Skip to main content
Log in

Post-transcriptional regulation of chloroplast gene expression in Chlamydomonas reinhardtii

  • Organelle
  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

The biosynthesis of the photosynthetic apparatus depends on the concerted action of the nuclear and chloroplast enetic systems. Numerous nuclear and chloroplast mutants of Chlamydomonas deficient in photosynthetic activity have been isolated and characterized. While several of these mutations alter the genes of components of the photosynthetic complexes, a large number of the mutations affect the expression of chloroplast genes involved in photosynthesis. Most of these mutations are nuclear and only affect the expression of a single chloroplast gene. The mutations examined appear to act principally at post-transcriptional steps such as RNA stability, RNA processing, cis- and trans-splicing and translation. Directed chloroplast DNA surgery through biolistic transformation has provided a powerful tool for identifying important cis elements involved in chloroplast gene expression. Insertion of chimeric genes consisting of chloroplast regulatory regions fused to reporter genes into the chloroplast genome has led to the identification of target sites of the nuclear-encoded functions affected in some of the mutants. Biochemical studies have identified a set of RNA-binding proteins that interact with the 5′-untranslated regions of plastid mRNAs. The binding activity of some of these factors appears to be modulated by light and by the growth conditions.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Bennoun P, Masson A, Delosme N: A method for complementation analysis of nuclear and chloroplast mutants of photosynthesis in Chlamydomonas. Genetics 95: 39–47 (1980).

    Google Scholar 

  2. Blowers A, Klein U, Ellmore GS, Bogorad L: Functional in vivo analysis of the 3′ flanking sequences of the Chlamydomonas chloroplast rbcL and psaB genes. Mol Gen Genet 238: 339–349 (1993).

    Google Scholar 

  3. Boynton JE, Gillham NW, Harris EH, Hosler JP, Johnson AR, Jones BL, Randolph-Anderson D, Robertson TM, Klein KB, Shark B, Sanford JC: Chloroplast transformation in Chlamydomonas with high velocity microprojectiles. Science 240: 1534–1538 (1988).

    Google Scholar 

  4. Buchanan BB: 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 (1991).

    Google Scholar 

  5. Chen X, Kindle KL, Stern DB: Initiation codon mutations in the Chlamydomonas chloroplast petD gene result in temperature-sensitive photosynthetic growth. EMBO J 12: 3627–3635 (1993).

    Google Scholar 

  6. Chen X, Kindle KL, Stern DB: The initiation codon determines the efficiency but not the site of translation initiation in Chlamydomonas chloroplasts. Plant Cell 7: 1295–1315 (1995).

    Google Scholar 

  7. Choquet Y, Goldschmidt-Clermont M, Girard-Bascou H, Kuck U, Bennoun P et al.: Mutant phenotypes support a trans-splicing mechanism for the expression of the tripartite psaA gene in the C. reinhardtii chloroplast. Cell 52: 903–913 (1988).

    Google Scholar 

  8. Chua NH, Bennoun P: Thylakoid membranes polypeptides of Chlamydomonas reinhardtii: wild-type and mutant strains deficient in photosystem II reaction center. Proc Natl Acad Sci USA 72: 2175–2179 (1975).

    Google Scholar 

  9. Collins RA, Lambowitz AM: RNA splicing in Neurospora mitochondria. Defective splicing of mitochondrial mRNA precursors in the nuclear mutant cyt 18–1. J Mol Biol 184: 413–428 (1985).

    Google Scholar 

  10. Danon A, Mayfield SPY: Light-regulated translational activators: identification of chloroplast gene-specific mRNA binding proteins. EMBO J 10: 3993–4002 (1991).

    Google Scholar 

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

    Google Scholar 

  12. Danon A, Mayfield SP: Light-regulated translation of chloroplast mRNAs through redox potential. Science 266: 1717–1719 (1995).

    Google Scholar 

  13. De Vitry C, Olive J, Drapier D, Recouvreur M, Wollman F-A: Posttranslational events leading to the assembly of photosystem II protein complex: a study using photosynthesis mutants from Chlamydomonas reinhardtii. J Cell Biol 109: 991–1006 (1989).

    Google Scholar 

  14. Debuchy R, Purton S, Rochaix J-D: The argininosuccinate lyase gene of Chlamydomonas reinhardtii: an important tool for nuclear transformation and for correlating the genetic and molecular maps of the ARG7 locus. EMBO J 8: 2803–2809 (1989).

    Google Scholar 

  15. Delepelaire P: Partial characterization of the biosynthesis and integration of the photosystem II reaction centers in the thylakoid membrane of Chlamydomonas reinhardtii. EMBO J 3: 701–706 (1984).

    Google Scholar 

  16. Deshpande NN, Hollingsworth M, Herrin DL: The atpF group II intron-containing gene from spinach chloroplasts is not spliced in transgenic Chlamydomonas chloroplasts. Curr Genet 28: 122–127 (1995).

    Google Scholar 

  17. Drapier D, Girard-Bascou J, Wollman FA: Evidence for a nuclear control on the expression of the atpA and atpB chloroplast genes in Chlamydomonas reinhardtii. Plant Cell 4: 283–295 (1992).

    Google Scholar 

  18. Dron M, Rahire M, Rochaix J-D: Sequence of the 16SrRNA gene and its surounding regions of Chlamydomonas reinhardtii. Nucl Acids Res 10: 7609–7620 (1982).

    Google Scholar 

  19. Dürrenberger F, Rochaix J-D: Chloroplast ribosomal intron of Chlamydomonas reinhardtii: in vitro self-splicing, DNA endonuclease activity and in vivo mobility. EMBO J 10: 3495–3501 (1991).

    Google Scholar 

  20. Erickson JM, Rahire M, Malnoe P, Girard-Bascou J, Pierre Y et al.: Lack of the D2 protein in a Chlamydomonas reinhardtii psbD mutant affects photosystem II stability and D1 expression. EMBO J 5: 1745–1754 (1986).

    Google Scholar 

  21. Erickson JM, Rahire M, Rochaix J-D: Chlamydomonas reinhardtii gene for the 32000 mol. wt. protein of photosystem II contains four large introns and is located entirely within the chloroplast inverted repeat. EMBO J 3: 2753–2762 (1984).

    Google Scholar 

  22. Gillham NW, Boynton JE, Hauser CR: Translational regulation of gene expression in chloroplasts and mitochondria. Annu Rev Genet 28: 71–93 (1994).

    Google Scholar 

  23. Girard-Bascou J, Choquet Y, Schneider M, Delosme M, Dron M: Characterization of a chloroplast mutation in the psaA2 gene of Chlamydomonas reinhardtii. Curr Genet 12: 489–495 (1987).

    Google Scholar 

  24. Girard-Bascou J, Pierre Y, Drapier D: A nuclear mutation affects the synthesis of the chloroplast psbA gene product in Chlamydomonas reinhardtii. Curr Genet 22: 47–52 (1992).

    Google Scholar 

  25. Gold L: Posttranscriptional regulatory mechanism in Escherichia coli. Annu Rev Biochem 57: 199–233 (1968).

    Google Scholar 

  26. Goldschmidt-Clermont M: Transgenic expression of amino-glycoside adenine transferase in the chloroplast: a selectable marker for site-directed transformation of Chlamydomonas. Nucl Acids Res 19: 4083–4090 (1991).

    Google Scholar 

  27. Goldschmidt-Clermont M, Girard-Bascou J, Choquet Y, Rochaix J-D: Trans-splicing mutants of Chlamydomonas reinhardtii. Mol Gen Genet 223: 417–425 (1990).

    Google Scholar 

  28. Goldschmidt-Clermont M, Choquet Y, Girard-Bascou H, Michel F, Schirmer-Rahire M, Rochaix J-D: A small chloroplast RNA may be required for trans-splicing in Chlamydomonas reinhardtii. Cell 65: 135–143 (1991).

    Google Scholar 

  29. Gruissem W, Schuster G: Control of mRNA degradation in organelles. In: Brawerman G, Belasco J (eds) Control of Messenger RNA Stability, pp. 329–365 Academic Press, Orlando, FL (1993).

    Google Scholar 

  30. Harris EH: The Chlamydomonas Sourcebook: A Comprehensive Guide to Biology and Laboratory Use. Academic Press, San Diego, CA (1989).

    Google Scholar 

  31. Hauser CR, Gillham NW, Boynton JE: Translational regulation of chloroplast mRNAs in Chlamydomonas reinhardtii. J Biol Chem, in press (1996).

  32. Herdenberger F, Hollander V, Kück U: Correct in vivo RNA splicing of a mitochondrial intron in algal chloroplasts. Nucl Acids Res 22: 2869–2875 (1994).

    Google Scholar 

  33. Herrin D, Michaels A: The chloroplast 32kDa protein is synthesized on thylakoid-bound ribosomes in Chlamydomonas reinhardtii. FEBS Lett 184: 90–94 (1985).

    Google Scholar 

  34. Herrin DL, Bao Y, Thompson AJ, Chen Y-F: Self-splicing of the Chlamydomonas chloroplast psbA introns. Plant Cell 3: 1095–1107 (1991).

    Google Scholar 

  35. Herrin DL, Chen Y-F, Schmidt GW: RNA splicing in Chlamydomonas chloroplasts: self-splicing of 23S preRNA. J Biol Chem 265: 21134–21140 (1990).

    Google Scholar 

  36. Herrin DL, Schmidt GW: Trans-splicing of transcripts for the chloroplast psaA1 gene. In vivo requirement for nuclear gene products. J Biol Chem 263: 14601–14604 (1988).

    Google Scholar 

  37. Hirose T, Sugita M, Sugiura M: In vitro analysis of cis- and trans-acting regulatory elements for translation of photosynthetic gene transcription in tobacco chloroplasts. Photosynth Res Suppl 1: 153 (1995).

    Google Scholar 

  38. Hong S, Spreitzer RJ: Nuclear mutation inhibits expression of the chloroplast gene that encodes the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase. Plant Physiol 106: 673–678 (1994).

    Google Scholar 

  39. Howe G, Merchant S: The biosynthesis of membrane and soluble plastic c-type cytochromes of Chlamydomonas reinhardtii is dependent on multiple common gene products. EMBO J 11: 2789–2801 (1992).

    Google Scholar 

  40. Howe G, Mets L, Merchant S: Biosynthesis of cytochrome f in Chlamydomonas reinhardtii: analysis of the pathway in gabaculine treated cells and in the heme attachment mutant B6. Mol Gen Genet 246: 156–165 (1995).

    Google Scholar 

  41. Ikeuchi M, Eggers B, Shen G, Webber A, Yu J, Hirano A, Inoue Y, Vermaas W: Cloning of the psbK gene from Synechocystis sp. PCC 6803 and characterization of photosystem II in mutants lacking PSII-K. J Biol Chem 266: 11111–11115 (1991).

    Google Scholar 

  42. Jensen KH, Herrin DL, Plumley FG, Schmidt GW: Biogenesis of photosystem II complexes: transcriptional translational and posttranslational regulation. J Cell Biol 103: 701–706 (1986).

    Google Scholar 

  43. Johnson CH and Schmidt GW. The psbB gene cluster of the Chlamydomonas reinhardtii chloroplast: sequence and transcriptional analyses of psbN and psbH. Plant Mol Biol 22: 645–658.

  44. Kindle KL: High frequency nuclear transformation of Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 87: 1228–1232 (1990).

    Google Scholar 

  45. Kindle KL, Schnell RA, Fernandez E, Lefebvre PA: Stable transformation of Chlamydomonas using the Chlamydomonas gene for nitrate reductase. J Cell Biol 109: 2589–2601 (1989).

    Google Scholar 

  46. Kuchka M, Goldschmidt-Clermont M, van Dillewijn J. Rochaix JD: Mutation at the Chlamydomonas nuclear NAC2 locus specifically affects stability of the chroloplast psbD transcript encoding polypeptide D2 of photosystem II in Chlamydomonas reinhardtii. Cell 58: 869–876 (1989).

    Google Scholar 

  47. Kuchka MR, Mayfield SP, Rochaix J.-D: 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 (1988).

    Google Scholar 

  48. Kück U, Choquet Y, Schneider M, Dron M, Bennoun P. Structural and transcription analysis of two homologous genes for the P700 chlorophyll a apoproteins Chlamydomonas reinhardtii: evidence for in vivo trans-splicing. EMBO J 6: 2185–2195 (1987).

    Google Scholar 

  49. Kück U, Godehart I, Schmidt U: A self-splicing group-II intron in the mitochondrial large subunit rRNA (LSUrRNA) gene of the eucaryotic alga Scenedesmus obliquus. Nucl Acids Res 18: 2691–2697 (1990).

    Google Scholar 

  50. Kuras R, Büschlen S, Wollman FA: Maturation of preapocytochrome f in vivo. J Biol Chem 270, in press (1995).

  51. Kuras R, Wollman F-A: The assembly of cytochrome b6/f complexes: An approach using genetic transformation of the green alga Chlamydomonas reinhardtii. EMBO J 13: 1019–1027 (1994).

    Google Scholar 

  52. Kuras R, Wollman FA, Joliot P: Conversion of cytochrome f to a soluble form in vivo in Chlamydomonas reinhardtii. Biochemistry 34: 7468–7475 (1995).

    Google Scholar 

  53. Lemaire C, Girard-Bascou J, Wollman F-A, Bennoun P: Studies on the cytochrome b6/f complex. I. Characterization of the complex subunits in Chlamydomonas reinhardtii. Biochim Biophys Acta 851: 229–238 (1986).

    Google Scholar 

  54. Liu X-Q, Hosler JP, Boynton JE, Gillham NW: mRNAs for two ribosomal proteins are preferentially translated in the chloroplast of Chlamydomonas reinhardtii under conditions of reduced protein synthesis. Plant Mol Biol 12: 385–394 (1989).

    Google Scholar 

  55. Malnoe P, Mayfield SP, Rochaix JD: Comparative analysis of the biogenesis of photosystem II in the wild-type and Y-1 mutant of Chlamydomonas reinhardtii. J Cell Biol 106: 609–616 (1988).

    Google Scholar 

  56. Mannan RM, Whitmarsh J, Nyman P, Pakrasi H: Directed mutagenesis of an iron-sulfur protein of the photosystem I complex in the filamentous cyanobacterium Anabaena variabilis ATCC 29413. Proc Natl Acad Sci USA 88: 10168–10172 (1991).

    Google Scholar 

  57. Mayfield SP: Chloroplast gene regulation: interaction of the nuclear and chloroplast genomes in the expression of photosynthetic proteins. Curr Opin Cell Biol 2: 509–513 (1990).

    Google Scholar 

  58. Mayfield SP, Kindle KL: Stable nuclear transformation of Chlamydomonas reinhardtii using a C. reinhardtii gene as the selectable marker. Proc Natl Acad Sci USA 87: 2087–2091 (1990).

    Google Scholar 

  59. Mayfield SP, Cohen A, Danon A, Yohn CB: 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 (1994).

    Google Scholar 

  60. Mayfield SP, Yohn CB, Cohen A, Danon A: Regulation of chloroplast gene expression. Annu Rev Plant Physiol Plant Mol Biol 46: 147–166 (1994).

    Google Scholar 

  61. Michel F, Jacquier A, Dujon B: Comparison of fungal mitochondrial introns reveals extensive homologous in RNA secondary structure. Biochimie 64: 867–881 (1982).

    Google Scholar 

  62. Michel F, Umesono K, and Ozeki H: Comparative and functional analysis of group II catalytic introns: a review. Gene 82: 5–30 (1989).

    Google Scholar 

  63. Monod C, Goldschmidt-Clermont M, Rochaix J.-D: Accumulation of chloroplast psbB RNA requires a nuclear factor in Chlamydomonas reinhardtii. Mol Gen Genet 231: 449–459 (1992).

    Google Scholar 

  64. Monod C, Takahashi Y, Goldschmidt-Clermont M, Rochaix J-D: The chloroplast ycf8 open reading frame encodes a photosystem II polypeptide which maintains photosynthetic activity under adverse growth conditions. EMBO J 13: 2747–2754 (1994).

    Google Scholar 

  65. Nickelsen J, Link G: The 54kDa RNA-binding protein from mustard chloroplasts mediates endonucleolytic transcript 3′ end formation in vitro. Plant J 3: 537–544 (1993).

    Google Scholar 

  66. Nickelsen J, Van Dillewijn J, Rahire M, Rochaix J-D: Determinants for stability of the chloroplast psbD RNA are located within its short leader region in Chlamydomonas reinhardtii. EMBO J 13: 3182–3191 (1994).

    Google Scholar 

  67. Petersen C: Translation and mRNA stability in bacteria: a complex relationship. In: Belasco JG, Brawerman G (eds) Control of Messenger RNA Stability, pp. 117–145. Academic Press, San Diego, CA (1993).

    Google Scholar 

  68. Purton S, Rochaix J-D: Complementation of a Chlamydomonas reinhardtii mutant using a genomic cosmid library. Plant Mol Biol 24: 533–537 (1994).

    Google Scholar 

  69. Robertson D, Boynton JE, Gillham NW: Cotranscription of the wild-type chloroplast atpE gene encoding the CF1/CF0 epsilon subunit with the 3′ half of the rps7 gene in Chlamydomonas reinhardtii and characterization of frameshift mutations in atpE. Mol Gen Genet 221: 155–163 (1990).

    Google Scholar 

  70. Rochaix J-D: Post-transcriptional steps in the expression of chloroplast genes. Annu Rev Cell Biol 8: 1–28 (1992).

    Google Scholar 

  71. Rochaix J-D, Rahire M, Michel F: The chloroplast ribosomal intron of Chlamydomonas reinhardtii codes for a polypeptide related to mitochondrial maturases. Nucl Acids Res 13: 975–984 (1985).

    Google Scholar 

  72. Rochaix JD, Erickson JM: Function and assembly of photosystem II: genetic and molecular analysis. Trends Biochem Sci 13: 56–59 (1988).

    Google Scholar 

  73. Rochaix J-D, Kuchka M, Mayfield S, Schirmer-Rahire M, Girard-Bascou J, Bennoun P: Nuclear and chloroplast mutations affect the synthesis or stability of the chloroplast psbC gene product in Chlamydomonas reinhardtii. EMBO J 8: 1013–1022 (1989).

    Google Scholar 

  74. Sakamoto W, Chen X, Kindle KL, Stern DB: Function of the Chlamydomonas reinhardtii petD 5′ untranslated region in regulating the accumulation of subunit IV of the cytochrome b6f complex. Plant J 6: 503–512 (1994).

    Google Scholar 

  75. Sakamoto W, Sturm NR, Kindle KL, Stern DB: petD mRNA maturation in Chlamydomonas reinhardtii chloroplasts: role of 5′ endonucleolytic processing. Mol Cell Biol 14: 6180–6186 (1994).

    Google Scholar 

  76. Sakamoto WK, Kindle KL, Stern DB: In vivo analysis of Chlamydomonas chloroplast petD gene expression using stable transformation of β-glucuronidase translational fusions. Proc Natl Acad Sci. USA 90: 497–501 (1993).

    Google Scholar 

  77. Salvador ML, Klein U, Bogard L: 5′ sequences are important positive and negative determinants of the longevity of Chlamydomonas chloroplast gene transcripts. Proc Natl Acad Sci USA 90: 1556–1560 (1993).

    Google Scholar 

  78. Salvador ML, Klein U, Bogorad L: Light-regulated and endogenous fluctuations of chloroplast transcript levels in Chlamydomonas. Regulation by transcription and RNA degradation. Plant J 3: 213–219 (1993).

    Google Scholar 

  79. Schuster G, Gruissem W: Chloroplast mRNA 3′ end processing requires a nuclear-encoded RNA binding protein. EMBO J 1: 1493–1502 (1982).

    Google Scholar 

  80. Sharp P: Five easy pieces. Science 254: 663 (1991).

    Google Scholar 

  81. Sieburth LE, Berry-Lowe S, Schmidt GW: Chloroplast RNA stability in Chlamydomonas: rapid degradation of psbB and psbC transcripts in two nuclear mutants. Plant Cell 3: 175–189 (1991).

    Google Scholar 

  82. Spreitzer RJ, Goldschmidt-Clermont M, Rahire M, Rochaix J-D: Nonsense mutations in the Chlamydomonas chloroplast gene that codes for the large subunit of ribulose carboxylase/oxygenase. Proc Natl Acad Sci USA 82: 5460–5464 (1985).

    Google Scholar 

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

    Google Scholar 

  84. Stern DB, Radwanski ER, Kindle KL: A 3′ stem/loop structure of the Chlamydomonas chloroplast atpB gene regulates mRNA accumulation in vivo. Plant Cell 3: 285–297 (1991).

    Google Scholar 

  85. Stern DB, Kindle KL. 3′ end maturation of the Chlamydomonas reinhardtii chloroplast atp mRNA is a two-step process Mol Cell Biol 13: 2277–2285 (1993).

    Google Scholar 

  86. Sturm NR, Kuras R, Büschlen S, Sakamoto W, Kindle KL, Stern DB, Wollman F-A. The petD gene is transcribed by functionally redundant promoters in Chlamydomonas reinhardtii chloroplasts. Mol Cell Biol 14: 6180–6186 (1994).

    Google Scholar 

  87. Takahashi Y, Goldschmidt-Clermont M, Soen S-Y, Franzen LG, Rochaix J-D: Directed chloroplast transformation in Chlamydomonas reinhardtii: insertional inactivation of the psaC gene encoding the iron sulfur protein destabilizes photosystem I. EMBO J 10: 2033–2040 (1991).

    Google Scholar 

  88. Takahashi Y, Matsumoto H, Goldschmidt-Clermont M, Rochaix J-D: Directed disruption of the Chlamydomonas chloroplast psbK gene destabilizes the photosystem II reaction center complex. Plant Mol Biol 24: 779–788 (1994).

    Google Scholar 

  89. Tam LW, Lefevbre PA: Cloning of flagellar genes in Chlamydomonas reinhardtii by insertional mutagenesis. Genetics 135: 375–394 (1993).

    Google Scholar 

  90. Turmel M, Choquet Y, Goldschmidt-Clermont M, Rochaix J-D, Otis C, Lemieux C: The trans-spliced intron 1 in the psaA gene of the Chlamydomonas chloroplast: a comparative analysis. Curr Genet 27: 270–279 (1995).

    Google Scholar 

  91. Wollman FA, Kuras R, Choquet Y: Epistatic effects in thylakoid protein synthesis: the example of cytochrome f. In: Proceedings 10th International Congress of Photosynthesis. Kluwer Academic Publishers, Dordrecht. in press (1995).

    Google Scholar 

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

    Google Scholar 

  93. Xu R, Bingham SE, Webber AN: Increased mRNA accumulation in psaB frame-shift mutant of Chlamydomonas reinhardtii suggests a role for translation in psaB mRNA stability. Plant Mol Biol 22: 465–474 (1993).

    Google Scholar 

  94. Zerges W, Rochaix J-D: 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 (1994).

    Google Scholar 

  95. Zhang H, Herman PL, Weeks DP: Gene isolation through genomic complementation using an indexed library of Chlamydomonas reinhardtii DNA. Plant Mol Biol 24: 663–672 (1994).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rochaix, JD. Post-transcriptional regulation of chloroplast gene expression in Chlamydomonas reinhardtii . Plant Mol Biol 32, 327–341 (1996). https://doi.org/10.1007/BF00039389

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00039389

Key words

Navigation