Chinese Science Bulletin

, Volume 51, Issue 20, pp 2451–2456 | Cite as

Identification and evolutionary implication of four novel box H/ACA snoRNAs from Giardia lamblia

  • Luo Jun 
  • Zhou Hui 
  • Chen Chongjian 
  • Li Yan 
  • Chen Yueqin 
  • Qu Lianghu Email author


From a specialized cDNA library, four novel box H/ACA snoRNAs, named GLsR22, GLsR23, GLsR24 and GLsR25, were identified from the primitive eukaryote, Giardia lamblia. Bioinformatics analyses indicated that all of them can be potentially folded into double hairpins, the typical secondary structures of box H/ACA snoRNAs. GLsR24 and GLsR25 are predicted to guide the site-specific pseudouridylation at U1753 and U2396 on 23S rRNA, respectively, while GLsR22 and GLsR23 belong to the family of “orphan” snoRNAs. All of the four novel snoRNAs are encoded by single copy genes and located in small intergenic regions. Interestingly, compared with the counterparts previously reported in Archaea and other unicellular protozoan, the box H/ACA snoRNAs identified from G. lamblia have unique structural features, implying that snoRNAs evolved from prokaryotes to eukaryotes in different ways.


Giardia lamblia box H/ACA snoRNA gene evolution 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Maden B E. The numerous modified nucleotides in eukaryotic ribosomal RNA. Nucl Acid Res Mol Biol, 1990, 39: 241–303CrossRefGoogle Scholar
  2. 2.
    Bachellerie J P, Cavaillé J. Small nucleolar RNAs guide the ribose methylations of eukaryotic rRNAs. In: Grosjean H, Benne R, eds. Modification and Editing of RNA: The Alteration of RNA Structure and Function. Washington DC: ASM Press, 1998. 255–272Google Scholar
  3. 3.
    Ofengand J, Fournier M J. The pseudouridine residues of rRNA: Number, location, biosynthesis and function. In: Grosjean H, Benne R, eds. Modification and Editing of RNA: The Alteration of RNA Structure and Function. Washington DC: ASM Press, 1998. 229–253Google Scholar
  4. 4.
    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: 823–834CrossRefGoogle Scholar
  5. 5.
    Kiss-Laszlo Z, Henry Y, Kiss T. Sequence and structural elements of methylation guide snoRNAs essential for site-specific ribose methylation of pre-rRNA. EMBO J, 1998, 17: 797–807CrossRefGoogle Scholar
  6. 6.
    Tycowski K T, Shu M D, Steitz J A. A mammalian gene with introns instead of exons generating stable RNA products. Nature, 1996, 379: 464–466CrossRefGoogle Scholar
  7. 7.
    Kiss-László 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: 1077–1088CrossRefGoogle Scholar
  8. 8.
    Cavaille J, Nicoloso M, Bachellerie J P. Targeted ribose methylation of RNA in vivo directed by tailored antisense RNA guides. Nature, 1996, 383: 732–735CrossRefGoogle Scholar
  9. 9.
    Ganot P, Caizergues-Ferrer M, Kiss T. The family of box ACA small nucleolar RNAs is defined by an evolutionarily conserved secondary structure and ubiquitous sequence elements essential for RNA accumulation. Genes Dev, 1997, 11: 941–956Google Scholar
  10. 10.
    Ganot P, Bortolin M L, Kiss, T. Site-specific pseudouridine formation in preribosomal RNA is guided by small nucleolar RNAs. Cell, 1997, 89: 799–809CrossRefGoogle Scholar
  11. 11.
    Bortolin M L, Ganot P, Kiss T. Elements essential for accumulation and function of small nucleolar RNAs directing site-specific pseudouridylation of ribosomal RNAs. EMBO J, 1999, 18: 457–469CrossRefGoogle Scholar
  12. 12.
    John W S, Manuel E, Qu L H. Plant snoRNAs: Functional evolution and new models of gene expression. Trends Plant Sci, 2003, 8: 42–49CrossRefGoogle Scholar
  13. 13.
    Darzacq X, Jady B E, Verheggen C, et al. Cajal body-specific small nucleolar RNAs: A novel class of 2′-O-methylation and psedouridylation guide RNAs. EMBO J, 2002, 21: 2746–2756CrossRefGoogle Scholar
  14. 14.
    Zhou H, Chen Y Q, Du Y P, et al. Schizosaccharomyces pombe mgU6-47 snoRNA is required for the methylation of U6 snRNA at 41. Nucleic Acids Res, 2002, 30: 894–902CrossRefGoogle Scholar
  15. 15.
    Kiss A M, Jady B E, Darzacq X, et al. A Cajal body-specific pseudouridylation guide RNA is composed of two box H/ACA snoRNA-like domains. Nucleic Acids Res, 2002, 30: 4643–4649CrossRefGoogle Scholar
  16. 16.
    Massenet S, Mougin A, Branlant C. Posttranscriptional modifications in the U snRNAs. In: Grosjean H, Benne R, eds. Modification and Editing of RNA: The Alteration of RNA Structure and Function. Washington, DC: ASM Press, 1998. 201–228Google Scholar
  17. 17.
    Burns C M, Chu H, Rueter S M, et al. Regulation of serotonin-2C receptor G-protein coupling by RNA editing. Nature, 1997, 387: 303–308CrossRefGoogle Scholar
  18. 18.
    Vitali P, Basyuk, E, le Meur E, et al. ADAR2-mediated editing of RNA substrates in the nucleolus is inhibited by C/D small nucleolar RNAs. J Cell Biol, 2005, 169: 745–753CrossRefGoogle Scholar
  19. 19.
    Kishore S, Stamm S. The snoRNA HB II-52 regulates alternative splicing of the serotonin receptor 2C. Science, 2006, 311: 230–232CrossRefGoogle Scholar
  20. 20.
    Clouet d’Orval B, Bortolin M L, Gaspin C, et al. Box C/D RNA guides for the ribose methylation of archaeal tRNAs. The tRNATrp intron guides the formation of two ribose-methylated nucleotides in the mature tRNATrp. Nucleic Acids Res, 2001, 29: 4518–4529CrossRefGoogle Scholar
  21. 21.
    Gaspin C, Cavaillé J, Erauso G, et al. Archaeal homologs of eukaryotic methylation guide small neucleolar RNAs: Lessons from the Pyrococcus Genomes. J Mol Biol, 2000, 297: 895–906CrossRefGoogle Scholar
  22. 22.
    Tang T H, Bachellerie J P, Rozhdestvensky T. Identification of 86 candidates for small non-messenger RNAs from the archaeon Archaeoglobus fulgidus. Proc Natl Acad Sci USA, 2002, 99: 7536–7541CrossRefGoogle Scholar
  23. 23.
    Adam R D. Biology of Giardia lamblia. Clin Microbiol Rev, 2001, 14: 447–475CrossRefGoogle Scholar
  24. 24.
    Sogin M L, Gunderson J H, Elwood H J, et al. Phylogenetic meaning of the kingdom concept: An unusual ribosomal RNA from Giardia lamblia. Science, 1989, 243: 75–77CrossRefGoogle Scholar
  25. 25.
    Kabnick K S, Peattie D A. Giardia: A missing link between prokaryotes and eukaryotes. American Scientist, 1991, 79: 36–43Google Scholar
  26. 26.
    He D, Dong J H, Wen J F, et al. Phylogenetic positions of several amitochondriate protozoa—Evidence from phylogenetic analysis of DNA topoisomerase II. Sci China Ser C-Life Sci, 2005, 35(2): 115–122Google Scholar
  27. 27.
    Graczyk T K. Is Giardia a living fossil? Trends Parasitol, 2005, 21: 104–107CrossRefGoogle Scholar
  28. 28.
    He D, Wen J F, Chen W Q, et al. Identification, characteristic and phylogenetic analysis of type II DNA topoisomerase gene in Giardia lamblia. Cell Res, 2005, 15: 474–482CrossRefGoogle Scholar
  29. 29.
    Xin D D, Wen J F, He D, et al. Identification of a Giardia krr1 homolog gene and the secondarily anucleolate condition of Giaridia lamblia. Mol Biol Evol, 2005, 22: 391–394CrossRefGoogle Scholar
  30. 30.
    Yang C Y, Zhou H, Luo J, et al. Identification of 20 snoRNA-like RNAs from the primitive eukaryote, Giardia lamblia. Biochem Biophys Res Commun, 2005, 328: 1224–1231CrossRefGoogle Scholar
  31. 31.
    Keister D B. Axenic culture of Giardia lamblia in TYI-S-33 medium supplemented with bile. Trans R Sot Trop Med Hyg, 1983, 77: 487–488CrossRefGoogle Scholar
  32. 32.
    Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem, 1987, 162: 732–735CrossRefGoogle Scholar
  33. 33.
    Schattner P, Decatur W A, Davis C A, et al. Genome-wide searching for pseudouridylation guide snoRNAs—Analysis of the Saccharomyces cerevisiae genome. Nucleic Acids Res, 2004, 32: 4281–4296CrossRefGoogle Scholar
  34. 34.
    Uliei S, Liang X H, Unger R, et al. Small nucleolar RNAs that guide modification in trypanosomatids: repertoire, targets, genome organization, and functions. Int J Parasitol, 2004, 34: 445–454CrossRefGoogle Scholar
  35. 35.
    Liang X H, Uliel S, Hury A, et al. Genome-wide analysis of C/D and H/ACA-like small nucleolar RNAs in Trypanosoma brucei reveals a trypanosome-specific pattern of rRNA modification. RNA, 2005, 11: 619–645CrossRefGoogle Scholar
  36. 36.
    Russell A G, Schnare M N, Gray M W. Pseudouridine-guide RNAs and other Cbf5p-associated RNAs in Euglena gracilis. RNA, 2004, 10: 1034–1046CrossRefGoogle Scholar

Copyright information

© Science in China Press 2006

Authors and Affiliations

  • Luo Jun 
    • 1
  • Zhou Hui 
    • 1
  • Chen Chongjian 
    • 1
  • Li Yan 
    • 1
  • Chen Yueqin 
    • 1
  • Qu Lianghu 
    • 1
    Email author
  1. 1.Key Laboratory of Gene Engineering of the Ministry of Education, State Key Laboratory for BiocontrolZhongshan UniversityGuangzhouChina

Personalised recommendations