4.8 Article

Zisupton-A Novel Superfamily of DNA Transposable Elements Recently Active in Fish

Journal

MOLECULAR BIOLOGY AND EVOLUTION
Volume 29, Issue 2, Pages 631-645

Publisher

OXFORD UNIV PRESS
DOI: 10.1093/molbev/msr208

Keywords

transposon; platyfish; sex chromosomes; SUMO; Ulp1 protease; HMGXB3; testis

Funding

  1. French Ministry of National Education, Research and Technology
  2. Bundesministerium fur Bildung und Forschung (BMBF)
  3. Agence Nationale de la Recherche (ANR)
  4. Institut National de la Recherche Agronomique (INRA, departement PHASE)
  5. Centre National de la Recherche Scientifique (CNRS)
  6. Fondation pour la Recherche Medicale (FRM)

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Transposable elements are widespread mobile DNA sequences able to integrate into new locations within genomes. Through transposition and recombination, they significantly contribute to genome plasticity and evolution. They can also regulate gene expression and provide regulatory and coding sequences (CDSs) for the evolution of novel gene functions. We have identified a new superfamily of DNA transposon on the Y chromosome of the platyfish Xiphophorus maculatus. This element is 11 kb in length and carries a single CDS of 24 exons. The N-terminal part of the putative protein, which is expressed in all adult tissues tested, contains several nucleic acid- and protein-binding domains and might correspond to a novel type of transposase/integrase not described so far in any transposon. In addition, a testis-specific splice isoform encodes a C-terminal Ulp1 SUMO protease domain, suggesting a function in posttranslational protein modification mediated by SUMO and/or ubiquitin small peptides. Accordingly, this element was called Zisupton, for Zinc finger SUMO protease transposon. Beside the Y-chromosomal sequence, five other very similar copies were identified in the platyfish genome. All copies are delimited by 99-bp conserved subterminal inverted repeats and flanked by copy-specific 8-nt target site duplications reflecting their integration at different positions in the genome. Zisupton elements are inserted at different genomic locations in different poeciliid species but also in different populations of X. maculatus. Such insertion polymorphisms between related species and populations indicate relatively recent transposition activity, with a high degree of nucleotide identity between species suggesting possible implication of horizontal gene transfer. Zisupton sequences were detected in other fish species, in urochordates, cephalochordates, and hemichordates as well as in more distant organisms, such as basidiomycete fungi, filamentous brown algae, and green algae. Possible examples of nuclear genes derived from Zisupton have been identified. To conclude, our analysis has uncovered a new superfamily of DNA transposons with potential roles in genome diversity and evolutionary innovation in fish and other organisms.

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