The SLO1 PPR protein is required for RNA editing at multiple sites with similar upstream sequences in Arabidopsis mitochondria

Plant Journal

Volumn 63, Issue 3, 2010, Pages 499-511

  Sung, Tzu Ying ^a   Tseng, Ching Chih ^a   Hsieh, Ming Hsiun ^a  

^a INSTITUTE OF PLANT AND MICROBIAL BIOLOGY   (Taiwan)

Author keywords

Arabidopsis; complex I; gene expression; mitochondria; PPR protein; RNA editing

Indexed keywords

ARABIDOPSIS; BANDING PATTERNS; COMPLEX I; GEL BLOT ANALYSIS; NUCLEAR GENES; OPEN READING FRAME; PENTATRICOPEPTIDE REPEAT PROTEIN; PLANT GROWTH; RNA EDITING; SEQUENCE COMPARISONS; SLOW GROWTH; STEADY-STATE LEVEL; UPSTREAM SEQUENCE; WILD TYPES;

GELS; GENE ENCODING; GENE TRANSFER; MITOCHONDRIA; PLANT LIFE EXTENSION; PLANTS (BOTANY); PROTEINS; RNA;

GENE EXPRESSION;

ARABIDOPSIS;

ARABIDOPSIS PROTEIN;

AMINO ACID SEQUENCE; ARABIDOPSIS; CHEMISTRY; GENE EXPRESSION PROFILING; GENETICS; GROWTH, DEVELOPMENT AND AGING; MITOCHONDRION; MOLECULAR GENETICS; MUTATION; PLANT GENE; RNA EDITING; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENE EXPRESSION PROFILING; GENES, PLANT; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; MUTATION; RNA EDITING; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 77954928070     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2010.04258.x     Document Type: Article

References (82)

1. Akagi, H., Nakamura, A., Yokozeki-Misono, Y., Inagaki, A., Takahashi, H., Mori, K. Fujimura, T. (2004) Positional cloning of the rice Rf-1 gene, a restorer of BT-type cytoplasmic male sterility that encodes a mitochondria-targeting PPR protein. Theor. Appl. Genet. 108, 1449 1457.
2. Andres, C., Lurin, C. Small, I.D. (2007) The multifarious roles of PPR proteins in plant mitochondrial gene expression. Physiol. Plant. 129, 14 22.
3. 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.
4. Bentolila, S., Alfonso, A.A. Hanson, M.R. (2002) A pentatricopeptide repeat-containing gene restores fertility to cytoplasmic male-sterile plants. Proc. Natl Acad. Sci. USA, 99, 10887 10892.
5. Bentolila, S., Chateigner-Boutin, A.L. Hanson, M.R. (2005) Ecotype allelic variation in C-to-U editing extent of a mitochondrial transcript identifies RNA-editing quantitative trait loci in Arabidopsis. Plant Physiol. 139, 2006 2016.
6. Bentolila, S., Elliott, L.E. Hanson, M.R. (2008) Genetic architecture of mitochondrial editing in Arabidopsis thaliana. Genetics, 178, 1693 1708.
7. Binder, S. Brennicke, A. (2003) Gene expression in plant mitochondria: transcriptional and post-transcriptional control. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358, 181 189.
8. Brown, G.G., Formanova, N., Jin, H., Wargachuk, R., Dendy, C., Patil, P., Laforest, M., Zhang, J., Cheung, W.Y. 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.
9. Cai, W., Ji, D., Peng, L., Guo, J., Ma, J., Zou, M., Lu, C. Zhang, L. (2009) LPA66 is required for editing psbF chloroplast transcripts in Arabidopsis. Plant Physiol. 150, 1260 1271.
10. Chateigner-Boutin, A.L., Ramos-Vega, M., Guevara-García, A. et al. (2008) CLB19, a pentatricopeptide repeat protein required for editing of rpoA and clpP chloroplast transcripts. Plant J. 56, 590 602.
11. Chaudhuri, S. Maliga, P. (1996) Sequences directing C to U editing of the plastid psbL mRNA are located within a 22 nucleotide segment spanning the editing site. EMBO J. 15, 5958 5964.
12. Chiu, W., Niwa, Y., Zeng, W., Hirano, T., Kobayashi, H. Sheen, J. (1996) Engineered GFP as a vital reporter in plants. Curr. Biol. 6, 325 330.
13. Clough, S.J. Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735 743.
14. Delannoy, E., Stanley, W.A., Bond, C.S. Small, I.D. (2007) Pentatricopeptide repeat (PPR) proteins as sequence-specificity factors in post-transcriptional processes in organelles. Biochem. Soc. Trans. 35, 1643 1647.
15. Desloire, S., Gherbi, H., Laloui, W. 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. Farré, J.-C., Leon, G., Jordana, X. Araya, A. (2001) Cis recognition elements in plant mitochondrion RNA editing. Mol. Cell. Biol. 21, 6731 6737.
17. Fisk, D.G., Walker, M.B. 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.
18. Giegé, P. Brennicke, A. (1999) RNA editing in Arabidopsis mitochondria effects 441 C to U changes in ORFs. Proc. Natl Acad. Sci. USA, 96, 15324 15329.
19. Giegé, P., Hoffmann, M., Binder, S. Brennicke, A. (2000) RNA degradation buffers asymmetries of transcription in Arabidopsis mitochondria. EMBO Rep. 1, 164 170.
20. Giegé, P., Sweetlove, L.J., Cognat, V. Leaver, C.J. (2005) Coordination of nuclear and mitochondrial genome expression during mitochondrial biogenesis in Arabidopsis. Plant Cell, 17, 1497 1512.
21. Gray, M.W. (1999) Evolution of organellar genomes. Curr. Opin. Genet. Dev. 9, 678 687.
22. Grohmann, L., Thieck, O., Herz, U., Schröder, W. Brennicke, A. (1994) Translation of nad9 mRNAs in mitochondria from Solanum tuberosum is restricted to completely edited transcripts. Nucleic Acids Res. 22, 3304 3311.
23. Gualberto, J.M., Bonnard, G., Lamattina, L. Grienenberger, J.M. (1991) Expression of the wheat mitochondrial nad3-rps12 transcription unit: correlation between editing and mRNA maturation. Plant Cell, 3, 1109 1120.
24. Hammani, K., Okuda, K., Tanz, S.K., Chateigner-Boutin, A.L., Shikanai, T. Small, I. (2009) A study of new Arabidopsis chloroplast RNA editing mutants reveals general features of editing factors and their target sites. Plant Cell, 21, 3686 3699.
25. Handa, H. (2003) The complete nucleotide sequence and RNA editing content of the mitochondrial genome of rapeseed (Brassica napus L.): comparative analysis of the mitochondrial genomes of rapeseed and Arabidopsis thaliana. Nucleic Acids Res. 31, 5907 5916.
26. Hashimoto, M., Endo, T., Peltier, G., Tasaka, M. Shikanai, T. (2003) A nucleus-encoded factor, CRR2, is essential for the expression of chloroplast ndhB in Arabidopsis. Plant J. 36, 541 549.
27. Hattori, M., Miyake, H. Sugita, M. (2007) A pentatricopeptide repeat protein is required for RNA processing of clpP Pre-mRNA in moss chloroplasts. J. Biol. Chem. 282, 10773 10782.
28. Hegeman, C.E., Hayes, M.L. Hanson, M.R. (2005) Substrate and cofactor requirements for RNA editing of chloroplast transcripts in Arabidopsis in vitro. Plant J. 42, 124 132.
29. Holec, S., Lange, H., Kühn, K., Alioua, M., Börner, T. Gagliardi, D. (2006) Relaxed transcription in Arabidopsis mitochondria is counterbalanced by RNA stability control mediated by polyadenylation and polynucleotide phosphorylase. Mol. Cell. Biol. 26, 2869 2876.
30. Itchoda, N., Nishizawa, S., Nagano, H., Kubo, T. Mikami, T. (2002) The sugar beet mitochondrial nad4 gene: an intron loss and its phylogenetic implication in the Caryophyllales. Theor. Appl. Genet. 104, 209 213.
31. Kazama, T. 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.
32. Kazama, T., Nakamura, T., Watanabe, M., Sugita, M. Toriyama, K. (2008) Suppression mechanism of mitochondrial ORF79 accumulation by Rf1 protein in BT-type cytoplasmic male sterile rice. Plant J. 55, 619 628.
33. Kim, S.R., Yang, J.I., Moon, S., Ryu, C.H., An, K., Kim, K.M., Yim, J. An, G. (2009) Rice OGR1 encodes a pentatricopeptide repeat-DYW protein and is essential for RNA editing in mitochondria. Plant J. 59, 738 749.
34. Kobayashi, Y., Matsuo, M., Sakamoto, K., Wakasugi, T., Yamada, K. Obokata, J. (2008) Two RNA editing sites with cis-acting elements of moderate sequence identity are recognized by an identical site-recognition protein in tobacco chloroplasts. Nucleic Acids Res. 36, 311 318.
35. Koizuka, N., Imai, R., Fujimoto, H., Hayakawa, T., Kimura, Y., Kohno-Murase, J., Sakai, T., Kawasaki, S. 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.
36. Komori, T., Ohta, S., Murai, N., Takakura, Y., Kuraya, Y., Suzuki, S., Hiei, Y., Imaseki, H. Nitta, N. (2004) Map-based cloning of a fertility restorer gene, Rf-1, in rice (Oryza sativa L.). Plant J. 37, 315 325.
37. Kotera, E., Tasaka, M. Shikanai, T. (2005) A pentatricopeptide repeat protein is essential for RNA editing in chloroplasts. Nature, 433, 326 330.
38. Kubo, T., Nishizawa, S., Sugawara, A., Itchoda, N., Estiati, A. Mikami, T. (2000) The complete nucleotide sequence of the mitochondrial genome of sugar beet (Beta vulgaris L.) reveals a novel gene for tRNA(Cys)(GCA). Nucleic Acids Res. 28, 2571 2576.
39. Lamattina, L. Grienenberger, J.M. (1991) RNA editing of the transcript coding for subunit 4 of NADH dehydrogenase in wheat mitochondria: uneven distribution of the editing sites among the four exons. Nucleic Acids Res. 19, 3275 3282.
40. Lee, B.H., Lee, H., Xiong, L. Zhu, J.K. (2002) A mitochondrial complex I defect impairs cold-regulated nuclear gene expression. Plant Cell, 14, 1235 1251.
41. Liu, Y.G., Mitsukawa, N., Oosumi, T. Whittier, R.F. (1995) Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. Plant J. 8, 457 463.
42. de Longevialle, A.F., Meyer, E.H., Andrés, C., Taylor, N.L., Lurin, C., Millar, A.H. Small, I.D. (2007) The pentatricopeptide repeat gene OTP43 is required for trans-splicing of the mitochondrial nad1 intron 1 in Arabidopsis thaliana. Plant Cell, 19, 3256 3266.
43. de Longevialle, A.F., Hendrickson, L., Taylor, N.L., Delannoy, E., Lurin, C., Badger, M., Millar, A.H. Small, I. (2008) The pentatricopeptide repeat gene OTP51 with two LAGLIDADG motifs is required for the cis-splicing of plastid ycf3 intron 2 in Arabidopsis thaliana. Plant J. 56, 157 168.
44. Lu, B. Hanson, M.R. (1994) A single homogeneous form of ATP6 protein accumulates in petunia mitochondria despite the presence of differentially edited atp6 transcripts. Plant Cell, 6, 1955 1968.
45. Lu, B. Hanson, M.R. (1996) Fully edited and partially edited nad9 transcripts differ in size and both are associated with polysomes in potato mitochondria. Nucleic Acids Res. 24, 1369 1374.
46. Lu, B., Wilson, R.K., Phreaner, C.G., Mulligan, R.M. Hanson, M.R. (1996) Protein polymorphism generated by differential RNA editing of a plant mitochondrial rps12 gene. Mol. Cell. Biol. 16, 1543 1549.
47. Lurin, C., Andres, C., Aubourg, S. et al. (2004) Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell, 16, 2089 2103.
48. Meierhoff, K., Felder, S., Nakamura, T., Bechtold, N. 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.
49. van der Merwe, J.A., Takenaka, M., Neuwirt, J., Verbitskiy, D. Brennicke, A. (2006) RNA editing sites in plant mitochondria can share cis-elements. FEBS Lett. 580, 268 272.
50. Meyer, E.H., Tomaz, T., Carroll, A.J., Estavillo, G., Delannoy, E., Tanz, S.K., Small, I.D., Pogson, B.J. Millar, A.H. (2009) Remodeled respiration in ndufs4 with low phosphorylation efficiency suppresses Arabidopsis germination and growth and alters control of metabolism at night. Plant Physiol. 151, 603 619.
51. Millar, A.H., Heazlewood, J.L., Kristensen, B.K., Braun, H. Moller, I.M. (2005) The plant mitochondrial proteome. Trends Plant Sci. 10, 36 43.
52. Miyamoto, T., Obokata, J. 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.
53. Nakamura, T., Meierhoff, K., Westhoff, P. 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.
54. Neuwirt, J., Takenaka, M., van der Merwe, J.A. Brennicke, A. (2005) An in vitro RNA editing system from cauliflower mitochondria: editing site recognition parameters can vary in different plant species. RNA, 11, 1563 1570.
55. Notsu, Y., Masood, S., Nishikawa, T., Kubo, N., Akiduki, G., Nakazono, M., Hirai, A. Kadowaki, K. (2002) The complete sequence of the rice (Oryza sativa L.) mitochondrial genome: frequent DNA sequence acquisition and loss during the evolution of flowering plants. Mol. Genet. Genomics, 268, 434 445.
56. Okuda, K., Myouga, F., Motohashi, R., Shinozaki, K. Shikanai, T. (2007) Conserved domain structure of pentatricopeptide repeat proteins involved in chloroplast RNA editing. Proc. Natl Acad. Sci. USA, 104, 8178 8183.
57. Okuda, K., Habata, Y., Kobayashi, Y. Shikanai, T. (2008) Amino acid sequence variations in Nicotiana CRR4 orthologs determine the species-specific efficiency of RNA editing in plastids. Nucleic Acids Res. 36, 6155 6164.
58. Okuda, K., Chateigner-Boutin, A.L., Nakamura, T., Delannoy, E., Sugita, M., Myouga, F., Motohashi, R., Shinozaki, K., Small, I. Shikanai, T. (2009) Pentatricopeptide repeat proteins with the DYW motif have distinct molecular functions in RNA editing and RNA cleavage in Arabidopsis chloroplasts. Plant Cell, 21, 146 156.
59. O'Toole, N., Hattori, M., Andres, C., Iida, K., Lurin, C., Schmitz-Linneweber, C., Sugita, M. Small, I. (2008) On the expansion of the pentatricopeptide repeat gene family in plants. Mol. Biol. Evol. 25, 1120 1128.
60. Pfalz, J., Liere, K., Kandlbinder, A., Dietz, K.J. Oelmüller, R. (2006) Ptac2, -6, and -12 are components of the transcriptionally active plastid chromosome that are required for plastid gene expression. Plant Cell, 18, 176 197.
61. Pfalz, J., Bayraktar, O.A., Prikryl, J. Barkan, A. (2009) Site-specific binding of a PPR protein defines and stabilizes 5′ and 3′ mRNA termini in chloroplasts. EMBO J. 28, 2042 2052.
62. Phreaner, C.G., Williams, M.A. Mulligan, R.M. (1996) Incomplete editing of rps12 transcripts results in the synthesis of polymorphic polypeptides in plant mitochondria. Plant Cell, 8, 107 117.
63. Robbins, J.C., Heller, W.P. Hanson, M.R. (2009) A comparative genomics approach identifies a PPR-DYW protein that is essential for C-to-U editing of the Arabidopsis chloroplast accD transcript. RNA, 15, 1142 1153.
64. Salone, V., Rüdinger, M., Polsakiewicz, M., Hoffmann, B., Groth-Malonek, M., Szurek, B., Small, I., Knoop, V. Lurin, C. (2007) A hypothesis on the identification of the editing enzyme in plant organelles. FEBS Lett. 581, 4132 4138.
65. Schmitz-Linneweber, C. Small, I. (2008) Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci. 13, 663 670.
66. Schmitz-Linneweber, C., Williams-Carrier, R. Barkan, A. (2005) RNA immunoprecipitation and microarray analysis show a chloroplast pentatricopeptide repeat protein to be associated with the 5′ region of mRNAs whose translation it activates. Plant Cell, 17, 2791 2804.
67. 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.
68. Shikanai, T. (2006) RNA editing in plant organelles: machinery, physiological function and evolution. Cell. Mol. Life Sci. 63, 698 708.
69. Small, I.D. Peeters, N. (2000) The PPR motif - a TPR-related motif prevalent in plant organellar proteins. Trends Biochem. Sci. 25, 46 47.
70. Takenaka, M. (2010) MEF9, an E-subclass pentatricopeptide repeat protein, is required for an RNA editing event in the nad7 transcript in mitochondria of Arabidopsis. Plant Physiol. 152, 939 947.
71. Takenaka, M., Verbitskiy, D., van der Merwe, J.A., Zehrmann, A. Brennicke, A. (2008) The process of RNA editing in plant mitochondria. Mitochondrion, 8, 35 46.
72. Tang, J., Kobayashi, K., Suzuki, M., Matsumoto, S. Muranaka, T. (2010) The mitochondrial PPR protein LOVASTATIN INSENSITIVE 1 plays regulatory roles in cytosolic and plastidial isoprenoid biosynthesis through RNA editing. Plant J. 61, 456 466.
73. Tseng, C.C., Sung, T.Y., Li, Y.C., Hsu, S.J., Lin, C.L. Hsieh, M.H. (2010) Editing of accD and ndhF chloroplast transcripts is partially affected in the Arabidopsis vanilla cream1 mutant. Plant Mol. Biol. 73, 309 323.
74. Unseld, M., Marienfeld, J.R., Brandt, P. Brennicke, A. (1997) The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366 924 nucleotides. Nat. Genet. 15, 57 61.
75. Verbitskiy, D., Zehrmann, A., van der Merwe, J.A., Brennicke, A. Takenaka, M. (2010) The PPR-protein encoded by the LOVASTATIN INSENSITIVE 1 gene is involved in RNA editing at three sites in mitochondria of Arabidopsis thaliana. Plant J. 61, 446 455.
76. Wang, Z., Zou, Y., Li, X. 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.
77. Williams, P.M. Barkan, A. (2003) A chloroplast-localized PPR protein required for plastid ribosome accumulation. Plant J. 36, 675 686.
78. Williams, M.A., Tallakson, W.A., Phreaner, C.G. Mulligan, R.M. (1998) Editing and translation of ribosomal protein S13 transcripts: unedited translation products are not detectable in maize mitochondria. Curr. Genet. 34, 221 226.
79. Yamazaki, H., Tasaka, M. 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.
80. Yu, Q.B., Jiang, Y., Chong, K. Yang, Z.N. (2009) AtECB2, a pentatricopeptide repeat protein, is required for chloroplast transcript accD RNA editing and early chloroplast biogenesis in Arabidopsis thaliana. Plant J. 59, 1011 1023.
81. Zehrmann, A., Verbitskiy, D., van der Merwe, J.A., Brennicke, A. Takenaka, M. (2009) A DYW domain-containing pentatricopeptide repeat protein is required for RNA editing at multiple sites in mitochondria of Arabidopsis thaliana. Plant Cell, 21, 558 567.
82. Zhou, W., Cheng, Y., Yap, A., Chateigner-Boutin, A.L., Delannoy, E., Hammani, K., Small, I. Huang, J. (2009) The Arabidopsis gene YS1 encoding a DYW protein is required for editing of rpoB transcripts and the rapid development of chloroplasts during early growth. Plant J. 58, 82 96.