Skip to main content

Plastid mRNA Translation

  • Protocol
  • First Online:
Chloroplast Biotechnology

Part of the book series: Methods in Molecular Biology ((MIMB,volume 1132))

Abstract

Overall translational machinery in plastids is similar to that of E. coli. Initiation is the crucial step for translation and this step in plastids is somewhat different from that of E. coli. Unlike the Shine-Dalgarno sequence in E. coli, cis-elements for translation initiation are not well conserved in plastid mRNAs. Specific trans-acting factors are generally required for translation initiation and its regulation in plastids. During translation elongation, ribosomes pause sometimes on photosynthesis-related mRNAs due probably to proper insertion of nascent polypeptides into membrane complexes. Codon usage of plastid mRNAs is different from that of E. coli and mammalian cells. Plastid mRNAs do not have the so-called rare codons. Translation efficiencies of several synonymous codons are not always correlated with codon usage in plastid mRNAs.

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

Access this chapter

Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 109.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 139.99
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

References

  1. Sugiura M (1992) The chloroplast genome. Plant Mol Biol 19:149–168

    CAS  PubMed  Google Scholar 

  2. Bock R (2007) Structure, function, and inheritance of plastid genomes. In: Bock R (ed) Cell and molecular biology of plastids. Springer, Potsdam-Golm, pp 29–63

    Google Scholar 

  3. Shinozaki K, Ohme M, Tanaka M et al (1986) The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J 5: 2043–2049

    CAS  PubMed Central  PubMed  Google Scholar 

  4. Sugita M, Sugiura M (1996) Regulation of gene expression in chloroplasts of higher plants. Plant Mol Biol 32:315–326

    CAS  PubMed  Google Scholar 

  5. Tanaka M, Obokata J, Chunwongse J et al (1987) Rapid splicing and stepwise processing of a transcript from the psbB operon in tobacco chloroplasts. Mol Gen Genet 209:427–431

    CAS  PubMed  Google Scholar 

  6. Matsubayashi T, Wakasugi T, Shinozaki K et al (1987) Six chloroplast genes (ndhA-F) homologous to human mitochondrial genes encoding components of the respiratory chain NADH dehydrogenase are actively expressed: determination of the splice sites in ndhA and ndhB pre-mRNAs. Mol Gen Genet 210:385–393

    CAS  PubMed  Google Scholar 

  7. Barkan A (1988) Proteins encoded by a complex chloroplast transcription unit are each translated from both monocistronic and polycistronic mRNAs. EMBO J 7:2637–2644

    CAS  PubMed Central  PubMed  Google Scholar 

  8. Westhoff P, Herrmann RG (1988) Complex RNA maturation in chloroplasts. The psbB operon from spinach. Eur J Biochem 171: 551–564

    CAS  PubMed  Google Scholar 

  9. Shinozaki K, Deno H, Sugita M et al (1986) Intron in the gene for the ribosomal protein Sl6 of tobacco chloroplast and its conserved boundary sequences. Mol Gen Genet 202:1–5

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  11. Sugiura M (2008) RNA editing in chloroplasts. In: Goringer HU (ed) RNA editing. Springer, Berlin, pp 123–142

    Google Scholar 

  12. Chateigner-Boutin AL, Small I (2010) Plant RNA editing. RNA Biol 7:213–219

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  14. Schuster G, Lisitsky I, Klaff P (1999) Polyadenylation and degradation of mRNA in the chloroplast. Plant Physiol 120:937–944

    CAS  PubMed Central  PubMed  Google Scholar 

  15. 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

    CAS  PubMed Central  PubMed  Google Scholar 

  16. Yukawa M, Sugiura M (2008) Termination codon-dependent translation of partially overlapping ndhC-ndhK transcripts in chloroplasts. Proc Natl Acad Sci USA 105: 19550–19554

    CAS  PubMed Central  PubMed  Google Scholar 

  17. Gruissem W (1989) Chloroplast gene expression: how plants turn their plastids on. Cell 56:161–170

    CAS  PubMed  Google Scholar 

  18. Romby P, Springer M (2007) Translational control in prokaryotes. In: Mathews MB, Sonenberg N, Hershey JWB (eds) Translational control in biology and medicine. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 803–827

    Google Scholar 

  19. Marín-Navarro J, Manuell AL, Wu J et al (2007) Chloroplast translation regulation. Photosynth Res 94:359–374

    PubMed  Google Scholar 

  20. Peled-Zehavi H, Danon A (2007) Translation and translational regulation in chloroplasts. In: Bock R (ed) Cell and molecular biology of plastids. Springer, Potsdam-Golm, pp 249–281

    Google Scholar 

  21. Waters MT, Langdale JA (2009) The making of a chloroplast. EMBO J 28:2861–2873

    CAS  PubMed Central  PubMed  Google Scholar 

  22. Wobbe L, Schwarz C, Nickelsen J et al (2008) Translational control of photosynthetic gene expression in phototrophic eukaryotes. Physiol Plant 133:507–515

    CAS  PubMed  Google Scholar 

  23. Rochaix J-D (2001) Posttranscriptional control of chloroplast gene expression. From RNA to photosynthetic complex. Plant Physiol 125:142–144

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  27. Schuster G, Stern D (2009) RNA polyadenylation and decay in mitochondria and chloroplasts. Prog Mol Biol Transl Sci 85:393–422

    CAS  PubMed  Google Scholar 

  28. Whitfeld PR, Jeaver CJ, Bottomley W et al (1978) Low-molecular-weight (4.5S) ribonucleic acid in higher-plant chloroplast ribosomes. Biochem J 175:1103–1112

    CAS  PubMed Central  PubMed  Google Scholar 

  29. Bowman CM, Dyer TA (1979) 4.5S ribonucleic acid, a novel ribosome component in the chloroplasts of flowering plants. Biochem J 183:605–613

    CAS  PubMed Central  PubMed  Google Scholar 

  30. Gantt JS (1988) Nucleotide sequences of cDNAs encoding four complete nuclear-encoded plastid ribosomal proteins. Curr Genet 14:519–528

    CAS  PubMed  Google Scholar 

  31. Sugiura M, Torazawa K, Wakasugi T et al (1991) Chloroplast genes coding for ribosomal proteins in land plants. In: Mache R, Stutz E, Subramanian AR (eds) The translational apparatus of photosynthetic organelles. Springer, Berlin, pp 59–69

    Google Scholar 

  32. Yamaguchi K, von 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

    CAS  PubMed  Google Scholar 

  33. 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

    CAS  PubMed  Google Scholar 

  34. Maki Y, Tanaka A, Wada A (2000) Stoichiometric analysis of barley plastid ribosomal proteins. Plant Cell Physiol 41: 289–299

    CAS  PubMed  Google Scholar 

  35. Yamaguchi K, Subramanian AR (2003) Proteomic identification of all plastid-specific ribosomal proteins in higher plant chloroplast 30S ribosomal subunit PSRP-2 (U1A-type domains), PSRP-3α/β (ycf65 homologue) and PSRP-4 (Thx homologue). Eur J Biochem 270:190–205

    CAS  PubMed  Google Scholar 

  36. Carol P, Li YF, Mache R (1991) Conservation and evolution of the nucleus-encoded and chloroplast-specific ribosomal proteins in pea and spinach. Gene 103:139–145

    CAS  PubMed  Google Scholar 

  37. Rolland N, Janosi L, Block MA et al (1999) Plant ribosome recycling factor homologue is a chloroplastic protein and is bactericidal in Escherichia coli carrying temperature-sensitive ribosome recycling factor. Proc Natl Acad Sci USA 96:5464–5469

    CAS  PubMed Central  PubMed  Google Scholar 

  38. Wittmann HG (1983) Architecture of prokaryotic ribosomes. Annu Rev Biochem 52:35–65

    CAS  PubMed  Google Scholar 

  39. Capel MS, Bourque DP (1982) Characterization of Nicotiana tabacum chloroplast and cytoplasmic ribosomal proteins. J Biol Chem 257:7746–7755

    CAS  PubMed  Google Scholar 

  40. Sugita C, Sugiura M, Sugita M (2000) A novel nucleic acid-binding protein in the cyanobacterium Synechococcus sp. PCC6301: a soluble 33-kDa polypeptide with high sequence similarity to ribosomal protein S1. Mol Gen Genet 263:655–663

    CAS  PubMed  Google Scholar 

  41. Sharma MR, Dönhöfer A, Barat C et al (2010) PSRP1 is not a ribosomal protein, but a ribosome-binding factor that is recycled by the ribosome-recycling factor (RRF) and elongation factor G (EF-G). J Biol Chem 285:4006–4014

    CAS  PubMed Central  PubMed  Google Scholar 

  42. Sharma MR, Wilson DN, Datta PP et al (2007) Cryo-EM study of the spinach chloroplast ribosome reveals the structural and functional roles of plastid-specific ribosomal proteins. Proc Natl Acad Sci USA 104: 19315–19320

    CAS  PubMed Central  PubMed  Google Scholar 

  43. Rogalski M, Schöttler MA, Thiele W et al (2008) Rpl33, a nonessential plastid-encoded ribosomal protein in tobacco, is required under cold stress conditions. Plant Cell 20:2221–2237

    CAS  PubMed Central  PubMed  Google Scholar 

  44. Fromm H, Devic M, Fluhr R et al (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

    CAS  PubMed Central  PubMed  Google Scholar 

  45. Sugiura M (1987) Structure and function of the tobacco chloroplast genome. Bot Mag Tokyo 100:407–436

    CAS  Google Scholar 

  46. Curran JF (1995) Decoding with the A:I wobble pair is inefficient. Nucleic Acids Res 23:683–688

    CAS  PubMed Central  PubMed  Google Scholar 

  47. Rogalski M, Karcher D, Bock R (2008) Superwobbling facilitates translation with reduced tRNA sets. Nat Struct Mol Biol 15:192–198

    CAS  PubMed  Google Scholar 

  48. Delannoy E, Le Ret M, Faivre-Nitschke E et al (2009) Arabidopsis tRNA adenosine deaminase arginine edits the wobble nucleotide of chloroplast tRNAArg(ACG) and is essential for efficient chloroplast translation. Plant Cell 21:2058–2071

    CAS  PubMed Central  PubMed  Google Scholar 

  49. Karcher D, Bock R (2009) Identification of the chloroplast adenosine-to-inosine tRNA editing enzyme. RNA 15:1251–1257

    CAS  PubMed Central  PubMed  Google Scholar 

  50. Jahn D, Verkamp E, Söll D (1992) Glutamyl-transfer RNA: a precursor of heme and chlorophyll biosynthesis. Trends Biochem Sci 17:215–218

    CAS  PubMed  Google Scholar 

  51. Wang MJ, Davis NW, Gegenheimer PA (1988) Novel mechanisms for maturation of chloroplast transfer RNA precursors. EMBO J 7:1567–1574

    CAS  PubMed Central  PubMed  Google Scholar 

  52. Gobert A, Gutmann B, Taschner A et al (2010) A single Arabidopsis organellar protein has RNase P activity. Nat Struct Mol Biol 17:740–744

    CAS  PubMed  Google Scholar 

  53. Wakasugi T, Nagai T, Kapoor M et al (1997) Complete sequencing of the chloroplast genome of the green alga Chlorella vulgaris reveals the existence of genes possibly involved in chloroplast division. Proc Natl Acad Sci USA 94:5967–5972

    CAS  PubMed Central  PubMed  Google Scholar 

  54. Hirose T, Ideue T, Wakasugi T et al (1999) The chloroplast infA gene with a functional UUA initiation codon. FEBS Lett 445: 169–172

    CAS  PubMed  Google Scholar 

  55. Kuroda H, Suzuki H, Kusumegi T et al (2007) Translation of psbC mRNAs starts from the downstream GUG, not the upstream AUG, and requires the extended Shine-Dalgarno sequence in tobacco chloroplasts. Plant Cell Physiol 48:1374–1378

    CAS  PubMed  Google Scholar 

  56. Kudla J, Igloi GL, Metzlaff M et al (1992) RNA editing in tobacco chloroplasts leads to the formation of a translatable psbL mRNA by a C to U substitution within the initiation codon. EMBO J 11:1099–1103

    CAS  PubMed Central  PubMed  Google Scholar 

  57. Neckermann K, Zeltz P, Igloi GL et al (1994) The role of RNA editing in conservation of start codons in chloroplast genomes. Gene 146:177–182

    CAS  PubMed  Google Scholar 

  58. Svab Z, Maliga P (1993) High-frequency plastid transformation in tobacco by selection for a chimeric aadA gene. Proc Natl Acad Sci USA 90:913–917

    CAS  PubMed Central  PubMed  Google Scholar 

  59. Maliga P (2004) Plastid transformation in higher plants. Annu Rev Plant Biol 55: 289–313

    CAS  PubMed  Google Scholar 

  60. Hartz D, McPheeters DS, Traut R et al (1988) Extension inhibition analysis of translation initiation complexes. Methods Enzymol 164:419–425

    CAS  PubMed  Google Scholar 

  61. 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

    CAS  PubMed  Google Scholar 

  62. 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

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  64. 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

    CAS  PubMed Central  PubMed  Google Scholar 

  65. Eibl C, Zou Z, Beck A et al (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

    CAS  PubMed  Google Scholar 

  66. 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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  68. 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

    CAS  PubMed  Google Scholar 

  69. Reinbothe S, Reinbothe C, Heintzen C et al (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

    CAS  PubMed Central  PubMed  Google Scholar 

  70. Barkan A, Walker M, Nolasco M et al (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

    CAS  PubMed Central  PubMed  Google Scholar 

  71. Monde RA, Greene JC, Stern DB (2000) Disruption of the petB-petD intergenic region in tobacco chloroplasts affects petD RNA accumulation and translation. Mol Gen Genet 263:610–618

    CAS  PubMed  Google Scholar 

  72. Felder S, Meierhoff K, Sane AP et al (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

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  74. Walter M, Piepenburg K, Schöttler MA et al (2010) Knockout of the plastid RNase E leads to defective RNA processing and chloroplast ribosome deficiency. Plant J 64:851–863

    CAS  PubMed  Google Scholar 

  75. Staub JM, Maliga P (1995) Expression of a chimeric uidA gene indicates that polycistronic mRNAs are efficiently translated in tobacco plastids. Plant J 7:845–848

    CAS  PubMed  Google Scholar 

  76. Quesada-Vargas T, Ruiz ON, Daniell H (2005) Characterization of heterologous multigene operons in transgenic chloroplasts: transcription, processing, and translation. Plant Physiol 138:1746–1762

    CAS  PubMed Central  PubMed  Google Scholar 

  77. Suzuki H, Kuroda H, Yukawa Y, Sugiura M (2011) The downstream atpE cistron is efficiently translated via its own cis-element in partially overlapping atpB-atpE dicistronic mRNAs in chloroplasts. Nucleic Acids Res 39:9405–9412

    CAS  PubMed Central  PubMed  Google Scholar 

  78. Yukawa M, Sugiura M (2013) Additional pathway to translate the downstream ndhK cistron in partially overlapping ndhC-ndhK mRNAs in chloroplasts. Proc Natl Acad Sci USA 110:5701–5706

    CAS  PubMed Central  PubMed  Google Scholar 

  79. Adachi Y, Kuroda H, Yukawa Y, Sugiura M (2012) Translation of partially overlapping psbD-psbC mRNAs in chloroplasts: the role of 5′-processing and translational coupling. Nucleic Acids Res 40:3152–3158

    CAS  PubMed Central  PubMed  Google Scholar 

  80. Yukawa M, Tsudzuki T, Sugiura M (2005) The 2005 version of the chloroplast DNA sequence from tobacco (Nicotiana tabacum). Plant Mol Biol Rep 23:359–365

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  82. 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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  84. Shine J, Dalgarno L (1974) The 3′-terminal sequence of Escherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites. Proc Natl Acad Sci USA 71:1342–1346

    CAS  PubMed Central  PubMed  Google Scholar 

  85. Chen H, Bjerknes M, Kumar R et al (1994) Determination of the optimal aligned spacing between the Shine-Dalgarno sequence and the translation initiation codon of Escherichia coli mRNAs. Nucleic Acids Res 22:4953–4957

    CAS  PubMed Central  PubMed  Google Scholar 

  86. Hui A, de Boer HA (1987) Specialized ribosome system: preferential translation of a single mRNA species by a subpopulation of mutated ribosomes in Escherichia coli. Proc Natl Acad Sci USA 84:4762–4766

    CAS  PubMed Central  PubMed  Google Scholar 

  87. Jacob WF, Santer M, Dahlberg AE (1987) A single base change in the Shine-Dalgarno region of 16S rRNA of Escherichia coli affects translation of many proteins. Proc Natl Acad Sci USA 84:4757–4761

    CAS  PubMed Central  PubMed  Google Scholar 

  88. Mutsuda M, Sugiura M (2006) Translation initiation of cyanobacterial rbcS mRNAs requires the 38-kDa ribosomal protein S1 but not the Shine-Dalgarno sequence: development of a cyanobacterial in vitro translation system. J Biol Chem 281:38314–38321

    CAS  PubMed  Google Scholar 

  89. 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

    CAS  PubMed  Google Scholar 

  90. Baecker JJ, Sneddon JC, Hollingsworth MJ (2009) Efficient translation in chloroplasts requires element(s) upstream of the putative ribosome binding site from atpI. Am J Bot 96:627–636

    CAS  PubMed  Google Scholar 

  91. Drechsel O, Bock R (2010) Selection of Shine-Dalgarno sequences in plastids. Nucleic Acids Res. doi:10.1093/nar/gkq978

    PubMed Central  PubMed  Google Scholar 

  92. Kuroda H, Maliga P (2001) Complementarity of the 16S rRNA penultimate stem with sequences downstream of the AUG destabilizes the plastid mRNAs. Nucleic Acids Res 29:970–975

    CAS  PubMed Central  PubMed  Google Scholar 

  93. Inamine G, Nash B, Weissbach H et al (1985) Light regulation of the synthesis of the large subunit of ribulose-1, 5-bisphosphate carboxylase in peas: evidence for translational control. Proc Natl Acad Sci USA 82:5690–5694

    CAS  PubMed Central  PubMed  Google Scholar 

  94. Shiina T, Allison L, Maliga P (1998) RbcL transcript levels in tobacco plastids are independent of light: reduced dark transcription rate is compensated by increased mRNA stability. Plant Cell 10:1713–1722

    CAS  PubMed Central  PubMed  Google Scholar 

  95. Kahlau S, Bock R (2008) Plastid transcriptomics and translatomics of tomato fruit development and chloroplast-to-chromoplast differentiation: chromoplast gene expression largely serves the production of a single protein. Plant Cell 20:856–874

    CAS  PubMed Central  PubMed  Google Scholar 

  96. 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

    CAS  PubMed Central  PubMed  Google Scholar 

  97. 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

    CAS  PubMed Central  PubMed  Google Scholar 

  98. Schult K, Meierhoff K, Paradies S et al (2007) The nuclear-encoded factor HCF173 is involved in the initiation of translation of the psbA mRNA in Arabidopsis thaliana. Plant Cell 19:1329–1346

    CAS  PubMed Central  PubMed  Google Scholar 

  99. Klaff P, Mundt SM, Steger G (1997) Complex formation of the spinach chloroplast psbA mRNA 5′ untranslated region with proteins is dependent on the RNA structure. RNA 3:1468–1479

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  101. Merhige PM, Both-Kim D, Robida MD et al (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

    CAS  PubMed  Google Scholar 

  102. 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

    CAS  PubMed  Google Scholar 

  103. Klaff P, Gruissem W (1995) A 43 kD light-regulated chloroplast RNA-binding protein interacts with the psbA 5′ non-translated leader RNA. Photosynth Res 46:235–248

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  108. Wostrikoff K, Stern D (2007) Rubisco large-subunit translation is autoregulated in response to its assembly state in tobacco chloroplasts. Proc Natl Acad Sci USA 104:6466–6471

    CAS  PubMed Central  PubMed  Google Scholar 

  109. Ichikawa K, Miyake C, Iwano M et al (2008) Ribulose 1,5-bisphosphate carboxylase/oxygenase large subunit translation is regulated in a small subunit-independent manner in the expanded leaves of tobacco. Plant Cell Physiol 49:214–225

    CAS  PubMed  Google Scholar 

  110. 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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  112. Kuroda H, Inagaki N, Satoh K (1992) The level of stromal ATP regulates translation of the D1 protein in isolated chloroplasts. Plant Cell Physiol 33:33–39

    CAS  Google Scholar 

  113. 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

    CAS  PubMed  Google Scholar 

  114. 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

    CAS  PubMed  Google Scholar 

  115. Mullet JE, Klein RR, Grossman AR (1986) Optimization of protein synthesis in isolated higher plant chloroplasts. Identification of paused translation intermediates. Eur J Biochem 155:331–338

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  117. van Wijk KJ, Bingsmark S, Aro E-M et al (1995) In vitro synthesis and assembly of photosystem II core proteins. The D1 protein can be incorporated into photosystem II in isolated chloroplasts and thylakoids. J Biol Chem 270:25685–25695

    PubMed  Google Scholar 

  118. Nilsson R, Brunner J, Hoffman NE et al (1999) Interactions of ribosome nascent chain complexes of the chloroplast-encoded D1 thylakoid membrane protein with cpSRP54. EMBO J 18:733–742

    CAS  PubMed Central  PubMed  Google Scholar 

  119. Zhang L, Paakkarinen V, van Wijk KJ et al (2000) Biogenesis of the chloroplast-encoded D1 protein: regulation of translation elongation, insertion, and assembly into photosystem II. Plant Cell 12:1769–1781

    CAS  PubMed Central  PubMed  Google Scholar 

  120. 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

    CAS  PubMed Central  PubMed  Google Scholar 

  121. Minami E, Shinohara K, Kawakami N et al (1988) Localization and properties of transcripts of psbA and rbcL genes in the stroma of spinach chloroplast. Plant Cell Physiol 29:1303–1309

    CAS  Google Scholar 

  122. Mühlbauer 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  Google Scholar 

  123. Ruhlman T, Verma D, Samson N et al (2010) The role of heterologous chloroplast sequence elements in transgene integration and expression. Plant Physiol 152:2088–2104

    CAS  PubMed Central  PubMed  Google Scholar 

  124. Li Y, Sugiura M (1990) Three distinct ribonucleoproteins from tobacco chloroplasts: each contains a unique amino terminal acidic domain and two ribonucleoprotein consensus motifs. EMBO J 9:3059–3066

    CAS  PubMed Central  PubMed  Google Scholar 

  125. Li Y, Sugiura M (1991) Nucleic acid-binding specificities of tobacco chloroplast ribonucleoproteins. Nucleic Acids Res 19: 2893–2896

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  128. 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

    CAS  PubMed Central  PubMed  Google Scholar 

  129. Tillich M, Hardel SL, Kupsch C et al (2009) Chloroplast ribonucleoprotein CP31A is required for editing and stability of specific chloroplast mRNAs. Proc Natl Acad Sci USA 106:6002–6007

    CAS  PubMed Central  PubMed  Google Scholar 

  130. Prikryl J, Rojas M, Schuster G et al (2010) Mechanism of RNA stabilization and translational activation by a pentatricopeptide repeat protein. Proc Natl Acad Sci USA 108: 1415–1420

    Google Scholar 

  131. Schmitz-Linneweber C, Small I (2008) Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci 13:663–670

    CAS  PubMed  Google Scholar 

  132. Sasaki T, Yukawa Y, Miyamoto T et al (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

    CAS  PubMed  Google Scholar 

  133. Nakamura M, Sugiura M (2007) Translation efficiencies of synonymous codons are not always correlated with codon usage in tobacco chloroplasts. Plant J 49:128–134

    CAS  PubMed  Google Scholar 

  134. Ikemura T (1985) Codon usage and tRNA content in unicellular and multicellular organisms. Mol Biol Evol 2:13–34

    CAS  PubMed  Google Scholar 

  135. Gustafsson C, Govindarajan S, Minshull J (2004) Codon bias and heterologous protein expression. Trends Biotechnol 22:346–353

    CAS  PubMed  Google Scholar 

  136. Nakamura M, Sugiura M (2009) Selection of synonymous codons for better expression of recombinant proteins in tobacco chloroplasts. Plant Biotechnol 26:53–56

    CAS  Google Scholar 

  137. Nakamura M, Sugiura M (2011) Translation efficiencies of synonymous codons for arginine differ dramatically and are not correlated with codon usage in chloroplasts. Gene 472:50–54

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Science+Business Media New York

About this protocol

Cite this protocol

Sugiura, M. (2014). Plastid mRNA Translation. In: Maliga, P. (eds) Chloroplast Biotechnology. Methods in Molecular Biology, vol 1132. Humana Press, Totowa, NJ. https://doi.org/10.1007/978-1-62703-995-6_4

Download citation

  • DOI: https://doi.org/10.1007/978-1-62703-995-6_4

  • Published:

  • Publisher Name: Humana Press, Totowa, NJ

  • Print ISBN: 978-1-62703-994-9

  • Online ISBN: 978-1-62703-995-6

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics