Abstract
By constructing and screening theSchizosaccharomyces pombe nuclear cDNA library, a novel small nucleolar RNAs (snoRNA) was identified. The novel snoRNA displays structural features typical of C/D box snoRNA family and possesses a 10-nt-long rRNA antisense element which is predicted to guide the 2′-O-methylation of the fission yeast 25S rRNA at G940. As expected, the rRNA ribose-methylation site predicted by the novel snoRNA was precisely mapped by a deoxynucleoside triphosphate concentrationdependent primer extension assay. The comparison of functional element of guide snoRNAs among eukaryotes reveals that the novel snoRNA is a partial counterpart of the budding yeast snR60 and was termed snR60-II. snR60-II gene nested in the intron of a non-coding RNA gene with an unknown function, which is the first example of a yeast snoRNA encoded in an intron of a non-coding RNA gene. Furthermore, a number of yeast snR60 homologues were also identified from other fungi and fly. Our results reveal that snR60 exhibits diverse genomic organization in eukaryotes, implying the high mobility of snR60 gene in the course of evolution.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Eichler, D. C., Craig, N., Processing of eukaryotic ribosomal RNA, Prog. Nucl. Acid Res. Mol. Biol., 1994, 49: 197–239.
Venema, J., Tollervey, D., Ribosome synthesis inSaccharomyces cerevisiae, Annu. Rev. Genet, 1999, 33: 261–311.
Maxwell, E. S., Fournier, M. J., The small nucleolar RNAs, Annu. Rev. Biochem., 1995, 35: 897–934.
Balakin, A. G., Smith, L., Fournier, M. J., The RNA world of the nucleolus: Two major families of small RNAs defined by different box elements with related functions, Cell, 1996, 86: 823–834.
Kiss-Laszlo, Z., Henry, Y., Bachellerie, J. P. et al., Site-specific ribose methylation of preribosomal RNA: A novel function for small nucleolar RNAs, Cell, 1996, 85: 1077–1088.
Ganot, P., Bortolin, M. L., Kiss, T., Site-specific pseudouridine formation in eukaryotic pre-rRNAs is guided by small nucleolar RNAs, Cell, 1997, 89: 799–809.
Ni, J., Tien, A. L., Fournier, M. J., Small nucleolar RNAs direct site-specific synthesis of pseudouridine in ribosomal RNA, Cell, 1997, 89: 565–573.
Bachellerie, J. P., Cavaillé, J., Hüttenhofer, A., The expanding snoRNA world, Biochimie, 2002, 84: 775–790.
Barneche, F., Gaspin, C., Guyot, R. et al., Identification of 66 box C/D snoRNAs inArabidopsis thaliana: Extensive gene duplications generated multiple isoforms predicting new ribosomal RNA 2′-O-methyltion sites, J. Mol. Biol., 2001, 311: 57–73.
Brown, J. W. S., Clark, G.P., Leader, D. J. et al., Multiple snoRNA gene clusters fromArabidopsis, RNA, 2001, 7: 1817–1832.
Chen, C. L., Liang, D., Zhou, H. et al., The high diversity of snoRNAs in plants: Identification and comparative study of 120 snoRNA genes fromOryza sativa, Nucleic Acids Res., 2003, 31: 2601–2613.
Qu, L. H., Meng, Q., Zhou, H. et al., Identification of 10 novel snoRNA gene clusters fromArabidopsis thaliana, Nucleic Acids Res., 2001, 29: 1623–1630.
Lowe, T. M., Eddy, S. R., A computational screen for methylation guide snoRNAs in yeast, Science, 1999, 283: 1168–1171.
Yuan, G., Klambt, C., Bachellerie, J. P. et al., RNomics in Drosophila melanogaster: Identification of 66 candidates for novel non-messenger RNAs, Nucleic Acids Res., 2003, 3: 2495–2507.
Huttenhofer, A., Kiefmann, M., Meier-Ewert, S. et al., RNomics: An experimental approach that identifies 201 candidates for novel, small, non-messenger RNAs in mouse, EMBO J., 2001, 20: 2943–2953.
Marker, C., Zemann, A., Terhörst, T. et al., Experimental RNomics: Identification of 140 candidates for small non-messenger RNAs in the plantArabidopsis thaliana, Curr. Biol., 2002, 12: 2002–2013.
Omer, A. D., Lowe, T. M., Russell, A. G. et al., Homologs of small nucleolar RNAs in Archaea, Science, 2000, 288: 517–522.
Gaspin, C., Cavaille, J., Erauso, G.et al., Archael homologs of eukaryotic methylation guide small nucleolar RNA: Lessons from Pyrococcus genomes, J. Mol. Biol., 2000, 297: 895–906.
Tang, T. H., Bachellerie, J. P., Rozhdestvensky, T. et al., Identification of 86 candidates for small non-messenger RNAs from the archaeon Archaeoglobus fulgidus, Proc. Natl. Acad. Sci. USA, 2002, 99: 7536–7541.
Filipowicz, W., Imprinted expression of small nucleolar RNAs in brain: time for RNomics, Proc. Natl. Acad. Sci. USA, 2000, 97: 14035–14037.
Cavaille, J., Buiting, K., Kiefmann, M. et al., Identification of brain-specific and imprinted small nucleolar RNA genes exhibiting an unusual genomic organization, Proc. Natl. Acad. Sci. USA, 2000, 97: 14311–14316.
Darzacq, X., Jady, B. E., Verheggen, C. et al., Cajal body-specific small nuclear RNAs: A novel class of 2′-O-methylation and pseudouridylation guide RNAs, EMBO J., 2002, 21, 2746–2756.
Dove, J. E., Brockenbrough, J. S., Aris, J. P., Isolation of nuclei and nucleoli from the yeastSaccharomyces cerevisiae, Methods Cell Biol., 1998, 53: 33–46.
Chomczynski, P., Sacchi, N., Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction, Anal. Biochem., 1987, 16: 156–159.
Zhou, H., Yue, Q., Du, Y. P. et al., Identification and characterization of Z15 snoRNA fromSchizosaccharomyces pombe, ACTA Scientiarum Naturalium Universitatis Sunyatseni, 2000, 39: 56–60.
Smith, C. M., Steitz, J. A., Classification of gas5 as a multi-small-nucleolar-RNA (snoRNA) host gene and a member of the 5′-terminal oligopyrimidine gene family reveals common features of snoRNA host genes, Mol. Cell Biol., 1998, 18: 6897–6909.
Coccia, E. M., Cicala, C., Charlesworth, A. et al., Regulation and expression of a growth arrest-specific gene (gas5) during growth, differentiation, and development, Mol. Cell Biol., 1992, 12: 3514–3521.
Liang, D., Zhou, H., Zhang, P. et al., A novel gene organization: intronic snoRNA gene clusters fromOryza Sativa, Nucleic Acid Res., 2002, 30: 3262–3272.
Bachellerie, J. P., Cavaille, J., Qu, L. H., Nucleotide modifications in eukaryotic rRNAs: The world of small nucleolar RNA guides revisited, The Ribosome Structure, Function, Antibiotics, and Cellular Interactions (eds. Garrett, R. A., Douthwaite, S. R., Liljas, A. et al.), Washington. D.C.: American Society of Microbiology Press, 2000, 191–203.
Qu, L. H., Henras, A., Lu, Y.J. et al., Seven novel methylation guide small nucleolar RNAs are processed from a common polycistronic transcript by Ratlp and RNase III in yeast, Mol. Cell Biol., 1999, 19: 1144–1158.
Author information
Authors and Affiliations
Corresponding author
About this article
Cite this article
Luo, Y., Zhuo, H., Li, S. et al. Identification and functional analysis of a novel box C/D snoRNA fromSchizosaccharomyces pombe . Chin. Sci. Bull. 49, 1929–1936 (2004). https://doi.org/10.1007/BF03184284
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF03184284