Trends in Genetics
Volume 19, Issue 12, December 2003, Pages 674-678
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Genome Analysis
Diversity of retrotransposable elements in compact pufferfish genomes

https://doi.org/10.1016/j.tig.2003.10.006Get rights and content

Abstract

The compact genomes of the pufferfish species Takifugu rubripes (Fugu) and Tetraodon nigroviridis contain less copies but unexpectedly more clades of reverse transcriptase retrotransposons than the much larger human and mouse genomes. This retrotransposon diversity, also observed in zebrafish, is characteristic of fish genomes and was not lost after genome compaction in pufferfish species. The response of pufferfish genomes to retrotransposition appears similar to that observed in Drosophila melanogaster, which also presents an important turnover of retroelements.

Section snippets

More clades of reverse transcriptase retrotransposons in smooth pufferfish species than in human and mouse

Only three clades of non-LTR retrotransposons [i.e. long interspersed nuclear element (LINE) 1, LINE2 and LINE3] and three ‘classes’ of endogenous retroviruses have been identified so far in human and mouse genomes 1, 18 (Table 1). By contrast, an unexpected high diversity of reverse transcriptase retrotransposons was observed in the compact genome of both smooth pufferfish species. In pufferfish six clades of non-LTR retrotransposons were identified. Numerous clades of LTR retrotransposons (15

Diversity of retrotransposable elements is a characteristic of fish genomes

To test whether the high diversity of reverse transcriptase (pseudo)genes is a characteristic feature of fish genomes, we compared both pufferfish species with the zebrafish Danio rerio (separated by at least 150 million years of divergence). To the best of our knowledge, no systematic analysis of retrotransposable elements has been performed so far for the zebrafish genome. Database analysis detected 23 clades in D. rerio (Table 1). Most of them are present in invertebrates, and the majority

Absence of correlation between genome compaction and reduction of retrotransposon diversity in Fugu

We estimated that Fugu and zebrafish genomes contain a similar number of clades of retrotransposable elements (∼23) (Table 1). This suggested that compaction of the genome of Fugu, which is approximately four times smaller than the zebrafish genome with a similar set of genes, was not associated with a drastic reduction of retrotransposon diversity. The zebrafish genome contains ∼8200 reverse transcriptase sequences almost equally distributed between non-LTR and LTR retrotransposons, the latter

Is the genome of Tetraodon nigroviridis more compact than Fugu?

Even if more clades of retrotransposons were also present in T. nigroviridis compared with mammals, the estimated total number of LTR and non-LTR retrotransposons was apparently lower than in Fugu (Table 1). Several groups of retrotransposons including R4/Rex6, LINE2/Maui and BEL were clearly most successful in Fugu than in T. nigroviridis. This suggested, according to previous size estimations ([6] and references therein; Figure 1), that the T. nigroviridis genome might be more compact than

Pufferfish and mammalian genomes respond differently to retrotransposons

Our analysis indicates major differences between the evolutionary dynamics of retrotransposable elements in pufferfish and mammals. The level of retrotransposon diversity is much higher in pufferfish and zebrafish, and numerous clades and families of retrotransposable elements have been active recently in fish 9, 10, 15. Nevertheless, pufferfish genomes certainly contain fewer retroelements than the human and mouse genomes, suggesting a higher turnover (i.e. frequent retrotransposition and

Acknowledgements

This work was supported by the BioFuture program of the German Ministry for Research and Education (to J.N.V.), by the French Muséum National d'Histoire Naturelle, the Centre National de la Recherche Scientifique and the Ministère de la Recherche et de la Technologie (to Muséum National d'Histoire Naturelle and Genoscope). We are grateful to Manfred Schartl (Würzburg) for encouragement and to the Genoscope sequencing and the informatics and bioinformatics teams for their work on the Tetraodon

Glossary

Glossary

Clade:
elements within a group that are grouped together with ample phylogenetic support and date back to the Precambrian era (i.e. are at least 600 million years old) [20].
Class:
transposons with a common general mechanism of transposition. Retrotransposons belong to class I, DNA transposons to class II [22].
Group:
subdivision of a subclass frequently including different clades [17]. Members of a group are phylogenetically related and generally present a common distinctive characteristic. In

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  • Cited by (103)

    • Cytogenomic analysis of several repetitive DNA elements in turbot (Scophthalmus maximus)

      2018, Gene
      Citation Excerpt :

      TE sequences have a huge potential to generate gene and chromosome structural mutations, and also important functions in the regulation and reparation of several genes (Shapiro, 2005). Although most fish genomes are compact, TEs are very diverse, containing all types of mobile elements described (Volff et al., 2003). These elements are classified in two categories depending on their method for “jumping” from one genomic position to another; class I or retroelements move through an RNA intermediate, while class II or DNA transposons move by cutting and pasting into other locations.

    • Not so bad after all: Retroviruses and long terminal repeat retrotransposons as a source of new genes in vertebrates

      2016, Clinical Microbiology and Infection
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      A fourth family called DIRS contains more divergent elements that encode a tyrosine recombinase instead of an integrase [4]. Active LTR retrotransposons are present in amphibians and fish but absent from the genomes of mammals [3,5,6]. Nine genera of retroviruses have been described so far in vertebrates [7].

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