Abstract
The expression of three chloroplastic genes, psbA (the gene for the reaction center D1 protein of PSII), psbC (the gene for the P700 apoprotein of PSI) and psaB (the gene for the intermediate antema of PSII), and a nuclear gene, cab (the gene for the chlorophyll a/bbinding protein), has been investigated during chloroplast development in Euglena gracilis Klebs. The polysomal fraction, mRNA stability and protein turnover were analysed under different conditions of cell greening. The results indicate that the main regulatory step for the nuclear and chloroplastic genes was at the translational level when greening of cells took place on a resting medium. When cell greening took place on a medium with balanced phosphate, carbon and nitrogen sources (nutritional medium), the main regulation occurred posttranscriptionally by mobilization of the transcripts onto the polysomes. These results indicate that in E. gracilis, for a given gene, regulation operates at different levels, and that although light is the principal effector in the regulation of the genes involved in chloroplast development, the effect of metabolites should also be considered. Interestingly, it appears that these various regulation levels are similar for the chloroplastic and nucleocytoplasmic compartments.
Similar content being viewed by others
Abbreviations
- CPI:
-
chlorophyll-protein complex I of PSI
- LHCI (II):
-
light-harvesting chlorophyll a/b-binding protein of PSI (II) encoded by the nuclear cab genes
- psaB:
-
gene for the P700 apoprotein of PSI
- psbA:
-
gene for the reaction center D1 protein of PSII
- psbC:
-
gene for the intermediate antenna of PSII
Referencess
Bennett, J., Jenkins, G.I., Hartley, M.R. (1984) Differential regulation of the accumulation of the light-harvesting chlorophyll a/b complex and ribulose bisphosphate carboxylase/oxygenase in greening pea leaves. J. Cell. Biochem. 25, 1–13
Brandt, P. (1981) Evidence for regulative transactions between the nucleocytoplasm and the chloroplasts in Euglena gracilis. Ber. Deutsch. Bot. Ges. 94, 419–433
Brandt, P. (1988) Stain and stage-specific high-temperature treatment of Euglena gracilis causes permanent apochlorosis. J. Plant Physiol. 133, 281–287
Brandt, P., Wiessner, W. (1977) Different temperature optima of the DNA-dependent RNA polymerases of Euglena gracilis Z and their role for the experimental bleaching by higher temperature. Z. Pflanzenphysiol. 85, 53–60
Cannons, A.C., Merrett, M.J. (1984) Regulation of synthesis of citrate synthase in regreening Euglena gracilis. Eur. J. Biochem. 142, 597–602
Chua, N.-H. (1980) Electrophoretic analysis of chloroplast proteins. Methods Enzymol. 69, 434–446
Chua, N.-H., Blobel, G., Siekevitz, P., Palade, G.E. (1976) Periodic variations in the ratio of free to thylakoid bound chloroplast ribosomes during the cell cycle of Chlamydomonas reinhardtii. J. Cell Biol. 71, 497–514
Cushman, J.C., Price, C.A. (1986) Synthesis and turnover of proteins in proplastids and chloroplasts of Euglena gracilis. Plant Physiol. 82, 972–977
Deng, X.-W., Gruissem, W. (1987) Control of plastid gene expression during development: the limited role of transcriptional regulation. Cell. 49, 379–387
Devic, M., Schantz, R. (1984) Light-induced biosynthesis of chlorophyll-binding proteins in Euglena. Adv. Photosynth. Res. 4, 575–578
Dubertret, G., Pineau, B. (1984) Biosynthetic and ultrastructural events associated with the selective formation of system II reaction centers in Euglena mature chloroplasts. Adv. Photosynth. Res. 4, 669–672
Freyssinet, G., Heizmann, P., Verdier, G., Trabuchet, G., Nigon, V. (1972) Influence des conditions nutritionnelles sur la réponse à l'éclairement chez les Euglènes étiolées. Physiol. Veg. 10, 421–442
Gallagher, T.F., Jenkins, G.I., Ellis, R.J. (1985) Rapid modulation of transcription of nuclear genes encoding chloroplast proteins by light. FEBS Lett. 186, 241–245
Gingrich, J.C., Hallick, R.B. (1985) The Euglena gracilis chloroplast ribulose-1,5-bisophosphate carboxylase gene. II The spliced mRNA and its products. J. Biol. Chem. 260, 16162–16168
Grebanier, A.E., Coen, D.M., Rich, A., Bogorad, L. (1978) Membrane proteins synthesized but not processed by isolated maize chloroplasts. J. Cell Biol. 78, 734–746
Gruissem, W. (1989) Chloroplast gene expression: how plants turn their plastid on. Cell. 56, 161–170
Heizmann, P., Trabucher, G., Verdier, G., Freyssinet, G., Nigon, V. (1972) Influence de l'éclairement sur l'évolution des polysomes dans des cultures d'Euglena gracilis étiolées. Biochim. Biophys. Acta 277, 149–160
Hollingsworth, M., Johanningmeier, U., Karabin, G.D., Stiegler, G.I., Hallick, R.B. (1984) Detection of multiple, unspliced precursor mRNA transcripts for the Mr 32000 thylakoid membrane protein from Euglena gracilis chloroplasts. Nucl. Acids Res. 12, 2001–2017
Houlné, G., Schantz, R. (1988) Characterization of cDNA sequences for LHCI apoproteins in Euglena gracilis: the mRNA encodes a large precursor containing several consecutive divergent polypeptides. Mol. Gen. Genet. 213, 479–486
Javed, Q., Merrett, M.J. (1987) Mobilisation of NADPH-glutamate dehydrogenase mRNA in regreening cultures of Euglena gracilis. Plant Sci. 49, 31–36
Klaff, P., Gruissem, W. (1991) Changes in chloroplast mRNA stability during leaf development. Plant Cell. 3, 517–529
Klein, R.R., Masson, H.S., Mullet, J.E. (1988) Light-regulated translation of chloroplast proteins. Transcripts of psA, psaB, psbA and RbcL are associated with polysomes in dark-grown and illuminated barley seedlings. J. Cell Biol. 106, 289–301
Krauspe, R., Scheer, A., Schaper, S., Bohley, P. (1986) Proteolysis in Euglena gracilis: II. Soluble and particle-bound acidic proteinase activities of the cysteine and aspartic types during growth and chloroplast development. Planta 167, 482–490
Krauspe, R., Lerbs, S., Parthier, B., Wollgiehn, R. (1987) Light induction or translatable mRNA for chloroplastic leucyl- and valyl-tRNA synthetases of Euglena gracilis. J. Plant Physiol. 130 327–342
Mullet, J.E. (1988) Chloroplast development and gene expression. Annu. Rev. Plant Physiol. 39, 475–502
Mullet, J.E., Klein, R.R. (1987) Transcription and RNA stability are important determinants of higher plant chloroplast RNA levels. EMBO J. 6, 1571–1579
Murphy, D.J. (1986) The molecular organization of the photosynthetic membranes of higher plants. Biochim. Biophys. Acta 864, 33–94
Ortiz, W. (1990) Protein synthesis during the initial phase of the temperature-induced bleaching response in Euglena gracilis. Plant Physiol. 93, 141–147
Ortiz, W., Reardon, E.M., Price, C.A. (1980) Preparation of chloroplasts from Euglena highly active in protein synthesis. Plant Physiol. 66, 291–294
Ortiz, W., Wilson, C.J. (1988) Induced changes in chloroplast protein accumulation during heat bleaching in Euglena gracilis. Plant Physiol. 86, 554–561
Reinbothe, S., Parthier, B. (1990) Translational regulation of plastid gene in Euglena gracilis. FEBS Lett. 265, 7–11
Rikin, A., Schwartzbach, S.D. (1988) Extremely large and slowly processed precursors to the Euglena light-harvesting chlorophyll a/b binding proteins of photosystem II. Proc. Natl. Acad. Sci. USA 85, 5117–5121
Rodermel, S.T., Bogorad, L. (1985) Maize plastid photogenes: mapping and photoregulation of transcript levels during lightinduced development. J. Cell Biol. 100, 463–476
Schantz, R., Blee, E., Chammai, A., Wolff, B. (1981) Origin and biosynthesis of some chloroplast specific components in Euglena gracilis. Z. Ber. Deutsch. Bot. Ges. 94, 449–461
Schantz, R. (1985) Mapping of the chloroplast genes for the chlorophyll a-binding proteins in Euglena gracilis. Plant Sci. 40, 43–49
Schwartzbach, S.D. (1990) Photocontrol of organelle biogenesis in Euglena. Photochem. Photobiol. 51, 231–254
Schwartzbach, S.D., Schiff, J.A. (1979) Events surrounding the early development of Euglena chloroplasts 17. Photocontrol of protein synthesis. Plant Cell Physiol. 20, 827–838
Skadsen, R.W., Scandalios, J.G. (1987) Translational control of photo-induced expression of the Cat2 catalase gene during leaf development in maize. Proc. Natl. Acad. Sci. USA 84, 2785–2789
Tobin, E.M., Silverthorne, J. (1985) Light regulation of gene expression in higher plants. Annu. Rev. Plant Physiol. 36, 569–593
Walter, P., Blobel, G. (1981a) Translocation of proteins across the endoplasmic reticulum 2. Signal recognition protein mediates the selective binding to microsomal membranes of in vitro assembled polysomes synthesizing secretory protein. J. Cell Biol. 91, 551–556
Walter, P., Blobel, G. (1981b) Translocation of proteins across the endoplasmic reticulum 3. Signal recognition protein causes signal sequence dependent and site specific arrest of chain elongation that is released by microsomal membranes. J. Cell Biol. 91, 557–561
Walter, P., Ibrahimi, I., Blobel, G. (1981) Translocation of proteins across the endoplasmic reticulum 1. Signal recognition protein binds to in vitro assembled polysomes synthesizing secretory protein. J. Cell Biol. 91, 545–550
Weiss, C., Houlné, G., Schantz, M.-L., Schantz, R. (1988) Photoregulation of the synthesis of chloroplast membrane proteins in Euglena gracilis. J. Plant Physiol. 133, 521–528
Westhoff, P., Zetsche, K. (1981) Regulation of the synthesis of ribulose 1,5 bisphosphate carboxylase and its subunits in the flagellate Chlorogonium elongatum. Different levels of translatable messenger RNAs for the large and the small subunits in autotrophic and heterotrophic cells as determined by immunological techniques. Eur. J. Biochem. 116, 261–267
Zhu, Y.S., Kung, S.D., Bogorad, L. (1985) Phytochrome control of levels of mRNA complementary to plastid and nuclear genes of maize. Plant Physiol. 79, 371–376
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Weiss, C., Houlné, G. & Schantz, R. Photocontrol of thylakoid protein synthesis in Euglena: differential post-transcriptional regulation depending on nutritional conditions. Planta 188, 468–477 (1992). https://doi.org/10.1007/BF00197037
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00197037