A DEAD box protein is required for formation of a hidden break in Arabidopsis chloroplast 23S rRNA

Plant Journal

Volumn 63, Issue 5, 2010, Pages 766-777

  Nishimura, Kenji ^a   Ashida, Hiroki ^a   Ogawa, Taro ^a   Yokota, Akiho ^a  

^a NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

Author keywords

23S rRNA; Arabidopsis thaliana; chloroplast; DEAD box protein; hidden break; RNA processing

Indexed keywords

23S RRNA; ARABIDOPSIS THALIANA; CHLOROPLAST; DEAD BOX PROTEIN; HIDDEN BREAK; RNA PROCESSING;

CHLOROPHYLL; GELS; PLANTS (BOTANY); PROTEINS;

RNA;

ARABIDOPSIS PROTEIN; CHLOROPLAST RNA; DEAD BOX PROTEIN; GREEN FLUORESCENT PROTEIN; RECOMBINANT PROTEIN; RH39 PROTEIN, ARABIDOPSIS; RIBULOSEBISPHOSPHATE CARBOXYLASE; RNA 23S;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; CHLOROPLAST; ESSENTIAL GENE; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; NORTHERN BLOTTING; PROTEIN BINDING; SEQUENCE HOMOLOGY; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BLOTTING, NORTHERN; BLOTTING, WESTERN; CHLOROPLASTS; DEAD-BOX RNA HELICASES; GENES, ESSENTIAL; GREEN FLUORESCENT PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN BINDING; RECOMBINANT PROTEINS; RIBULOSE-BISPHOSPHATE CARBOXYLASE; RNA, CHLOROPLAST; RNA, RIBOSOMAL, 23S; SEQUENCE HOMOLOGY, AMINO ACID;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 77956088343     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2010.04276.x     Document Type: Article

References (57)

1. Alonso, J.M., Stepanova, A.N., Leisse, T.J. et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science, 301, 653 657.
2. Barkan, A. (1993) Nuclear mutants of maize with defects in chloroplast polysome assembly have altered chloroplast RNA metabolism. Plant Cell, 5, 389 402.
3. Barkan, A., Voelker, R., Mendel-Hartvig, J., Johnson, D. Walker, M. (1995) Genetic analysis of chloroplast biogenesis in higher plants. Physiol. Plant. 93, 163 170.
4. Beick, S., Schmitz-Linneweber, C., Williams-Carrier, R., Jensen, B. Barkan, A. (2008) The pentatricopeptide repeat protein PPR5 stabilizes a specific tRNA precursor in maize chloroplasts. Mol. Cell. Biol. 28, 5337 5347.
5. Beligni, M.V. Mayfield, S.P. (2008) Arabidopsis thaliana mutants reveal a role for CSP41a and CSP41b, two ribosome-associated endonucleases, in chloroplast ribosomal RNA metabolism. Plant Mol. Biol. 67, 389 401.
6. Bell, C.J. Ecker, J.R. (1994) Assignment of 30 microsatellite loci to the linkage map of Arabidopsis. Genomics, 19, 137 144.
7. Bellaoui, M., Keddie, J.S. Gruissem, W. (2003) DCL is a plant-specific protein required for plastid ribosomal RNA processing and embryo development. Plant Mol. Biol. 53, 531 543.
8. Bisanz, C., Bégot, L., Carol, P., Perez, P., Bligny, M., Pesey, H., Gallois, J.-L., Lerbs-Mache, S. Mache, R. (2003) The Arabidopsis nuclear DAL gene encodes a chloroplast protein which is required for the maturation of the plastid ribosomal RNAs and is essential for chloroplast differentiation. Plant Mol. Biol. 51, 651 663.
9. Bohnsack, M.T., Martin, R., Granneman, S., Ruprecht, M., Schleiff, E. Tollervey, D. (2009) Prp43 bound at different sites on the pre-rRNA performs distinct functions in ribosome synthesis. Mol. Cell, 36, 583 592.
10. Bollenbach, T.J., Lange, H., Gutierrez, R., Erhardt, M., Stern, D.B. Gagliardi, D. (2005) RNR1, a 3′-5′ exoribonuclease belonging to the RNR superfamily, catalyzes 3′ maturation of chloroplast ribosomal RNAs in Arabidopsis thaliana. Nucleic Acids Res. 33, 2751 2763.
11. Clough, S.J. Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735 743.
12. Coburn, G.A., Miao, X., Briant, D.J. Mackie, G.A. (1999) Reconstitution of a minimal RNA degradosome demonstrates functional coordination between a 3′ exonuclease and a DEAD-box RNA helicase. Genes Dev. 13, 2594 2603.
13. Connolly, K. Culver, G. (2009) Deconstruction of ribosome construction. Trends Biochem. Sci. 34, 256 263.
14. Cordin, O., Banroques, J., Tanner, N.K. Linder, P. (2006) The DEAD-box protein family of RNA helicases. Gene, 367, 17 37.
15. Du, M.X., Johnson, R.B., Sun, X.-L., Staschke, K.A., Colacino, J. Wang, Q.M. (2002) Comparative characterization of two DEAD-box RNA helicases in superfamily II: human translation-initiation factor 4A and hepatitis C virus non-structural protein 3 (NS3) helicase. Biochem. J. 363, 147 155.
16. Evguenieva-Hackenberg, E. (2005) Bacterial ribosomal RNA in pieces. Mol. Microbiol. 57, 318 325.
17. Harris, E.H., Boynton, J.E. Gillham, N.W. (1994) Chloroplast ribosomes and protein synthesis. Microbiol. Rev. 58, 700 754.
18. Iost, I., Dreyfus, M. Linder, P. (1999) Ded1p, a DEAD-box protein required for translation initiation in Saccharomyces cerevisiae, is an RNA helicase. J. Biol. Chem. 274, 17677 17683.
19. Kaczanowska, M. Rydén-Aulin, M. (2007) Ribosome biogenesis and the translation process in Escherichia coli. Microbiol. Mol. Biol. Rev. 71, 477 494.
20. Kishine, M., Takabayashi, A., Munekage, Y., Shikanai, T., Endo, T. Sato, F. (2004) Ribosomal RNA processing and an RNase R family member in chloroplasts of Arabidopsis. Plant Mol. Biol. 55, 595 606.
21. Konieczny, A. Ausubel, F.M. (1993) A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers. Plant J. 4, 403 410.
22. Kössel, H., Natt, E., Strittmatter, G., Fritzsche, E., Gozdzicka-Jozefiak, A. Przybyl, D. (1985) Structure and expression of rRNA operons from plastids of higher plants. In Molecular Form and Function of the Plant Genome (van Vloten-Doting, L., Groot, G.S.P. Hall, T.C., eds). New York : Plenum Press, pp. 183 198.
23. Koussevitzky, S., Stanne, T.M., Peto, C.A., Giap, T., Sjögren, L.L., Zhao, Y., Clarke, A.K. Chory, J. (2007) An Arabidopsis thaliana virescent mutant reveals a role for ClpR1 in plastid development. Plant Mol. Biol. 63, 85 96.
24. Leal-Klevezas, D.S., Martinez-Soriano, J.P. Nazar, R.N. (2000) Transcription and processing map of the 4.5S-5S rRNA intergenic region (ITS3) from rapeseed (Brassica napus) chloroplasts. Plant Cell Rep. 19, 667 673.
25. 6f complex in Arabidopsis. Plant Cell, 13, 2539 2551.
26. Linder, P. (2006) Dead-box proteins: a family affair - active and passive players in RNP-remodeling. Nucleic Acids Res. 34, 4168 4180.
27. Martínez-García, J.F., Monte, E. Quail, P.H. (1999) Simple, rapid and quantitative method for preparing Arabidopsis protein extracts for immunoblot analysis. Plant J. 20, 251 257.
28. Melen, G.J., Pesce, C.G., Rossi, M.S. Kornblihtt, A.R. (1999) Novel processing in a mammalian nuclear 28S pre-rRNA: tissue-specific elimination of an 'intron' bearing a hidden break site. EMBO J. 18, 3107 3118.
29. Motohashi, R., Yamazaki, T., Myouga, F. et al. (2007) Chloroplast ribosome release factor 1 (AtcpRF1) is essential for chloroplast development. Plant Mol. Biol. 64, 481 497.
30. Mudd, E.A., Sullivan, S., Gisby, M.F., Mironov, A., Kwon, C.S., Chung, W.I. Day, A. (2008) A 125 kDa RNase E/G-like protein is present in plastids and is essential for chloroplast development and autotrophic growth in Arabidopsis. J. Exp. Bot. 59, 2597 2610.
31. Nakagawa, T., Kurose, T., Hino, T., Tanaka, K., Kawamukai, M., Niwa, Y., Toyooka, K., Matsuoka, K., Jinbo, T. Kimura, T. (2007) Development of series of Gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J. Biosci. Bioeng. 104, 34 41.
32. Nishimura, K., Ogawa, T., Ashida, H. Yokota, A. (2008) Molecular mechanisms of RuBisCO biosynthesis in higher plants. Plant Biotechnol. 25, 285 290.
33. Nissen, P., Hansen, J., Ban, N., Moore, P.B. Steitz, T.A. (2000) The structural basis of ribosome activity in peptide bond synthesis. Science, 289, 920 930.
34. Ogawa, T., Nishimura, K., Aoki, T., Ashida, H. Yokota, A. (2009) A phosphofructokinase B-type carbohydrate kinase family protein, NARA5, for massive expressions of plastid-encoded photosynthetic genes in Arabidopsis. Plant Physiol. 151, 114 128.
35. Olinares, P.D.B., Ponnala, L. van Wijk, K.J. (2010) Megadalton complexes in the chloroplast stroma of arabidopsis thaliana characterized by size exclusion chromatography, mass spectrometry and hierarchical clustering. Mol. Cell Proteomics, in press.
36. Pertschy, B., Schneider, C., Gnädig, M., Schäfer, T., Tollervey, D. Hurt, E. (2009) RNA helicase Prp43 and its co-factor Pfa1 promote 20 to 18S rRNA processing catalyzed by the endonuclease Nob1. J. Biol. Chem. 284, 35079 35091.
37. Pesaresi, P., Varotto, C., Meurer, J., Jahns, P., Salamini, F. Leister, D. (2001) Knock-out of the plastid ribosomal protein L11 in Arabidopsis: effects on mRNA translation and photosynthesis. Plant J. 27, 179 189.
38. Prikryl, J., Watkins, K.P., Friso, G., van Wijk, K.J. Barkan, A. (2008) A member of the Whirly family is a multifunctional RNA- and DNA-binding protein that is essential for chloroplast biogenesis. Nucleic Acids Res. 36, 5152 5165.
39. Rocak, S. Linder, P. (2004) DEAD-box proteins: the driving forces behind RNA metabolism. Nat. Rev. Mol. Cell Biol. 5, 232 241.
40. Rozier, C., Rocipon, M. Mache, R. (1979) Post-maturation of the plastid ribosomal RNA in the plant kingdom. J. Mol. Evol. 13, 271 279.
41. Schmitz-Linneweber, C., Williams-Carrier, R.E., Williams-Voelker, P.M., Kroeger, T.S., Vichas, A. Barkan, A. (2006) A pentatricopeptide repeat protein facilitates the trans-splicing of the maize chloroplast rps12 pre-mRNA. Plant Cell, 18, 2650 2663.
42. Seki, M., Carninci, P., Nishiyama, Y., Hayashizaki, Y. Shinozaki, K. (1998) High-efficiency cloning of Arabidopsis full-length cDNA by biotinylated CAP trapper. Plant J. 15, 707 720.
43. Sharma, M.R., Wilson, D.N., Datta, P.P., Barat, C., Schluenzen, F., Fucini, P. Agrawal, R.K. (2007) Cryo-EM study of the spinach chloroplast ribosome reveals the structural and functional roles of plastid-specific ribosomal proteins. Proc. Natl. Acad. Sci. USA, 104, 19315 19320.
44. Stone, A.R. (1973) A simplified method for preparing sucrose gradient. Biochem. J. 137, 117 118.
45. Walter, M., Kilian, J. Kudla, J. (2002) PNPase activity determines the efficiency of mRNA 3′-end processing, the degradation of tRNA and the extent of polyadenylation in chloroplasts. EMBO J. 21, 6905 6914.
46. Wang, Y., Duby, G., Purnelle, B. Boutry, M. (2000) Tobacco VDL gene encodes a plastid DEAD box RNA helicase and is involved in chloroplast differentiation and plant morphogenesis. Plant Cell, 12, 2129 2142.
47. Watkins, K.P., Kroeger, T.S., Cooke, A.M., Williams-Carrier, R.E., Friso, G., Belcher, S.E., van Wijk, K.J. Barkan, A. (2007) A ribonuclease III domain protein functions in group II intron splicing in maize chloroplasts. Plant Cell, 19, 2606 2623.
48. Williams-Carrier, R., Kroeger, T. Barkan, A. (2008) Sequence-specific binding of a chloroplast pentatricopeptide repeat protein to its native group II intron ligand. RNA, 14, 1930 1941.
49. Wostrikoff, K. Stern, D. (2007) Rubisco large-subunit translation is autoregulated in response to its assembly state in tobacco chloroplasts. Proc. Natl. Acad. Sci. USA, 104, 6466 6471.
50. Yamaguchi, K. Subramanian, A.R. (2000) The plastid ribosomal proteins. Identification of all the proteins in the 50S subunit of an organelle ribosome (chloroplast). J. Biol. Chem. 275, 28466 28482.
51. Yamaguchi, K. Subramanian, A.R. (2003) Proteomic identification of all plastid-specific ribosomal proteins in higher plant chloroplast 30S ribosomal subunit. Eur. J. Biochem. 270, 190 205.
52. Yamaguchi, K., von Knoblauch, K. Subramanian, A.R. (2000) The plastid ribosomal proteins. Identification of all the proteins in the 30S subunit of an organelle ribosome (chloroplast). J. Biol. Chem. 275, 28455 28465.
53. Yamaguchi, K., Beligni, M.V., Prieto, S., Haynes, P.A., McDonald, W.H., Yates, J.R. 3rd. Mayfield, S.P. (2003) Proteomic characterization of the Chlamydomonas reinhardtii chloroplast ribosome. Identification of proteins unique to the 70S ribosome. J. Biol. Chem. 278, 33774 33785.
54. Yokota, A. Shigeoka, S. (2008) Engineering of photosynthetic pathways. In Bioengineering and Molecular Biology of Plant Pathways, 1 (Bohnert, H.J., Nguyen, H. Lewis, N.G., eds). Dordrecht, The Netherlands : Elsevier, pp. 81 105.
55. Yu, F., Liu, X., Alsheikh, M., Park, S. Rodermel, S. (2008) Mutations in SUPPRESSOR OF VARIEGATION1, a factor required for normal chloroplast translation, suppress var2-mediated leaf variegation in Arabidopsis. Plant Cell, 20, 1786 1804.
56. Zybailov, B., Rutschow, H., Friso, G., Rudella, A., Emanuelsson, O., Sun, Q. van Wijk, K.J. (2008) Sorting signals, N-terminal modifications and abundance of the chloroplast proteome. PLoS ONE, 3, e1994.
57. Zybailov, B., Friso, G., Kim, J., Rudella, A., Rodríguez, V.R., Asakura, Y., Sun, Q. van Wijk, K.J. (2009) Large scale comparative proteomics of a chloroplast Clp protease mutant reveals folding stress, altered protein homeostasis, and feedback regulation of metabolism. Mol. Cell Proteomics, 8, 1789 1810.