Skip to main content
SpringerLink
Log in

Nematode sbRNAs: Homologs of Vertebrate Y RNAs

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

Stem-bulge RNAs (sbRNAs) are a group of small, functionally yet uncharacterized noncoding RNAs first described in C. elegans, with a few homologous sequences postulated in C. briggsae. In this study, we report on a comprehensive survey of this ncRNA family in the phylum Nematoda. Employing homology search strategies based on both sequence and secondary structure models and a computational promoter screen we identified a total of 240 new sbRNA homologs. For the majority of these loci we identified both promoter regions and transcription termination signals characteristic for pol-III transcripts. Sequence and structure comparison with known RNA families revealed that sbRNAs are homologs of vertebrate Y RNAs. Most of the sbRNAs show the characteristic Ro protein binding motif, and contain a region highly similar to a functionally required motif for DNA replication previously thought to be unique to vertebrate Y RNAs. The single Y RNA that was previously described in C. elegans, however, does not show this motif, and in general bears the hallmarks of a highly derived family member.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abad P, Gouzy J, Aury JM, Castagnone-Sereno P, Danchin EG, Deleury E, Perfus-Barbeoch L, Anthouard V, Artiguenave F, Blok VC, Caillaud MC, Coutinho PM, Dasilva C, De Luca F, Deau F, Esquibet M, Flutre T, Goldstone JV, Hamamouch N, Hewezi T, Jaillon O, Jubin C, Leonetti P, Magliano M, Maier TR, Markov GV, McVeigh P, Pesole G, Poulain J, Robinson-Rechavi M, Sallet E, Ségurens B, Steinbach D, Tytgat T, Ugarte E, van Ghelder C, Veronico P, Baum TJ, Blaxter M, Bleve-Zacheo T, Davis EL, Ewbank JJ, Favery B, Grenier E, Henrissat B, Jones JT, Laudet V, Maule AG, Quesneville H, Rosso MN, Schiex T, Smant G, Weissenbach J, Wincker P (2008) Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nat Biotechnol 26:909–915

    Article  CAS  PubMed  Google Scholar 

  • Aerts S, Van Loo P, Thijs G, Moreau Y, De Moor B (2003) Computational detection of cis-regulatory modules. Bioinformatics 19:5–14

    Article  Google Scholar 

  • Aftab MN, He H, Skogerbø G, Chen R (2008) Microarray analysis of ncRNA expression patterns in Caenorhabditis elegans after RNAi against snoRNA associated proteins. BMC Genom 9:278–278

    Article  Google Scholar 

  • Barrière A, Yang SP, Pekarek E, Thomas CG, Haag ES, Ruvinsky I (2009) Detecting heterozygosity in shotgun genome assemblies: lessons from obligately outcrossing nematodes. Genome Res 19:470–480

    Article  PubMed  Google Scholar 

  • Bernhart SH, Hofacker IL, Will S, Gruber AR, Stadler PF (2008) RNAalifold: improved consensus structure prediction for RNA alignments. BMC Bioinform 9:474–474

    Article  PubMed  Google Scholar 

  • Blaxter ML, De Ley P, Garey JR, Liu LX, Scheldeman P, Vierstraete A, Vanfleteren JR, Mackey LY, Dorris M, Frisse LM, Vida JT, Thomas WK (1998) A molecular evolutionary framework for the phylum Nematoda. Nature 392:71–75

    Article  CAS  PubMed  Google Scholar 

  • Chen X, Wurtmann EJ, Van Batavia J, Zybailov B, Washburn MP, Wolin SL (2007) An ortholog of the Ro autoantigen functions in 23s rRNA maturation in D. radiodurans. Genes Dev 21:1328–1339

    Article  CAS  PubMed  Google Scholar 

  • Chilton NB, Huby-Chilton F, Gasser RB, Beveridge I (2006) The evolutionary origins of nematodes within the order Strongylida are related to predilection sites within hosts. Mol Phylogenet Evol 40:118–128

    Article  CAS  PubMed  Google Scholar 

  • Christov CP, Gardiner TJ, Szüts D, Krude T (2006) Functional requirement of noncoding Y RNAs for human chromosomal DNA replication. Mol Cell Biol 26:6993–7004

    Article  CAS  PubMed  Google Scholar 

  • Christov CP, Trivier E, Krude T (2008) Noncoding human Y RNAs are overexpressed in tumours and required for cell proliferation. Br J Cancer 98:981–988

    Article  CAS  PubMed  Google Scholar 

  • Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14:1188–1190

    Article  CAS  PubMed  Google Scholar 

  • Dávila López M, Rosenblad MA, Samuelsson T (2008) Computational screen for spliceosomal RNA genes aids in defining the phylogenetic distribution of major and minor spliceosomal components. Nucleic Acids Res 36:3001–3010

    Article  PubMed  Google Scholar 

  • Deng W, Zhu X, Skogerbø G, Zhao Y, Fu Z, Wang Y, He H, Cai L, Sun H, Liu C, Li B, Bai B, Wang J, Jia D, Sun S, He H, Cui Y, Wang Y, Bu D, Chen R (2006) Organization of the Caenorhabditis elegans small non-coding transcriptome: genomic features, biogenesis, and expression. Genome Res 16:20–29

    Article  CAS  PubMed  Google Scholar 

  • Gardiner TJ, Christov CP, Langley AR, Krude T (2009) A conserved motif of vertebrate Y RNAs essential for chromosomal DNA replication. RNA 15:1375–1385

    Article  CAS  PubMed  Google Scholar 

  • Green CD, Long KS, Shi H, Wolin SL (1998) Binding of the 60-kDa Ro autoantigen to Y RNAs: evidence for recognition in the major groove of a conserved helix. RNA 4:750–765

    Article  CAS  PubMed  Google Scholar 

  • Griffiths-Jones S (2005) RALEE–RNA alignment editor in emacs. Bioinformatics 21:257–259

    Article  CAS  PubMed  Google Scholar 

  • Gruber AR, Kilgus C, Mosig A, Hofacker IL, Hennig W, Stadler PF (2008) Arthropod 7SK RNA. Mol Biol Evol 25:1923–1930

    Article  CAS  PubMed  Google Scholar 

  • Guffanti E, Corradini R, Ottonello S, Dieci G (2004) Functional dissection of RNA polymerase III termination using a peptide nucleic acid as a transcriptional roadblock. J Biol Chem 279:20708–20716

    Article  CAS  PubMed  Google Scholar 

  • Gunnery S, Ma Y, Mathews MB (1999) Termination sequence requirements vary among genes transcribed by RNA polymerase III. J Mol Biol 286:745–757

    Article  CAS  PubMed  Google Scholar 

  • Hernandez N (2001) Small nuclear RNA genes: a model system to study fundamental mechanisms of transcription. J Biol Chem 276:26733–26736

    Article  CAS  PubMed  Google Scholar 

  • Hertel J, Hofacker IL, Stadler PF (2008) SnoReport: computational identification of snoRNAs with unknown targets. Bioinformatics 24:158–164

    Article  CAS  PubMed  Google Scholar 

  • Hertel J, de Jong D, Marz M, Rose D, Tafer H, Tanzer A, Schierwater B, Stadler PF (2009) Non-coding RNA annotation of the genome of Trichoplax adhaerens. Nucleic Acids Res 37:1602–1615

    Article  CAS  PubMed  Google Scholar 

  • Hofacker IL, Fekete M, Stadler PF (2002) Secondary structure prediction for aligned RNA sequences. J Mol Biol 319:1059–1066

    Article  CAS  PubMed  Google Scholar 

  • Hogg RJ, Collins K (2008) Structured non-coding RNAs and the RNP Renaissance. Curr Opin Chem Biol 12:684–689

    Article  CAS  PubMed  Google Scholar 

  • Kaczkowski B, Torarinsson E, Reiche K, Havgaard JH, Stadler PF, Gorodkin J (2009) Structural profiles of miRNA families from pairwise clustering. Bioinformatics 25:291–294

    Article  CAS  PubMed  Google Scholar 

  • Kamath RS, Fraser AG, Dong Y, Poulin G, Durbin R, Gotta M, Kanapin A, Le Bot N, Moreno S, Sohrmann M, Welchman DP, Zipperlen P, Ahringer J (2003) Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421:231–237

    Article  CAS  PubMed  Google Scholar 

  • Kel AE, Gössling E, Reuter I, Cheremushkin E, Kel-Margoulis OV, Wingender E (2003) MATCH: a tool for searching transcription factor binding sites in DNA sequences. Nucleic Acids Res 31:3576–3579

    Article  CAS  PubMed  Google Scholar 

  • Li T, He H, Wang Y, Zheng H, Skogerbø G, Chen R (2008) In vivo analysis of Caenorhabditis elegans noncoding RNA promoter motifs. BMC Mol Biol 9:71–71

    Article  CAS  PubMed  Google Scholar 

  • Marz M, Kirsten T, Stadler PF (2008) Evolution of spliceosomal snRNA genes in metazoan animals. J Mol Evol 67:594–607

    Article  CAS  PubMed  Google Scholar 

  • Missal K, Zhu X, Rose D, Deng W, Skogerbø G, Chen R, Stadler PF (2006) Prediction of structured non-coding RNAs in the genomes of the nematodes Caenorhabditis elegans and Caenorhabditis briggsae. J Exp Zool B Mol Dev Evol 306:379–392

    Article  Google Scholar 

  • Mitreva M, Blaxter ML, Bird DM, McCarter JP (2005) Comparative genomics of nematodes. Trends Genet 21:573–581

    Article  CAS  PubMed  Google Scholar 

  • Mosig A, Guofeng M, Stadler BM, Stadler PF (2007a) Evolution of the vertebrate Y RNA cluster. Theory Biosci 126:9–14

    Article  CAS  PubMed  Google Scholar 

  • Mosig A, Chen JL, Stadler PF (2007b) Homology search with fragmented nucleic acid sequence patterns. In: Giancarlo R, Hannenhalli S (eds) Algorithms in bioinformatics (WABI 2007), Volume 4645 of Lecture Notes in Computer Science. Springer Verlag, Berlin, Heidelberg, pp 335–345

    Google Scholar 

  • Pagano A, Castelnuovo M, Tortelli F, Ferrari R, Dieci G, Cancedda R (2007) New small nuclear RNA gene-like transcriptional units as sources of regulatory transcripts. PLoS Genet 3:e1

    Article  PubMed  Google Scholar 

  • Ploner A, Ploner C, Lukasser M, Niederegger H, Hüttenhofer A (2009) Methodological obstacles in knocking down small noncoding RNAs. RNA 15:1797–1804

    Article  CAS  PubMed  Google Scholar 

  • Perreault J, Perreault JP, Boire G (2007) Ro-associated Y RNAs in metazoans: evolution and diversification. Mol Biol Evol 24:1678–1689

    Article  CAS  PubMed  Google Scholar 

  • Sönnichsen B, Koski LB, Walsh A, Marschall P, Neumann B, Brehm M, Alleaume AM, Artelt J, Bettencourt P, Cassin E, Hewitson M, Holz C, Khan M, Lazik S, Martin C, Nitzsche B, Ruer M, Stamford J, Winzi M, Heinkel R, Röder M, Finell J, Häntsch H, Jones SJ, Jones M, Piano F, Gunsalus KC, Oegema K, Gönczy P, Coulson A, Hyman AA, Echeverri CJ (2005) Full-genome RNAi profiling of early embryogenesis in Caenorhabditis elegans. Nature 434:462–469

    Article  PubMed  Google Scholar 

  • Stein AJ, Fuchs G, Fu C, Wolin SL, Reinisch KM (2005) Structural insights into RNA quality control: the Ro autoantigen binds misfolded RNAs via its central cavity. Cell 121:529–539

    Article  CAS  PubMed  Google Scholar 

  • Sudhaus W, Kiontke K (2007) Comparison of the cryptic nematode species Caenorhabditis brenneri sp. n. and C. remanei (Nematoda: Rhabditidae) with the stem species pattern of the Caenorhabditis elegans group. Zootaxa 1456:45–62

    Google Scholar 

  • Tanzer A, Stadler PF (2004) Molecular evolution of a microRNA cluster. J Mol Biol 339:327–335

    Article  CAS  PubMed  Google Scholar 

  • Tanzer A, Stadler PF (2006) Evolution of MicroRNAs. In: Ying SY (ed) MicroRNA protocols. Humana Press, Totowa, NJ, pp 335–350

    Google Scholar 

  • Thomas J, Lea K, Zucker-Aprison E, Blumenthal T (1990) The spliceosomal snRNAs of Caenorhabditis elegans. Nucleic Acids Res 18:2633–2642

    Article  CAS  PubMed  Google Scholar 

  • Van Horn DJ, Eisenberg D, O’Brien CA, Wolin SL (1995) Caenorhabditis elegans embryos contain only one major species of Ro RNP. RNA 1:293–303

    PubMed  Google Scholar 

  • Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ (2009) Jalview Version 2—a multiple sequence alignment editor and analysis workbench. Bioinformatics 25:1189–1191

    Article  CAS  PubMed  Google Scholar 

  • Will S, Reiche K, Hofacker IL, Stadler PF, Backofen R (2007) Inferring noncoding RNA families and classes by means of genome-scale structure-based clustering. PLoS Comput Biol 3:e65

    Article  PubMed  Google Scholar 

  • Zemann A, op de Bekke A, Kiefmann M, Brosius J, Schmitz J (2006) Evolution of small nucleolar RNAs in nematodes. Nucleic Acids Res 34:2676–2685

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research originated from an RNA Bioinformatics course at the University of Vienna in the fall semester 2008. Subsequently, it was then funded in part by the Austrian GEN-AU projects “Bioinformatics Integration Network III” and “Noncoding RNA”, the AMS Vienna and the DFG under the auspices of the SPPs 1174 “Deep Metazoan Phylogeny” and 1258 “Sensory and Regulatory RNAs”.

Author information

Authors and Affiliations

  1. Department of Medical Sciences and Interdisciplinary Research Centre for Autoimmune Diseases, Università del Piemonte Orientale, via Solaroli 17, 28100, Novara, Italy

    Ilenia Boria

  2. Institute for Theoretical Chemistry, University of Vienna, Währingerstraße 17, 1090, Wien, Austria

    Ilenia Boria, Andreas R. Gruber, Andrea Tanzer, Stephan H. Bernhart, Ronny Lorenz, Ivo L. Hofacker & Peter F. Stadler

  3. Bioinformatics Group, Department of Computer Science; and Interdisciplinary Center for Bioinformatics, University of Leipzig, Härtelstraße 16-18, 04107, Leipzig, Germany

    Andreas R. Gruber, Andrea Tanzer & Peter F. Stadler

  4. Department of Chromosome Biology, Max F. Perutz Laboratories, University of Vienna, 1030, Vienna, Austria

    Michael M. Mueller

  5. Max-Planck Institute for Mathematics in the Sciences, Inselstraße 22, 04103, Leipzig, Germany

    Peter F. Stadler

  6. Fraunhofer Institut für Zelltherapie und Immunologie (IZI), Perlickstraße 1, 04103, Leipzig, Germany

    Peter F. Stadler

  7. Santa Fe Institute, 1399 Hyde Park Rd., Santa Fe, NM, 87501, USA

    Peter F. Stadler

Authors
  1. Ilenia Boria
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andreas R. Gruber
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Andrea Tanzer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Stephan H. Bernhart
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ronny Lorenz
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Michael M. Mueller
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ivo L. Hofacker
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Peter F. Stadler
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Peter F. Stadler.

Additional information

I. Boria, A. R. Gruber, and A. Tanzer contributed equally to this work.

Electronic supplementary material

An Electronic Supplement located at http://www.bioinf.uni-leipzig.de/Publications/SUPPLEMENTS/09-020/ compiles a list of detected sbRNAs, sequence data, and alignments in machine-readable form.

239_2010_9332_MOESM1_ESM.pdf

Structure evolution of sbRNA loop regions. Gene duplication coincides with duplication of substructures within the loops regions as shown here for members ofthe long sbRNAs residing on C. elegans chromosome V. The ancestral gene of this family possibly consisted of four hairpins. During subsequent gene duplications,individual hairpins were lost. The hairpin B (yellow) shows high sequence similarity to the adjacent hairpin A (green) and probably arose by local duplication of astructural element. A,B,C,D: RNA secondary structures of representatives of each family. family ABCD: Cn4 (A); family AB_D: CeN73_1 (B); family A_CD: Cn8(C); family _BCD: Cr26 (D). (E) hand curated CLUSTAL W multiple sequence alignments including the consensus structure and location of structural motifs. PDF (188 KB)

EPS (624 KB)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Boria, I., Gruber, A.R., Tanzer, A. et al. Nematode sbRNAs: Homologs of Vertebrate Y RNAs. J Mol Evol 70, 346–358 (2010). https://doi.org/10.1007/s00239-010-9332-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-010-9332-4

Keywords

Search

Navigation