Abstract
The chloroplast genome in flowering plants contains about 80 protein-coding genes. The chloroplast translational machinery, which is similar to that of Escherichia coli, reads the corresponding mRNAs. Translation initiation is critical to produce a correct protein. There are multiple possible initiation codons, either AUG or GUG, around an initiation region. Generally, cis-elements residing in a 5′-untranslated region and trans-acting factors are responsible for selection of genuine initiation codons. Unlike eubacterial mRNAs, a limited number of chloroplast mRNAs use Shine-Dalgarno-like sequences as their cis-elements, and many chloroplast mRNAs require specific trans-acting factors. As the chloroplast genome is compact, some genes (cistrons) partially overlap; namely, the start codon of a downstream cistron is located in front of the stop codon of its upstream cistron. In such a case, the downstream cistron is translated in a special manner called “translational coupling” and by an additional mechanism to produce the necessary amount of its product.
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References
Adachi Y, Kuroda H, Yukawa Y et al (2012) Translation of partially overlapping psbD-psbC mRNAs in chloroplasts: the role of 5′-processing and translational coupling. Nucl Acids Res 40:3152–3158
Alexander C, Faber N, Klaff P (1998) Characterization of protein-binding to the spinach chloroplast psbA mRNA 5′untranslated region. Nucl Acids Res 26:2265–2272
Alkatib S, Scharff LB, Rogalski M (2012) The contributions of wobbling and superwobbling to the reading of the genetic code. PLoS Genet 8:e1003076
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
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
Barneche F, Winter V, Crèvecoeur M et al (2006) ATAB 2 is a novel factor in the signalling pathway of light-controlled synthesis of photosystem proteins. EMBO J 25:5907–5918
Barrell BG, Anderson S, Bankier AT et al (1980) Different pattern of codon recognition by mammalian mitochondrial tRNAs. Proc Natl Acad Sci USA 77:3164–3166
Bock R (2007) Structure, function, and inheritance of plastid genomes. In: Bock R (ed) Cell and molecular biology of plastids. Springer, Potsdam-Golm, pp p29–p63
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. Nucl Acids Res 22:4953–4957
Choquet Y, Wollman F-A (2002) Translational regulations as specific traits of chloroplast gene expression. FEBS Lett 529:39–42
Cohen BN, Coleman TA, Schmitt JJ et al (1984) In vitro expression and characterization of the translation start site of the psbA gene product (QB protein) from higher plants. Nucl Acids Res 12:6221–6230
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
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
Eyal Y, Goloubinoff P, Edelman M (1987) The amino terminal region delimited by Met1 and Met37 is an integral part of the 32 kDa herbicide binding protein. Plant Mol Biol 8:337–343
Giege P, Brennicke A (1999) RNA editing in Arabidopsis mitochondria effects 441 C to U changes in ORFs. Proc Natl Acad Sci USA 96:15324–15329
Hiratsuka J, Shimada H, Whhittier R et al (1989) The complete sequence of the rice (Oryza sativa) chloroplast genome: Intermolecular recombination between distinct tRNA genes accounts for a major plastid DNA inversion during the evolution of the cereals. Mol Gen Genet 217:185–194
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
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
Hirose T, Sugiura M (2004a) Functional Shine-Dalgarno-like sequences for translational initiation of chloroplast mRNAs. Plant Cell Physiol 45:114–117
Hirose T, Sugiura M (2004b) Multiple elements required for translation of plastid atpB mRNA lacking the Shine-Dalgarno sequence. Nucl Acids Res 32:3503–3510
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
Hirose T, Ideue T, Wakasugi T et al (1999) The chloroplast infA gene with a functional UUG initiation codon. FEBS 445:169–172
Hotto AM, Schmitz RJ, Fei Z et al (2011) Unexpected diversity of chloroplast noncoding RNAs as revealed by deep sequencing of the Arabidopsis transcriptome. G3(1):559–570
Ikemura T (1985) Codon usage and tRNA content in unicellular and multicellular organisms. Mol Biol Evol 2:13–34
Jackson RJ, Kaminski A, Pöyry TAA (2007) Coupled termination-reinitiation events in mRNA translation. In: Mathews MB, Sorenberg N, Herskey JWB (eds) Translational control in biology and medicine, Cold Spring Harbor Lab Press, Cold Spring Harbor, pp 197–223
Kanaya S, Yamada Y, Kinouchi M et al (2001) Codon usage and tRNA genes in eukaryotes: correlation of codon usage diversity with translation efficiency and with CG-dinucleotide usage as assessed by multivariate analysis. J Mol Evol 53:290–298
Kapoor S, Wakasugi T, Deno H et al (1994) An atpE-specific promoter within the coding region of the atpB gene in tobacco chloroplast DNA. Curr Genet 26:263–268
Karcher D, Bock R (2009) Identification of the chloroplast adenosine-to-inosine tRNA editing enzyme. RNA 15:1251–1257
Kawaguchi H, Fukuda I, Shiina T et al (1992) Dynamical behavior of psb gene transcripts in greening wheat seedlings. I. Time course of accumulation of the psbA through psbN gene transcripts during light-induced greening. Plant Mol Biol 20:695–704
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
Krebbers ET, Larrinua IM, McIntosh L et al (1982) The maize chloroplast genes for theβ and ε subunits of the photosynthetic coupling factor CF1 are fused. Nucl Acids Res 10:4985–5002
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
Lengyel P (1974) The process of translation: a bird’s-eye view. In: Nomura M, Tissières A, Lengyel P (eds) Ribosomes. Cold Spring Harbor Lab Press, Cold Spring Harbor, pp p13–p52
Link S, Engelmann K, Meierhoff K et al (2012) The Atypical short-chain dehydrogenases HCF173 and HCF244 are jointly involved in translational initiation of the psbA mRNA of Arbidopsis. Plant Physiol 160:2202–2218
Lung B, Zemann A, Madej MJ et al (2006) Identification of small non-coding RNAs from mitochondria and chloroplasts. Nucl Acids Res 34:3842–3852
Lyska D, Meierhoff K, Westhoff P (2013) How to build functional thylakoid membranes: from plastid transcription to protein complex assembly. Planta 237:413–428
Magee AM, Aspinall S, Rice DW et al (2010) Localized hypermutation and associated gene losses in legume chloroplast genomes. Genome Res 20:1700–1710
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
Manuell AL, Quispe J, Mayfield S (2007) Structure of the chloroplast ribosomes: Novel domains for translation regulation. PLoS Biol 5:e209
Marder JB, Goloubinoff P, Edelman M (1984) Molecular architecture of the rapidly metabolized 32-kilodalton protein of photosystem II. J Biol Chem 259:3900–3908
Marín-Navarro J, Manuell AL, Wu J et al (2007) Chloroplast translation regulation. Photosynth Res 94:359–374
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
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
Meierhoff K, Felder S, Nakamura T et al (2003) HCF152, an Arabidopsis RNA binding pentatricopeptide repeat protein involved in the processing of chloroplast psbB-psbT-psbH-petB-petD RNAs. Plant Cell 15:1480–1495
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
Nakamura M, Sugiura M (2009) Selection of synonymous codons for better expression of recombinant proteins in tobacco chloroplasts. Plant Biotech 26:53–56
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
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
Ohto C, Torazawa K, Tanaka M et al (1988) Transcription of ten ribosomal protein genes from tobacco chloroplasts: a compilation of ribosomal protein genes found in the tobacco chloroplast genome. Plant Mol Biol 11:589–600
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 p249–p281
Pfalz J, Bayraktar OA, Prikryl J et al (2009) Site-specific binding of a PPR protein defines and stabilizes 5′ and 3′ mRNA termini in chloroplasts. EMBO J 28:2042–2052
Pillay DTN, Guillemaut G, Weil JH (1984) Nucleotide sequences of three soybean chloroplast tRNAsLeu and re-examination of bean chloroplast tRNA Leu2 sequence. Nucl Acids Res 12:2997–3001
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
Prikryl J, Rojas M, Schuster G et al (2011) Mechanism of RNA stabilization and translational activation by a pentatricopeptide repeat protein. Proc Natl Acad Sci USA 108:415–420
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
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
Robinson M, Lilley R, Little S et al (1984) Codon usage can affect efficiency of translation of genes in Escherichia coli. Nucl Acids Res 12:6663–6671
Rochaix J-D (2001) Posttranscriptional control of chloroplast gene expression. From RNA to photosynthetic complex. Plant Physiol 125:142–144
Samuelsson T, Elias P, Lustig F et al (1980) Aberrations of the classic codon reading scheme during protein synthesis in vitro. J Biol Chem 255:4583–4588
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
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
Schmitz-Linneweber C, Small I (2008) Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci 13:663–670
Schmitz-Linneweber C, Maier RM, Alcaraz J-P et al (2001) The plastid chromosome of spinach (Spinacia oleracea): complete nucleotide sequence and gene organization. Plant Mol Biol 45:307–315
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
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
Sexton TB, Christopher DA, Mullet JE (1990) Light-induced switch in barley psbD-psbC promoter utilization: a novel mechanism regulating chloroplast gene expression. EMBO J 9:4485–4494
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
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
Shinozaki K, Deno H, Kato A et al (1983) Overlap and cotranscription of the genes for the beta and epsilon subunits of tobacco chloroplast ATPase. Gene 24:l47–l55
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
Shteiman-Kotler A, Schuster G (2000) RNA-binding characteristics of the chloroplast S1-like ribosomal protein CS1. Nucl Acids Res 28:3310–3315
Sørensen MA, Pedersen S (1991) Absolute in vivo translation rates of individual codons in Escherichia coli. The two glutamic acid codons GAA and GAG are translated with a threefold difference in rate. J Mol Biol 222:265–280
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
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
Sugita M, Sugiura M (1984) Nucleotide sequence and transcription of the gene for the 32,000 dalton thylakoid membrane protein from Nicotiana tabacum. Mol Gen Genet l95:308–3l3
Sugiura M (1987) Structure and function of the tobacco chloroplast genome. Bot Mag Tokyo 100:407–436
Sugiura M (1992) The chloroplast genome. Plant Mol Biol 19:149–168
Sugiura M (2008) RNA editing in chloroplasts. In: Goringer HU (ed) RNA editing. Springer, Berlin, pp 123–142
Sugiura M, Hirose T, Sugita M (1998) Evolution and mechanism of translation in chloroplasts. Annu Rev Genet 32:437–459
Suzuki H, Kuroda H, Yukawa Y et al (2011) The downstream atpE cistron is efficiently translated via its own cis-element in partially overlapping atpB-atpE dicistronic mRNAs in chloroplasts. Nucl Acids Res 39:9405–9412
Takahashi M, Shiraishi T, Asada K (1988) COOH-terminal residues of D1 and the 44 kDa CPa-2 at spinach photosystem II core complex. FEBS Lett 240:6–8
Vera A, Sugiura M (1994) A novel RNA gene in the tobacco plastid genome: its possible role in the maturation of 16S rRNA. EMBO J 13:2211–2217
Vera A, Matsubayashi T, Sugiura M (1992) Active transcription from a promoter positioned within the coding region of a divergently oriented gene: the tobacco chloroplast rpl32 gene. Mol Gen Genet 233:151–156
Wakasugi T, Nagai T, Kapoor M et al (1997) Complete nucleotide sequence of the chloroplast genome from the green alga Chlorella vulgaris: The existence of genes possibly involved in chloroplast division. Proc Natl Acad Sci USA 94:5967–5972
Wakasugi T, Tsudzuki T, Sugiura M (2001) The genomics of land plant chloroplasts: Gene content and alteration of genomic information by RNA editing. Photosynth Res 70:107–118
Wicke S, Schneeweiss GM, Claude W et al (2011) The evolution of the plastid chromosome in land plants: gene content, gene order, gene function. Plant Mol Biol 76:273–297
Wobbe L, Schwarz C, Nickelsen J et al (2008) Translational control of photosynthetic gene expression in phototrophic eukaryotes. Physiol Plant 133:507–515
Wolfe KH, Morden CW, Ems SC et al (1992) Rapid evolution of the plastid translational apparatus in a nonphotosynthetic plant: loss or accelerated sequence evolution of tRNA and ribosomal protein genes. J Mol Evol 35:304–317
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
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
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
Yao WB, Meng BY, Tanaka M et al (1989) An additional promoter within the protein-coding region of the psbD-psbC gene cluster in tobacco chloroplast DNA. Nucl Acids Res 17:9583–9591
Yukawa M, Sugiura M (2008) Termination codon-dependent translation of partially overlapping ndhC-ndhK transcripts in chloroplasts. Proc Natl Acad Sci USA 105:19549–19553
Yukawa M, Sugiura M (2013) Additional pathway to translate the downstream ndhK cistron in partially overlapping ndhC-ndhK mRNAs in chloroplasts. Proc Nucl Acid Sci USA 110:5701–5706
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
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
Zurawski G, Bottomley W, Whitfeld PR (1982) Structures of the genes for the β and ε subunits of spinach chloroplast ATPase indicate a dicistronic mRNA and an overlapping translation stop/start signal. Proc Natl Acad Sci USA 79:6260–6264
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Sugiura, M. (2013). Translation in Chloroplasts of Flowering Plants. In: Duchêne, AM. (eds) Translation in Mitochondria and Other Organelles. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-39426-3_9
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