Skip to main content

Translation and translational regulation in chloroplasts

  • Chapter
  • First Online:
Cell and Molecular Biology of Plastids

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

Abstract

The translation mechanism of chloroplast mRNAs originated as prokaryotic-type, but has sinceevolved considerably. Chloroplast translation became, in large part, uncoupled from transcription,and turned into a highly regulated process. Concomitantly, chloroplast ribosomes, general translationfactors, and transcripts changed substantially from their prokaryotic counterparts. A multitudeof nucleus encoded regulatory proteins evolved that interact in a specific manner with elementsin mRNAs to allow translation regulation in response to environmental and developmental cues. Inthis chapter, we sum up the current knowledge regarding the translation machinery in the chloroplastusing examples of mechanisms utilized for chloroplast translation regulation.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Akkaya MS, Breitenberger CA (1992) Light regulation of protein synthesis factor EF-G in pea chloroplasts. Plant Mol Biol 20:791–800

    Article  PubMed  CAS  Google Scholar 

  2. Alergand T, Peled-Zehavi H, Katz Y, Danon A (2006) The chloroplast protein disulfide isomerase RB60 reacts with a regulatory disulfide of the RNA-binding protein RB47. Plant Cell Physiol 47:540–548

    Article  PubMed  CAS  Google Scholar 

  3. Alexander C, Faber N, Klaff P (1998) Characterization of protein-binding to the spinach chloroplast psbA mRNA 5' untranslated region. Nucleic Acids Res 26:2265–2272

    Article  PubMed  CAS  Google Scholar 

  4. Barkan A, Goldschmidt-Clermont M (2000) Participation of nuclear genes in chloroplast gene expression. Biochimie 82:559–572

    Article  PubMed  CAS  Google Scholar 

  5. Barkan A, Walker M, Nolasco M, Johnson D (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 13:3170–3181

    PubMed  CAS  Google Scholar 

  6. Barneche F, Winter V, Crevecoeur M, Rochaix JD (2006) ATAB2 is a novel factor in the signalling pathway of light-controlled synthesis of photosystem proteins. EMBO J 25:5907–5918

    Article  PubMed  CAS  Google Scholar 

  7. Beligni MV, Yamaguchi K, Mayfield SP (2004) Chloroplast elongation factor ts pro-protein is an evolutionarily conserved fusion with the s1 domain-containing plastid-specific ribosomal protein-7. Plant Cell 16:3357–3369

    Article  PubMed  CAS  Google Scholar 

  8. Betts L, Spremulli LL (1994) Analysis of the role of the Shine-Dalgarno sequence and mRNA secondary structure on the efficiency of translational initiation in the Euglena gracilis chloroplast atpH mRNA. J Biol Chem 269:26456–26463

    PubMed  CAS  Google Scholar 

  9. Bhaya D, Jagendorf AT (1985) Synthesis of the alpha and beta subunits of coupling factor 1 by polysomes from pea chloroplasts. Arch Biochem Biophys 237:217–223

    Article  PubMed  CAS  Google Scholar 

  10. Bolli R, Mendiola-Morgenthaler L, Boschetti A (1981) Isolation and characterization of polysomes from thylakoid membranes of Chlamydomonas reinhardii. Biochim Biophys Acta 653:276–287

    Article  PubMed  CAS  Google Scholar 

  11. Boni IV, Isaeva DM, Musychenko ML, Tzareva NV (1991) Ribosome-messenger recognition: mRNA target sites for ribosomal protein S1. Nucleic Acids Res 19:155–162

    Article  PubMed  CAS  Google Scholar 

  12. Boudreau E, Nickelsen J, Lemaire SD, Ossenbuhl 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  PubMed  CAS  Google Scholar 

  13. Breidenbach E, Jenni E, Boschetti A (1988) Synthesis of two proteins in chloroplasts and mRNA distribution between thylakoids and stroma during the cell cycle of Chlamydomonas reinhardii. Eur J Biochem 177:225–232

    Article  PubMed  CAS  Google Scholar 

  14. Breitenberger CA, Graves MC, Spremulli LL (1979) Evidence for the nuclear location of the gene for chloroplast elongation factor G. Arch Biochem Biophys 194:265–270

    Article  PubMed  CAS  Google Scholar 

  15. Bruick RK, Mayfield SP (1998) Processing of the psbA 5' untranslated region in Chlamydomonas reinhardtii depends upon factors mediating ribosome association. J Cell Biol 143:1145–1153

    Article  PubMed  CAS  Google Scholar 

  16. Cahoon AB, Timko MP (2000) yellow-in-the-dark mutants of chlamydomonas lack the CHLL subunit of light-independent protochlorophyllide reductase. Plant Cell 12:559–568

    PubMed  CAS  Google Scholar 

  17. Campos F, Garcia-Gomez BI, Solorzano RM, Salazar E, Estevez J, Leon P, Alvarez-Buylla ER, Covarrubias AA (2001) A cDNA for nuclear-encoded chloroplast translational initiation factor 2 from a higher plant is able to complement an infB Escherichia coli null mutant. J Biol Chem 276:28388–28394

    Article  PubMed  CAS  Google Scholar 

  18. Choquet Y, Stern DB, Wostrikoff K, Kuras R, Girard-Bascou J, Wollman FA (1998) Translation of cytochrome f is autoregulated through the 5' untranslated region of petA mRNA in Chlamydomonas chloroplasts. Proc Natl Acad Sci USA 95:4380–4385

    Article  PubMed  CAS  Google Scholar 

  19. Choquet Y, Vallon O (2000) Synthesis, assembly and degradation of thylakoid membrane proteins. Biochimie 82:615–634

    Article  PubMed  CAS  Google Scholar 

  20. Choquet Y, Wollman FA (2002) Translational regulations as specific traits of chloroplast gene expression. FEBS Lett 529:39–42

    Article  PubMed  CAS  Google Scholar 

  21. Choquet Y, Wostrikoff K, Rimbault B, Zito F, Girard-Bascou J, Drapier D, Wollman FA (2001) Assembly-controlled regulation of chloroplast gene translation. Biochem Soc Trans 29:421–426

    Article  PubMed  CAS  Google Scholar 

  22. Choquet Y, Zito F, Wostrikoff K, Wollman FA (2003) Cytochrome f translation in Chlamydomonas chloroplast is autoregulated by its carboxyl-terminal domain. Plant Cell 15:1443–1454

    Article  PubMed  CAS  Google Scholar 

  23. Chua NH, Blobel G, Siekevitz P, Palade GE (1973) Attachment of chloroplast polysomes to thylakoid membranes in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 70:1554–1558

    Article  PubMed  CAS  Google Scholar 

  24. Chua NH, Blobel G, Siekevitz P, Palade GE (1976) Periodic variations in the ratio of free to thylakoid-bound chloroplast ribosomes during the cell cycle of Chlamydomonas reinhardtii. J Cell Biol 71:497–514

    Article  PubMed  CAS  Google Scholar 

  25. Cohen I, Knopf JA, Irihimovitch V, Shapira M (2005) A proposed mechanism for the inhibitory effects of oxidative stress on Rubisco assembly and its subunit expression. Plant Physiol 137:738–746

    Article  PubMed  CAS  Google Scholar 

  26. Danon A (1997) Translational regulation in the chloroplast. Plant Physiol 115:1293–1298

    Article  PubMed  CAS  Google Scholar 

  27. Danon A, Mayfield SP (1991) Light regulated translational activators: identification of chloroplast gene specific mRNA binding proteins. EMBO J 10:3993–4001

    PubMed  CAS  Google Scholar 

  28. Danon A, Mayfield SP (1994a) ADP-dependent phosphorylation regulates RNA-binding in vitro: implications in light-modulated translation. EMBO J 13:2227–2235

    PubMed  CAS  Google Scholar 

  29. Danon A, Mayfield SP (1994b) Light-regulated translation of chloroplast messenger RNAs through redox potential. Science 266:1717–1719

    Article  PubMed  CAS  Google Scholar 

  30. Dauvillee D, Stampacchia O, Girard-Bascou J, Rochaix JD (2003) Tab2 is a novel conserved RNA binding protein required for translation of the chloroplast psaB mRNA. EMBO J 22:6378–6388

    Article  PubMed  CAS  Google Scholar 

  31. Drapier D, Girard-Bascou J, Wollman FA (1992) Evidence for nuclear control of the expression of the atpA and atpB chloroplast genes in Chlamydomonas. Plant Cell 4:283–295

    PubMed  CAS  Google Scholar 

  32. Dron M, Rahire M, Rochaix JD (1982) Sequence of the chloroplast 16S rRNA gene and its surrounding regions of Chlamydomonas reinhardii. Nucleic Acids Res 10:7609–7620

    Article  PubMed  CAS  Google Scholar 

  33. 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  PubMed  CAS  Google Scholar 

  34. Edhofer I, Muhlbauer SK, Eichacker LA (1998) Light regulates the rate of translation elongation of chloroplast reaction center protein D1. Eur J Biochem 257:78–84

    Article  PubMed  CAS  Google Scholar 

  35. Eibl C, Zou Z, Beck A, Kim M, Mullet J, Koop HU (1999) In vivo analysis of plastid psbA, rbcL and rpl32 UTR elements by chloroplast transformation: tobacco plastid gene expression is controlled by modulation of transcript levels and translation efficiency. Plant J 19:333–345

    Article  PubMed  CAS  Google Scholar 

  36. Esposito D, Fey JP, Eberhard S, Hicks AJ, Stern DB (2003) In vivo evidence for the prokaryotic model of extended codon-anticodon interaction in translation initiation. EMBO J 22:651–656

    Article  PubMed  CAS  Google Scholar 

  37. Esposito D, Hicks AJ, Stern DB (2001) A role for initiation codon context in chloroplast translation. Plant Cell 13:2373–2384

    PubMed  CAS  Google Scholar 

  38. Fargo DC, Boynton JE, Gillham NW (1999) Mutations altering the predicted secondary structure of a chloroplast 5' untranslated region affect its physical and biochemical properties as well as its ability to promote translation of reporter mRNAs both in the Chlamydomonas reinhardtii chloroplast and in Escherichia coli. Mol Cell Biol 19:6980–6990

    PubMed  CAS  Google Scholar 

  39. Fargo DC, Boynton JE, Gillham NW (2001) Chloroplast ribosomal protein S7 of Chlamydomonas binds to chloroplast mRNA leader sequences and may be involved in translation initiation. Plant Cell 13:207–218

    PubMed  CAS  Google Scholar 

  40. Fargo DC, Zhang M, Gillham NW, Boynton JE (1998) Shine-Dalgarno-like sequences are not required for translation of chloroplast mRNAs in Chlamydomonas reinhardtii chloroplasts or in Escherichia coli. Mol Gen Genet 257:271–282

    Article  PubMed  CAS  Google Scholar 

  41. 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

    PubMed  CAS  Google Scholar 

  42. Fong CL, Lentz A, Mayfield SP (2000) Disulfide bond formation between RNA binding domains is used to regulate mRNA binding activity of the chloroplast poly(A)-binding protein. J Biol Chem 275:8275–8278

    Article  PubMed  CAS  Google Scholar 

  43. Fox L, Erion J, Tarnowski J, Spremulli L, Brot N, Weissbach H (1980) Euglena gracilis chloroplast EF-Ts. Evidence that it is a nuclear-coded gene product. J Biol Chem 255:6018–6019

    PubMed  CAS  Google Scholar 

  44. Fox T (1996) Translational control of endogenous and recoded nuclear genes in yeast mitochondria: regulation and membrane targeting. Experientia 52:1130–1135

    Article  PubMed  CAS  Google Scholar 

  45. Franch T, Gerdes K (1996) Programmed cell death in bacteria: translational repression by mRNA end-pairing. Mol Microbiol 21:1049–1060

    Article  PubMed  CAS  Google Scholar 

  46. Franzetti B, Carol P, Mache R (1992) Characterization and RNA-binding properties of a chloroplast S1-like ribosomal protein. J Biol Chem 267:19075–19081

    PubMed  CAS  Google Scholar 

  47. Friso G, Giacomelli L, Ytterberg AJ, Peltier JB, Rudella A, Sun Q, Wijk KJ (2004) In-depth analysis of the thylakoid membrane proteome of Arabidopsis thaliana chloroplasts: new proteins, new functions, and a plastid proteome database. Plant Cell 16:478–499

    Article  PubMed  CAS  Google Scholar 

  48. Fromm H, Devic M, Fluhr R, Edelman M (1985) Control of psbA gene expression: in mature Spirodela chloroplasts light regulation of 32-kd protein synthesis is independent of transcript level. EMBO J 4:291–295

    PubMed  CAS  Google Scholar 

  49. Gallie DR (1998) A tale of two termini: a functional interaction between the termini of an mRNA is a prerequisite for efficient translation initiation. Gene 216:1–11

    Article  PubMed  CAS  Google Scholar 

  50. Gamble PE, Mullet JE (1989) Translation and stability of proteins encoded by the plastid psbA and psbB genes are regulated by a nuclear gene during light-induced chloroplast development in barley. J Biol Chem 264:7236–7243

    PubMed  CAS  Google Scholar 

  51. Gillham NW, Boynton JE, Hauser CR (1994) Translational regulation of gene expression in chloroplasts and mitochondria. Annu Rev Genet 28:71–93

    Article  PubMed  CAS  Google Scholar 

  52. Girard-Bascou J, Pierre Y, Drapier D (1992) A nuclear mutation affects the synthesis of the chloroplast psbA gene production Chlamydomonas reinhardtii. Curr Genet 22:47–52

    Article  PubMed  CAS  Google Scholar 

  53. Gold L (1988) Posttranscriptional regulatory mechanisms in Escherichia coli. Annu Rev Biochem 57:199–233

    Article  PubMed  CAS  Google Scholar 

  54. Gray MW (1993) Origin and evolution of organelle genomes. Curr Opin Genet Dev 3:884–890

    Article  PubMed  CAS  Google Scholar 

  55. Gruissem W, Tonkyn JC (1993) Control mechanisms of plastid gene-expression. Crit Rev Plant Sci 12:19–55

    CAS  Google Scholar 

  56. Hattori T, Margulies MM (1986) Synthesis of large subunit of ribulosebisphosphate carboxylase by thylakoid-bound polyribosomes from spinach chloroplasts. Arch Biochem Biophys 244:630–640

    Article  PubMed  CAS  Google Scholar 

  57. Hauser CR, Gillham NW, Boynton JE (1996) Translational regulation of chloroplast genes. Proteins binding to the 5'-untranslated regions of chloroplast mRNAs in Chlamydomonas reinhardtii. J Biol Chem 271:1486–1497

    Article  PubMed  CAS  Google Scholar 

  58. Hieronymus H, Silver PA (2004) A systems view of mRNP biology. Genes Dev 18:2845–2860

    Article  PubMed  CAS  Google Scholar 

  59. Higgs DC, Shapiro RS, Kindle KL, Stern DB (1999) Small cis-acting sequences that specify secondary structures in a chloroplast mRNA are essential for RNA stability and translation. Mol Cell Biol 19:8479–8491

    PubMed  CAS  Google Scholar 

  60. Hirose T, Kusumegi T, Sugiura M (1998) Translation of tobacco chloroplast rps14 mRNA depends on a Shine-Dalgarno-like sequence in the 5'-untranslated region but not on internal RNA editing in the coding region. FEBS Lett 430:257–260

    Article  PubMed  CAS  Google Scholar 

  61. Hirose T, Sugiura M (1996) Cis-acting elements and trans-acting factors for accurate translation of chloroplast psbA mRNAs: development of an in vitro translation system from tobacco chloroplasts. EMBO J 15:1687–1695

    PubMed  CAS  Google Scholar 

  62. Hirose T, Sugiura M (2004a) Functional Shine-Dalgarno-like sequences for translational initiation of chloroplast mRNAs. Plant Cell Physiol 45:114–117

    Article  PubMed  CAS  Google Scholar 

  63. Hirose T, Sugiura M (2004b) Multiple elements required for translation of plastid atpB mRNA lacking the Shine-Dalgarno sequence. Nucleic Acids Res 32:3503–3510

    Article  PubMed  CAS  Google Scholar 

  64. Hotchkiss TL, Hollingsworth MJ (1999) ATP synthase 5' untranslated regions are specifically bound by chloroplast polypeptides. Curr Genet 35:512–520

    Article  PubMed  CAS  Google Scholar 

  65. Jackson RJ (2005) Alternative mechanisms of initiating translation of mammalian mRNAs. Biochem Soc Trans 33:1231–1241

    Article  PubMed  CAS  Google Scholar 

  66. Katz YS, Danon A (2002) The 3'-untranslated region of chloroplast psbA mRNA stabilizes binding of regulatory proteins to the leader of the message. J Biol Chem 277:18665–18669

    Article  PubMed  CAS  Google Scholar 

  67. Keene JD, Lager PJ (2005) Post-transcriptional operons and regulons co-ordinating gene expression. Chromosome Res 13:327–337

    Article  PubMed  CAS  Google Scholar 

  68. Khrebtukova I, Spreitzer RJ (1996) Elimination of the Chlamydomonas gene family that encodes the small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase. Proc Natl Acad Sci USA 93:13689–13693

    Article  PubMed  CAS  Google Scholar 

  69. Kim J, Klein PG, Mullet JE (1991) Ribosomes pause at specific sites during synthesis of membrane-bound chloroplast reaction center protein D1. J Biol Chem 266:14931–14938

    PubMed  CAS  Google Scholar 

  70. Kim J, Klein PG, Mullet JE (1994a) Synthesis and turnover of photosystem II reaction center protein D1. Ribosome pausing increases during chloroplast development. J Biol Chem 269:17918–17923

    PubMed  CAS  Google Scholar 

  71. Kim J, Klein PG, Mullet JE (1994b) Vir-115 gene product is required to stabilize D1 translation intermediates in chloroplasts. Plant Mol Biol 25:459–467

    Article  PubMed  CAS  Google Scholar 

  72. Kim J, Mayfield SP (1997) Protein disulfide isomerase as a regulator of chloroplast translational activation. Science 278:1954–1957

    Article  PubMed  CAS  Google Scholar 

  73. Kim J, Mullet JE (1994) Ribosome-binding sites on chloroplast rbcL and psbA mRNAs and light-induced initiation of D1 translation. Plant Mol Biol 25:437–448

    Article  PubMed  CAS  Google Scholar 

  74. Kim J, Mullet JE (2003) A mechanism for light-induced translation of the rbcL mRNA encoding the large subunit of ribulose-1,5-bisphosphate carboxylase in barley chloroplasts. Plant Cell Physiol 44:491–499

    Article  PubMed  CAS  Google Scholar 

  75. Klein RR, Mason HS, Mullet JE (1988) Light-regulated translation of chloroplast proteins. I. Transcripts of psaA-psaB, psbA, and rbcL are associated with polysomes in dark-grown and illuminated barley seedlings. J Cell Biol 106:289–301

    Article  PubMed  CAS  Google Scholar 

  76. Klinkert B, Elles I, Nickelsen J (2006) Translation of chloroplast psbD mRNA in Chlamydomonas is controlled by a secondary RNA structure blocking the AUG start codon. Nucleic Acids Res 34:386–394

    Article  PubMed  CAS  Google Scholar 

  77. Koo JS, Spremulli LL (1994) Analysis of the translational initiation region on the Euglena gracilis chloroplast ribulose-bisphosphate carboxylase/oxygenase (rbcL) messenger RNA. J Biol Chem 269:7494–7500

    PubMed  CAS  Google Scholar 

  78. Kozak M (2005) Regulation of translation via mRNA structure in prokaryotes and eukaryotes. Gene 361:13–37

    Article  PubMed  CAS  Google Scholar 

  79. Kramzar LM, Mueller T, Erickson B, Higgs DC (2006) Regulatory sequences of orthologous petD chloroplast mRNAs are highly specific among Chlamydomonas species. Plant Mol Biol 60:405–422

    Article  PubMed  CAS  Google Scholar 

  80. Krupinska K, Apel K (1989) Light-induced transformation of etioplasts to chloroplasts of barley without transcriptional control of plastid gene expression. Mol Gen Genet 219:467–473

    Article  CAS  Google Scholar 

  81. 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  PubMed  CAS  Google Scholar 

  82. Kuchka MR, Mayfield SP, Rochaix JD (1988) Nuclear mutations specifically affect the synthesis and/or degradation of the chloroplast-encoded D2 polypeptide of photosystem II in Chlamydomonas reinhardtii. EMBO J 7:319–324

    PubMed  CAS  Google Scholar 

  83. Kuras R, Wollman FA (1994) The assembly of cytochrome b6/f complexes: an approach using genetic transformation of the green alga Chlamydomonas reinhardtii. EMBO J 13:1019–1027

    PubMed  CAS  Google Scholar 

  84. Laursen BS, Sorensen HP, Mortensen KK, Sperling-Petersen HU (2005) Initiation of protein synthesis in bacteria. Microbiol Mol Biol Rev 69:101–123

    Article  PubMed  CAS  Google Scholar 

  85. Lennartz K, Bossmann S, Westhoff P, Bechtold N, Meierhoff K (2006) HCF153, a novel nuclear-encoded factor necessary during a post-translational step in biogenesis of the cytochrome bf complex. Plant J 45:101–112

    Article  PubMed  CAS  Google Scholar 

  86. Lennartz K, Plucken H, Seidler A, Westhoff P, Bechtold N, Meierhoff K (2001) HCF164 encodes a thioredoxin-like protein involved in the biogenesis of the cytochrome b(6)f complex in Arabidopsis. Plant Cell 13:2539–2551

    PubMed  CAS  Google Scholar 

  87. Lin Q, Yu NJ, Spremulli LL (1996) Expression and functional analysis of Euglena Gracilis chloroplast initiation factor 3. Plant Mol Biol 32:937–945

    Article  PubMed  CAS  Google Scholar 

  88. Lindahl L, Hinnebusch A (1992) Diversity of mechanisms in the regulation of translation in prokaryotes and lower eukaryotes. Curr Opin Genet Dev 2:720–726

    Article  PubMed  CAS  Google Scholar 

  89. Lorkovic ZJ, Barta A (2002) Genome analysis: RNA recognition motif (RRM) and K homology (KH) domain RNA-binding proteins from the flowering plant Arabidopsis thaliana. Nucleic Acids Res 30:623–635

    Article  PubMed  CAS  Google Scholar 

  90. 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 

  91. Ma L, Spremulli LL (1990) Identification and characterization of large, complex forms of chloroplast translational initiation factor 2 from Euglena gracilis. J Biol Chem 265:13560–13565

    PubMed  CAS  Google Scholar 

  92. Maidak BL, Olsen GJ, Larsen N, Overbeek R, McCaughey MJ, Woese CR (1996) The Ribosomal Database Project (RDP). Nucleic Acids Res 24:82–85

    Article  PubMed  CAS  Google Scholar 

  93. Malnoe P, Mayfield SP, Rochaix JD (1988) Comparative analysis of the biogenesis of photosystem II in the wild-type and Y-1 mutant of Chlamydomonas reinhardtii. J Cell Biol 106:609–616

    Article  PubMed  CAS  Google Scholar 

  94. Mangus DA, Evans MC, Jacobson A (2003) Poly(A)-binding proteins: multifunctional scaffolds for the post-transcriptional control of gene expression. Genome Biol 4:223

    Article  PubMed  Google Scholar 

  95. Manuell A, Beligni MV, Yamaguchi K, Mayfield SP (2004) Regulation of chloroplast translation: interactions of RNA elements, RNA-binding proteins and the plastid ribosome. Biochem Soc Trans 32:601–605

    Article  PubMed  CAS  Google Scholar 

  96. Margulies MM (1983) Synthesis of photosynthetic membrane proteins directed by RNA from rough thylakoids of Chlamydomonas reinhardtii. Eur J Biochem 137:241–248

    Article  PubMed  CAS  Google Scholar 

  97. Margulies MM, Michaels A (1974) Ribosomes bound to chloroplast membranes in Chlamydomonas reinhardtii. J Cell Biol 60:65–77

    Article  PubMed  CAS  Google Scholar 

  98. Margulies MM, Michaels A (1975) Free and membrane-bound chloroplast polyribosomes Chlamydomonas reinhardtii. Biochim Biophys Acta 402:297–308

    Article  PubMed  CAS  Google Scholar 

  99. Margulies MM, Tiffany HL, Hattori T (1987) Photosystem I reaction center polypeptides of spinach are synthesized on thylakoid-bound ribosomes. Arch Biochem Biophys 254:454–461

    Article  PubMed  CAS  Google Scholar 

  100. Margulies MM, Weistrop JS (1980) Sub-thylakoid fractions containing ribosomes. Biochim Biophys Acta 606:20–33

    Article  PubMed  CAS  Google Scholar 

  101. Martin W, Herrmann RG (1998) Gene transfer from organelles to the nucleus: how much, what happens, and Why? Plant Physiol 118:9–17

    Article  PubMed  CAS  Google Scholar 

  102. Mayfield SP, Cohen A, Danon A, Yohn CB (1994) Translation of the psbA mRNA of Chlamydomonas reinhardtii requires a structured RNA element contained within the 5' untranslated region. J Cell Biol 127:1537–1545

    Article  PubMed  CAS  Google Scholar 

  103. Mayfield SP, Yohn CB, Cohen A, Danon A (1995) Regulation of chloroplast gene expression. Annu Rev Plant Physiol Plant Mol Biol 46:147–166

    Article  CAS  Google Scholar 

  104. McCormac DJ, Barkan A (1999) A nuclear gene in maize required for the translation of the chloroplast atpB/E mRNA. Plant Cell 11:1709–1716

    PubMed  CAS  Google Scholar 

  105. Merendino L, Falciatore A, Rochaix JD (2003) Expression and RNA binding properties of the chloroplast ribosomal protein S1 from Chlamydomonas reinhardtii. Plant Mol Biol 53:371–382

    Article  PubMed  CAS  Google Scholar 

  106. Merhige PM, Both-Kim D, Robida MD, Hollingsworth MJ (2005) RNA-protein complexes that form in the spinach chloroplast atpI 5' untranslated region can be divided into two subcomplexes, each comprised of unique cis-elements and trans-factors. Curr Genet 48:256–264

    Article  PubMed  CAS  Google Scholar 

  107. Meurer J, Grevelding C, Westhoff P, Reiss B (1998) The PAC protein affects the maturation of specific chloroplast mRNAs in Arabidopsis thaliana. Mol Gen Genet 258:342–351

    Article  PubMed  CAS  Google Scholar 

  108. Meurer J, Meierhoff K, Westhoff P (1996) Isolation of high-chlorophyll-fluorescence mutants of Arabidopsis thaliana and their characterisation by spectroscopy, immunoblotting and northern hybridisation. Planta 198:385–396

    Article  PubMed  CAS  Google Scholar 

  109. Minai L, Wostrikoff K, Wollman FA, Choquet Y (2006) Chloroplast biogenesis of photosystem II cores involves a series of assembly-controlled steps that regulate translation. Plant Cell 18:159–175

    Article  PubMed  CAS  Google Scholar 

  110. Minami E, Watanabe A (1984) Thylakoid membranes: the translational site of chloroplast DNA-regulated thylakoid polypeptides. Arch Biochem Biophys 235:562–570

    Article  PubMed  CAS  Google Scholar 

  111. Moll I, Grill S, Gualerzi CO, Blasi U (2002) Leaderless mRNAs in bacteria: surprises in ribosomal recruitment and translational control. Mol Microbiol 43:239–246

    Article  PubMed  CAS  Google Scholar 

  112. Monde RA, Greene JC, Stern DB (2000a) The sequence and secondary structure of the 3'-UTR affect 3'-end maturation, RNA accumulation, and translation in tobacco chloroplasts. Plant Mol Biol 44:529–542

    Article  PubMed  CAS  Google Scholar 

  113. Monde RA, Zito F, Olive J, Wollman FA, Stern DB (2000b) Post-transcriptional defects in tobacco chloroplast mutants lacking the cytochrome b6/f complex. Plant J 21:61–72

    Article  PubMed  CAS  Google Scholar 

  114. Muhlbauer SK, Eichacker LA (1998) Light-dependent formation of the photosynthetic proton gradient regulates translation elongation in chloroplasts. J Biol Chem 273:20935–20940

    Article  PubMed  CAS  Google Scholar 

  115. Muhlbauer SK, Eichacker LA (1999) The stromal protein large subunit of ribulose-1,5-bisphosphate carboxylase is translated by membrane-bound ribosomes. Eur J Biochem 261:784–788

    Article  PubMed  CAS  Google Scholar 

  116. Mullet JE (1988) Chloroplast development and gene-expression. Annu Rev Plant Physiol Plant Mol Biol 39:475–502

    Article  CAS  Google Scholar 

  117. Mullet JE, Klein PG, Klein RR (1990) Chlorophyll regulates accumulation of the plastid-encoded chlorophyll apoproteins CP43 and D1 by increasing apoprotein stability. Proc Natl Acad Sci USA 87:4038–4042

    Article  PubMed  CAS  Google Scholar 

  118. 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 

  119. Nickelsen J (1999) Transcripts containing the 5' untranslated regions of the plastid genes psbA and psbB from higher plants are unstable in Chlamydomonas reinhardtii chloroplasts. Mol Gen Genet 262:768–771

    Article  PubMed  CAS  Google Scholar 

  120. Nickelsen J (2003) Chloroplast RNA-binding proteins. Curr Genet 43:392–399

    Article  PubMed  CAS  Google Scholar 

  121. 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

    PubMed  CAS  Google Scholar 

  122. Nickelsen J, van Dillewijn J, Rahire M, Rochaix JD (1994) Determinants for stability of the chloroplast psbD RNA are located within its short leader region in Chlamydomonas reinhardtii. EMBO J 13:3182–3191

    PubMed  CAS  Google Scholar 

  123. Ossenbuhl 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  CAS  Google Scholar 

  124. Plader W, Sugiura M (2003) The Shine-Dalgarno-like sequence is a negative regulatory element for translation of tobacco chloroplast rps2 mRNA: an additional mechanism for translational control in chloroplasts. Plant J 34:377–382

    Article  PubMed  CAS  Google Scholar 

  125. Plucken H, Muller B, Grohmann D, Westhoff P, Eichacker LA (2002) The HCF136 protein is essential for assembly of the photosystem II reaction center in Arabidopsis thaliana. FEBS Lett 532:85–90

    Article  PubMed  CAS  Google Scholar 

  126. Race HL, Herrmann RG, Martin W (1999) Why have organelles retained genomes? Trends Genet 15:364–370

    Article  PubMed  CAS  Google Scholar 

  127. Robida MD, Merhige PM, Hollingsworth MJ (2002) Proteins are shared among RNA-protein complexes that form in the 5' untranslated regions of spinach chloroplast mRNAs. Curr Genet 41:53–62

    Article  PubMed  CAS  Google Scholar 

  128. Rochaix JD (2001) Posttranscriptional control of chloroplast gene expression. From RNA to photosynthetic complex. Plant Physiol 125:142–144

    Article  PubMed  CAS  Google Scholar 

  129. Rochaix JD, Kuchka M, Mayfield S, Schirmer-Rahire M, Girard-Bascou J, Bennoun P (1989) Nuclear and chloroplast mutations affect the synthesis or stability of the chloroplast psbC gene product in Chlamydomonas reinhardtii. EMBO J 8:1013–1021

    PubMed  CAS  Google Scholar 

  130. Rodermel S (1999) Subunit control of Rubisco biosynthesis – a relic of an endosymbiotic past? Photosynthesis Res 59:105–123

    Article  CAS  Google Scholar 

  131. Rodermel S, Haley J, Jiang CZ, Tsai CH, Bogorad L (1996) A mechanism for intergenomic integration: abundance of ribulose bisphosphate carboxylase small-subunit protein influences the translation of the large-subunit mRNA. Proc Natl Acad Sci USA 93:3881–3885

    Article  PubMed  CAS  Google Scholar 

  132. Rodermel SR, Abbott MS, Bogorad L (1988) Nuclear-organelle interactions: nuclear antisense gene inhibits ribulose bisphosphate carboxylase enzyme levels in transformed tobacco plants. Cell 55:673–681

    Article  PubMed  CAS  Google Scholar 

  133. Rott R, Levy H, Drager RG, Stern DB, Schuster G (1998) 3'-Processed mRNA is preferentially translated in Chlamydomonas reinhardtii chloroplasts. Mol Cell Biol 18:4605–4611

    PubMed  CAS  Google Scholar 

  134. Sakamoto W, Chen X, Kindle KL, Stern DB (1994) Function of the Chlamydomonas reinhardtii petd 5' untranslated region in regulating the accumulation of subunit IV of the cytochrome b6/f complex. Plant J 6:503–512

    Article  PubMed  CAS  Google Scholar 

  135. Sane AP, Stein B, Westhoff P (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 42:720–730

    Article  PubMed  CAS  Google Scholar 

  136. Sato N, Rolland N, Block MA, Joyard J (1999) Do plastid envelope membranes play a role in the expression of the plastid genome? Biochimie 81:619–629

    Article  PubMed  CAS  Google Scholar 

  137. Schmitz-Linneweber C, Williams-Carrier R, Barkan A (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 17:2791–2804

    Article  PubMed  CAS  Google Scholar 

  138. Sengupta J, Agrawal RK, Frank J (2001) Visualization of protein S1 within the 30S ribosomal subunit and its interaction with messenger RNA. Proc Natl Acad Sci USA 98:11991–11996

    Article  PubMed  CAS  Google Scholar 

  139. Shen Y, Danon A, Christopher DA (2001) RNA binding-proteins interact specifically with the Arabidopsis chloroplast psbA mRNA 5' untranslated region in a redox-dependent manner. Plant Cell Physiol 42:1071–1078

    Article  PubMed  CAS  Google Scholar 

  140. Shinohara K, Minami E, Watanabe A (1988) Synthesis and assembly of H+-ATPase complex by isolated "rough" thylakoids. Arch Biochem Biophys 260:452–460

    Article  PubMed  CAS  Google Scholar 

  141. Shteiman-Kotler A, Schuster G (2000) RNA-binding characteristics of the chloroplast S1-like ribosomal protein CS1. Nucleic Acids Res 28:3310–3315

    Article  PubMed  CAS  Google Scholar 

  142. Singh BN, Mishra RN, Agarwal PK, Goswami M, Nair S, Sopory SK, Reddy MK (2004) A pea chloroplast translation elongation factor that is regulated by abiotic factors. Biochem Biophys Res Commun 320:523–530

    Article  PubMed  CAS  Google Scholar 

  143. Somanchi A, Barnes D, Mayfield SP (2005) A nuclear gene of Chlamydomonas reinhardtii, Tba1, encodes a putative oxidoreductase required for translation of the chloroplast psbA mRNA. Plant J 42:341–352

    Article  PubMed  CAS  Google Scholar 

  144. Sorensen MA, Fricke J, Pedersen S (1998) Ribosomal protein S1 is required for translation of most, if not all, natural mRNAs in Escherichia coli in vivo. J Mol Biol 280:561–569

    Article  PubMed  CAS  Google Scholar 

  145. Sreedharan SP, Beck CM, Spremulli LL (1985) Euglena gracilis chloroplast elongation factor Tu. Purification and initial characterization. J Biol Chem 260:3126–3131

    PubMed  CAS  Google Scholar 

  146. Stampacchia O, Girard-Bascou J, Zanasco JL, Zerges W, Bennoun P, Rochaix JD (1997) A nuclear-encoded function essential for translation of the chloroplast psaB mRNA in Chlamydomonas. Plant Cell 9:773–782

    PubMed  CAS  Google Scholar 

  147. Staub JM, Maliga P (1994) Translation of psbA mRNA is regulated by light via the 5'-untranslated region in tobacco plastids. Plant J 6:547–553

    Article  PubMed  CAS  Google Scholar 

  148. Steege DA, Graves MC, Spremulli LL (1982) Euglena gracilis chloroplast small subunit rRNA. Sequence and base pairing potential of the 3' terminus, cleavage by colicin E3. J Biol Chem 257:10430–10439

    PubMed  CAS  Google Scholar 

  149. Stern DB, Higgs DC, Yang JJ (1997) Transcription and translation in chloroplasts. Trends in Plant Science 2:308–315

    Article  Google Scholar 

  150. Stollar NE, Kim JK, Hollingsworth MJ (1994) Ribosomes pause during the expression of the large ATP synthase gene cluster in spinach chloroplasts. Plant Physiol 105:1167–1177

    Article  PubMed  CAS  Google Scholar 

  151. Subramanian AR (1983) Structure and functions of ribosomal protein S1. Prog Nucleic Acid Res Mol Biol 28:101–142

    Article  PubMed  CAS  Google Scholar 

  152. Sugita M, Sugita C, Sugiura M (1995) Structure and expression of the gene encoding ribosomal protein S1 from the cyanobacterium Synechococcus sp. strain PCC 6301: striking sequence similarity to the chloroplast ribosomal protein CS1. Mol Gen Genet 246:142–147

    Article  PubMed  CAS  Google Scholar 

  153. Sugiura M, Hirose T, Sugita M (1998) Evolution and mechanism of translation in chloroplasts. Annu Rev Genet 32:437–459

    Article  PubMed  CAS  Google Scholar 

  154. Taniguchi M, Kuroda H, Satoh K (1993) ATP-dependent protein synthesis in isolated pea chloroplasts. Evidence for accumulation of a translation intermediate of the D1 protein. FEBS Lett 317:57–61

    Article  PubMed  CAS  Google Scholar 

  155. Trebitsh T, Danon A (2001) Translation of chloroplast psbA mRNA is regulated by signals initiated by both photosystems II and I. Proc Natl Acad Sci USA 98:12289–12294

    Article  PubMed  CAS  Google Scholar 

  156. Trebitsh T, Levitan A, Sofer A, Danon A (2000) Translation of chloroplast psbA mRNA is modulated in the light by counteracting oxidizing and reducing activities. Mol Cell Biol 20:1116–1123

    Article  PubMed  CAS  Google Scholar 

  157. Trebitsh T, Meiri E, Ostersetzer O, Adam Z, Danon A (2001) The protein disulfide isomerase-like RB60 is partitioned between stroma and thylakoids in Chlamydomonas reinhardtii chloroplasts. J Biol Chem 276:4564–4569

    Article  PubMed  CAS  Google Scholar 

  158. van Wijk KJ (2004) Plastid proteomics. Plant Physiol Biochem 42:963–977

    Article  PubMed  CAS  Google Scholar 

  159. Voorma HO (1996) Control of translation initiation in prokaryotes In: Hershey JWB, Mathhews MB, Sonenberg N (eds) Translational control. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, pp 759–777

    Google Scholar 

  160. Wang CC, Spremulli LL (1991) Chloroplast translational initiation factor 3. Purification and characterization of multiple forms from Euglena gracilis. J Biol Chem 266:17079–17083

    PubMed  CAS  Google Scholar 

  161. Wostrikoff K, Choquet Y, Wollman FA, Girard-Bascou J (2001) TCA1, a single nuclear-encoded translational activator specific for petA mRNA in Chlamydomonas reinhardtii chloroplast. Genetics 159:119–132

    PubMed  CAS  Google Scholar 

  162. Wostrikoff K, Girard-Bascou J, Wollman FA, Choquet Y (2004) Biogenesis of PSI involves a cascade of translational autoregulation in the chloroplast of Chlamydomonas. EMBO J 23:2696–2705

    Article  PubMed  CAS  Google Scholar 

  163. Yamaguchi K, Beligni MV, Prieto S, Haynes PA, McDonald WH, Yates JR 3rd, Mayfield SP (2003) Proteomic characterization of the Chlamydomonas reinhardtii chloroplast ribosome. Identification of proteins unique to th e70 S ribosome. J Biol Chem 278:33774–33785

    Article  PubMed  CAS  Google Scholar 

  164. Yamaguchi K, Prieto S, Beligni MV, Haynes PA, McDonald WH, Yates JR 3rd, Mayfield SP (2002) Proteomic characterization of the small subunit of Chlamydomonas reinhardtii chloroplast ribosome: identification of a novel S1 domain-containing protein and unusually large orthologs of bacterial S2, S3, and S5. Plant Cell 14:2957–2974

    Article  PubMed  CAS  Google Scholar 

  165. Yamaguchi K, Subramanian AR (2000) The plastid ribosomal proteins. Identification of all the proteins in the 50 S subunit of an organelle ribosome (chloroplast). J Biol Chem 275:28466–28482

    Article  PubMed  CAS  Google Scholar 

  166. Yamaguchi K, von Knoblauch K, Subramanian AR (2000) The plastid ribosomal proteins. Identification of all the proteins in the 30 S subunit of an organelle ribosome (chloroplast). J Biol Chem 275:28455–28465

    Article  PubMed  CAS  Google Scholar 

  167. Yohn CB, Cohen A, Danon A, Mayfield SP (1996) Altered mRNA binding activity and decreased translational initiation in a nuclear mutant lacking translation of the chloroplast psbA mRNA. Mol Cell Biol 16:3560–3566

    PubMed  CAS  Google Scholar 

  168. Yohn CB, Cohen A, Danon A, Mayfield SP (1998a) A poly(A) binding protein functions in the chloroplast as a message-specific translation factor. Proc Natl Acad Sci USA 95:2238–2243

    Article  PubMed  CAS  Google Scholar 

  169. Yohn CB, Cohen A, Rosch C, Kuchka MR, Mayfield SP (1998b) Translation of the chloroplast psbA mRNA requires the nuclear-encoded poly(A)-binding protein, RB47. J Cell Biol 142:435–442

    Article  PubMed  CAS  Google Scholar 

  170. Yu NJ, Spremulli LL (1998) Regulation of the activity of chloroplast translational initiation factor 3 by NH2- and COOH-terminal extensions. J Biol Chem 273:3871–3877

    Article  PubMed  CAS  Google Scholar 

  171. Zerges W (2000) Translation in chloroplasts. Biochimie 82:583–601

    Article  PubMed  CAS  Google Scholar 

  172. Zerges W, Auchincloss AH, Rochaix JD (2003) Multiple translational control sequences in the 5' leader of the chloroplast psbC mRNA interact with nuclear gene products in Chlamydomonas reinhardtii. Genetics 163:895–904

    PubMed  CAS  Google Scholar 

  173. Zerges W, Girard-Bascou J, Rochaix JD (1997) Translation of the chloroplast psbC mRNA is controlled by interactions between its 5' leader and the nuclear loci TBC1 and TBC3 in Chlamydomonas reinhardtii. Mol Cell Biol 17:3440–3448

    PubMed  CAS  Google Scholar 

  174. Zerges W, Rochaix JD (1994) The 5' leader of a chloroplast mRNA mediates the translational requirements for two nucleus-encoded functions in Chlamydomonas reinhardtii. Mol Cell Biol 14:5268–5277

    PubMed  CAS  Google Scholar 

  175. Zerges W, Rochaix JD (1998) Low density membranes are associated with RNA-binding proteins and thylakoids in the chloroplast of Chlamydomonas reinhardtii. J Cell Biol 140:101–110

    Article  PubMed  CAS  Google Scholar 

  176. Zhang L, Aro EM (2002) Synthesis, membrane insertion and assembly of the chloroplast-encoded D1 protein into photosystem II. FEBS Lett 512:13–18

    Article  PubMed  CAS  Google Scholar 

  177. Zhang L, Paakkarinen V, van Wijk KJ, Aro EM (1999) Co-translational assembly of the D1 protein into photosystem II. J Biol Chem 274:16062–16067

    Article  PubMed  CAS  Google Scholar 

  178. Zhang L, Paakkarinen V, van Wijk KJ, Aro EM (2000) Biogenesis of the chloroplast-encoded D1 protein: regulation of translation elongation, insertion, and assembly into photosystem II. Plant Cell 12:1769–1782

    PubMed  CAS  Google Scholar 

  179. 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  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Avihai Danon .

Editor information

Ralph Bock

Rights and permissions

Reprints and permissions

Copyright information

© 2007 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Peled-Zehavi, H., Danon, A. (2007). Translation and translational regulation 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_0234

Download citation

Publish with us

Policies and ethics