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Function of chloroplast RNA-binding proteins

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Abstract

Chloroplasts are eukaryotic organelles which represent evolutionary chimera with proteins that have been derived from either a prokaryotic endosymbiont or a eukaryotic host. Chloroplast gene expression starts with transcription of RNA and is followed by multiple post-transcriptional processes which are mediated mainly by an as yet unknown number of RNA-binding proteins. Here, we review the literature to date on the structure and function of these chloroplast RNA-binding proteins. For example, the functional protein domains involved in RNA binding, such as the RNA-recognition motifs, the chloroplast RNA-splicing and ribosome maturation domains, and the pentatricopeptide-repeat motifs, are summarized. We also describe biochemical and forward genetic approaches that led to the identification of proteins modifying RNA stability or carrying out RNA splicing or editing. Such data will greatly contribute to a better understanding of the biogenesis of a unique organelle found in all photosynthetic organisms.

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References

  1. Arnon DI (1959) Conversion of light into chemical energy in photosynthesis. Nature 184:10–21

    CAS  PubMed  Google Scholar 

  2. Wakasugi T, Tsudzuki T, Sugiura M (2001) The genomics of land plant chloroplasts: gene content and alteration of genomic information by RNA editing. Photosynth Res 70:107–118

    Article  CAS  PubMed  Google Scholar 

  3. Sagan L (1967) On the origin of mitosing cells. J Theor Biol 14:255–274

    Article  CAS  PubMed  Google Scholar 

  4. Gray MW, Burger G, Lang BF (2001) The origin and early evolution of mitochondria. Genome Biol 2:reviews1018.1011–1018.1015

    Google Scholar 

  5. Gould SB, Waller RF, McFadden GI (2008) Plastid evolution. Annu Rev Plant Biol 59:491–517

    Article  CAS  PubMed  Google Scholar 

  6. Delwiche CF (1999) Tracing the thread of plastid diversity through the tapestry of life. Am Nat 154:S164–S177

    Article  PubMed  Google Scholar 

  7. Timmis JN, Ayliffe MA, Huang CY, Martin W (2004) Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet 5:123–135

    Article  CAS  PubMed  Google Scholar 

  8. Kaneko T, Tabata S (1997) Complete genome structure of the unicellular cyanobacterium Synechocystis sp. PCC6803. Plant Cell Physiol 38:1171–1176

    CAS  PubMed  Google Scholar 

  9. Meeks JC, Elhai J, Thiel T, Potts M, Larimer F, Lamerdin J, Predki P, Atlas R (2001) An overview of the genome of Nostoc punctiforme, a multicellular, symbiotic cyanobacterium. Photosynth Res 70:85–106

    Article  CAS  PubMed  Google Scholar 

  10. Richly E, Leister D (2004) An improved prediction of chloroplast proteins reveals diversities and commonalities in the chloroplast proteomes of Arabidopsis and rice. Gene 329:11–16

    Article  CAS  PubMed  Google Scholar 

  11. Jarvis P (2004) Organellar proteomics: chloroplasts in the spotlight. Curr Biol 14:R317–R319

    Article  CAS  PubMed  Google Scholar 

  12. Barbrook AC, Howe CJ, Kurniawan DP, Tarr SJ (2010) Organization and expression of organellar genomes. Philos Trans R Soc Lond B Biol Sci 365:785–797

    Article  CAS  PubMed  Google Scholar 

  13. Woodson JD, Chory J (2008) Coordination of gene expression between organellar and nuclear genomes. Nat Rev Genet 9:383–395

    Article  CAS  PubMed  Google Scholar 

  14. Bohne AV, Schwarz C, Jallal A, Ossenbühl F, Nickelsen J (2009) Control of organellar gene expression in Chlamydomonas reinhardtii – future perspectives. Endocytobiosis Cell Res 19:70–80

    Google Scholar 

  15. Del Campo EM (2009) Post-transcriptional control of chloroplast gene expression. Gene Regul Syst Bio 3:31–47

    PubMed  Google Scholar 

  16. Fedoroff NV (2002) RNA-binding proteins in plants: the tip of an iceberg? Curr Opin Plant Biol 5:452–459

    Article  CAS  PubMed  Google Scholar 

  17. Stern DB, Goldschmidt-Clermont M, Hanson MR (2010) Chloroplast RNA metabolism. Annu Rev Plant Biol 61:125–155

    Article  CAS  PubMed  Google Scholar 

  18. Lunde BM, Moore C, Varani G (2007) RNA-binding proteins: modular design for efficient function. Nat Rev Mol Cell Biol 8:479–490

    Article  CAS  PubMed  Google Scholar 

  19. Lorkovic ZJ (2009) Role of plant RNA-binding proteins in development, stress response and genome organization. Trends Plant Sci 14:229–236

    Article  CAS  PubMed  Google Scholar 

  20. Ostersetzer O, Cooke AM, Watkins KP, Barkan A (2005) CRS1, a chloroplast group II intron splicing factor, promotes intron folding through specific interactions with two intron domains. Plant Cell 17:241–255

    Article  CAS  PubMed  Google Scholar 

  21. 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

    Article  CAS  PubMed  Google Scholar 

  22. Boudreau E, Nickelsen J, Lemaire SD, Ossenbühl F, Rochaix JD (2000) The Nac2 gene of Chlamydomonas encodes a chloroplast TPR-like protein involved in psbD mRNA stability. EMBO J 19:3366–3376

    Article  CAS  PubMed  Google Scholar 

  23. Maris C, Dominguez C, Allain FH (2005) The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression. FEBS J 272:2118–2131

    Article  CAS  PubMed  Google Scholar 

  24. Maruyama K, Sato N, Ohta N (1999) Conservation of structure and cold-regulation of RNA-binding proteins in cyanobacteria: probable convergent evolution with eukaryotic glycine-rich RNA-binding proteins. Nucleic Acids Res 27:2029–2036

    Article  CAS  PubMed  Google Scholar 

  25. Adam SA, Nakagawa T, Swanson MS, Woodruff TK, Dreyfuss G (1986) mRNA polyadenylate-binding protein: gene isolation and sequencing and identification of a ribonucleoprotein consensus sequence. Mol Cell Biol 6:2932–2943

    CAS  PubMed  Google Scholar 

  26. Clery A, Blatter M, Allain FH (2008) RNA recognition motifs: boring? Not quite. Curr Opin Struct Biol 18:290–298

    Article  CAS  PubMed  Google Scholar 

  27. Burd CG, Dreyfuss G (1994) Conserved structures and diversity of functions of RNA-binding proteins. Science 265:615–621

    Article  CAS  PubMed  Google Scholar 

  28. Ostheimer GJ, Williams-Carrier R, Belcher S, Osborne E, Gierke J, Barkan A (2003) Group II intron splicing factors derived by diversification of an ancient RNA-binding domain. EMBO J 22:3919–3929

    Article  CAS  PubMed  Google Scholar 

  29. Barkan A, Klipcan L, Ostersetzer O, Kawamura T, Asakura Y, Watkins KP (2007) The CRM domain: an RNA binding module derived from an ancient ribosome-associated protein. RNA 13:55–64

    Article  CAS  PubMed  Google Scholar 

  30. Ostheimer GJ, Barkan A, Matthews BW (2002) Crystal structure of E. coli YhbY: a representative of a novel class of RNA binding proteins. Structure 10:1593–1601

    Article  CAS  PubMed  Google Scholar 

  31. Keren I, Klipcan L, Bezawork-Geleta A, Kolton M, Shaya F, Ostersetzer-Biran O (2008) Characterization of the molecular basis of group II intron RNA recognition by CRS1-CRM domains. J Biol Chem 283:23333–23342

    Article  CAS  PubMed  Google Scholar 

  32. Siomi H, Matunis MJ, Michael WM, Dreyfuss G (1993) The premessenger RNA-binding K-protein contains a novel evolutionarily conserved motif. Nucleic Acids Res 21:1193–1198

    Article  CAS  PubMed  Google Scholar 

  33. Valverde R, Edwards L, Regan L (2008) Structure and function of KH domains. FEBS J 275:2712–2726

    Article  CAS  PubMed  Google Scholar 

  34. Grishin NV (2001) KH domain: one motif, two folds. Nucleic Acids Res 29:638–643

    Article  CAS  PubMed  Google Scholar 

  35. Andres C, Lurin C, Small ID (2007) The multifarious roles of PPR proteins in plant mitochondrial gene expression. Physiol Plant 129:14–22

    Article  CAS  Google Scholar 

  36. Small ID, Peeters N (2000) The PPR motif – a TPR-related motif prevalent in plant organellar proteins. Trends Biochem Sci 25:46–47

    Article  CAS  PubMed  Google Scholar 

  37. Das AK, Cohen PT, Barford D (1998) The structure of the tetratricopeptide repeats of protein phosphatase 5: implications for TPR-mediated protein-protein interactions. EMBO J 17:1192–1199

    Article  CAS  PubMed  Google Scholar 

  38. Beick S, Schmitz-Linneweber C, Williams-Carrier R, Jensen B, Barkan A (2008) The pentatricopeptide repeat protein PPR5 stabilizes a specific tRNA precursor in maize chloroplasts. Mol Cell Biol 28:5337–5347

    Article  CAS  PubMed  Google Scholar 

  39. Schmitz-Linneweber C, Williams-Carrier RE, Williams-Voelker PM, Kroeger TS, Vichas A, Barkan A (2006) A pentatricopeptide repeat protein facilitates the trans-splicing of the maize chloroplast rps12 pre-mRNA. Plant Cell 18:2650–2663

    Article  CAS  PubMed  Google Scholar 

  40. 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 U S A 104:8178–8183

    Article  CAS  PubMed  Google Scholar 

  41. Gray MW, Lang BF (1998) Transcription in chloroplasts and mitochondria: a tale of two polymerases. Trends Microbiol 6:1–3

    Article  CAS  PubMed  Google Scholar 

  42. Hess WR, Borner T (1999) Organellar RNA polymerases of higher plants. Int Rev Cytol 190:1–59

    Article  CAS  PubMed  Google Scholar 

  43. Maliga P (1998) Two plastid RNA polymerases of higher plants: an evolving story. Trends Plant Sci 3:4–6

    Article  Google Scholar 

  44. Hedtke B, Borner T, Weihe A (1997) Mitochondrial and chloroplast phage-type RNA polymerases in Arabidopsis. Science 277:809–811

    Article  CAS  PubMed  Google Scholar 

  45. Liere K, Maliga P (1999) In vitro characterization of the tobacco rpoB promoter reveals a core sequence motif conserved between phage-type plastid and plant mitochondrial promoters. EMBO J 18:249–257

    Article  CAS  PubMed  Google Scholar 

  46. Somanchi A, Mayfield SP (1999) Nuclear-chloroplast signalling. Curr Opin Plant Biol 2:404–409

    Article  CAS  PubMed  Google Scholar 

  47. Hajdukiewicz PTJ, Allison LA, Maliga P (1997) The two RNA polymerases encoded by the nuclear and the plastid compartments transcribe distinct groups of genes in tobacco plastids. EMBO J 16:4041–4048

    Article  CAS  PubMed  Google Scholar 

  48. Deng XW, Gruissem W (1987) Control of plastid gene expression during development: the limited role of transcriptional regulation. Cell 49:379–387

    Article  CAS  PubMed  Google Scholar 

  49. Eberhard S, Drapier D, Wollman FA (2002) Searching limiting steps in the expression of chloroplast-encoded proteins: relations between gene copy number, transcription, transcript abundance and translation rate in the chloroplast of Chlamydomonas reinhardtii. Plant J 31:149–160

    Article  CAS  PubMed  Google Scholar 

  50. Choquet Y (2009) 5′ and 3′ ends of chloroplast transcripts can both be stabilised by protein ‘caps’: a new model for polycistronic RNA maturation. EMBO J 28:1989–1990

    Article  CAS  PubMed  Google Scholar 

  51. Monde RA, Schuster G, Stern DB (2000) Processing and degradation of chloroplast mRNA. Biochimie 82:573–582

    Article  CAS  PubMed  Google Scholar 

  52. Nakamura T, Ohta M, Sugiura M, Sugita M (2001) Chloroplast ribonucleoproteins function as a stabilizing factor of ribosome-free mRNAs in the stroma. J Biol Chem 276:147–152

    Article  CAS  PubMed  Google Scholar 

  53. Reddy MK, Nair S, Singh BN, Mudgil Y, Tewari KK, Sopory SK (2001) Cloning and expression of a nuclear encoded plastid specific 33 kDa ribonucleoprotein gene (33RNP) from pea that is light stimulated. Gene 263:179–187

    Article  CAS  PubMed  Google Scholar 

  54. Schuster G, Gruissem W (1991) Chloroplast mRNA 3’ end processing requires a nuclear-encoded RNA-binding protein. EMBO J 10:1493–1502

    CAS  PubMed  Google Scholar 

  55. Ohta M, Sugita M, Sugiura M (1995) Three types of nuclear genes encoding chloroplast RNA-binding proteins (cp29, cp31 and cp33) are present in Arabidopsis thaliana: presence of cp31 in chloroplasts and its homologue in nuclei/cytoplasms. Plant Mol Biol 27:529–539

    Article  CAS  PubMed  Google Scholar 

  56. Cook WB, Walker JC (1992) Identification of a maize nucleic acid-binding protein (NBP) belonging to a family of nuclear-encoded chloroplast proteins. Nucleic Acids Res 20:359–364

    Article  CAS  PubMed  Google Scholar 

  57. Churin Y, Hess WR, Borner T (1999) Cloning and characterization of three cDNAs encoding chloroplast RNA-binding proteins from barley (Hordeum vulgare L.): differential regulation of expression by light and plastid development. Curr Genet 36:173–181

    Article  CAS  PubMed  Google Scholar 

  58. Nakamura T, Ohta M, Sugiura M, Sugita M (1999) Chloroplast ribonucleoproteins are associated with both mRNAs and intron-containing precursor tRNAs. FEBS Lett 460:437–441

    Article  CAS  PubMed  Google Scholar 

  59. Nakamura T, Schuster G, Sugiura M, Sugita M (2004) Chloroplast RNA-binding and pentatricopeptide repeat proteins. Biochem Soc Trans 32:571–574

    Article  CAS  PubMed  Google Scholar 

  60. Drager RG, Zeidler M, Simpson CL, Stern DB (1996) A chloroplast transcript lacking the 3′ inverted repeat is degraded by 3′–>5′ exoribonuclease activity. RNA 2:652–663

    CAS  PubMed  Google Scholar 

  61. Rott R, Drager RG, Stern DB, Schuster G (1996) The 3′ untranslated regions of chloroplast genes in Chlamydomonas reinhardtii do not serve as efficient transcriptional terminators. Mol Gen Genet 252:676–683

    CAS  PubMed  Google Scholar 

  62. Stern DB, Gruissem W (1987) Control of plastid gene expression: 3′ inverted repeats act as mRNA processing and stabilizing elements, but do not terminate transcription. Cell 51:1145–1157

    Article  CAS  PubMed  Google Scholar 

  63. Fargo DC, Hu E, Boynton JE, Gillham NW (2000) Mutations that alter the higher-order structure of its 5′ untranslated region affect the stability of chloroplast rps7 mRNA. Mol Gen Genet 264:291–299

    Article  CAS  PubMed  Google Scholar 

  64. Nickelsen J, Fleischmann M, Boudreau E, Rahire M, Rochaix JD (1999) Identification of cis-acting RNA leader elements required for chloroplast psbD gene expression in Chlamydomonas. Plant Cell 11:957–970

    Article  CAS  PubMed  Google Scholar 

  65. Ossenbühl F, Nickelsen J (2000) cis- and trans-acting determinants for translation of psbD mRNA in Chlamydomonas reinhardtii. Mol Cell Biol 20:8134–8142

    Article  PubMed  Google Scholar 

  66. Suay L, Salvador ML, Abesha E, Klein U (2005) Specific roles of 5′ RNA secondary structures in stabilizing transcripts in chloroplasts. Nucleic Acids Res 33:4754–4761

    Article  CAS  PubMed  Google Scholar 

  67. Zou Z, Eibl C, Koop HU (2003) The stem-loop region of the tobacco psbA 5′ UTR is an important determinant of mRNA stability and translation efficiency. Mol Genet Genomics 269:340–349

    Article  CAS  PubMed  Google Scholar 

  68. Loiselay C, Gumpel NJ, Girard-Bascou J, Watson AT, Purton S, Wollman FA, Choquet Y (2008) Molecular identification and function of cis- and trans-acting determinants for petA transcript stability in Chlamydomonas reinhardtii chloroplasts. Mol Cell Biol 28:5529–5542

    Article  CAS  PubMed  Google Scholar 

  69. Gumpel NJ, Ralley L, Girard-Bascou J, Wollman FA, Nugent JH, Purton S (1995) Nuclear mutants of Chlamydomonas reinhardtii defective in the biogenesis of the cytochrome b6 f complex. Plant Mol Biol 29:921–932

    Article  CAS  PubMed  Google Scholar 

  70. Raynaud C, Loiselay C, Wostrikoff K, Kuras R, Girard-Bascou J, Wollman FA, Choquet Y (2007) Evidence for regulatory function of nucleus-encoded factors on mRNA stabilization and translation in the chloroplast. Proc Natl Acad Sci U S A 104:9093–9098

    Article  CAS  PubMed  Google Scholar 

  71. Johnson X, Wostrikoff K, Finazzi G, Kuras R, Schwarz C, Bujaldon S, Nickelsen J, Stern DB, Wollman FA, Vallon O (2010) MRL1, a conserved pentatricopeptide repeat protein, is required for stabilization of rbcL mRNA in Chlamydomonas and Arabidopsis. Plant Cell 22:234–248

    Article  CAS  PubMed  Google Scholar 

  72. Kuchka MR, Goldschmidt-Clermont M, van Dillewijn J, Rochaix JD (1989) Mutation at the Chlamydomonas nuclear NAC2 locus specifically affects stability of the chloroplast psbD transcript encoding polypeptide D2 of PS II. Cell 58:869–876

    Article  CAS  PubMed  Google Scholar 

  73. Schwarz C, Elles I, Kortmann J, Piotrowski M, Nickelsen J (2007) Synthesis of the D2 protein of photosystem II in Chlamydomonas is controlled by a high molecular mass complex containing the RNA stabilization factor Nac2 and the translational activator RBP40. Plant Cell 19:3627–3639

    Article  CAS  PubMed  Google Scholar 

  74. Monod C, Goldschmidt-Clermont M, Rochaix JD (1992) Accumulation of chloroplast psbB RNA requires a nuclear factor in Chlamydomonas reinhardtii. Mol Gen Genet 231:449–459

    Article  CAS  PubMed  Google Scholar 

  75. Vaistij FE, Goldschmidt-Clermont M, Wostrikoff K, Rochaix JD (2000) Stability determinants in the chloroplast psbB/T/H mRNAs of Chlamydomonas reinhardtii. Plant J 21:469–482

    Article  CAS  PubMed  Google Scholar 

  76. Vaistij FE, Boudreau E, Lemaire SD, Goldschmidt-Clermont M, Rochaix JD (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 U S A 97:14813–14818

    Article  CAS  PubMed  Google Scholar 

  77. Murakami S, Kuehnle K, Stern DB (2005) A spontaneous tRNA suppressor of a mutation in the Chlamydomonas reinhardtii nuclear MCD1 gene required for stability of the chloroplast petD mRNA. Nucleic Acids Res 33:3372–3380

    Article  CAS  PubMed  Google Scholar 

  78. Felder S, Meierhoff K, Sane AP, Meurer J, Driemel C, Plucken H, Klaff P, Stein B, Bechtold N, Westhoff P (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 13:2127–2141

    Article  CAS  PubMed  Google Scholar 

  79. Lezhneva L, Meurer J (2004) The nuclear factor HCF145 affects chloroplast psaA-psaB-rps14 transcript abundance in Arabidopsis thaliana. Plant J 38:740–753

    Article  CAS  PubMed  Google Scholar 

  80. Pfalz J, Bayraktar OA, Prikryl J, Barkan A (2009) Site-specific binding of a PPR protein defines and stabilizes 5′ and 3′ mRNA termini in chloroplasts. EMBO J 28:2042–2052

    Article  CAS  PubMed  Google Scholar 

  81. Michel F, Ferat JL (1995) Structure and activities of group II introns. Annu Rev Biochem 64:435–461

    Article  CAS  PubMed  Google Scholar 

  82. Vallès Y, Halanych KM, Boore JL (2008) Group II introns break new boundaries: presence in a bilaterian’s genome. PLoS ONE 3:e1488

    Article  PubMed  CAS  Google Scholar 

  83. Haugen P, Simon DM, Bhattacharya D (2005) The natural history of group I introns. Trends Genet 21:111–119

    Article  CAS  PubMed  Google Scholar 

  84. Fedorova O, Zingler N (2007) Group II introns: structure, folding and splicing mechanism. Biol Chem 388:665–678

    Article  CAS  PubMed  Google Scholar 

  85. Toor N, Hausner G, Zimmerly S (2001) Coevolution of group II intron RNA structures with their intron-encoded reverse transcriptases. RNA 7:1142–1152

    Article  CAS  PubMed  Google Scholar 

  86. Wahl MC, Will CL, Luhrmann R (2009) The spliceosome: design principles of a dynamic RNP machine. Cell 136:701–718

    Article  CAS  PubMed  Google Scholar 

  87. Bonen L, Vogel J (2001) The ins and outs of group II introns. Trends Genet 17:322–331

    Article  CAS  PubMed  Google Scholar 

  88. Lambowitz AM, Caprara MG, Zimmerly S, Perlman PS (1999) Group I and II ribozymes as RNPs: clues from the past and guides to the future. In: Gesteland RF (ed) The RNA world. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY

    Google Scholar 

  89. Kück U, Godehardt I, Schmidt U (1990) A self-splicing group II intron in the mitochondrial large subunit rRNA (LSUrRNA) gene of the eukaryotic alga Scenedesmus obliquus. Nucleic Acids Res 18:2691–2697

    Article  PubMed  Google Scholar 

  90. Holländer V, Kück U (1999) Group II intron splicing in chloroplasts: identification of mutations determining intron stability and fate of exon RNA. Nucleic Acids Res 27:2345–2353

    Article  PubMed  Google Scholar 

  91. Holländer V, Kück U (1999) Group II intron splicing in Escherichia coli: phenotypes of cis-acting mutations resemble splicing defects observed in organelle RNA processing. Nucleic Acids Res 27:2339–2344

    Article  PubMed  Google Scholar 

  92. Dai L, Zimmerly S (2002) Compilation and analysis of group II intron insertions in bacterial genomes: evidence for retroelement behavior. Nucleic Acids Res 30:1091–1102

    Article  CAS  PubMed  Google Scholar 

  93. Belfort M, Perlman PS (1995) Mechanisms of intron mobility. J Biol Chem 270:30237–30240

    Article  CAS  PubMed  Google Scholar 

  94. Toor N, Keating KS, Pyle AM (2009) Structural insights into RNA splicing. Curr Opin Struct Biol 19:260–266

    Article  CAS  PubMed  Google Scholar 

  95. Faßbender S, Brühl KH, Ciriacy M, Kück U (1994) Reverse transcriptase activity of an intron encoded polypeptide. EMBO J 13:2075–2083

    PubMed  Google Scholar 

  96. Yang J, Mohr G, Perlman PS, Lambowitz AM (1998) Group II intron mobility in yeast mitochondria: target DNA-primed reverse transcription activity of aI1 and reverse splicing into DNA transposition sites in vitro. J Mol Biol 282:505–523

    Article  CAS  PubMed  Google Scholar 

  97. Kück U (1989) The intron of a plastid gene from a green alga contains an open reading frame for a reverse transcriptase-like enzyme. Mol Gen Genet 218:257–265

    Article  PubMed  Google Scholar 

  98. Jenkins BD, Kulhanek DJ, Barkan A (1997) Nuclear mutations that block group II RNA splicing in maize chloroplasts reveal several intron classes with distinct requirements for splicing factors. Plant Cell 9:283–296

    Article  CAS  PubMed  Google Scholar 

  99. Vogel J, Borner T, Hess WR (1999) Comparative analysis of splicing of the complete set of chloroplast group II introns in three higher plant mutants. Nucleic Acids Res 27:3866–3874

    Article  CAS  PubMed  Google Scholar 

  100. Till B, Schmitz-Linneweber C, Williams-Carrier R, Barkan A (2001) CRS1 is a novel group II intron splicing factor that was derived from a domain of ancient origin. RNA 7:1227–1238

    Article  CAS  PubMed  Google Scholar 

  101. Jenkins BD, Barkan A (2001) Recruitment of a peptidyl-tRNA hydrolase as a facilitator of group II intron splicing in chloroplasts. EMBO J 20:872–879

    Article  CAS  PubMed  Google Scholar 

  102. Ostheimer GJ, Rojas M, Hadjivassiliou H, Barkan A (2006) Formation of the CRS2-CAF2 group II intron splicing complex is mediated by a 22-amino acid motif in the COOH-terminal region of CAF2. J Biol Chem 281:4732–4738

    Article  CAS  PubMed  Google Scholar 

  103. Asakura Y, Barkan A (2006) Arabidopsis orthologs of maize chloroplast splicing factors promote splicing of orthologous and species-specific group II introns. Plant Physiol 142:1656–1663

    Article  CAS  PubMed  Google Scholar 

  104. Watkins KP, Kroeger TS, Cooke AM, Williams-Carrier RE, Friso G, Belcher SE, van Wijk KJ, Barkan A (2007) A ribonuclease III domain protein functions in group II intron splicing in maize chloroplasts. Plant Cell 19:2606–2623

    Article  CAS  PubMed  Google Scholar 

  105. Kroeger TS, Watkins KP, Friso G, van Wijk KJ, Barkan A (2009) A plant-specific RNA-binding domain revealed through analysis of chloroplast group II intron splicing. Proc Natl Acad Sci U S A 106:4537–4542

    Article  CAS  PubMed  Google Scholar 

  106. Asakura Y, Barkan A (2007) A CRM domain protein functions dually in group I and group II intron splicing in land plant chloroplasts. Plant Cell 19:3864–3875

    Article  CAS  PubMed  Google Scholar 

  107. Asakura Y, Bayraktar OA, Barkan A (2008) Two CRM protein subfamilies cooperate in the splicing of group IIB introns in chloroplasts. RNA 14:2319–2332

    Article  CAS  PubMed  Google Scholar 

  108. Kück U, Choquet Y, Schneider M, Dron M, Bennoun P (1987) Structural and transcriptional analysis of two homologous genes for the P700 chlorophyll α-apoproteins in Chlamydomonas reinhardtii: evidence for in vivo trans-splicing. EMBO J 6:2185–2195

    PubMed  Google Scholar 

  109. Goldschmidt-Clermont M, Girard-Bascou J, Choquet Y, Rochaix JD (1990) Trans-splicing mutants of Chlamydomonas reinhardtii. Mol Gen Genet 223:417–425

    Article  CAS  PubMed  Google Scholar 

  110. Choquet Y, Goldschmidt-Clermont M, Girard-Bascou J, Kück U, Bennoun P, Rochaix JD (1988) Mutant phenotypes support a trans-splicing mechanism for the expression of the tripartite psaA gene in the C. reinhardtii chloroplast. Cell 52:903–913

    Article  CAS  PubMed  Google Scholar 

  111. Hahn D, Nickelsen J, Hackert A, Kück U (1998) A single nuclear locus is involved in both chloroplast RNA trans-splicing and 3′ end processing. Plant J 15:575–581

    Article  CAS  Google Scholar 

  112. Goldschmidt-Clermont M, Choquet Y, Girard-Bascou J, Michel F, Schirmer-Rahire M, Rochaix JD (1991) A small chloroplast RNA may be required for trans-splicing in Chlamydomonas reinhardtii. Cell 65:135–143

    Article  CAS  PubMed  Google Scholar 

  113. Glanz S, Bunse A, Wimbert A, Balczun C, Kück U (2006) A nucleosome assembly protein-like polypeptide binds to chloroplast group II intron RNA in Chlamydomonas reinhardtii. Nucleic Acids Res 34:5337–5351

    Article  CAS  PubMed  Google Scholar 

  114. Rivier C, Goldschmidt-Clermont M, Rochaix JD (2001) Identification of an RNA-protein complex involved in chloroplast group II intron trans-splicing in Chlamydomonas reinhardtii. EMBO J 20:1765–1773

    Article  CAS  PubMed  Google Scholar 

  115. Merendino L, Perron K, Rahire M, Howald I, Rochaix JD, Goldschmidt-Clermont M (2006) A novel multifunctional factor involved in trans-splicing of chloroplast introns in Chlamydomonas. Nucleic Acids Res 34:262–274

    Article  CAS  PubMed  Google Scholar 

  116. Perron K, Goldschmidt-Clermont M, Rochaix JD (1999) A factor related to pseudouridine synthases is required for chloroplast group II intron trans-splicing in Chlamydomonas reinhardtii. EMBO J 18:6481–6490

    Article  CAS  PubMed  Google Scholar 

  117. Balczun C, Bunse A, Schwarz C, Piotrowski M, Kück U (2006) Chloroplast heat shock protein Cpn60 from Chlamydomonas reinhardtii exhibits a novel function as a group II intron-specific RNA-binding protein. FEBS Lett 580:4527–4532

    Article  CAS  PubMed  Google Scholar 

  118. Balczun C, Bunse A, Hahn D, Bennoun P, Nickelsen J, Kück U (2005) Two adjacent nuclear genes are required for functional complementation of a chloroplast trans-splicing mutant from Chlamydomonas reinhardtii. Plant J 43:636–648

    Article  CAS  PubMed  Google Scholar 

  119. Jacobs J, Glanz S, Bunse-Graßmann A, Kruse O, Kück U (2010) RNA trans-splicing: identification of components of a putative chloroplast spliceosome. Eur J Cell Biol. doi:10.1016/j.ejcb.2010.06.015

  120. Bunse AA, Nickelsen J, Kück U (2001) Intron-specific RNA binding proteins in the chloroplast of the green alga Chlamydomonas reinhardtii. Biochim Biophys Acta 1519:46–54

    CAS  PubMed  Google Scholar 

  121. Sperling J, Azubel M, Sperling R (2008) Structure and function of the pre-mRNA splicing machine. Structure 16:1605–1615

    Article  CAS  PubMed  Google Scholar 

  122. Knoop V (2004) The mitochondrial DNA of land plants: peculiarities in phylogenetic perspective. Curr Genet 46:123–139

    Article  CAS  PubMed  Google Scholar 

  123. Freyer R, KieferMeyer MC, Kossel H (1997) Occurrence of plastid RNA editing in all major lineages of land plants. Proc Natl Acad Sci U S A 94:6285–6290

    Article  CAS  PubMed  Google Scholar 

  124. Lenz H, Rudinger M, Volkmar U, Fischer S, Herres S, Grewe F, Knoop V (2010) Introducing the plant RNA editing prediction and analysis computer tool PREPACT and an update on RNA editing site nomenclature. Curr Genet 56:189–201

    Article  CAS  PubMed  Google Scholar 

  125. Maier RM, Neckermann K, Igloi GL, Kossel H (1995) Complete sequence of the maize chloroplast genome – gene content, hotspots of divergence and fine-tuning of genetic information by transcript editing. J Mol Biol 251:614–628

    Article  CAS  PubMed  Google Scholar 

  126. 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 31:2417–2423

    Article  CAS  PubMed  Google Scholar 

  127. Freyer R, Hoch B, Neckermann K, Maier RM, Kossel H (1993) RNA editing in maize chloroplasts is a processing step independent of splicing and cleavage to monocistronic messenger-RNAs. Plant J 4:621–629

    Article  CAS  PubMed  Google Scholar 

  128. Ruf S, Zeltz P, Kossel H (1994) Complete RNA editing of unspliced and dicistronic transcripts of the intron-containing reading frame irf170 from maize chloroplasts. Proc Natl Acad Sci U S A 91:2295–2299

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  130. Lurin C, Andres C, Aubourg S, Bellaoui M, Bitton F, Bruyere C, Caboche M, Debast C, Gualberto J, Hoffmann B, Lecharny A, Le Ret M, Martin-Magniette ML, Mireau H, Peeters N, Renou JP, 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

    Article  CAS  PubMed  Google Scholar 

  131. Chateigner-Boutin AL, Ramos-Vega M, Guevara-Garcia A, Andres C, de la Luz Gutierrez-Nava M, Cantero A, Delannoy E, Jimenez LF, Lurin C, Small I, Leon P (2008) CLB19, a pentatricopeptide repeat protein required for editing of rpoA and clpP chloroplast transcripts. Plant J 56:590–602

    Article  CAS  PubMed  Google Scholar 

  132. Okuda K, Chateigner-Boutin AL, Nakamura T, Delannoy E, Sugita M, Myouga F, Motohashi R, Shinozaki K, Small I, Shikanaia 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

    Article  CAS  PubMed  Google Scholar 

  133. 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

    Article  CAS  PubMed  Google Scholar 

  134. Zhou W, Cheng Y, Yap A, Chateigner-Boutin AL, 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 58:82–96

    Article  CAS  Google Scholar 

  135. 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

    Article  CAS  PubMed  Google Scholar 

  136. Cai W, Ji D, Peng L, Guo J, Ma J, Zou M, Lu C, Zhang L (2009) LPA66 is required for editing psbF chloroplast transcripts in Arabidopsis. Plant Physiol 150:1260–1271

    Article  CAS  PubMed  Google Scholar 

  137. Yu QB, Jiang Y, Chong K, Yang ZN (2009) AtECB2, a pentatricopeptide repeat protein, is required for chloroplast transcript accD RNA editing and early chloroplast biogenesis in Arabidopsis thaliana. Plant J 59:1011–1023

    Article  CAS  PubMed  Google Scholar 

  138. Hammani K, Okuda K, Tanz SK, Chateigner-Boutin AL, 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

    Article  CAS  PubMed  Google Scholar 

  139. Xu RM, Jokhan L, Cheng XD, Mayeda A, Krainer AR (1997) Crystal structure of human UP1, the domain of hnRNP A1 that contains two RNA-recognition motifs. Structure 5:559–570

    Article  CAS  PubMed  Google Scholar 

  140. Drager RG, Girard-Bascou J, Choquet Y, Kindle KL, Stern DB (1998) In vivo evidence for 5′–>3′ exoribonuclease degradation of an unstable chloroplast mRNA. Plant J 13:85–96

    Article  CAS  PubMed  Google Scholar 

  141. Meierhoff K, Felder S, Nakamura T, Bechtold N, Schuster G (2003) HCF152, an Arabidopsis RNA binding pentatricopeptide repeat protein involved in the processing of chloroplast psbB-psbT-psbH-petB-petD RNAs. Plant Cell 15:1480–1495

    Article  CAS  PubMed  Google Scholar 

  142. de Longevialle AF, Hendrickson L, Taylor NL, Delannoy E, Lurin C, Badger M, Millar AH, Small I (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 56:157–168

    Article  PubMed  CAS  Google Scholar 

  143. Hattori M, Miyake H, Sugita M (2007) A pentatricopeptide repeat protein is required for RNA processing of clpP pre-mRNA in moss chloroplasts. J Biol Chem 282:10773–10782

    Article  CAS  PubMed  Google Scholar 

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  1. Department for General and Molecular Biology, Ruhr-University Bochum, Universitätsstraße 150, 44780, Bochum, Germany

    Jessica Jacobs & Ulrich Kück

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Jacobs, J., Kück, U. Function of chloroplast RNA-binding proteins. Cell. Mol. Life Sci. 68, 735–748 (2011). https://doi.org/10.1007/s00018-010-0523-3

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