Identification of protein factors and U3 snoRNAs from a Brassica oleracea RNP complex involved in the processing of pre-rRNA

Plant Journal

Volumn 61, Issue 3, 2010, Pages 383-398

  Samaha, Hala ^a,c   Delorme, Valérie ^a   Pontvianne, Frederic ^a,d   Cooke, Richard ^a   Delalande, Francois ^b   Van Dorsselaer, Alain ^b   Echeverria, Manuel ^a   Sáez Vásquez, Julio ^a  

^a Laboratoire Génome et Développement des Plantes   (France)

^b INSTITUT DE RECHERCHES SUBATOMIQUES   (France)

^c UNIVERSITÉ DE PICARDIE JULES VERNE   (France)

^d WASHINGTON UNIVERSITY   (United States)

Author keywords

Arabidopsis; Pre rRNA; Processing; Proteomic; Ribosome; U3 snoRNP

Indexed keywords

RIBONUCLEOPROTEIN; RNA PRECURSOR; RNA, U3 SMALL NUCLEOLAR; SMALL NUCLEOLAR RNA; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BRASSICA; CHEMISTRY; CONFORMATION; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; BASE SEQUENCE; BRASSICA; CONSERVED SEQUENCE; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; PLANT PROTEINS; RIBONUCLEOPROTEINS; RNA PRECURSORS; RNA, SMALL NUCLEOLAR; SEQUENCE ALIGNMENT;

ARABIDOPSIS; BRASSICA OLERACEA; BRASSICA OLERACEA VAR. CAPITATA;

EID: 75749135270     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2009.04061.x     Document Type: Article

References (74)

1. Abe, S., Sakai, M., Yagi, K., Hagino, T., Ochi, K., Shibata, K. Davies, E. (2003) A Tudor protein with multiple SNc domains from pea seedlings: cellular localization, partial characterization, sequence analysis, and phylogenetic relationships. J. Exp. Bot. 54 (384 971 983.
2. Ahmad, Y., Boisvert, F.M., Gregor, P., Cobley, A. Lamond, A.I. (2009) NOPdb: Nucleolar Proteome Database - 2008 update. Nucleic Acids Res. 37 (Database issue D181 D184.
3. Balczun, C., Bunse, A., Schwarz, C., Piotrowski, M. Kuck, U. (2006) Chloroplast heat shock protein Cpn60 from Chlamydomonas reinhardtii exhibits a novel function as a group II intron-specific RNA-binding protein. FEBS Lett. 580 (18 4527 4532.
4. Barneche, F., Steinmetz, F. Echeverria, M. (2000) Fibrillarin genes encode both a conserved nucleolar protein and a novel small nucleolar RNA involved in ribosomal RNA methylation in Arabidopsis thaliana. J. Biol. Chem. 275 (35 27212 27220.
5. Barneche, F., Gaspin, C., Guyot, R. Echeverria, M. (2001) Identification of 66 box C/D snoRNAs in Arabidopsis thaliana: extensive gene duplications generated multiple isoforms predicting new ribosomal RNA 2'-O-methylation sites. J. Mol. Biol. 311 (1 57 73.
6. Beltrame, M. Tollervey, D. (1992) Identification and functional analysis of two U3 binding sites on yeast pre-ribosomal RNA. EMBO J. 11 (4 1531 1542.
7. Beltrame, M. Tollervey, D. (1995) Base pairing between U3 and the pre-ribosomal RNA is required for 18S rRNA synthesis. EMBO J. 14 (17 4350 4356.
8. Borovjagin, A.V. Gerbi, S.A. (2001) Xenopus U3 snoRNA GAC-Box A' and Box A sequences play distinct functional roles in rRNA processing. Mol. Cell. Biol. 21 (18 6210 6221.
9. Brown, J.W., Echeverria, M. Qu, L.H. (2003a) Plant snoRNAs: functional evolution and new modes of gene expression. Trends Plant Sci. 8 (1 42 49.
10. Brown, J.W., Echeverria, M., Qu, L.H., Lowe, T.M., Bachellerie, J.P., Huttenhofer, A., Kastenmayer, J.P., Green, P.J., Shaw, P. Marshall, D.F. (2003b) Plant snoRNA database. Nucleic Acids Res. 31 (1 432 435.
11. Brown, J.W., Marshall, D.F. Echeverria, M. (2008) Intronic noncoding RNAs and splicing. Trends Plant Sci. 13 (7 335 342. Epub 2008 Jun 2012.
12. Brukhin, V., Gheyselinck, J., Gagliardini, V., Genschik, P. Grossniklaus, U. (2005) The RPN1 subunit of the 26S proteasome in Arabidopsis is essential for embryogenesis. Plant Cell, 17 (10 2723 2737.
13. Calikowski, T.T., Meulia, T. Meier, I. (2003) A proteomic study of the arabidopsis nuclear matrix. J. Cell. Biochem. 90 (2 361 378.
14. Caparros-Ruiz, D., Lahmy, S., Piersanti, S. Echeverria, M. (1997) Two ribosomal DNA-binding factors interact with a cluster of motifs on the 5' external transcribed spacer, upstream from the primary pre-rRNA processing site in a higher plant. Eur. J. Biochem. 247 (3 981 989.
15. Chaboute, M.E., Clement, B., Sekine, M., Philipps, G. Chaubet-Gigot, N. (2000) Cell cycle regulation of the tobacco ribonucleotide reductase small subunit gene is mediated by E2F-like elements. Plant Cell, 12 (10 1987 2000.
16. Chen, C.L., Liang, D., Zhou, H., Zhuo, M., Chen, Y.Q. Qu, L.H. (2003) The high diversity of snoRNAs in plants: identification and comparative study of 120 snoRNA genes from Oryza sativa. Nucleic Acids Res. 31 (10 2601 2613.
17. Clery, A., Senty-Segault, V., Leclerc, F., Raue, H.A. Branlant, C. (2007) Analysis of sequence and structural features that identify the B/C motif of U3 small nucleolar RNA as the recognition site for the Snu13p-Rrp9p protein pair. Mol. Cell. Biol. 27 (4 1191 1206.
18. Comella, P., Pontvianne, F., Lahmy, S., Vignols, F., Barbezier, N., Debures, A., Jobet, E., Brugidou, E., Echeverria, M. Saez-Vasquez, J. (2008) Characterization of a ribonuclease III-like protein required for cleavage of the pre-rRNA in the 3'ETS in Arabidopsis. Nucleic Acids Res. 36 (4 1163 1175.
19. Dragon, F., Gallagher, J.E., Compagnone-Post, P.A. et al. (2002) A large nucleolar U3 ribonucleoprotein required for 18S ribosomal RNA biogenesis. Nature, 417 (6892 967 970.
20. Eichler, D.C. Craig, N. (1994) Processing of eukaryotic ribosomal RNA. Prog. Nucleic Acid Res. Mol. Biol. 49, 197 239.
21. Elias, J.E. Gygi, S.P. (2007) Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat. Methods, 4 (3 207 214.
22. Fatica, A. Tollervey, D. (2002) Making ribosomes. Curr. Opin. Cell Biol. 14 (3 313 318.
23. Fromont-Racine, M., Senger, B., Saveanu, C. Fasiolo, F. (2003) Ribosome assembly in eukaryotes. Gene, 313 (2003 17 42.
24. Gallagher, J.E., Dunbar, D.A., Granneman, S., Mitchell, B.M., Osheim, Y., Beyer, A.L. Baserga, S.J. (2004) RNA polI transcription and pre-rRNA processing are linked by specific SSU processome components. Genes Dev. 18 (20 2506 2517.
25. Giavalisco, P., Wilson, D., Kreitler, T., Lehrach, H., Klose, J., Gobom, J. Fucini, P. (2005) High heterogeneity within the ribosomal proteins of the Arabidopsis thaliana 80S ribosome. Plant Mol. Biol. 57 (4 577 591.
26. Grandi, P., Rybin, V., Bassler, J. et al. (2002) 90S pre-ribosomes include the 35S pre-rRNA, the U3 snoRNP, and 40S subunit processing factors but predominantly lack 60S synthesis factors. Mol. Cell, 10 (1 105 115.
27. Granneman, S., Pruijn, G.J., Horstman, W., van Venrooij, W.J., Luhrmann, R. Watkins, N.J. (2002) The hU3-55K protein requires 15.5K binding to the box B/C motif as well as flanking RNA elements for its association with the U3 small nucleolar RNA in vitro. J. Biol. Chem. 277 (50 48490 48500.
28. Griffith, M.E., Mayer, U., Capron, A., Ngo, Q.A., Surendrarao, A., McClinton, R., Jurgens, G. Sundaresan, V. (2007) The TORMOZ gene encodes a nucleolar protein required for regulated division planes and embryo development in Arabidopsis. Plant Cell, 19 (7 2246 2263.
29. Hartshorne, T. Agabian, N. (1994) A common core structure for U3 small nucleolar RNAs. Nucleic Acids Res. 22 (16 3354 3364.
30. Hughes, J.M. Ares, M. Jr. (1991) Depletion of U3 small nucleolar RNA inhibits cleavage in the 5' external transcribed spacer of yeast pre-ribosomal RNA and impairs formation of 18S ribosomal RNA. EMBO J. 10 (13 4231 4239.
31. Jones, K.W., Gorzynski, K., Hales, C.M., Fischer, U., Badbanchi, F., Terns, R.M. Terns, M.P. (2001) Direct interaction of the spinal muscular atrophy disease protein SMN with the small nucleolar RNA-associated protein fibrillarin. J. Biol. Chem. 276 (42 38645 38651.
32. Kass, S., Tyc, K., Steitz, J.A. Sollner-Webb, B. (1990) The U3 small nucleolar ribonucleoprotein functions in the first step of preribosomal RNA processing. Cell, 60 (6 897 908.
33. Kiss, T. Solymosy, F. (1990) Molecular analysis of a U3 RNA gene locus in tomato: transcription signals, the coding region, expression in transgenic tobacco plants and tandemly repeated pseudogenes. Nucleic Acids Res. 18 (8 1941 1949.
34. Kufel, J., Dichtl, B. Tollervey, D. (1999) Yeast Rnt1p is required for cleavage of the pre-ribosomal RNA in the 3' ETS but not the 5' ETS. RNA, 5 (7 909 917.
35. Lafontaine, D.L. Tollervey, D. (1999) Nop58p is a common component of the box C+D snoRNPs that is required for snoRNA stability. RNA, 5 (3 455 467.
36. Lalev, A.I. Nazar, R.N. (2001) A chaperone for ribosome maturation. J. Biol. Chem. 276 (20 16655 16659.
37. Larkin, M.A., Blackshields, G., Brown, N.P. et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics, 23 (21 2947 2948.
38. Leader, D.J., Clark, G.P., Watters, J., Beven, A.F., Shaw, P.J. Brown, J.W. (1997) Clusters of multiple different small nucleolar RNA genes in plants are expressed as and processed from polycistronic pre-snoRNAs. EMBO J. 16 (18 5742 5751.
39. Leary, D.J., Terns, M.P. Huang, S. (2004) Components of U3 snoRNA-containing complexes shuttle between nuclei and the cytoplasm and differentially localize in nucleoli: implications for assembly and function. Mol. Biol. Cell, 15 (1 281 293.
40. Leung, A.K., Trinkle-Mulcahy, L., Lam, Y.W., Andersen, J.S., Mann, M. Lamond, A.I. (2006) NOPdb: Nucleolar Proteome Database. Nucleic Acids Res. 34 (Database issue D218 D220.
41. Lukowiak, A.A., Granneman, S., Mattox, S.A., Speckmann, W.A., Jones, K., Pluk, H., Venrooij, W.J., Terns, R.M. Terns, M.P. (2000) Interaction of the U3-55k protein with U3 snoRNA is mediated by the box B/C motif of U3 and the WD repeats of U3-55k. Nucleic Acids Res. 28 (18 3462 3471.
42. Markham, N.R. Zuker, M. (2005) DINAMelt web server for nucleic acid melting prediction. Nucleic Acids Res. 33 (Web Server issue W577 W581.
43. Marshallsay, C., Kiss, T. Filipowicz, W. (1990) Amplification of plant U3 and U6 snRNA gene sequences using primers specific for an upstream promoter element and conserved intragenic regions. Nucleic Acids Res. 18 (12 3459 3466.
44. Mathieu, O., Yukawa, Y., Prieto, J.L., Vaillant, I., Sugiura, M. Tourmente, S. (2003) Identification and characterization of transcription factor IIIA and ribosomal protein L5 from Arabidopsis thaliana. Nucleic Acids Res. 31 (9 2424 2433.
45. Meier, U.T. (2005) The many facets of H/ACA ribonucleoproteins. Chromosoma, 114 (1 1 14.
46. Miles, T.D., Jakovljevic, J., Horsey, E.W., Harnpicharnchai, P., Tang, L. Woolford, J.L. Jr. (2005) Ytm1, Nop7, and Erb1 form a complex necessary for maturation of yeast 66S preribosomes. Mol. Cell. Biol. 25 (23 10419 10432.
47. Moll, C., von Lyncker, L., Zimmermann, S., Kagi, C., Baumann, N., Twell, D., Grossniklaus, U. Gross-Hardt, R. (2008) CLO/GFA1 and ATO are novel regulators of gametic cell fate in plants. Plant J. 56 (6 913 921.
48. Nomura, M. (2001) Ribosomal RNA genes, RNA polymerases, nucleolar structures, and synthesis of rRNA in the yeast Saccharomyces cerevisiae. Cold Spring Harb. Symp. Quant. Biol. 66, 555 565.
49. Pagnussat, G.C., Yu, H.J., Ngo, Q.A., Rajani, S., Mayalagu, S., Johnson, C.S., Capron, A., Xie, L.F., Ye, D. Sundaresan, V. (2005) Genetic and molecular identification of genes required for female gametophyte development and function in Arabidopsis. Development 132 (3 603 614.
50. Pendle, A.F., Clark, G.P., Boon, R., Lewandowska, D., Lam, Y.W., Andersen, J., Mann, M., Lamond, A.I., Brown, J.W. Shaw, P.J. (2005) Proteomic analysis of the Arabidopsis nucleolus suggests novel nucleolar functions. Mol. Biol. Cell, 16 (1 260 269.
51. Peng, J., Elias, J.E., Thoreen, C.C., Licklider, L.J. Gygi, S.P. (2003) Evaluation of multidimensional chromatography coupled with tandem mass spectrometry (LC/LC-MS/MS) for large-scale protein analysis: the yeast proteome. J. Proteome Res. 2 (1 43 50.
52. Pih, K.T., Yi, M.J., Liang, Y.S., Shin, B.J., Cho, M.J., Hwang, I. Son, D. (2000) Molecular cloning and targeting of a fibrillarin homolog from Arabidopsis. Plant Physiol. 123 (1 51 58.
53. Pontvianne, F., Matia, I., Douet, J., Tourmente, S., Medina, F.J., Echeverria, M. Saez-Vasquez, J. (2007) Characterization of AtNUC-L1 reveals a central role of nucleolin in nucleolus organization and silencing of AtNUC-L2 gene in Arabidopsis. Mol. Biol. Cell, 18 (2 369 379.
54. Preuss, S.B., Costa-Nunes, P., Tucker, S. et al. (2008) Multimegabase silencing in nucleolar dominance involves siRNA-directed DNA methylation and specific methylcytosine-binding proteins. Mol. Cell, 32 (5 673 684.
55. Ruggero, D., Ciammaruconi, A. Londei, P. (1998) The chaperonin of the archaeon Sulfolobus solfataricus is an RNA-binding protein that participates in ribosomal RNA processing. EMBO J. 17 (12 3471 3477.
56. Saez-Vasquez, J. Echeverria, M. (2006) Polymerase I transcription. In Regulation of Transcription in Plants (Grasser, K.D., ed.). Oxford, UK : Blackwell, pp. 162 183.
57. Saez-Vasquez, J. Medina, F.J. (2008) The plant nucleolus. In Botanical Research: Incorporating Advances in Plant Pathology, Vol. 47 (Kader, J.-C. Delseny, M., eds). San Diego : Elsevier Academic Press Inc, pp. 1 46.
58. Saez-Vasquez, J., Caparros-Ruiz, D., Barneche, F. Echeverria, M. (2004a) Characterization of a crucifer plant pre-rRNA processing complex. Biochem. Soc. Trans. 32 (Pt 4 578 580.
59. Saez-Vasquez, J., Caparros-Ruiz, D., Barneche, F. Echeverria, M. (2004b) A plant snoRNP complex containing snoRNAs, fibrillarin, and nucleolin-like proteins is competent for both rRNA gene binding and pre-rRNA processing in vitro. Mol. Cell. Biol. 24 (16 7284 7297.
60. Schafer, T., Strauss, D., Petfalski, E., Tollervey, D. Hurt, E. (2003) The path from nucleolar 90S to cytoplasmic 40S pre-ribosomes. EMBO J. 22 (6 1370 1380.
61. Schlatter, H., Langer, T., Rosmus, S., Onneken, M.L. Fasold, H. (2002) A novel function for the 90 kDa heat-shock protein (Hsp90): facilitating nuclear export of 60 S ribosomal subunits. Biochem. J. 362 (Pt 3 675 684.
62. Segault, V., Mougin, A., Gregoire, A., Banroques, J. Branlant, C. (1992) An experimental study of Saccharomyces cerevisiae U3 snRNA conformation in solution. Nucleic Acids Res. 20 (13 3443 3451.
63. Shaw, P.J. Brown, J.W. (2004) Plant nuclear bodies. Curr. Opin. Plant Biol. 7 (6 614 620.
64. Shaw, D.J., Eggleton, P. Young, P.J. (2008) Joining the dots: production, processing and targeting of U snRNP to nuclear bodies. Biochim. Biophys. Acta, 1783 (11 2137 2144.
65. Speckmann, W., Narayanan, A., Terns, R. Terns, M.P. (1999) Nuclear retention elements of U3 small nucleolar RNA. Mol. Cell. Biol. 19 (12 8412 8421.
66. Stavreva, D.A., Kawasaki, M., Dundr, M. et al. (2006) Potential roles for ubiquitin and the proteasome during ribosome biogenesis. Mol. Cell. Biol. 26 (13 5131 5145.
67. Thiry, M. Lafontaine, D.L. (2005) Birth of a nucleolus: the evolution of nucleolar compartments. Trends Cell Biol. 15 (4 194 199.
68. Tschochner, H. Hurt, E. (2003) Pre-ribosomes on the road from the nucleolus to the cytoplasm. Trends Cell Biol. 13 (5 255 263.
69. Turner, A.J., Knox, A.A., Prieto, J.L., McStay, B. Watkins, N.J. (2009) A novel SSU processome assembly intermediate that contains the U3 snoRNP, nucleolin, RRP5 and DBP4. Mol. Cell. Biol. 30, 30.
70. Valasek, L., Hasek, J., Nielsen, K.H. Hinnebusch, A.G. (2001) Dual function of eIF3j/Hcr1p in processing 20 S pre-rRNA and translation initiation. J. Biol. Chem. 276 (46 43351 43360.
71. Venema, J. Tollervey, D. (1995) Processing of pre-ribosomal RNA in Saccharomyces cerevisiae. Yeast, 11 (16 1629 1650.
72. Wassenegger, M. Krczal, G. (2006) Nomenclature and functions of RNA-directed RNA polymerases. Trends Plant Sci. 10, 10.
73. Whittaker, E., Lossky, M. Beggs, J.D. (1990) Affinity purification of spliceosomes reveals that the precursor RNA processing protein PRP8, a protein in the U5 small nuclear ribonucleoprotein particle, is a component of yeast spliceosomes. Proc. Natl Acad. Sci. USA, 87 (6 2216 2219.
74. Zanetti, M.E., Chang, I.F., Gong, F., Galbraith, D.W. Bailey-Serres, J. (2005) Immunopurification of polyribosomal complexes of Arabidopsis for global analysis of gene expression. Plant Physiol. 138 (2 624 635.