Summary
Plastid gene expression is highly regulated in response to environmental parameters, such as light, during plant growth and development. The integrated regulation of post-transcriptional events, such as mRNA stability, mRNA processing, and translation, has been shown to play amajor role in chloroplast gene expression. Biosynthesis of many chloroplast proteins shows a requirement for nuclear-encoded proteins and hence a coordination of the two genomes. Genetic analysis of mutants and biochemical analysis of proteins involved in gene expression have begun to reveal mechanisms of plastid gene expression. Analyses of mutants in green algae and plants have identified trans-acting nuclear encoded proteins, and cis-elements in the messenger RNAs that are involved in the expression of specific chloroplast genes. Biochemical studies have identified interactions of these trans-acting proteins with cis-elements found in both the 5′and 3′ untranslated regions of plastid mRNAs. Translation initiation in chloroplast mRNAs has both prokaryotic and eukaryotic features indicating that chloroplast translational regulation is a hybrid between the two systems. An emerging theme suggests that translational regulation relies on specific RNA-protein and protein-protein interactions that influence the ability of the ribosome to correctly initiate translation at the start codon. Understanding the involvement of nuclear gene products in the regulation of chloroplast translation should allow for the identification of the mechanisms of chloroplast gene expression that facilitate the coordination of a prokaryotic-like organelle with the eukaryotic nuclear host.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Alexander C, Faber N and Klaff P (1998) Characterization of protein-binding to the spinach chloroplast psbA mRNA 5′ untranslated region. Nucleic Acids Res 26: 2265–72
Barkan A (1988) Proteins encoded by a complex chloroplast transcription unit are each translated from both monocistronic and polycistronic mRNAs. EMBO J 9: 2637–44
Barkan A (1993) Nuclear mutants of maize with defects in chloroplast polysome assembly have altered chloroplast RNA metabolism. Plant Cell 5: 389–402
Barkan A, Walker M, Nolasco M and 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
Berry JO, Nikolau BJ, Carr JP and Klessig DF (1986) Translational regulation of light-induced ribulose 1, 5-bisphosphate carboxylase gene expression in amaranth. Mol Cell Biol 6: 2347–2353
Berry JO, Breiding DE and Klessig DF (1990) Light-mediated control of translational initiation of ribulose-1,5-bisphosphate carboxylase in amaranth cotyledons. Plant Cell 2: 795–803
Betts L and 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
Blowers AD, Klein U, Ellmore GS and Bogorad (1993) Functional in vivo analyses of the 3′ flanking sequences of the Chlamydomonas chloroplast rbcL and psaB genes. Mol Gen Genet 238: 339–349
Bolle C, Herrmann RG and Oelmuller R (1996) Different sequences for 5′-untranslated leaders of nuclear genes for plastid proteins affect the expression of the beta-glucuronidase gene. Plant Mol Biol 32: 861–868
Bonham-Smith PC and Bourque DP (1989) Translation of chloroplast-encoded mRNA: Potential initiation and termination signals. Nucleic Acids Res 17: 2057–2080
Bruick RK and 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
Buchanan BB (1991) Regulation of CO2 assimilation in oxygenic photosynthesis—the ferredoxin thioredoxin system—perspective on its discovery, present status, and future development. Arch Biochem Biophys 288: 1–9
Chen Q, Osteryoung K and Vierling E (1994) A 21-kDa chloroplast heat shock protein assembles into high molecular weight complexes in vivo and in organelle. J Biol Chem 269: 13216–13223
Chen X, Kindle KL and Stern DB (1995) The initiation codon determines the efficiency but not the site of translation initiation in Chlamydomonas chloroplasts. Plant Cell 8: 1295–1305
Choquet Y, Stern DB, Wostrikoff K, Kuras R, Girard-Bascou J and 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
Christopher DA, Kim M and Mullet JE (1992) A novel light-regulated promoter is conserved in cereal and dicot chloroplasts. Plant Cell 4: 785–798
Danon A (1997) Translational regulation in the chloroplast. Plant Physiol 115: 1293–8
Danon A and Mayfield SP (1991) Light regulated translational activators: identification of chloroplast gene specific mRNA binding proteins. EMBO J 10: 3993–4001
Danon A and Mayfield SP (1994a) Light-regulated translation of chloroplast messenger RNAs through redox potential. Science 266: 1717–1719
Danon A and Mayfield SP (1994b) ADP-dependent phosphorylation regulates RNA-binding in vitro: Implications in light-modulated translation. EMBO J 13: 2227–2235
Drager RG, Zeidler M, Simpson CL and Stern DB (1996) A chloroplast transcript lacking the 3′ inverted repeat is degraded by 3′→5′ exoribonuclease activity. RNA 2: 652–63
Drager RG, Girard-Basou J, Choquet Y, Kindle KL and Stern DB (1998) In vivo evidence for 5′-3′ exoribonuclease degradation of an unstable chloroplast mRNA. Plant J 13: 85–96
Drager RG, Higgs DC, Kindle KL and Stern DB (1999) 5′ to 3′ exoribonucleolytic activity is a normal component of chloroplast mRNA decay pathways. Plant J 19: 521–531
Draper DE (1995) Protein-RNA recognition. Annu Rev Biochem 64: 593–620
Drapier D, Girard-Bascou J and Wollman FA (1992) Evidence for nuclear control of the gene expression of the atpA and atpB chloroplast genes in Chlamydomonas reinhardtii. Curr Genet 22: 47–52
Edhofer I, Muhlbauer SK and Eichacker LA (1998) Light regulates the rate of translation elongation of chloroplast reaction center protein D1. Eur J Biochem 257: 78–84
Eibl C, Zou Z, Beck A, Kim M, Mullet J and 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
Fargo DC, Zhang M, Gillham NW and 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: 271–82
Fargo DC, Boynton JE and 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
Fisk DG, Walker MB and 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
Gillham NW, Boynton JE and Hauser CR (1994) Translational regulation of gene expression in chloroplasts and mitochondria. Annu Rev Genet 28: 71–93
Gold L (1988) Post transcriptional regulatory mechanisms in Escherichia coli. Annu Rev Biochem 57: 199–233
Goldschmidt-Clermont M (1998) Coordination of nuclear and chloroplast gene expression in plant cells. Int Rev Cyt 177: 115–180
Goossen B and Hentze MW (1992) Position is the critical determinant for function of iron-responsive elements as translational regulators. Mol Cell Biol 12:1959–1966
Gruissem W and Schuster G (1993) Control ofmRNA degradation in organelles. In: Belasco JG and Brawermann G (eds) Control of Messenger RNA Stability, pp 329–365. Academic Press, San Diego
Gumpel NJ, Ralley L, Girard-Bascou J, Wollman FA, Nugent JH and Purton S (1995) Nuclear mutants of Chlamydomonas reinhardtii defective in the biogenesis of the cytochrome b6f complex. Plant Mol Biol 29: 921–32
Hampp R, Goller M and Ziegler H (1982) Adenylate levels, energy charge, and phosphorylation potential during dark-light and light-dark transition in chloroplasts, mitochondria and cytosol of mesophyll protoplasts from Avena sativa L. Plant Physiol 69: 448–455
Harris EH, Boynton JE and Gillham NW (1994) Chloroplast ribosomes and protein synthesis. Microbiol Rev 58: 700–754
Hauser CR, Randolph-Anderson BL, Hohl TM, Harris EH, Boynton JE and Gillham NW (1993) Molecular genetics of chloroplast ribosomes in Chlamydomonas reinhardtii. In: Nierhaus KH, Fraceschi F, Subramanian AR, Erdmann VA and Wittmann-Liebold (eds) The Translational Apparatus, pp 545–554. Plenum, New York
Hauser CR, Gillham NW and 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
Hauser CR, Gillham NW and Boynton JE (1998) Regulation of chloroplast translation. In: Rochaix J-D, Goldschmidt-Clermont M and Merchant S (eds) Molecular Biology of Chlamydomonas: Chloroplasts and Mitochondria. Kluwer Academic Publishers, Dordrecht
Hayes R, Kudla J, Schuster G, Gabay L, Maliga P and Gruissem W (1996) Chloroplast mRNA 3′-end processing by a high molecular weight protein complex is regulated by nuclear encoded RNA binding proteins. EMBO J 15: 1132–1141
Herrin DL, Chen YF and Schmidt GW (1990) RNA splicing in Chlamydomonas chloroplasts. Self-splicing of 23 S preRNA. J Biol Chem 265: 21134–21140
Herrin DL and Bao Y, Thompson AJ and Chen YF (1991) Self-splicing of the Chlamydomonas chloroplast psbA introns. Plant Cell 3: 1095–1107
Hirose T and 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, Kusumegi T and 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
Hotchkiss TL and Hollingsworth MJ (1995) Factors in a chloroplast extract specifically bind to the 5′ untranslated regions of chloroplast mRNAs. Nucleic Acids Symp Ser 33: 207–208
Hotchkiss TL and Hollingsworth MJ (1999) ATP synthase 5′ untranslated regions are specifically bound by chloroplast polypeptides. Curr Genet 35: 512–520
Inamine G, Nash B, Weissbach H and Brot N (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
Jackson RJ (1996) A comparative view of initiation site selection mechanisms. In: Hershey JWB, Matthews MB and Sonenberg N (eds) Translational Control, pp71–112. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
Keller M, Chan RL, Tessier LH, Weil JH and Imbault P (1991) Post-transcriptional regulation by light of the biosynthesis of Euglena ribulose-1, 5-bisphosphate carboxylase/oxygenase small subunit. Plant Mol Biol 17: 73–82
Kenan DJ, Query CC and Keene JD (1991) RNA recog-nition: Towards identifying determinants of specificity. Trends Biochem Sci 16: 214–220
Kim J and 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
Kim J and Mayfield SP (1997) Protein disulfide isomerase as a regulator of chloroplast translational activation. Science 278: 1954–1957
Kim J, Klein PG and Mullet JE (1994) Vir-115 gene product is required to stabilize D1 translation intermediates in chloroplasts. Plant Mol Biol 25: 459–467
Kim M, Christopher DA and Mullet JE (1993) Direct evidence for selective modulation of psbA, rpoA, rbcL and 16S RNA stability during barley chloroplast development. Plant Mol Biol 22: 447–463
Kim M, Thum KE, Morishige DT and Mullet JE (1999) Detailed architecture of the barley chloroplast psbD–psbC blue light-responsive promoter. J Biol Chem 274: 4684–4692
Klaff P and Gruissem W (1991) Changes in chloroplast mRNA stability during leaf development. Plant Cell 3: 517–529
Klaff P and Gruissem W (1995) A 43 kD light-regulated chloroplast RNA-binding protein interacts with the psbA non-translated leader RNA. Photosynth Res 46: 235–248
Klein RR and Mullet JE (1986) Regulation of chloroplast-encoded chlorophyll-binding protein translation during higher plant chloroplast biogenesis. J Biol Chem 261: 11138–11145
Koo JS and 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
Kozak M (1992) Regulation of translation in eukaryotic systems. Annu Rev Cell Biol 8: 197–225
Kozak M (1999) Initiation of translation in prokaryotes and eukaryotes. Gene 234: 187–208
Kuchka MR, Mayfield SP and 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
Kuchka MR, Goldschmidt-Clermont M, van Dillewijn J and Rochaix JD (1989) Mutations at the Chlamydomonas nuclear Nac2 locus specifically affects stability of the chloroplast psbD transcript encoding polypeptide D2 of PS II. Cell 58: 869–876
Laing W, Kruenz K and Apel K (1988) Light dependent, but phytochrome-independent, translational control of the accumulation of the P700 chlorophyll —a protein of Photosystem I in barley (Hordeum vulgare L.). Planta 176: 269–276
Lisitsky I and Schuster G (1995) Phosphorylation of a chloroplast RNA-binding protein changes its affinity to RNA. Nucleic Acids Res 23: 2506–2511
Lisitsky I, Klaff P and Schuster G (1996) Addition of destabilizing poly (A)-rich sequences to endonuclease cleavage sites during the degradation of chloroplast mRNA. Proc Natl Acad Sci USA 93: 13398–13403
Mader S and Sonenberg N (1995) Cap binding complexes and cellular growth control. Biochimie 77: 40–44
Malnoe P, Mayfield SP and Rochaix JD (1988) Comparative analysis of the biogenesis of Photosystem II in the wild-type and Y-I mutant of Chlamydomonas reinhardtii. J Cell Biol 106:609–616
Mayfield SP, Cohen A, Danon A and 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
McCarthy JEG and Gualerzi C (1990) Translational control of prokaryotic gene expression. Trends Genet 6: 78–85
McCormac DJ and Barkan A (1999) A Nuclear gene in maize required for the translation of the Chloroplast atpB/E mRNA. Plant Cell 11: 1709–1716
Memon AR, Meng B and Mullet JE (1996) RNA-binding proteins of 37/38 kDa bind specifically to the barley psbA 3′-end untranslated RNA. Plant Mol Biol 30: 1195–1205
Meurer J, Berger A and Westhoff P (1996) A nuclear mutant of Arabidopsis with impaired stability on distinct transcripts of the plastid psbB, psbD/C, ndhH and ndhC operons. Plant Cell 7: 1749–1761
Meurer J, Plucken H, Kowallik KV and Westhoff P (1998) A nuclear-encoded protein of prokaryotic origin is essential for the stability of Photosystem II in Arabidopsis thaliana. EMBO J 17: 5286–5297
Monod C, Goldschmidt-Clermont M and Rochaix, JD (1992) Accumulation of psbB RNA requires a nuclear factor in Chlamydomonas reinhardtii. Mol Gen Genet 231: 449–459
Muhlbauer SK and Eichacker LA (1998) Light-dependent formation of the photosynthetic proton gradient regulates translation elongation in chloroplasts. J Biol Chem 273: 20935–20940
Myers AM, Harris EH, Gillham NW and Boynton JE (1984) Mutations in a nuclear gene of Chlamydomonas cause the loss of two chloroplast ribosomal proteins, one synthesized in the chloroplast and the other in the cytoplasm. Curr Genet 8: 369–378
Nickelsen J, van Dillewijn J, Rahire M and Rochaix JD (1994) Determinants for stability of the chloroplast psbD RNA are locatedwithin its short leader region in Chlamydomonas reinhardtii. EMBO J 13: 3182–3191
Nickelsen J, Fleischmann M, Boudreau E, Rahire M and Rochaix JD (1999) Identification of cis-acting RNA leader elements required for chloroplast psbD gene expression in Chlamydomonas. Plant Cell 11: 957–970
Preiss T and Hentze MW (1999) From factors to mechanisms: Translation and translational control in eukaryotes. Curr Opin Genet Dev 9: 515–521
Rattanachaikunsopon P, Rosch C and Kuchka MR (1999) Cloning and characterization of the nuclear AC115 gene of Chlamydomonas reinhardtii. Plant Mol Biol 39: 1–10
Rochaix JD (1996) Post-transcriptional regulation of chloroplast gene expression in Chlamydomonas reinhardtii. Plant Mol Biol 32: 327–341
Rochaix JD, Kuchka M, Mayfield S, Schirmer-Rahire M, Girard-Bascou J and 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
Rott R, Levy H, Drager RG, Stern DB and Schuster G (1998) 3′-Processed mRNA is preferentially translated in Chlamydomonas reinhardtii chloroplasts. Mol Cell Biol 18: 4605–4611
Rott R, Liveanu V, Drager RG, Higgs D, Stern DB and Schuster G (1999) Altering the 3 UTR endonucleolytic cleavage site of a Chlamydomonas chloroplast mRNA affects 3-end maturation in vitro but not in vivo. Plant Mol Biol 40: 679–686
Ruf M and Kossel H (1988) Structure and expression of the gene coding for the alpha-subunit of DNA-dependent RNA polymerase from the chloroplast genome of Zea mays. Nucleic Acids Res 16: 5741–5754
Sakamoto W, Chen X, Kindle KL and Stern DB (1994a) 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
Sakamoto W, Chen X, Kindle KL and Stern DB (1994b) petD mRNA maturation in Chlamydomonas reinhardtii chloroplasts: Role of 5′ endonucleolytic processing. Mol Cell Biol. 14: 6180–6186
Stampacchia O, Girard-Bascou J, Zanasco JL, Zerges W, Bennoun P and Rochaix JD (1997) A nuclear-encoded function essential for translation of the chloroplast psaB mRNA in Chlamydomonas. Plant Cell 9: 773–782
Staub JM and Maliga P (1994) Translation of psbA mRNA is regulated by light via the 5′-untranslated region in tobacco plastids. Plant J 6: 547–553
Stern DB, Jones H and Gruissem W (1989) Function of plastid mRNA 3′ inverted repeats. RNA stabilization and gene-specific protein binding. J Biol Chem 264: 18742–18750
Stern DB and Kindle KL (1993) 3′ end maturation of the Chlamydomonas reinhardtii chloroplast atpB mRNA is a two-step process. Mol Cell Biol 13: 2277–2285
Stitt M, Wirtz W and Heldt HW (1980) Metabolite levels during induction in the chloroplast and extrachloroplast compartments of spinach protoplasts. Biochim Biophys Acta 593: 85–102
Sugita M and Sugiura M (1996) Regulation of gene expression in chloroplasts of higher plants. Plant Mol Biol 32: 315–326
Sugiura M, Hirose T and Sugita M (1998) Evolution and mechanism of translation in chloroplasts. Annu Rev Genet 32: 437–459
Tarun SZ and Sachs AB (1996) Association of the yeast poly(A) tail binding protein with translation initiation factor eIF-4G. EMBOJ 15: 7168–7177
Taylor WC (1989) Regulatory interactions between nuclear and plastid genomes. Annu Rev Plant Physiol Plant Mol Biol 406: 211–233
Tzareva NV, Makhno VI and Boni IV (1994) Ribosome-messenger recognition in the absence of the Shine-Dalgarno interactions. FEBS Lett 337: 189–194
Yang J and Stern DB (1997) The spinach chloroplast endoribonuclease CSP41 cleaves the 3′-untranslated region of petD mRNA primarily within its terminal stem-loop structure. J Biol Chem 272: 12874–12880
Yohn CB, Cohen A, Danon A and 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
Yohn CB, Cohen A, Danon A and 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
Yohn CB, Cohen A, Rosch C, Kuchka MR and Mayfield SP (1998b) Translation of the chloroplast psbA mRNA requires the nuclear-encoded poly(A)-binding protein, RB47. J Cell Biol 142: 435–442
Wada T, Tunoyama Y, Shiina T and Toyoshima Y (1994) In vitro analysis of light-induced transcription in the wheat psbD/C gene cluster using plastid extracts from dark-grown and short-term-illuminated seedlings. Plant Physiol 104:1259–1267
Wu HY and 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
Wulczyn FG and Kahmann R (1991) Translational stimulation: RNA sequence and structural requirements for binding of Com protein. Cell 65: 259–269
Zerges W and 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
Zerges W and 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
Zerges W, Girard-Bascou J and 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
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2001 Kluwer Academic Publishers
About this chapter
Cite this chapter
Somanchi, A., Mayfield, S.P. (2001). Regulation of Chloroplast Translation. In: Aro, EM., Andersson, B. (eds) Regulation of Photosynthesis. Advances in Photosynthesis and Respiration, vol 11. Springer, Dordrecht. https://doi.org/10.1007/0-306-48148-0_8
Download citation
DOI: https://doi.org/10.1007/0-306-48148-0_8
Publisher Name: Springer, Dordrecht
Print ISBN: 978-0-7923-6332-3
Online ISBN: 978-0-306-48148-2
eBook Packages: Springer Book Archive