Comprehensive identification of potentially functional genes for transposon mobility in the C. elegans genome

Transposons are mobile DNA elements that encode genes for their own mobility. Whereas transposon copies accumulate on the genome during evolution, many lose their mobile activity due to mutations. Here, we focus on transposon-encoded genes that are directly involved in the replication, excision, and integration of transposon DNA, which we refer to as “transposon-mobility genes”, in the Caenorhabditis elegans genome. Among the 62,773 copies of retro- and DNA transposons in the latest assembly of the C. elegans genome (VC2010), we found that the complete open reading frame structure was conserved in 290 transposon-mobility genes. Critical amino acids at the catalytic core were conserved in only 145 of these 290 genes. Thus, in contrast to the huge number of transposon copies in the genome, only a limited number of transposons are autonomously mobile. We conclude that the comprehensive identification of potentially functional transposon-mobility genes in all transposon orders of a single species can provide a basis of molecular analysis for revealing the developmental, aging, and evolutionary roles of transposons.

[1]  C. Mello,et al.  The CERV protein of Cer1, a C. elegans LTR retrotransposon, is required for nuclear export of viral genomic RNA and can form giant nuclear rods , 2023, PLoS genetics.

[2]  Rebecca S. Moore,et al.  The role of the Cer1 transposon in horizontal transfer of transgenerational memory , 2021, Cell.

[3]  A. Engelman,et al.  Structure and function of retroviral integrase , 2021, Nature Reviews Microbiology.

[4]  C. Feschotte,et al.  A Field Guide to Eukaryotic Transposable Elements. , 2020, Annual review of genetics.

[5]  Shinichi Morishita,et al.  Recompleting the Caenorhabditis elegans genome , 2019, Genome research.

[6]  N. Holroyd,et al.  Biology and genome of a newly discovered sibling species of Caenorhabditis elegans , 2018, Nature Communications.

[7]  Peter N. Robinson,et al.  L1Base 2: more retrotransposition-active LINE-1s, more mammalian genomes , 2016, Nucleic Acids Res..

[8]  F. Dyda,et al.  DNA Transposition at Work. , 2016, Chemical reviews.

[9]  D. Adelson,et al.  LINEs between Species: Evolutionary Dynamics of LINE-1 Retrotransposons across the Eukaryotic Tree of Life , 2016, bioRxiv.

[10]  V. Belancio,et al.  The endonuclease domain of the LINE-1 ORF2 protein can tolerate multiple mutations , 2016, Mobile DNA.

[11]  Andreas Gogol-Döring,et al.  A Helitron transposon reconstructed from bats reveals a novel mechanism of genome shuffling in eukaryotes , 2016, Nature Communications.

[12]  E. Koonin,et al.  A novel group of diverse Polinton-like viruses discovered by metagenome analysis , 2015, BMC Biology.

[13]  O. Kohany,et al.  Repbase Update, a database of repetitive elements in eukaryotic genomes , 2015, Mobile DNA.

[14]  E. Koonin,et al.  Origins and evolution of viruses of eukaryotes: The ultimate modularity , 2015, Virology.

[15]  E. Koonin,et al.  Polintons: a hotbed of eukaryotic virus, transposon and plasmid evolution , 2014, Nature Reviews Microbiology.

[16]  Chao Xie,et al.  Fast and sensitive protein alignment using DIAMOND , 2014, Nature Methods.

[17]  M. Blaxter,et al.  The Evolution of Tyrosine-Recombinase Elements in Nematoda , 2014, PloS one.

[18]  F. Dyda,et al.  Breaking and joining single-stranded DNA: the HUH endonuclease superfamily , 2013, Nature Reviews Microbiology.

[19]  Anton J. Enright,et al.  The zebrafish reference genome sequence and its relationship to the human genome , 2013, Nature.

[20]  K. Katoh,et al.  MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability , 2013, Molecular biology and evolution.

[21]  J. Boeke,et al.  Active transposition in genomes. , 2012, Annual review of genetics.

[22]  S. L. Le Grice Human Immunodeficiency Virus Reverse Transcriptase: 25 Years of Research, Drug Discovery, and Promise* , 2012, The Journal of Biological Chemistry.

[23]  P. Cherepanov,et al.  3′-Processing and strand transfer catalysed by retroviral integrase in crystallo , 2012, The EMBO journal.

[24]  J. Priess,et al.  C. elegans Germ Cells Show Temperature and Age-Dependent Expression of Cer1, a Gypsy/Ty3-Related Retrotransposon , 2012, PLoS pathogens.

[25]  S. Wessler,et al.  The catalytic domain of all eukaryotic cut-and-paste transposase superfamilies , 2011, Proceedings of the National Academy of Sciences.

[26]  P. Hackett,et al.  DDE transposases: Structural similarity and diversity. , 2010, Advanced drug delivery reviews.

[27]  E. Skordalakes,et al.  Structural basis for telomerase catalytic subunit TERT binding to RNA template and telomeric DNA , 2010, Nature Structural &Molecular Biology.

[28]  J. Jurka,et al.  Ginger DNA transposons in eukaryotes and their evolutionary relationships with long terminal repeat retrotransposons , 2010, Mobile DNA.

[29]  M. Batzer,et al.  The impact of retrotransposons on human genome evolution , 2009, Nature Reviews Genetics.

[30]  M. Walkinshaw,et al.  Molecular Architecture of the Mos1 Paired-End Complex: The Structural Basis of DNA Transposition in a Eukaryote , 2009, Cell.

[31]  L. Kruglyak,et al.  Molecular basis of the copulatory plug polymorphism in Caenorhabditis elegans , 2008, Nature.

[32]  J. Jurka,et al.  A universal classification of eukaryotic transposable elements implemented in Repbase , 2008, Nature Reviews Genetics.

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

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

[35]  J. Jurka,et al.  Helitrons on a roll: eukaryotic rolling-circle transposons. , 2007, Trends in genetics : TIG.

[36]  C. Feschotte,et al.  Mavericks, a novel class of giant transposable elements widespread in eukaryotes and related to DNA viruses. , 2007, Gene.

[37]  I. Arkhipova Distribution and phylogeny of Penelope-like elements in eukaryotes. , 2006, Systematic biology.

[38]  Michael Ashburner,et al.  Recurrent insertion and duplication generate networks of transposable element sequences in the Drosophila melanogaster genome , 2006, Genome Biology.

[39]  B. Preston,et al.  Hypersusceptibility to Substrate Analogs Conferred by Mutations in Human Immunodeficiency Virus Type 1 Reverse Transcriptase , 2006, Journal of Virology.

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

[41]  Z. Sauna,et al.  The A‐loop, a novel conserved aromatic acid subdomain upstream of the Walker A motif in ABC transporters, is critical for ATP binding , 2006, FEBS letters.

[42]  J. Bessereau Transposons in C. elegans. , 2006, WormBook : the online review of C. elegans biology.

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

[44]  R. Ghirlando,et al.  Molecular architecture of a eukaryotic DNA transposase , 2005, Nature Structural &Molecular Biology.

[45]  D. Voytas,et al.  A eukaryotic gene family related to retroelement integrases. , 2005, Trends in genetics : TIG.

[46]  I. Arkhipova,et al.  Reverse transcriptase and endonuclease activities encoded by Penelope-like retroelements. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[47]  Ian Korf,et al.  Gene finding in novel genomes , 2004, BMC Bioinformatics.

[48]  S. Wessler,et al.  Genome-wide comparative analysis of the transposable elements in the related species Arabidopsis thaliana and Brassica oleracea. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[49]  R. Poulter,et al.  Cryptons: a group of tyrosine-recombinase-encoding DNA transposons from pathogenic fungi. , 2003, Microbiology.

[50]  V. Wood,et al.  Retrotransposons and their recognition of pol II promoters: a comprehensive survey of the transposable elements from the complete genome sequence of Schizosaccharomyces pombe. , 2003, Genome research.

[51]  R. Plasterk,et al.  Continuous exchange of sequence information between dispersed Tc1 transposons in the Caenorhabditis elegans genome. , 2003, Genetics.

[52]  J. V. Moran,et al.  Hot L1s account for the bulk of retrotransposition in the human population , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[53]  K. Katoh,et al.  MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. , 2002, Nucleic acids research.

[54]  J. V. Moran,et al.  DNA repair mediated by endonuclease-independent LINE-1 retrotransposition , 2002, Nature Genetics.

[55]  W. Reznikoff,et al.  Tn5 Transposase Active Site Mutants* , 2002, The Journal of Biological Chemistry.

[56]  I. Rayment,et al.  Two-metal active site binding of a Tn5 transposase synaptic complex , 2002, Nature Structural Biology.

[57]  E. Ganko,et al.  Evolutionary history of Cer elements and their impact on the C. elegans genome. , 2001, Genome research.

[58]  R. Poulter,et al.  The DIRS1 group of retrotransposons. , 2001, Molecular biology and evolution.

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

[60]  M. G. Kidwell,et al.  PERSPECTIVE: TRANSPOSABLE ELEMENTS, PARASITIC DNA, AND GENOME EVOLUTION , 2001, Evolution; international journal of organic evolution.

[61]  W. Reznikoff,et al.  Three-dimensional structure of the Tn5 synaptic complex transposition intermediate. , 2000, Science.

[62]  M. Hall,et al.  Helicase motifs: the engine that powers DNA unwinding , 1999, Molecular microbiology.

[63]  N. Bowen,et al.  Genomic analysis of Caenorhabditis elegans reveals ancient families of retroviral-like elements. , 1999, Genome research.

[64]  S. Velankar,et al.  Crystal Structures of Complexes of PcrA DNA Helicase with a DNA Substrate Indicate an Inchworm Mechanism , 1999, Cell.

[65]  M. Labrador,et al.  Evolutionary relationships among the members of an ancient class of non-LTR retrotransposons found in the nematode Caenorhabditis elegans. , 1998, Molecular biology and evolution.

[66]  D. Voytas,et al.  Transposable elements and genome organization: a comprehensive survey of retrotransposons revealed by the complete Saccharomyces cerevisiae genome sequence. , 1998, Genome research.

[67]  S. Walker,et al.  Mutational analysis of the adeno-associated virus type 2 Rep68 protein helicase motifs , 1997, Journal of virology.

[68]  S. Weller,et al.  Biochemical Analyses of Mutations in the HSV-1 Helicase-Primase That Alter ATP Hydrolysis, DNA Unwinding, and Coupling Between Hydrolysis and Unwinding* , 1997, The Journal of Biological Chemistry.

[69]  S. Peltz,et al.  Genetic and biochemical characterization of mutations in the ATPase and helicase regions of the Upf1 protein , 1996, Molecular and cellular biology.

[70]  S. Sarafianos,et al.  Biochemical analysis of catalytically crucial aspartate mutants of human immunodeficiency virus type 1 reverse transcriptase. , 1996, Biochemistry.

[71]  P. Capy,et al.  Relationships between transposable elements based upon the integrase-transposase domains: Is there a common ancestor? , 1996, Journal of Molecular Evolution.

[72]  R. Plasterk,et al.  Rte‐1, a retrotransposon‐like element in Caenorhabditis elegans , 1996, FEBS letters.

[73]  N. Kleckner,et al.  The Three Chemical Steps of Tn10/IS10 Transposition Involve Repeated Utilization of a Single Active Site , 1996, Cell.

[74]  R. Brosh,et al.  Mutations in motif II of Escherichia coli DNA helicase II render the enzyme nonfunctional in both mismatch repair and excision repair with differential effects on the unwinding reaction , 1995, Journal of bacteriology.

[75]  A. D. Clark,et al.  Crystal structure of human immunodeficiency virus type 1 reverse transcriptase complexed with double-stranded DNA at 3.0 A resolution shows bent DNA. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[76]  E V Koonin,et al.  A common set of conserved motifs in a vast variety of putative nucleic acid-dependent ATPases including MCM proteins involved in the initiation of eukaryotic DNA replication. , 1993, Nucleic acids research.

[77]  Eugene V. Koonin,et al.  Helicases: amino acid sequence comparisons and structure-function relationships , 1993 .

[78]  R. Plasterk,et al.  Mutational analysis of the integrase protein of human immunodeficiency virus type 2. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[79]  J. Mous,et al.  Identification of amino acid residues critical for endonuclease and integration activities of HIV-1 IN protein in vitro. , 1992, Virology.

[80]  A. Skalka,et al.  Residues critical for retroviral integrative recombination in a region that is highly conserved among retroviral/retrotransposon integrases and bacterial insertion sequence transposases , 1992, Molecular and cellular biology.

[81]  P. Boyer,et al.  Cassette mutagenesis of the reverse transcriptase of human immunodeficiency virus type 1 , 1992, Journal of virology.

[82]  T. Naas,et al.  Subunit‐selective mutagenesis indicates minimal polymerase activity in heterodimer‐associated p51 HIV‐1 reverse transcriptase. , 1991, The EMBO journal.

[83]  T. Eickbush,et al.  Origin and evolution of retroelements based upon their reverse transcriptase sequences. , 1990, The EMBO journal.

[84]  P Argos,et al.  An attempt to unify the structure of polymerases. , 1990, Protein engineering.

[85]  I Sauvaget,et al.  Identification of four conserved motifs among the RNA‐dependent polymerase encoding elements. , 1989, The EMBO journal.

[86]  H. Lodish,et al.  Sequence of Dictyostelium DIRS-1: An apparent retrotransposon with inverted terminal repeats and an internal circle junction sequence , 1985, Cell.

[87]  J. Walker,et al.  Distantly related sequences in the alpha‐ and beta‐subunits of ATP synthase, myosin, kinases and other ATP‐requiring enzymes and a common nucleotide binding fold. , 1982, The EMBO journal.

[88]  M. Butler,et al.  Tyrosine Recombinase Retrotransposons and Transposons. , 2015, Microbiology spectrum.

[89]  K. Raney,et al.  Structure and Mechanisms of SF1 DNA Helicases. , 2013, Advances in experimental medicine and biology.

[90]  P. Capy,et al.  Do the integrases of LTR-retrotransposons and class II element transposases have a common ancestor? , 2004, Genetica.

[91]  Mouse Genome Sequencing Consortium Initial sequencing and comparative analysis of the mouse genome , 2002, Nature.

[92]  International Human Genome Sequencing Consortium Initial sequencing and analysis of the human genome , 2001, Nature.

[93]  N. Kurosawa,et al.  Sequence analysis of three family B DNA polymerases from the thermoacidophilic crenarchaeon Sulfurisphaera ohwakuensis. , 2000, DNA research : an international journal for rapid publication of reports on genes and genomes.