Pentatricopeptide repeat (PPR) proteins constitute one of the largest protein families in land plants, with more than 400 members in most species. Over the past decade, much has been learned about the molecular functions of these proteins, where they act in the cell, and what physiological roles they play during plant growth and development. A typical PPR protein is targeted to mitochondria or chloroplasts, binds one or several organellar transcripts, and influences their expression by altering RNA sequence, turnover, processing, or translation. Their combined action has profound effects on organelle biogenesis and function and, consequently, on photosynthesis, respiration, plant development, and environmental responses. Recent breakthroughs in understanding how PPR proteins recognize RNA sequences through modular base-specific contacts will help match proteins to potential binding sites and provide a pathway toward designing synthetic RNA-binding proteins aimed at desired targets.


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Literature Cited

  1. Akagi H, Nakamura A, Yokozeki-Misono Y, Inagaki A, Takahashi H. 1.  et al. 2004. Positional cloning of the rice Rf-1 gene, a restorer of BT-type cytoplasmic male sterility that encodes a mitochondria-targeting PPR protein. Theor. Appl. Genet. 108:1449–57 [Google Scholar]
  2. Arenas-M A, Takenaka M, Moreno S, Gómez I, Jordana X. 2.  2013. Contiguous RNA editing sites in the mitochondrial nad1 transcript of Arabidopsis thaliana are recognized by different proteins. FEBS Lett. 587:887–91 [Google Scholar]
  3. Aubourg S, Boudet N, Kreis M, Lecharny A. 3.  2000. In Arabidopsis thaliana, 1% of the genome codes for a novel protein family unique to plants. Plant Mol. Biol. 42:603–13 [Google Scholar]
  4. Auchincloss A, Zerges W, Perron K, Girard-Bascou J, Rochaix JD. 4.  2002. Characterization of Tbc2, a nucleus-encoded factor specifically required for translation of the chloroplast psbC mRNA in Chlamydomonas reinhardtii. J. Cell Biol. 157:953–62 [Google Scholar]
  5. Ban T, Ke J, Chen R, Gu X, Tan MH. 5.  et al. 2013. Structure of a PLS-class pentatricopeptide repeat protein provides insights into mechanism of RNA recognition. J. Biol. Chem. 288:31540–48 [Google Scholar]
  6. Barkan A, Rojas M, Fujii S, Yap A, Chong YS. 6.  et al. 2012. A combinatorial amino acid code for RNA recognition by pentatricopeptide repeat proteins. PLoS Genet. 8:e1002910 [Google Scholar]
  7. Barkan A, Walker M, Nolasco M, Johnson D. 7.  1994. A nuclear mutation in maize blocks the processing and translation of several chloroplast mRNAs and provides evidence for the differential translation of alternative mRNA forms. EMBO J. 13:3170–81 [Google Scholar]
  8. Beick S, Schmitz-Linneweber C, Williams-Carrier R, Jensen B, Barkan A. 8.  2008. The pentatricopeptide repeat protein PPR5 stabilizes a specific tRNA precursor in maize chloroplasts. Mol. Cell. Biol. 28:5337–47 [Google Scholar]
  9. Bentolila S, Alfonso A, Hanson M. 9.  2002. A pentatricopeptide repeat-containing gene restores fertility to cytoplasmic male-sterile plants. Proc. Natl. Acad. Sci. USA 99:10887–92 [Google Scholar]
  10. Bentolila S, Heller WP, Sun T, Babina AM, Friso G. 10.  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:E1453–61 [Google Scholar]
  11. Bentolila S, Oh J, Hanson MR, Bukowski R. 11.  2013. Comprehensive high-resolution analysis of the role of an Arabidopsis gene family in RNA editing. PLoS Genet. 9:e1003584 [Google Scholar]
  12. Binder S, Hölzle A, Jonietz C. 12.  2011. RNA processing and RNA stability in plant mitochondria. Plant Mitochondria F Kempken 107–30 New York: Springer [Google Scholar]
  13. Bock R, Hermann M, Kossel H. 13.  1996. In vivo dissection of cis-acting determinants for plastid RNA editing. EMBO J. 15:5052–59 [Google Scholar]
  14. Bolle N, Kempken F. 14.  2006. Mono- and dicotyledonous plant-specific RNA editing sites are correctly edited in both in organello systems. FEBS Lett. 580:4443–48 [Google Scholar]
  15. Boudreau E, Nickelsen J, Lemaire SD, Ossenbuhl F, Rochaix JD. 15.  2000. The Nac2 gene of Chlamydomonas encodes a chloroplast TPR-like protein involved in psbD mRNA stability. EMBO J. 19:3366–76 [Google Scholar]
  16. Boulouis A, Raynaud C, Bujaldon S, Aznar A, Wollman FA, Choquet Y. 16.  2011. The nucleus-encoded trans-acting factor MCA1 plays a critical role in the regulation of cytochrome f synthesis in Chlamydomonas chloroplasts. Plant Cell 23:333–49 [Google Scholar]
  17. Boussardon C, Salone V, Avon A, Berthome R, Hammani K. 17.  et al. 2012. Two interacting proteins are necessary for the editing of the NdhD-1 site in Arabidopsis plastids. Plant Cell 24:3684–94 [Google Scholar]
  18. Brown GG, Formanova N, Jin H, Wargachuk R, Dendy C. 18.  et al. 2003. The radish Rfo restorer gene of Ogura cytoplasmic male sterility encodes a protein with multiple pentatricopeptide repeats. Plant J. 35:262–72 [Google Scholar]
  19. Bryant N, Lloyd J, Sweeney C, Myouga F, Meinke D. 19.  2011. Identification of nuclear genes encoding chloroplast-localized proteins required for embryo development in Arabidopsis thaliana. Plant Physiol. 155:1678–89 [Google Scholar]
  20. Cai W, Ji D, Peng L, Guo J, Ma J. 20.  et al. 2009. LPA66 is required for editing psbF chloroplast transcripts in Arabidopsis. Plant Physiol. 150:1260–71 [Google Scholar]
  21. Cai W, Okuda K, Peng L, Shikanai T. 21.  2011. PROTON GRADIENT REGULATION 3 recognizes multiple targets with limited similarity and mediates translation and RNA stabilization in plastids. Plant J. 67:318–27 [Google Scholar]
  22. Castandet B, Araya A. 22.  2012. The nucleocytoplasmic conflict, a driving force for the emergence of plant organellar RNA editing. IUBMB Life 64:120–25 [Google Scholar]
  23. Cazalet C, Gomez-Valero L, Rusniok C, Lomma M, Dervins-Ravault D. 23.  et al. 2010. Analysis of the Legionella longbeachae genome and transcriptome uncovers unique strategies to cause Legionnaires' disease. PLoS Genet. 6:e1000851 [Google Scholar]
  24. Chase CD. 24.  2007. Cytoplasmic male sterility: a window to the world of plant mitochondrial-nuclear interactions. Trends Genet. 23:81–90 [Google Scholar]
  25. Chateigner-Boutin AL, Colas des Francs-Small C, Delannoy E, Kahlau S, Tanz SK. 25.  et al. 2011. OTP70 is a pentatricopeptide repeat protein of the E subgroup involved in splicing of the plastid transcript rpoC1. Plant J. 65:532–42 [Google Scholar]
  26. Chateigner-Boutin AL, Colas des Francs-Small C, Fujii S, Okuda K, Tanz S, Small I. 26.  2013. The E domains of pentatricopeptide repeat proteins from different organelles are not functionally equivalent for RNA editing. Plant J. 74:935–45 [Google Scholar]
  27. Chateigner-Boutin AL, Hanson MR. 27.  2002. Cross-competition in transgenic chloroplasts expressing single editing sites reveals shared cis elements. Mol. Cell. Biol. 22:8448–56 [Google Scholar]
  28. Chateigner-Boutin AL, Ramos-Vega M, Guevara-Garcia A, Andrés C, de la Luz Gutiérrez-Nava M. 28.  et al. 2008. CLB19, a pentatricopeptide repeat protein required for editing of rpoA and clpP chloroplast transcripts. Plant J. 56:590–602 [Google Scholar]
  29. Chateigner-Boutin AL, Small I. 29.  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 [Google Scholar]
  30. Chateigner-Boutin AL, Small I. 30.  2010. Plant RNA editing. RNA Biol. 7:213–19 [Google Scholar]
  31. Chaudhuri S, Maliga P. 31.  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. 15:5958–64 [Google Scholar]
  32. Chen Y, Varani G. 32.  2013. Engineering RNA-binding proteins for biology. FEBS J. 280:3734–54 [Google Scholar]
  33. Choury D, Araya A. 33.  2006. RNA editing site recognition in heterologous plant mitochondria. Curr. Genet. 50:405–16 [Google Scholar]
  34. Choury D, Farré J, Jordana X, Araya A. 34.  2005. Gene expression studies in isolated mitochondria: Solanum tuberosum rps10 is recognized by cognate potato but not by the transcription, splicing and editing machinery of wheat mitochondria. Nucleic Acids Res. 33:7058–65 [Google Scholar]
  35. Cottage A, Mott E, Kempster J, Gray J. 35.  2010. The Arabidopsis plastid-signalling mutant gun1 (genomes uncoupled1) shows altered sensitivity to sucrose and abscisic acid and alterations in early seedling development. J. Exp. Bot. 61:3773–86 [Google Scholar]
  36. Dahan J, Mireau H. 36.  2013. The Rf and Rf-like PPR in higher plants, a fast-evolving subclass of PPR genes. RNA Biol. 10:1286–93 [Google Scholar]
  37. Desloire S, Gherbi H, Laloui W, Marhadour S, Clouet V. 37.  et al. 2003. Identification of the fertility restoration locus, Rfo, in radish, as a member of the pentatricopeptide-repeat protein family. EMBO Rep. 4:588–94 [Google Scholar]
  38. Ding YH, Liu NY, Tang ZS, Liu J, Yang WC. 38.  2006. Arabidopsis GLUTAMINE-RICH PROTEIN23 is essential for early embryogenesis and encodes a novel nuclear PPR motif protein that interacts with RNA polymerase II subunit III. Plant Cell 18:815–30 [Google Scholar]
  39. Doniwa Y, Ueda M, Ueta M, Wada A, Kadowaki K, Tsutsumi N. 39.  2010. The involvement of a PPR protein of the P subfamily in partial RNA editing of an Arabidopsis mitochondrial transcript. Gene 454:39–46 [Google Scholar]
  40. Eberhard S, Loiselay C, Drapier D, Bujaldon S, Girard-Bascou J. 40.  et al. 2011. Dual functions of the nucleus-encoded factor TDA1 in trapping and translation activation of atpA transcripts in Chlamydomonas reinhardtii chloroplasts. Plant J. 67:1055–66 [Google Scholar]
  41. Falcon de Longevialle AF, Hendrickson L, Taylor N, Delannoy E, Lurin C. 41.  et al. 2008. The pentatricopeptide repeat gene OTP51 with two LAGLIDADG motifs is required for the cis-splicing of plastid ycf3 intron 2 in Arabidopsis thaliana. Plant J. 56:157–68 [Google Scholar]
  42. Falcon de Longevialle AF, Meyer EH, Andrès C, Taylor NL, Lurin C. 42.  et al. 2007. The pentatricopeptide repeat gene OTP43 is required for trans-splicing of the mitochondrial nad1 intron 1 in Arabidopsis thaliana. Plant Cell 19:3256–65 [Google Scholar]
  43. Falcon de Longevialle AF, Small I, Lurin C. 43.  2010. Nuclearly encoded splicing factors implicated in RNA splicing in higher plant organelles. Mol. Plant 3:691–705 [Google Scholar]
  44. Farré JC, Leon G, Jordana X, Araya A. 44.  2001. cis Recognition elements in plant mitochondrion RNA editing. Mol. Cell. Biol. 21:6731–37 [Google Scholar]
  45. Felder S, Meurer J, Meierhoff K, Klaff P, Bechtold N, Westhoff P. 45.  2001. The nucleus-encoded HCF107 gene of Arabidopsis provides a link between intercistronic RNA processing and the accumulation of translation-competent psbH transcripts in chloroplasts. Plant Cell 13:2127–41 [Google Scholar]
  46. Filipovska A, Rackham O. 46.  2012. Modular recognition of nucleic acids by PUF, TALE and PPR proteins. Mol. Biosyst. 8:699–708 [Google Scholar]
  47. Fisk DG, Walker MB, Barkan A. 47.  1999. Molecular cloning of the maize gene crp1 reveals similarity between regulators of mitochondrial and chloroplast gene expression. EMBO J. 18:2621–30 [Google Scholar]
  48. Forner J, Hölzle A, Jonietz C, Thuss S, Schwarzlander M. 48.  et al. 2008. Mitochondrial mRNA polymorphisms in different Arabidopsis accessions. Plant Physiol. 148:1106–16 [Google Scholar]
  49. Fujii S, Bond CS, Small I. 49.  2011. Selection patterns on restorer-like genes reveal a conflict between nuclear and mitochondrial genomes throughout angiosperm evolution. Proc. Natl. Acad. Sci. USA 108:1723–28 [Google Scholar]
  50. Fujii S, Small I. 50.  2011. The evolution of RNA editing and pentatricopeptide repeat genes. New Phytol. 191:37–47 [Google Scholar]
  51. Fukui K, Kuramitsu S. 51.  2011. Structure and function of the small MutS-related domain. Mol. Biol. Int. 2011:691735 [Google Scholar]
  52. Geddy R, Brown GG. 52.  2007. Genes encoding pentatricopeptide repeat (PPR) proteins are not conserved in location in plant genomes and may be subject to diversifying selection. BMC Genomics 8:130 [Google Scholar]
  53. Germain A, Hotto AM, Barkan A, Stern DB. 53.  2013. RNA processing and decay in plastids. Wiley Interdiscip. Rev. RNA 4:295–316 [Google Scholar]
  54. Gillman JD, Bentolila S, Hanson MR. 54.  2007. The petunia restorer of fertility protein is part of a large mitochondrial complex that interacts with transcripts of the CMS-associated locus. Plant J. 49:217–27 [Google Scholar]
  55. Gobert A, Gutmann B, Taschner A, Gossringer M, Holzmann J. 55.  et al. 2010. A single Arabidopsis organellar protein has RNase P activity. Nat. Struct. Mol. Biol. 17:740–44 [Google Scholar]
  56. Gobert A, Pinker F, Fuchsbauer O, Gutmann B, Boutin R. 56.  et al. 2013. Structural insights into protein-only RNase P complexed with tRNA. Nat. Commun. 4:1353 [Google Scholar]
  57. Gray MW, Lukes J, Archibald JM, Keeling PJ, Doolittle WF. 57.  2010. Cell biology: irremediable complexity?. Science 330:920–21 [Google Scholar]
  58. Gutierrez-Marcos JF, Dal Pra M, Giulini A, Costa LM, Gavazzi G. 58.  et al. 2007. empty pericarp4 encodes a mitochondrion-targeted pentatricopeptide repeat protein necessary for seed development and plant growth in maize. Plant Cell 19:196–210 [Google Scholar]
  59. Gutmann B, Gobert A, Giegé P. 59.  2012. PRORP proteins support RNase P activity in both organelles and the nucleus in Arabidopsis. Genes Dev. 26:1022–27 [Google Scholar]
  60. Haili N, Arnal N, Quadrado M, Amiar S, Tcherkez G. 60.  et al. 2013. The pentatricopeptide repeat MTSF1 protein stabilizes the nad4 mRNA in Arabidopsis mitochondria. Nucleic Acids Res. 41:6650–63 [Google Scholar]
  61. Hammani K, Cook W, Barkan A. 61.  2012. RNA binding and RNA remodeling activities of the half-a-tetratricopeptide (HAT) protein HCF107 underlie its effects on gene expression. Proc. Natl. Acad. Sci. USA 109:5651–16 [Google Scholar]
  62. Hammani K, Colas des Francs-Small C, Takenaka M, Tanz SK, Okuda K. 62.  et al. 2011. The pentatricopeptide repeat protein OTP87 is essential for RNA editing of nad7 and atp1 transcripts in Arabidopsis mitochondria. J. Biol. Chem. 286:21361–71 [Google Scholar]
  63. Hammani K, Gobert A, Hleibieh K, Choulier L, Small I, Giegé P. 63.  2011. An Arabidopsis dual-localized pentatricopeptide repeat protein interacts with nuclear proteins involved in gene expression regulation. Plant Cell 23:730–40 [Google Scholar]
  64. Hammani K, Okuda K, Tanz SK, Chateigner-Boutin AL, Shikanai T, Small I. 64.  2009. A study of new Arabidopsis chloroplast RNA editing mutants reveals general features of editing factors and their target sites. Plant Cell 21:3686–99 [Google Scholar]
  65. Hashimoto M, Endo T, Peltier G, Tasaka M, Shikanai T. 65.  2003. A nucleus-encoded factor, CRR2, is essential for the expression of chloroplast ndhB in Arabidopsis. Plant J. 36:541–49 [Google Scholar]
  66. Hattori M, Miyake H, Sugita M. 66.  2007. A pentatricopeptide repeat protein is required for RNA processing of clpP pre-mRNA in moss chloroplasts. J. Biol. Chem. 282:10773–82 [Google Scholar]
  67. Hattori M, Sugita M. 67.  2009. A moss pentatricopeptide repeat protein binds to the 3′ end of plastid clpP pre-mRNA and assists with mRNA maturation. FEBS J. 276:5860–69 [Google Scholar]
  68. Hauler A, Jonietz C, Stoll B, Stoll K, Braun HP, Binder S. 68.  2013. RNA PROCESSING FACTOR 5 is required for efficient 5′ cleavage at a processing site conserved in RNAs of three different mitochondrial genes in Arabidopsis thaliana. Plant J. 74:593–604 [Google Scholar]
  69. Hayes ML, Hanson M. 69.  2008. High conservation of a 5′ element required for RNA editing of a C target in chloroplast psbE transcripts. J. Mol. Evol. 67:233–45 [Google Scholar]
  70. Hayes ML, Mulligan RM. 70.  2011. Pentatricopeptide repeat proteins constrain genome evolution in chloroplasts. Mol. Biol. Evol. 28:2029–39 [Google Scholar]
  71. Hernandez Mora JR, Rivals E, Mireau H, Budar F. 71.  2010. Sequence analysis of two alleles reveals that intra-and intergenic recombination played a role in the evolution of the radish fertility restorer (Rfo). BMC Plant Biol. 10:35 [Google Scholar]
  72. Hölzle A, Jonietz C, Törjek O, Altmann T, Binder S, Forner J. 72.  2011. A RESTORER OF FERTILITY-like PPR gene is required for 5′-end processing of the nad4 mRNA in mitochondria of Arabidopsis thaliana. Plant J. 65:737–44 [Google Scholar]
  73. Howard MJ, Lim WH, Fierke CA, Koutmos M. 73.  2012. Mitochondrial ribonuclease P structure provides insight into the evolution of catalytic strategies for precursor-tRNA 5′ processing. Proc. Natl. Acad. Sci. USA 109:16149–54 [Google Scholar]
  74. Hu J, Wang K, Huang W, Liu G, Gao Y. 74.  et al. 2012. The rice pentatricopeptide repeat protein RF5 restores fertility in Hong-Lian cytoplasmic male-sterile lines via a complex with the glycine-rich protein GRP162. Plant Cell 24:109–22 [Google Scholar]
  75. Ichinose M, Tasaki E, Sugita C, Sugita M. 75.  2012. A PPR-DYW protein is required for splicing of a group II intron of cox1 pre-mRNA in Physcomitrella patens. Plant J. 70:271–78 [Google Scholar]
  76. Ikeda T, Gray M. 76.  1999. Characterization of a DNA-binding protein implicated in transcription in wheat mitochondria. Mol. Cell. Biol. 19:8113–22 [Google Scholar]
  77. Iyer LM, Zhang D, Rogozin IB, Aravind L. 77.  2011. Evolution of the deaminase fold and multiple origins of eukaryotic editing and mutagenic nucleic acid deaminases from bacterial toxin systems. Nucleic Acids Res. 39:9473–97 [Google Scholar]
  78. Johnson X, Wostrikoff K, Finazzi G, Kuras R, Schwarz C. 78.  et al. 2010. MRL1, a conserved pentatricopeptide repeat protein, is required for stabilization of rbcL mRNA in Chlamydomonas and Arabidopsis. Plant Cell 22:234–48 [Google Scholar]
  79. Jonietz C, Forner J, Hildebrandt T, Binder S. 79.  2011. RNA PROCESSING FACTOR3 is crucial for the accumulation of mature ccmC transcripts in mitochondria of Arabidopsis accession Columbia. Plant Physiol. 157:1430–39 [Google Scholar]
  80. Jonietz C, Forner J, Hölzle A, Thuss S, Binder S. 80.  2010. RNA PROCESSING FACTOR2 is required for 5′ end processing of nad9 and cox3 mRNAs in mitochondria of Arabidopsis thaliana. Plant Cell 22:443–53 [Google Scholar]
  81. Karcher D, Kahlau S, Bock R. 81.  2008. Faithful editing of a tomato-specific mRNA editing site in transgenic tobacco chloroplasts. RNA 14:217–24 [Google Scholar]
  82. Karpenahalli MR, Lupas AN, Soding J. 82.  2007. TPRpred: a tool for prediction of TPR-, PPR- and SEL1-like repeats from protein sequences. BMC Bioinforma. 8:2 [Google Scholar]
  83. Kazama T, Nakamura T, Watanabe M, Sugita M, Toriyama K. 83.  2008. Suppression mechanism of mitochondrial ORF79 accumulation by Rf1 protein in BT-type cytoplasmic male sterile rice. Plant J. 55:619–28 [Google Scholar]
  84. Kazama T, Toriyama K. 84.  2003. A pentatricopeptide repeat-containing gene that promotes the processing of aberrant atp6 RNA of cytoplasmic male-sterile rice. FEBS Lett. 544:99–102 [Google Scholar]
  85. Ke J, Chen RZ, Ban T, Zhou XE, Gu X. 85.  et al. 2013. Structural basis for RNA recognition by a dimeric PPR-protein complex. Nat. Struct. Mol. Biol. 20:1377–82 [Google Scholar]
  86. Khrouchtchova A, Monde RA, Barkan A. 86.  2012. A short PPR protein required for the splicing of specific group II introns in angiosperm chloroplasts. RNA 18:1197–209 [Google Scholar]
  87. Kim S, Yang J, Moon S, Ryu C, An K. 87.  et al. 2009. Rice OGR1 encodes a pentatricopeptide repeat–DYW protein and is essential for RNA editing in mitochondria. Plant J. 59:738–49 [Google Scholar]
  88. Klein RR, Klein PE, Mullet JE, Minx P, Rooney WL, Schertz KF. 88.  2005. Fertility restorer locus Rf1 of sorghum (Sorghum bicolor L.) encodes a pentatricopeptide repeat protein not present in the colinear region of rice chromosome 12. Theor. Appl. Genet. 111:994–1012 [Google Scholar]
  89. Kleine T. 89.  2012. Arabidopsis thaliana mTERF proteins: evolution and functional classification. Front. Plant Sci. 3:233 [Google Scholar]
  90. Klodmann J, Senkler M, Rode C, Braun HP. 90.  2011. Defining the protein complex proteome of plant mitochondria. Plant Physiol. 157:587–98 [Google Scholar]
  91. Knoop V, Rüdinger M. 91.  2010. DYW-type PPR proteins in a heterolobosean protist: plant RNA editing factors involved in an ancient horizontal gene transfer?. FEBS Lett. 584:4287–91 [Google Scholar]
  92. Kobayashi K, Suzuki M, Tang J, Nagata N, Ohyama K. 92.  et al. 2007. LOVASTATIN INSENSITIVE 1, a novel pentatricopeptide repeat protein, is a potential regulatory factor of isoprenoid biosynthesis in Arabidopsis. Plant Cell Physiol. 48:322–31 [Google Scholar]
  93. Kobayashi Y, Matsuo M, Sakamoto K, Wakasugi T, Yamada K, Obokata J. 93.  2008. 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. 36:311–18 [Google Scholar]
  94. Kobe B, Kajava AV. 94.  2000. When protein folding is simplified to protein coiling: the continuum of solenoid protein structures. Trends Biochem. Sci. 25:509–15 [Google Scholar]
  95. Koizuka N, Imai R, Fujimoto H, Hayakawa T, Kimura Y. 95.  et al. 2003. Genetic characterization of a pentatricopeptide repeat protein gene, orf687, that restores fertility in the cytoplasmic male-sterile Kosena radish. Plant J. 34:407–15 [Google Scholar]
  96. Komori T, Ohta S, Murai N, Takakura Y, Kuraya Y. 96.  et al. 2004. Map-based cloning of a fertility restorer gene, Rf-1, in rice (Oryza sativa L.). Plant J. 37:315–25 [Google Scholar]
  97. Koprivova A, Colas des Francs-Small C, Calder G, Mugford ST, Tanz S. 97.  et al. 2010. Identification of a pentatricopeptide repeat protein implicated in splicing of intron 1 of mitochondrial nad7 transcripts. J. Biol. Chem. 285:32192–99 [Google Scholar]
  98. Kotera E, Tasaka M, Shikanai T. 98.  2005. A pentatricopeptide repeat protein is essential for RNA editing in chloroplasts. Nature 433:326–30 [Google Scholar]
  99. Koussevitzky S, Nott A, Mockler TC, Hong F, Sachetto-Martins G. 99.  et al. 2007. Signals from chloroplasts converge to regulate nuclear gene expression. Science 316:715–19 [Google Scholar]
  100. Krishnasamy S, Makaroff CA. 100.  1994. Organ-specific reduction in the abundance of a mitochondrial protein accompanies fertility restoration in cytoplasmic male-sterile radish. Plant Mol. Biol. 26:935–46 [Google Scholar]
  101. Liu S, Melonek J, Boykin L, Small I, Howell K. 101.  2013. PPR-SMRs: ancient proteins with enigmatic functions. RNA Biol. 10:1312–21 [Google Scholar]
  102. Liu X, Yu F, Rodermel S. 102.  2010. An Arabidopsis pentatricopeptide repeat protein, SUPPRESSOR OF VARIEGATION7, is required for FtsH-mediated chloroplast biogenesis. Plant Physiol. 154:1588–601 [Google Scholar]
  103. Liu Y, He J, Chen Z, Ren X, Hong X, Gong Z. 103.  2010. ABA overly-sensitive 5 (ABO5), encoding a pentatricopeptide repeat protein required for cis-splicing of mitochondrial nad2 intron 3, is involved in the abscisic acid response in Arabidopsis. Plant J. 63:749–65 [Google Scholar]
  104. Liu YJ, Xiu ZH, Meeley R, Tan BC. 104.  2013. Empty pericarp5 encodes a pentatricopeptide repeat protein that is required for mitochondrial RNA editing and seed development in maize. Plant Cell 25:868–83 [Google Scholar]
  105. Loiselay C, Gumpel NJ, Girard-Bascou J, Watson AT, Purton S. 105.  et al. 2008. Molecular identification and function of cis- and trans-acting determinants for petA transcript stability in Chlamydomonas reinhardtii chloroplasts. Mol. Cell. Biol. 28:5529–42 [Google Scholar]
  106. Lu Y, Li C, Wang H, Chen H, Berg H, Xia Y. 106.  2011. AtPPR2, an Arabidopsis pentatricopeptide repeat protein, binds to plastid 23S rRNA and plays an important role in the first mitotic division during gametogenesis and in cell proliferation during embryogenesis. Plant J. 67:13–25 [Google Scholar]
  107. Lukes J, Archibald JM, Keeling PJ, Doolittle WF, Gray MW. 107.  2011. How a neutral evolutionary ratchet can build cellular complexity. IUBMB Life 63:528–37 [Google Scholar]
  108. Lurin C, Andrés C, Aubourg S, Bellaoui M, Bitton F. 108.  et al. 2004. Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16:2089–103 [Google Scholar]
  109. Maier UG, Bozarth A, Funk HT, Zauner S, Rensing SA. 109.  et al. 2008. Complex chloroplast RNA metabolism: just debugging the genetic programme?. BMC Biol. 6:36 [Google Scholar]
  110. Maliga P, Bock R. 110.  2011. Plastid biotechnology: food, fuel, and medicine for the 21st century. Plant Physiol. 155:1501–10 [Google Scholar]
  111. Manavski N, Guyon V, Meurer J, Wienand U, Brettschneider R. 111.  2012. An essential pentatricopeptide repeat protein facilitates 5′ maturation and translation initiation of rps3 mRNA in maize mitochondria. Plant Cell 24:3087–105 [Google Scholar]
  112. Meierhoff K, Felder S, Nakamura T, Bechtold N, Schuster G. 112.  2003. HCF152, an Arabidopsis RNA binding pentatricopeptide repeat protein involved in the processing of chloroplast psbB-psbT-psbH-petB-petD RNAs. Plant Cell 15:1480–95 [Google Scholar]
  113. Merendino L, Perron K, Rahire M, Howald I, Rochaix JD, Goldschmidt-Clermont M. 113.  2006. A novel multifunctional factor involved in trans-splicing of chloroplast introns in Chlamydomonas. Nucleic Acids Res. 34:262–74 [Google Scholar]
  114. Miyamoto T, Obokata J, Sugiura M. 114.  2004. A site-specific factor interacts directly with its cognate RNA editing site in chloroplast transcripts. Proc. Natl. Acad. Sci. USA 101:48–52 [Google Scholar]
  115. Murayama M, Hayashi S, Nishimura N, Ishide M, Kobayashi K. 115.  et al. 2012. Isolation of Arabidopsis ahg11, a weak ABA hypersensitive mutant defective in nad4 RNA editing. J. Exp. Bot. 63:5301–10 [Google Scholar]
  116. Nakamura T, Meierhoff K, Westhoff P, Schuster G. 116.  2003. RNA-binding properties of HCF152, an Arabidopsis PPR protein involved in the processing of chloroplast RNA. Eur. J. Biochem. 270:4070–81 [Google Scholar]
  117. Nakamura T, Sugita M. 117.  2008. A conserved DYW domain of the pentatricopeptide repeat protein possesses a novel endoribonuclease activity. FEBS Lett. 582:4163–68 [Google Scholar]
  118. O'Toole N, Hattori M, Andrés C, Iida K, Lurin C. 118.  et al. 2008. On the expansion of the pentatricopeptide repeat gene family in plants. Mol. Biol. Evol. 25:1120–28 [Google Scholar]
  119. Okuda K, Chateigner-Boutin AL, Nakamura T, Delannoy E, Sugita M. 119.  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 21:146–56 [Google Scholar]
  120. Okuda K, Myouga F, Motohashi R, Shinozaki K, Shikanai T. 120.  2007. Conserved domain structure of pentatricopeptide repeat proteins involved in chloroplast RNA editing. Proc. Natl. Acad. Sci. USA 104:8178–83 [Google Scholar]
  121. Okuda K, Nakamura T, Sugita M, Shimizu T, Shikanai T. 121.  2006. A pentatricopeptide repeat protein is a site recognition factor in chloroplast RNA editing. J. Biol. Chem. 281:37661–67 [Google Scholar]
  122. Okuda K, Shikanai T. 122.  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. 40:5052–64 [Google Scholar]
  123. Petricka J, Clay N, Nelson T. 123.  2008. Vein patterning screens and the defectively organized tributaries mutants in Arabidopsis thaliana. Plant J. 56:251–63 [Google Scholar]
  124. Pfalz J, Bayraktar O, Prikryl J, Barkan A. 124.  2009. Site-specific binding of a PPR protein defines and stabilizes 5′ and 3′ mRNA termini in chloroplasts. EMBO J. 28:2042–52 [Google Scholar]
  125. Pfalz J, Liere K, Kandlbinder A, Dietz KJ, Oelmüller R. 125.  2006. pTAC2, -6, and -12 are components of the transcriptionally active plastid chromosome that are required for plastid gene expression. Plant Cell 18:176–97 [Google Scholar]
  126. Preker PJ, Keller W. 126.  1998. The HAT helix, a repetitive motif implicated in RNA processing. Trends Biochem. Sci. 23:15–16 [Google Scholar]
  127. Prikryl J, Rojas M, Schuster G, Barkan A. 127.  2011. Mechanism of RNA stabilization and translational activation by a pentatricopeptide repeat protein. Proc. Natl. Acad. Sci. USA 108:415–20 [Google Scholar]
  128. Rahire M, Laroche F, Cerutti L, Rochaix JD. 128.  2012. Identification of an OPR protein involved in the translation initiation of the PsaB subunit of photosystem I. Plant J. 72:652–61 [Google Scholar]
  129. Raynaud C, Loiselay C, Wostrikoff K, Kuras R, Girard-Bascou J. 129.  et al. 2007. Evidence for regulatory function of nucleus-encoded factors on mRNA stabilization and translation in the chloroplast. Proc. Natl. Acad. Sci. USA 104:9093–98 [Google Scholar]
  130. Ringel R, Sologub M, Morozov YI, Litonin D, Cramer P, Temiakov D. 130.  2011. Structure of human mitochondrial RNA polymerase. Nature 478:269–73 [Google Scholar]
  131. Rivals E, Bruyére C, Toffano-Nioche C, Lecharny A. 131.  2006. Formation of the Arabidopsis pentatricopeptide repeat family. Plant Physiol. 141:825–39 [Google Scholar]
  132. Rubinson EH, Eichman BF. 132.  2012. Nucleic acid recognition by tandem helical repeats. Curr. Opin. Struct. Biol. 22:101–9 [Google Scholar]
  133. Ruckle M, Larkin R. 133.  2009. Plastid signals that affect photomorphogenesis in Arabidopsis thaliana are dependent on GENOMES UNCOUPLED 1 and cryptochrome 1. New Phytol. 182:367–79 [Google Scholar]
  134. Rüdinger M, Fritz-Laylin L, Polsakiewicz M, Knoop V. 134.  2011. Plant-type mitochondrial RNA editing in the protist Naegleria gruberi. RNA 17:2058–62 [Google Scholar]
  135. Rüdinger M, Kindgren P, Zehrmann A, Small I, Knoop V. 135.  2013. A DYW-protein knockout in Physcomitrella affects two closely spaced mitochondrial editing sites and causes a severe developmental phenotype. Plant J. 76:420–32 [Google Scholar]
  136. Rüdinger M, Volkmar U, Lenz H, Groth-Malonek M, Knoop V. 136.  2012. Nuclear DYW-type PPR gene families diversify with increasing RNA editing frequencies in liverwort and moss mitochondria. J. Mol. Evol. 74:37–51 [Google Scholar]
  137. Ruwe H, Schmitz-Linneweber C. 137.  2012. Short non-coding RNA fragments accumulating in chloroplasts: footprints of RNA binding proteins?. Nucleic Acids Res. 40:3106–16 [Google Scholar]
  138. Salone V, Rüdinger M, Polsakiewicz M, Hoffmann B, Groth-Malonek M. 138.  et al. 2007. A hypothesis on the identification of the editing enzyme in plant organelles. FEBS Lett. 581:4132–38 [Google Scholar]
  139. Sane AP, Stein B, Westhoff P. 139.  2005. The nuclear gene HCF107 encodes a membrane-associated R-TPR (RNA tetratricopeptide repeat)-containing protein involved in expression of the plastidial psbH gene in Arabidopsis. Plant J. 42:720–30 [Google Scholar]
  140. Schallenberg-Rüdinger M, Lenz H, Polsakiewicz M, Gott J, Knoop V. 140.  2013. A survey of PPR proteins identifies DYW domains like those of land plant RNA editing factors in diverse eukaryotes. RNA Biol. 10:1343–50 [Google Scholar]
  141. Schmitz-Linneweber C, Small I. 141.  2008. Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci. 13:663–70 [Google Scholar]
  142. Schmitz-Linneweber C, Williams-Carrier RE, Barkan A. 142.  2005. RNA immunoprecipitation and microarray analysis show a chloroplast pentatricopeptide repeat protein to be associated with the 5′-region of mRNAs whose translation it activates. Plant Cell 17:2791–804 [Google Scholar]
  143. Schmitz-Linneweber C, Williams-Carrier RE, Williams-Voelker PM, Kroeger TS, Vichas A, Barkan A. 143.  2006. A pentatricopeptide repeat protein facilitates the trans-splicing of the maize chloroplast rps12 pre-mRNA. Plant Cell 18:2650–63 [Google Scholar]
  144. Shikanai T, Fujii S. 144.  2013. Function of PPR proteins in plastid gene expression. RNA Biol. 10:1263–73 [Google Scholar]
  145. Small I, Peeters N. 145.  2000. The PPR motif—a TPR-related motif prevalent in plant organellar proteins. Trends Biochem. Sci. 25:46–47 [Google Scholar]
  146. Sosso D, Canut M, Gendrot G, Dedieu A, Chambrier P. 146.  et al. 2012. PPR8522 encodes a chloroplast-targeted pentatricopeptide repeat protein necessary for maize embryogenesis and vegetative development. J. Exp. Bot. 63:5843–57 [Google Scholar]
  147. Sosso D, Mbelo S, Vernoud V, Gendrot G, Dedieu A. 147.  et al. 2012. PPR2263, a DYW-subgroup pentatricopeptide repeat protein, is required for mitochondrial nad5 and cob transcript editing, mitochondrion biogenesis, and maize growth. Plant Cell 24:676–91 [Google Scholar]
  148. Sun T, Germain A, Giloteaux L, Hammani K, Barkan A. 148.  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:E1169–78 [Google Scholar]
  149. Sung T, Tseng C, Hsieh M. 149.  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 [Google Scholar]
  150. Takenaka M, Brennicke A. 150.  2012. Using multiplex single-base extension typing to screen for mutants defective in RNA editing. Nat. Protoc. 7:1931–45 [Google Scholar]
  151. Takenaka M, Neuwirt J, Brennicke A. 151.  2004. Complex cis-elements determine an RNA editing site in pea mitochondria. Nucleic Acids Res. 32:4137–44 [Google Scholar]
  152. Takenaka M, Zehrmann A, Brennicke A, Graichen K. 152.  2013. Improved computational target site prediction for pentatricopeptide repeat RNA editing factors. PLoS ONE 8:e65343 [Google Scholar]
  153. Takenaka M, Zehrmann A, Verbitskiy D, Kugelmann M, Hartel B, Brennicke A. 153.  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 109:5104–9 [Google Scholar]
  154. Tameshige T, Fujita H, Watanabe K, Toyokura K, Kondo M. 154.  et al. 2013. Pattern dynamics in adaxial-abaxial specific gene expression are modulated by a plastid retrograde signal during Arabidopsis thaliana leaf development. PLoS Genet. 9:e1003655 [Google Scholar]
  155. Tasaki E, Hattori M, Sugita M. 155.  2010. The moss pentatricopeptide repeat protein with a DYW domain is responsible for RNA editing of mitochondrial ccmFc transcript. Plant J. 62:560–70 [Google Scholar]
  156. Taylor NL, Heazlewood JL, Millar AH. 156.  2011. The Arabidopsis thaliana 2-D gel mitochondrial proteome: refining the value of reference maps for assessing protein abundance, contaminants and post-translational modifications. Proteomics 11:1720–33 [Google Scholar]
  157. Terry M, Smith A. 157.  2013. A model for tetrapyrrole synthesis as the primary mechanism for plastid-to-nucleus signaling during chloroplast biogenesis. Front. Plant Sci. 4:14 [Google Scholar]
  158. Tillich M, Poltnigg P, Kushnir S, Schmitz-Linneweber C. 158.  2006. Maintenance of plastid RNA editing activities independently of their target sites. EMBO Rep. 7:308–13 [Google Scholar]
  159. Touzet P, Budar F. 159.  2004. Unveiling the molecular arms race between two conflicting genomes in cytoplasmic male sterility?. Trends Plant Sci. 9:568–70 [Google Scholar]
  160. Tseng C, Sung T, Li Y, Hsu S, Lin C, Hsieh M. 160.  2010. Editing of accD and ndhF chloroplast transcripts is partially affected in the Arabidopsis vanilla cream1 mutant. Plant Mol. Biol. 73:309–23 [Google Scholar]
  161. Uyttewaal M, Arnal N, Quadrado M, Martin-Canadell A, Vrielynck N. 161.  et al. 2008. Characterization of Raphanus sativus pentatricopeptide repeat proteins encoded by the fertility restorer locus for Ogura cytoplasmic male sterility. Plant Cell 20:3331–45 [Google Scholar]
  162. Uyttewaal M, Mireau H, Rurek M, Hammani K, Arnal N. 162.  et al. 2008. PPR336 is associated with polysomes in plant mitochondria. J. Mol. Biol. 375:626–36 [Google Scholar]
  163. Vaistij FE, Boudreau E, Lemaire SD, Goldschmidt-Clermont M, Rochaix JD. 163.  2000. Characterization of Mbb1, a nucleus-encoded tetratricopeptide-like repeat protein required for expression of the chloroplast psbB/psbT/psbH gene cluster in Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 97:14813–18 [Google Scholar]
  164. Wang X, McLachlan J, Zamore PD, Hall TM. 164.  2002. Modular recognition of RNA by a human pumilio-homology domain. Cell 110:501–12 [Google Scholar]
  165. Wang Y, Wang Z, Hall TM. 165.  2013. Engineered proteins with Pumilio/fem-3 mRNA binding scaffold to manipulate RNA metabolism. FEBS J. 280:3755–67 [Google Scholar]
  166. Wang Z, Zou Y, Li X, Zhang Q, Chen L. 166.  et al. 2006. Cytoplasmic male sterility of rice with Boro II cytoplasm is caused by a cytotoxic peptide and is restored by two related PPR motif genes via distinct modes of mRNA silencing. Plant Cell 18:676–87 [Google Scholar]
  167. Williams P, Barkan A. 167.  2003. A chloroplast-localized PPR protein required for plastid ribosome accumulation. Plant J. 36:675–86 [Google Scholar]
  168. Williams-Carrier R, Kroeger T, Barkan A. 168.  2008. Sequence-specific binding of a chloroplast pentatricopeptide repeat protein to its native group II intron ligand. RNA 14:1930–41 [Google Scholar]
  169. Yagi Y, Hayashi S, Kobayashi K, Hirayama T, Nakamura T. 169.  2013. Elucidation of the RNA recognition code for pentatricopeptide repeat proteins involved in organelle RNA editing in plants. PLoS ONE 8:e57286 [Google Scholar]
  170. Yagi Y, Tachikawa M, Noguchi H, Satoh S, Obokata J, Nakamura T. 170.  2013. Pentatricopeptide repeat proteins involved in plant organellar RNA editing. RNA Biol. 10:1236–42 [Google Scholar]
  171. Yamazaki H, Tasaka M, Shikanai T. 171.  2004. PPR motifs of the nucleus-encoded factor, PGR3, function in the selective and distinct steps of chloroplast gene expression in Arabidopsis. Plant J. 38:152–63 [Google Scholar]
  172. Yin P, Li Q, Yan C, Liu Y, Liu J. 172.  et al. 2013. Structural basis for the modular recognition of single-stranded RNA by PPR proteins. Nature 504:168–71 [Google Scholar]
  173. Yu Q, Jiang Y, Chong K, Yang Z. 173.  2009. AtECB2, a pentatricopeptide repeat protein, is required for chloroplast transcript accD RNA editing and early chloroplast biogenesis in Arabidopsis thaliana. Plant J. 59:1011–23 [Google Scholar]
  174. Yuan H, Liu D. 174.  2012. Functional disruption of the pentatricopeptide protein SLG1 affects mitochondrial RNA editing, plant development, and responses to abiotic stresses in Arabidopsis. Plant J. 70:432–44 [Google Scholar]
  175. Yukawa M, Kuroda H, Sugiura M. 175.  2007. A new in vitro translation system for non-radioactive assay from tobacco chloroplasts: effect of pre-mRNA processing on translation in vitro. Plant J. 49:367–76 [Google Scholar]
  176. Zhang YF, Hou MM, Tan BC. 176.  2013. The requirement of WHIRLY1 for embryogenesis is dependent on genetic background in maize. PLoS ONE 8:e67369 [Google Scholar]
  177. Zhelyazkova P, Hammani K, Rojas M, Voelker R, Vargas-Suárez M. 177.  et al. 2012. Protein-mediated protection as the predominant mechanism for defining processed mRNA termini in land plant chloroplasts. Nucleic Acids Res. 40:3092–105 [Google Scholar]
  178. Zhou W, Cheng Y, Yap A, Chateigner-Boutin A, Delannoy E. 178.  et al. 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 [Google Scholar]
  179. Zhu Q, Dugardeyn J, Zhang C, Takenaka M, Kuhn K. 179.  et al. 2012. SLO2, a mitochondrial pentatricopeptide repeat protein affecting several RNA editing sites, is required for energy metabolism. Plant J. 71:836–49 [Google Scholar]
  180. Zoschke R, Kroeger T, Belcher S, Schottler MA, Barkan A, Schmitz-Linneweber C. 180.  2012. The pentatricopeptide repeat-SMR protein ATP4 promotes translation of the chloroplast atpB/E mRNA. Plant J. 72:547–58 [Google Scholar]
  181. Zoschke R, Qu Y, Zubo YO, Börner T, Schmitz-Linneweber C. 181.  2013. Mutation of the pentatricopeptide repeat-SMR protein SVR7 impairs accumulation and translation of chloroplast ATP synthase subunits in Arabidopsis thaliana. J. Plant Res. 126:403–14 [Google Scholar]
  182. Zoschke R, Watkins K, Barkan A. 182.  2013. A rapid microarray-based ribosome profiling method elucidates chloroplast ribosome behavior in vivo. Plant Cell 25:2265–75 [Google Scholar]
  183. Zsigmond L, Szepesi A, Tari I, Rigó G, Király A, Szabados L. 183.  2012. Overexpression of the mitochondrial PPR40 gene improves salt tolerance in Arabidopsis. Plant Sci. 182:87–93 [Google Scholar]

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