Genome-wide analysis of chicken snoRNAs provides unique implications for the evolution of vertebrate snoRNAs

BackgroundSmall nucleolar RNAs (snoRNAs) represent one of the largest groups of functionally diverse trans-acting non-protein-coding (npc) RNAs currently known in eukaryotic cells. Chicken snoRNAs have been very poorly characterized when compared to other vertebrate snoRNAs. A genome-wide analysis of chicken snoRNAs is therefore of great importance to further understand the functional evolution of snoRNAs in vertebrates.ResultsTwo hundred and one gene variants encoding 93 box C/D and 62 box H/ACA snoRNAs were identified in the chicken genome and are predicted to guide 86 2'-O-ribose methylations and 69 pseudouridylations of rRNAs and spliceosomal RNAs. Forty-four snoRNA clusters were grouped into four categories based on synteny characteristics of the clustered snoRNAs between chicken and human. Comparative analyses of chicken snoRNAs revealed extensive recombination and separation of guiding function, with cooperative evolution between the guiding duplexes and modification sites. The gas5-like snoRNA host gene appears to be a hotspot of snoRNA gene expansion in vertebrates. Our results suggest that the chicken is a good model for the prediction of functional snoRNAs, and that intragenic duplication and divergence might be the major driving forces responsible for expansion of novel snoRNA genes in the chicken genome.ConclusionWe have provided a detailed catalog of chicken snoRNAs that aids in understanding snoRNA gene repertoire differences between avians and other vertebrates. Our genome-wide analysis of chicken snoRNAs improves annotation of the 'darkness matter' in the npcRNA world and provides a unique perspective into snoRNA evolution in vertebrates.

[1]  Miriam K. Konkel,et al.  Genome analysis of the platypus reveals unique signatures of evolution , 2008, Nature.

[2]  Michel J. Weber,et al.  Correction: Mammalian Small Nucleolar RNAs Are Mobile Genetic Elements , 2007, PLoS Genetics.

[3]  H. Satoh,et al.  Intronic U50 small‐nucleolar‐RNA (snoRNA) host gene of no protein‐coding potential is mapped at the chromosome breakpoint t(3;6)(q27;q15) of human B‐cell lymphoma , 2000, Genes to cells : devoted to molecular & cellular mechanisms.

[4]  J. Cavaille,et al.  Imprinted small RNA genes , 2004, Biological chemistry.

[5]  Wei Yan,et al.  A PCR-based method for detection and quantification of small RNAs. , 2006, Biochemical and biophysical research communications.

[6]  P. Chomczyński,et al.  The single-step method of RNA isolation by acid guanidinium thiocyanate–phenol–chloroform extraction: twenty-something years on , 2006, Nature Protocols.

[7]  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.

[8]  Wei Yan,et al.  Cloning and expression profiling of testis-expressed microRNAs. , 2007, Developmental biology.

[9]  C. Branlant,et al.  The nuclear 5S RNAs from chicken, rat and man. U5 RNAs are encoded by multiple genes. , 1981, Nucleic acids research.

[10]  Todd M Lowe,et al.  A computational screen for mammalian pseudouridylation guide H/ACA RNAs. , 2006, RNA.

[11]  J Ofengand,et al.  Mapping to nucleotide resolution of pseudouridine residues in large subunit ribosomal RNAs from representative eukaryotes, prokaryotes, archaebacteria, mitochondria and chloroplasts. , 1997, Journal of molecular biology.

[12]  Martina Paulsen,et al.  Identification of tandemly-repeated C/D snoRNA genes at the imprinted human 14q32 domain reminiscent of those at the Prader-Willi/Angelman syndrome region. , 2002, Human molecular genetics.

[13]  R. F. Furlong Insights into vertebrate evolution from the chicken genome sequence , 2005, Genome Biology.

[14]  J. Bachellerie,et al.  Intron-encoded, antisense small nucleolar RNAs: the characterization of nine novel species points to their direct role as guides for the 2'-O-ribose methylation of rRNAs. , 1996, Journal of molecular biology.

[15]  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.

[16]  Jürgen Brosius,et al.  Evolution of small nucleolar RNAs in nematodes , 2006, Nucleic acids research.

[17]  J. Graves,et al.  Bmc Evolutionary Biology the Evolution of Imprinting: Chromosomal Mapping of Orthologues of Mammalian Imprinted Domains in Monotreme and Marsupial Mammals , 2007 .

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

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

[20]  J. Steitz,et al.  A mammalian gene with introns instead of exons generating stable RNA products , 1996, Nature.

[21]  Yuping Li,et al.  Genome-wide analyses of retrogenes derived from the human box H/ACA snoRNAs , 2006, Nucleic acids research.

[22]  Kevin R. Thornton,et al.  The origin of new genes: glimpses from the young and old , 2003, Nature Reviews Genetics.

[23]  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.

[24]  X. Darzacq,et al.  A Cajal body-specific pseudouridylation guide RNA is composed of two box H/ACA snoRNA-like domains. , 2002, Nucleic acids research.

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

[26]  W. Filipowicz,et al.  The Host Gene for Intronic U17 Small Nucleolar RNAs in Mammals Has No Protein-Coding Potential and Is a Member of the 5′-Terminal Oligopyrimidine Gene Family , 1998, Molecular and Cellular Biology.

[27]  D. Haig,et al.  What good is genomic imprinting: the function of parent-specific gene expression , 2003, Nature Reviews Genetics.

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

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

[30]  E. Bertrand,et al.  Human Box H/ACA Pseudouridylation Guide RNA Machinery , 2004, Molecular and Cellular Biology.

[31]  F. Amaldi,et al.  TOP genes: a translationally controlled class of genes including those coding for ribosomal proteins. , 1997, Progress in molecular and subcellular biology.

[32]  Chong-Jian Chen,et al.  A combined computational and experimental analysis of two families of snoRNA genes from Caenorhabditis elegans, revealing the expression and evolution pattern of snoRNAs in nematodes. , 2007, Genomics.

[33]  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.

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

[35]  Liang-Hu Qu,et al.  Genome-wide analyses of two families of snoRNA genes from Drosophila melanogaster, demonstrating the extensive utilization of introns for coding of snoRNAs. , 2005, RNA.

[36]  M. Bortolin,et al.  Human U19 intron-encoded snoRNA is processed from a long primary transcript that possesses little potential for protein coding. , 1998, RNA.

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

[38]  Sam Griffiths-Jones,et al.  Annotating noncoding RNA genes. , 2007, Annual review of genomics and human genetics.

[39]  Liang-Hu Qu,et al.  A novel experimental approach for systematic identification of box H/ACA snoRNAs from eukaryotes , 2005, Nucleic acids research.

[40]  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.

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

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

[43]  Tamás Kiss,et al.  Site-Specific Pseudouridine Formation in Preribosomal RNA Is Guided by Small Nucleolar RNAs , 1997, Cell.

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

[45]  John W. S. Brown,et al.  Intronic noncoding RNAs and splicing. , 2008, Trends in plant science.

[46]  J. Steitz,et al.  Sno Storm in the Nucleolus: New Roles for Myriad Small RNPs , 1997, Cell.