A Zinc Finger Motif-Containing Protein Is Essential for Chloroplast RNA Editing

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Transcripts encoding chloroplast and mitochondrial proteins of flowering plants are profoundly affected by RNA editing. In Arabidopsis, over 600 genomically-encoded Cs are modified to Us in organelle transcripts, altering the encoded amino acids and creating stop and start codons. Pentatricopeptide proteins are known to bind to cis-elements near C targets of editing and chloroplast RNA editing also requires members of two additional protein families. Nevertheless, not all protein components of the editosome have been identified. We now report the discovery of a member of fourth gene family essential for chloroplast RNA editing: OZ1, member of a family of Arabidopsis RanBP2-type zinc finger proteins. Identifying all of the proteins in the RNA editosome is critical for understanding the mechanism behind the remarkable specificity of C-to-U editing.

Vyšlo v časopise: A Zinc Finger Motif-Containing Protein Is Essential for Chloroplast RNA Editing. PLoS Genet 11(3): e32767. doi:10.1371/journal.pgen.1005028
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005028

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Zdroje

1. Covello PS, Gray MW (1989) RNA editing in plant mitochondria. Nature 341: 662–666. 2552326

2. Gualberto JM, Lamattina L, Bonnard G, Weil J-H, Grienenberger J-M (1989) RNA editing in wheat mitochondria results in the conservation of protein sequences. Nature 341: 660–662. 2552325

3. Hiesel R, Wissinger B, Schuster W, Brennicke A (1989) RNA editing in plant mitochondria. Science 246: 1632–1634. 2480644

4. Bentolila S, Oh J, Hanson MR, Bukowski R (2013) Comprehensive high-resolution analysis of the role of an Arabidopsis gene family in RNA editing. PLoS Genet 9: e1003584. doi: 10.1371/journal.pgen.1003584 23818871

5. Chateigner-Boutin A-L, 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. 17726051

6. Gray MW, Covello PS (1993) RNA editing in plant mitochondria and chloroplasts. FASEB J 7: 64–71. 8422976

7. Bentolila S, Heller WP, Sun T, Babina AM, Friso G, et al. (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. doi: 10.1073/pnas.1121465109 22566615

8. 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. 8918473

9. Hayes ML, Hanson MR (2007) Identification of a sequence motif critical for editing of a tobacco chloroplast transcript. RNA 13: 281–288. 17158709

10. Okuda K, Nakamura T, Sugita M, Shimizu T, Shikanai T (2006) A pentatricopeptide repeat protein is a site recognition factor in chloroplast RNA editing. J Biol Chem 281: 37661–37667. 17015439

11. Barkan A, Rojas M, Fujii S, Yap A, Chong YS, et al. (2012) A combinatorial amino acid code for RNA recognition by pentatricopeptide repeat proteins. PLoS Genet 8: e1002910. doi: 10.1371/journal.pgen.1002910 22916040

12. Yin P, Li Q, Yan C, Liu Y, Liu J, et al. (2013) Structural basis for the modular recognition of single-stranded RNA by PPR proteins. Nature 504: 168–171. doi: 10.1038/nature12651 24162847

13. Lurin C, Andrés C, Aubourg S, Bellaoui M, Bitton F, et al. (2004) Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16: 2089–2103. 15269332

14. Salone V, Rüdinger M, Polsakiewicz M, Hoffmann B, Groth-Malonek M, et al. (2007) A hypothesis on the identification of the editing enzyme in plant organelles. FEBS Lett 581: 4132–4138. 17707818

15. Chateigner-Boutin A-L, Ramos-Vega M, Guevara-García A, Andrés C, De La Luz Gutiérrez-Nava M, et al. (2008) CLB19, a pentatricopeptide repeat protein required for editing of rpoA and clpP chloroplast transcripts. Plant J 56: 590–602. doi: 10.1111/j.1365-313X.2008.03634.x 18657233

16. Hayes ML, Giang K, Berhane B, Mulligan RM (2013) Identification of two pentatricopeptide repeat genes required for RNA editing and zinc binding by C-terminal cytidine deaminase-like domains. J Biol Chem 288: 36519–36529. doi: 10.1074/jbc.M113.485755 24194514

17. Kotera E, Tasaka M, Shikanai T (2005) A pentatricopeptide repeat protein is essential for RNA editing in chloroplasts. Nature 433: 326–330. 15662426

18. 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. 17483454

19. Okuda K, Chateigner-Boutin A-L, Nakamura T, Delannoy E, Sugita M, et al. (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. doi: 10.1105/tpc.108.064667 19182104

20. Okuda K, Hammani K, Tanz SK, Peng L, Fukao Y, et al. (2010) The pentatricopeptide repeat protein OTP82 is required for RNA editing of plastid ndhB and ndhG transcripts. Plant J Cell Mol Biol 61: 339–349.

21. Nakamura T, Sugita M (2008) A conserved DYW domain of the pentatricopeptide repeat protein possesses a novel endoribonuclease activity. FEBS Lett 582: 4163–4168. doi: 10.1016/j.febslet.2008.11.017 19041647

22. Boussardon C, Salone V, Avon A, Berthomé R, Hammani K, et al. (2012) Two interacting proteins are necessary for the editing of the ndhD-1 site in Arabidopsis plastids. Plant Cell 24: 3684–3694. doi: 10.1105/tpc.112.099507 23001034

23. Boussardon C, Avon A, Kindgren P, Bond CS, Challenor M, et al. (2014) The cytidine deaminase signature HxE(x)n CxxC of DYW1 binds zinc and is necessary for RNA editing of ndhD-1. New Phytol 203: 1090–1095. doi: 10.1111/nph.12928 25041347

24. Wagoner JA, Sun T, Lin L, Hanson MR. (2014) Cytidine deaminase motifs within the DYW domain of two pentatricopeptide repeat-containing proteins are required for site-specific chloroplast RNA editing. J Biol Chem.

25. Sun T, Germain A, Giloteaux L, Hammani K, Barkan A, et al. (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. doi: 10.1073/pnas.1220162110 23487777

26. Takenaka M, Zehrmann A, Verbitskiy D, Kugelmann M, Härtel B, et al. (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. doi: 10.1073/pnas.1202452109 22411807

27. Yoo S-D, Cho Y-H, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2: 1565–1572. 17585298

28. Næsted H, Holm A, Jenkins T, Nielsen HB, Harris CA, et al. (2004) Arabidopsis VARIEGATED 3 encodes a chloroplast-targeted, zinc-finger protein required for chloroplast and palisade cell development. J Cell Sci 117: 4807–4818. 15340011

29. Robbins JC, Heller WP, Hanson MR (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. doi: 10.1261/rna.1533909 19395655

30. Emanuelsson O, Nielsen H, Brunak S, von Heijne G (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300: 1005–1016. 10891285

31. Zhang F, Tang W, Hedtke B, Zhong L, Liu L, et al. (2014) Tetrapyrrole biosynthetic enzyme protoporphyrinogen IX oxidase 1 is required for plastid RNA editing. Proc Natl Acad Sci USA 111: 2023–2028. doi: 10.1073/pnas.1316183111 24497494

32. Hegeman CE, Hayes ML, Hanson MR (2005) Substrate and cofactor requirements for RNA editing of chloroplast transcripts in Arabidopsis in vitro. Plant J 42: 124–132. 15773858

33. Lyska D, Engelmann K, Meierhoff K, Westhoff P (2013) pAUL: a gateway-based vector system for adaptive expression and flexible tagging of proteins in Arabidopsis. PloS One 8: e53787. doi: 10.1371/journal.pone.0053787 23326506

34. Crowe ML, Serizet C, Thareau V, Aubourg S, Rouzé P, et al. (2003) CATMA: a complete Arabidopsis GST database. Nucleic Acids Res 31: 156–158. 12519971

35. Weigel D, Glazebrook J (2006) Root transformation of Arabidopsis. Cold Spring Harb Protoc 2006: pdb.prot4671.

36. Friso G, Olinares PDB, van Wijk KJ (2011) The workflow for quantitative proteome analysis of chloroplast development and differentiation, chloroplast mutants, and protein interactions by spectral counting. Methods Mol Biol 775: 265–282. doi: 10.1007/978-1-61779-237-3_14 21863448

37. Peeters NM, Hanson MR (2002) Transcript abundance supercedes editing efficiency as a factor in developmental variation of chloroplast gene expression. RNA 8: 497–511. 11991643

38. Jakoby MJ, Weinl C, Pusch S, Kuijt SJH, Merkle T, et al. (2006) Analysis of the subcellular localization, function, and proteolytic control of the Arabidopsis cyclin-dependent kinase inhibitor ICK1/KRP1. Plant Physiol 141: 1293–1305. 16766674

39. Notredame C, Higgins DG, Heringa J (2000) T-Coffee: A novel method for fast and accurate multiple sequence alignment. J Mol Biol 302: 205–217. 10964570

40. Yagi Y, Tachikawa M, Noguchi H, Satoh S, Obokata J, Nakamura T (2013) Pentatricopeptide repeat proteins involved in plant organellar RNA editing. RNA Biol. 10:1419–1425. doi: 10.4161/rna.24908 23669716

41. Yap A, Kindgren P, Colas des Francs-Small C, Kazama T, Tanz SK, et al. (2015) AEF1/MPR25 is implicated in RNA editing of plastid atpF and mitochondrial nad5 and also promotes atpF splicing in Arabidopsis and rice. Plant J.