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Chloroplast translation regulation

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Abstract

Chloroplast gene expression is primarily controlled during the translation of plastid mRNAs. Translation is regulated in response to a variety of biotic and abiotic factors, and requires a coordinate expression with the nuclear genome. The translational apparatus of chloroplasts is related to that of bacteria, but has adopted novel mechanisms in order to execute the specific roles that this organelle performs within a eukaryotic cell. Accordingly, plastid ribosomes contain a number of chloroplast-unique proteins and domains that may function in translational regulation. Chloroplast translation regulation involves cis-acting RNA elements (located in the mRNA 5′ UTR) as well as a set of corresponding trans-acting protein factors. While regulation of chloroplast translation is primarily controlled at the initiation steps through these RNA-protein interactions, elongation steps are also targets for modulating chloroplast gene expression. Translation of chloroplast mRNAs is regulated in response to light, and the molecular mechanisms underlying this response involve changes in the redox state of key elements related to the photosynthetic electron chain, fluctuations of the ADP/ATP ratio and the generation of a proton gradient. Photosynthetic complexes also experience assembly-related autoinhibition of translation to coordinate the expression of different subunits of the same complex. Finally, the localization of all these molecular events among the different chloroplast subcompartments appear to be a crucial component of the regulatory mechanisms of chloroplast gene expression.

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Abbreviations

ROS:

Radical oxygen species

NADH dh :

NADH dehydrogenase

nt:

Nucleotides

PDI:

Protein disulfide isomerase

References

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Algire MA, Lorsch JR (2006) Where to begin? The mechanism of translation initiation codon selection in eukaryotes. Curr Opin Chem Biol 10:480–486

    PubMed  CAS  Google Scholar 

  • Allen JF (2005) Photosynthesis: the processing of redox signals in chloroplasts. Curr Biol 15:R929–R932

    PubMed  CAS  Google Scholar 

  • Allen JF, Forsberg J (2001) Molecular recognition in thylakoid structure and function. Trends Plant Sci 6:317–326

    PubMed  CAS  Google Scholar 

  • Auchincloss AH, Zerges W, Perron K, Girard-Bascou J, Rochaix JD (2002) Characterization of Tbc2, a nucleus-encoded factor specifically required for translation of the chloroplast psbC mRNA in Chlamydomonas reinhardtii. J Cell Biol 157:953–962

    PubMed  CAS  Google Scholar 

  • Balmer Y, Koller A, Val GD, Schurmann P, Buchanan BB (2004) Proteomics uncovers proteins interacting electrostatically with thioredoxin in chloroplasts. Photosynth Res 79:275–280

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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 

  • Barnes D, Cohen A, Bruick RK, Kantardjieff K, Fowler S, Efuet E, Mayfield SP (2004) Identification and characterization of a novel RNA binding protein that associates with the 5′-untranslated region of the chloroplast psbA mRNA. Biochemistry 43:8541–8550

    PubMed  CAS  Google Scholar 

  • Barnes D, Franklin S, Schultz J, Henry R, Brown E, Coragliotti A, Mayfield SP (2005) Contribution of 5′- and 3′-untranslated regions of plastid mRNAs to the expression of Chlamydomonas reinhardtii chloroplast genes. Mol Genet Genomics 274:625–636

    PubMed  CAS  Google Scholar 

  • Beligni MV, Yamaguchi K, Mayfield SP (2004a) The translational apparatus of Chlamydomonas reinhardtii chloroplast. Photosynth Res 82:315–325

    PubMed  CAS  Google Scholar 

  • Beligni MV, Yamaguchi K, Mayfield SP (2004b) 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

    PubMed  CAS  Google Scholar 

  • Bollenbach TJ, Tatman DA, Stern DB (2003) CSP41a, a multifunctional RNA-binding protein, initiates mRNA turnover in tobacco chloroplasts. Plant J 36:842–852

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Breidenbach E, Leu S, Michaels A, Boschetti A (1990) Synthesis of EF-Tu and distribution of its mRNA between stroma and thylakoids during the cell cycle of Chlamydomonas reinhardii. Biochim Biophys Acta 1048:209–216

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Brutnell TP, Sawers RJ, Mant A, Langdale JA (1999) BUNDLE SHEATH DEFECTIVE2, a novel protein required for post-translational regulation of the rbcL gene of maize. Plant Cell 11:849–864

    PubMed  CAS  Google Scholar 

  • Chen X, Simpson CL, Kindle KL, Stern DB (1997) A dominant mutation in the Chlamydomonas reinhardtii nuclear gene SIM30 suppresses translational defects caused by initiation codon mutations in chloroplast genes. Genetics 145:935–943

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Cohen I, Sapir Y, Shapira M (2006) A conserved mechanism controls translation of Rubisco large subunit in different photosynthetic organisms. Plant Physiol 141:1089–1097

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Drager RG, Higgs DC, Kindle KL, Stern DB (1999) 5′ to 3′ exoribonucleolytic activity is a normal component of chloroplast mRNA decay pathways. Plant J 19:521–531

    PubMed  CAS  Google Scholar 

  • 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 

  • Dresios J, Chappell SA, Zhou W, Mauro VP (2006) An mRNA-rRNA base-pairing mechanism for translation initiation in eukaryotes. Nat Struct Mol Biol 13:30–34

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Fey V, Wagner R, Brautigam K, Pfannschmidt T (2005) Photosynthetic redox control of nuclear gene expression. J Exp Bot 56:1491–1498

    PubMed  CAS  Google Scholar 

  • Fisk DG, Walker MB, Barkan A (1999) Molecular cloning of the maize gene crp1 reveals similarity between regulators of mitochondrial and chloroplast gene expression. EMBO J 18:2621–2630

    PubMed  CAS  Google Scholar 

  • 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 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Gold JC, Spremulli LL (1985) Euglena gracilis chloroplast initiation factor 2. Identification and initial characterization. J Biol Chem 260:14897–14900

    PubMed  CAS  Google Scholar 

  • Groves MR, Mant A, Kuhn A, Koch J, Dubel S, Robinson C, Sinning I (2001) Functional characterization of recombinant chloroplast signal recognition particle. J Biol Chem 276:27778–27786

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Herrin DL, Nickelsen J (2004) Chloroplast RNA processing and stability. Photosynth Res 82:301–314

    PubMed  CAS  Google Scholar 

  • 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 

  • 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 

  • 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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Kanamaru K, Tanaka K (2004) Roles of chloroplast RNA polymerase sigma factors in chloroplast development and stress response in higher plants. Biosci Biotechnol Biochem 68:2215–2223

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Komar AA, Hatzoglou M (2005) Internal Ribosome Entry Sites in Cellular mRNAs: mistery of their existence. J Biol Chem 280:23425–23428

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Kraus BL, Spremulli LL (1986) Chloroplast initiation factor 3 from Euglena gracilis. Identification and initial characterization. J Biol Chem 261:4781–4784

    PubMed  CAS  Google Scholar 

  • Kuroda H, Maliga P (2001) Sequences downstream of the translation initiation codon are important determinants of translation efficiency in chloroplasts. Plant Physiol 125:430–436

    PubMed  CAS  Google Scholar 

  • Laidler V, Chaddock AM, Knott TG, Walker D, Robinson C (1995) A SecY homolog in Arabidopsis thaliana. Sequence of a full-length cDNA clone and import of the precursor protein into chloroplasts. J Biol Chem 270:17664–17667

    PubMed  CAS  Google Scholar 

  • Lemaire SD, Guillon B, Le MP, Keryer E, Miginiac-Maslow M, Decottignies P (2004) New thioredoxin targets in the unicellular photosynthetic eukaryote Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 101:7475–7480

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Mayfield SP, Franklin SE (2005) Expression of human antibodies in eukaryotic micro-algae. Vaccine 23:1828–1832

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Mayfield SP, Franklin SE, Lerner RA (2003) Expression and assembly of a fully active antibody in algae. Proc Natl Acad Sci USA 100:438–442

    PubMed  CAS  Google Scholar 

  • McCarthy JE, Gualerzi C (1990) Translational control of prokaryotic gene expression. Trends Genet 6:78–85

    PubMed  CAS  Google Scholar 

  • 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 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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 

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

    PubMed  CAS  Google Scholar 

  • Nilsson R, van Wijk KJ (2002) Transient interaction of cpSRP54 with elongating nascent chains of the chloroplast-encoded D1 protein; ‘cpSRP54 caught in the act’. FEBS Lett 524:127–133

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Ossenbuhl F, Hartmann K, Nickelsen J (2002) A chloroplast RNA binding protein from stromal thylakoid membranes specifically binds to the 5′ untranslated region of the psbA mRNA. Eur J Biochem 269:3912–3919

    PubMed  CAS  Google Scholar 

  • Pfannschmidt T (2003) Chloroplast redox signals: how photosynthesis controls its own genes. Trends Plant Sci 8:33–41

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Rattanachaikunsopon P, Rosch C, Kuchka MR (1999) Cloning and characterization of the nuclear AC115 gene of Chlamydomonas reinhardtii. Plant Mol Biol 39:1–10

    PubMed  CAS  Google Scholar 

  • Reinbothe S, Reinbothe C, Heintzen C, Seidenbecher C, Parthier B (1993) A methyl jasmonate-induced shift in the length of the 5′ untranslated region impairs translation of the plastid rbcL transcript in barley. EMBO J 12:1505–1512

    PubMed  CAS  Google Scholar 

  • 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 

  • Rochaix JD, Perron K, Dauvillee D, Laroche F, Takahashi Y, Goldschmidt-Clermont M (2004) Post-transcriptional steps involved in the assembly of photosystem I in Chlamydomonas. Biochem Soc Trans 32:567–570

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Rosenblad MA, Samuelsson T (2004) Identification of chloroplast signal recognition particle RNA genes. Plant Cell Physiol 45:1633–1639

    PubMed  CAS  Google Scholar 

  • 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 

  • 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

    PubMed  CAS  Google Scholar 

  • Salvador ML, Klein U (1999) The redox state regulates RNA degradation in the chloroplast of Chlamydomonas reinhardtii. Plant Physiol 121:1367–1374

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Schuenemann D, Amin P, Hartmann E, Hoffman NE (1999) Chloroplast SecY is complexed to SecE and involved in the translocation of the 33-kDa but not the 23-kDa subunit of the oxygen-evolving complex. J Biol Chem 274:12177–12182

    PubMed  CAS  Google Scholar 

  • Shapira M, Lers A, Heifetz PB, Irihimovitz V, Osmond CB, Gillham NW, Boynton JE (1997) Differential regulation of chloroplast gene expression in Chlamydomonas reinhardtii during photoacclimation: light stress transiently suppresses synthesis of the Rubisco LSU protein while enhancing synthesis of the PS II D1 protein. Plant Mol Biol 33:1001–1011

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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 

  • 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 

  • Staub JM, Maliga P (1993) Accumulation of D1 polypeptide in tobacco plastids is regulated via the untranslated region of the psbA mRNA. EMBO J 12:601–606

    PubMed  CAS  Google Scholar 

  • Strand A, Asami T, Alonso J, Ecker JR, Chory J (2003) Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrinIX. Nature 421:79–83

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Vaistij FE, Boudreau E, Lemaire SD, Goldschmidt-Clermont M, Rochaix JD (2000b) Characterization of Mbb1, a nucleus-encoded tetratricopeptide-like repeat protein required for expression of the chloroplast psbB/psbT/psbH gene cluster in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 97:14813–14818

    PubMed  CAS  Google Scholar 

  • Wagner V, Gessner G, Heiland I, Kaminski M, Hawat S, Scheffler K, Mittag M (2006) Analysis of the phosphoproteome of Chlamydomonas reinhardtii provides new insights into various cellular pathways. Eukaryot Cell 5:457–468

    PubMed  CAS  Google Scholar 

  • 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 

  • 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

    PubMed  CAS  Google Scholar 

  • Wu HY, Kuchka MR (1995) A nuclear suppressor overcomes defects in the synthesis of the chloroplast psbD gene product caused by mutations in two distinct nuclear genes of Chlamydomonas. Curr Genet 27:263–269

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Yamaguchi K, Prieto S, Beligni MV, Haynes PA, McDonald WH, Yates JR III, 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

    PubMed  CAS  Google Scholar 

  • Yamaguchi K, Beligni MV, Prieto S, Haynes PA, McDonald WH, Yates JR III, Mayfield SP (2003) Proteomic characterization of the Chlamydomonas reinhardtii chloroplast ribosome. Identification of proteins unique to the 70S ribosome. J Biol Chem 278:33774–33785

    PubMed  CAS  Google Scholar 

  • 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 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Yosef I, Irihimovitch V, Knopf JA, Cohen I, Orr-Dahan I, Nahum E, Keasar C, Shapira M (2004) RNA binding activity of the ribulose-1,5–bisphosphate carboxylase/oxygenase large subunit from Chlamydomonas reinhardtii. J Biol Chem 279:10148–10156

    PubMed  CAS  Google Scholar 

  • Yukawa M, Kuroda H, Sugiura M (2007) A new in vitro translation system for non-radioactive assay from tobacco chloroplasts: effect of pre-mRNA processing on translation in vitro. Plant J 49:367–376

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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 

  • Zerges W, Wang S, Rochaix JD (2002) Light activates binding of membrane proteins to chloroplast RNAs in Chlamydomonas reinhardtii. Plant Mol Biol 50:573–585

    PubMed  CAS  Google Scholar 

  • 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 

  • 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 

  • Zhang L, Paakkarinen V, Suorsa M, Aro EM (2001) A SecY homologue is involved in chloroplast-encoded D1 protein biogenesis. J Biol Chem 276:37809–37814

    PubMed  CAS  Google Scholar 

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Acknowledgments

We would like to thank Maria Verónica Beligni for review of this manuscript, the Fundación Ramón Areces from Spain for funding of J.M.-N., and the William and Sharon Bauce Family Foundation and the Skaggs Institute for Chemical Biology for support of A.L.M.

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Correspondence to Stephen P. Mayfield.

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Marín-Navarro, J., Manuell, A.L., Wu, J. et al. Chloroplast translation regulation. Photosynth Res 94, 359–374 (2007). https://doi.org/10.1007/s11120-007-9183-z

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  • DOI: https://doi.org/10.1007/s11120-007-9183-z

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