Planta

, Volume 173, Issue 2, pp 267–274 | Cite as

Fractional control of photosynthesis by the QB protein, the cytochrome f/b6 complex and other components of the photosynthesic apparatus

  • U. Heber
  • S. Neimanis
  • K. -J. Dietz
Article

Abstract

In order to obtain information on fractional control of photosynthesis by individual catalysts, catalytic activities in photosynthetic electron transport and carbon metabolism were modified by the addition of inhibitors, and the effect on photosynthetic flux was measured using chloroplasts of Spinacia oleracea L. In thylakoids with coupled electron transport, light-limited electron flow to ferricyanide was largely controlled by the QB protein of the electron-transport chain. Fractional control by the cytochrome f/b6 complex was insignificant under these conditions. Control by the cytochrome f/b6 complex dominated at high energy fluence rates where the contribution to control of the QB protein was very small. Uncoupling shifted control from the cytochrome f/b6 complex to the QB protein. Control of electron flow was more complex in assimilating chloroplasts than in thylakoids. The contributions of the cytochrome f/b6 complex and of the QB protein to control were smaller in intact chloroplasts than in thylakoids. Thus, even though the transit time for an electron through the electron-transport chain may be below 5 ms in leaves, oxidation of plastohydroquinone was only partially responsible for limiting photosynthesis under conditions of light and CO2 saturation. The energy fluence rate influenced control coefficients. Fractional control of photosynthesis by the ATP synthetase, the cytochrome f/b6 complex and by ribulose-1,5-bisphosphate carboxylase increased with increasing fluence rates, whereas the contributions of the QB protein and of enzymes sensitive to SH-blocking agents decreased. The results show that the burdens of control are borne by several components of the photosynthetic apparatus, and that burdens are shifted as conditions for photosynthesis change.

Key words

Electron transport (photosynthesis) Light and electron transport Photosynthesis (light control) Spinacia (photosynthesis) QB protein-cytochrome of f/b6 complex 

Abbreviations

Chl

chlorophyll

DCMU

3-(3′,4′-dichlorophenyl)-1,1-dimethylurea

DNP-INT

2,4-dinitro phenylether of 2-iodo-4-nitrothymol

pCMBS

p-chloromercuribenzosulfonate

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Bendall, D.S. (1982) Photosynthetic cytochromes of oxygenic organisms. Biochim. Biophys. Acta 683, 119–151Google Scholar
  2. Buchanan, B.B. (1980) Role of light in the regulation of chloroplast enzymes. Annu. Rev. Plant Physiol. 31, 341–374Google Scholar
  3. Dietz, K.-J. (1986) An evaluation of light and CO2 limitation of leaf photosynthesis by CO2 gas exchange analysis. Planta 167, 260–263Google Scholar
  4. Dietz, K.-J., Foyer, C. (1986) The relationship between phosphate status and photosynthesis in leaves. Reversibility of the effects of phosphate deficiency on photosynthesis. Planta 167, 376–381Google Scholar
  5. Dietz, K.-J., Heber, U. (1984) Rate-limiting factors in leaf photosynthesis. I. Carbon fluxes in the Calvin cycle. Biochim. Biophys. Acta 767, 432–443Google Scholar
  6. Dietz, K.-J., Neimanis, S., Heber, U. (1984) Rate-limiting factors in leaf photosynthesis. II. Electron transport. Biochim. Biophys. Acta 767, 444–450Google Scholar
  7. Dietz, K.-J., Schreiber, U., Heber, U. (1985) The relationship between the redox state of QA and photosynthesis in leaves at various carbon dioxide, oxygen and light regimes. Planta 166, 219–226Google Scholar
  8. Good, N.E., Izawa, S. (1973) Inhibition of photosynthesis. In: Metabolic inhibitors, vol. IV, pp 179–214, Hochster, R.M., Quastel, J.H., eds. Academic Press, New YorkGoogle Scholar
  9. Hachnel, W. (1984) Photosynthetic electron transport in higher plants. Annu. Rev. Plant Physiol. 35, 659–693Google Scholar
  10. Hauska, G., Hurt, E., Gabellini, N., Lockau, W. (1983) Comparative aspects of quinol-cytochrome c/plastocyanin oxidoreductases. Biochim. Biophys. Acta 726, 97–133Google Scholar
  11. Heber, U., Boardman, N.K., Anderson, J.M. (1976a) Cytochrome b 563 redox changes in intact CO2-fixing spinach chloroplasts and in developing pea chloroplasts. Biochim. Biophys Acta 423, 275–292Google Scholar
  12. Heber, U., Boardman, N.K., Anderson, J.M. (1976b) Effects of pH and oxygen on photosynthetic reactions of intact chloroplasts. Plant Physiol. 57, 277–283Google Scholar
  13. Heber, U., Neimanis, S., Dietz, K.-J., Viil, J. (1986) Assimilatory power as a driving force in photosynthesis. Biochim. Biophys. Acta 852, 144–155Google Scholar
  14. Heber, U., Santarius, K.A. (1970) Direct and indirect transport of ATP and ADP across the chloroplast envelope. Z. Naturforsch. 25b, 718–728Google Scholar
  15. Hill, R., Hartree, E.F. (1953) Hematin compounds in plants. Annu. Rev. Plant Physiol. 4, 115–150Google Scholar
  16. Izawa, S., Good, N.E. (1965) The number of sites sensitive to 3-(3,4-dichlorophenyl)-1,1-dimethylurea, 3-(4-chlorophenyl)-1,1-dimethylurea and 2-chloro-4-(2-propylamino)-6-ethylamino-s-triazine in isolated chloroplasts. Biochim. Biophys. Acta 102, 20–38Google Scholar
  17. Izawa, S., Winget, G.D., Good, N.E. (1966) Phlorizin, a specific inhibitor of photophosphorylation and phosphorylationcoupled electron transport in chloroplasts. Biochem. Biophys. Res. Comm. 22, 223–226Google Scholar
  18. Jensen, R.G., Bassham, J.A. (1966) Photosynthesis by isolated chloroplasts. Proc. Natl. Acad. Sci. USA 56, 1095–1101Google Scholar
  19. Kacser, H., Burns, J.A. (1979) Molecular democracy: Who shares the controls? Biochem. Soc. Trans. 7, 1149–1160Google Scholar
  20. Laasch, H., Pfister, K., Urbach, W. (1982) High- and lowaffinity binding of photosystem II-herbicides to isolated thylakoid membranes and intact algal cells. Z. Naturforsch. 37c, 620–631Google Scholar
  21. Laisk, A., Walker, D.A. (1986) Control of phosphate turnover as a rate-limiting factor and possible cause of oscillations in photosynthesis: A mathematical model. Proc. R. Soc. London, Ser. B 227, 281–302Google Scholar
  22. Leegood, R.C., Kobayshi, Y., Neimanis, S., Walker, D.A., Heber, U. (1982) Cooperative activation of chloroplast fructose-1,6-bisphosphatase by reductant, pH and substrate. Biochim. Biophys. Acta 682, 168–178Google Scholar
  23. Li, Y.S., Gibbs, M. (1985) Pyridoxal phosphate and 3-phosphoglycerate overcome the D,l-glyceraldehyde inhibition of carbon dioxide fixation by intact chloroplasts. Plant Physiol. 77, 42Google Scholar
  24. Madsen, N.B. (1963) Mercaptide forming agents. In Metabolic inhibitors, vol 2, pp. 119–143, Hochster, R.M., Quastel, J.H., eds. Academic Press, New YorkGoogle Scholar
  25. McCarty, R.E. (1980) Deineation of the mechanism of ATP synthesis in chloroplasts: use of uncoplers, energy transfer inhibitors, and modifiers of coupling factor I. Methods Enzymol. 69, 719–728Google Scholar
  26. Ohmori, M., Gimmler, H., Schreiber, U., Heber, U. (1985) Relative insensitivity of photosynthesis to the dissipation of a transthylakoid proton gradient in intact chloroplasts. Physiol. Vég. 23, 801–812Google Scholar
  27. Sharkey, T.D., Stitt, M., Heinecke, D., Gerhardt, R., Raschke, K., Heldt, H.W. (1986) Limitation of photosynthesis by carbon metabolism. II. Oxygen insensitive CO2 uptake results from limitation of triosephosphate utilization. Plant Physiol. 81, 1123–1129Google Scholar
  28. Sivak, M.N., Walker, D.A. (1986) Photosynthesis in vivo can be limited by phosphate supply. New Phytol. 102, 499–512Google Scholar
  29. Slabas, A.R., Walker, D.A. (1978) Inhibition of spinach phosphoribulokinase by D,l-glyceraldehyde. Biochem. J. 153, 613–619Google Scholar
  30. Stitt, M. (1986) Limitation of photosynthesis by carbon metabolism. I. Evidence for excess electron transport capacity in leaves carrying out photosynthesis in saturating light and CO2. Plant Physiol. 81, 1115–1122Google Scholar
  31. Stitt, M. (1987) Limitation of photosynthesis by sucrose synthesis. In: Progress in photosynthesis research, vol. 3, pp. 685–692, Biggins, J., ed. Martinus Nijhoff Publishers, Dordrecht Boston LancasterGoogle Scholar
  32. Takahama, U., Shimidzu-Takahama, M., Heber, U. (1981) The redox state of the NADP system in illuminated chloroplasts. Biochim. Biophys. Acta 637, 530–539Google Scholar
  33. Trebst, A. (1980) Inhibitors in electron flow: Tools for the functional and structural localization of carriers and energy conservation sites. Methods Enzymol. 69, 675–715Google Scholar
  34. Trebst, A., Wietoska, H., Draber, W., Knops, H.J. (1978) The inhibition of photosynthetic electron flow in chloroplasts by the dinitrophenylether of bromo-or iodo-nitrothymol. Z. Naturforsch. 33c, 919–927Google Scholar
  35. von Caemmerer, S., Farquhar, G.D. (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153, 376–387Google Scholar
  36. Witt, H.T. (1979) Energy conversion in the functional membrane of photosynthesis. Analysis by light pulse and electric pulse methods. Biochim. Biophys. Acta 505, 355–427Google Scholar
  37. Wishnick, M., Lane, M.D. (1971) Ribulose diphosphate carboxylase from spinach leaves. Methods Enzymol. 23, 570–577Google Scholar
  38. Woodrow, I.E. (1986) Control of the rate of photosynthetic carbon dioxide fixation. Biochim. Biophys. Acta 851, 181–192Google Scholar
  39. Woodrow, I.E., Ball, J.T., Berry, J.A. (1986) A general expression for the control of the rate of photosynthetic CO2 fixation by stomata, the boundary layer and radiation exchange. In: Progress in photosynthesis research, vol. 4, pp. 225–228, Biggins, J. ed. Martinus Nijhoff Publishers, Dordrecht Boston LancasterGoogle Scholar

Copyright information

© Springer-Verlag 1988

Authors and Affiliations

  • U. Heber
    • 1
  • S. Neimanis
    • 1
  • K. -J. Dietz
    • 1
  1. 1.Institute of Botany and Pharmaceutical Biology of the UniversityWürzburgGermany

Personalised recommendations