Rodriguez Fernando

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  • Preprint
    Giant reverse transcriptase-encoding transposable elements at telomeres
    ( 2017-05) Arkhipova, Irina R. ; Yushenova, Irina A. ; Rodriguez, Fernando
    Transposable elements are omnipresent in eukaryotic genomes and have a profound impact on chromosome structure, function and evolution. Their structural and functional diversity is thought to be reasonably well-understood, especially in retroelements, which transpose via an RNA intermediate copied into cDNA by the element-encoded reverse transcriptase, and are characterized by a compact structure. Here we report a novel type of expandable eukaryotic retroelements, which we call Terminons. These elements can attach to G-rich telomeric repeat overhangs at the chromosome ends, in a process apparently facilitated by complementary C-rich repeats at the 3’-end of the RNA template immediately adjacent to a hammerhead ribozyme motif. Terminon units, which can exceed 40 kb in length, display an unusually complex and diverse structure, and can form very long chains, with host genes often captured between units. As the principal polymerizing component, Terminons contain Athena reverse transcriptases previously described in bdelloid rotifers and belonging to the enigmatic group of Penelope-like elements, but can additionally accumulate multiple co-oriented ORFs, including DEDDy 3’-exonucleases, GDSL esterases/lipases, GIY-YIG-like endonucleases, rolling-circle replication initiator (Rep) proteins, and putatively structural ORFs with coiled-coil motifs and transmembrane domains. The extraordinary length and complexity of Terminons and the high degree of inter-family variability in their ORF content challenge the current views on the structural organization of eukaryotic retroelements, and highlight their possible connections with the viral world and the implications for the elevated frequency of gene transfer.
  • Article
    LTR-retrotransposons from Bdelloid rotifers capture additional ORFs shared between highly diverse retroelement types
    (MDPI AG, 2017-04-11) Rodriguez, Fernando ; Kenefick, Aubrey W. ; Arkhipova, Irina R.
    Rotifers of the class Bdelloidea, microscopic freshwater invertebrates, possess a highlydiversified repertoire of transposon families, which, however, occupy less than 4% of genomic DNA in the sequenced representative Adineta vaga. We performed a comprehensive analysis of A. vaga retroelements, and found that bdelloid long terminal repeat (LTR)retrotransposons, in addition to conserved open reading frame (ORF) 1 and ORF2 corresponding to gag and pol genes, code for an unusually high variety of ORF3 sequences. Retrovirus-like LTR families in A. vaga belong to four major lineages, three of which are rotiferspecific and encode a dUTPase domain. However only one lineage contains a canonical envlike fusion glycoprotein acquired from paramyxoviruses (non-segmented negative-strand RNA viruses), although smaller ORFs with transmembrane domains may perform similar roles. A different ORF3 type encodes a GDSL esterase/lipase, which was previously identified as ORF1 in several clades of non-LTR retrotransposons, and implicated in membrane targeting. Yet another ORF3 type appears in unrelated LTR-retrotransposon lineages, and displays strong homology to DEDDy-type exonucleases involved in 3′-end processing of RNA and single-stranded DNA. Unexpectedly, each of the enzymatic ORF3s is also associated with different subsets of Penelope-like Athena retroelement families. The unusual association of the same ORF types with retroelements from different classes reflects their modular structure with a high degree of flexibility, and points to gene sharing between different groups of retroelements.
  • Article
    Endonuclease-containing Penelope retrotransposons in the bdelloid rotifer Adineta vaga exhibit unusual structural features and play a role in expansion of host gene families
    (BioMed Central, 2013-08-27) Arkhipova, Irina R. ; Yushenova, Irina A. ; Rodriguez, Fernando
    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. 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. 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.
  • Article
    Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga
    (Nature Publishing Group, 2013-07-21) Flot, Jean-Francois ; Hespeels, Boris ; Li, Xiang ; Noel, Benjamin ; Arkhipova, Irina R. ; Danchin, Etienne G. J. ; Hejno, Andreas ; Henrissat, Bernard ; Koszul, Romain ; Aury, Jean-Marc ; Barbe, Valerie ; Barthelemy, Roxane-Marie ; Bast, Jens ; Bazykin, Georgii A. ; Chabrol, Olivier ; Couloux, Arnaud ; Da Rocha, Martine ; Da Silva, Corinne ; Gladyshev, Eugene A. ; Gouret, Philippe ; Hallatschek, Oskar ; Hecox-Lea, Bette ; Labadie, Karine ; Lejeune, Benjamin ; Piskurek, Oliver ; Poulain, Julie ; Rodriguez, Fernando ; Ryan, Joseph F. ; Vakhrusheva, Olga A. ; Wajnberg, Eric ; Wirth, Benedicte ; Yushenova, Irina A. ; Kellis, Manolis ; Kondrashov, Alexey S. ; Mark Welch, David B. ; Pontarotti, Pierre ; Weissenbach, Jean ; Wincker, Patrick ; Jaillon, Olivier ; Van Doninck, Karine
    Loss of sexual reproduction is considered an evolutionary dead end for metazoans, but bdelloid rotifers challenge this view as they appear to have persisted asexually for millions of years1. Neither male sex organs nor meiosis have ever been observed in these microscopic animals: oocytes are formed through mitotic divisions, with no reduction of chromosome number and no indication of chromosome pairing2. However, current evidence does not exclude that they may engage in sex on rare, cryptic occasions. Here we report the genome of a bdelloid rotifer, Adineta vaga (Davis, 1873)3, and show that its structure is incompatible with conventional meiosis. At gene scale, the genome of A. vaga is tetraploid and comprises both anciently duplicated segments and less divergent allelic regions. However, in contrast to sexual species, the allelic regions are rearranged and sometimes even found on the same chromosome. Such structure does not allow meiotic pairing; instead, we find abundant evidence of gene conversion, which may limit the accumulation of deleterious mutations in the absence of meiosis. Gene families involved in resistance to oxidation, carbohydrate metabolism and defence against transposons are significantly expanded, which may explain why transposable elements cover only 3% of the assembled sequence. Furthermore, 8% of the genes are likely to be of non-metazoan origin and were probably acquired horizontally. This apparent convergence between bdelloids and prokaryotes sheds new light on the evolutionary significance of sex.
  • Preprint
    Transposable elements and polyploid evolution in animals
    ( 2018-04) Rodriguez, Fernando ; Arkhipova, Irina R.
    Polyploidy in animals is much less common than in plants, where it is thought to be pervasive in all higher plant lineages. Recent studies have highlighted the impact of polyploidization and the associated process of diploidy restoration on the evolution and speciation of selected taxonomic groups in the animal kingdom: from vertebrates represented by salmonid fishes and African clawed frogs to invertebrates represented by parasitic root-knot nematodes and bdelloid rotifers. In this review, we focus on the unique and diverse roles that transposable elements may play in these processes, from marking and diversifying subgenome-specific chromosome sets prior to hybridization, to influencing genome restructuring during rediploidization, to affecting subgenome-specific regulatory evolution, and occasionally providing opportunities for domestication and gene amplification to restore and improve functionality. There is still much to be learned from the future comparative genomic studies of chromosome-sized and haplotype-aware assemblies, and from post-genomic studies elucidating genetic and epigenetic regulatory phenomena across short and long evolutionary distances in the metazoan tree of life.
  • Preprint
    Ancient mitochondrial pseudogenes reveal hybridization between distant lineages in the evolution of the Rupicapra genus
    ( 2017-07) Pérez, Trinidad ; Rodriguez, Fernando ; Fernández, M. ; Albornoz, Jesús ; Domínguez, Ana
    Mitochondrial pseudogenes (numts) inserted in the nuclear genome are frequently found in population studies. Its presence is commonly connected with problems and errors when they are confounded with true mitochondrial sequences. In the opposite side, numts can provide valuable phylogenetic information when they are copies of ancient mitochondrial lineages. We show that Rupicapra individuals of different geographic origin from the Cantabrian Mountains to the Apennines and the Caucasus share a nuclear COI fragment. The numt copies are monophyletic, and their pattern of differentiation shows two outstanding features: a long evolution as differentiated true mitochondrial lineage, and a recent integration and spread through the chamois populations. The COI pseudogene is much older than the present day mitochondrial clades of Rupicapra and occupies a basal position within the Rupicapra-Ammotragus- Arabitragus node. Joint analysis of this numt and a cytb pseudogene with a similar pattern of evolution places the source mitochondrial lineage as a sister branch that separated from the Ammotragus-Arabitragus lineage 6 million years ago (Mya). The occurrence of this sequence in the nucleus of chamois suggests hybridization between highly divergent lineages. The integration event seems to be very recent, more recent than the split of the present day mtDNA lineages of Rupicapra (1.9 Mya). This observation invites to think of the spread across the genus by horizontal transfer through recent male-biased dispersal.