Evolution of Spliceosomal snRNA Genes in Metazoan Animals

While studies of the evolutionary histories of protein families are commonplace, little is known on noncoding RNAs beyond microRNAs and some snoRNAs. Here we investigate in detail the evolutionary history of the nine spliceosomal snRNA families (U1, U2, U4, U5, U6, U11, U12, U4atac, and U6atac) across the completely or partially sequenced genomes of metazoan animals. Representatives of the five major spliceosomal snRNAs were found in all genomes. None of the minor splicesomal snRNAs were detected in nematodes or in the shotgun traces of Oikopleura dioica, while in all other animal genomes at most one of them is missing. Although snRNAs are present in multiple copies in most genomes, distinguishable paralogue groups are not stable over long evolutionary times, although they appear independently in several clades. In general, animal snRNA secondary structures are highly conserved, albeit, in particular, U11 and U12 in insects exhibit dramatic variations. An analysis of genomic context of snRNAs reveals that they behave like mobile elements, exhibiting very little syntenic conservation.

[1]  E. Wieben,et al.  The small nuclear RNAs of Drosophila. , 1984, Journal of molecular biology.

[2]  T. Pederson,et al.  Upstream elements required for efficient transcription of a human U6 RNA gene resemble those of U1 and U2 genes even though a different polymerase is used. , 1988, Genes & development.

[3]  C. Guthrie,et al.  Evolution of small nuclear RNAs in S. cerevisiae, C. albicans, and other hemiascomycetous yeasts. , 2007, RNA.

[4]  R. J. Herrera,et al.  The silk moth Bombyx mori U1 and U2 snRNA variants are differentially expressed. , 2005, Gene.

[5]  Sean R. Eddy,et al.  Rfam: annotating non-coding RNAs in complete genomes , 2004, Nucleic Acids Res..

[6]  C. Branlant,et al.  Primary and secondary structures of chicken, rat and man nuclear U4 RNAs. Homologies with U1 and U5 RNAs. , 1981, Nucleic acids research.

[7]  J. Steitz,et al.  Three novel functional variants of human U5 small nuclear RNA , 1992, Molecular and cellular biology.

[8]  J. Manley,et al.  Protein-free spliceosomal snRNAs catalyze a reaction that resembles the first step of splicing. , 2007, RNA.

[9]  D. Gautheret,et al.  Direct RNA motif definition and identification from multiple sequence alignments using secondary structure profiles. , 2001, Journal of molecular biology.

[10]  C. Will,et al.  Splicing of a rare class of introns by the U12-dependent spliceosome , 2005, Biological chemistry.

[11]  R. Padgett,et al.  U4 small nuclear RNA can function in both the major and minor spliceosomes , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[12]  A. Weiner,et al.  Concerted evolution of the tandemly repeated genes encoding primate U2 small nuclear RNA (the RNU2 locus) does not prevent rapid diversification of the (CT)n.(GA)n microsatellite embedded within the U2 repeat unit. , 1995, Genomics.

[13]  Christian Schlötterer,et al.  Chromosomal homogeneity of Drosophila ribosomal DNA arrays suggests intrachromosomal exchanges drive concerted evolution , 1994, Current Biology.

[14]  R. J. Herrera,et al.  Multiple forms of U2 snRNA coexist in the silk moth Bombyx mori , 2002, Insect molecular biology.

[15]  Stephen M. Mount,et al.  Sequence of U1 RNA from Drosophila melanogaster: implications for U1 secondary structure and possible involvement in splicing. , 1981, Nucleic acids research.

[16]  G. Kunkel,et al.  Multiple, dispersed human U6 small nuclear RNA genes with varied transcriptional efficiencies. , 2003, Nucleic acids research.

[17]  V. Moulton,et al.  Neighbor-net: an agglomerative method for the construction of phylogenetic networks. , 2002, Molecular biology and evolution.

[18]  Colin N. Dewey,et al.  Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution , 2004, Nature.

[19]  Walter Fontana,et al.  Fast folding and comparison of RNA secondary structures , 1994 .

[20]  I. Cross,et al.  Molecular characterization and chromosomal mapping of the 5S rRNA gene in Solea senegalensis: a new linkage to the U1, U2, and U5 small nuclear RNA genes. , 2006, Genome.

[21]  J. Steitz,et al.  U12 snRNA in vertebrates: evolutionary conservation of 5' sequences implicated in splicing of pre-mRNAs containing a minor class of introns. , 1995, RNA.

[22]  A. Weiner,et al.  Concerted evolution of the tandemly repeated genes encoding human U2 snRNA (the RNU2 locus) involves rapid intrachromosomal homogenization and rare interchromosomal gene conversion , 1997, The EMBO journal.

[23]  R. J. Herrera,et al.  U6 snRNA variants isolated from the posterior silk gland of the silk moth Bombyx mori. , 2006, Insect biochemistry and molecular biology.

[24]  D. Liao,et al.  Concerted evolution: molecular mechanism and biological implications. , 1999, American journal of human genetics.

[25]  Pontus Larsson,et al.  Identification of the Major Spliceosomal RNAs in Dictyostelium discoideum Reveals Developmentally Regulated U2 Variants and Polyadenylated snRNAs , 2006, Eukaryotic Cell.

[26]  Andrea Barta,et al.  Evolutionary conservation of minor U12-type spliceosome between plants and humans. , 2005, RNA.

[27]  B. Stefanovic,et al.  Characterization of two developmentally regulated sea urchin U2 small nuclear RNA promoters: a common required TATA sequence and independent proximal and distal elements , 1992, Molecular and cellular biology.

[28]  David Penny,et al.  Searching for ncRNAs in eukaryotic genomes: Maximizing biological input with RNAmotif , 2004, J. Integr. Bioinform..

[29]  Abhijit A. Patel,et al.  Splicing double: insights from the second spliceosome , 2003, Nature Reviews Molecular Cell Biology.

[30]  Lesley J. Collins,et al.  Searching for ncRNAs in eukaryotic genomes: Maximizing biological input with RNAmotif , 2004, J. Integr. Bioinform..

[31]  J. Steitz,et al.  Additional low-abundance human small nuclear ribonucleoproteins: U11, U12, etc. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[32]  D. Hillis,et al.  Ribosomal DNA: Molecular Evolution and Phylogenetic Inference , 1991, The Quarterly Review of Biology.

[33]  A. Krol,et al.  High evolutionary conservation of the secondary structure and of certain nucleotide sequences of U5 RNA. , 1983, Nucleic acids research.

[34]  J. M. Sierra-Montes,et al.  Variants of U1 small nuclear RNA assemble into spliceosomal complexes , 2004, Insect molecular biology.

[35]  C. Ebel,et al.  Trans-splicing and cis-splicing in the colourless Euglenoid, Entosiphon sulcatum , 1999, Current Genetics.

[36]  W. Stumph,et al.  Identification of Proximal Sequence Element Nucleotides Contributing to the Differential Expression of Variant U4 Small Nuclear RNA Genes (*) , 1995, The Journal of Biological Chemistry.

[37]  Marcela Dávila López,et al.  Computational screen for spliceosomal RNA genes aids in defining the phylogenetic distribution of major and minor spliceosomal components , 2008, Nucleic acids research.

[38]  Jean L. Chang,et al.  Initial sequence of the chimpanzee genome and comparison with the human genome , 2005, Nature.

[39]  R. Sachidanandam,et al.  Comprehensive splice-site analysis using comparative genomics , 2006, Nucleic acids research.

[40]  E. Lund,et al.  The Genes and Transcription of the Major Small Nuclear RNAs , 1988 .

[41]  N. Hernandez,et al.  Small Nuclear RNA Genes: a Model System to Study Fundamental Mechanisms of Transcription* , 2001, The Journal of Biological Chemistry.

[42]  A. Weiner,et al.  Evidence for base-pairing between mammalian U2 and U6 small nuclear ribonucleoprotein particles. , 1990, Genes & development.

[43]  F. Pelliccia,et al.  5S ribosomal and U1 small nuclear RNA genes: a new linkage type in the genome of a crustacean that has three different tandemly repeated units containing 5S ribosomal DNA sequences. , 2001, Genome.

[44]  A. Russell,et al.  An early evolutionary origin for the minor spliceosome , 2006, Nature.

[45]  Jürgen Brosius,et al.  Retroposed SNOfall--a mammalian-wide comparison of platypus snoRNAs. , 2008, Genome research.

[46]  M. Kirschner,et al.  Differential expression of multiple U1 small nuclear RNAs in oocytes and embryos of Xenopus laevis , 1984, Cell.

[47]  Peter F. Stadler,et al.  Non-coding RNAs in Ciona intestinalis , 2005, ECCB/JBI.

[48]  D. Ecker,et al.  RNAMotif, an RNA secondary structure definition and search algorithm. , 2001, Nucleic acids research.

[49]  Lesley Collins,et al.  Complex spliceosomal organization ancestral to extant eukaryotes. , 2005, Molecular biology and evolution.

[50]  Valer Gotea,et al.  Spliceosomal small nuclear RNA genes in 11 insect genomes. , 2006, RNA.

[51]  R. Padgett,et al.  Conservation of functional features of U6atac and U12 snRNAs between vertebrates and higher plants. , 1999, RNA.

[52]  P. Carbon,et al.  Characterization of snRNA and snRNA-type genes in the pufferfish Fugu rubripes. , 2004, Gene.

[53]  David L. Wheeler,et al.  GenBank , 2015, Nucleic Acids Res..

[54]  Nicholas H. Putnam,et al.  The amphioxus genome and the evolution of the chordate karyotype , 2008, Nature.

[55]  P. Holland,et al.  Evolution of 28S Ribosomal DNA in Chaetognaths: Duplicate Genes and Molecular Phylogeny , 1997, Journal of Molecular Evolution.

[56]  S. Valadkhan.  The spliceosome: caught in a web of shifting interactions. , 2007, Current opinion in structural biology.

[57]  Robert Walgate,et al.  Proliferation , 1985, Nature.

[58]  R. J. Herrera,et al.  A diversity of U1 small nuclear RNAs in the silk moth Bombyx mori. , 2003, Insect biochemistry and molecular biology.

[59]  Sam Griffiths-Jones,et al.  RALEE--RNA ALignment Editor in Emacs , 2005, Bioinform..

[60]  J. Thomas,et al.  The spliceosomal snRNAs of Caenorhabditis elegans. , 1990, Nucleic acids research.

[61]  Xenopus laevis U2 snRNA genes: tandemly repeated transcription units sharing 5' and 3' flanking homology with other RNA polymerase II transcribed genes. , 1984, EMBO Journal.

[62]  P. Stadler,et al.  Secondary structure prediction for aligned RNA sequences. , 2002, Journal of molecular biology.

[63]  P. Stadler,et al.  Prediction of structured non-coding RNAs in the genomes of the nematodes Caenorhabditis elegans and Caenorhabditis briggsae. , 2006, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[64]  T. Nilsen,et al.  The spliceosomal U small nuclear RNAs of Ascaris lumbricoides. , 1994, Molecular and biochemical parasitology.

[65]  R. Zeller,et al.  Xenopus laevis U2 snRNA genes: tandemly repeated transcription units sharing 5′ and 3′ flanking homology with other RNA polymerase II transcribed genes. , 1983, The EMBO journal.

[66]  Pontus Larsson,et al.  U1-like snRNAs lacking complementarity to canonical 5' splice sites. , 2006, RNA.

[67]  B. Stefanovic,et al.  Isolation and characterization of developmentally regulated sea urchin U2 snRNA genes. , 1991, Developmental biology.

[68]  Stephen M. Mount,et al.  Drosophila melanogaster genes for U1 snRNA variants and their expression during development. , 1990, Nucleic acids research.

[69]  S. Celniker,et al.  Identification and analysis of U5 snRNA variants in Drosophila. , 2005, RNA.

[70]  J. Steitz,et al.  The divergent U12-type spliceosome is required for pre-mRNA splicing and is essential for development in Drosophila. , 2002, Molecular cell.

[71]  F. Pelliccia,et al.  Identification and characterization of U1 small nuclear RNA genes from two crustacean isopod species , 2004, Chromosome Research.

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

[73]  F. Müller,et al.  Splicing Segregation: The Minor Spliceosome Acts outside the Nucleus and Controls Cell Proliferation , 2007, Cell.

[74]  Damian Smedley,et al.  Ensembl 2005 , 2004, Nucleic Acids Res..

[75]  Andreas Prlic,et al.  Ensembl 2008 , 2007, Nucleic Acids Res..

[76]  S. Valadkhan.  snRNAs as the catalysts of pre-mRNA splicing. , 2005, Current opinion in chemical biology.

[77]  Erhard Rahm,et al.  BioFuice: Mapping-Based Data Integration in Bioinformatics , 2006, DILS.

[78]  A. Dress,et al.  A canonical decomposition theory for metrics on a finite set , 1992 .

[79]  Michel J. Weber,et al.  Mammalian Small Nucleolar RNAs Are Mobile Genetic Elements , 2006, PLoS genetics.

[80]  I. Cross,et al.  5S rDNA and U2 snRNA are linked in the genome of Crassostrea angulata and Crassostrea gigas oysters: does the (CT)n.(GA)n microsatellite stabilize this novel linkage of large tandem arrays? , 2005, Genome.

[81]  A. Weiner,et al.  Abundant pseudogenes for small nuclear RNAs are dispersed in the human genome. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[82]  T. Nilsen.  The spliceosome: the most complex macromolecular machine in the cell? , 2003, BioEssays : news and reviews in molecular, cellular and developmental biology.

[83]  Jürgen Brosius,et al.  Identification of an evolutionarily divergent U11 small nuclear ribonucleoprotein particle in Drosophila. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[84]  M. Nei,et al.  Concerted and birth-and-death evolution of multigene families. , 2005, Annual review of genetics.

[85]  Sonja J. Prohaska,et al.  Evolutionary patterns of non-coding RNAs , 2005, Theory in Biosciences.

[86]  X. Caubit,et al.  Systematics of Chaetognatha under the light of molecular data, using duplicated ribosomal 18S DNA sequences. , 2006, Molecular phylogenetics and evolution.

[87]  K. Hastings.  SL trans-splicing: easy come or easy go? , 2005, Trends in genetics : TIG.

[88]  A. Weiner,et al.  Concerted evolution of the tandem array encoding primate U2 snRNA (the RNU2 locus) is accompanied by dramatic remodeling of the junctions with flanking chromosomal sequences , 1999, The EMBO journal.

[89]  J. Sumerel,et al.  Identification of developmentally regulated sea urchin U5 snRNA genes. , 1997, DNA sequence : the journal of DNA sequencing and mapping.

[90]  International Human Genome Sequencing Consortium.  Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution , 2004 .

[91]  U. Pettersson,et al.  Genes for human U4 small nuclear RNA. , 1986, Gene.

[92]  M. Birnstiel,et al.  Structure and Function of Major and Minor Small Nuclear Ribonucleoprotein Particles , 1988, Springer Berlin Heidelberg.

[93]  J. Sylvester,et al.  Human rDNA: evolutionary patterns within the genes and tandem arrays derived from multiple chromosomes. , 2001, Genomics.

[94]  W. Stumph,et al.  Chicken U2 and U1 RNA genes are found in very different genomic environments but have similar promoter structures. , 1986, Biochemistry.

[95]  R. Padgett,et al.  Domains of human U4atac snRNA required for U12-dependent splicing in vivo. , 2002, Nucleic acids research.

[96]  Gonzalo Giribet,et al.  Arthropod phylogeny based on eight molecular loci and morphology , 2001, Nature.

[97]  D. Huson,et al.  Application of phylogenetic networks in evolutionary studies. , 2006, Molecular biology and evolution.