Science China Life Sciences

, Volume 61, Issue 2, pp 162–169 | Cite as

RNA editing machinery in plant organelles

  • Junjie Yan
  • Qunxia Zhang
  • Ping Yin


RNA editing is a type of post-transcriptional modification that includes nucleotide insertion/deletion or conversion. Different categories of RNA editing have been widely observed in distinct RNAs from divergent organisms. In flowering plants, RNA editing usually alters cytidine to uridine in plastids and mitochondria, playing important roles in various plant developmental processes, including organelle biogenesis, adaptation to environmental changes, and signal transduction. Numerous studies have demonstrated that a number of factors are involved in plant RNA editing, such as pentatricopeptide repeat (PPR) proteins, multiple organelle RNA editing factors (MORF, also known as RIP), organelle RNA recognition motif (ORRM) containing proteins, protoporphyrinogen IX oxidase 1 (PPO1) and organelle zinc finger 1 (OZ1). These factors play diverse roles in plant RNA editing due to their distinct characteristics. In this review, we discuss the functional roles of the individual editing factors and their associations in plant RNA editing.


RNA editing editosome plant organelles 


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This work was supported by the Ministry of Science and Technology (2015CB910900), the Fok Ying-Tong Education Foundation (151021), the Fundamental Research Funds for the Central Universities (2017PY031 to Ping Yin), China Postdoctoral Science Foundation (2015M572163, 2017T100561) and National Natural Science Foundation of China (31700203 to Junjie Yan).


  1. Barkan, A., and Small, I. (2014). Pentatricopeptide repeat proteins in plants. Annu Rev Plant Biol 65, 415–442.CrossRefPubMedGoogle Scholar
  2. Bayer-Császár, E., Haag, S., Jörg, A., Glass, F., Härtel, B., Obata, T., Meyer, E.H., Brennicke, A., and Takenaka, M. (2017). The conserved domain in MORF proteins has distinct affinities to the PPR and E elements in PPR RNA editing factors. Biochim Biophys Acta 1860, 813–828.CrossRefPubMedGoogle Scholar
  3. Bentolila, S., Heller, W.P., Sun, T., Babina, A.M., Friso, G., van Wijk, K.J., and Hanson, M.R. (2012). RIP1, a member of an Arabidopsis protein family, interacts with the protein RARE1 and broadly affects RNA editing. Proc Natl Acad Sci USA 109, E1453–E1461.CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bentolila, S., Oh, J., Hanson, M.R., and Bukowski, R. (2013). Comprehensive high-resolution analysis of the role of an Arabidopsis gene family in RNA editing. PLoS Genet 9, e1003584.CrossRefPubMedPubMedCentralGoogle Scholar
  5. Boussardon, C., Avon, A., Kindgren, P., Bond, C.S., Challenor, M., Lurin, C., and Small, I. (2014). The cytidine deaminase signature HxE(x)nCxxC of DYW1 binds zinc and is necessary for RNA editing of ndhD-1. New Phytol 203, 1090–1095.CrossRefPubMedGoogle Scholar
  6. Boussardon, C., Salone, V., Avon, A., Berthomé, R., Hammani, K., Okuda, K., Shikanai, T., Small, I., and Lurin, C. (2012). Two interacting proteins are necessary for the editing of the NdhD-1 site in Arabidopsis plastids. Plant Cell 24, 3684–3694.CrossRefPubMedPubMedCentralGoogle Scholar
  7. Cai, W., Ji, D., Peng, L., Guo, J., Ma, J., Zou, M., Lu, C., and Zhang, L. (2009). LPA66 is required for editing psbF chloroplast transcripts in Arabidopsis. Plant Physiol 150, 1260–1271.CrossRefPubMedPubMedCentralGoogle Scholar
  8. Chateigner-Boutin, A.L., Ramos-Vega, M., Guevara-García, A., Andrés, C., de la Luz Gutiérrez-Nava, M.Ã., Cantero, A., Delannoy, E., Jiménez, L.F., Lurin, C., Small, I., and León, P. (2008). CLB19, a pentatricopeptide repeat protein required for editing of rpoA and clpP chloroplast transcripts. Plant J 56, 590–602.CrossRefPubMedGoogle Scholar
  9. Ciuzan, O., Hancock, J., Pamfil, D., Wilson, I., and Ladomery, M. (2015). The evolutionarily conserved multifunctional glycine-rich RNA-binding proteins play key roles in development and stress adaptation. Physiol Plantarum 153, 1–11.CrossRefGoogle Scholar
  10. Coquille, S., Filipovska, A., Chia, T., Rajappa, L., Lingford, J.P., Razif, M.F.M., Thore, S., and Rackham, O. (2014). An artificial PPR scaffold for programmable RNA recognition. Nat Commun 5, 5729.CrossRefPubMedGoogle Scholar
  11. Covello, P.S., and Gray, M.W. (1989). RNA editing in plant mitochondria. Nature 341, 662–666.CrossRefPubMedGoogle Scholar
  12. Glass, F., Härtel, B., Zehrmann, A., Verbitskiy, D., and Takenaka, M. (2015). MEF13 requires MORF3 and MORF8 for RNA editing at eight targets in mitochondrial mRNAs in Arabidopsis thaliana. Mol Plant 8, 1466–1477.CrossRefPubMedGoogle Scholar
  13. Golas, M.M., Böhm, C., Sander, B., Effenberger, K., Brecht, M., Stark, H., and Göringer, H.U. (2009). Snapshots of the RNA editing machine in trypanosomes captured at different assembly stages in vivo. EMBO J 28, 766–778.CrossRefPubMedPubMedCentralGoogle Scholar
  14. Göringer, H.U. (2012). ‘Gestalt,’ composition and function of the Trypanosoma brucei editosome. Annu Rev Microbiol 66, 65–82.CrossRefPubMedGoogle Scholar
  15. Gualberto, J.M., Lamattina, L., Bonnard, G., Weil, J.H., and Grienenberger, J.M. (1989). RNA editing in wheat mitochondria results in the conservation of protein sequences. Nature 341, 660–662.CrossRefPubMedGoogle Scholar
  16. Gully, B.S., Shah, K.R., Lee, M., Shearston, K., Smith, N.M., Sadowska, A., Blythe, A.J., Bernath-Levin, K., Stanley, W.A., Small, I.D., and Bond, C.S. (2015). The design and structural characterization of a synthetic pentatricopeptide repeat protein. Acta Crystlogr D Biol Crystlogr 71, 196–208.CrossRefGoogle Scholar
  17. Haag, S., Schindler, M., Berndt, L., Brennicke, A., Takenaka, M., and Weber, G. (2017). Crystal structures of the Arabidopsis thaliana organellar RNA editing factors MORF1 and MORF9. Nucleic Acids Res 45, 4915–4928.CrossRefPubMedPubMedCentralGoogle Scholar
  18. Hackett, J.B., Shi, X., Kobylarz, A.T., Lucas, M.K., Wessendorf, R.L., Hines, K.M., Bentolila, S., Hanson, M.R., and Lu, Y. (2017). An organelle RNA recognition motif protein is required for photosystem II subunit psbF transcript editing. Plant Physiol 173, 2278–2293.PubMedPubMedCentralGoogle Scholar
  19. Hammani, K., Colas des Francs-Small, 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.CrossRefPubMedPubMedCentralGoogle Scholar
  20. Härtel, B., Zehrmann, A., Verbitskiy, D., van der Merwe, J.A., Brennicke, A., and Takenaka, M. (2013). MEF10 is required for RNA editing at nad2-842 in mitochondria of Arabidopsis thaliana and interacts with MORF8. Plant Mol Biol 81, 337–346.CrossRefPubMedGoogle Scholar
  21. Hiesel, R., Wissinger, B., Schuster, W., and Brennicke, A. (1989). RNA editing in plant mitochondria. Science 246, 1632–1634.CrossRefPubMedGoogle Scholar
  22. Hoch, B., Maier, R.M., Appel, K., Igloi, G.L., and Kössel, H. (1991). Editing of a chloroplast mRNA by creation of an initiation codon. Nature 353, 178–180.CrossRefPubMedGoogle Scholar
  23. Jiang, S.C., Mei, C., Liang, S., Yu, Y.T., Lu, K., Wu, Z., Wang, X.F., and Zhang, D.P. (2015). Crucial roles of the pentatricopeptide repeat protein SOAR1 in Arabidopsis response to drought, salt and cold stresses. Plant Mol Biol 88, 369–385.CrossRefPubMedPubMedCentralGoogle Scholar
  24. Ke, J., Chen, R.Z., Ban, T., Zhou, X.E., Gu, X., Tan, M.H.E., Chen, C., Kang, Y., Brunzelle, J.S., Zhu, J.K., Melcher, K., and Xu, H.E. (2013). Structural basis for RNA recognition by a dimeric PPR-protein complex. Nat Struct Mol Biol 20, 1377–1382.CrossRefPubMedGoogle Scholar
  25. Kim, S.R., Yang, J.I., Moon, S., Ryu, C.H., An, K., Kim, K.M., Yim, J., and An, G. (2009). RiceOGR1 encodes a pentatricopeptide repeat-DYW protein and is essential for RNA editing in mitochondria. Plant J 59, 738–749.CrossRefPubMedGoogle Scholar
  26. Komor, A.C., Badran, A.H., and Liu, D.R. (2017). CRISPR-based technologies for the manipulation of eukaryotic genomes. Cell 168, 20–36.CrossRefPubMedGoogle Scholar
  27. Kotera, E., Tasaka, M., and Shikanai, T. (2005). A pentatricopeptide repeat protein is essential for RNA editing in chloroplasts. Nature 433, 326–330.CrossRefPubMedGoogle Scholar
  28. Li, F., Ge, P., Hui, W.H., Atanasov, I., Rogers, K., Guo, Q., Osato, D., Falick, A.M., Zhou, Z.H., and Simpson, L. (2009). Structure of the core editing complex (L-complex) involved in uridine insertion/deletion RNA editing in trypanosomatid mitochondria. Proc Natl Acad Sci USA 106, 12306–12310.CrossRefPubMedPubMedCentralGoogle Scholar
  29. Lin, D., Gong, X., Jiang, Q., Zheng, K., Zhou, H., Xu, J., Teng, S., and Dong, Y. (2015). The rice ALS3 encoding a novel pentatricopeptide repeat protein is required for chloroplast development and seedling growth. Rice (N Y) 8, 17.CrossRefGoogle Scholar
  30. Liu, Y.J., Xiu, Z.H., Meeley, R., and Tan, B.C. (2013). Empty Pericarp5 encodes a pentatricopeptide repeat protein that is required for mitochondrial RNA editing and seed development in maize. Plant Cell 25, 868–883.CrossRefPubMedPubMedCentralGoogle Scholar
  31. Lurin, C., Andrés, C., Aubourg, S., Bellaoui, M., Bitton, F., Bruyère, C., Caboche, M., Debast, C., Gualberto, J., Hoffmann, B., Lecharny, A., Le Ret, M., Martin-Magniette, M.L., Mireau, H., Peeters, N., Renou, J.P., Szurek, B., Taconnat, L., and Small, I. (2004). Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16, 2089–2103.CrossRefPubMedPubMedCentralGoogle Scholar
  32. Maris, C., Masse, J., Chester, A., Navaratnam, N., and Allain, F.H.T. (2005). NMR structure of the apoB mRNA stem-loop and its interaction with the C to U editing APOBEC1 complementary factor. RNA 11, 173–186.CrossRefPubMedPubMedCentralGoogle Scholar
  33. Mehta, A., and Driscoll, D.M. (2002). Identification of domains in apobec-1 complementation factor required for RNA binding and apolipoprotein-B mRNA editing. RNA 8, 69–82.CrossRefPubMedPubMedCentralGoogle Scholar
  34. Nishikura, K. (2010). Functions and regulation of RNA editing by ADAR deaminases. Annu Rev Biochem 79, 321–349.CrossRefPubMedPubMedCentralGoogle Scholar
  35. Okuda, K., Chateigner-Boutin, A.L., 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.CrossRefPubMedPubMedCentralGoogle Scholar
  36. Okuda, K., and Shikanai, T. (2012). A pentatricopeptide repeat protein acts as a site-specificity factor at multiple RNA editing sites with unrelated cis-acting elements in plastids. Nucleic Acids Res 40, 5052–5064.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Okuda, K., Shoki, H., Arai, M., Shikanai, T., Small, I., and Nakamura, T. (2014). Quantitative analysis of motifs contributing to the interaction between PLS-subfamily members and their target RNA sequences in plastid RNA editing. Plant J 80, 870–882.CrossRefPubMedGoogle Scholar
  38. Pyo, Y.J., Kwon, K.C., Kim, A., and Cho, M.H. (2013). Seedling Lethal1, a pentatricopeptide repeat protein lacking an E/E+ or DYW domain in Arabidopsis, is involved in plastid gene expression and early chloroplast development. Plant Physiol 163, 1844–1858.CrossRefPubMedPubMedCentralGoogle Scholar
  39. Shen, C., Zhang, D., Guan, Z., Liu, Y., Yang, Z., Yang, Y., Wang, X., Wang, Q., Zhang, Q.X., Fan, S., Zou, T., and Yin, P. (2016). Structural basis for specific single-stranded RNA recognition by designer pentatricopeptide repeat proteins. Nat Commun 7, 11285.CrossRefPubMedPubMedCentralGoogle Scholar
  40. Shi, X., Castandet, B., Germain, A., Hanson, M.R., and Bentolila, S. (2017). ORRM5, an RNA recognition motif-containing protein, has a unique effect on mitochondrial RNA editing. J Exp Bot 68, 2833–2847.CrossRefPubMedGoogle Scholar
  41. Shi, X., Germain, A., Hanson, M.R., and Bentolila, S. (2016). RNA recognition motif-containing protein ORRM4 broadly affects mitochondrial RNA editing and impacts plant development and flowering. Plant Physiol 170, 294–309.CrossRefPubMedGoogle Scholar
  42. Shi, X., Hanson, M.R., and Bentolila, S. (2015). Two RNA recognition motif-containing proteins are plant mitochondrial editing factors. Nucleic Acids Res 43, 3814–3825.CrossRefPubMedPubMedCentralGoogle Scholar
  43. Sosso, D., Mbelo, S., Vernoud, V., Gendrot, G., Dedieu, A., Chambrier, P., Dauzat, M., Heurtevin, L., Guyon, V., Takenaka, M., and Rogowsky, P.M. (2012). PPR2263, a DYW-subgroup pentatricopeptide repeat protein, is required for mitochondrial nad5 and cob transcript editing, mitochondrion biogenesis, and maize growth. Plant Cell 24, 676–691.CrossRefPubMedPubMedCentralGoogle Scholar
  44. Sun, T., Germain, A., Giloteaux, L., Hammani, K., Barkan, A., Hanson, M.R., and Bentolila, S. (2013). An RNA recognition motif-containing protein is required for plastid RNA editing in Arabidopsis and maize. Proc Natl Acad Sci USA 110, e1169–E1178.CrossRefPubMedPubMedCentralGoogle Scholar
  45. Sun, T., Shi, X., Friso, G., Van Wijk, K., Bentolila, S., and Hanson, M.R. (2015). A zinc finger motif-containing protein is essential for chloroplast RNA editing. PLoS Genet 11, e1005028.CrossRefPubMedPubMedCentralGoogle Scholar
  46. Sung, T.Y., Tseng, C.C., and Hsieh, M.H. (2010). The SLO1 PPR protein is required for RNA editing at multiple sites with similar upstream sequences in Arabidopsis mitochondria. Plant J 63, 499–511.CrossRefPubMedGoogle Scholar
  47. Takenaka, M., Zehrmann, A., Verbitskiy, D., Härtel, B., and Brennicke, A. (2013). RNA editing in plants and its evolution. Annu Rev Genet 47, 335–352.CrossRefPubMedGoogle Scholar
  48. Takenaka, M., Zehrmann, A., Verbitskiy, D., Kugelmann, M., Härtel, B., and Brennicke, A. (2012). Multiple organellar RNA editing factor (MORF) family proteins are required for RNA editing in mitochondria and plastids of plants. Proc Natl Acad Sci USA 109, 5104–5109.CrossRefPubMedPubMedCentralGoogle Scholar
  49. Verbitskiy, D., Zehrmann, A., Härtel, B., Brennicke, A., and Takenaka, M. (2012). Two related RNA-editing proteins target the same sites in mitochondria of Arabidopsis thaliana. J Biol Chem 287, 38064–38072.CrossRefPubMedPubMedCentralGoogle Scholar
  50. Wagoner, J.A., Sun, T., Lin, L., and Hanson, M.R. (2015). Cytidine deaminase motifs within the DYW domain of two pentatricopeptide repeatcontaining proteins are required for site-specific chloroplast RNA editing. J Biol Chem 290, 2957–2968.CrossRefPubMedGoogle Scholar
  51. Yan, J., Zhang, Q., Guan, Z., Wang, Q., Li, L., Ruan, F., Lin, R., Zou, T., and Yin, P. (2017). MORF9 increases the RNA-binding activity of PLS-type pentatricopeptide repeat protein in plastid RNA editing. Nat Plants 3, 17037.CrossRefPubMedGoogle Scholar
  52. Yin, P., Li, Q., Yan, C., Liu, Y., Liu, J., Yu, F., Wang, Z., Long, J., He, J., Wang, H.W., Wang, J., Zhu, J.K., Shi, Y., and Yan, N. (2013). Structural basis for the modular recognition of single-stranded RNA by PPR proteins. Nature 504, 168–171.CrossRefPubMedGoogle Scholar
  53. Zehrmann, A., Härtel, B., Glass, F., Bayer-Császár, E., Obata, T., Meyer, E., Brennicke, A., and Takenaka, M. (2015). Selective homo- and heteromer interactions between the multiple organellar RNA editing factor (MORF) proteins in Arabidopsis thaliana. J Biol Chem 290, 6445–6456.CrossRefPubMedPubMedCentralGoogle Scholar
  54. Zhang, F., Tang, W., Hedtke, B., Zhong, L., Liu, L., Peng, L., Lu, C., Grimm, B., and Lin, R. (2014). Tetrapyrrole biosynthetic enzyme protoporphyrinogen IX oxidase 1 is required for plastid RNA editing. Proc Natl Acad Sci USA 111, 2023–2028.CrossRefPubMedPubMedCentralGoogle Scholar
  55. Zhou, W., Cheng, Y., Yap, A., Chateigner-Boutin, A.L., Delannoy, E., Hammani, K., Small, I., and 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.CrossRefPubMedGoogle Scholar
  56. Zhou, W., Lu, Q., Li, Q., Wang, L., Ding, S., Zhang, A., Wen, X., Zhang, L., and Lu, C. (2017). PPR-SMR protein SOT1 has RNA endonuclease activity. Proc Natl Acad Sci USA 114, E1554–E1563.CrossRefPubMedPubMedCentralGoogle Scholar
  57. Zhu, Q., Dugardeyn, J., Zhang, C., Mühlenbock, P., Eastmond, P.J., Valcke, R., De Coninck, B., Oden, S., Karampelias, M., Cammue, B.P.A., Prinsen, E., and Van Der Straeten, D. (2014). The Arabidopsis thaliana RNA editing factor SLO2, which affects the mitochondrial electron transport chain, participates in multiple stress and hormone responses. Mol Plant 7, 290–310.CrossRefPubMedGoogle Scholar

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© Science China Press and Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  1. 1.National Key Laboratory of Crop Genetic Improvement and National Centre of Plant Gene ResearchHuazhong Agricultural UniversityWuhanChina

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