Comparative Analysis of Transposable Elements Highlights Mobilome Diversity and Evolution in Vertebrates

Transposable elements (TEs) are major components of vertebrate genomes, with major roles in genome architecture and evolution. In order to characterize both common patterns and lineage-specific differences in TE content and TE evolution, we have compared the mobilomes of 23 vertebrate genomes, including 10 actinopterygian fish, 11 sarcopterygians, and 2 nonbony vertebrates. We found important variations in TE content (from 6% in the pufferfish tetraodon to 55% in zebrafish), with a more important relative contribution of TEs to genome size in fish than in mammals. Some TE superfamilies were found to be widespread in vertebrates, but most elements showed a more patchy distribution, indicative of multiple events of loss or gain. Interestingly, loss of major TE families was observed during the evolution of the sarcopterygian lineage, with a particularly strong reduction in TE diversity in birds and mammals. Phylogenetic trends in TE composition and activity were detected: Teleost fish genomes are dominated by DNA transposons and contain few ancient TE copies, while mammalian genomes have been predominantly shaped by nonlong terminal repeat retrotransposons, along with the persistence of older sequences. Differences were also found within lineages: The medaka fish genome underwent more recent TE amplification than the related platyfish, as observed for LINE retrotransposons in the mouse compared with the human genome. This study allows the identification of putative cases of horizontal transfer of TEs, and to tentatively infer the composition of the ancestral vertebrate mobilome. Taken together, the results obtained highlight the importance of TEs in the structure and evolution of vertebrate genomes, and demonstrate their major impact on genome diversity both between and within lineages.

[1]  A. Meyer,et al.  Evolutionary active transposable elements in the genome of the coelacanth. , 2014, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[2]  C. Ellison,et al.  Dosage Compensation via Transposable Element Mediated Rewiring of a Regulatory Network , 2013, Science.

[3]  S. Boissinot,et al.  Lizards and LINEs: Selection and Demography Affect the Fate of L1 Retrotransposons in the Genome of the Green Anole (Anolis carolinensis) , 2013, Genome biology and evolution.

[4]  S. Searle,et al.  The duck genome and transcriptome provide insight into an avian influenza virus reservoir species , 2013, Nature Genetics.

[5]  Keith L. Ligon,et al.  DNA hypomethylation within specific transposable element families associates with tissue-specific enhancer landscape , 2013, Nature Genetics.

[6]  G. Bourque,et al.  The Majority of Primate-Specific Regulatory Sequences Are Derived from Transposable Elements , 2013, PLoS genetics.

[7]  Jing He,et al.  Peregrine and saker falcon genome sequences provide insights into evolution of a predatory lifestyle , 2013, Nature Genetics.

[8]  Sonja J. Prohaska,et al.  Analysis of the African coelacanth genome sheds light on tetrapod evolution , 2013, Nature.

[9]  Zev N. Kronenberg,et al.  Transposable Elements Are Major Contributors to the Origin, Diversification, and Regulation of Vertebrate Long Noncoding RNAs , 2013, PLoS genetics.

[10]  Angel Amores,et al.  The genome of the platyfish, Xiphophorus maculatus, provides insights into evolutionary adaptation and several complex traits , 2013, Nature Genetics.

[11]  D. Casane,et al.  Accommodating the load , 2013, Mobile genetic elements.

[12]  M. Evgen’ev What happens when Penelope comes? , 2013, Mobile genetic elements.

[13]  A. Luchetti,et al.  Non-LTR R2 Element Evolutionary Patterns: Phylogenetic Incongruences, Rapid Radiation and the Maintenance of Multiple Lineages , 2013, PloS one.

[14]  Horizontal transfer of OC1 transposons in the Tasmanian devil , 2013, BMC Genomics.

[15]  D. Adelson,et al.  Widespread horizontal transfer of retrotransposons , 2012, Proceedings of the National Academy of Sciences.

[16]  A. Blinov,et al.  Vertical evolution and horizontal transfer of CR1 non-LTR retrotransposons and Tc1/mariner DNA transposons in Lepidoptera species. , 2012, Molecular biology and evolution.

[17]  Pall I. Olason,et al.  The genomic landscape of species divergence in Ficedula flycatchers , 2012, Nature.

[18]  D. Mager,et al.  Transposable elements: an abundant and natural source of regulatory sequences for host genes. , 2012, Annual review of genetics.

[19]  M. Syvanen,et al.  Evolutionary implications of horizontal gene transfer. , 2012, Annual review of genetics.

[20]  J. Jurka,et al.  Horizontal transfers of Mariner transposons between mammals and insects , 2012, Mobile DNA.

[21]  A. Meyer,et al.  Horizontal Transfers of Tc1 Elements between Teleost Fishes and Their Vertebrate Parasites, Lampreys , 2012, Genome biology and evolution.

[22]  M. F. Ortiz,et al.  Horizontal Transposon Transfer in Eukarya: Detection, Bias, and Perspectives , 2012, Genome biology and evolution.

[23]  D. C. Hancks,et al.  Active human retrotransposons: variation and disease. , 2012, Current opinion in genetics & development.

[24]  J. Boeke,et al.  Human Transposon Tectonics , 2012, Cell.

[25]  S. Boissinot,et al.  Accumulation and Rapid Decay of Non-LTR Retrotransposons in the Genome of the Three-Spine Stickleback , 2012, Genome biology and evolution.

[26]  Alex A. Pollen,et al.  The genomic basis of adaptive evolution in threespine sticklebacks , 2012, Nature.

[27]  J. Volff,et al.  Zisupton--a novel superfamily of DNA transposable elements recently active in fish. , 2012, Molecular biology and evolution.

[28]  C. Feschotte,et al.  Rampant horizontal transfer of SPIN transposons in squamate reptiles. , 2012, Molecular biology and evolution.

[29]  R. Mueller,et al.  LTR Retrotransposons Contribute to Genomic Gigantism in Plethodontid Salamanders , 2011, Genome biology and evolution.

[30]  M. Batzer,et al.  Repetitive Elements May Comprise Over Two-Thirds of the Human Genome , 2011, PLoS genetics.

[31]  N. Jeffery,et al.  A guided tour of large genome size in animals: what we know and where we are heading , 2011, Chromosome Research.

[32]  J. Jurka,et al.  Crypton transposons: identification of new diverse families and ancient domestication events , 2011, Mobile DNA.

[33]  D. Higgins,et al.  Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega , 2011, Molecular systems biology.

[34]  J. Brookfield Host-parasite relationships in the genome , 2011, BMC Biology.

[35]  J. V. Moran,et al.  Dynamic interactions between transposable elements and their hosts , 2011, Nature Reviews Genetics.

[36]  S. Wright,et al.  Co-evolution between transposable elements and their hosts: a major factor in genome size evolution? , 2011, Chromosome Research.

[37]  Samuel E. Fox,et al.  Discovery of Highly Divergent Repeat Landscapes in Snake Genomes Using High-Throughput Sequencing , 2011, Genome biology and evolution.

[38]  D. Jackson,et al.  Tracking the ancestry of a deeply conserved eumetazoan SINE domain. , 2011, Molecular biology and evolution.

[39]  D. Ray,et al.  The limited distribution of Helitrons to vesper bats supports horizontal transfer. , 2011, Gene.

[40]  E. Sarropoulou,et al.  Comparative genomics in teleost species: Knowledge transfer by linking the genomes of model and non-model fish species. , 2011, Comparative biochemistry and physiology. Part D, Genomics & proteomics.

[41]  A. Wagner,et al.  BEL/Pao retrotransposons in metazoan genomes , 2011, BMC Evolutionary Biology.

[42]  Albert J. Vilella,et al.  Multi-Platform Next-Generation Sequencing of the Domestic Turkey (Meleagris gallopavo): Genome Assembly and Analysis , 2010, PLoS biology.

[43]  O. Gascuel,et al.  SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. , 2010, Molecular biology and evolution.

[44]  S. Boissinot,et al.  Independent and parallel lateral transfer of DNA transposons in tetrapod genomes. , 2010, Gene.

[45]  D. Kordis Transposable Elements in Reptilian and Avian (Sauropsida) Genomes , 2010, Cytogenetic and Genome Research.

[46]  Igor Vorechovsky,et al.  Transposable elements in disease-associated cryptic exons , 2010, Human Genetics.

[47]  M. A. McClure,et al.  The evolutionary dynamics of autonomous non-LTR retrotransposons in the lizard Anolis carolinensis shows more similarity to fish than mammals. , 2009, Molecular biology and evolution.

[48]  B. Venkatesh,et al.  Rapidly evolving fish genomes and teleost diversity. , 2008, Current opinion in genetics & development.

[49]  Marlen S. Clark,et al.  Repeated horizontal transfer of a DNA transposon in mammals and other tetrapods , 2008, Proceedings of the National Academy of Sciences.

[50]  H. Kazazian,et al.  Retrotransposons Revisited: The Restraint and Rehabilitation of Parasites , 2008, Cell.

[51]  T. Eickbush,et al.  The diversity of retrotransposons and the properties of their reverse transcriptases. , 2008, Virus research.

[52]  C. Feschotte Transposable elements and the evolution of regulatory networks , 2008, Nature Reviews Genetics.

[53]  Laura Wegener Parfrey,et al.  The dynamic nature of eukaryotic genomes. , 2008, Molecular biology and evolution.

[54]  Jean-Nicolas Volff,et al.  Transposable elements as drivers of genomic and biological diversity in vertebrates , 2008, Chromosome Research.

[55]  C. Feschotte,et al.  DNA transposons and the evolution of eukaryotic genomes. , 2007, Annual review of genetics.

[56]  J. Bennetzen,et al.  A unified classification system for eukaryotic transposable elements , 2007, Nature Reviews Genetics.

[57]  T. Markow,et al.  Analysis of Drosophila Species Genome Size and Satellite DNA Content Reveals Significant Differences Among Strains as Well as Between Species , 2007, Genetics.

[58]  M. A. McClure,et al.  Identification of Novel Retroid Agents in Danio rerio, Oryzias latipes, Gasterosteus aculeatus and Tetraodon nigroviridis , 2007, Evolutionary bioinformatics online.

[59]  N. Okada,et al.  Poxviruses as possible vectors for horizontal transfer of retroposons from reptiles to mammals , 2007, Proceedings of the National Academy of Sciences.

[60]  Cédric Feschotte,et al.  Massive amplification of rolling-circle transposons in the lineage of the bat Myotis lucifugus , 2007, Proceedings of the National Academy of Sciences.

[61]  Joel Dudley,et al.  TimeTree: a public knowledge-base of divergence times among organisms , 2006, Bioinform..

[62]  H. Krambeck,et al.  Competition may determine the diversity of transposable elements. , 2006, Theoretical population biology.

[63]  Arnaud Le Rouzic,et al.  Population Genetics Models of Competition Between Transposable Element Subfamilies , 2006, Genetics.

[64]  J. Volff Turning junk into gold: domestication of transposable elements and the creation of new genes in eukaryotes , 2006, BioEssays : news and reviews in molecular, cellular and developmental biology.

[65]  J. Jurka,et al.  Self-synthesizing DNA transposons in eukaryotes. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[66]  P. Capy,et al.  Theoretical Approaches to the Dynamics of Transposable Elements in Genomes, Populations, and Species , 2006 .

[67]  S. Yi,et al.  Genome size is negatively correlated with effective population size in ray-finned fish. , 2005, Trends in genetics : TIG.

[68]  C. Feschotte,et al.  Non-mammalian c-integrases are encoded by giant transposable elements. , 2005, Trends in genetics : TIG.

[69]  R. Poulter,et al.  DIRS-1 and the other tyrosine recombinase retrotransposons , 2005, Cytogenetic and Genome Research.

[70]  J. Weissenbach,et al.  Diversity and clustered distribution of retrotransposable elements in the compact genome of the pufferfish Tetraodon nigroviridis , 2005, Cytogenetic and Genome Research.

[71]  J. Jurka,et al.  RAG1 Core and V(D)J Recombination Signal Sequences Were Derived from Transib Transposons , 2005, PLoS biology.

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

[73]  E. Eichler,et al.  Lineage-Specific Expansions of Retroviral Insertions within the Genomes of African Great Apes but Not Humans and Orangutans , 2005, PLoS biology.

[74]  P. Capy,et al.  The First Steps of Transposable Elements Invasion , 2005, Genetics.

[75]  M. Kimura A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences , 1980, Journal of Molecular Evolution.

[76]  J. Volff Genome evolution and biodiversity in teleost fish , 2005, Heredity.

[77]  Charles E. Chapple,et al.  Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype , 2004, Nature.

[78]  D. Duvernell,et al.  Teleost Fish Genomes Contain a Diverse Array of L1 RetrotransposonLineages That Exhibit a Low Copy Number and High Rate of Turnover , 2004, Journal of Molecular Evolution.

[79]  C. Feschotte Merlin, a new superfamily of DNA transposons identified in diverse animal genomes and related to bacterial IS1016 insertion sequences. , 2004, Molecular biology and evolution.

[80]  Burkhard Morgenstern,et al.  AUGUSTUS: a web server for gene finding in eukaryotes , 2004, Nucleic Acids Res..

[81]  H. Kazazian Mobile Elements: Drivers of Genome Evolution , 2004, Science.

[82]  M. Tristem,et al.  The Evolution, Distribution and Diversity of Endogenous Retroviruses , 2003, Virus Genes.

[83]  M. G. Kidwell,et al.  Transposable elements and the evolution of genome size in eukaryotes , 2002, Genetica.

[84]  John M. Hancock Genome size and the accumulation of simple sequence repeats: implications of new data from genome sequencing projects , 2002, Genetica.

[85]  S. Boissinot,et al.  L1 (LINE-1) retrotransposon diversity differs dramatically between mammals and fish. , 2004, Trends in genetics : TIG.

[86]  G. Barlow,et al.  Fishes of the world , 2004, Environmental Biology of Fishes.

[87]  J. Volff,et al.  Diversity of retrotransposable elements in compact pufferfish genomes. , 2003, Trends in genetics : TIG.

[88]  J. V. Moran,et al.  Mobile elements and mammalian genome evolution. , 2003, Current opinion in genetics & development.

[89]  M. Lynch,et al.  The Origins of Genome Complexity , 2003, Science.

[90]  J. Weissenbach,et al.  Remarkable compartmentalization of transposable elements and pseudogenes in the heterochromatin of the Tetraodon nigroviridis genome , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[91]  C. Vieira,et al.  Evolution of genome size in Drosophila. is the invader's genome being invaded by transposable elements? , 2002, Molecular biology and evolution.

[92]  M. Miya,et al.  V-SINEs: a new superfamily of vertebrate SINEs that are widespread in vertebrate genomes and retain a strongly conserved segment within each repetitive unit. , 2002, Genome research.

[93]  M. Schartl,et al.  Medaka — a model organism from the far east , 2002, Nature Reviews Genetics.

[94]  T. Gregory The bigger the C-value, the larger the cell: genome size and red blood cell size in vertebrates. , 2001, Blood cells, molecules & diseases.

[95]  J. Jurka,et al.  Rolling-circle transposons in eukaryotes , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[96]  J. Volff,et al.  Non-LTR Retrotransposons Encoding a Restriction Enzyme-Like Endonuclease in Vertebrates , 2001, Journal of Molecular Evolution.

[97]  D. Petrov Evolution of genome size: new approaches to an old problem. , 2001, Trends in genetics : TIG.

[98]  J. Jurka Repbase update: a database and an electronic journal of repetitive elements. , 2000, Trends in genetics : TIG.

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

[100]  T. Eickbush,et al.  The age and evolution of non-LTR retrotransposable elements. , 1999, Molecular biology and evolution.

[101]  D. Kordis,et al.  Horizontal transfer of non-LTR retrotransposons in vertebrates. , 1999, Genetica.

[102]  T. Garland,et al.  Effects of branch length errors on the performance of phylogenetically independent contrasts. , 1998, Systematic biology.

[103]  M. Gellert,et al.  DNA Transposition by the RAG1 and RAG2 Proteins A Possible Source of Oncogenic Translocations , 1998, Cell.

[104]  David G. Schatz,et al.  Transposition mediated by RAG1 and RAG2 and its implications for the evolution of the immune system , 1998, Nature.

[105]  Jerzy Jurka,et al.  Censor - a Program for Identification and Elimination of Repetitive Elements From DNA Sequences , 1996, Comput. Chem..

[106]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[107]  D. Finnegan,et al.  Eukaryotic transposable elements and genome evolution. , 1989, Trends in genetics : TIG.

[108]  J. Felsenstein Phylogenies and the Comparative Method , 1985, The American Naturalist.