Evolutionary dynamics of the LTR retrotransposons roo and rooA inferred from twelve complete Drosophila genomes

BackgroundRoo is the most abundant retrotransposon in the fruit fly Drosophila melanogaster. Its evolutionary origins and dynamics are thus of special interest for understanding the evolutionary history of Drosophila genome organization. We here study the phylogenetic distribution and evolution of roo, and its highly diverged relative rooA in 12 completely sequenced genomes of the genus Drosophila.ResultsWe identify a total of 164 roo copies, 57 of which were previously unidentified copies that occur in 9 of the 12 genomes. Additionally we find 66 rooA copies in four genomes and remnants of this element in two additional genomes. We further increased the number of elements by searching for individual roo/rooA sequence domains. Most of our roo and rooA elements have been recently inserted. Most elements within a genome are highly similar. A comparison of the phylogenetic tree of our roo and rooA elements shows that the split between roo and rooA took place early in Drosophila evolution. Furthermore there is one incongruency between the species tree and the phylogenetic tree of the roo element. This incongruency regards the placement of elements from D. mojavensis, which are more closely related to D. melanogaster than elements from D. willistoni.ConclusionWithin genomes, the evolutionary dynamics of roo and rooA range from recent transpositional activity to slow decay and extinction. Among genomes, the balance of phylogenetic evidence, sequence divergence distribution, and the occurrence of solo-LTR elements suggests an origin of roo/rooA within the Drosophila clade. We discuss the possibility of a horizontal gene transfer of roo within this clade.

[1]  A. P. Kotnova,et al.  Polymorphism of canonical and noncanonical gypsy sequences in different species of Drosophila melanogaster subgroup: possible evolutionary relations , 2008, Molecular Genetics and Genomics.

[2]  C. Vieira,et al.  Wake up of transposable elements following Drosophila simulans worldwide colonization. , 1999, Molecular biology and evolution.

[3]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

[4]  K. Katoh,et al.  MAFFT version 5: improvement in accuracy of multiple sequence alignment , 2005, Nucleic acids research.

[5]  Alexander Souvorov,et al.  Genomic BLAST: custom-defined virtual databases for complete and unfinished genomes. , 2002, FEMS microbiology letters.

[6]  D. Higgins,et al.  T-Coffee: A novel method for fast and accurate multiple sequence alignment. , 2000, Journal of molecular biology.

[7]  H. Lasker,et al.  Phylogeography and morphological variation of the branching octocoral Pseudopterogorgia elisabethae. , 2009, Molecular phylogenetics and evolution.

[8]  C. Tschudi,et al.  B104, a new dispersed repeated gene family in Drosophila melanogaster and its analogies with retroviruses. , 1982, Journal of molecular biology.

[9]  D. Haussler,et al.  Hidden Markov models in computational biology. Applications to protein modeling. , 1993, Journal of molecular biology.

[10]  G. Fink,et al.  Movement of yeast transposable elements by gene conversion. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[11]  Volff Jn Genome evolution and biodiversity in teleost fish , 2005 .

[12]  C. Walsh,et al.  Cytosine methylation and the ecology of intragenomic parasites. , 1997, Trends in genetics : TIG.

[13]  Chuong B. Do,et al.  ProbCons: Probabilistic consistency-based multiple sequence alignment. , 2005, Genome research.

[14]  I. Longden,et al.  EMBOSS: the European Molecular Biology Open Software Suite. , 2000, Trends in genetics : TIG.

[15]  B. Charlesworth,et al.  High rate of horizontal transfer of transposable elements in Drosophila. , 2005, Trends in genetics : TIG.

[16]  Ruggiero Caizzi,et al.  A genome-wide screening of BEL-Pao like retrotransposons in Anopheles gambiae by the LTR_STRUC program. , 2005, Gene.

[17]  O. Gascuel,et al.  Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. , 2006, Systematic biology.

[18]  T. Heidmann,et al.  Taming of transposable elements by homology-dependent gene silencing , 1999, Nature Genetics.

[19]  Phillip SanMiguel,et al.  The paleontology of intergene retrotransposons of maize , 1998, Nature Genetics.

[20]  Ziheng Yang PAML 4: phylogenetic analysis by maximum likelihood. , 2007, Molecular biology and evolution.

[21]  C. Vieira,et al.  The heterochromatic copies of the LTR retrotransposons as a record of the genomic events that have shaped the Drosophila melanogaster genome. , 2008, Gene.

[22]  Wolfgang Stephan,et al.  The evolutionary dynamics of repetitive DNA in eukaryotes , 1994, Nature.

[23]  C. Biémont,et al.  Distribution of transposable elements in Drosophila species , 2004, Genetica.

[24]  A. Wagner,et al.  A survey of bacterial insertion sequences using IScan , 2007, Nucleic acids research.

[25]  Melanie A. Huntley,et al.  Evolution of genes and genomes on the Drosophila phylogeny , 2007, Nature.

[26]  J. Bennetzen,et al.  Mechanisms and rates of genome expansion and contraction in flowering plants , 2002, Genetica.

[27]  A. Löytynoja,et al.  Phylogeny-Aware Gap Placement Prevents Errors in Sequence Alignment and Evolutionary Analysis , 2008, Science.

[28]  E. Hafen,et al.  The dominant mutation Glazed is a gain-of-function allele of wingless that, similar to loss of APC, interferes with normal eye development. , 1999, Developmental biology.

[29]  Alan M. Lambowitz,et al.  Mobile DNA III , 2002 .

[30]  Y. Miki Retrotransposal integration of mobile genetic elements in human diseases , 1998, Journal of Human Genetics.

[31]  C. Langley,et al.  Chromosome rearrangement by ectopic recombination in Drosophila melanogaster: genome structure and evolution. , 1991, Genetics.

[32]  Emmanuelle Lerat,et al.  Sequence divergence within transposable element families in the Drosophila melanogaster genome. , 2003, Genome research.

[33]  J. Galagan,et al.  RIP: the evolutionary cost of genome defense. , 2004, Trends in genetics : TIG.

[34]  O. Gascuel,et al.  A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. , 2003, Systematic biology.

[35]  I. K. Jordan,et al.  Evidence for the Role of Recombination in the Regulatory Evolution of Saccharomyces cerevisiae Ty Elements , 1998, Journal of Molecular Evolution.

[36]  M. Ashburner,et al.  The transposable elements of the Drosophila melanogaster euchromatin: a genomics perspective , 2002, Genome Biology.

[37]  Dmitri A. Petrov,et al.  DNA loss and evolution of genome size in Drosophila , 2002, Genetica.

[38]  Francisco J. Ayala,et al.  Fluctuating Mutation Bias and the Evolution of Base Composition in Drosophila , 2000, Journal of Molecular Evolution.

[39]  Elliot M. Meyerowitz,et al.  Molecular organization of a Drosophila puff site that responds to ecdysone , 1982, Cell.

[40]  Robert D. Finn,et al.  The Pfam protein families database , 2004, Nucleic Acids Res..

[41]  R. Plasterk,et al.  RNAi protects the Caenorhabditis elegans germline against transposition. , 2004, Trends in genetics : TIG.

[42]  L. Holm,et al.  The Pfam protein families database , 2005, Nucleic Acids Res..

[43]  N. Bowen,et al.  Drosophila euchromatic LTR retrotransposons are much younger than the host species in which they reside. , 2001, Genome research.

[44]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[45]  Xabier Bello,et al.  Widespread evidence for horizontal transfer of transposable elements across Drosophila genomes , 2008, Genome Biology.

[46]  R. Poulter,et al.  New BEL-like LTR-retrotransposons in Fugu rubripes, Caenorhabditis elegans, and Drosophila melanogaster. , 2001, Gene.

[47]  Robert D. Finn,et al.  Pfam: clans, web tools and services , 2005, Nucleic Acids Res..