The Role of Nucleus- and Chloroplast-Encoded Factors in the Synthesis of the Photosynthetic Apparatus

  • Jean-David Rochaix
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 23)

The biogenesis of the photosynthetic apparatus depends on the concerted interactions between the nucleo-cytosolic and chloroplast genetic systems. Combined genetic and biochemical approaches in Chlamydomonas and land plants revealed a surprisingly large number of nucleus-encoded factors that are required for the different post-transcriptional steps of chloroplast gene expression. These steps include RNA processing, RNA stability, splicing, translation and assembly of the chloroplast-encoded proteins into functional complexes. The genes of several of these proteins were cloned and their products characterized.


Thylakoid Membrane Chloroplast Genome Ribosome Recycling Factor Chloroplast Gene Expression Plastid Ribosome 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Akins RA and Lambowitz AM (1987) A protein required for splicing group I introns in Neurospora mitochondria is mi-tochondrial tyrosyl-tRNA synthetase or a derivative thereof. Cell 50: 331-345PubMedGoogle Scholar
  2. Allison LA (2000) The role of sigma factors in plastid transcrip-tion. Biochimie 82: 537-548PubMedGoogle Scholar
  3. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, Gadrinab C, Heller C, Jeske A, Koesema E, Meyers CC, Parker H, Pred-nis L, Ansari Y, Choy N, Deen H, Geralt M, Hazari N, Hom E, Karnes M, Mulholland C, Ndubaku R, Schmidt I, Guzman P, Aguilar-Henonin L, Schmid M, Weigel D, Carter DE, Marc-hand T, Risseeuw E, Brogden D, Zeko A, Crosby WL, Berry CC and Ecker JR (2003) Genome-wide insertional mutagen-esis of Arabidopsis thaliana. Science 301: 653-657PubMedGoogle Scholar
  4. Auchincloss AH, Zerges W, Perron K, Girard-Bascou J and 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: 953-962PubMedGoogle Scholar
  5. Baginsky S, Shteiman-Kotler A, Liveanu V, Yehudai-Resheff S, Bellaoui M, Settlage RE, Shabanowitz J, Hunt DF, Schuster G and Gruissem W (2001) Chloroplast PNPase exists as a homo-multimer enzyme complex that is distinct from the Escherichia coli degradosome. RNA 7: 1464-1475PubMedGoogle Scholar
  6. Bellafiore S, Ferris P, Naver H, Gohre V and Rochaix JD (2002) Loss of Albino3 leads to the specific depletion of the light-harvesting system. Plant Cell 14: 2303-2314PubMedGoogle Scholar
  7. Bellaoui M, Keddie JS and Gruissem W (2003) DCL is a plant-specific protein required for plastid ribosomal RNA pro-cessing and embryo development. Plant Mol Biol 53: 531-543PubMedGoogle Scholar
  8. Bennoun P and Levine RP (1967) Detecting mutants that have impaired photosynthesis by their increased level of fluores-cence. Plant Physiol 42: 1284-1287PubMedGoogle Scholar
  9. Boudreau E, Takahashi Y, Lemieux C, Turmel M and Rochaix JD (1997a) The chloroplast ycf3 and ycf4 open reading frames of Chlamydomonas reinhardtii are required for the accumu lation of the photosystem I complex. EMBO J 16: 6095-6104Google Scholar
  10. Boudreau E, Turmel M, Goldschmidt-Clermont M, Rochaix JD, Sivan S, Michaels A and Leu S (1997b) A large open reading frame (orf1995) in the chloroplast DNA of Chlamydomonas reinhardtii encodes an essential protein. Mol Gen Genet 253: 649-653Google Scholar
  11. Boudreau E, Nickelsen J, Lemaire SL, Ossenb ühl F and Rochaix J-D (2000) The Nac2 gene of Chlamydomonas encodes a chloroplast TPR-like protein involved in psbD mRNA sta-bility. EMBO J 19: 3366-3376PubMedGoogle Scholar
  12. Boynton JE and Gillham NW (1996) Chloroplast transformation in Chlamydomonas. Meth Enzymol 264: 279-296PubMedGoogle Scholar
  13. Caponigro G and Parker R (1996) mRNA turnover in yeast pro-moted by the MATalpha1 instability element. Nucleic Acids Res 24: 4304-4312PubMedGoogle Scholar
  14. Choquet Y, Goldschmidt-Clermont M, Girard-Bascou J, K ück U, Bennoun P and Rochaix JD (1988) Mutant phenotypes sup-port a trans-splicing mechanism for expression of the tripartite psaA gene in the C. reinhardtii chloroplast. Cell 52:903-913PubMedGoogle Scholar
  15. Choquet Y, Stern DB, Wostrikoff K, Kuras R, Girard-Bascou J and Wollman FA (1998) Translation of cytochrome f is au- toregulated through the 5 untranslated region of petA mRNA in Chlamydomonas chloroplasts. Proc Natl Acad Sci USA 95: 4380-4385PubMedGoogle Scholar
  16. Choquet Y, Wostrikoff K, Rimbault B, Zito F, Girard-Bascou J, Drapier D and Wollman FA (2001) Assembly-controlled regulation of chloroplast gene translation. Biochem Soc Trans 29: 421-426PubMedGoogle Scholar
  17. Choquet Y, Zito F, Wostrikoff K and Wollman FA (2003) Cy-tochrome f translation in Chlamydomonas chloroplast is au-toregulated by its carboxyl-terminal domain. Plant Cell 15: 1443-1454PubMedGoogle Scholar
  18. Cline K (1986) Import of proteins into chloroplasts. Membrane integration of a thylakoid precursor protein reconstituted in chloroplast lysates. J Biol Chem 261: 14804-14810PubMedGoogle Scholar
  19. Cline K and Henry R (1996) Import and routing of nucleus-encoded chloroplast proteins. Ann Rev Cell Devel Biol 12: 1-26Google Scholar
  20. Coffin JW, Dhillon R, Ritzel RG and Nargang FE (1997) The Neurospora crassa cya-5 nuclear gene encodes a protein with a region of homology to the Saccharomyces cerevisiae PET309 protein and is required in a post-transcriptional step for the expression of the mitochondrially encoded COXI protein. Curr Genet 32: 273-280PubMedGoogle Scholar
  21. Danon A and Mayfield SP (1991) Light regulated translational activators: identification of chloroplast gene specific mRNA binding proteins. EMBO J 10: 3993-4001PubMedGoogle Scholar
  22. Danon A and Mayfield SP (1994a) Light-regulated translation of chloroplast messenger RNAs through redox potential. Science 266: 1717-1719Google Scholar
  23. Danon A and Mayfield SP (1994b) ADP-dependent phosphory-lation regulates RNA-binding in vitro: implications in light-modulated translation. EMBO J 13: 2227-2235Google Scholar
  24. Das AK, Cohen PW and Barford D (1998) The structure of the tetratricopeptide repeats of protein phosphatase 5: implica-tions for TPR-mediated protein-protein interactions. EMBO J 17: 1192-1199PubMedGoogle Scholar
  25. Dauvillee D, Stampacchia O, Girard-Bascou J and Rochaix JD (2003) Tab2 is a novel conserved RNA binding protein required for translation of the chloroplast psaB mRNA. EMBO J 22: 6378-6388PubMedGoogle Scholar
  26. Deng XW and Gruissem W (1987) Control of plastid gene ex-pression during development: the limited role of transcrip-tional regulation. Cell 49:379-387PubMedGoogle Scholar
  27. Deshpande NN, Bao Y and Herrin DL (1997) Evidence for light/redox-regulated splicing of psbA pre-RNAs in Chlamy-domonas chloroplasts. RNA 3: 37-48PubMedGoogle Scholar
  28. Drager RG, Girard-Bascou J, Choquet Y, Kindle KL and Stern DB (1998) In vivo evidence for 5 ->3 exoribonuclease degra-dation of an unstable chloroplast mRNA. Plant J 13: 85-96PubMedGoogle Scholar
  29. Drapier D, Girard-Bascou J and Wollman FA (1992) Evidence for nuclear control of the expression of the atpA and atpB chloroplast genes in Chlamydomonas. Plant Cell 4: 283-295PubMedGoogle Scholar
  30. Drescher A, Ruf S, Calsa T, Jr., Carrer H and Bock R (2000) The two largest chloroplast genome-encoded open reading frames of higher plants are essential genes. Plant J 22: 97-104PubMedGoogle Scholar
  31. Durrenberger F and Rochaix JD (1991) Chloroplast ribosomal intron of Chlamydomonas reinhardtii: in vitro self-splicing, DNA endonuclease activity and in vivo mobility. EMBO J 10: 3495-3501PubMedGoogle Scholar
  32. Edwards TA, Pyle SE, Wharton RP and Aggarwal AK (2001) Structure of Pumilio reveals similarity between RNA and pep-tide binding motifs. Cell 105:281-289PubMedGoogle Scholar
  33. Fargo DC, Boynton JE and Gillham NW (2001) Chloroplast ri-bosomal protein S7 of Chlamydomonas binds to chloroplast mRNA leader sequences and may be involved in translation initiation. Plant Cell 13: 207-218PubMedGoogle Scholar
  34. Felder S, Meierhoff K, Sane AP, Meurer J, Driemel C, Plucken H, Klaff P, Stein B, Bechtold N and Westhoff P (2001) The nucleus-encoded HCF107 gene of Arabidopsis provides a link between intercistronic RNA processing and the accumula-tion of translation-competent psbH transcripts in chloroplasts. Plant Cell 13: 2127-2141PubMedGoogle Scholar
  35. 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: 2621-2630PubMedGoogle Scholar
  36. Gamble PE and Mullet JE (1989) Translation and stability of pro-teins encoded by the plastid psbA and psbB genes are regulated by a nuclear gene during light-induced chloroplast development in barley. J Biol Chem 264:7236-7243PubMedGoogle Scholar
  37. Girard J, Chua NH, Bennoun P, Schmidt G and Delosme M (1980) Studies on mutants deficient in the photosystem I reaction centers in Chlamydomonas reinhardtii. Curr Genet 2: 215-221Google Scholar
  38. Girard-Bascou J, Choquet Y, Schneider M, Delosme M and Dron M (1987) Characterization of a chloroplast mutation in the psaA2 gene of Chlamydomonas reinhardtii. Curr Genet 12: 489-495PubMedGoogle Scholar
  39. Girard-Bascou J, Pierre Y and Drapier D (1992) A nuclear mu-tation affects the synthesis of the chloroplast psbA gene pro-duction Chlamydomonas reinhardtii. Curr Genet 22:47-52PubMedGoogle Scholar
  40. Girard-Bascou J, Choquet Y, Gumpel N, Culler D, Purton S, Merchant S, Laquerri ère F and Wollman FA (1995) In: Mathis P (ed) Photosynthesis: From Light to the Biosphere, pp 683-686. Kluwer, Dordrecht, The NetherlandsGoogle Scholar
  41. Gold L (1988) Posttranscriptional regulatory mechanisms in Es-cherichia coli. Annu Rev Biochem 57: 199-233PubMedGoogle Scholar
  42. Goldschmidt-Clermont M (1991) Transgenic expression of aminoglycoside adenine transferase in the chloroplast: a selectable marker of site-directed transformation of Chlamy-domonas. Nucleic Acids Res 19: 4083-4089PubMedGoogle Scholar
  43. Goldschmidt-Clermont M, Girard-Bascou J, Choquet Y and Rochaix JD (1990) Trans-splicing mutants of Chlamydomonas reinhardtii. Mol Gen Genet 223: 417-425PubMedGoogle Scholar
  44. Goldschmidt-Clermont M, Choquet Y, Girard-Bascou J, Michel F, Schirmer-Rahire M and Rochaix JD (1991) A small chloro-plast RNA may be required for trans-splicing in Chlamy-domonas reinhardtii. Cell 65: 135-143PubMedGoogle Scholar
  45. Groves MR, Hanlon N, Turowski P, Hemmings BA and Barford D (1999) The structure of the protein phosphatase 2A PR65/A subunit reveals the conformation of its 15 tandemly repeated HEAT motifs. Cell 96: 99-110PubMedGoogle Scholar
  46. Grunberg-Manago M (1999) Messenger RNA stability and its role in control of gene expression in bacteria and phages. Annu Rev Genet 33: 193-227PubMedGoogle Scholar
  47. 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: 921-932PubMedGoogle Scholar
  48. Hajdukiewicz PT, Allison LA and Maliga P (1997) The two RNA polymerases encoded by the nuclear and the plastid compart-ments transcribe distinct groups of genes in tobacco plastids. EMBO J 16: 4041-4048PubMedGoogle Scholar
  49. Harris EH (1989) The Chlamydomonas Source Book: a Com-prehensive Guide to Biology and Laboratory Use. Academic Press, San DiegoGoogle Scholar
  50. Hashimoto M, Endo T, Peltier G, Tasaka M and Shikanai T (2003) A nucleus-encoded factor, CRR2, is essential for the expres-sion of chloroplast ndhB in Arabidopsis. Plant J 36: 541-549PubMedGoogle Scholar
  51. Herbert CJ, Labouesse M, Dujardin G and Slonimski PP (1988) The NAM2 proteins from S. cerevisiae and S. douglasii are mitochondrial leucyl-tRNA synthetases, and are involved in mRNA splicing. EMBO J 7: 473-483PubMedGoogle Scholar
  52. Herrin DL, Chen YF and Schmidt GW (1990) RNA splicing in Chlamydomonas chloroplasts. Self-splicing of 23 S preRNA. J Biol Chem 265: 21134-21140PubMedGoogle Scholar
  53. Herrin DL, Bao Y, Thompson AJ and Chen YF (1991) Self-splicing of the Chlamydomonas chloroplast psbA introns. Plant Cell 3: 1095-1107PubMedGoogle Scholar
  54. Hoober JK, Boyd CO and Paavola LG (1991) Origin of thylakoid membranes in Chlamydomonas reinhardtii y-1 at 38C. Plant Physiol 96: 1321-1328PubMedGoogle Scholar
  55. Howe G and Merchant S (1993) Maturation of thylakoid lumen proteins proceeds post-translationally through an intermediate in vivo. Proc Natl Acad Sci USA 90: 1862-1866PubMedGoogle Scholar
  56. Huber AH, Nelson WJ and Weis WI (1997) Three-dimensional structure of the armadillo repeat region of beta-catenin. Cell 90: 871-882PubMedGoogle Scholar
  57. Hugueney P, Bouvier F, Badillo A, d’Harlingue A, Kuntz M and Camara B (1995) Identification of a plastid protein involved in vesicle fusion and/or membrane protein translocation. Proc Natl Acad Sci USA 92: 5630-5634PubMedGoogle Scholar
  58. Jenkins BD and Barkan A (2001) Recruitment of a peptidyl-tRNA hydrolase as a facilitator of group II intron splicing in chloroplasts. EMBO J 20:872-879PubMedGoogle Scholar
  59. Jenkins BD, Kulhanek DJ and Barkan A (1997) Nuclear mu-tations that block group II RNA splicing in maize chloro-plasts reveal several intron classes with distinct requirements for splicing factors. Plant Cell 9: 283-296PubMedGoogle Scholar
  60. Keddie JS, Carroll B, Jones JD and Gruissem W (1996) The DCL gene of tomato is required for chloroplast development and palisade cell morphogenesis in leaves. EMBO J 15: 4208-4217PubMedGoogle Scholar
  61. Kim J and Mayfield SP (1997) Protein disulfide isomerase as a regulator of chloroplast translational activation. Science 278: 1954-1957PubMedGoogle Scholar
  62. Kim J, Klein PG and Mullet JE (1991) Ribosomes pause at spe-cific sites during synthesis of membrane-bound chloroplast reaction center protein D1. J Biol Chem 266: 14931-14938PubMedGoogle Scholar
  63. Kim J, Mullet JE and Klein PG (1994) Ribosome-binding sites on chloroplast rbcL and psbA mRNAs and light-induced initiation of D1 translation. Plant Mol Biol 25: 437-448PubMedGoogle Scholar
  64. Krause K, Maier RM, Kofer W, Krupinska K and Herrmann RG (2000) Disruption of plastid-encoded RNA polymerase genes in tobacco: expression of only a distinct set of genes is not based on selective transcription of the plastid chromosome. Mol Gen Genet 263: 1022-1030PubMedGoogle Scholar
  65. Kroll D, Meierhoff K, Bechtold N, Kinoshita M, Westphal S, Vothknecht UC, Soll J and Westhoff P (2001) VIPP1, a nuclear gene of Arabidopsis thaliana essential for thylakoid membrane formation. Proc Natl Acad Sci USA 98: 4238-4242PubMedGoogle Scholar
  66. Kuchka M, Mayfield SP and Rochaix JD (1988) Nuclear mu-tations specifically affect the synthesis and/or degradation of the chloroplast encoded D2 polypeptide of photosystem II in Chlamydomonas reinhardtii. EMBO J 7: 319-324PubMedGoogle Scholar
  67. Kuchka MR, Goldschmidt-Clermont M, van Dillewijn J and Rochaix JD (1989) Mutation at the Chlamydomonas nu-clear NAC2 locus specifically affects stability of the chloro-plast psbD transcript encoding polypeptide D2 of PS II. Cell 58:869-876PubMedGoogle Scholar
  68. K ück U, Choquet Y, Schneider M, Dron M and Bennoun P (1987) Structural and transcriptional analysis of two homolo-gous genes for the P700 chlorophyll a-apoproteins in Chlamy-domonas reinhardtii: evidence for in vivo trans splicing. EMBO J 6:2185-2195Google Scholar
  69. Kuhn A, Stuart R, Henry R and Dalbey RE (2003) The Alb3/Oxa1/YidC protein family: membrane-localized chap-erones facilitating membrane protein insertion? Trends Cell Biol 13: 510-516PubMedGoogle Scholar
  70. Legen J, Kemp S, Krause K, Profanter B, Herrmann RG and Maier RM (2002) Comparative analysis of plastid transcrip-tion profiles of entire plastid chromosomes from tobacco attributed to wild-type and PEP-deficient transcription ma-chineries. Plant J 31: 171-188PubMedGoogle Scholar
  71. Lerbs-Mache S (1993) The 110-kDa polypeptide of spinach plas-tid DNA-dependent RNA polymerase: single-subunit enzyme or catalytic core of multimeric enzyme complexes? Proc Natl Acad Sci USA 90: 5509-5513PubMedGoogle Scholar
  72. Levine RP (1960) Genetic control of photosynthesis in Chlamy-domonas reinhardtii. Proc Natl Acad Sci USA 46: 972-977PubMedGoogle Scholar
  73. Lezhneva L and Meurer J (2004) The nuclear factor HCF145 affects chloroplast psaA-psaB-rps14 transcript abundance in Arabidopsis thaliana. Plant J 38: 740-753PubMedGoogle Scholar
  74. Lezhneva L, Amann K and Meurer J (2004) The universally con-served HCF101 protein is involved in assembly of [4Fe-4S]-cluster-containing complexes in Arabidopsis thaliana chloro-plasts. Plant J 37: 174-185PubMedGoogle Scholar
  75. Li F, Holloway SP, Lee J and Herrin DL (2002) Nuclear genes that promote splicing of group I introns in the chloroplast 23S rRNA and psbA genes in Chlamydomonas reinhardtii. Plant J 32: 467-480PubMedGoogle Scholar
  76. Li J, Goldschmidt-Clermont M and Timko MP (1993) Chloroplast-encoded chlB is required for light-independent protochlorophyllide reductase activity in Chlamydomonas reinhardtii. Plant Cell 5: 1817-1829PubMedGoogle Scholar
  77. Liere K and Link G (1997) Chloroplast endoribonuclease p54 involved in RNA 3 -end processing is regulated by phospho-rylation and redox state. Nucleic Acids Res 25: 2403-2408PubMedGoogle Scholar
  78. Liere K and Maliga P (2001) Plastid RNA polymerases in higher plants. In: Aro EM and Andersson B (eds) Regulation of Pho-tosynthesis, pp 29-49. Kluwer, Dordrecht, The NetherlandsGoogle Scholar
  79. Lisitsky I, Kotler A and Schuster G (1997) The mechanism of preferential degradation of polyadenylated RNA in the chloro-plast. The exoribonuclease 100RNP/polynucleotide phospho-rylase displays high binding affinity for poly(A) sequence. J Biol Chem 272: 17648-17653PubMedGoogle Scholar
  80. Lown FJ, Watson AT and Purton S (2001) Chlamydomonas nu-clear mutants that fail to assemble respiratory or photosyn-thetic electron transfer complexes. Biochem Soc Trans 29: 452-455PubMedGoogle Scholar
  81. Maliga P (1998) Two plastid RNA polymerases of higher plants: an evolving story. Trends Plant Sci 3: 4-6Google Scholar
  82. Malnoe P, Mayfield SP and Rochaix JD (1988) Comparative anal-ysis of the biogenesis of photosystem II in the wild- type and Y -1 mutant of Chlamydomonas reinhardtii. J Cell Biol 106: 609-616PubMedGoogle Scholar
  83. Manthey GM, Przybyla-Zawislak BD and McEwen JE (1998) The Saccharomyces cerevisiae Pet309 protein is embedded in the mitochondrial inner membrane. Eur J Biochem 255:156-161PubMedGoogle Scholar
  84. McCormac DJ and Barkan A (1999) A nuclear gene in maize required for the translation of the chloroplast atpB/E mRNA. Plant Cell 11: 1709-1716PubMedGoogle Scholar
  85. Meierhoff K, Felder S, Nakamura T, Bechtold N and Schuster G (2003) HCF152, an Arabidopsis RNA binding pentatricopep-tide repeat protein involved in the processing of chloroplast psbB-psbT-psbH-petB-petD RNAs. Plant Cell 15: 1480-1495PubMedGoogle Scholar
  86. Merendino L, Falciatore A and Rochaix JD (2003) Expression and RNA binding properties of the chloroplast ribosomal protein S1 from Chlamydomonas reinhardtii. Plant Mol Biol 53: 371-382PubMedGoogle Scholar
  87. Meurer J, Plucken H, Kowallik KV and Westhoff P (1998a) A nuclear-encoded protein of prokaryotic origin is essential for the stability of photosystem II in Arabidopsis thaliana. EMBO J 17: 5286-5297Google Scholar
  88. Meurer J, Grevelding C, Westhoff P and Reiss B (1998b) The PAC protein affects the maturation of specific chloroplast mRNAs in Arabidopsis thaliana. Mol Gen Genet 258: 342-351Google Scholar
  89. Meurer J, Lezhneva L, Amann K, Godel M, Bezhani S, Sheram-eti I and Oelmuller R (2002) A peptide chain release factor 2 affects the stability of UGA-containing transcripts in Ara-bidopsis chloroplasts. Plant Cell 14: 3255-3269PubMedGoogle Scholar
  90. Miles D (1982) The use of mutations to probe photosynthesis in higher plants. In: Edelman M, Hallick RB and Chua NH (eds) Methods in Chloroplast Molecular Biology, pp 75-107. Elsevier Biomedical Press, AmsterdamGoogle Scholar
  91. Monde RA, Zito F, Olive J, Wollman FA and Stern DB (2000) Post-transcriptional defects in tobacco chloroplast mutants lacking the cytochrome b6/f complex. Plant J 21: 61-72PubMedGoogle Scholar
  92. Monod C, Goldschmidt-Clermont M and Rochaix JD (1992) Ac-cumulation of chloroplast psbB RNA requires a nuclear factor in Chlamydomonas reinhardtii. Mol Gen Genet 231:449-459PubMedGoogle Scholar
  93. Moore M, Harrison MS, Peterson EC and Henry R (2000) Chloroplast Oxa1p homolog albino3 is required for post-translational integration of the light harvesting chlorophyll-binding protein into thylakoid membranes. J Biol Chem 275:1529-1532PubMedGoogle Scholar
  94. Morr é DJ, Selld én G, Sundquist C and Sandelius AS (1991) Stromal low temperature compartment derived from the in-ner membrane of the chloroplast envelope. Plant Physiol 97: 1558-1564Google Scholar
  95. Mullet JE (1993) Dynamic regulation of chloroplast transcrip-tion. Plant Physiol 103: 309-313PubMedGoogle Scholar
  96. Naver H, Boudreau E and Rochaix JD (2001) Functional studies of Ycf3: its role in assembly of photosystem I and interactions with some of its subunits. Plant Cell 13: 2731-2745PubMedGoogle Scholar
  97. Nickelsen J and Link G (1993) The 54-kDa RNA-binding protein from mustard chloroplasts mediates endonucleolytic transcript 3 -end formation in vitro. Plant J 3: 537-544PubMedGoogle Scholar
  98. Nickelsen J, van Dillewijn J, Rahire M and Rochaix JD (1994) Determinants for stability of the chloroplast psbD RNA are located within its short leader region in Chlamydomonas reinhardtii. EMBO J 13: 3182-3191PubMedGoogle Scholar
  99. 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: 957-970PubMedGoogle Scholar
  100. Oldenburg DJ and Bendich AJ (2003) Most chloroplast DNA of maize seedlings in linear molecules with defined ends and branched forms. J Mol Biol 335: 953-970Google Scholar
  101. Ossenbuhl F and Nickelsen J (2000) cis- and trans-acting de-terminants for translation of psbD mRNA in Chlamydomonas reinhardtii. Mol Cell Biol 20: 8134-8142PubMedGoogle Scholar
  102. Ossenbuhl F, Gohre V, Meurer J, Liszkay-Krieger A, Rochaix JD and Eichacker LA (2004) Efficient assembly of photo-system II in Chlamydomonas reinhardtii requires Alb3.1p, a homolog of Arabidopsis ALBINO3. Plant Cell 16: 1790-1800PubMedGoogle Scholar
  103. Ostheimer GJ, Williams-Carrier R, Belcher S, Osborne E, Gierke J and Barkan A (2003) Group II intron splicing factors derived by diversification of an ancient RNA-binding domain. EMBO J 22: 3919-3929PubMedGoogle Scholar
  104. Park JM, Cho JH, Kang SG, Jang HJ, Pih KT, Piao HL, Cho MJ and Hwang I (1998) A dynamin-like protein in Arabidopsis thaliana is involved in biogenesis of thylakoid membranes. EMBO J 17: 859-867PubMedGoogle Scholar
  105. Perron K, Goldschmidt-Clermont M and Rochaix JD (1999) A factor related to pseudouridine synthases is required for chloroplast group II intron trans-splicing in Chlamydomonas reinhardtii. EMBO J 18: 6481-6490PubMedGoogle Scholar
  106. Perron K, Goldschmidt-Clermont M and Rochaix JD (2004) A multiprotein complex involved in chloroplast group II intron splicing. RNA 10:704-711PubMedGoogle Scholar
  107. Purton S and Rochaix JD (1994) Complementation of a Chlamy-domonas reinhardtii mutant using a genomic cosmid library. Plant Mol Biol 24: 533-537PubMedGoogle Scholar
  108. Rattanachaikunsopon P, Rosch C and Kuchka MR (1999) Cloning and characterization of the nuclear AC115 gene of Chlamydomonas reinhardtii. Plant Mol Biol 39: 1-10PubMedGoogle Scholar
  109. Reed JE, Cline K, Stephens LC, Bacot KO and Viitanen PV (1990) Early events in the import/assembly pathway of an in-tegral thylakoid protein. Eur J Biochem 194: 33-42PubMedGoogle Scholar
  110. Ris H and Plaut W (1962) Ultrastructure of DNA-containing areas in the chloroplast of Chlamydomonas. J Cell Biol 13: 383-391PubMedGoogle Scholar
  111. Rivier C, Goldschmidt-Clermont M and Rochaix JD (2001) Iden-tification of an RNA-protein complex involved in chloroplast group II intron trans-splicing in Chlamydomonas reinhardtii. EMBO J 20: 1765-1773PubMedGoogle Scholar
  112. Rochaix JD (1996) Post-transcriptional regulation of chloroplast gene expression in Chlamydomonas reinhardtii. Plant Mol Biol 32: 327-341PubMedGoogle Scholar
  113. 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: 1013-1021PubMedGoogle Scholar
  114. Rolland N, Janosi L, Block MA, Shuda M, Teyssier E, Miege C, Cheniclet C, Carde JP, Kaji A and Joyard J (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: 5464-5469PubMedGoogle Scholar
  115. Roy LM and Barkan A (1998) A SecY homologue is required for the elaboration of the chloroplast thylakoid membrane and for normal chloroplast gene expression. J Cell Biol 141: 385-395PubMedGoogle Scholar
  116. Ruf S, K össel H and Bock R (1997) Targeted inactivation of a tobacco intron-containing open reading frame reveals a novel chloroplast-encoded photosystem I-related gene. J Cell Biol 139: 95-102PubMedGoogle Scholar
  117. Schuster G, Lisitsky I and Klaff P (1999) Polyadenylation and degradation of mRNA in the chloroplast. Plant Physiol 120: 937-944PubMedGoogle Scholar
  118. Sieburth LE, Berry-Lowe S and Schmidt GW (1991) Chloroplast RNA stability in Chlamydomonas: rapid degradation of psbB and psbC transcripts in two nuclear mutants. Plant Cell 3: 175-189PubMedGoogle Scholar
  119. Small ID and Peeters N (2000) The PPR motif-a TPR-related motif prevalent in plant organellar proteins. Trends Biochem Sci 25: 46-47PubMedGoogle Scholar
  120. Smeekens S, Bauerle C, Hageman J, Keegstra K and Weisbeek P (1986) The role of the transit peptide in the routing of pre-cursors toward different chloroplast compartments. Cell 46: 365-375PubMedGoogle Scholar
  121. Stampacchia O, Girard-Bascou J, Zanasco JL, Zerges W, Ben-noun P and Rochaix JD (1997) A nuclear-encoded function essential for translation of the chloroplast psaB mRNA in Chlamydomonas. Plant Cell 9: 773-782PubMedGoogle Scholar
  122. Stern DB, Hanson MR and Barkan A (2004) Genetics and ge-nomics of chloroplast biogenesis: maize as a model system. Trends Plant Sci 9: 293-301PubMedGoogle Scholar
  123. Sugiura M (1992) The chloroplast genome. Plant Mol Biol 19: 149-168PubMedGoogle Scholar
  124. Sundberg E, Slagter JG, Fridborg I, Cleary SP, Robinson C and Coupland G (1997) ALBINO3, an Arabidopsis nuclear gene essential for chloroplast differentiation, encodes a chloroplast protein that shows homology to proteins present in bacterial membranes and yeast mitochondria. Plant Cell 9: 717-730PubMedGoogle Scholar
  125. Swiatek M, Kuras R, Sokolenko A, Higgs D, Olive J, Cinque G, Muller B, Eichacker LA, Stern DB, Bassi R, Herrmann RG and Wollman FA (2001) The chloroplast gene ycf9 en-codes a photosystem II (PSII) core subunit, PsbZ, that partici-pates in PSII supramolecular architecture. Plant Cell 13:1347-1367PubMedGoogle Scholar
  126. Tam LW and Lefebvre PA (1995) Insertional mutagenesis and isolation of tagged genes in Chlamydomonas. Meth Cell Biol 47: 519-523Google Scholar
  127. Till B, Schmitz-Linneweber C, Williams-Carrier R and Barkan A (2001) CRS1 is a novel group II intron splicing factor that was derived from a domain of ancient origin. RNA 7: 1227-1238PubMedGoogle Scholar
  128. Trebitsh T, Levitan A, Sofer A and Danon A (2000) Translation of chloroplast psbA mRNA is modulated in the light by coun-teracting oxidizing and reducing activities. Mol Cell Biol 20: 1116-1123PubMedGoogle Scholar
  129. Trebitsh T, Meiri E, Ostersetzer O, Adam Z and Danon A (2001) The protein disulfide isomerase-like RB60 is partitioned be-tween stroma and thylakoids in Chlamydomonas reinhardtii chloroplasts. J Biol Chem 276: 4564-4569PubMedGoogle Scholar
  130. Vaistij FE, Goldschmidt-Clermont M, Wostrikoff K and Rochaix JD (2000a) Stability determinants in the chloroplast psbB/T /H mRNAs of Chlamydomonas reinhardtii. Plant J 21:469-482Google Scholar
  131. Vaistij FE, Boudreau E, Lemaire SD, Goldschmidt-Clermont M and Rochaix JD (2000b) Characterization of Mbb1, a nucleus-encoded tetratricopeptide-like repeat protein required for ex-pression of the chloroplast psbB/psbT/psbH gene cluster in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 97: 14813-14818Google Scholar
  132. Westphal S, Soll J and Vothknecht UC (2001) A vesicle transport system inside chloroplasts. FEBS Lett 506: 257-261PubMedGoogle Scholar
  133. Wilde A, Hartel H, Hubschmann T, Hoffmann P, Shestakov SV and Borner T (1995) Inactivation of a Synechocystis sp strain PCC 6803 gene with homology to conserved chloro-plast open reading frame 184 increases the photosystem II-to-photosystem I ratio. Plant Cell 7: 649-658PubMedGoogle Scholar
  134. Williams PM and Barkan A (2003) A chloroplast-localized PPR protein required for plastid ribosome accumulation. Plant J 36: 675-686PubMedGoogle Scholar
  135. Wostrikoff K, Choquet Y, Wollman FA and Girard-Bascou J (2001) TCA1, a single nuclear-encoded translational activa-tor specific for petA mRNA in Chlamydomonas reinhardtii chloroplast. Genetics 159: 119-132PubMedGoogle Scholar
  136. Wostrikoff K, Girard-Bascou J, Wollman FA and Choquet Y (2004) Biogenesis of PSI involves a cascade of translational autoregulation in the chloroplast of Chlamydomonas. EMBO J 23: 2696-2705PubMedGoogle Scholar
  137. Xie Z and Merchant S (1996) The plastid-encoded ccsA gene is required for heme attachment to chloroplast c-type cy-tochromes. J Biol Chem 271:4632-4639PubMedGoogle Scholar
  138. Yamaguchi K and 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: 28466-28482PubMedGoogle Scholar
  139. Yamaguchi K and Subramanian AR (2003) Proteomic identifi-cation of all plastid-specific ribosomal proteins in higher plant chloroplast 30S ribosomal subunit. Eur J Biochem 270: 190-205PubMedGoogle Scholar
  140. Yamaguchi K, Prieto S, Beligni MV, Haynes PA, McDon-ald WH, Yates JR, 3rd and Mayfield SP (2002) Proteomic characterization of the small subunit of Chlamydomonas rein-hardtii chloroplast ribosome: identification of a novel S1 domain-containing protein and unusually large orthologs ofbacterial S2, S3, and S5. Plant Cell 14: 2957-2974PubMedGoogle Scholar
  141. Yamaguchi K, Beligni MV, Prieto S, Haynes PA, McDonald WH, Yates JR, 3rd and Mayfield SP (2003) Proteomic characteriza-tion of the Chlamydomonas reinhardtii chloroplast ribosome; identification of proteins unique to the 70S ribosome. J Biol Chem 278: 33774-33785PubMedGoogle Scholar
  142. Yamazaki H, Tasaka M and Shikanai T (2004) PPR motifs of the nucleus-encoded factor, PGR3, function in the selective and distinct steps of chloroplast gene expression in Arabidopsis. Plant J 38: 152-163PubMedGoogle Scholar
  143. Yang J and Stern DB (1997) The spinach chloroplast endonucle-ase CSP41cleaves the 3 untranslated region of petD mRNA primarily within its 3 stem loop structure. J Biol Chem 272: 12784-12880Google Scholar
  144. Yang J, Schuster G and Stern DB (1996) CSP41, a sequence-specific chloroplast mRNA binding protein, is an endoribonu-clease. Plant Cell 8:1409-1420PubMedGoogle Scholar
  145. Yehudai-Resheff S, Hirsh M and Schuster G (2001) Polynu-cleotide phosphorylase functions as both an exonuclease and a poly(A) polymerase in spinach chloroplasts. Mol Cell Biol 21: 5408-5416PubMedGoogle Scholar
  146. 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: 2238-2243Google Scholar
  147. 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: 435-442Google Scholar
  148. Zerges W and Rochaix JD (1994) The 5 leader of a chloro-plast mRNA mediates the translational requirements for two nucleus-encoded functions in Chlamydomonas reinhardtii. Mol Cell Biol 14: 5268-5277PubMedGoogle Scholar
  149. 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: 101-110PubMedGoogle Scholar
  150. 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: 3440-3448PubMedGoogle Scholar
  151. Zhang H, Herman PL and Weeks DP (1994) Gene isolation through genomic complementation using an indexed library of Chlamydomonas reinhardtii DNA. Plant Mol Biol 24:663-672PubMedGoogle Scholar

Copyright information

© Springer 2007

Authors and Affiliations

  • Jean-David Rochaix
    • 1
  1. 1.Departments of Molecular Biology and Plant BiologyUniversity of GenevaSwitzerland

Personalised recommendations