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Background   Penelope -like elements (PLEs) are an enigmatic group of retroelements sharing a common ancestor with telomerase reverse transcriptases. In our previous studies, we identified endonuclease-deficient PLEs that are associated with telomeres in bdelloid rotifers, small freshwater invertebrates best known for their long-term asexuality and high foreign DNA content. Completion of the high-quality draft genome sequence of the bdelloid rotifer  Adineta vaga  provides us with the opportunity to examine its genomic transposable element (TE) content, as well as TE impact on genome function and evolution.    Results  We performed an exhaustive search of the  A. vaga  genome assembly, aimed at identification of canonical PLEs combining both the reverse transcriptase (RT) and the GIY-YIG endonuclease (EN) domains. We find that the RT/EN-containing  Penelope  families co-exist in the  A. vaga  genome with the EN-deficient RT-containing  Athena  retroelements. Canonical PLEs are present at very low copy numbers, often as a single-copy, and there is no evidence that they might preferentially co-mobilize EN-deficient PLEs. We also find that  Penelope  elements can participate in expansion of  A. vaga  multigene families via  trans -action of their enzymatic machinery, as evidenced by identification of intron-containing host genes framed by the  Penelope  terminal repeats and characteristic target-site duplications generated upon insertion. In addition, we find that  Penelope  open reading frames (ORFs) in several families have incorporated long stretches of coding sequence several hundred amino acids (aa) in length that are highly enriched in asparagine residues, a phenomenon not observed in other retrotransposons.    Conclusions  Our results show that, despite their low abundance and low transcriptional activity in the  A. vaga  genome, endonuclease-containing  Penelope  elements can participate in expansion of host multigene families. We conclude that the terminal repeats represent the  cis -acting sequences required for mobilization of the intervening region in  trans  by the  Penelope -encoded enzymatic activities. We also hypothesize that the unusual capture of long N-rich segments by the  Penelope  ORF occurs as a consequence of peculiarities of its replication mechanism. These findings emphasize the unconventional nature of  Penelope  retrotransposons, which, in contrast to all other retrotransposon types, are capable of dispersing intron-containing genes, thereby questioning the validity of traditional estimates of gene retrocopies in PLE-containing eukaryotic genomes.

mobile dna

Endonuclease-containing Penelope retrotransposons in the bdelloid rotifer Adineta vaga exhibit unusual structural features and play a role in expansion of host gene families