Photosynthesis Research

, Volume 25, Issue 2, pp 83–100 | Cite as

The mechanisms contributing to photosynthetic control of electron transport by carbon assimilation in leaves

  • Christine Foyer
  • Robert Furbank
  • Jeremy Harbinson
  • Peter Horton
Mini Review


‘Photosynthetic control’ describes the processes that serve to modify chloroplast membrane reactions in order to co-ordinate the synthesis of ATP and NADPH with the rate at which these metabolites can be used in carbon metabolism. At low irradiance, optimisation of the use of excitation energy is required, while at high irradiance photosynthetic control serves to dissipate excess excitation energy when the potential rate of ATP and NADPH synthesis exceed demand. The balance between ΔpH, ATP synthesis and redox state adjusts supply to demand such that the [ATP]/[ADP] and [NADPH]/[NADP+] ratios are remarkably constant in steady-state conditions and modulation of electron transport occurs without extreme fluctuations in these pools.

Key words

Photosynthesis Photosystem II Photosystem I Chlorophyll fluorescence Pi Benson-Calvin cycle metabolites 





Photosystem I


Photosystem II


inorganic phosphate


glycerate 3-phosphate




the bound quinone electron acceptor of PS II


Photochemical quenching of chlorophyll fluorescence associated with the oxidation of QA


non-photochemical quenching of chlorophyll fluorescence


non-photochemical quenching associated with the high energy state of the membrane




triose phosphate


intrinsic quantum yield of PS II


quantum yield of electron transport


quantum yield of CO2 assimilation


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Allen JF, Bennett J, Steinback KE and Arntzen CJ (1981) Chloroplast protein phosphorylation couples plastoquinone redox state to distribution of excitation energy between photosystems. Nature 291: 25–29Google Scholar
  2. Anderson JW, Foyer CH and Walker DA (1983) Light-dependent reduction of hydrogen peroxide by intact spinach chloroplasts. Biochim Biophys Acta 724: 69–74Google Scholar
  3. Amesz J, van den Engh GH and Visser JWM (1972) Reactions of plastoquinone and photosynthetic intermediates in intact algae and chloroplasts. In: Forti G, Avron M and Melandri A (eds) Proceedings of IInd International Congress on Photosynthetic Research. Dr W Junk, The Hague. pp 420–430Google Scholar
  4. Bendall DS (1982) Photosynthetic cytochromes of oxygenic organisms. Biochim Biophys Acta 683: 119–157Google Scholar
  5. Bennett J, Shaw EK and Michel H (1988) Cytochrome b 6f complex is required for phosphorylation of light-harvesting chlorophyll a/b complex II in chloroplast photosynthetic membranes. Eur J Biochem 171: 95–100Google Scholar
  6. Brooks A, Portis AR Jr and Sharkey TD (1988) Effects of irradiance and methyl viologen treatment on ATP, ADP and activation of ribulose bisphosphate carboxylase in spinach leaves. Plant Physiol 88: 850–853Google Scholar
  7. Demmig B, Winter K, Kruger A and Czygan FC (1987) Photoinhibition and zeaxanthin formation in intact leaves. A possible role of the xanthophyll cycle in the dissipation of excess light energy. Plant Physiol 84: 218–224Google Scholar
  8. Demmig-Adams D, Adams WW, Heber U, Neimanis S, Winter K, Kruger A, Czygan F-C, Bilger W and Bjorkman O (1990) Inhibition of zeaxanthin formation and of rapid changes in radiationless energy, dissipation by dithiothreitol in spinach leaves and chloroplasts. Plant Physiol 92: 293–301Google Scholar
  9. Dietz KJ and Foyer CH (1986) The relationship between phosphate status and photosynthesis in leaves. Reversibility of the effects of phosphate deficiency on photosynthesis. Planta 167: 376–381Google Scholar
  10. Dietz KJ and Heber U (1984) Rate-limiting factors in leaf photosynthesis 1. Carbon fluxes in the Calvin Cycle. Biochim Biophys Acta 767: 432–443Google Scholar
  11. Dietz KJ and Heber U (1986) Light and CO2 limitation of photosynthesis and states of the reactions regenerating ribulose-1,5-biophosphate and reducing 3-phosphoglycerate. Biochim Biophys Acta 848: 392–404Google Scholar
  12. Dietz KJ, Schreiber U and 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
  13. Dilley RA, Theg SM and Beard WA (1987) Membrane-proton interactions in chloroplast bioenergetics. Ann Rev Plant Physiol 38: 347–389Google Scholar
  14. Doncaster H, Adcock M and Leegood RC (1989) Regulation of photosynthesis in leaves of C4 plants following transition from high to low light. Biochim Biophys Acta 973: 176–184Google Scholar
  15. Falkowski PG, Kolber Z and Fujita Y (1988) Effect of redox state on the dynamics of photosystem II during steady-state photosynthesis in eukaryotic algae. Biochim Biophys Acta 933: 432–443Google Scholar
  16. Fernyhough P, Foyer CH and Horton P (1984) Increase in the level of thylakoid protein phosphorylation in maize mesophyll chloroplasts by decrease in the transthylakoid pH gradient. FEBS Lett 176: 133–138Google Scholar
  17. Foyer CH (1988) Feedback inhibition of photosynthesis through source-sink regulation in leaves. Plant Physiol Biochem 26: 483–492Google Scholar
  18. Foyer CH, Furbank RT and Walker DA (1989) Co-regulation of electron transport and Benson-Calvin cycle activity in isolated spinach chloroplasts. Studies on glycerate 3-phosphate reduction. Arch Biochem Biophys 268: 687–697Google Scholar
  19. Foyer CH and Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts. A proposed role in ascorbic acid metabolism. Planta 133: 21–25Google Scholar
  20. Furbank RT and Foyer CH (1986) Oscillations in levels of metabolites from the photosynthetic carbon reduction cycle in spinach leaf discs generated by the transition from air to 5% CO2. Arch Biochem Biophys 246: 240–244Google Scholar
  21. Furbank RT, Foyer CH and Walker DA (1987) Regulation of photosynthesis in isolated spinach chloroplasts during orthophosphate limitation. Biochim Biophys Acta 552–561Google Scholar
  22. Genty B, Briantais J-M and Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990: 87–92Google Scholar
  23. Giersch C, Heber U, Kobayashi Y, Inoue Y, Shibata K and Heldt HW (1980) Energy charge, phosphorylation potential and proton motive force in chloroplasts. Biochim Biophys Acta 590: 59–73Google Scholar
  24. Giersch C and Robinson SP (1987) Regulation of photosynthetic carbon metabolism during phosphate limitation of photosynthesis in isolated spinach chloroplasts. Photosyn Res 14: 211–227Google Scholar
  25. Haehnel W (1982) On the functional organisation of electron transport from plastoquinone to photosystem I. Biochem Biophys Acta 682: 245–257Google Scholar
  26. Haehnel W, Propper A and Krause H (1980) Evidence for platocyanin as the immediate electron donor to P700. Biochim Biophys Acta 593: 384–399Google Scholar
  27. Harbinson J and Hedley CL (1989) The kinetics of P700 reduction in leaves: a novel in situ probe of thylakoid functioning. Plant Cell Environ 12: 357–369Google Scholar
  28. Harbinson J and Woodward FI (1987) The use of light-induced absorbance changes at 820 nm to moniter the oxidation state of P700 in leaves. Plant Cell Environ 10: 131–140Google Scholar
  29. Heber U, Kirk MR and Boardman NK (1979) Photoreactions of cytochrome b 559and cyclic electron flow in photosystem II of intact chloroplasts. Biochim Biophys Acta 546: 292–306Google Scholar
  30. Heber U, Neimanis S, Dietz KJ and Uiil J (1986) Assimilatory power as a driving force in photosynthesis. Biochim Biophys Acta 852: 144–155Google Scholar
  31. Heldt HW, Chon C-J and Lorimer GH (1978) Phosphate requirement for the light activation of ribulose 1,5-bisphosphate carboxylase in intact spinach chloroplasts. FEBS Lett 92: 234–240Google Scholar
  32. Horton P (1983) Control of electron transport by the thylakoid protein kinase. FEBS Lett 152: 47–52Google Scholar
  33. Horton P (1985a) Interactions between electron transfer and carbon assimilation. In: Barber J and Baker NR (eds) Photosynthetic Mechanisms and the Environment, pp 135–187. Elsevier, Amsterdam, New YorkGoogle Scholar
  34. Horton P (1985b) Regulation of photochemistry and its interaction with carbon metabolism. In: Jeffcoat B, Hawkings AG and Stead AD (eds) Regulation of sources and sinks in crop plants. British Plant Growth Regulator Group, Monograph 12, 19–33. Long Ashton Research Station, BristolGoogle Scholar
  35. Horton P (1989) Interactions between electron transport and carbon assimilation: regulation of light harvesting and photochemistry. In: Briggs WR (ed) Photosynthesis. Alan Liss Inc, New York, pp 393–406Google Scholar
  36. Horton P and Black MT (1980) Activation of ATP-induced quenching of chlorophyll fluorescence by reduced plastoquinone. FEBS Lett 119: 141–144Google Scholar
  37. Horton P and Hague A (1988) Studies on the induction of chlorophyll fluorescence in barley protoplasts IV Resolution of non-photochemical quenching. Biochim Biophys Acta 932: 107–115Google Scholar
  38. Horton P, Crofts J, Gordon S, Oxborough K, Rees D and Scholes JD (1989a) Regulation of photosystem II by metabolic and environmental factors. Phil Trans Roy Soc Lond B 323: 269–279Google Scholar
  39. Horton P, Noctor G and Rees D (1989b) Regulation of light harvesting and electron transport in photosystem II. In: Zelitch I (ed) Perspectives in Biochemical and Genetic Regulation of Photosynthesis. Alan Liss Inc, New York, pp 145–158Google Scholar
  40. Horton P, Oxborough K, Rees D and Scholes JD (1988) Regulation of the photochemical efficiency of Photosystem II: consequences for the light response of field photosynthesis. Plant Physiol Biochem 26: 453–460Google Scholar
  41. Hossain MA, Nakano Y and Asada K (1984) Monodehydro-ascorbate reductase in spinach chloroplasts and its participation in regeneration of ascorbate for scavenging hydrogen peroxide. Plant Cell Physiol 25: 385–395Google Scholar
  42. Kyle DJ, Ohad I and Arntzen CJ (1985) Membrane protein damage and repair: selective loss of quinone protein function in chloroplast membranes. Proc Natl Acad Sci (U.S.A.) 81: 4070–4074Google Scholar
  43. Krause GH and Laasch H (1987) Energy-dependent chlorophyll fluorescence quenching in chloroplasts correlated with quantum yield of photosynthesis. Z Naturforsch 42c: 581–584Google Scholar
  44. Krause GH, Laasch H and Weis E (1988) Regulation of thermal dissipation of absorbed light energy in choroplasts indicated by energy-dependent fluorescence quenching. Plant Physiol Biochem 26: 445–452Google Scholar
  45. Mills JD and Mitchell P (1984) Thiol-modulation of the chloroplast proton motive ATPase and its effect on photophosphorylation. Biochim Biophys Acta 764: 93–104Google Scholar
  46. Noctor G and Mills JD (1987) Control of CO2 fixation during the induction period. The role of thiol-mediated enzyme activation in the alga Dunaliella. Biochim Biophys Acta 894: 295–303Google Scholar
  47. Noctor G and Mills JD (1988) Thiol-modulation of the thylakoid ATPase. Lack of oxidation of the enzyme in the presence of ΔμH+ in vivo and a possible explanation of the physiological requirement for thiol regulation of the enzyme. Biochim Biophys Acta 935: 53–60Google Scholar
  48. Noctor G and Horton P (1990) Uncoupler titration of energy dependent chlorophyll fluorescence quenching and photosystem II photochemical yield in intact pea chloroplasts. Biochem Biophys Acta 1016: 228–234Google Scholar
  49. Oxborough K and Horton P (1987) Characterisation of the effects of antimycin A upon high energy state quenching of chlorophyll fluorescence (qE) in spinach and pea chloroplasts. Photosyn Res 12: 119–128Google Scholar
  50. Oxborough K and Horton P (1988) A study of the regulation and function of energy-dependent quenching in pea chloroplasts. Biochim Biophys 934: 135–143Google Scholar
  51. Oxborough K, Lee P and Horton P (1987) Regulation of thylakoid protein phosphorylation by high energy state quenching. FEBS Lett 221: 211–214Google Scholar
  52. Parry M, Keys A, Foyer CH, Furbank RT and Walker DA (1988) Regulation of ribulose 1,5-bisphosphate carboxylase activity by the activase system in lysed spinach chloroplasts. Plant Physiol 87: 558–561Google Scholar
  53. Pearcy RW (1988) Photosynthetic utilization of sunflecks by understory plants. Aust J Plant Physiol 15: 223–238Google Scholar
  54. Peterson RB, Sivak MN and Walker DA (1988) Relationship between steady state fluorescence yield and photosynthetic efficiency in spinach leaf tissue. Plant Physiol 88: 158–163Google Scholar
  55. Powles SB (1984) Photoinhibition of photosynthesis induced by visible light. Ann Rev Plant Physiol 35: 15–44Google Scholar
  56. Quick WP and Horton P (1984) Studies on the induction of chlorophyll fluorescence in barley protoplasts. II Resolution of fluorescence quenching by redox state and the transthylakoid pH gradient. Proc R Soc Lond B220: 371–382Google Scholar
  57. Quick WP and Horton P (1986) Studies on the induction of chlorophyll fluorescence in barley protoplasts. III Correlation between changes in the level of glycerate 3-phosphate and the pattern of fluorescence quenching. Biochim Biophys Acta 849: 1–6Google Scholar
  58. Rebeille F and Hatch MD (1986a) Regulation of NADP-malate dehydrogenase in C4 plants. Effects of varying NADPH and NADP ratios and thioredoxin redox state on enzyme activity in reconstituted systems. Arch Biochem Biophys 249: 164–170Google Scholar
  59. Rebeille F and Hatch MD (1986b) Regulation of NADP-malate dehydrogenase in C4 plants. Relationships among enzyme activity, NADPH to NADP ratios and thioredoxin redox states in intact maize mesophyll chloroplasts. Arch Biochem Biophys 249: 171–179Google Scholar
  60. Rees D, Young A, Britton G and Horton P (1989) Enhancement of the ΔpH-dependent dissipation of excitation energy in spinach chloroplasts by light activation: correlation with the synthesis of zeaxanthin. FEBS Lett 256: 85–90Google Scholar
  61. Rees D and Horton P (1990) The mechanisms of changes in photosystem II efficiency in spinach thylakoids. Biochem Biophys Acta 1016: 219–227Google Scholar
  62. Rich P (1982) A physicochemical model of quinone-cytochrome b-c complex electron transfers. In: Trumpower BL (ed) Functions of Quinones in Energy Consuming Systems, pp 73–83. Academic Press, New YorkGoogle Scholar
  63. Robinson SP and Portis AR Jr (1988) Involvement of stromal ATP in the light activation of ribulose 1,5-bisphosphate carboxylase/oxygenase in intact isolated chloroplasts. Plant Physiol 86: 293–298Google Scholar
  64. Scheibe R and Stitt M (1988) Comparison of NADP-malate dehydrogenase activation, QA reduction and O2 evolution in spinach leaves. Plant Physiol Biochem 26: 473–481Google Scholar
  65. Schreiber U and Rienits KG (1986) ATP-induced photochemical quenching of variable chlorophyll fluorescence. FEBS Lett 211: 99–104Google Scholar
  66. Schreiber U, Schliwa W and Bilger U (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorimeter. Photosyn Res 10: 51–62Google Scholar
  67. Selman BR and Selman-Reimer S (1981) Steady-state kinetics of photophosphorylation. J Biol Chem 256: 1722–1726Google Scholar
  68. Sharkey TD, Berry JA and Sage RF (1989) Regulation of photosynthetic electron transport in Phaseolus vulgaris L as determined by room temperature chlorophyll a fluorescence. Planta 176: 415–424Google Scholar
  69. Sivak MN, Heber U and Walker DA (1985) Chlorophyll a fluorescence and light-scattering kinetics displayed by leaves during induction of photosynthesis. Planta 163: 419–423Google Scholar
  70. Sivak MN and Walker DA (1986) Photosynthesis in vivo can be limited by phosphate supply. New Phytol 102: 499–512Google Scholar
  71. Slovacek RE and Hind G (1980) Energetic factors affecting carbon dioxide fixation in isolated chloroplasts. Plant Physiol 65: 526–532Google Scholar
  72. Stiehl HH and Witt HT (1969) Quantitative treatment of the function of plastoquinone in photosynthesis. Z Naturforsch 246: 1588–1598Google Scholar
  73. Stitt M (1986) Limitation of photosynthesis by carbon metabolism I evidence for excess electron transfer capacity in leaves, carrying out photosynthesis in saturating light and CO2. Plant Physiol 81: 1115–1222Google Scholar
  74. Telfer A, Allen JF, Barber J and Bennett J (1983) Thylakoid protein phosphorylation during state 1-state 2 transitions in osmotically shocked pea chloroplasts. Biochim Biophys Acta 722: 176–181Google Scholar
  75. Tillberg JE, Giersch C and Heber U (1977) CO2 reduction by intact chloroplasts under a diminished proton gradient. Biochim Biophys Acta 461: 31–47Google Scholar
  76. Weis E, Ball JR and Berry J (1987) Photosynthetic control of electron transport in leaves of Phaseolus Vulgaris. Evidence for regulation of photosystem 2 by the proton gradient. In: Biggins J. (ed) Progress in Photosynthesis Research, Vol 2, pp 553–556. Martinus-Nijhoff Publishers, DordrechtGoogle Scholar
  77. Weis E and Berry J (1987) Quantum efficiency of photosystem II in relation to energy-dependent quenching of chlorophyll fluorescence. Biochim Biophys Acta 894: 198–208Google Scholar
  78. Woodrow IE and Berry JA (1985) Enzymatic regulation of photosynthetic CO2 fixation in C3 plants. Ann Rev Plant Physiol 39: 533–594Google Scholar
  79. Yamamoto HY (1979) Biochemistry of the violaxanthin cycle in higher plants. Pure and Appl Chem 51: 639–648Google Scholar

Copyright information

© Kluwer Academic Publishers 1990

Authors and Affiliations

  • Christine Foyer
    • 1
  • Robert Furbank
    • 2
  • Jeremy Harbinson
    • 3
  • Peter Horton
    • 4
  1. 1.Laboratoire du MétabolismeI.N.R.A.VersaillesFrance
  2. 2.Division of Plant IndustryC.S.I.R.O.CanberraAustralia
  3. 3.ATO/AgrotechnologieWageningenThe Netherlands
  4. 4.Robert Hill Intitute, Department of Molecular Biology and BiotechnologyUniversity of SheffieldSheffieldUK

Personalised recommendations