Abstract
This work reports on the regulation of synthesis of the P700 chlorophyll-a apoprotein of photosystem I in barley. The mRNA for the P700 apoprotein is almost exclusively confined to the plastid membrane-bound polysomes. However, the mRNA for the 32-kDa herbicide-binding protein of photosystem II is found in both the soluble and membrane-bound polysomes.
The mRNA for the P700 apoprotein is found in similar amounts in dark-grown and light-grown wild-type as well as mutant xantha-l81 barley. The latter mutant is deficient in chlorophyll biosynthesis. However, while wild-type leaves accumulate the P700 chlorophyll-a protein only in the light, mutant leaves never accumulate the P700 apoprotein.
A more sensitive approach was taken using isolated plastids to study P700 apoprotein synthesis. Etioplasts did not synthesize detectable P700 apoprotein even when the etioplasts were exposed to light. However, only a 1-min exposure of leaves to light was necessary to induce P700 apoprotein synthesis by isolated plastids.
Phytochrome involvement in controlling P700 apoprotein synthesis was tested by using red/farred light treatment of leaves. These treatments showed no far-red reversibility of red-induced P700-apoprotein synthesis in isolated plastids even after 3 h of darkness after the light treatments. From these data we conclude that the accumulation of P700 apopootein is not under the control of phytochrome and that the light induction of P700 apoprotein is most likely mediated through the protochlorophyllide/chlorophyllide system. This control, however, may also involve cytoplasmic signals as the synthesis of the P700 apoprotein is not turned on in illuminated etioplasts.
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References
Apel, K. (1979) Phytochrome-induced appearance of mRNA activity for the apoprotein of the light-harvesting chlorophyll a/b protein of barley (Hordeum vulgare). Eur. J. Biochem. 97, 183–188
Batschauer, A., Mösinger, E., Kreuz, K., Dörr, I., Apel, K. (1986) The implication of a plastid-derived factor in the transcriptional control of nuclear genes encoding the light-harvesting chlorophyll a/b protein. Eur. J. Biochem. 154, 625–634
Berry, J.O., Nikolau, B.J., Carr, J.P., Klessig, D.F. (1986) Translational regulation of light-induced ribulose 1,5-bisphosphate carboxylase gene expression in Amaranth. Mol. Cell. Biol. 6, 2347–2353
Berry-Lowe, S.L., Meagher, R.B. (1985) Transcriptional regulation of a gene encoding the small subunit of ribulose-1,5-bisphosphate carboxylase in soybean tissue is linked to the phytochrome response. Mol. Cell. Biol. 5, 1910–1917
Bhaya, D., Jagendorf, A.T. (1985) Synthesis of the α and β subunits of coupling factor I by polysomes from pea chloroplasts. Arch. Biochem. Biophys. 237, 217–223
Bogorad, L. (1975) Evolution of organelles and eukaryotic genomes. Science 188, 891–898
Bradbeer, J.W., Atkinson, Y.E., Börner, T., Hagemann, R. (1979) Cytoplasmic synthesis of plastid polypeptides may be controlled by plastid-synthesized RNA. Nature 279, 816–817
Deng, X.-W., Gruissem, W. (1987) Control of plastid gene expression during development: The limited role of transcriptional regulation. Cell 49, 379–387
Deng, X.-W., Stern, D.B., Tonkyn, J.C., Gruissem, W. (1987) Plastic run-on transcription. Application to determine the transcriptional regulation of spinach plastid genes. J. Biol. Chem. 262, 9641–9648
Ellis, R.J. (1981) Chloroplast proteins: synthesis, transport and assembly. Annu. Rev. Plant Physiol. 32, 111–137
Fromm, H., Devic, M., Fluhr, R., Edelman, M. (1985) Control of psb A gene expression: in mature Spirodela chloroplasts light regulation of 32-Kd protein synthesis is independent of transcript level. EMBO J 4, 291–295
Gallagher, T.F., Ellis, R.J. (1982) Light-stimulated transcription of genes for two chloroplast polypeptides in isolated pea leaf nuclei. EMBO J 1, 1493–1498
Harpster, M., Apel, K. (1985) The light-depedent regulation of gene expression during plastid development in higher plants. Physiol. Plant. 64, 147–152
Henningsen, K.W., Stummann, B.M. (1982) Use of mutants in the study of chloroplast biogenesis. In: Encyclopedia of plant physiology, N.S., vol. 14B: Nucleic acids and proteins in plants II, pp. 597–644, Parthier, B., Boulter, D., eds. Springer, Berlin Heidelberg New York
Herrin, D., Michaels, A., Hickey, E. (1981) Synthesis of chloroplast membrane polypeptide on thylakoid-bound ribosomes during the cell cycle of Chlamydomonas reinhardtii 137+. Biochim. Biophys. Acta 644, 136–145
Inamine, G., Nash, B., Weissbach, H., 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. Nat. Acad. Sci. USA 82, 5690–5694
Klein, R.R., Mullet, J.E. (1986) Regulation of chloroplast-encoded chlorophyll-binding protein translation during higher plant chloroplast biogenesis. J. Biol. Chem. 261, 11138–11145
Klein, R.R., Mullet, J.E. (1987) Control of gene expression during higher plant chloroplast biogenesis. Protein synthesis and transcript levels of psbA, psaA-psaB, and rbcL in dark-grown and illuminated barley seedlings. J. Biol. Chem. 262, 4341–4348
Kreuz, K., Dehesh, K., Apel, K. (1986) The light-dependent accumulation of the P700 chlorophyll a protein of the photosystem I reaction center in barley. Evidence for translational control. Eur. J. Biochem. 159, 459–467
Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685
Link, G. (1982) Phytochrome control of plastid mRNA in mustard (Sinapis alba L.). Planta 154, 81–86
Margulies, M.M., Tiffany, H.L., Hattori, T. (1987) Photosystem I reaction center polypeptides of spinach are synthesized on thylakoid-bound ribosomes. Arch. Biochem. Biophys. 254, 454–461
Mayfield, S.P., Taylor, W.C. (1984) Carotenoid-deficient maize seedlings fail to accumulate light-harvesting chlorophyll a/b binding protein (LHCP) mRNA. Eur. J. Biochem. 144, 79–84
Minami, E.-I., Watanabe, A. (1984) Thylakoid membranes: The translational site of chloroplast DNA-regulated thylakoid polypeptides. Arch. Biochem. Biophys. 235, 562–570
Mösinger, E., Batschauer, A., Schäfer, E., Apel, K. (1985) Phytochrome-control of in vitro transcription of specific genes in isolated nuclei from barley (Hordeum vulgare). Eur. J. Biochem. 147, 137–142
Mösinger, E., Batschauer, A., Vierstra, R., Apel, K., Schäfer, E. (1987) Comparison of the effects of exogenous native phytochrome and in-vitro irradiation on in-vitro transcription in isolated nuclei from barley (Hordeum vulgare). Planta 170, 505–514
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
Oelmüller, R., Mohr, H. (1986) Photooxidative destruction of chloroplasts and its consequences for expression of nuclear genes. Planta 167, 106–113
Rodermel, S.R., Bogorad, L. (1985) Maize plastid photogenes: Mapping and photoregulation of transcript levels during light-induced development. J. Cell Biol. 100, 463–476
Shropshire, W., Jr, Mohr, H., eds. (1983) Encyclopedia of plant physiol., N.S., vol. 16A: Photomorphogenesis. Springer, Berlin Heidelberg New York Tokyo
Silverthorne, J., Tobin, E. (1984) Demonstration of transcriptional regulation of specific genes by phytochrome action. Proc. Natl. Acad. Sci. USA 81, 1112–1116
Thompson, W.F., Everett, M., Polans, N.O., Jorgensen, R.A., Palmer, J.D. (1983) Phytochrome control of RNA levels of developing pea and mungbean leaves. Planta 158, 487–500
Tobin, E., Silverthorne, J. (1985) Light regulation of gene expression in higher plants. Annu. Rev. Plant Physiol. 36, 569–593
Vierling, E., Alberte, R.S. (1983) Regulation of synthesis of the photosystem I reaction center. J. Cell Biol. 97, 1806–1814
von Wettstein, D., Henningsen, K.W., Boynton, J.E., Kannangara, G.C., Nielsen, O.F. (1971) The genetic control of chloroplast development in barley. In: Autonomy and biogenesis of mitochondria and chloroplasts, pp. 205–223. Boardman, N.K., Linnane, A.W., Smillie, R.M., eds. North-Holland Publishing Company, Amsterdam
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
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Laing, W., Kreuz, K. & Apel, K. 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 (1988). https://doi.org/10.1007/BF00392455
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DOI: https://doi.org/10.1007/BF00392455