, Volume 167, Issue 1, pp 106–113

Photooxidative destruction of chloroplasts and its consequences for expression of nuclear genes

  • R. Oelmüller
  • H. Mohr


Expression of nuclear genes involved in plastidogenesis is known to be controlled by light via phytochrome. Examples are the small subunit (SSU) of ribulose-1,5-bisphosphate carboxylase and the light harvesting chlorophyll a/b binding protein of photosystem II (LHCP). In the present study we show that, beside phytochrome, the integrity of the plastid is essential for the expression of the pertinent nuclear genes as measured at the level of translatable mRNA. When the plastids are severely damaged by photooxidation in virtually carotenoid-free mustard (Sinapis alba L.) seedling cotyledons (made carotenoid-free by the application of Norflurazon, NF), almost no SSU, no SSU precursor, LHCP and LHCP precursor can be detected by immunological assays, and almost no translatable mRNA of SSU and LHCP can be found, although the levels and rates of phytochrome-mediated syntheses of representative cytoplasmic, mitochondrial and glyoxisomal enzymes are not adversely affected and morphogenesis of the mustard seedling proceeds normally (Reiß et al. 1983; Planta 159, 518–528). Norflurazon per se has no effect on the amount of translatable mRNA of SSU and LHCP as shown by irradiation of NF-treated seedlings with far-red light (FR) which strongly activates phytochrome but does not cause photooxidation in the plastids. It is concluded that a signal from the plastid is required to allow the phytochrome-mediated appearance of translatable mRNA for SSU and LHCP. Seedlings not treated with NF show a higher level of translatable mRNALHCP in red light (RL) compared to FR, whereas the mRNASSU levels are the same in RL and FR. These facts indicate that the level of translatable mRNALHCP is adversely affected if the apoprotein is not incorporated into the thylakoid membrane.

Key words

Chloroplast photooxidation Gene expression Photooxidation (chloroplast) Phytochrome, chloroplasts, gene expression Sinapis 



far-red light (3.5 W m-2)


light harvesting chlorophyll a/b binding protein of photosystem II


large subunit of RuBPCase




red light (6.8 W m-2)


ribulose-1,5-bisphosphate carboxylase (EC


small subunit of RuBPCase


white light (28 W m-2)


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 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, 183–188Google Scholar
  2. Apel, K., Kloppstech, K. (1980) The effect of light on the biosynthesis of the light-harvesting chlorophyll a/b protein. Evidence for the requirement of chlorophyll a for the stabilization of the apoprotein. Planta 150, 426–430Google Scholar
  3. Bennett, J. (1981) Biosynthesis of the light-harvesting chlorophyll a/b protein. Polypeptide turnover in darkness. Eur. J. Biochem. 118, 61–70Google Scholar
  4. Blair, G.E., Ellis, R.J. (1973) Protein synthesis in chloroplasts. I. Light driven synthesis of the large subunit of fraction I protein by isolated pea chloroplasts. Biochim. Biophys. Acta 319, 223–234Google Scholar
  5. Bonner, W.M., Laskey, R.A. (1974) A film detection method for tritium labelled proteins and nucleic acids in polyacrylamide gels. Eur. J. Biochem. 46, 83–88Google Scholar
  6. Bradford, M.J. (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254Google Scholar
  7. Brüning, K., Drumm, H., Mohr, H. (1975) One the role of phytochrome in controlling enzyme levels in plastids. Biochem. Physiol. Pflanz 168, 141–156Google Scholar
  8. Cashmore, A.R. (1979) Reteration frequency of the gene coding for the small subunit of ribulose-1,5-bisphosphate carboxylase. Cell 17, 383–388Google Scholar
  9. Coen, D.M., Bedbrook, J.R., Bogorad, L., Rich, A. (1977) Maize chloroplast DNA fragment encoding the large subunit of ribulosebisphosphate carboxylase. Proc. Natl. Acad. Sci. USA 74, 5487–5491Google Scholar
  10. Dobberstein, B., Blobel, G., Chua, N.-H. (1977) In vitro synthesis and processing of a putative precursor for the small subunit of ribulose-1,5-bisphosphate carboxylase of Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 74, 1082–1085Google Scholar
  11. Drumm-Herrel, H., Bergfeld, R., Mohr, H. (1984) Photooxidative destruction of chloroplasts and its consequences for anthocyanin synthesis. Proc. Indian Acad. Sci. 93, 245–251Google Scholar
  12. Fairbanks, G., Steck, T.L., Wallach, D.F.H. (1971) Electrophoretic analysis of the major polypeptides of the human erythrocyte membrane. Biochemistry 10, 2606–2617Google Scholar
  13. Fourcroy, P., Klein-Eude, D., Lambert, C. (1985) Phytochrome control of gene expression in radish seedlings. II. Far-red light mediated appearance of the ribulose 1,5-bisphosphate carboxylase and the mRNA for its small subunit. Plant Sci. Lett. 37, 235–244Google Scholar
  14. Frosch, S., Bergfeld, R., Mohr, H. (1976) Light control of plastogenesis and ribulosebisphosphate carboxylase levels in mustard seedling cotyledons. Planta 133, 53–56Google Scholar
  15. Frosch, S., Jabben, M., Bergfeld, R., Kleinig, H., Mohr, H. (1979) Inhibition of carotenoid biosynthesis by the herbicide SAN 9789 and its consequences for the action of phytochrome on plastogenesis. Planta 145, 497–505Google Scholar
  16. Goldthwaite, J.J., Bogorad, L. (1971) A one-step method for the isolation and determination of leaf ribulose-1,5-diphosphate carboxylase. Anal. Biochem. 41, 57–66Google Scholar
  17. Gottmann, K., Schäfer, E. (1982) In vitro synthesis of phytochrome apoprotein directed by mRNA from light and dark grown Avena seedlings. Photochem. Photobiol. 35, 521–525Google Scholar
  18. Harpster, M.H., Mayfield, S.P., Taylor, W.C. (1984) Effects of pigment-deficient mutants on the accumulation of photosynthetic proteins in maize. Plant Mol. Biol. 3, 59–71Google Scholar
  19. Highfield, P.E., Ellis, R.J. (1978) Synthesis and transport of the small subunit of chloroplast ribulose bisphosphate carboxylase. Nature 271, 420–424Google Scholar
  20. Kreuz, K., Kleinig, H. (1984) Synthesis of prenyl lipids in cells of spinach leaf. Compartimentation of enzymes for formation of isopentenyl diphosphate. Eur. J. Biochem. 141, 531–535Google Scholar
  21. Kung, S.D., Thornber, J.P., Wildman, S.G. (1972) Nuclear DNA codes for the photosystem II chlorophyll-protein of chloroplast membranes. FEBS Lett. 24, 185–188Google Scholar
  22. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of Bacteriophage T4. Nature 227, 680–685Google Scholar
  23. Lowry, O.H., Rosebrough, N.J., Farr, A.L., Randall, R.J. (1951) Protein measurement with the folin phenol reagent. J. Biol. Chem. 193, 265–275Google Scholar
  24. 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, 79–84Google Scholar
  25. Mohr, H. (1966) Untersuchungen zur phytochrominduzierten Photomorphogenese des Senfkeimlings (Sinapis alba L.) Z. Pflanzenphysiol. 54, 63–83Google Scholar
  26. Mohr, H. (1972) Lectures on photomorphogenesis. Springer, Berlin Heidelberg New YorkGoogle Scholar
  27. Oelmüller, R., Mohr, H. (1985) Carotenoid composition in milo (Sorghum vulgare) shoots as affected by phytochrome and chlorophyll. Planta 164, 390–395Google Scholar
  28. Occhterlony, O. (1968) Handbook of immunodiffusion and immunoelectrophoresis. Ann Arbor Science Publishers, Ann Arbor, Mich.Google Scholar
  29. Pelham, H.R.B., Jackson, R.J. (1976) An efficient mRNA-dependent translation system from reticulocyte lysates. Eur. J. Biochem. 67, 247–256Google Scholar
  30. Reiß, T., Bergfeld, R., Link, G., Thien, W., Mohr, H. (1983) Photooxidative destruction of chloroplasts and its consequences of cytocolic enzyme levels and plant development. Planta 159, 518–528Google Scholar
  31. Roscoe, T.J., Ellis, R.J. (1982) Two-dimensional gel-electrophoresis of chloroplast proteins. In: Methods in chloroplast molecular biology, pp. 1015–1028, Edelman, M., Hallick, R.B., Chua, N.-H., eds. Elsevier Biomedical Press, Amsterdam New York OxfordGoogle Scholar
  32. Schmidt, G.W., Bartlett, S.G., Grossman, A.R., Cashmore, A.R., Chua, N.-H. (1981) Biosynthetic pathways of two polypeptide subunits of the light-harvesting chlorophyll a/b protein complex. J. Cell Biol. 91, 468–478Google Scholar
  33. Silverthorne, J., Tobin, E.M. (1984) Demonstration of transcriptional regulation of specific genes by phytochrome action. Proc. Natl. Acad. Sci. USA 81, 1112–1116Google Scholar
  34. Slovin, J.P., Tobin, E.M. (1982) Synthesis and turnover of the light-harvesting chlorophyll a/b-protein in Lemma gibba grown with intermittent red light: possible translational control. Planta 154, 465–472Google Scholar
  35. Thornber, J.P. (1975) Chlorophyll-proteins: light-harvesting and reaction center components of plants. Annu. Rev. Plant Physiol. 26, 127–158Google Scholar
  36. Tobin, E.M. (1981) Phytochrome-mediated regulation of messenger RNAs for the small subunit of ribulose-1,5-bisphosphate carboxylase and the light-harvesting chlorophyll a/b protein in Lemna gibba. Plant Mol. Biol. 1, 35–51Google Scholar
  37. Towbin, H., Staehelin, T., Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76, 4350–4354Google Scholar

Copyright information

© Springer-Verlag 1986

Authors and Affiliations

  • R. Oelmüller
    • 1
  • H. Mohr
    • 1
  1. 1.Biologisches Institut II der UniversitätFreiburgGermany

Personalised recommendations