Abstract
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.
Similar content being viewed by others
References
Barkan, A., and Small, I. (2014). Pentatricopeptide repeat proteins in plants. Annu Rev Plant Biol 65, 415–442.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Covello, P.S., and Gray, M.W. (1989). RNA editing in plant mitochondria. Nature 341, 662–666.
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.
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.
Göringer, H.U. (2012). ‘Gestalt,’ composition and function of the Trypanosoma brucei editosome. Annu Rev Microbiol 66, 65–82.
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.
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.
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.
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.
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.
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.
Hiesel, R., Wissinger, B., Schuster, W., and Brennicke, A. (1989). RNA editing in plant mitochondria. Science 246, 1632–1634.
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.
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.
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.
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.
Komor, A.C., Badran, A.H., and Liu, D.R. (2017). CRISPR-based technologies for the manipulation of eukaryotic genomes. Cell 168, 20–36.
Kotera, E., Tasaka, M., and Shikanai, T. (2005). A pentatricopeptide repeat protein is essential for RNA editing in chloroplasts. Nature 433, 326–330.
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.
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.
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.
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.
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.
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.
Nishikura, K. (2010). Functions and regulation of RNA editing by ADAR deaminases. Annu Rev Biochem 79, 321–349.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Acknowledgements
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).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Yan, J., Zhang, Q. & Yin, P. RNA editing machinery in plant organelles. Sci. China Life Sci. 61, 162–169 (2018). https://doi.org/10.1007/s11427-017-9170-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11427-017-9170-3