Genome-wide analysis of arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis

Plant Cell

Volumn 16, Issue 8, 2004, Pages 2089-2103

  Lurin, Claire ^a   Andrés, Charles ^a   Aubourg, Sébastien ^a   Bellaoui, Mohammed ^a   Bitton, Frédérique ^a   Bruyère, Clémence ^a   Caboche, Michel ^a   Debast, Cédrig ^b   Gualberto, José ^c   Hoffmann, Beate ^a   Lecharny, Alain ^a   Le Ret, Monique ^c   Martin Magniette, Marie Laure ^a,b   Mireau, Hakim ^b   Peeters, Nemo ^b,d   Renou, Jean Pierre ^a   Szurek, Boris ^a   Taconnat, Ludivine ^a   Small, Ian ^a  

^a INSTITUTE OF PLANT SCIENCES PARIS SACLAY IPS2   (France)

^b CEMAGREF   (France)

^c INST DE BIOL MOLEC DES PLANTES   (France)

^d LABORATOIRE DES INTERACTIONS PLANTES MICROORGANISMES LIPM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DATA REDUCTION; FLUORESCENCE; GENES; INFORMATION ANALYSIS; RNA;

ORGANELLE BIOGENESIS; PUTATIVE FUNCTIONS;

PROTEINS;

DATA PROCESSING; FLUORESCENCE; GENES; PLASTIDS; PROTEINS;

ANIMALIA; ARABIDOPSIS; ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS); EMBRYOPHYTA; INSERTION SEQUENCES;

EID: 4043172772     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.104.022236     Document Type: Article

References (71)

1. Akashi, K., Grandjean, O., and Small, I. (1998). Potential dual targeting of an Arabidopsis archaebacterial-like histidyl-tRNA synthetase to mitochondria and chloroplasts. FEBS Lett. 431, 39-44.
2. Alonso, J.M., et al. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301, 653-657.
3. Arabidopsis Genome Initiative. (2000). Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796-815.
4. Aubourg, S., Boudet, N., Kreis, M., and Lecharny, A. (2000). In Arabidopsis thaliana, 1% of the genome codes for a novel protein family unique to plants. Plant Mol. Biol. 42, 603-613.
5. Barkan, A., and Goldschmidt-Clermont, M. (2000). Participation of nuclear genes in chloroplast gene expression. Biochimie 82, 559-572.
6. Bentolila, S., Alfonso, A.A., and Hanson, M.R. (2002). A pentatrico-peptide repeat-containing gene restores fertility to cytoplasmic male-sterile plants. Proc. Natl. Acad. Sci. USA 99, 10887-10892.
7. Brown, G.G., Formanova, H., Jin, H., Wargachuk, R., Dendy, C., Patil, P., Laforest, M., Zhang, J., Cheung, W.Y., and Landry, B.S. (2003). The radish Rfo restorer gene of Ogura cytoplasmic male sterility encodes a protein with multiple pentatricopeptide repeats. Plant J. 35, 262-272.
8. Budziszewski, G.J., et al. (2001). Arabidopsis genes essential for seedling viability: Isolation of insertional mutants and molecular cloning. Genetics 159, 1765-1778.
9. Chateigner-Boutin, A.L., and Hanson, M.R. (2002). Cross-competition in transgenic chloroplasts expressing single editing sites reveals shared cis elements. Mol. Cell. Biol. 22, 8448-8456.
10. Chateigner-Boutin, A.L., and Hanson, M.R. (2003). Developmental co-variation of RNA editing extent of plastid editing sites exhibiting similar cis-elements. Nucleic Acids Res. 31, 2586-2594.
11. Chupeau, Y., Bourgin, J.P., Missonier, C., Dorion, N., and Morel, G. (1974). Préparation et culture de protoplastes de divers Nicotiana. C. R. Acad. Sci. Paris 278, 1565-1568.
12. 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.
13. Costanzo, M.C., Bonnefoy, N., Williams, E.H., Clark-Walker, G.D., and Fox, T.D. (2000). Highly diverged homologs of Saccharomyces cerevisiae mitochondrial mRNA-specific translational activators have orthologous functions in other budding yeasts. Genetics 154, 999-1012.
14. 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.
15. Eddy, S.R. (1998). Profile hidden Markov models. Bioinformatics 14, 755-763.
16. Edwards, T.A., Wilkinson, B.D., Wharton, R.P., and Aggarwal, A.K. (2003). Model of the brain tumor-Pumilio translation repressor complex. Genes Dev. 17, 2508-2513.
17. 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.
18. 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.
19. Ge, Y., Dudoit, S., and Speed, T.P. (2003). Resampling-based multiple testing for microarray data analysis. TEST 12, 1-44.
20. Giege, P., and Brennicke, A. (1999). RNA editing in Arabidopsis mitochondria effects 441 C to U changes in ORFs. Proc. Natl. Acad. Sci. USA 96, 15324-15329.
21. Giege, P., and Brennicke, A. (2001). From gene to protein in higher plant mitochondria. C. R. Acad. Sci. III 324, 209-217.
22. Hannaert, V., Saavedra, E., Duffieux, F., Szikora, J.P., Rigden, D.J., Michels, P.A., and Opperdoes, F.R. (2003). Plant-like traits associated with metabolism of Trypanosoma parasites. Proc. Natl. Acad. Sci. USA 100, 1067-1071.
23. Hashimoto, M., Tsuyoshi, E., 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.
24. Heazlewood, J.L., Tonti-Filippini, J.S., Gout, A.M., Day, D.A., Whelan, J., and Millar, A.H. (2004). Experimental analysis of the Arabidopsis mitochondrial proteome highlights signaling and regulatory components, provides assessment of targeting prediction programs, and indicates plant-specific mitochondrial proteins. Plant Cell 16, 241-256.
25. Hellens, R.P., Edwards, E.A., Leyland, N.R., Bean, S., and Mullineaux, P.M. (2000). pGreen: A versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation. Plant Mol. Biol. 42, 819-832.
26. Hilson, P., et al. (2004). Versatile gene-specific sequence tags for Arabidopsis functional genomics: Transcript profiling and reverse genetics applications. Genome Res., in press.
27. Hirose, T., Kusumegi, T., Tsudzuki, T., and Sugiura, M. (1999). RNA editing sites in tobacco chloroplast transcripts: Editing as a possible regulator of chloroplast RNA polymerase activity. Mol. Gen. Genet. 262, 462-467.
28. 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.
29. Jelesko, J.G., Harper, R., Furuya, M., and Gruissem, W. (1999). Rare germinal unequal crossing-over leading to recombinant gene formation and gene duplication in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 95, 10302-10307.
30. 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.
31. Kleffmann, T., Russenberger, D., von Zychlinski, A., Christopher, W., Sjolander, K., Gruissem, W., and Baginsky, S. (2004). The Arabidopsis thaliana chloroplast proteome reveals pathway abundance and novel protein functions. Curr. Biol. 14, 354-362.
32. 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.
33. Komori, T., Ohta, S., Murai, N., Takakura, Y., Kuraya, Y., Suzuki, S., Hiei, Y., Imaseki, H., and Nitta, N. (2004). Map-based cloning of a fertility restorer gene, Rf-1, in rice (Oryza sativa L.). Plant J. 37, 315-325.
34. 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.
35. Lecharny, A., Boudet, N., Gy, I., Aubourg, S., and Kreis, M. (2003). Introns in, introns out in plant gene families: A genomic approach of the dynamics of gene structure. J. Struct. Funct. Genomics 3, 111-116.
36. Li, Y., Rosso, M.G., Strizhov, H., Viehoever, P., and Weisshaar, B. (2003). GABI-Kat SimpleSearch: A flanking sequence tag (FST) database for the identification of T-DNA insertion mutants in Arabidopsis thaliana. Bioinformatics 19, 1441-1442.
37. Liu, L., Amy, V., Liu, G., and McKeehan, W.L. (2002). Novel complex integrating mitochondria and the microtubular cytoskeleton with chromosome remodeling and tumor suppressor RASSF1 deduced by in silico homology analysis, interaction cloning in yeast, and colocalization in cultured cells. In Vitro Cell. Dev. Biol. Anim. 38, 582-594.
38. Liu, L., and McKeehan, W.L. (2002). Sequence analysis of LRPPRC and its SEC1 domain interaction partners suggests roles in cytoskeletal organization, vesicular trafficking, nucleocytosolic shuttling, and chromosome activity. Genomics 79, 124-136.
39. Lown, F.J., Watson, A.T., and Purton, S. (2001). Chlamydomonas nuclear mutants that fail to assemble respiratory or photosynthetic electron transfer complexes. Biochem. Soc. Trans. 29, 452-455.
40. Mancebo, R., Zhou, X., Shillinglaw, W., Henzel, W., and Macdonald, P.M. (2001). BSF binds specifically to the bicoid mRNA 3′ untranslated region and contributes to stabilization of bicoid mRNA. Mol. Cell. Biol. 21, 3462-3471.
41. 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.
42. Manthey, G.M., Przybyla-Zawislak, B.D., and McEwen, J.E. (1998). The Saccharomyces cerevisiae Pet309 protein is embedded in the mitochondrial inner membrane. Eur. J. Biochem. 255, 156-161.
43. Martin, W., and Borst, P. (2003). Secondary loss of chloroplasts in trypanosomes. Proc. Natl. Acad. Sci. USA 100, 765-767.
44. Matsuzaki, M., et al. (2004). Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428, 653-657.
45. 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.
46. Meyers, B.C., Kozik, A., Griego, A., Kuang, H., and Michelmore, R.W. (2003). Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15, 809-834.
47. Michelmore, R.W., and Meyers, B.C. (1998). Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res. 8, 1113-1130.
48. 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.
49. Miyamoto, T., Obokata, J., and Sugiura, M. (2002). Recognition of RNA editing sites is directed by unique proteins in chloroplasts: Biochemical identification of cis-acting elements and trans-acting factors involved in RNA editing in tobacco and pea chloroplasts. Mol. Cell. Biol. 22, 6726-6734.
50. Miyamoto, T., Obokata, J., and Sugiura, M. (2004). A site-specific factor interacts directly with its cognate RNA editing site in chloroplast transcripts. Proc. Natl. Acad. Sci. USA 101, 48-52.
51. Mootha, V.K., et al. (2003). Identification of a gene causing human cytochrome c oxidase deficiency by integrative genomics. Proc. Natl. Acad. Sci. USA 100, 605-610.
52. 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.
53. Peeters, N.M., Chapron, A., Giritch, A., Grandjean, O., Lancelin, D., Lhomme, T., Vivrel, A., and Small, I. (2000). Duplication and quadruplicate of Arabidopsis thaliana cysteinyl- and asparaginyl-tRNA synthetase genes of organellar origin. J. Mol. Evol. 50, 413-423.
54. Puskas, L.G., Zvara, A., Hackler, L., Jr., and Van Hummelen, P. (2002). RNA amplification results in reproducible microarray data with slight ratio bias. Biotechniques 32, 1330-1334, 1336, 1338, 1340.
55. Rost, B., and Liu, J. (2003). The PredictProtein server. Nucleic Acids Res. 31, 3300-3304.
56. Salanoubat, M., et al. (2002). Genome sequence of the plant pathogen Ralstonia solanacearum. Nature 415, 497-502.
57. Samson, F., Brunaud, V., Balzergue, S., Dubreucq, B., Lepiniec, L., Pelletier, G., Caboche, M., and Lecharny, A. (2002). FLAGdb/FST: A database of mapped flanking insertion sites (FSTs) of Arabidopsis thaliana T-DNA transformants. Nucleic Acids Res, 30, 94-97.
58. Samson, F., Brunaud, V., Duchene, S., De Oliveira, Y., Caboche, M., Lecharny, A., and Aubourg, S. (2004). FLAGdb++: A database for the functional analysis of the Arabidopsis genome. Nucleic Acids Res. 32 (Database issue), D347-D350.
59. 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.
60. Small, I.D., and Peeters, N. (2000). The PPR motif - A TPR-related motif prevalent in plant organellar proteins. Trends Biochem. Sci. 25, 46-47.
61. Sonoda, J., and Wharton, R.P. (1999). Recruitment of Nanos to hunchback mRNA by Pumilio. Genes Dev. 13, 2704-2712.
62. Steinhauser, S., Beckert, S., Capesius, I., Malek, O., and Knoop, V. (1999). Plant mitochondrial RNA editing. J. Mol. Evol. 48, 303-312.
63. Thompson, J.D., Higgins, D.G., and Gibson, T.J. (1994). CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680.
64. Tsuchiya, N., Fukuda, H., Sugimura, T., Nagao, M., and Nakagama, H. (2002). LRP130, a protein containing nine pentatricopeptide repeat motifs, interacts with a single-stranded cytosine-rich sequence of mouse hypervariable minisatellite Pc-1. Eur. J. Biochem. 269, 2927-2933.
65. Tsudzuki, T., Wakasugi, T., and Sugiura, M. (2001). Comparative analysis of RNA editing sites in higher plant chloroplasts. J. Mol. Evol. 53, 327-332.
66. Tzafrir, I., Dickerman, A., Brazhnik, O., Nguyen, Q., McElver, J., Frye, C., Patton, D., and Meinke, D. (2003). The Arabidopsis SeedGenes project. Nucleic Acids Res. 31, 90-93.
67. Vermel, M., Guermann, B., Delage, L., Grienenberger, J.M., Marechal-Drouard, L., and Gualberto, J.M. (2002). A family of RRM-type RNA-binding proteins specific to plant mitochondria. Proc. Natl. Acad. Sci. USA 99, 5866-5871.
68. Williams, P.M., and Barkan, A. (2003). A chloroplast-localized PPR protein required for plastid ribosome accumulation. Plant J. 36, 675-686.
69. 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.
70. Yang, Y.H., Dudoit, S., Luu, P., Lin, D.M., Peng, V., Ngai, J., and Speed, T.P. (2002). Normalization for cDNA microarray data: A robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res. 30, e15.
71. Yang, Y.H., and Thorne, N.P. (2003). Normalization for two-colour cDNA microarray data. In Science and Statistics: A Festschrift for Terry Speed, D.R. Goldstein, ed (Bethesda, MD: IMS), pp. 403-418.