A pentatricopeptide repeat protein acts as a site-specificity factor at multiple RNA editing sites with unrelated cis-acting elements in plastids

Nucleic Acids Research

Volumn 40, Issue 11, 2012, Pages 5052-5064

  Okuda, Kenji ^a   Shikanai, Toshiharu ^b  

^a CHUO UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

PENTATRICOPEPTIDE REPEAT PROTEIN; RECOMBINANT CHLORORESPIRATORY REDUCTION 22; RECOMBINANT OTP82 PROTEIN; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; PLASTID; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION; PROTEIN RNA BINDING; RNA EDITING;

BINDING SITES; PLANT PROTEINS; PLASTIDS; RECOMBINANT FUSION PROTEINS; RNA; RNA EDITING; RNA-BINDING PROTEINS;

EID: 84862224565     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks164     Document Type: Article

References (52)

1. Schmitz-Linneweber, C. and Small, I. (2008) Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci., 13, 663-670.
2. Lurin, C., André s, C., Aubourg, S., Bellaoui, M., Bitton, F., Bruyè re, C., Caboche, M., Debast, C., Gualberto, J., Hoffmann, B. et al. (2004) Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell, 16, 2089-2103. (Pubitemid 39059730)
3. Delannoy, E., Stanley, W.A., Bond, C.S. and Small, I.D. (2007) Pentatricopeptide repeat (PPR) proteins as sequence-specificity factors in post-transcriptional processes in organelles. Biochem. Soc. Trans., 35, 1643-1647.
4. Prikryl, J., Rojas, M., Schuster, G. and Barkan, A. (2011) Mechanism of RNA stabilization and translational activation by a pentatricopeptide repeat protein. Proc. Natl Acad. Sci. USA, 108, 415-420.
5. O'Toole, N., Hattori, M., Andres, C., Iida, K., Lurin, C., Schmitz-Linneweber, C., Sugita, M. and Small, I. (2008) On the expansion of the pentatricopeptide repeat gene family in plants. Mol. Biol. Evol., 25, 1120-1128.
6. Knoop, V. and Rüdinger, M. (2010) DYW-type PPR proteins in a heterolobosean protist: plant RNA editing factors involved in an ancient horizontal gene transfer? FEBS Lett., 584, 4287-4291.
7. Salone, V., Rüdinger, M., Polsakiewicz, M., Hoffmann, B., Groth-Malonek, M., Szurek, B., Small, I., Knoop, V. and Lurin, C. (2007) A hypothesis on the identification of the editing enzyme in plant organelles. FEBS Lett., 581, 4132-4138. (Pubitemid 47301862)
8. Rüdinger, M., Polsakiewicz, M. and Knoop, V. (2008) Organellar RNA editing and plant-specific extensions of pentatricopeptide repeat proteins in jungermanniid but not in marchantiid liverworts. Mol. Biol. Evol., 25, 1405-1414. (Pubitemid 351882014)
9. Shikanai, T. (2006) RNA editing in plant organelles: machinery, physiological function and evolution. Cell Mol. Life Sci., 63, 698-708.
10. Chateigner-Boutin, A.L. and Small, I. (2010) Plant RNA editing. RNA Biol., 7, 213-219.
11. Chateigner-Boutin, A.L. and Small, I. (2007) A rapid high-throughput method for the detection and quantification of RNA editing based on high-resolution melting of amplicons. Nucleic Acids Res., 35, e114.
12. Giegé, 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. (Pubitemid 30019810)
13. Bentolila, S., Elliott, L.E. and Hanson, M.R. (2008) Genetic architecture of mitochondrial editing in Arabidopsis thaliana. Genetics, 178, 1693-1708.
14. Zehrmann, A., Van der Merwe, J.A., Verbitskiy, D., Brennicke, A. and Takenaka, M. (2008) Seven large variations in the extent of RNA editing in plant mitochondria between three ecotypes of Arabidopsis thaliana. Mitochondrion, 8, 319-327.
15. Chaudhuri, S. and 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. (Pubitemid 26375517)
16. 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.
17. Takenaka, M., Neuwirt, J. and Brennicke, A. (2004) Complex ciselements determine an RNA editing site in pea mitchoncdria. Nucleic Acids Res., 32, 4137-4144. (Pubitemid 39232286)
18. Kotera, E., Tasaka, M. and Shikanai, T. (2005) A pentatricopeptide repeat protein is essential for RNA editing in chloroplasts. Nature, 433, 326-330.
19. Okuda, K., Nakamura, T., Sugita, M., Shimizu, T. and Shikanai, T. (2006) A pentatricopeptide repeat protein is a site recognition factor in chloroplast RNA editing. J. Biol. Chem., 281, 37661-37667. (Pubitemid 46042069)
20. Hammani, K., Okuda, K., Tanz, S.K., Chateigner-Boutin, A.L., Shikanai, T. and 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.
21. Zehrmann, A., Verbitskiy, D., Van der Merwe, J.A., Brennicke, A. and Takenaka, M. (2009) A DYW domain-containing pentatricopeptide repeat proteins is required for RNA editing at multiple sites in mitochondria of Arabidopsis thaliana. Plant Cell, 21, 558-567.
22. Verbitsliy, D., Zehrmann, A., Van der Merwe, J.A., Brennicke, A. and 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.
23. Verbitskiy, D., Härtel, B., Zehrmann, A., Brennicke, A. and Takenaka, M. (2011) The DYW-E-PPR protein MEF14 is required for RNA editing at site matR-1895 in mitochondria of Arabidopsis thaliana. FEBS Lett., 585, 700-704.
24. 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.
25. Takenaka, M., Verbitskiy, D., Zehrmann, A. and Brennicke, A. (2010) Reverse genetic screening identifies five E-class PPR proteins involved in RNA editing in mitochondria of Arabidopsis thaliana. J. Biol. Chem., 285, 22122-22129.
26. Bentolila, S., Knight, W. and Hanson, M. (2010) Natural variation in Arabidospis leads to the identification of REME1, a pentatricopeptide repeat-DYW protein controlling the editing of mitochondrial transcripts. Plant Physiol., 154, 1966-1982.
27. Ohtani, S., Ichinose, M., Tasaki, E., Aoki, Y., Komura, Y. and Sugita, M. (2010) Targeted gene disruption identifies three PPR-DYW proteins involved in RNA editing for five editing sites of the moss mitochondrial transcripts. Plant Cell Physiol., 51, 1942-1949.
28. Tasaki, E., Hattori, M. and Sugita, M. (2010) The moss pentatricopeptide repeat protein with a DYW domain is responsible for RNA editing of mitochondrial ccmFc transcript. Plant J., 62, 560-570.
29. Kim, S.R., Yang, J.I., Moon, S., Ryu, C.H., An, K., Kim, K.M., Yim, J. and An, G. (2009) Rice OGR1 encodes a pentatricopeptide repeat-DYW protein and is essential for RNA editing in mitochondria. Plant J., 59, 738-749.
30. Hammani, K., des Francs-Small, C.C., Takenaka, M., Tanz, S.K., Okuda, K., Shikanai, T., Brennicke, A. and Small, I. (2011) The pentatricopeptide repeat protein OTP87 is essential for RNA editing of nad7 and atp1 transcripts in Arabidopsis mitochondria. J. Biol. Chem., 286, 21361-21371.
31. 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. (Pubitemid 35397161)
32. 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. (Pubitemid 37441743)
33. Kobayashi, Y., Matsuo, M., Sakamoto, K., Wakasugi, T., Yamada, K. and Obokata, J. (2007) 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.
34. Heller, W.P., Hayes, M.L. and Hanson, M.R. (2008) Cross-competition in editing of chloroplast RNA transcripts in vitro implicates sharing of trans-factors between different C targets. J. Biol. Chem., 283, 7314-7319.
35. Okuda, K., Chateigner-Boutin, A., Nakamura, T., Delannoy, E., Sugita, M., Myouga, F., Motohashi, R., Shinozaki, K., Small, I. and 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.
36. Schmitz-Linneweber, C., Williams-Carrier, R. and Barkan, A. (2005) RNA immunoprecipitation and microarray analysis show a chloroplast Pentatricopeptide repeat protein to be associated with the 50 region of mRNAs whose translation it activates. Plant Cell, 17, 2791-2804.
37. Pfalz, J., Bayraktar, O.A., Prikryl, J. and Barkan, A. (2009) Site-specific binding of a PPR protein defines and stabilizes 50 and 30 mRNA termini in chloroplasts. EMBO J., 28, 2042-2052.
38. Cai, W., Okuda, K., Peng, L. and Shikanai, T. (2011) PROTON GRADIENT REGULATION 3 recognizes multiple targets with limited similarity and mediates translation and RNA stabilization in plastids. Plant J., 67, 318-327.
39. Navaratnam, N., Fujino, T., Bayliss, J., Jarmuz, A., How, A., Richardson, N., Somasekaram, A., Bhattacharya, S., Carter, C. and Scott, J. (1998) Escherichia coli cytidine deaminase provides a molecular model for ApoB RNA editing and a mechanism for RNA substrate recognition. J. Mol. Biol., 275, 695-714. (Pubitemid 28064211)
40. Sambrrok, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Clonign: A laboratory manual, 2nd edn. Cold Spring Habor Press, Cold Spring Harbor.
41. Okuda, K., Hammani, K., Tanz, S.K., Peng, L., Fukao, Y., Myouga, F., Motohashi, R., Shinozaki, K., Small, I. and Shikanai, T. (2010) The pentatricopeptide repeat protein OTP82 is required for RNA editing of plastid ndhB and ndhG transcripts. Plant J., 61, 339-349.
42. Williams-Carrier, R., Kroeger, T. and Barkan, A. (2008) Sequence-specific binding of a chloroplast pentatricopeptide repeat protein to its native group II intron ligand. RNA, 14, 1930-1941.
43. Bock, R., Hermann, M. and Kössel, H. (1996) In vivo dissection of cis-acting determinants for plastid RNA editing. EMBO J., 15, 5052-5059. (Pubitemid 26315815)
44. Reed, M.L., Peeters, N.M. and Hanson, M.R. (2001) A single alteration 20 nt 50 to an editing target inhibits chloroplast RNA editing in vivo. Nucleic Acids Res., 29, 1507-1513. (Pubitemid 32288498)
45. Hirose, T. and Sugiura, M. (2001) Involvement of a site-specific trans-acting factor and a common RNA-binding protein in the editing of chloroplast mRNAs: development of a chloroplast in vitro RNA editing system. EMBO J., 20, 1144-1152. (Pubitemid 32186804)
46. 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. (Pubitemid 38084201)
47. Okuda, K., Myouga, F., Motohashi, R., Shinozaki, K. and Shikanai, T. (2007) Conserved domain structure of pentatricopeptide repeat proteins involved in chloroplast RNA editing. Proc. Natl Acad. Sci. USA, 104, 8178-8183. (Pubitemid 47185895)
48. Fujii, S., Bond, C.S. and Small, I.D. (2011) Selection patterns on restorer-like genes reveal a conflict between nuclear and mitochondrial genomes throughout angiosperm evolution. Proc. Natl Acad. Sci. USA, 108, 1723-1728.
49. Robbins, J.C., Heller, W.P. and 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.
50. Yu, Q.B., Jiang, Y., Chong, K. and 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.
51. Tseng, C.C., Sung, T.Y., Li, Y.C., Hsu, S.J., Lin, C.L. and 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.
52. Hattori, M. and Sugita, M. (2009) A moss pentatricopeptide repeat protein binds to the 30 end of plastid clpP pre-mRNA and assists with mRNA maturation. FEBS J., 276, 5860-5869.