Plant U13 orthologues and orphan snoRNAs identified by RNomics of RNA from Arabidopsis nucleoli

Small nucleolar RNAs (snoRNAs) and small Cajal body-specific RNAs (scaRNAs) are non-coding RNAs whose main function in eukaryotes is to guide the modification of nucleotides in ribosomal and spliceosomal small nuclear RNAs, respectively. Full-length sequences of Arabidopsis snoRNAs and scaRNAs have been obtained from cDNA libraries of capped and uncapped small RNAs using RNA from isolated nucleoli from Arabidopsis cell cultures. We have identified 31 novel snoRNA genes (9 box C/D and 22 box H/ACA) and 15 new variants of previously described snoRNAs. Three related capped snoRNAs with a distinct gene organization and structure were identified as orthologues of animal U13snoRNAs. In addition, eight of the novel genes had no complementarity to rRNAs or snRNAs and are therefore putative orphan snoRNAs potentially reflecting wider functions for these RNAs. The nucleolar localization of a number of the snoRNAs and the localization to nuclear bodies of two putative scaRNAs was confirmed by in situ hybridization. The majority of the novel snoRNA genes were found in new gene clusters or as part of previously described clusters. These results expand the repertoire of Arabidopsis snoRNAs to 188 snoRNA genes with 294 gene variants.

[1]  T. Kiss,et al.  A small nucleolar guide RNA functions both in 2′‐O‐ribose methylation and pseudouridylation of the U5 spliceosomal RNA , 2001, The EMBO journal.

[2]  Sang Hyon Kim,et al.  Aberrant mRNA Transcripts and the Nonsense-Mediated Decay Proteins UPF2 and UPF3 Are Enriched in the Arabidopsis Nucleolus[W][OA] , 2009, The Plant Cell Online.

[3]  D. Tollervey,et al.  Ribosome synthesis in Saccharomyces cerevisiae. , 1999, Annual review of genetics.

[4]  Jürgen Brosius,et al.  Experimental RNomics Identification of 140 Candidates for Small Non-Messenger RNAs in the Plant Arabidopsis thaliana , 2002, Current Biology.

[5]  P J Shaw,et al.  Localization and processing from a polycistronic precursor of novel snoRNAs in maize. , 1998, Journal of cell science.

[6]  Edouard Bertrand,et al.  ADAR2-mediated editing of RNA substrates in the nucleolus is inhibited by C/D small nucleolar RNAs , 2005, The Journal of cell biology.

[7]  J. Steitz,et al.  Guide RNAs with 5′ Caps and Novel Box C/D snoRNA-like Domains for Modification of snRNAs in Metazoa , 2004, Current Biology.

[8]  Hui Zhou,et al.  Genomewide Analysis of Box C/D and Box H/ACA snoRNAs in Chlamydomonas reinhardtii Reveals an Extensive Organization Into Intronic Gene Clusters , 2008, Genetics.

[9]  W. Filipowicz,et al.  Alteration of the RNA polymerase specificity of U3 snRNA genes during evolution and in vitro , 1991, Cell.

[10]  Sang Hyon Kim,et al.  Dynamic Behavior of Arabidopsis eIF4A-III, Putative Core Protein of Exon Junction Complex: Fast Relocation to Nucleolus and Splicing Speckles under Hypoxia[W] , 2009, The Plant Cell Online.

[11]  A. Hüttenhofer,et al.  A Novel Brain-specific Box C/D Small Nucleolar RNA Processed from Tandemly Repeated Introns of a Noncoding RNA Gene in Rats* , 2001, The Journal of Biological Chemistry.

[12]  S. Stamm,et al.  The snoRNA HBII-52 Regulates Alternative Splicing of the Serotonin Receptor 2C , 2006, Science.

[13]  A. Hüttenhofer,et al.  The expanding snoRNA world. , 2002, Biochimie.

[14]  A. Marchfelder,et al.  Processing of a Dicistronic tRNA-snoRNA Precursor: Combined Analysis in Vitro and in Vivo Reveals Alternate Pathways and Coupling to Assembly of snoRNP1 , 2009, Plant Physiology.

[15]  Manuel Echeverria,et al.  Plant snoRNAs: functional evolution and new modes of gene expression. , 2003, Trends in plant science.

[16]  P J Shaw,et al.  Clusters of multiple different small nucleolar RNA genes in plants are expressed as and processed from polycistronic pre‐snoRNAs , 1997, The EMBO journal.

[17]  Liang-Hu Qu,et al.  snoSeeker: an advanced computational package for screening of guide and orphan snoRNA genes in the human genome , 2006, Nucleic acids research.

[18]  J. Bachellerie,et al.  Antisense snoRNAs: a family of nucleolar RNAs with long complementarities to rRNA. , 1995, Trends in biochemical sciences.

[19]  A. Hüttenhofer,et al.  RNomics: an experimental approach that identifies 201 candidates for novel, small, non‐messenger RNAs in mouse , 2001, The EMBO journal.

[20]  J. Mattick,et al.  Small RNAs derived from snoRNAs. , 2009, RNA.

[21]  Benedict C. Arnold,et al.  Systematic Spatial Analysis of Gene Expression during Wheat Caryopsis Developmentw⃞ , 2005, The Plant Cell Online.

[22]  Laurent Lestrade,et al.  snoRNA-LBME-db, a comprehensive database of human H/ACA and C/D box snoRNAs , 2005, Nucleic Acids Res..

[23]  A. Hüttenhofer,et al.  Identification of brain-specific and imprinted small nucleolar RNA genes exhibiting an unusual genomic organization. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[24]  N. Rajewsky,et al.  A human snoRNA with microRNA-like functions. , 2008, Molecular cell.

[25]  M. Fournier,et al.  Mis-targeted methylation in rRNA can severely impair ribosome synthesis and activity , 2008, RNA biology.

[26]  M. Mann,et al.  Proteomic analysis of the Arabidopsis nucleolus suggests novel nucleolar functions. , 2004, Molecular biology of the cell.

[27]  T. Kiss Small Nucleolar RNAs An Abundant Group of Noncoding RNAs with Diverse Cellular Functions , 2002, Cell.

[28]  J. Bachellerie,et al.  Processing of mammalian rRNA precursors at the 3' end of 18S rRNA. Identification of cis-acting signals suggests the involvement of U13 small nucleolar RNA. , 1996, European journal of biochemistry.

[29]  Tamás Kiss,et al.  A common sequence motif determines the Cajal body‐specific localization of box H/ACA scaRNAs , 2003, The EMBO journal.

[30]  C Gaspin,et al.  Identification of 66 box C/D snoRNAs in Arabidopsis thaliana: extensive gene duplications generated multiple isoforms predicting new ribosomal RNA 2'-O-methylation sites. , 2001, Journal of molecular biology.

[31]  R. Terns,et al.  Non-coding RNAs: lessons from the small nuclear and small nucleolar RNAs , 2007, Nature Reviews Molecular Cell Biology.

[32]  Peter F. Stadler,et al.  SnoReport: computational identification of snoRNAs with unknown targets , 2008, Bioinform..

[33]  Paul D. Shaw,et al.  Plant snoRNA database , 2003, Nucleic Acids Res..

[34]  Meng Qing,et al.  Identification of 10 novel snoRNA gene clusters from Arabidopsis thaliana , 2001 .

[35]  E. Bertrand,et al.  A Dynamic Scaffold of Pre-snoRNP Factors Facilitates Human Box C/D snoRNP Assembly , 2007, Molecular and Cellular Biology.

[36]  A. Marchfelder,et al.  Plant dicistronic tRNA–snoRNA genes: a new mode of expression of the small nucleolar RNAs processed by RNase Z , 2003, The EMBO journal.

[37]  Valery Shepelev,et al.  snoTARGET shows that human orphan snoRNA targets locate close to alternative splice junctions. , 2008, Gene.

[38]  T. Lowe,et al.  Multiple snoRNA gene clusters from Arabidopsis. , 2001, RNA.

[39]  Geoffrey J. Barton,et al.  Jalview Version 2—a multiple sequence alignment editor and analysis workbench , 2009, Bioinform..

[40]  M. Fournier,et al.  Interference probing of rRNA with snoRNPs: a novel approach for functional mapping of RNA in vivo. , 2004, RNA.

[41]  Liang-Hu Qu,et al.  The high diversity of snoRNAs in plants: identification and comparative study of 120 snoRNA genes from Oryza sativa. , 2003, Nucleic acids research.

[42]  Wayne A. Decatur,et al.  rRNA modifications and ribosome function. , 2002, Trends in biochemical sciences.

[43]  Michael Zuker,et al.  Mfold web server for nucleic acid folding and hybridization prediction , 2003, Nucleic Acids Res..

[44]  Gwenael Badis,et al.  A snoRNA that guides the two most conserved pseudouridine modifications within rRNA confers a growth advantage in yeast. , 2003, RNA.

[45]  L. Qu,et al.  Identification of 10 novel snoRNA gene clusters from Arabidopsis thaliana. , 2001, Nucleic acids research.

[46]  Ashesh A. Saraiya,et al.  snoRNA, a Novel Precursor of microRNA in Giardia lamblia , 2008, PLoS pathogens.

[47]  M. Fournier,et al.  Ribosome structure and activity are altered in cells lacking snoRNPs that form pseudouridines in the peptidyl transferase center. , 2003, Molecular cell.

[48]  W. Filipowicz,et al.  Biogenesis of small nucleolar ribonucleoproteins. , 2002, Current opinion in cell biology.

[49]  Tamás Kiss,et al.  Cajal body‐specific small nuclear RNAs: a novel class of 2′‐O‐methylation and pseudouridylation guide RNAs , 2002, The EMBO journal.

[50]  Shu-Hsing Wu,et al.  Mining small RNA sequencing data: a new approach to identify small nucleolar RNAs in Arabidopsis , 2009, Nucleic acids research.

[51]  R. Lührmann,et al.  Conserved Stem II of the Box C/D Motif Is Essential for Nucleolar Localization and Is Required, Along with the 15.5K Protein, for the Hierarchical Assembly of the Box C/D snoRNP , 2002, Molecular and Cellular Biology.

[52]  Zoran Radić,et al.  Structural insights into ligand interactions at the acetylcholinesterase peripheral anionic site , 2003, The EMBO journal.