Advertisement

The Organization of Photosynthetic Enzymes on the Chloroplast Membrane

  • David W. Krogmann

Abstract

Early observations with the light microscope indicated that the chloroplast is the site of photosynthesis in the higher plant cell. The chloroplast contains all of the chlorophyll which must absorb light energy for the process. After illumination of an intact leaf previously held in darkness, the chloroplast is seen to contain new starch grains which are an obvious end product of photosynthesis. Electron microscopy reveals the chloroplast as bounded by a limiting membrane or outer envelope and containing within a complex series of membranes or lamellae (Figure 1). It appears that many of the enzymes involved in the conversion of carbon dioxide into starch and other reduced products of photosynthesis are loosely held within the chloroplast. These enzymes may reside in the stroma or matrix space within the chloroplast and are readily released on rupture of the outer envelope. One enzyme of the carbon reduction path is clearly associated with the lamellar membrane surface. The enzyme ribulose diphosphate carboxylase is quite large (mol. wt. 550,000) and can be recognized as a 120 Å cuboidal particle on the outer surface of the lamellae. The detailed catalytic properties of this enzyme are only beginning to emerge, and one can expect that enzyme-membrane interaction will be an interesting study when both the pure ribulose diphosphate carboxylase and the membrane become a bit more manageable. At present there is no evidence that association with membrane structure, other than containment within the chloroplast outer envelope, imposes any special influences on the carbon reduction pathways of photosynthesis.

Keywords

Coupling Factor Spinach Chloroplast Chloroplast Membrane Outer Envelope Intact Chloroplast 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Amesz, J., 1973, The function of plastoquinone in photosynthetic electron transport, Biochim. Biophys. Acta 301:35.PubMedGoogle Scholar
  2. Arntzen, C. J., Dilley, R. A., and Crane, F. L., 1969, A comparison of chloroplast membrane surfaces visualized by freeze-etch and negative staining techniques: And ultrastructural characterization of membrane fractions obtained from digitonin treated spinach chloroplasts, J. Cell Biol. 43:16.CrossRefGoogle Scholar
  3. Arntzen, C. J., Dilley, R. A., Peters, G. A., and Shaw, E. R., 1972, Photochemical activity and structural studies of photosystems derived from chloroplast grana and stroma lamellae, Biochim. Biophys. Acta 256:85.PubMedCrossRefGoogle Scholar
  4. Arntzen, C. J., Vernotte, C., Briantais, J. M., and Armond, P., 1974, Evidence for the surface localization of photosystem II reaction centers, Biochim. Biophys. Acta 368:39.PubMedCrossRefGoogle Scholar
  5. Asada, K., Tamura, C., and Bandurski, R. A., 1968, Methyl viologen-linked sulfite reductase from spinach leaves: A hemoprotein, Biochem. Biophys. Res. Commun. 30:554.PubMedCrossRefGoogle Scholar
  6. Avron, M., 1963, A coupling factor in photophosphorylation, Biochim. Biophys. Acta. 77:699.CrossRefGoogle Scholar
  7. Bendall, D. S., and Hill, R., 1968, Haem-proteins in photosynthesis, Annu. Rev. Plant Physiol. 19:167.CrossRefGoogle Scholar
  8. Berg, S., Dodge, S., Krogmann, D. W., and Dilley, R. A., 1974, Chloroplast membrane carboxyl groups, their involvement in membrane association, Plant Physiol. 53:619.PubMedCrossRefGoogle Scholar
  9. Berzborn, R. J., 1969, Untersuchungen uber die Oberflachenstruktur des Thylokoid Systems der Plasten mit Hilfe von Antikorpern gegen die Ferredoxin-NADP-reductase, Z. Naturforsch. 24b:436.Google Scholar
  10. Berzborn, R. J., Menke, W., Trebst, A., and Pistorius, A., 1966, Ober die Hemmung photosynthetischer Reaktionen isolierter Chloroplasten durch Chloroplastenantikorper, Z. Naturforsch. 21b:1057.Google Scholar
  11. Berzborn, R. J., Kopp, F., and Muhlethaler, K., 1974, Coupling factor 1 (CF1), a mobile peripheral protein in the thylakoid surface of spinach chloroplasts, Abstracts, Third International Congress on Photosynthesis, Rehovot, Israel, p. 10.Google Scholar
  12. Boardman, N. K., and Anderson, J. M., 1967, Fractionation of the photochemical systems of photosynthesis, Biochim. Biophys. Acta 143:187.PubMedCrossRefGoogle Scholar
  13. Brand, J., and San Pietro, A., 1973, Polylysine enhanced effectiveness of plastocyanin in photo-system I, Biochim. Biophys. Acta 325:255.PubMedCrossRefGoogle Scholar
  14. Brand, J., Baszynski, T., Crane, F. L., and Krogmann, D. W., 1972a, Selective inhibition of photosynthetic reactions by polycations, J. Biol. Chem. 247:2814.PubMedGoogle Scholar
  15. Brand, J., San Pietro, A., and Mayne, B. C., 1972b, Site of polylysine inhibition of photosystem I in spinach chloroplasts, Arch. Biochem. Biophys. 152:426.PubMedCrossRefGoogle Scholar
  16. Branton, D., 1968, Structure of the photosynthetic apparatus, in: Photophysiology (A. C. Giese, ed.), Vol. 3, pp. 197–224, Academic Press, New York.Google Scholar
  17. Branton, D., and Park, R. B., 1967, Subunits in chloroplast lamellae, J. Ultrastruct. Res. 19:283.PubMedCrossRefGoogle Scholar
  18. Briantais, J. M., 1967, Rétablissement du lien entre deux structures chloroplastiques isolées par action du Triton X-100, Biochim. Biophys. Acta 143:650.PubMedCrossRefGoogle Scholar
  19. Briantais, J. M., and Pigaud, M., 1972, Immunological evidence for a localization of system I on the outside face and system II on the inside face of the chloroplast lamella, FEBS Lett. 20:100.PubMedCrossRefGoogle Scholar
  20. Buchanan, B. B., Sghurmann, P., and Kalberer, P. P., 1971, Ferredoxin-activated frutose diphos-phatase of spinach chloroplasts, J. Biol. Chem. 246:5952.PubMedGoogle Scholar
  21. Cheniae, G. M., 1970, Photosystem II and oxygen evolution, Annu. Rev. Plant Physiol. 21:467.CrossRefGoogle Scholar
  22. Cohen, W. S., and Jagendorf, A. T., 1972, Inhibition of energy linked reactions in chloroplasts by polygalacturonate, Arch. Biochem. Biophys. 150:235.PubMedCrossRefGoogle Scholar
  23. Cramer, W. A., and Butler, W. L., 1967, Light induced absorbance changes of two cytochrome b components in the electron transport system of spinach chloroplasts, Biochim. Biophys. Acta 143:332.PubMedCrossRefGoogle Scholar
  24. Cramer, W. A., and Horton, P., 1974, On the oxidation mechanism of cytochrome b-559 by photosystem I, Abstracts, Third International Congress on Photosynthesis, Rehovot, Israel, p. 23.Google Scholar
  25. Cramer, W. A., Fan, H. N., and Böhme, H., 1971, High and low potential states of the chloroplast cytochrome b-559 and thermodynamic control of non-cyclic electron transport, J. Bioenerg. 2:289.PubMedCrossRefGoogle Scholar
  26. Dilley, R. A., Peters, G. A., and Shaw, E. R., 1972, A test of the binary chloroplast membrane hypothesis by using a non-penetrating chemical probe, p-(diazonium) benzene sulfonic acid, J. Membr. Biol. 8:163.CrossRefGoogle Scholar
  27. Duysens, L. N. M., 1964, Photosynthesis, Prog. Biophys. Molec. Biol. 14:1.CrossRefGoogle Scholar
  28. Elstner, E., Pistorius, E., Boger, P., and Trebst, A., 1968, Zur Rolle von Plastocyanin und Cyto-chrom/inphotosynthetischen Electronen Transport, Planta 79:146.CrossRefGoogle Scholar
  29. Fan, H. N., and Cramer, W. A., 1970, The redox potentials of cytochromes b-559 and b-563 in spinach chloroplasts, Biochim. Biophys. Acta 216:200.PubMedCrossRefGoogle Scholar
  30. Forti, G., Rosa, L., and Garlasghi, F., 1972, Synthesis of ADP by isolated CF1 of chloroplasts, FEBS Lett. 27:23.PubMedCrossRefGoogle Scholar
  31. Foust, G. P. Mayhew, S. G., and Massey, V., 1969, Complex formation between ferredoxin triphosphopyridine nucleotide reductase and electron transfer proteins, J. Biol. Chem. 244:964.PubMedGoogle Scholar
  32. Fredricks, W. W., and Kohlmann, J. M. 1969, Inhibitors of the transhydrogenase activity of spinach ferredoxin-nicotinamide adenine dinucleotide phosphate reductase, J. Biol. Chem. 244:522.PubMedGoogle Scholar
  33. Fredricks, W. W., and Gehl, J. W., 1973, Multiple forms of ferredoxin-nicotinamide nucleotide phosphate reductase, Fed. Proc. 32:477.Google Scholar
  34. Garewal, H. S., Singh, J., and Wasserman, A. R., 1971, Purification of chloroplast cytochrome b-559, Biochem. Biophys. Res. Commun. 44:1300.PubMedCrossRefGoogle Scholar
  35. Giaquinta, R., Dilley, R. A., and Anderson, B. J., 1974, Photosystem II dependent membrane conformational changes revealed by binding of diazonium benzene sulfonic acid, Abstracts, Third International Congress on Photosynthesis, Rehovot, Israel, p. 36.Google Scholar
  36. Girault, G., and Galmighe, J. M., 1972, Reversible light induced pH rise in CF1 deficient chloroplasts, FEBS Lett. 19:315.PubMedCrossRefGoogle Scholar
  37. Harnischfeger, G., and Shavit, N., 1974, Effect of divalent cations on ferredoxin linked electron transport in chloroplasts, FEBS Lett. 45:286.PubMedCrossRefGoogle Scholar
  38. Hauska, G. A., McCarty, R. E., Berzborn, R. J., and Racker, E., 1971, The function of plastocyanin and its interaction with a specific antibody, J. Biol. Chem. 246:3524.PubMedGoogle Scholar
  39. Heidemann-VanWyk, D., and Kannangara, C. G., 1971, Localization of ferredoxin in the thyla-koid membrane with immunological methods, Z. Naturforsch. 26b:46.Google Scholar
  40. Hiyama, T., and Ke, B., 1971, A new photosynthetic pigment, “P 430”: Its possible role as the primary electron acceptor of photosystem I, Proc. Natl. Acad. Sci. U.S.A. 68:1010.PubMedCrossRefGoogle Scholar
  41. Honeycutt, R. C., and Krogmann, D. W., 1972, Further studies on the oxygen-reducing system of Anabaena variabilis, Biochim. Biophys. Acta 256:467.PubMedCrossRefGoogle Scholar
  42. Howell, S. H., and Moudrianakis, E. N., 1967a, Hill reaction site in chloroplast membranes: non-participation of the quantasome particle in photoreduction J. Mol. Biol. 27:323.PubMedCrossRefGoogle Scholar
  43. Howell, S. H. and Moudrianakis E.N. 1967b, Function of the “quantasome” in photosynthesis: Structure and properties of a membrane bound particle active in the dark reactions of photo-phosphorylation, Proc. Natl. Acad. Sci. U.S.A. 58:1261.PubMedCrossRefGoogle Scholar
  44. Joliot, P., Joliot, A., and Kok, B., 1968, Analysis of the interactions between the two photosystems in isolated chloroplasts, Biochim. Biophys. Acta 153:635.PubMedCrossRefGoogle Scholar
  45. Katoh, S., and San Pietro, A., 1967, The role of G-type cytochrome in the Hill reaction with Euglena chloroplasts, Arch. Biochem. Biophys. 118:488.PubMedCrossRefGoogle Scholar
  46. Ke, B., The primary electron acceptor of photosystem I, Biochim. Biophys. Acta 301:1.Google Scholar
  47. Kierns, J. J., and Wang, J. H., 1972, Studies on nicotinamide dinucleotide phosphate reductase of spinach chloroplasts, J. Biol. Chem. 247:7374.Google Scholar
  48. Kimimura, M., and Katoh, S., 1972, Functional site of plastocyanin: Inhibitory effects of HgCl2 on electron transport and plastocyanin in chloroplasts, Biochim. Biophys. Acta 283:279.PubMedCrossRefGoogle Scholar
  49. Kimimura, M., and Katoh, S., 1973, The reduction sites of various Hill oxidants in the photosyn-thetic electron transport system, Biochim. Biophys. Acta 325:167.PubMedCrossRefGoogle Scholar
  50. Kok, B., 1961, Partial purification and determination of oxidation reduction potential of the photo-synthetic chlorophyll complex absorbing at 700 mμ, Biochim, Biophys. Acta 48:527.CrossRefGoogle Scholar
  51. Krogmann, D. W., and Olivero, E., 1962, The specificity of plastoquinone as a cofactor for photo-phosphorylation, J. Biol. Chem. 237:3292.PubMedGoogle Scholar
  52. Lea, P. J., and Mifflin, B. J., 1974, Alternative route for nitrogen assimilation in higher plants, Nature 251:614.PubMedCrossRefGoogle Scholar
  53. Livine, A., and Racker, E. 1969, Interaction of CF1 from chloroplasts with RNA and lipid, J. Biol. Chem. 244:1332.Google Scholar
  54. Losada M. J. Ramirez, J. M., Paneque, A., and Del Campo, F. F., 1965, Light and dark reduction of nitrate in a reconstituted chloroplast system, Biochim. Biophys. Acta 109:86.PubMedCrossRefGoogle Scholar
  55. Magree, L., Henninger, M. D., and Crane, F. L., 1966, Effect of hydrocarbon solvent extraction on chloroplast membrane structure, J. Biol. Chem. 241:5197.PubMedGoogle Scholar
  56. Malkin, B., and Bearden, A. J., 1971, Primary reactions of photosynthesis: Photoreduction of a bound chloroplast ferredoxin at low temperature as detected by EPR spectroscopy, Proc. Natl. Acad. Sci. U.S.A. 68:16.PubMedCrossRefGoogle Scholar
  57. Malkin, R., and Bearden, A. J., 1973, Light induced changes of bound chloroplast plastocyanin as studied by EPR spectroscopy: The role of plastocyanin in noncyclic photosynthetic electron transport, Biochim. Biophys. Acta 292:169.PubMedCrossRefGoogle Scholar
  58. Malkin, S., and Kok, B., 1966, Fluorescence induction studies in isolated chloroplasts: Number of components involved in the reaction and quantum yield, Biochim. Biophys. Acta 126:413.PubMedCrossRefGoogle Scholar
  59. Malkin, R., Aparicio, R. J., and Arnon, D. I., 1974, The isolation and characterization of a new iron-sulfur protein from photosynthetic membranes, Proc. Natl. Acad. Sci. U.S.A. 71:2362.PubMedCrossRefGoogle Scholar
  60. McCarty, R. E., and Racker, E., 1968, Activation of ATPase and P32-ATP exchange in chloroplasts, J. Biol. Chem. 243:129.PubMedGoogle Scholar
  61. McCarty, R. E., and Fagan, J., 1973, Light stimulated incorporation of N-ethylmaleimide into CF1 in spinach chloroplasts, Biochem. J. 12:1503.CrossRefGoogle Scholar
  62. McEvoy, F. A., and Lynn, W. S., 1973, The peptides of chloroplast membranes: The soluble coupling factor (Ca2+-ATPase), Arch. Biochem. Biophys. 156:335.PubMedCrossRefGoogle Scholar
  63. Nakamura, S., and Kimura, T., 1971, Studies on spinach ferredoxin-nicotinamide adenine dinucleotide phosphate reductase, J. Biol. Chem. 246:6235.PubMedGoogle Scholar
  64. Nakamura, S., Kimura, T., and Chu, J. W., 1972a, Studies on aggregated multienzyme systems: Effects of basic proteins and phospholipids on oxidase reaction catalysed by flavoprotein-iron— sulfur protein complexes, FEBS Letts. 25:249.CrossRefGoogle Scholar
  65. Nakamura, S., Kazin, A. L., Wang, H. P., Chu, J. W., and Kimura, T., 1972b, Polyamine effect on NADPH oxidation catalyzed by spinach and adrenal flavoprotein-iron-sulfur protein complexes and a possible regulatory mechanism, FEBS Lett. 28:209.PubMedCrossRefGoogle Scholar
  66. Nelson, N., and Bengis, C., 1974, Reaction center P 700 from chloroplasts, Abstracts, Third International Congress on Photosynthesis, Rehovot, Israel, p. 70.Google Scholar
  67. Nelson, N., and Neuman, J., 1969, Interaction between ferredoxin and ferredoxin nicotinamide dinucleotide phosphate reductase in pyridine nucleotide reduction and some partial reactions, J. Biol. Chem. 244:1926.PubMedGoogle Scholar
  68. Nelson, N., and Racker, E., 1972, Purification of spinach cytochrome f and its photooxidation by resolved photosystem I particles, J. Biol. Chem. 247:3848.PubMedGoogle Scholar
  69. Nelson, N., Nelson, H., and Racker, E., 1972a, Magnesium dependent ATPase: Properties of the heat activated CF1 from chloroplasts, J. Biol. Chem. 247:6506.PubMedGoogle Scholar
  70. Nelson, N., Nelson, H., and Racker, E., 1972b, Purification and properties of an inhibitor isolated from chloroplast coupling factor 1, J. Biol. Chem. 247:7657.PubMedGoogle Scholar
  71. Nelson, N., Deters, D. W., Nelson, H., and Racker, E., 1973, Properties of the isolated subunits of CF1 from spinach chloroplasts, J. Biol. Chem. 248:2049.PubMedGoogle Scholar
  72. Ogawa, T., and Vernon, L. P., 1970, Properties of partially purified reaction centers from Scene-desmus mutant 6e and Anabaena variabilis grown in the presence of diphenylamine, Biochim. Biophys. Acta 197:292.PubMedCrossRefGoogle Scholar
  73. Ouitrakul, R., and Izawa, S., 1973, Electron transport and photophosphorylation in chloroplasts as a function of the electron acceptor: Acceptor-specific inhibition by KCN, Biochim. Biophys. Acta 304:105.Google Scholar
  74. Park, R. B., and Sane P. V., 1971, Distribution of function and structure on chloroplast lamellae, Annu. Rev. Plant Physiol. 22:395.CrossRefGoogle Scholar
  75. Plesnicar, M., and Bendall, D. S., 1970, The plastocyanin content of chloroplasts from some higher plants estimated by a sensitive enzymatic assay, Biochim. Biophys. Acta 216:192.PubMedCrossRefGoogle Scholar
  76. Pratt, L. H., and Bishop, N. I., 1968, Chloroplast reactions of photosynthetic mutants of Scenedemus obliquus, Biochim. Biophys. Acta 153:664.PubMedCrossRefGoogle Scholar
  77. Racker, E., Hauska, G. A., Lien, S., Berzborn, R. J., and Nelson, N., 1971, Resolution and reconstitution of the system of photophosphorylation, Second International Congress on Photosynthesis, Stresa, Vol. II, p. 1097.Google Scholar
  78. Ramshaw, J. A. M., Scawen, M. D., Bailey, C. J., and Boulter, D., 1974, Amino acid sequence of plastocyanin from Solanum tuberosum L. (potato), Biochem. J. 139:583.PubMedGoogle Scholar
  79. Regitz, G., and Ohad, I., 1974, Changes in the protein organization in developing thylakoids of Chlamydomonas reinhardi y–l as shown by sensitivity to trypsin, Abstracts, Third International Congress on Photosynthesis, Rehovot, Israel p. 76.Google Scholar
  80. Roy, H., and Moudrianakis, E. N., 1971, Interactions between ADP and the coupling factor of photophosphorylation, Proc. Natl. Acad. Sci. U.S.A., 68:464.PubMedCrossRefGoogle Scholar
  81. Ryrie, I. J., and Jagendorf, A. T., 1971, An energy linked conformational change in the coupling factor protein in chloroplasts, J. Biol. Chem. 246:3771.PubMedGoogle Scholar
  82. Schmid, G. H., and Radunz, A., Reactions of a monospecific antiserum to ferredoxin-NADP reductase with chloroplast preparations, Z. Naturforsch. 29C:384.Google Scholar
  83. Schneeman, R., Berg, S., and Krogmann, D. W., 1974, Polylysine and cyanide interactions with individual electron transport catalysts on the chloroplast membrane, Abstracts, Third International Congress on Photosynthesis, Rehovot, Israel, p. 80.Google Scholar
  84. Selman, R. B., and Bannister, T. T., 1971, Trypsin inhibition of photosystem II, Biochim, Biophys. Acta 253:428.CrossRefGoogle Scholar
  85. Selman, R. B., Giaquinta, R. T., and Dilley, R. A., 1974a, Effects of diazonium coupling on electron transfer in photosystem I, Arch. Biochem. Biophys. 162:210.PubMedCrossRefGoogle Scholar
  86. Selman, R. B., Johnson, G. L., and Dilley, R. A., 1974b, Diazonium benzene sulfonic acid incorporation into membrane bound versus soluble plastocyanin, Abstracts, Third International Congress on Photosynthesis, Rehovot, Israel, p. 82.Google Scholar
  87. Shin, M., 1973, Complex formation by ferredoxin-NADP reductase with ferredoxin or NADP, Biochim, Biophys. Acta 292:13.CrossRefGoogle Scholar
  88. Shoshan, E., Tel-Or, E., and Shavit, N., 1974, Interaction of membrane-bound coupling factor with whole and fragmented antibodies, Abstracts, Third International Congress on Photosynthesis, Rehovot, Israel p. 105.Google Scholar
  89. Singh, J., and Wasserman, A. R., 1971, The use of disc gel electrophoresis with non-ionic detergents in the purification of cytochrome f from spinach grana membranes, J. Biol. Chem. 246:3532.PubMedGoogle Scholar
  90. Stocking, C. R., and Larson, S., 1969, A chloroplast cytoplasmic shuttle and the reduction of extraplastid NAD, Biochem. Biophys. Res. Commun. 37:278.PubMedCrossRefGoogle Scholar
  91. Susor, W. A., and Krogmann, D. W., 1966, TPN photoreduction with cell-free preparations of Anabaena variabilis, Biochim. Biophys. Acta 120:65.PubMedCrossRefGoogle Scholar
  92. Tel-Or, E., Fuchs, S., and Avron, M., 1973, Antibodies to plant ferredoxins, FEBS Lett. 29:156.PubMedCrossRefGoogle Scholar
  93. Trebst, A., 1974, Energy conservation in photosynthetic electron transport of chloroplasts, Annu. Rev. Plant Physiol. 25:423.CrossRefGoogle Scholar
  94. Trebst,. A., Harth, E., and Draber, W., 1970, On a new inhibitor of photosynthetic electron-transport in isolated chloroplasts, Z. Naturforsch. 25b:1157.Google Scholar
  95. Tsuji, T., and Fujita, Y., 1973, Electron donor specificity observed in photosystem 1 reactions of membrane fragments of the blue-green alga Anabaena variabilis and the higher plant Spinacea oleracea, Plant Cell Physiol. 13:93.Google Scholar
  96. Weaver, E., 1968, EPR studies of free radicals in photosynthetic systems, Annu. Rev. Plant Physiol. 19:283.CrossRefGoogle Scholar
  97. Wildner, G. F., and Hauska, G. A., 1974, Localization and function of cytochrome 552 in Euglena gracilis, Abstracts, Third International Congress on Photosynthesis, Rehovot, Israel, p. 101.Google Scholar
  98. Witt, H. T., 1971, Coupling of quanta, electrons, fields, ions and phosphorylation in the functional membrane of photosynthesis, Q. Rev. Biophys. 4:365.PubMedCrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1976

Authors and Affiliations

  • David W. Krogmann
    • 1
  1. 1.Department of BiochemistryPurdue UniversityWest LafayetteUSA

Personalised recommendations