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RNA splicing and RNA editing in chloroplasts

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Cell and Molecular Biology of Plastids

Part of the book series: Topics in Current Genetics ((TCG,volume 19))

Abstract

During the evolution of chloroplasts from their bacterial ancestor traits emerged that are absentor rare in bacteria. Prominent among these acquired traits are RNA splicing and RNA editing. Thenumbers and distribution of introns and editing sites in different taxa suggest that editing and splicinghave taken different evolutionary pathways in different chloroplast lineages. Both processes aredependent on nuclear-encoded factors and, intriguingly, PPR (pentatricopeptide repeat) proteins haverecently been recognized as a common player. This review summarizes recent progress in understandingthe mechanisms, regulation, and trans-acting factors for thesetwo types of RNA processing.

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References

  1. 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  PubMed  CAS  Google Scholar 

  2. Balczun C, Bunse A, Hahn D, Bennoun P, Nickelsen J, Kuck 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  PubMed  CAS  Google Scholar 

  3. Balczun C, Bunse A, Schwarz C, Piotrowski M, Kuck 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  PubMed  CAS  Google Scholar 

  4. Barkan A (1989) Tissue-dependent plastid RNA splicing in maize: transcripts from four plastid genes are predominantly unspliced in leaf meristems and roots. Plant Cell 1:437–445

    PubMed  CAS  Google Scholar 

  5. 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  PubMed  CAS  Google Scholar 

  6. Benne R, Van den Burg J, Brakenhoff JP, Sloof P, Van Boom JH, Tromp MC (1986) Major transcript of the frameshifted coxII gene from trypanosome mitochondria contains four nucleotides that are not encoded in the DNA. Cell 46:819–826

    Article  PubMed  CAS  Google Scholar 

  7. Bhattacharya S, Navaratnam N, Morrison JR, Scott J, Taylor WR (1994) Cytosine nucleoside/nucleotide deaminases and apolipoprotein B mRNA editing. Trends Biochem Sci 19:105–106

    Article  PubMed  CAS  Google Scholar 

  8. Bock R (2000) Sense from nonsense: how the genetic information of chloroplasts is altered by RNA editing. Biochimie 82:549–557

    Article  PubMed  CAS  Google Scholar 

  9. Bock R, Hagemann R, Kossel H, Kudla J (1993) Tissue- and stage-specific modulation of RNA editing of the psbF and psbL transcript from spinach plastids–a new regulatory mechanism? Mol Gen Genet 240:238–244

    Article  PubMed  CAS  Google Scholar 

  10. Bock R, Hermann M, Fuchs M (1997) Identification of critical nucleotide positions for plastid RNA editing site recognition. RNA 3:1194–1200

    PubMed  CAS  Google Scholar 

  11. Bock R, Hermann M, Kossel H (1996) In vivo dissection of cis-acting determinants for plastid RNA editing. EMBO J 15:5052–5059

    PubMed  CAS  Google Scholar 

  12. Bock R, Koop HU (1997) Extraplastidic site-specific factors mediate RNA editing in chloroplasts. EMBO J 16:3282–3288

    Article  PubMed  CAS  Google Scholar 

  13. Bock R, Kossel 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 13:4623–4628

    PubMed  CAS  Google Scholar 

  14. Bock R, Maliga P (1995) In vivo testing of a tobacco plastid DNA segment for guide RNA function in psbL editing. Mol Gen Genet 247:439–443

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  16. Cech TR (1986) The generality of self-splicing RNA: relationship to nuclear mRNA splicing. Cell 44:207–210

    Article  PubMed  CAS  Google Scholar 

  17. Chateigner-Boutin AL, Hanson MR (2002) Cross-competition in transgenic chloroplasts expressing single editing sites reveals shared cis elements. Mol Cell Biol 22:8448–8456

    Article  PubMed  CAS  Google Scholar 

  18. Chateigner-Boutin AL, Hanson MR (2003) Developmental co-variation of RNA editing extent of plastid editing sites exhibiting similar cis-elements. Nucleic Acids Res 31:2586–2594

    Article  PubMed  CAS  Google Scholar 

  19. Chaudhuri S, Carrer H, Maliga P (1995) Site-specific factor involved in the editing of the psbL mRNA in tobacco plastids. EMBO J 14:2951–2957

    PubMed  CAS  Google Scholar 

  20. Chaudhuri S, Maliga P (1996) Sequences directing C to U editing of the plastid psbL mRNA are located within a 22 nucleotide segment spanning the editing site. EMBO J 15:5958–5964

    PubMed  CAS  Google Scholar 

  21. Choquet Y, Goldschmidt-Clermont M, Girard-Bascou J, Kuck 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  PubMed  CAS  Google Scholar 

  22. Christopher DA, Hallick RB (1989) Euglena gracilis chloroplast ribosomal protein operon: a new chloroplast gene for ribosomal protein L5 and description of a novel organelle intron category designated group III. Nucleic Acids Res 17:7591–7608

    Article  PubMed  CAS  Google Scholar 

  23. Copertino DW, Hallick RB (1993) Group II and group III introns of twintrons: potential relationships with nuclear pre-mRNA introns. Trends Biochem Sci 18:467–471

    Article  PubMed  CAS  Google Scholar 

  24. Daniels DL, Michels WJ Jr, Pyle AM (1996) Two competing pathways for self-splicing by group II introns: a quantitative analysis of in vitro reaction rates and products. J Mol Biol 256:31–49

    Article  PubMed  CAS  Google Scholar 

  25. Del Campo EM, Sabater B, Martin M (2002) Post-transcriptional control of chloroplast gene expression: Accumulation of stable psaC mRNA is due to downstream RNA cleavages in ndhD gene. J Biol Chem 277:36457–36464

    Article  PubMed  CAS  Google Scholar 

  26. Deshpande NN, Bao Y, Herrin DL (1997) Evidence for light/redox-regulated splicing of psbA pre-RNAs in Chlamydomonas chloroplasts. RNA 3:37–48

    PubMed  CAS  Google Scholar 

  27. Driscoll DM, Wynne JK, Wallis SC, Scott J (1989) An in vitro system for the editing of apolipoprotein B mRNA. Cell 58:519–525

    Article  PubMed  CAS  Google Scholar 

  28. Duff RJ, Moore FB (2005) Pervasive RNA editing among hornwort rbcL transcripts except Leiosporoceros. J Mol Evol 61:571–578

    Article  PubMed  CAS  Google Scholar 

  29. Durrenberger F, Rochaix JD (1991) Chloroplast ribosomal intron of Chlamydomonas reinhardtii: in vitro self-splicing, DNA endonuclease activity and in vivo mobility. EMBO J 10:3495–3501

    PubMed  CAS  Google Scholar 

  30. Eberhard S, Drapier D, Wollman F (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  PubMed  CAS  Google Scholar 

  31. Ems SC, Morden CW, Dixon CK, Wolfe KH, dePamphilis CW, Palmer JD (1995) Transcription, splicing and editing of plastid RNAs in the nonphotosynthetic plant Epifagus virginiana. Plant Mol Biol 29:721–733

    Article  PubMed  CAS  Google Scholar 

  32. Faivre-Nitschke SE, Grienenberger JM, Gualberto JM (1999) A prokaryotic-type cytidine deaminase from Arabidopsis thaliana gene expression and functional characterization. Eur J Biochem 263:896–903

    Article  PubMed  CAS  Google Scholar 

  33. Fiebig A, Stegemann S, Bock R (2004) Rapid evolution of editing sites in a small non-essential plastid gene. Nucl Acids Res 7:3615–3622

    Article  CAS  Google Scholar 

  34. 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 mRNAs. Plant J 4:621–629

    Article  PubMed  CAS  Google Scholar 

  35. Freyer R, Kiefer-Meyer MC, Kossel H (1997) Occurrence of plastid RNA editing in all major lineages of land plants. Proc Natl Acad Sci USA 94:6285–6290

    Article  PubMed  CAS  Google Scholar 

  36. Fromm H, Edelman M, Koller B, Goloubinoff P, Galun E (1986) The enigma of the gene coding for ribosomal protein S12 in the chloroplast of Nicotiana. Nucleic Acids Res 14:883–898

    Article  PubMed  CAS  Google Scholar 

  37. Fuchs M, Maier RM, Zeltz P (2001) RNA editing in higher plant plastids: oligoribonucleotide SSCP analysis allows the proof of base conversion directly at the RNA level. Curr Genet 39:384–387

    Article  PubMed  CAS  Google Scholar 

  38. Glanz S, Bunse A, Wimbert A, Balczun C, Kuck 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  PubMed  CAS  Google Scholar 

  39. Golden BL, Gooding AR, Podell ER, Cech TR (1998) A preorganized active site in the crystal structure of the Tetrahymena ribozyme. Science 282:259–264

    Article  PubMed  CAS  Google Scholar 

  40. 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  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  42. Gott JM, Emeson RB (2000) Functions and mechanisms of RNA editing. Annu Rev Genet 34:499–531

    Article  PubMed  CAS  Google Scholar 

  43. Hallick RB, Hong L, Drager RG, Favreau MR, Monfort A, Orsat B, Spielmann A, Stutz E (1993) Complete sequence of Euglena gracilis chloroplast DNA. Nucleic Acids Res 21:3537–3544

    Article  PubMed  CAS  Google Scholar 

  44. Halls C, Mohr S, Del Campo M, Yang Q, Jankowsky E, Lambowitz AM (2007) Involvement of DEAD-box proteins in group I and group II intron splicing. Biochemical characterization of Mss116p, ATP hydrolysis-dependent and -independent mechanisms, and general RNA chaperone activity. J Mol Biol 365:835–855

    Article  PubMed  CAS  Google Scholar 

  45. Halter C, Peeters N, Hanson M (2004) RNA editing in ribosome-less plastids of iojap maize. Curr Genet 45:331–337

    Article  PubMed  CAS  Google Scholar 

  46. Hashimoto M, Endo T, Peltier G, Tasaka M, Shikanai T (2003) A nucleus-encoded factor, CRR2, is essential for the expression of chloroplast ndhB in Arabidopsis. Plant J 36:541–549

    Article  PubMed  CAS  Google Scholar 

  47. Hayes ML, Reed ML, Hegeman CE, Hanson MR (2006) Sequence elements critical for efficient RNA editing of a tobacco chloroplast transcript in vivo and in vitro. Nucleic Acids Res 34:3742–3754

    Article  PubMed  CAS  Google Scholar 

  48. Hegeman CE, Halter CP, Owens TG, Hanson MR (2005a) Expression of complementary RNA from chloroplast transgenes affects editing efficiency of transgene and endogenous chloroplast transcripts. Nucleic Acids Res 33:1454–1464

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  50. Herrin DL, Bao Y, Thompson AJ, Chen Y-F (1991) Self-splicing of the Chlamydomonas chloroplast psbA introns. Plant Cell 3:10951107

    Google Scholar 

  51. Herrin DL, Chen Y-F, Schmidt GW (1990) RNA splicing in Chlamydomonas chloroplasts: self-splicing of 23S preRNA. J Biol Chem 265:21134–21140

    PubMed  CAS  Google Scholar 

  52. Herrin DL, Schmidt GW (1988) trans-splicing of transcripts for the chloroplast psaA1 gene. In vivo requirement for nuclear gene products. J Biol Chem 263:14601–14604

    PubMed  CAS  Google Scholar 

  53. Herschlag D (1995) RNA chaperones and the RNA folding problem. J Biol Chem 270:20871–20874

    PubMed  CAS  Google Scholar 

  54. Hess WR, Hoch B, Zeltz P, Hubschmann T, Kossel H, Borner T (1994) Inefficient rpl2 splicing in barley mutants with ribosome-deficient plastids. Plant Cell 6:1455–1465

    PubMed  CAS  Google Scholar 

  55. Hetzer M, Wurzer G, Schweyen R, Mueller M (1997) Trans-activation of group II intron splicing by nuclear U5 snRNA. Nature 386:417–420

    Article  PubMed  CAS  Google Scholar 

  56. Hirose T, Fan H, Suzuki JY, Wakasugi T, Tsudzuki T, Kossel H, Sugiura M (1996) Occurrence of silent RNA editing in chloroplasts: its species specificity and the influence of environmental and developmental conditions. Plant Mol Biol 30:667–672

    Article  PubMed  CAS  Google Scholar 

  57. Hirose T, Kusumegi T, Tsudzuki T, Sugiura M (1999) RNA editing sites in tobacco chloroplast transcripts: editing as a possible regulator of chloroplast RNA polymerase activity. Mol Gen Genet 262:462–467

    Article  PubMed  CAS  Google Scholar 

  58. Hirose T, Miyamoto T, Obokata J, Sugiura M (2004) In vitro RNA editing systems from higher plant chloroplasts. Methods Mol Biol 265:333–344

    PubMed  CAS  Google Scholar 

  59. Hirose T, Sugiura M (1997) Both RNA editing and RNA cleavage are required for translation of tobacco chloroplast ndhD mRNA: a possible regulatory mechanism for the expression of a chloroplast operon consisting of functionally unrelated genes. EMBO J 16:6804–6811

    Article  PubMed  CAS  Google Scholar 

  60. 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

    Article  PubMed  CAS  Google Scholar 

  61. Hoch B, Maier RM, Appel K, Igloi GL, Kossel H (1991) Editing of a chloroplast mRNA by creation of an initiation codon. Nature 353:178–180

    Article  PubMed  CAS  Google Scholar 

  62. Holloway SP, Deshpande NN, Herrin DL (1999) The catalytic group-I introns of the psbA gene of Chlamydomonas reinhardtii : core structures, ORFs and evolutionary implications. Curr Genet 36:69–78

    Article  PubMed  CAS  Google Scholar 

  63. Horlitz M, Klaff P (2000) Gene-specific trans-regulatory functions of magnesium for chloroplast mRNA stability in higher plants. J Biol Chem 275:35638–35645

    Article  PubMed  CAS  Google Scholar 

  64. Inada M, Sasaki T, Yukawa M, Tsudzuki T, Sugiura M (2004) A systematic search for RNA editing sites in pea chloroplasts: an editing event causes diversification from the evolutionarily conserved amino acid sequence. Plant Cell Physiol 45:1615–1622

    Article  PubMed  CAS  Google Scholar 

  65. Iost I, Guillerez J, Dreyfus M (1992) Bacteriophage T7 RNA polymerase travels far ahead of ribosomes in vivo. J Bacteriol 174:619–622

    PubMed  CAS  Google Scholar 

  66. 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  PubMed  CAS  Google Scholar 

  67. 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

    PubMed  CAS  Google Scholar 

  68. Johanningmeier U, Heiss S (1993) Construction of a Chlamydomonas reinhardtii mutant with an intronless psbA gene. Plant Mol Biol 22:91–99

    Article  PubMed  CAS  Google Scholar 

  69. Kapoor M, Nagai T, Wakasugi T, Yoshinaga K, Sugiura M (1997) Organization of chloroplast ribosomal RNA genes and in vitro self-splicing activity of the large subunit rRNA intron from the green alga Chlorella vulgaris C-27. Curr Genet 31:503–510

    Article  PubMed  CAS  Google Scholar 

  70. Karcher D, Bock R (1998) Site-selective inhibition of plastid RNA editing by heat shock and antibiotics: a role for plastid translation in RNA editing. Nucleic Acids Res 26:1185–1190

    Article  PubMed  CAS  Google Scholar 

  71. Karcher D, Bock R (2002a) The amino acid sequence of a plastid protein is developmentally regulated by RNA editing. J Biol Chem 277:5570–5574

    Article  PubMed  CAS  Google Scholar 

  72. Karcher D, Bock R (2002b) Temperature sensitivity of RNA editing and intron splicing reactions in the plastid ndhB transcript. Curr Genet 41:48–52

    Article  PubMed  CAS  Google Scholar 

  73. Kim M, Rapp JC, Mullet JE (1993) Direct evidence for selective modulation of psbA, rpoA, rbcL, and 16S RNA stability during barley chloroplast development. Plant Mol Biol 22:447–463

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  75. Kuck U, Choquet Y, Schneider M, Dron M, Bennoun P (1987) Structural and transcription analysis of two homologous genes for the P700 chlorophyll a-apoproteins in Chlamydomonas reinhardii: evidence for in vivo trans-splicing. EMBO J 6:2185–2195

    PubMed  CAS  Google Scholar 

  76. Kugita M, Kaneko A, Yamamoto Y, Takeya Y, Matsumoto T, Yoshinaga K (2003a) The complete nucleotide sequence of the hornwort (Anthoceros formosae) chloroplast genome: insight into the earliest land plants. Nucleic Acids Res 31:716–721

    Article  PubMed  CAS  Google Scholar 

  77. Kugita M, Yamamoto Y, Fujikawa T, Matsumoto T, Yoshinaga K (2003b) RNA editing in hornwort chloroplasts makes more than half the genes functional. Nucleic Acids Res 31:2417–2423

    Article  PubMed  CAS  Google Scholar 

  78. Lahmy S, Barneche F, Derancourt J, Filipowicz W, Delseny M, Echeverria M (2000) A chloroplastic RNA-binding protein is a new member of the PPR family. FEBS Lett 480:255–260

    Article  PubMed  CAS  Google Scholar 

  79. Lambowitz AM, Caprara MG, Zimmerly S, Perlman PS (1999) Group I and group II ribozymes as RNPs: clues to the past and guides to the future. In: Gesteland RF, Cech TR, Atkins JF (eds) The RNA World. 2nd edn Cold Spring Harbor: Cold Spring Harbor Laboratory Press, pp 451–485

    Google Scholar 

  80. Lambowitz AM, Zimmerly S (2004) Mobile group II introns. Annu Rev Genet 38:1–35

    Article  PubMed  CAS  Google Scholar 

  81. Lee J, Herrin DL (2003) Mutagenesis of a light-regulated psbA intron reveals the importance of efficient splicing for photosynthetic growth. Nucleic Acids Res 31:4361–4372

    Article  PubMed  CAS  Google Scholar 

  82. Lehnert V, Jaeger L, Michel F, Westhof E (1996) New loop-loop tertiary interactions in self-splicing introns of subgroup IC and ID: a complete 3D model of the Tetrahymena thermophila ribozyme. Chem Biol 3:993–1009

    Article  PubMed  CAS  Google Scholar 

  83. Lemieux C, Otis C, Turmel M (2000) Ancestral chloroplast genome in Mesostigma viride reveals an early branch of green plant evolution. Nature 403:649–652

    Article  PubMed  CAS  Google Scholar 

  84. Liere K, Link G (1994) Structure and expression characteristics of the chloroplast DNA region containing the split gene for tRNA-gly (UCC) from mustard. Curr Genet 26:557–563

    Article  PubMed  CAS  Google Scholar 

  85. Liere K, Link G (1995) RNA-binding activity of the matK protein encoded by the chloroplast trnK intron from mustard (Sinapis alba L). Nucleic Acids Res 23:917–921

    Article  PubMed  CAS  Google Scholar 

  86. Lorsch JR (2002) RNA chaperones exist and DEAD box proteins get a life. Cell 109:797–800

    Article  PubMed  CAS  Google Scholar 

  87. 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  PubMed  CAS  Google Scholar 

  88. Lynch M, Koskella B, Schaack S (2006) Mutation pressure and the evolution of organelle genomic architecture. Science 311:1727–1730

    Article  PubMed  CAS  Google Scholar 

  89. Maier RM, Hoch B, Zeltz P, Kossel H (1992a) Internal editing of the maize chloroplast ndhA transcript restores codons for conserved amino acids. Plant Cell 4:609–616

    PubMed  CAS  Google Scholar 

  90. Maier RM, Neckermann K, Hoch B, Akhmedov NB, Kossel H (1992b) Identification of editing positions in the ndhB transcript from maize chloroplasts reveals sequence similarities between editing sites of chloroplasts and plant mitochondria. Nucleic Acids Res 20:6189–6194

    Article  PubMed  CAS  Google Scholar 

  91. 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  PubMed  CAS  Google Scholar 

  92. Maier RM, Zeltz P, Kossel H, Bonnard G, Gualberto JM, Grienenberger JM (1996) RNA editing in plant mitochondria and chloroplasts. Plant Mol Biol 32:343–365

    Article  PubMed  CAS  Google Scholar 

  93. Maul JE, Lilly JW, Cui L, dePamphilis CW, Miller W, Harris EH, Stern DB (2002) The Chlamydomonas reinhardtii plastid chromosome: islands of genes in a sea of repeats. Plant Cell 14:2659–2679

    Article  PubMed  CAS  Google Scholar 

  94. McCullough AJ, Kangasjarvi J, Gengenback BG, Jones RJ (1992) Plastid DNA in developing maize endosperm. Plant Physiol 100:958–964

    Article  PubMed  CAS  Google Scholar 

  95. 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  PubMed  CAS  Google Scholar 

  96. 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  PubMed  CAS  Google Scholar 

  97. Michel F, Dujon B (1983) Conservation of RNA secondary structures in two intron families including mitochondrial-, chloroplast- and nuclear-encoded members. EMBO J 2:33–38

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  99. Michel F, Umesono K, Ozeki H (1989) Comparative and functional anatomy of group II catalytic introns–a review. Gene 82:5–30

    Article  PubMed  CAS  Google Scholar 

  100. Michel F, Westhof E (1990) Modelling of the three-dimensional architecture of group I catalytic introns based on comparative sequence analysis. J Mol Biol 216:585–610

    Article  PubMed  CAS  Google Scholar 

  101. 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

    Article  PubMed  CAS  Google Scholar 

  102. Miyamoto T, Obokata J, Sugiura M (2004) A site-specific factor interacts directly with its cognate RNA editing site in chloroplast transcripts. Proc Natl Acad Sci USA 101:48–52

    Article  PubMed  CAS  Google Scholar 

  103. Miyata Y, Sugita M (2004) Tissue- and stage-specific RNA editing of rps14 transcripts in moss (Physcomitrella patens) chloroplasts. J Plant Physiol 161:113–115

    Article  PubMed  CAS  Google Scholar 

  104. Miyata Y, Sugiura C, Kobayashi Y, Hagiwara M, Sugita M (2002) Chloroplast ribosomal S14 protein transcript is edited to create a translation initiation codon in the moss Physcomitrella patens. Biochim Biophys Acta 1576:346–349

    Article  PubMed  CAS  Google Scholar 

  105. Mohr G, Lambowitz AM (2003) Putative proteins related to group II intron reverse transcriptase/maturases are encoded by nuclear genes in higher plants. Nucleic Acids Res 31:647–652

    Article  PubMed  CAS  Google Scholar 

  106. Morton BR (2003) The role of context-dependent mutations in generating compositional and codon usage bias in grass chloroplast DNA. J Mol Evol 56:616–629

    Article  PubMed  CAS  Google Scholar 

  107. Morton BR, Oberholzer VM, Clegg MT (1997) The influence of specific neighboring bases on substitution bias in noncoding regions of the plant chloroplast genome. J Mol Evol 45:227–231

    Article  PubMed  CAS  Google Scholar 

  108. Nakajima Y, Mulligan RM (2001) Heat stress results in incomplete C-to-U editing of maize chloroplast mRNAs and correlates with changes in chloroplast transcription rate. Curr Genet 40:209–213

    Article  PubMed  CAS  Google Scholar 

  109. Nakajima Y, Mulligan RM (2005) Nucleotide specificity of the RNA editing reaction in pea chloroplasts. J Plant Physiol 162:1347–1354

    Article  PubMed  CAS  Google Scholar 

  110. Nakamura T, Meierhoff K, Westhoff P, Schuster G (2003) RNA-binding properties of HCF152, an Arabidopsis PPR protein involved in the processing of chloroplast RNA. Eur J Biochem 270:4070–4081

    Article  PubMed  CAS  Google Scholar 

  111. Navaratnam N, Morrison JR, Bhattacharya S, Patel D, Funahashi T, Giannoni F, Teng BB, Davidson NO, Scott J (1993) The p27 catalytic subunit of the apolipoprotein B mRNA editing enzyme is a cytidine deaminase. J Biol Chem 268:20709–20712

    PubMed  CAS  Google Scholar 

  112. Neuhaus H, Link G (1987) The chloroplast tRNA(Lys)(UUU) gene from mustard (Sinapis alba) contains a class II intron potentially encoding for a maturase-related polypeptide. Curr Genet 11:251–257

    Article  PubMed  CAS  Google Scholar 

  113. Odom OW, Holloway SP, Deshpande NN, Lee J, Herrin DL (2001) Mobile self-splicing group I introns from the psbA gene of Chlamydomonas reinhardtii: highly efficient homing of an exogenous intron containing its own promoter. Mol Cell Biol 21:3472–3481

    Article  PubMed  CAS  Google Scholar 

  114. .Odom OW, Shenkenberg DL, Garcia JA, Herrin DL (2004) A horizontally acquired group II intron in the chloroplast psbA gene of a psychrophilic Chlamydomonas: in vitro self-splicing and genetic evidence for maturase activity. RNA 10:1097–1107

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  116. 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  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  118. Ostheimer GJ, Hadjivasiliou H, Kloer DP, Barkan A, Matthews BW (2005) Structural analysis of the group II intron splicing factor CRS2 yields insights into its protein and RNA interaction surfaces. J Mol Biol 345:51–68

    Article  PubMed  CAS  Google Scholar 

  119. 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  PubMed  CAS  Google Scholar 

  120. 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  PubMed  CAS  Google Scholar 

  121. Palmer JD (1990) Contrasting modes and tempos of genome evolution in land plant organelles. Trends Genet 6:115–120

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  123. 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  PubMed  CAS  Google Scholar 

  124. Perron K, Goldschmidt-Clermont M, Rochaix JD (2004) A multiprotein complex involved in chloroplast group II intron splicing. RNA 10:704–711

    Article  PubMed  CAS  Google Scholar 

  125. Pyle A (2002) Metal ions in the structure and function of RNA. J Biol Inorg Chem 7:679–690

    Article  PubMed  CAS  Google Scholar 

  126. Qin PZ, Pyle AM (1998) The architectural organization and mechanistic function of group II intron structural elements. Curr Opin Struct Biol 8:301–308

    Article  PubMed  CAS  Google Scholar 

  127. Rajasekhar VK, Mulligan RM (1993) RNA editing in plant mitochondria: [alpha]-phosphate is retained during C-to-U conversion in mRNAs. Plant Cell 5:1843–1852

    PubMed  CAS  Google Scholar 

  128. Reed ML, Hanson MR (1997) A heterologous maize rpoB editing site is recognized by transgenic tobacco chloroplasts. Mol Cell Biol 17:6948–6952

    PubMed  CAS  Google Scholar 

  129. Reed ML, Lyi SM, Hanson MR (2001a) Edited transcripts compete with unedited mRNAs for trans-acting editing factors in higher plant chloroplasts. Gene 272:165–171

    Article  PubMed  CAS  Google Scholar 

  130. Reed ML, Peeters NM, Hanson MR (2001b) A single alteration 20 nt 5′ to an editing target inhibits chloroplast RNA editing in vivo. Nucleic Acids Res 29:1507–1513

    Article  PubMed  CAS  Google Scholar 

  131. 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  PubMed  CAS  Google Scholar 

  132. Roitgrund C, Mets JL (1990) Localization of two novel chloroplast genome functions: trans-splicing of RNA and protochlorophyllide reduction. Curr Genet 17:147–153

    Article  CAS  Google Scholar 

  133. Ruf S, Kössel H (1997) Tissue-specific and differential editing of the two ycf3 editing sites in maize plastids. Curr Genet 32:19–23

    Article  PubMed  CAS  Google Scholar 

  134. 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 USA 91:2295–2299

    Article  PubMed  CAS  Google Scholar 

  135. Sasaki T, Yukawa Y, Miyamoto T, Obokata J, Sugiura M (2003) Identification of RNA editing sites in chloroplast transcripts from the maternal and paternal progenitors of tobacco (Nicotiana tabacum): comparative analysis shows the involvement of distinct trans-factors for ndhB editing. Mol Biol Evol 20:1028–1035

    Article  PubMed  CAS  Google Scholar 

  136. Sasaki T, Yukawa Y, Wakasugi T, Yamada K, Sugiura M (2006) A simple in vitro RNA editing assay for chloroplast transcripts using fluorescent dideoxynucleotides: distinct types of sequence elements required for editing of ndh transcripts. Plant J 47:802–810

    Article  PubMed  CAS  Google Scholar 

  137. Sasaki Y, Kozaki A, Ohmori A, Iguchi H, Nagano Y (2001) Chloroplast RNA editing required for functional acetyl-CoA carboxylase in plants. J Biol Chem 276:3937–3940

    Article  PubMed  CAS  Google Scholar 

  138. Sashital DG, Cornilescu G, McManus CJ, Brow DA, Butcher SE (2004) U2-U6 RNA folding reveals a group II intron-like domain and a four-helix junction. Nat Struct Mol Biol 11:1237–1242

    Article  PubMed  CAS  Google Scholar 

  139. Schmitz-Linneweber C, Kushnir S, Babiychuk E, Poltnigg P, Herrmann RG, Maier RM (2005a) Pigment deficiency in nightshade/tobacco cybrids is caused by the failure to edit the plastid ATPase alpha-subunit mRNA. Plant Cell 17:1815–1828

    Article  PubMed  CAS  Google Scholar 

  140. Schmitz-Linneweber C, Regel R, Du TG, Hupfer H, Herrmann RG, Maier RM (2002) The plastid chromosome of Atropa belladonna and its comparison with that of Nicotiana tabacum: the role of RNA editing in generating divergence in the process of plant speciation. Mol Biol Evol 19:1602–1612

    Article  PubMed  CAS  Google Scholar 

  141. Schmitz-Linneweber C, Tillich M, Herrmann RG, Maier RM (2001) Heterologous, splicing-dependent RNA editing in chloroplasts: allotetraploidy provides trans-factors. EMBO J 20:4874–4883

    Article  PubMed  CAS  Google Scholar 

  142. Schmitz-Linneweber C, Williams-Carrier R, Barkan A (2005b) 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 17:2791–2804

    Article  PubMed  CAS  Google Scholar 

  143. Schmitz-Linneweber C, Williams-Carrier R, Williams P, Kroeger T, Vichas A, Barkan A (2006) A pentatricopeptide repeat protein binds to and facilitates the trans-splicing of the maize chloroplast rps12 pre-mRNA. Plant Cell 18:2650–2663

    Article  PubMed  CAS  Google Scholar 

  144. Sheveleva EV, Hallick RB (2004) Recent horizontal intron transfer to a chloroplast genome. Nucleic Acids Res 32:803–810

    Article  PubMed  CAS  Google Scholar 

  145. Shields DC, Wolfe KH (1997) Accelerated evolution of sites undergoing mRNA editing in plant mitochondria and chloroplasts. Mol Biol Evol 14:344–349

    Article  PubMed  CAS  Google Scholar 

  146. Shikanai T (2006) RNA editing in plant organelles: machinery, physiological function and evolution. Cell Mol Life Sci 63:698–708

    Article  PubMed  CAS  Google Scholar 

  147. Shukla G, Padgett R (2002) A catalytically active group II intron domain 5 can function in the U12-dependent spliceosome. Mol Cell 9:1145–1150

    Article  PubMed  CAS  Google Scholar 

  148. Simon D, Fewer D, Friedl T, Bhattacharya D (2003) Phylogeny and self-splicing ability of the plastid tRNA-Leu group I Intron. J Mol Evol 57:710–720

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  150. Smith H, Gott J, Hanson M (1997) A guide to RNA editing. RNA 3:1105–1123

    PubMed  CAS  Google Scholar 

  151. Sugita M, Miyata Y, Maruyama K, Sugiura C, Arikawa T, Higuchi M (2006) Extensive RNA editing in transcripts from the PsbB operon and RpoA gene of plastids from the enigmatic moss Takakia lepidozioides. Biosci Biotechnol Biochem 70:2268–2274

    Article  PubMed  CAS  Google Scholar 

  152. Sugiura C, Kobayashi Y, Aoki S, Sugita C, Sugita M (2003) Complete chloroplast DNA sequence of the moss Physcomitrella patens: evidence for the loss and relocation of rpoA from the chloroplast to the nucleus. Nucleic Acids Res 31:5324–5331

    Article  PubMed  CAS  Google Scholar 

  153. Swisher J, Su L, Brenowitz M, Anderson V, Pyle A (2002) Productive folding to the native state by a group II intron ribozyme. J Mol Biol 315:297–310

    Article  PubMed  CAS  Google Scholar 

  154. Thompson AJ, Herrin DL (1991) In vitro self-splicing reactions of the chloroplast group I intron Cr.LSU from Chlamydomonas reinhardtii and in vivo manipulation via gene-replacement. Nucleic Acids Res 19:6611–6618

    Article  PubMed  CAS  Google Scholar 

  155. 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  PubMed  CAS  Google Scholar 

  156. Tillich M, Funk HT, Schmitz-Linneweber C, Poltnigg P, Sabater B, Martin M, Maier RM (2005) Editing of plastid RNA in Arabidopsis thaliana ecotypes. Plant J 43:708–715

    Article  PubMed  CAS  Google Scholar 

  157. Tillich M, Lehwark P, Morton BR, Maier UG (2006a) The evolution of chloroplast RNA editing. Mol Biol Evol 23:1912–1921

    Article  PubMed  CAS  Google Scholar 

  158. Tillich M, Poltnigg P, Kushnir S, Schmitz-Linneweber C (2006b) Maintenance of plastid RNA editing activities independently of their target sites. EMBO Rep 7:308–313

    Article  PubMed  CAS  Google Scholar 

  159. Tsudzuki T, Wakasugi T, Sugiura M (2001) Comparative analysis of RNA editing sites in higher plant chloroplasts. J Mol Evol 53:327–332

    Article  PubMed  CAS  Google Scholar 

  160. Turmel M, Choquet Y, Goldschmidt-Clermont M, Rochaix JD, Otis C, Lemieux C (1995) The trans-spliced intron 1 in the psaA gene of the Chlamydomonas chloroplast: a comparative analysis. Curr Genet 27:270–279

    Article  PubMed  CAS  Google Scholar 

  161. Turmel M, Otis C, Lemieux C (2002) The chloroplast and mitochondrial genome sequences of the charophyte Chaetosphaeridium globosum: insights into the timing of the events that restructured organelle DNAs within the green algal lineage that led to land plants. Proc Natl Acad Sci USA 99:11275–11280

    Article  PubMed  CAS  Google Scholar 

  162. Turmel M, Otis C, Lemieux C (2006) The chloroplast genome sequence of Chara vulgaris sheds new light into the closest green algal relatives of land plants. Mol Biol Evol 23:1324–1338

    Article  PubMed  CAS  Google Scholar 

  163. Villa T, Pleiss J, Guthrie C (2002) Spliceosomal snRNAs: Mg2+- dependent chemistry at the catalytic core? Cell 109:149–152

    Article  PubMed  CAS  Google Scholar 

  164. Vogel J, Borner T (2002) Lariat formation and a hydrolytic pathway in plant chloroplast group II intron splicing. EMBO J 21:3794–3803

    Article  PubMed  CAS  Google Scholar 

  165. 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  PubMed  CAS  Google Scholar 

  166. Vogel J, Hubschmann T, Borner T, Hess WR (1997) Splicing and intron-internal RNA editing of trnK-matK transcripts in barley plastids: support for MatK as an essential splice factor. J Mol Biol 270:179–187

    Article  PubMed  CAS  Google Scholar 

  167. Wakasugi T, Tsudzuki J, Ito S, Nakashima K, Tsudzuki T, Sugiura M (1994) Loss of all ndh genes as determined by sequencing the entire chloroplast genome of the black pine Pinus thunbergii. Proc Natl Acad Sci USA 91:9794–9798

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  169. Weeks KM (1997) Protein-facilitated RNA folding. Curr Opin Struct Biol 7:336–342

    Article  PubMed  CAS  Google Scholar 

  170. Weihe A (2004) The transcription of plant organelle genomes. In: Daniell H, Chase C (eds) Molecular biology and biotechnology of plant Organelles. Chloroplasts and mitochondria. Springer, Dordrecht, pp 213–237

    Chapter  Google Scholar 

  171. Westhof E (2002) Group I introns and RNA folding. Biochem Soc Trans 30:1149–1152

    Article  PubMed  CAS  Google Scholar 

  172. Williams PM, Barkan A (2003) A chloroplast-localized PPR protein required for plastid ribosome accumulation. Plant J 36:675–686

    Article  PubMed  CAS  Google Scholar 

  173. Wolf PG, Rowe CA, Hasebe M (2004) High levels of RNA editing in a vascular plant chloroplast genome: analysis of transcripts from the fern Adiantum capillus-veneris. Gene 339:89–97

    Article  PubMed  CAS  Google Scholar 

  174. Wolfe KH, Morden CW, Palmer JD (1992) Function and evolution of a minimal plastid genome from a nonphotosynthetic parasitic plant. Proc Natl Acad Sci USA 89:10648–10652

    Article  PubMed  CAS  Google Scholar 

  175. Xu MQ, Kathe SD, Goodrich-Blair H, Nierzwicki-Bauer SA, Shub DA (1990) Bacterial origin of a chloroplast intron: conserved self-splicing group I introns in cyanobacteria. Science 250:1566–1570

    Article  PubMed  CAS  Google Scholar 

  176. Yoshinaga K, Iinuma H, Masuzawa T, Uedal K (1996) Extensive RNA editing of U to C in addition to C to U substitution in the rbcL transcripts of hornwort chloroplasts and the origin of RNA editing in green plants. Nucleic Acids Res 24:1008–1014

    Article  PubMed  CAS  Google Scholar 

  177. Yoshinaga K, Kakehi T, Shima Y, Iinuma H, Masuzawa T, Ueno M (1997) Extensive RNA editing and possible double-stranded structures determining editing sites in the atpB transcripts of hornwort chloroplasts. Nucleic Acids Res 25:4830–4834

    Article  PubMed  CAS  Google Scholar 

  178. Yu W, Schuster W (1995) Evidence for a site-specific cytidine deamination reaction involved in C to U RNA editing of plant mitochondria. J Biol Chem 270:18227–18233

    Article  PubMed  CAS  Google Scholar 

  179. Zaita N, Torazawa K, Shinozaki K, Sugiura M (1987) Trans-splicing in vivo: joining of transcripts from the "divided" gene for ribosomal protein S12 in the chloroplasts of tobacco. FEBS Lett 210:153–156

    Article  CAS  Google Scholar 

  180. Zeltz P, Hess WR, Neckermann K, Borner T, Kossel H (1993) Editing of the chloroplast rpoB transcript is independent of chloroplast translation and shows different patterns in barley and maize. EMBO J 12:4291–4296

    PubMed  CAS  Google Scholar 

  181. Zito F, Kuras R, Choquet Y, Kossel H, Wollman FA (1997) Mutations of cytochrome b6 in Chlamydomonas reinhardtii disclose the functional significance for a proline to leucine conversion by petB editing in maize and tobacco. Plant Mol Biol 33:79–86

    Article  PubMed  CAS  Google Scholar 

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Schmitz-Linneweber, C., Barkan, A. (2007). RNA splicing and RNA editing in chloroplasts. In: Bock, R. (eds) Cell and Molecular Biology of Plastids. Topics in Current Genetics, vol 19. Springer, Berlin, Heidelberg. https://doi.org/10.1007/4735_2007_0233

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