A pentatricopeptide repeat protein facilitates the trans-splicing of the maize chloroplast rps12 pre-mRNA

Plant Cell

Volumn 18, Issue 10, 2006, Pages 2650-2663

  Schmitz Linneweber, Christian ^a,b   Williams Carrier, Rosalind E ^a   Williams Voelker, Pascale M ^a   Kroeger, Tiffany S ^a   Vichas, Athea ^a,c   Barkan, Alice ^a  

^a UNIVERSITY OF OREGON   (United States)

^b HUMBOLDT UNIVERSITY   (Germany)

^c Weill Cornell Graduate School of Biomedical Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CROPS; RNA;

BIOINFORMATIC DATA; PENTATRICOPEPTIDE REPEAT (PPR); POSTTRANSCRIPTIONAL STEPS; PROTEIN HARBORING;

PROTEINS;

AMINO ACIDS; CORN; NUCLEIC ACIDS; PROTEINS;

ALGAE; EUKARYOTA; TRACHEOPHYTA; ZEA MAYS;

EID: 33750967640     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.106.046110     Document Type: Article

References (76)

1. Alonso, J.M., et al. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301, 653-657.
2. Auchincloss, A., Zerges, W., Perron, K., Girard-Bascou, J., and Rochaix, J.-D. (2002). Characterization of Tbc2, a nucleus-encoded factor specifically required for translation of the chloroplast psbC mRNA in Chlamydomonas reinhardtii. J. Cell Biol. 157, 953-962.
3. Barkan, A. (1993). Nuclear mutants of maize with defects in chloroplast polysome assembly have altered chloroplast RNA metabolism. Plant Cell 5, 389-402.
4. Barkan, A. (1998). Approaches to investigating nuclear genes that function in chloroplast biogenesis in land plants. Methods Enzymol. 297, 38-57.
5. Barkan, A. (2004). Intron splicing in plant organelles. In Molecular Biology and Biotechnology of Plant Organelles, H. Daniell and C. Chase, eds (Dordrecht, The Netherlands: Springer), pp. 295-322.
6. Barkan, A., Walker, M., Nolasco, M., and Johnson, D. (1994). A nuclear mutation in maize blocks the processing and translation of several chloroplast mRNAs and provides evidence for the differential translation of alternative mRNA forms. EMBO J. 13, 3170-3181.
7. Bentolila, S., Alfonso, A.A., and Hanson, M.R. (2002). A pentatricopeptide repeat-containing gene restores fertility to cytoplasmic male-sterile plants. Proc. Natl. Acad. Sci. USA 99, 10887-10892.
8. Carignani, G., Groudinsky, O., Frezza, D., Schiavon, E., Bergantino, E., and Slonimski, P.P. (1983). An mRNA maturase is encoded by the first intron of the mitochondrial gene for the subunit I of cytochrome oxidase in S. cerevisiae. Cell 35, 733-742.
9. Carignani, G., Netter, P., Bergantino, E., and Robineau, S. (1986). Expression of the mitochondrial split gene coding for cytochrome oxidase subunit I in S. cerevisiae: RNA splicing pathway. Curr. Genet. 11, 55-63.
10. Coffin, J.W., Dhillon, R., Ritzel, R.G., and Nargang, F.E. (1997). The Neurospora crassa cya-5 nuclear gene encodes a protein with a region of homology to the Saccharomyces cerevisiae PET309 protein and is required in a post-transcriptional step for the expression of the mitochondrially encoded COXI protein. Curr. Genet. 32, 273-280.
11. Cukras, A.R., Southworth, D.R., Brunelle, J.L., Culver, G.M., and Green, R. (2003). Ribosomal proteins S12 and S13 function as control elements for translocation of the mRNA:tRNA complex. Mol. Cell 12, 321-328.
12. Culver, G.M., and Noller, H.F. (1999). Efficient reconstitution of functional Escherichia coli 30S ribosomal subunits from a complete set of recombinant small subunit ribosomal proteins. RNA 5, 832-843.
13. Cushing, D.A., Forsthoefel, N.R., Gestaut, D.R., and Vernon, D.M. (2005). Arabidopsis emb175 and other ppr knockout mutants reveal essential roles for pentatricopeptide repeat (PPR) proteins in plant embryogenesis. Planta 221, 424-436.
14. Dahlberg, A.E., Dahlberg, J.E., Lund, E., Tokimatsu, H., Rabson, A.B., Calvert, P.C., Reynolds, F., and Zahalak, M. (1978). Processing of the 5′ end of Escherichia coli 16S ribosomal RNA. Proc. Natl. Acad. Sci. USA 75, 3598-3602.
15. Desloire, S., et al. (2003). Identification of the fertility restoration locus, Rfo, in radish, as a member of the pentatricopeptide-repeat protein family. EMBO Rep. 4, 588-594.
16. Ding, Y.H., Liu, N.Y., Tang, Z.S., Liu, J., and Yang, W.C. (2006). Arabidopsis GLUTAMINE-RICH PROTEIN23 is essential for early embryogenesis and encodes a novel nuclear PPR motif protein that interacts with RNA polymerase II subunit III. Plant Cell 18, 815-830.
17. Drescher, A., Ruf, S., Calsa, T., Jr., Carrer, H., and Bock, R. (2000). The two largest chloroplast genome-encoded open reading frames of higher plants are essential genes. Plant J. 22, 97-104.
18. Dyall, S.D., Brown, M.T., and Johnson, P.J. (2004). Ancient invasions: From endosymbionts to organelles. Science 304, 253-257,
19. Emanuelsson, O., Nielsen, H., Brunak, S., and von Heijne, G. (2000). Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 300, 1005-1016.
20. Fisk, D.G., Walker, M.B., and Barkan, A. (1999). Molecular cloning of the maize gene crp1 reveals similarity between regulators of mitochondrial and chloroplast gene expression. EMBO J. 18, 2621-2630.
21. Goldschmidt-Clermont, M., Girard-Bascou, J., Choquet, Y., and Rochaix, J.D. (1990). Trans-splicing mutants of Chlamydomonas reinhardtii. Mol. Gen. Genet. 223, 417-425.
22. Gray, M.W. (2004). The evolutionary origins of plant organelles. In Molecular Biology and Biotechnology of Plant Organelles, Chloroplasts and Mitochondria, H. Daniell and C. Chase, eds (Dordrecht, The Netherlands: Springer), pp. 15-36.
23. Hajdukiewicz, P.T., Allison, L.A., and Maliga, P. (1997). The two RNA polymerases encoded by the nuclear and the plastid compartments transcribe distinct groups of genes in tobacco plastids. EMBO J. 16, 4041-4048.
24. Han, C.D., Coe, E.H., Jr., and Martienssen, R.A. (1992). Molecular cloning and characterization of iojap (ij), a pattern striping gene of maize. EMBO J. 11, 4037-4046.
25. Han, C.-d., Derby, R.J., Schnable, P.S., and Martienssen, R.A. (1995). Characterization of the plastids affected by class II albino mutations of maize at the morphological and transcript levels. Maydica 40, 13-22.
26. Han, C.-D., Patrie, W., Polacco, M., and Coe, E.H. (1993). Aberrations in plastid transcripts and deficiency of plastid DNA in striped and albino mutants in maize. Planta 191, 552-563.
27. Hashimoto, M., Endo, T., Peltier, G., Tasaka, M., and Shikanai, T. (2003). A nucleus-encoded factor, CRR2, is essential for the expression of chloroplast ndhB in Arabidopsis. Plant J. 36, 541-549.
28. Hess, W.R., Prombona, A., Fieder, B., Subramanian, A.R., and Borner, T. (1993). Chloroplast rps15 and the rpoB/C1/C2 gene cluster are strongly transcribed in ribosome-deficient plastids: Evidence for a functioning non-chloroplast-encoded RNA polymerase. EMBO J. 12, 563-571.
29. Hildebrand, M., Hallick, R.B., Passavant, C.W., and Bourque, D.P. (1988). Trans-splicing in chloroplasts: The rps 12 loci of Nicotiana tabacum. Proc. Natl. Acad. Sci. USA 85, 372-376.
30. Huang, H.R., Rowe, C.E., Mohr, S., Jiang, Y., Lambowitz, A.M., and Perlman, P.S. (2005). The splicing of yeast mitochondrial group I and group II introns requires a DEAD-box protein with RNA chaperone function. Proc. Natl. Acad. Sci. USA 102, 163-168.
31. Ikeda, T.M., and Gray, M.W. (1999). Characterization of a DNA-binding protein implicated in transcription in wheat mitochondria. Mol. Cell. Biol. 19, 8113-8122.
32. Jenkins, B.D., and Barkan, A. (2001). Recruitment of a peptidyl-tRNA hydrolase as a facilitator of group II intron splicing in chloroplasts. EMBO J. 20, 872-879.
33. Jenkins, B.D., Kulhanek, D.J., and Barkan, A. (1997). Nuclear mutations that block group II RNA splicing in maize chloroplasts reveal several intron classes with distinct requirements for splicing factors. Plant Cell 9, 283-296.
34. Kazama, T., and Toriyama, K. (2003). A pentatricopeptide repeat-containing gene that promotes the processing of aberrant atp6 RNA of cytoplasmic male-sterile rice. FEBS Lett. 544, 99-102.
35. Kode, V., Mudd, E.A., Iamtham, S., and Day, A. (2005). The tobacco plastid accD gene is essential and is required for leaf development. Plant J. 44, 237-244.
36. Koizuka, N., Imai, R., Fujimoto, H., Hayakawa, T., Kimura, Y., Kohno-Murase, J., Sakai, T., Kawasaki, S., and Imamura, J. (2003). Genetic characterization of a pentatricopeptide repeat protein gene, orf687, that restores fertility in the cytoplasmic male-sterile Kosena radish. Plant J. 34, 407-415.
37. Koller, B., Fromm, H., Galun, E., and Edelman, M. (1987). Evidence for in vivo trans splicing of pre-mRNAs in tobacco chloroplasts. Cell 48, 111-119.
38. Kotera, E., Tasaka, M., and Shikanai, T. (2005). A pentatricopeptide repeat protein is essential for RNA editing in chloroplasts. Nature 433, 326-330.
39. Lahmy, S., Barneche, F., Derancourt, J., Filipowicz, W., Delseny, M., and Echeverria, M. (2000). A chloroplastic RNA-binding protein is a new member of the PPR family. FEBS Lett. 480, 255-260.
40. Lambowitz, A.M., and Perlman, P.S. (1990). Involvement of aminoacyl-tRNA synthetases and other proteins in group I and group II intron splicing. Trends Biochem. Sci. 15, 440-444.
41. Lown, F., Watson, A., and Purton, S. (2001). Chlamydomonas nuclear mutants that fail to assemble respiratory or photosynthetic electron transfer complexes. Biochem. Soc. Trans. 29, 452-455.
42. Lurin, C., et al. (2004). Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16, 2089-2103.
43. Maier, R.M., Neckermann, K., Igloi, G.L., and Kossei, H. (1995). Complete sequence of the maize chloroplast genome: Gene content, hotspots of divergence and fine tuning of genetic information by transcript editing. J. Mol. Biol. 251, 614-628.
44. Mancebo, R., Zhou, X., Shillinglaw, W., Henzel, W., and Macdonald, P. (2001). BSF binds specifically to the bicoid mRNA 3′ untranslated region and contributes to stabilization of bicoid mRNA. Mol. Cell. Biol. 21, 3462-3471.
45. Manthey, G.M., and McEwen, J.E. (1995). The product of the nuclear gene PET309 is required for translation of mature mRNA and stability or production of intron-containing RNAs derived from the mitochondrial COX1 locus of Saccharomyces cerevisiae. EMBO J. 14, 4031-4043.
46. McCormac, D.J., and Barkan, A. (1999). A nuclear gene in maize required for the translation of the chloroplast atpB/E mRNA. Plant Cell 11, 1709-1716.
47. Meierhoff, K., Felder, S., Nakamura, T., Bechtold, N., and Schuster, G. (2003). HCF152, an Arabidopsis RNA binding pentatricopeptide repeat protein involved in the processing of chloroplast psbB-psbT-psbH-petB-petD RNAs. Plant Cell 15, 1480-1495.
48. Merendino, L., Perron, K., Rahire, M., Howald, I., Rochaix, J.D., and Goldschmidt-Clermont, M. (2006). A novel multifunctional factor involved in trans-splicing of chloroplast introns in Chlamydomonas. Nucleic Acids Res. 34, 262-274.
49. Michel, F., and Ferat, J.L. (1995). Structure and activities of group II introns. Annu. Rev. Biochem. 64, 435-461.
50. Michel, F., Umesono, K., and Ozeki, H. (1989). Comparative and functional anatomy of group II catalytic introns - A review. Gene 82, 5-30.
51. Mili, S., and Pinol-Roma, S. (2003). LRP130, a pentatricopeptide motif protein with a noncanonical RNA-binding domain, is bound in vivo to mitochondrial and nuclear RNAs. Mol. Cell. Biol. 23, 4972-4982.
52. Mingler, M.K., Hingst, A.M., Clement, S.L., Yu, L.E., Reifur, L., and Koslowsky, D.J. (2006). Identification of pentatricopeptide repeat proteins in Trypanosoma brucei. Mol. Biochem. Parasitol. 150, 37-45.
53. Mizushima, S., and Nomura, M. (1970). Assembly mapping of 30S ribosomal proteins from E. coli. Nature 226, 1214.
54. Mohr, S., Matsuura, M., Perlman, P.S., and Lambowitz, A.M. (2006). A DEAD-box protein alone promotes group II intron splicing and reverse splicing by acting as an RNA chaperone. Proc. Natl. Acad. Sci. USA 103, 3569-3574.
55. Nakamura, T., Meierhoff, K., Westhoff, P., and Schuster, G. (2003). RNA-binding properties of HCF152, an Arabidopsis PPR protein involved in the processing of chloroplast RNA. Eur. J. Biochem. 270, 4070-4081.
56. Ostheimer, G.J., Williams-Carrier, R., Belcher, S., Osborne, E., Gierke, J., and Barkan, A. (2003). Group II intron splicing factors derived by diversification of an ancient RNA-binding domain. EMBO J. 22, 3919-3929.
57. Perron, K., Goldschmidt-Clermont, M., and Rochaix, J.D. (1999). A factor related to pseudouridine synthases is required for chloroplast group II intron trans-splicing in Chlamydomonas reinhardtii. EMBO J. 18, 6481-6490.
58. Prasad, A.M., Sivanandan, C., Resminath, R., Thakare, D.R., Bhat, S.R., and Srinivasan. (2005). Cloning and characterization of a pentatricopeptide protein encoding gene (LOJ) that is specifically expressed in lateral organ junctions in Arabidopsis thaliana. Gene 353, 67-79.
59. Rivier, C., Goldschmidt-Clermont, M., and Rochaix, J.D. (2001). Identification of an RNA-protein complex involved in chloroplast group II intron trans-splicing in Chlamydomonas reinhardtii. EMBO J. 20, 1765-1773.
60. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual. (Cold Spring Harbor. NY: Cold Spring Harbor Laboratory Press).
61. Schmitz-Linneweber, C., Williams-Carrier, R., and Barkan, A. (2005) RNA immunoprecipitation and microarray analysas show a chloroplast pentatricopeptide repeat protein to be associated with the 5′ region of mRNAs whose translation it activates. Plant Cell 17, 2791-2804.
62. Small, I., and Peeters, N. (2000). The PPR motif - A TPR-related motif prevalent in plant organellar proteins. Trends Biochem. Sci. 25, 46-47.
63. Small, I., Peeters, N., Legeai, F., and Lurin, C. (2004) Predotar: A tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics 4, 1581-1590.
64. Srivastava, A., and Schlessinger, D. (1989). Processing pathway of E. coli 16S precursor rRNA. Nucleic Acids Res. 17, 1649-1663.
65. Srivastava, A.K., and Schlessinger, D. (1990). Mechanism and regulation of bacterial ribosomal RNA processing. Annu. Rev. Microbiol. 44, 105-129.
66. Stern, D.B., Hanson, M.R., and Barkan, A. (2004). Genetics and genomics of chloroplast biogenesis: Maize as a model system. Trends Plant Sci. 9, 293-301.
67. Till, B., Schmitz-Linneweber, C., Williams-Carrier, R., and Barkan, A. (2001). CRS1 is a novel group II intron splicing factor that was derived from a domain of ancient origin. RNA 7, 1227-1238.
68. Turmel, M., Otis, C., and Lemieux, C. (2002). The chloroplast and mitochondrial genome sequences of the charophyte Chaetosphaeridium globosum: Insights into the timing of the events that restructured organelle DNAs within the green algal lineage that led to land plants. Proc. Natl. Acad. Sci. USA 99, 11275-11280.
69. Turmel, M., Otis, C., and Lemieux, C. (2005). The complete chloroplast DNA sequences of the charophycean green algae Staurastrum and Zygnema reveal that the chloroplast genome underwent extensive changes during the evolution of the Zygnematales. BMC Biol 3, 22.
70. Tzafrir, I., Pena-Muralla, R., Dickerman, A., Berg, M., Rogers, R., Hutchens, S., Sweeney, T.C., McElver, J., Aux, G., Patton, D., and Meinke, D. (2004). Identification of genes required for embryo development in Arabidopsis. Plant Physiol. 135, 1206-1220.
71. Voelker, R., and Barkan, A. (1995). Two nuclear mutations disrupt distinct pathways for targeting proteins to the chloroplast thylakoid. EMBO J. 14, 3905-3914.
72. Walbot, V., and Coe, E.H. (1979). Nuclear gene iojap conditions a programmed change to ribosome-less plastids in Zea mays. Proc. Natl. Acad. Sci. USA 76, 2760-2764.
73. Wang, Z., et al. (2006). Cytoplasmic male sterility of rice with boro II cytoplasm is caused by a cytotoxic peptide and is restored by two related PPR motif genes via distinct modes of mRNA silencing. Plant Cell 18, 676-687.
74. Williams, P.M., and Barkan, A. (2003). A chloroplast-localized PPR protein required for plastid ribosome accumulation. Plant J. 36, 675-686.
75. Xu, F., Morin, C., Mitchell, G., Ackerley, C., and Robinson, B.H. (2004). The role of the LRPPRC (leucine-rich pentatricopeptide repeat cassette) gene in cytochrome oxidase assembly: Mutation causes lowered levels of COX (cytochrome c oxidase) I and COX III mRNA. Biochem. J. 382, 331-336.
76. Yamazaki, H., Tasaka, M., and Shikanai, T. (2004). PPR motifs of the nucleus-encoded factor, PGR3, function in the selective and distinct steps of chloroplast gene expression in Arabidopsis. Plant J. 38, 152-163.