Requirement of Various Protein Combinations for Each C-to-U RNA Editosome in Plant Organelles

  • Mizuki TakenakaEmail author
  • Anja Jörg
  • Matthias Burger
  • Sascha Haag
Part of the Nucleic Acids and Molecular Biology book series (NUCLEIC, volume 34)


In flowering plants, RNA editing converts several hundreds of organelle cytidines to uridines. Targeted cytidines are recognized by PLS class pentatricopeptide repeat (PPR) proteins, which bind RNA sequences upstream of the C targets in a sequence-specific manner. In the past several years, different types of proteins have been identified as RNA editing factors, including multiple organellar RNA editing factors/RNA editing factor interacting proteins (MORFs/RIPs), organelle RNA recognition motif (ORRM) proteins, organelle zinc finger (OZ) proteins, a P class PPR protein NUWA, short DYW proteins, and protoporphyrinogen oxidase 1 (PPO1). These proteins seem to contribute to individual RNA editing complexes in a different manner. Despite many key players for the assembly of editosomes having been revealed, the complete mechanism of the editing machinery including the deaminase enzymatic activity is still unclear. Plant editosomes are highly diverse not only due to the PLS class PPR proteins they contain but also in other components that are present. In this review, we introduce the recent progress in the field and discuss possible functions of each component in RNA editosomes in plant mitochondria and chloroplasts.



Recent work on RNA editing was supported by grants from the Deutsche Forschungsgemeinschaft [TA642/10-1, TA 642/6-1, TA 642/3-1 to MT]. Authors thank Axel Brennicke for helpful suggestions.


  1. Andrés-Colás N, Zhu Q, Takenaka M, De Rybel B, Weijers D, Van Der Straeten D (2017) Multiple PPR protein interactions are involved in the RNA editing system in Arabidopsis mitochondria and plastids. Proc Natl Acad Sci 114:8883–8888. CrossRefPubMedPubMedCentralGoogle Scholar
  2. Barkan A, Small I (2014) Pentatricopeptide repeat proteins in plants. Annu Rev Plant Biol 65:415–442CrossRefPubMedGoogle Scholar
  3. Barkan A, Rojas M, Fujii S, Yap A, Chong YS, Bond CS, Small I (2012) A combinatorial amino acid code for RNA recognition by pentatricopeptide repeat proteins. PLoS Genet 8:e1002910. CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bass BL, Weintrau H (1988) An unwinding activity that covalently modifies its double-stranded RNA substrate. Cell 55:1089–1098. CrossRefPubMedGoogle Scholar
  5. Bayer-Császár E, Haag S, Jörg A, Glass F, Härtel B, Obata T, Meyer EH, Brennicke A, 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
  6. Bentolila S, Heller WP, Sun T, Babina a M, Friso G, van Wijk KJ, Hanson MR (2012) RIP1, a member of an Arabidopsis protein family, interacts with the protein RARE1 and broadly affects RNA editing. Proc Natl Acad Sci U S A 109:E1453–E1461. CrossRefPubMedPubMedCentralGoogle Scholar
  7. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bisanz C, Bégot L, Carol P, Perez P, Bligny M, Pesey H, Gallois J-L, Lerbs-Mache S, Mache R (2003) The Arabidopsis nuclear DAL gene encodes a chloroplast protein which is required for the maturation of the plastid ribosomal RNAs and is essential for chloroplast differentiation. Plant Mol Biol 51:651–663CrossRefPubMedGoogle Scholar
  9. Blanc V, Litvak S, Araya A (1995) RNA editing in wheat mitochondria proceeds by a deamination mechanism. FEBS Lett 373:56–60. CrossRefPubMedGoogle Scholar
  10. Bock R (2000) Sense from nonsense: how the genetic information of chloroplastsis altered by RNA editing. Biochimie 82:549–557. CrossRefPubMedGoogle Scholar
  11. Bock R, Koop HU (1997) Extraplastidic site-specific factors mediate RNA editing in chloroplasts. EMBO J 16:3282–3288. CrossRefPubMedPubMedCentralGoogle Scholar
  12. Bock R, Kössel H, Maliga P (1994) Introduction of a heterologous editing site into the tobacco plastid genome: the lack of RNA editing leads to a mutant phenotype. EMBO J 13:4623–4628PubMedPubMedCentralCrossRefGoogle Scholar
  13. Bock R, Hermann M, Kössel H (1996) In vivo dissection of cis-acting determinants for plastid RNA editing. EMBO J 15:5052–5059PubMedPubMedCentralCrossRefGoogle Scholar
  14. Boussardon C, Salone V, Avon A, Berthomé R, Hammani K, Okuda K, Shikanai T, Small I, 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
  15. Boussardon C, Avon A, Kindgren P, Bond CS, Challenor M, Lurin C, 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
  16. Chateigner-Boutin A-L, Small I (2010) Plant RNA editing. RNA Biol 7:213–219CrossRefPubMedGoogle Scholar
  17. Chateigner-Boutin A-L, Ramos-Vega M, Guevara-García A, Andrés C, de la Luz Gutiérrez-Nava M, Cantero A, Delannoy E, Jiménez LF, Lurin C, Small I, León P (2008) CLB19, a pentatricopeptide repeat protein required for editing of rpoA and clpP chloroplast transcripts. Plant J 56:590–602. CrossRefPubMedGoogle Scholar
  18. Chatterjee M, Sparvoli S, Edmunds C, Garosi P, Findlay K, Martin C (1996) DAG, a gene required for chloroplast differentiation and palisade development in Antirrhinum majus. EMBO J 15:4194–4207PubMedPubMedCentralCrossRefGoogle Scholar
  19. Cheng S, Gutmann B, Zhong X, Ye Y, Fisher MF, Bai F, Castleden I, Song Y, Song B, Huang J, Liu X, Xu X, Lim BL, Bond CS, Yiu S-M, Small I (2016) Redefining the structural motifs that determine RNA binding and RNA editing by pentatricopeptide repeat proteins in land plants. Plant J 85:532–547. CrossRefPubMedGoogle Scholar
  20. Covello PS, Gray MW (1989) RNA editing in plant mitochondria. Nature 341:662–666. CrossRefPubMedGoogle Scholar
  21. Delannoy E, Stanley WA, Bond CS, Small ID (2007) Pentatricopeptide repeat (PPR) proteins as sequence-specificity factors in post-transcriptional processes in organelles. Biochem Soc Trans 35:1643–1647. CrossRefPubMedGoogle Scholar
  22. Diaz MF, Bentolila S, Hayes ML, Hanson MR, Mulligan RM (2017) A protein with an unusually short PPR domain, MEF8, affects editing at over 60 Arabidopsis mitochondrial C targets of RNA editing. Plant J 92:638–649. CrossRefPubMedGoogle Scholar
  23. Doniwa Y, Ueda M, Ueta M, Wada A, Kadowaki K, Tsutsumi N (2010) The involvement of a PPR protein of the P subfamily in partial RNA editing of an Arabidopsis mitochondrial transcript. Gene 454:39–46. CrossRefPubMedGoogle Scholar
  24. Farré JC, Araya A (2001) Gene expression in isolated plant mitochondria: high fidelity of transcription, splicing and editing of a transgene product in electroporated organelles. Nucleic Acids Res 29:2484–2491. CrossRefPubMedPubMedCentralGoogle Scholar
  25. Farré JC, Leon G, Jordana X, Araya A (2001) cis recognition elements in plant mitochondrion RNA editing. Mol Cell Biol 21:6731–6737. CrossRefPubMedPubMedCentralGoogle Scholar
  26. Fujii S, Small I (2011) The evolution of RNA editing and pentatricopeptide repeat genes. New Phytol 191:37–47. CrossRefPubMedGoogle Scholar
  27. García-Andrade J, Ramírez V, López A, Vera P (2013) Mediated plastid RNA editing in plant immunity. PLoS Pathog 9:1–13. CrossRefGoogle Scholar
  28. Giegé P, Brennicke A (1999) RNA editing in Arabidopsis mitochondria effects 441 C to U changes in ORFs. Proc Natl Acad Sci U S A 96:15324–15329. CrossRefPubMedPubMedCentralGoogle Scholar
  29. Glass F, Hä Rtel B, Zehrmann A, Verbitskiy D, 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
  30. Gray MW (2012) Evolutionary origin of RNA editing. Biochemistry 51:5235–5242. CrossRefPubMedGoogle Scholar
  31. Grewe F, Viehoever P, Weisshaar B, Knoop V (2009) A trans-splicing group I intron and tRNA-hyperediting in the mitochondrial genome of the lycophyte Isoetes engelmannii. Nucleic Acids Res 37:5093–5104. CrossRefPubMedPubMedCentralGoogle Scholar
  32. Grohmann L, Thieck O, Herz U, Schrüoder 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. CrossRefPubMedPubMedCentralGoogle Scholar
  33. 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. CrossRefPubMedGoogle Scholar
  34. Guillaumot D, Lopez-Obando M, Baudry K, Avon A, Rigaill G, Falcon De Longevialle A, Broche B, Takenaka M, Berthomé R, De Jaeger G, Delannoy E, Lurin C (2017) Two interacting PPR proteins are major Arabidopsis editing factors in plastid and mitochondria. Proc Natl Acad Sci U S A 114:8877–8882. CrossRefPubMedPubMedCentralGoogle Scholar
  35. Gully BS, Shah KR, Lee M, Shearston K, Smith NM, Sadowska A, Blythe AJ, Bernath-Levin K, Stanley WA, Small ID, Bond CS (2015) The design and structural characterization of a synthetic pentatricopeptide repeat protein. Acta Crystallogr Sect D 71:196–208. CrossRefGoogle Scholar
  36. Guo W, Grewe F, Fan W, Young GJ, Knoop V, Palmer JD, Mower JP (2016) Ginkgo and Welwitschia mitogenomes reveal extreme contrasts in gymnosperm mitochondrial evolution. Mol Biol Evol 33:1448–1460. CrossRefPubMedGoogle Scholar
  37. Haag S, Schindler M, Berndt L, Brennicke A, Takenaka M, Weber G (2017) Crystal structures of the Arabidopsis thaliana organellar RNA editing factors MORF1 and MORF9. Nucleic Acids Res 45:4915–4928. CrossRefPubMedPubMedCentralGoogle Scholar
  38. Hackett JB, Shi X, Kobylarz AT, Lucas MK, Wessendorf RL, Hines KM, Bentolila S, Hanson MR, Lu Y (2017) An organelle RNA recognition motif protein is required for photosystem II subunit psbF transcript editing. Plant Physiol 173:2278–2293. CrossRefPubMedPubMedCentralGoogle Scholar
  39. Halter CP, Peeters NM, Hanson MR (2004) RNA editing in ribosome-less plastids of iojap maize. Curr Genet 45:331–337. CrossRefPubMedGoogle Scholar
  40. Hammani K, Okuda K, Tanz SK, 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. CrossRefPubMedPubMedCentralGoogle Scholar
  41. Hayes ML, Hanson MR (2007) Assay of editing of exogenous RNAs in chloroplast extracts of Arabidopsis, maize, pea, and tobacco. Methods Enzymol 424:459–482. CrossRefPubMedGoogle Scholar
  42. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  43. Hayes ML, Dang KN, Diaz MF, Mulligan RM (2015) A conserved glutamate residue in the C-terminal deaminase domain of pentatricopeptide repeat proteins is required for RNA editing activity. J Biol Chem 290:10136–10142. CrossRefPubMedPubMedCentralGoogle Scholar
  44. He P, Huang S, Xiao G, Zhang Y, Yu J (2016) Abundant RNA editing sites of chloroplast protein-coding genes in Ginkgo biloba and an evolutionary pattern analysis. BMC Plant Biol 16:257. CrossRefPubMedPubMedCentralGoogle Scholar
  45. He S, Sun Y, Yang Q, Zhang X, Huang Q, Zhao P, Sun M, Liu J, Qian W, Qin G, Gu H, Qu L-J (2017) A novel imprinted gene NUWA controls mitochondrial function in early seed development in Arabidopsis. PLoS Genet 13:e1006553. CrossRefPubMedPubMedCentralGoogle Scholar
  46. 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. CrossRefPubMedGoogle Scholar
  47. Herbert CJ, Golik P, Bonnefoy N (2013) Yeast PPR proteins, watchdogs of mitochondrial gene expression. RNA Biol 10:1477–1494. CrossRefPubMedPubMedCentralGoogle Scholar
  48. Hiesel R, Wissinger B, Schuster W, Brennicke A (1989) RNA editing in plant mitochondria. Science 246:1632–1634. CrossRefPubMedGoogle Scholar
  49. Hirose T, 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. CrossRefPubMedPubMedCentralGoogle Scholar
  50. Huang C, Yu Q-B, Li Z-R, Ye L-S, Xu L, Yang Z-N (2017) Porphobilinogen deaminase HEMC interacts with the PPR-protein AtECB2 for chloroplast RNA editing. Plant J 92:546–556. CrossRefPubMedGoogle Scholar
  51. Ichinose M, Sugita M (2017) RNA editing and its molecular mechanism in plant organelles. Genes (Basel) 8(1):5. CrossRefGoogle Scholar
  52. Kim U, Wang Y, Sanford T, Zeng Y, Nishikura K (1994a) Molecular cloning of cDNA for double-stranded RNA adenosine deaminase, a candidate enzyme for nuclear RNA editing. Proc Natl Acad Sci U S A 91:11457–11461. CrossRefPubMedPubMedCentralGoogle Scholar
  53. Kim U, Garner TL, Sanford T, Speicher D, Murray JM, Nishikura K (1994b) Purification and characterization of double-stranded RNA adenosine deaminase from bovine nuclear extracts. J Biol Chem 269:13480–13489PubMedGoogle Scholar
  54. 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. CrossRefPubMedGoogle Scholar
  55. Kindgren P, Yap A, Bond CS, Small I (2015) Predictable alteration of sequence recognition by RNA editing factors from Arabidopsis. Plant Cell 27:403–416. CrossRefPubMedPubMedCentralGoogle Scholar
  56. Knie N, Grewe F, Fischer S, Knoop V (2016) Reverse U-to-C editing exceeds C-to-U RNA editing in some ferns - a monilophyte-wide comparison of chloroplast and mitochondrial RNA editing suggests independent evolution of the two processes in both organelles. BMC Evol Biol 16:134. CrossRefPubMedPubMedCentralGoogle Scholar
  57. Knoop V (2011) When you can’t trust the DNA: RNA editing changes transcript sequences. Cell Mol Life Sci 68:567–586. CrossRefPubMedGoogle Scholar
  58. Knoop V, 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. CrossRefPubMedGoogle Scholar
  59. Kotera E, Tasaka M, Shikanai T (2005) A pentatricopeptide repeat protein is essential for RNA editing in chloroplasts. Nature 433:326–330. CrossRefPubMedGoogle Scholar
  60. Kugita M, Yamamoto Y, Fujikawa T, Matsumoto T, Yoshinaga K (2003) RNA editing in hornwort chloroplasts makes more than half the genes functional. Nucleic Acids Res 31:2417–2423CrossRefPubMedPubMedCentralGoogle Scholar
  61. Lightowlers RN, Chrzanowska-Lightowlers ZM (2013) Human pentatricopeptide proteins: only a few and what do they do? RNA Biol 10:1433–1438. CrossRefPubMedPubMedCentralGoogle Scholar
  62. Lu B, Hanson MRR (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. CrossRefPubMedPubMedCentralGoogle Scholar
  63. Lu B, Wilson RK, Phreaner CG, Mulligan RM, Hanson MR (1996) Protein polymorphism generated by differential RNA editing of a plant mitochondrial rps12 gene. Mol Cell Biol 16:1543–1549CrossRefPubMedPubMedCentralGoogle Scholar
  64. Luo M, Cai M, Zhang J, Li Y, Zhang R, Song W, Zhang K, Xiao H, Yue B, Zheng Y, Zhao Y, Zhao J, Qiu F (2017) Functional divergence and origin of the DAG-like gene family in plants. Sci Rep 7:5688. CrossRefPubMedPubMedCentralGoogle Scholar
  65. 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, 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
  66. Lutz KA, Maliga P (2007) Transformation of the plastid genome to study RNA editing. Methods Enzymol 424:501–518. CrossRefPubMedGoogle Scholar
  67. Mehta A, Driscoll DM (1998) A sequence-specific RNA-binding protein complements apobec-1 to edit apolipoprotein B mRNA. Mol Cell Biol 18:4426–4432. CrossRefPubMedPubMedCentralGoogle Scholar
  68. Mehta A, Driscoll DM (2002) Identification of domains in apobec-1 complementation factor required for RNA binding and apolipoprotein-B mRNA editing. RNA 8:69–82CrossRefPubMedPubMedCentralGoogle Scholar
  69. Melcher T, Maas S, Herb A, Sprengel R, Seeburg PH, Higuchi M (1996) A mammalian RNA editing enzyme. Nature 379:460–464. CrossRefPubMedGoogle Scholar
  70. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  71. Naested H, Holm A, Jenkins T, Nielsen HB, Harris CA, Beale MH, Andersen M, Mant A, Scheller H, Camara B, Mattsson O, Mundy J (2004) Arabidopsis VARIEGATED 3 encodes a chloroplast-targeted, zinc-finger protein required for chloroplast and palisade cell development. J Cell Sci 117:4807–4818. CrossRefPubMedGoogle Scholar
  72. Nakamura T, Sugita M (2008) A conserved DYW domain of the pentatricopeptide repeat protein possesses a novel endoribonuclease activity. FEBS Lett 582:4163–4168. CrossRefPubMedGoogle Scholar
  73. Neuwirt J, Takenaka M, van der Merwe JA, 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. CrossRefPubMedPubMedCentralGoogle Scholar
  74. Oda K, Yamato K, Ohta E, Nakamura Y, Takemura M, Nozato N, Akashi K, Kanegae T, Ogura Y, Kohchi T, Ohyama K (1992) Gene organization deduced from the complete sequence of liverwort Marchantia polymorpha mitochondrial DNA. A primitive form of plant mitochondrial genome. J Mol Biol 223:1–7CrossRefPubMedGoogle Scholar
  75. 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 104:8178–8183. CrossRefPubMedPubMedCentralGoogle Scholar
  76. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  77. Okuda K, Hammani K, Tanz SK, Peng L, Fukao Y, Myouga F, Motohashi R, Shinozaki K, Small I, Shikanai T (2010) The pentatricopeptide repeat protein OTP82 is required for RNA editing of plastid ndhB and ndhG transcripts. Plant J 61:339–349. CrossRefPubMedGoogle Scholar
  78. Okuda K, Shoki H, Arai M, Shikanai T, Small I, 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
  79. Oldenkott B, Yamaguchi K, Tsuji-Tsukinoki S, Knie N, Knoop V (2014) Chloroplast RNA editing going extreme: more than 3400 events of C-to-U editing in the chloroplast transcriptome of the lycophyte Selaginella uncinata. RNA 20:1499–1506CrossRefPubMedPubMedCentralGoogle Scholar
  80. Phreaner CGG, Williams MA, Mulligan RM (1996) Incomplete editing of rps12 transcripts results in the synthesis of polymorphic polypeptides in plant mitochondria. Plant Cell 8:107–117. CrossRefPubMedPubMedCentralGoogle Scholar
  81. Pyo YJ, Kwon K-C, Kim A, Cho MH (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
  82. Rüdinger M, Funk HT, Rensing SA, Maier UG, Knoop V (2009) RNA editing: only eleven sites are present in the Physcomitrella patens mitochondrial transcriptome and a universal nomenclature proposal. Mol Gen Genomics 281:473–481. CrossRefGoogle Scholar
  83. Rudinger M, Fritz-Laylin L, Polsakiewicz M, Knoop V (2011) Plant-type mitochondrial RNA editing in the protist Naegleria gruberi. RNA 17:2058–2062. CrossRefPubMedPubMedCentralGoogle Scholar
  84. 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 581:4132–4138CrossRefPubMedGoogle Scholar
  85. Schmitz-Linneweber C, Small I (2008) Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci 13:663–670. CrossRefPubMedGoogle Scholar
  86. Shen C, Zhang D, Guan Z, Liu Y, Yang Z, Yang Y, Wang X, Wang Q, Zhang Q, Fan S, Zou T, Yin P (2016) Structural basis for specific single-stranded RNA recognition by designer pentatricopeptide repeat proteins. Nat Commun 7:11285. CrossRefPubMedPubMedCentralGoogle Scholar
  87. Shi X, Hanson MR, Bentolila S (2015) Two RNA recognition motif-containing proteins are plant mitochondrial editing factors. Nucleic Acids Res 43:3814–3825. CrossRefPubMedPubMedCentralGoogle Scholar
  88. Shi X, Germain A, Hanson MR, 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
  89. Shi X, Castandet B, Germain A, Hanson MR, Bentolila S (2017) ORRM5, an RNA recognition motif-containing protein, has a unique effect on mitochondrial RNA editing. J Exp Bot 68:2833–2847. CrossRefPubMedPubMedCentralGoogle Scholar
  90. Shikanai T (2006) RNA editing in plant organelles: machinery, physiological function and evolution. Cell Mol Life Sci 63:698–708. CrossRefPubMedGoogle Scholar
  91. Shikanai T (2015) RNA editing in plants: machinery and flexibility of site recognition. Biochim Biophys Acta 1847:779–785. CrossRefPubMedGoogle Scholar
  92. Shikanai T, Fujii S (2013) Function of PPR proteins in plastid gene expression. RNA Biol 10:1446–1456. CrossRefPubMedPubMedCentralGoogle Scholar
  93. Sommer B, Köhler M, Sprengel R, Seeburg PH (1991) RNA editing in brain controls a determinant of ion flow in glutamate-gated channels. Cell 67:11–19. CrossRefPubMedGoogle Scholar
  94. Sosso D, Mbelo S, Vernoud V, Gendrot G, Dedieu A, Chambrier P, Dauzat M, Heurtevin L, Guyon V, Takenaka M, Rogowsky PM (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
  95. Staudinger M, Bolle N, Kempken F (2005) Mitochondrial electroporation and in organello RNA editing of chimeric atp6 transcripts. Mol Gen Genomics 273:130–136. CrossRefGoogle Scholar
  96. Stein JC, Howlett B, Boyes DC, Nasrallah ME, Nasrallah JB (1991) Molecular cloning of a putative receptor protein kinase gene encoded at the self-incompatibility locus of Brassica oleracea. Proc Natl Acad Sci U S A 88:8816–8820CrossRefPubMedPubMedCentralGoogle Scholar
  97. Stoltzfus A (2012) Constructive neutral evolution: exploring evolutionary theory’s curious disconnect. Biol Direct 7:35. CrossRefPubMedPubMedCentralGoogle Scholar
  98. Sugita M, Ichinose M, Ide M, Sugita C (2013) Architecture of the PPR gene family in the moss Physcomitrella patens. RNA Biol 10:1439–1445CrossRefPubMedPubMedCentralGoogle Scholar
  99. Sun T, Germain A, Giloteaux L, Hammani K, Barkan A, Hanson MR, Bentolila S (2013) An RNA recognition motif-containing protein is required for plastid RNA editing in Arabidopsis and maize. Proc Natl Acad Sci U S A 110:E1169–E1178. CrossRefPubMedPubMedCentralGoogle Scholar
  100. Sun T, Shi X, Friso G, Van Wijk K, Bentolila S, Hanson MR (2015) A zinc finger motif-containing protein is essential for chloroplast RNA editing. PLoS Genet 11:e1005028. CrossRefPubMedPubMedCentralGoogle Scholar
  101. Sun T, Bentolila S, Hanson MR (2016) The unexpected diversity of plant organelle RNA editosomes. Trends Plant Sci 21:962–973. CrossRefPubMedGoogle Scholar
  102. Sung T-Y, Tseng C-C, 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 63:1–13. CrossRefGoogle Scholar
  103. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  104. Takenaka M (2014) How complex are the editosomes in plant organelles? Mol Plant 7:582–585. CrossRefPubMedGoogle Scholar
  105. Takenaka M, Brennicke A (2003) In vitro RNA editing in pea mitochondria requires NTP or dNTP, suggesting involvement of an RNA helicase. J Biol Chem 278:47526–47533. CrossRefPubMedGoogle Scholar
  106. Takenaka M, Verbitskiy D, van der Merwe JA, Zehrmann A, Plessmann U, Urlaub H, Brennicke A (2007) In vitro RNA editing in plant mitochondria does not require added energy. FEBS Lett 581:2743–2747. CrossRefPubMedGoogle Scholar
  107. Takenaka M, Zehrmann A, Verbitskiy D, Kugelmann M, Härtel B, 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 U S A 109:5104–5109. CrossRefPubMedPubMedCentralGoogle Scholar
  108. Takenaka M, Zehrmann A, Verbitskiy D, Härtel B, Brennicke A (2013a) RNA editing in plants and its evolution. Annu Rev Genet 47:335–352. CrossRefPubMedGoogle Scholar
  109. Takenaka M, Zehrmann A, Brennicke A, Graichen K (2013b) Improved computational target site prediction for pentatricopeptide repeat RNA editing factors. PLoS One 8:e65343. CrossRefPubMedPubMedCentralGoogle Scholar
  110. Teng B, Burant CF, Davidson NO (1993) Molecular cloning of an apolipoprotein B messenger RNA editing protein. Science 260:1816–1819CrossRefGoogle Scholar
  111. Tillich M, Lehwark P, Morton BR, Maier UG (2006) The evolution of chloroplast RNA editing. Mol Biol Evol 23:1912–1921. CrossRefPubMedGoogle Scholar
  112. Tillich M, Hardel SL, Kupsch C, Armbruster U, Delannoy E, Gualberto JM, Lehwark P, Leister D, Small ID, Schmitz-Linneweber C (2009) Chloroplast ribonucleoprotein CP31A is required for editing and stability of specific chloroplast mRNAs. Proc Natl Acad Sci U S A 106:6002–6007. CrossRefPubMedPubMedCentralGoogle Scholar
  113. Verbitskiy D, Takenaka M, Neuwirt J, van der Merwe JA, Brennicke A (2006) Partially edited RNAs are intermediates of RNA editing in plant mitochondria. Plant J 47:408–416. CrossRefPubMedGoogle Scholar
  114. Verbitskiy D, van der Merwe Ja, Zehrmann A, Brennicke A, Takenaka M (2008) Multiple specificity recognition motifs enhance plant mitochondrial RNA editing in vitro. J Biol Chem 283:24374–24381. CrossRefPubMedPubMedCentralGoogle Scholar
  115. Verbitskiy D, Zehrmann A, Hartel B, Brennicke A, 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
  116. Wagner RW, Smith JE, Cooperman BS, Nishikura K (1989) A double-stranded RNA unwinding activity introduces structural alterations by means of adenosine to inosine conversions in mammalian cells. Proc Natl Acad Sci U S A 86:2647–2651. CrossRefPubMedPubMedCentralGoogle Scholar
  117. Wagoner JA, Sun T, Lin L, Hanson MR (2015) Cytidine deaminase motifs within the DYW domain of two pentatricopeptide repeat-containing proteins are required for site-specific chloroplast RNA editing. J Biol Chem 290:2957–2968. CrossRefPubMedGoogle Scholar
  118. Yagi Y, Hayashi S, Kobayashi K, Hirayama T, Nakamura T (2013) Elucidation of the RNA recognition code for pentatricopeptide repeat proteins involved in organelle RNA editing in plants. PLoS One 8:e57286. CrossRefPubMedPubMedCentralGoogle Scholar
  119. Yan J, Zhang Q, Guan Z, Wang Q, Li L, Ruan F, Lin R, Zou T, 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
  120. 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, Yan N (2013) Structural basis for the modular recognition of single-stranded RNA by PPR proteins. Nature 504:168–171. CrossRefPubMedGoogle Scholar
  121. Zehrmann A, Verbitskiy D, van der Merwe JA, 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. CrossRefPubMedPubMedCentralGoogle Scholar
  122. Zehrmann A, Verbitskiy D, Härtel B, Brennicke A, Takenaka M (2010) RNA editing competence of trans-factor MEF1 is modulated by ecotype-specific differences but requires the DYW domain. FEBS Lett 584:4181–4186. CrossRefPubMedGoogle Scholar
  123. Zehrmann A, Härtel B, Glass F, Bayer-Császár E, Obata T, Meyer E, Brennicke A, 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
  124. Zeltz P, Hess WR, Neckermann K, Börner T, Kössel H (1993) Editing of the chloroplast rpoB transcript is independent of chloroplast translation and shows different patterns in barley and maize. EMBO J 12:4291–4296PubMedPubMedCentralCrossRefGoogle Scholar
  125. Zhang F, Tang W, Hedtke B, Zhong L, Liu L, Peng L, Lu C, Grimm B, Lin R (2014) Tetrapyrrole biosynthetic enzyme protoporphyrinogen IX oxidase 1 is required for plastid RNA editing. Proc Natl Acad Sci U S A 111:2023–2028. CrossRefPubMedPubMedCentralGoogle Scholar
  126. Zhang H-D, Cui Y-L, Huang C, Yin Q-Q, Qin X-M, Xu T, He X-F, Zhang Y, Li Z-R, Yang Z-N (2015) PPR protein PDM1/SEL1 is involved in RNA editing and splicing of plastid genes in Arabidopsis thaliana. Photosynth Res 126:311–321. CrossRefPubMedGoogle Scholar
  127. Zhou W, Cheng Y, Yap A, Chateigner-Boutin A-L, Delannoy E, Hammani K, Small I, Huang J (2008) 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 58:1–15. CrossRefGoogle Scholar
  128. Zhu Q, Dugardeyn J, Zhang C, Takenaka M, Kühn K, Craddock C, Smalle J, Karampelias M, Denecke J, Peters J, Gerats T, Brennicke A, Eastmond P, Meyer EHEH, Van Der Straeten D, Kuhn K, Craddock C, Smalle J, Karampelias M, Denecke J, Peters J, Gerats T, Brennicke A, Eastmond P, Meyer EHEH, Van Der SD (2012) SLO2, a mitochondrial pentatricopeptide repeat protein affecting several RNA editing sites, is required for energy metabolism. Plant J 71:836–849. CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Mizuki Takenaka
    • 1
    • 2
    Email author
  • Anja Jörg
    • 1
  • Matthias Burger
    • 1
  • Sascha Haag
    • 1
  1. 1.Molekulare Botanik, Universität UlmUlmGermany
  2. 2.Department of BotanyGraduate School of Science, Kyoto UniversityKyotoJapan

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