Photosynthetic Enzyme Regulation by the Ferredoxin/Thioredoxin and the Ferralterin Mechanisms

  • Bob B. Buchanan


One type of covalent enzyme modification that has been used in studies on the structure and mechanism of action of enzymes is a change in the oxidation state of a “nonprosthetic” part of the protein, such as a sulfhydryl group. Limited attention has been given to the idea that oxidation-reduction changes may be used to regulate the activation of enzymes in a manner analogous to other types of reversible covalent modification, such as phosphorylation-dephosphorylation and adenylation-deadenylation. We summarize in this report evidence that enzyme regulation due to a reversible oxidation-reduction change is a process fundamental to photosyn-thetic and perhaps to other types of living cells. In this article we will first describe work from our own laboratory that led to the finding of a redox-based regulatory mechanism in photosynthesis; we will then relate these findings to other mechanisms of light-dependent enzyme regulation in chloroplasts, including the recently found ferralterin mechanism.


Protein Factor Enzyme Regulation Spinach Chloroplast Chloroplast Membrane Chloroplast Enzyme 
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  1. Anderson, L. E., 1980, Light modulation of enzyme activity in green plants: the LEM system, Federation Proc., 39:1931.Google Scholar
  2. Anderson, L. E., and Avron, M., 1976, Light modulation of enzyme activity in chloroplasts, Plant Physiol., 57:209.PubMedCrossRefGoogle Scholar
  3. Ashton, A. R., and Anderson, L. E., 1979, Reconstitution of the light activation system for pea leaf chloroplast malate dehydrogenase, Plant Physiol., 63,suppl. 24.Google Scholar
  4. Ashton, A. R., and Anderson, L. E., 1980, Resolution and reconstitution of the light-dependent modulation system of chloroplast enzymes, Abstracts, 5th Intl. Congr. Photosynthesis, Halkidiki, Greece.Google Scholar
  5. Binder, A., Jagendorf, A., and Ngo, E., 1978, Isolation and composition of the subunits of spinach chloroplast coupling factor protein, J. Biol. Chem., 253:3094.PubMedGoogle Scholar
  6. Black, S., Harte, E. M., Hudson, B., and Wartofsky, L., 1960, A specific enzymatic reduction of L(-) methionine sulfoxide and a related nonspecific reduction of disulfides, J. Biol. Chem., 235:2910.Google Scholar
  7. Breazeale, V. D., Buchanan, B. B., and Wolosiuk, R. A., 1978, Chloroplast sedoheptulase 1, 7-biphosphatase: Evidence for regulation by the ferredoxin/thioredoxin system, Zeit. Naturforsch. 33c:521.Google Scholar
  8. Brill, W. J., Westphal, J., Stieghorst, M., Davis, L. C., and Shah, V. K., 1974, Detection of nitrogenase components and other non-heme iron proteins in Polyacrylamide gels, Anal. Biochem., 60:237.PubMedCrossRefGoogle Scholar
  9. Buchanan, B. B., Kalberer, P. P., and Arnon, D. E., 1967, Ferredoxin-activated fructose diphosphatase in isolated chloroplasts, Biochem. Biophys. Res. Commun., 29:74.PubMedCrossRefGoogle Scholar
  10. Buchanan, B. B., Schürmann, P., and Kalberer, P. P., 1971, Ferre-doxin-activated fructose diphosphatase of spinach chloroplasts, J. Biol. Chem., 246:5952.PubMedGoogle Scholar
  11. Buchanan, B. B., and Wolosiuk, R. A., 1976, Photosynthetic regulatory protein found in animal and bacterial cells, Nature, 264:669.PubMedCrossRefGoogle Scholar
  12. Buchanan, B. B., Wolosiuk, R. A., Crawford, N. A., and Yee, B. C., 1978, Evidence for three thioredoxins in leaves, Plant Physiol., 61:38S.CrossRefGoogle Scholar
  13. Buchanan, B. B., Crawford, N. A., and Wolosiuk, R. A., 1979, Activation of plant acid phosphatases by oxidized glutathionine and dehydroascorbate, Plant Sci. Lett., 14:245.CrossRefGoogle Scholar
  14. Crawford, N. A., Yee, B. C., Nishizawa, A. N., and Buchanan, B. B., 1979, Occurrence of cytoplasmic f and m-type thioredoxins in leaves, FEBS Lett., 104:141.CrossRefGoogle Scholar
  15. Frieden, C., 1971, Protein-protein interaction and enzymatic activity, Ann. Rev. Biochem., 40:653.PubMedCrossRefGoogle Scholar
  16. Groden, D., and Beck, E., 1977, Characterization of a membrane bound, ascorbate specific peroxidase from spinach chloroplasts, Abstracts, 4th Int. Cong. Photosynthesis, Reading, U.K.Google Scholar
  17. Haddox, M. K., Stephenson, J. H., Moser, M. E., and Goldberg, N. D., 1978, Oxidative-reductive modulation of Guinea pig splenic cell cyclase activity, J. Biol. Chem., 253:3143.PubMedGoogle Scholar
  18. Hardy, R. W. F., and Burns, C., 1973, Comparative biochemistry of iron-sulfur proteins and dinitrogen fixation, in: “Iron-Sulfur Proteins,” W. Lovenberg, ed., Vol. 1, Academic Press, NY.Google Scholar
  19. Heldt, H. W., Chon, C. J., Lilley, R. McC., and Portis, A., 1978, The role of fructose—and sedoheptulose bisphosphatase in the control of CO2 fixation. Evidence from the effects of Mg++ concentration, pH and H2O2, Proc. 4th Int. Congr. Photosynthesis, The Biochem. Soc., London.Google Scholar
  20. Holmgren, A., Buchanan, B. B., and Wolosuik, R. A., 1977, Different receptors for somatostatin and opioids in neuroblastoma x glioma hybrid cells, FEBS Lett., 82:351.PubMedCrossRefGoogle Scholar
  21. Holmgren, A., 1977, Bovine thioredoxin system, J. Biol. Chem., 252:4600.PubMedGoogle Scholar
  22. Jacquot, J. P., Vidal, J., and Gadal, P., 1976, Identification of a protein factor involved in dithiothreitol activation of NADP malate dehydrogenase from French bean leaves, FEBS Lett., 71: 223.PubMedCrossRefGoogle Scholar
  23. Jacquot, J. P., Vidal, J., Gadal, P., and Schürmann, P., 1978, Evidence for the existence of several enzyme specific thioredoxins in plants, FEBS Lett., 96:243.CrossRefGoogle Scholar
  24. Kagawa, T., and Hatch, M. D., 1977, Regulation of C4 photosynthesis: characterization of a protein factor mediating the activation and inactivation of NADP-malate dehydrogenase, Arch. Biochem. Biophys., 184:290.PubMedCrossRefGoogle Scholar
  25. Lara, C., de la Torre, A., and Buchanan, B. B., 1980, A new protein factor functional in the ferredoxin-independent light activation of chloroplast fructose 1, 6-biphosphatase, Biochem. Biophys. Res. Commun., 93:544.PubMedCrossRefGoogle Scholar
  26. Lara, C., de la Torre, A., and Buchanan, B. B., 1980, Ferraltrin: an iron-sulfur protein functional in enzyme regulation in photosynthesis, Biochem. Biophys. Res. Commun., 94:1337.PubMedCrossRefGoogle Scholar
  27. Laurent, T. C., Moore, E. C., and Reichard, P., 1964, Enzymatic synthesis of deoxyribonucleotides, J. Biol. Chem., 239:3436.PubMedGoogle Scholar
  28. Lendzian, K., and Bassham, J. A., 1975, Regulation of glucose-6-phosphate dehydrogenase in spinach chloroplasts by ribulose 1, 5-diphosphate NADPH/NADP+ ratios, Biochem. Biophys. Acta, 396:260.PubMedCrossRefGoogle Scholar
  29. Lorimer, G. H., Badger, M. R., and Andrews, T. J., 1976, The activation of ribulose-1, 5-bisphosphate carboxylase by carbon dioxide and magnesium ions. Equilibria, kinetics, a suggested mechanism and physiological implications, Biochemistry, 15:529.PubMedCrossRefGoogle Scholar
  30. Malkin, R., 1973, The chemical properties of ferredoxins, in: “Iron-Sulfur Proteins,” W. Lovenberg, ed., Vol. 2, Academic Press, New York.Google Scholar
  31. Mark, D. F., and Richardson, C. C., 1976, Escherichia coli thio-redoxin: a subunit of bacteriophage T7 DNA polymerase, Proc. Natl. Acad. Sci. USA, 73:780.PubMedCrossRefGoogle Scholar
  32. McKinney, D. W., Buchanan, B. B., and Wolosiuk, R. A., 1978, Activation of chloroplast ATPase by reduced thioredoxin, Phyto-chemistry, 17:794.Google Scholar
  33. McKinney, D. W., Buchanan, B. B., and Wolosiuk, R. A., 1979, Association of a thioredoxin-like protein with chloroplast coupling factor (CF1), Biochem. Biophys. Res. Commun., 86:1178.PubMedCrossRefGoogle Scholar
  34. Mills, J. D., Mitchell, P., and Schürmann, P., 1980, Modulation of coupling factor ATPase activity in intact chloroplasts, FEBS Lett., 112:173.CrossRefGoogle Scholar
  35. Moreno, C. G., Aparacio, P. J., Palacian, E., and Losada, M., 1972, Association of a Thioredoxin-like protein with chloroplast coupling factor (CF1), FEBS Lett., 26:11.PubMedCrossRefGoogle Scholar
  36. Müller, B., Ziegler, I., and Ziegler, H., 1969, Lichtinduzierté, reversible aktivitatssteigerung der NADP-abhangigen glycerin-aldehyde−3-phosphat-dehydrogenase in chloroplasta, Eur. J. Biochem., 9:101.PubMedCrossRefGoogle Scholar
  37. Nelson, N., Deters, H., Nelson, D. W., and Racker, E., 1973, Partial resolution of the enzymes catalyzing photophosphorylation, J. Biol. Chem., 248:2049.PubMedGoogle Scholar
  38. Nelson, N., 1976, Structure and function of chloroplast ATPase, Biochem. Biophys. Acta, 456:314.PubMedGoogle Scholar
  39. Nishizawa, A. N., Wolosiuk, R. A., and Buchanan, B. B., 1979, Chloroplast phenylalanine ammonia-lyase from spinach leaves, Planta, 145:7.CrossRefGoogle Scholar
  40. Petersen, T. A., Kirk, M., and Bassham, J. A., 1966, Light-dark transients in levels of intermediate compounds during photosynthesis in air-adapted Chlorella, Physiol. Plant., 19:219.CrossRefGoogle Scholar
  41. Pigiet, V., and Conley, R. R., 1978, Isolation and characterization of phosphothioredoxin from Escherichia coli, J. Biol. Chem., 253:1910.PubMedGoogle Scholar
  42. Porque, P. G., Baldesten, A., and Reichard, J. P., 1970, Purification of a thioredoxin system from yeast, J. Biol. Chem., 245:2363.Google Scholar
  43. Pupillo, P., and Giuliani-Piccari, G. G., 1975, The reversible de-polymerization of spinach chloroplast glyceraldehyde-phosphate dehydrogenase, Eur. J. Biochem., 51:475.PubMedCrossRefGoogle Scholar
  44. Reichard, P., 1968, The biosynthesis of deoxyribonucleotides, Eur. J. Biochem., 3:259.PubMedCrossRefGoogle Scholar
  45. Scheibe, R., 1980, On the dark modulation of chloroplast enzymes, Federation Proc., 39:1771.Google Scholar
  46. Schürmann, P., and Buchanan, B. B., 1975, Role of ferredoxin in the activation of sedoheptulose diphosphatase in isolated chloro-plasts, Biochem. Biophys. Acta, 376:189.PubMedCrossRefGoogle Scholar
  47. Schürmann, P., Wolosiuk, R. A., Breazeale, V. D., and Buchanan, B. B., 1976, Two proteins function in the regulation of photosyn-thetic CO2 assimilation in chloroplasts, Nature, 263:257.CrossRefGoogle Scholar
  48. Suske, G., Wagner, W., and Follmann, H., NADPH-dependent thioredoxin reductase and a new thioredoxin from wheat, Zeit. Naturforsch., 34:214.Google Scholar
  49. Wagner, W., and Follmann, H., 1977, A thioredoxin from green algae, Biochem. Biophys. Res. Commun., 77:1044.CrossRefGoogle Scholar
  50. Wagner, W., Follmann, H., and Schmidt, A., 1978, Multiple functions of thioredoxins, Zeit. Naturforsch., 33c:517.Google Scholar
  51. Wilson, L. G., Asahi, T., and Bandurski, R. S., 1971, Yeast sulfate-reducing system, J. Biol. Chem., 236:1822.Google Scholar
  52. Wildner, G. F., 1975, The regulation of glucose-6-phosphate dehydrogenase in chloroplasts, Zeit. Naturforsch., 30c:756.Google Scholar
  53. Wolosiuk, R. A., Crawford, N. A., Yee, B. C., and Buchanan, B. B., 1979, Isolation of three thioredoxins from spinach leaves, J. Biol. Chem., 254:1627.PubMedGoogle Scholar
  54. Wolosiuk, R. A., and Buchanan, B. B., 1977, Thioredoxin and glutathione regulate photosynthesis in chloroplasts, Nature, 266:565.CrossRefGoogle Scholar
  55. Wolosiuk, R. A., and Buchanan, B. B., 1978, Regulation of chloroplast phosphoribulokinase by the ferredoxin/thioredoxin system, Arch. Biochem. Biophys., 189:97.PubMedCrossRefGoogle Scholar
  56. Wolosiuk, R. A., Buchanan, B. B., and Crawford, N. A., 1977, Regulation of NADP-malate dehydrogenase by the light-activated ferredoxin/thioredoxin system of chloroplasts, FEBS Lett., 81:253.CrossRefGoogle Scholar
  57. Wolosiuk, R. A., and Buchanan, B. B., 1978, Activation of chloroplast NADP-linked glyceraldehyde-3-phosphate dehydrogenase by the ferredoxin/thioredoxin system, Plant Physiol., 61:669.PubMedCrossRefGoogle Scholar
  58. Ziegler, H., and Ziegler, I., 1965, Der einfluss der belichtung auf die NADP+-abhängige glycerinaldehyd-3-phosphat-dehydrog-enase, Planta (Berlin), 65:369.CrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1981

Authors and Affiliations

  • Bob B. Buchanan
    • 1
  1. 1.Section of Cell Physiology, Department of Plant and Soil BiologyUniversity of CaliforniaBerkeleyUSA

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