Elements, which also included a session devoted to the unified classification and nomenclature of TEs. During this conference, which was attended by 150 scientists working in the field, an International Committee on the Classification of Transposable Elements was constituted.

References

  1. Wicker, T. et al. A unified classification system for eukaryotic transposable elements. Nature Rev. Genet. 8, 973–982 (2007).
    Article CAS Google Scholar
  2. Jurka, J. et al. Repbase Update, a database of eukaryotic repetitive elements. Cytogenet. Genome Res. 110, 462–467 (2005).
    Article CAS Google Scholar
  3. Jurka, J., Walichiewicz, J. & Milosavljevic, A. Prototypic sequences for human repetitive DNA. J. Mol. Evol. 35, 286–291 (1992).
    Article CAS Google Scholar
  4. Jurka, J. Repbase Update: a database and an electronic journal of repetitive elements. Trends Genet. 16, 418–420 (2000).
    Article CAS Google Scholar
  5. Kapitonov, V. V. & Jurka, J. Rolling-circle transposons in eukaryotes. Proc. Natl Acad. Sci. USA 98, 8714–8719 (2001).
    Article CAS Google Scholar
  6. Kapitonov, V. V. & Jurka, J. Molecular paleontology of transposable elements in the Drosophila melanogaster genome. Proc. Natl Acad. Sci. USA 100, 6569–6574 (2003).
    Article CAS Google Scholar
  7. Kapitonov, V. V. & Jurka, J. A novel class of SINE elements derived from 5S rRNA. Mol. Biol. Evol. 20, 694–702 (2003).
    Article CAS Google Scholar
  8. Kapitonov, V. V. & Jurka, J. The esterase and PHD domains in CR1-like non-LTR retrotransposons. Mol. Biol. Evol. 20, 38–46 (2003).
    Article CAS Google Scholar
  9. Kapitonov, V. V. & Jurka, J. Harbinger transposons and an ancient HARBI1 gene derived from a transposase. DNA Cell Biol. 23, 311–324 (2004).
    Article CAS Google Scholar
  10. Kapitonov, V. V. & Jurka, J. RAG1 core and V(D)J recombination signal sequences were derived from Transib transposons. PLoS Biol. 3, e181 (2005).
    Article Google Scholar
  11. Kapitonov, V. V. & Jurka, J. Self-synthesizing DNA transposons in eukaryotes. Proc. Natl Acad. Sci. USA 103, 4540–4545 (2006).
    Article CAS Google Scholar
  12. Kapitonov, V. V. & Jurka, J. Helitrons on a roll: eukaryotic rolling-circle transposons. Trends Genet. 23, 521–529 (2007).
    Article CAS Google Scholar
  13. Kapitonov, V. V., Pavlicek, A. & Jurka, J. in Encyclopedia of Molecular Cell Biology and Molecular Medicine (ed. Meyers, R. A.) 251–305 (Wiley-VCH, Weinheim, 2004).
    Google Scholar
  14. Jurka, J. & Kapitonov, V. V. PIFs meet Tourists and Harbingers: a superfamily reunion. Proc. Natl Acad. Sci. USA 98, 12315–12316 (2001).
    Article CAS Google Scholar
  15. Jurka, J., Kapitonov, V. V., Kohany, O. & Jurka, M. V. Repetitive sequences in complex genomes: structure and evolution. Annu. Rev. Genomics Hum. Genet. 8, 241–259 (2007).
    Article CAS Google Scholar
  16. Smit, A. F. & Riggs, A. D. Tiggers and other DNA transposon fossils in the human genome. Proc. Natl Acad. Sci. USA 93, 1443–1448 (1996).
    Article CAS Google Scholar
  17. Armbrust, E. V. et al. The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306, 79–86 (2004).
    Article CAS Google Scholar
  18. Merchant, S. S. et al. The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318, 245–250 (2007).
    Article CAS Google Scholar
  19. Galagan, J. E. et al. Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 438, 1105–1115 (2005).
    Article CAS Google Scholar
  20. Putnam, N. H. et al. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317, 86–94 (2007).
    Article CAS Google Scholar
  21. Mikkelsen, T. S. et al. Genome of the marsupial Monodelphis domestica reveals innovation in non-coding sequences. Nature 447, 167–177 (2007).
    Article CAS Google Scholar

Download references

Acknowledgements

This work was supported by the National Institutes of Health grant 5 P41 LM06252-09.

Author information

Authors and Affiliations

  1. Vladimir V. Kapitonov and Jerzy Jurka are at the Genetic Information Research Institute, 1925 Landings Drive, Mountain View, California 94043, USA. vladimir@girinst.org jurka@girinst.org,
    Vladimir V. Kapitonov & Jerzy Jurka

Authors

  1. Vladimir V. Kapitonov
    You can also search for this author inPubMed Google Scholar
  2. Jerzy Jurka
    You can also search for this author inPubMed Google Scholar

Rights and permissions

About this article

Cite this article

Kapitonov, V., Jurka, J. A universal classification of eukaryotic transposable elements implemented in Repbase.Nat Rev Genet 9, 411–412 (2008). https://doi.org/10.1038/nrg2165-c1

Download citation