, Volume 56, Issue 1, pp 139–149 | Cite as

On the quantitative relation between dark kinetics of NPQ-induced changes in variable fluorescence and the activation state of the CF0·CF1·ATPase in leaves

  • W.J. Vredenberg
Open Access


The variable fluorescence at the maximum Fm of the fluorescence induction (Kautsky) curve is known to be substantially suppressed shortly after light adaption due to nonphotochemical qE quenching. The kinetic pattern of the dark decay at Fm consists of three components with rates ~20, ~1, and ~0.1 s–1, respectively. Light adaptation has no or little effect on these rate constants. It causes a decrease in the ratio between the amplitudes of the slow and fast one with negligible change in the small amplitude of the ultra-slow component. Results add to evidence for the hypothesis that the dark-reversible decrease in variable fluorescence accompanying light adaptation during the P–S phase of the fluorescence induction curve is due to an alteration in nonphotochemical qE quenching caused by changes in the trans-thylakoid proton motive force in response to changes in the proton conductance gH+ of the CF0-channel of the CF0·CF1·ATPase.

Additional key words

CF0·F1·ATPase chlorophyll fluorescence kinetics nonphotochemical quenching Kautsky fluorescence induction curve quenching mechanisms system analysis 



cyclic electron transport involving PSI


subunits of chloroplasts ATPase


absorbance changes associated with the electrochromic band shift


fluorescence level of dark-adapted system with 100% open RCs


fluorescence level of dark-adapted system with 100% closed RCs after fluorescence saturating pulse excitation


the conductivity of the thylakoid membrane to protons, predominantly determined by the activity of the ATP synthase


H+ conductance of the closed CF0 channel of the CF0·F1·ATPase


H+ conductance of the open CF0 channel of the CF0·F1·ATPase


linear electron transport involving PSI and PSII


time range (~30 s) at which the final F-decline in the Kautsky induction curve starts


nonphotochemical quenching


Kautsky fluorescence induction curve


time range (~0.5–2 s) in Kautsky induction curve where stimulation of variable chlorophyll fluorescence F by pmf and release of photochemical and electrochemical quenching is maximal


proton motive force


reaction center of photosystem


time range (~15 s) in Kautsky induction curve where the contribution of the slow component of F-decay has become minimal


fluorescence saturating pulse with duration exceeding 3,000 ms


short fluorescence excitation light pulse with duration between 0.25 and 3,000 ms

3k (0.05k) pulse

light pulse with intensity 3,000 (50) μmol(photon) m–2 s–1


time range (> 2 min) in Kautsky induction curve where a (quasi) steady state in the light is reached


fraction of system with inactivated CF0·F1·ATPase


trans-membrane proton motive force


proton flux generated by light-driven proton pump


  1. Belyaeva N.E., Bulychev A.A., Riznichenko G.Y., Rubin A.B.: Thylakoid membrane model of the Chl a fluorescence transient and P700 induction kinetics in plant leaves.–Photosynth. Res. 130: 491–515, 2016CrossRefPubMedGoogle Scholar
  2. Bulychev A.A., Vredenberg W.J.: Modulation of photosystem II chlorophyll fluorescence by electrogenic events generated by photosystem I.–Bioelectrochemistry 54: 157–168, 2001.CrossRefPubMedGoogle Scholar
  3. Cardol P., De Paepe R., Franck F. et al.: The onset of NPQ and ΔμH+ upon illumination of tobacco plants studied through the influence of mitochondrial electron transport.–BBABioenergetics 1797: 177–188, 2010.CrossRefGoogle Scholar
  4. Chylla R.A., Whitmarsh J.: Inactive photosystem II complexes in leaves turnover rate and quantitation.–Plant Physiol. 90: 765–772, 1989.CrossRefPubMedPubMedCentralGoogle Scholar
  5. Cruz J.A., Sacksteder C.A., Kanazawa A., Kramer D.M.: Contribution of electric field (ΔΨ) to steady-state transthylakoid proton motive force (pmf) in vitro and in vivo. Control of pmf parsing into Δφ and ΔpH by ionic strength.–Biochemistry 40: 1226–1237, 2001.CrossRefPubMedGoogle Scholar
  6. Daisuke T., Amako K., Hashiguchi M. et al.: Chloroplastic ATPsynthase Functions as an H+-Gatekeeper to Prevent the Over-Reduction State in Photosystem I: H+-Efflux Management is Critical for the Regulation of Δph across the Thylakoid Membranes. Abstract 5A.12–In: 17th International Congress Photosynthesis (PS17). Pp. 238. Maastricht 2016.Google Scholar
  7. Ebenhöh O., Fucile G., Finazzi G. et al.: Short-term acclimation of the photosynthetic electron transfer to changing light: a mathematical model.–Philos. T. Roy. Soc. B 369: 20130223, 2014.CrossRefGoogle Scholar
  8. Harbinson J., Hedley C.L.: Changes in P-700 oxidation during the early stages of the induction of photosynthesis.–Plant Physiol. 103: 649–660, 1993.CrossRefPubMedPubMedCentralGoogle Scholar
  9. Horton P., Ruban A.V., Walters R.G.: Regulation of light harvesting in green plants.–Annu. Rev. Plant Phys. 47: 655–684, 1996.CrossRefGoogle Scholar
  10. Johnson M.P., Ruban A.V.: Rethinking the existence of a steadystate ΔΨ component of the proton motive force across plant thylakoid membranes.–Photosynth. Res. 119: 233–242, 2014.CrossRefPubMedGoogle Scholar
  11. Junge W.: Membrane potentials in photosynthesis.–Annu. Rev. Plant Physiol. 28: 503–536, 1977.CrossRefGoogle Scholar
  12. Kanazawa A., Kramer D.M.: In vivo modulation of nonphotochemical exciton quenching (NPQ) by regulation of the chloroplast ATP synthase.–P. Natl. Acad. Sci. USA 99: 12789–12794, 2002.CrossRefGoogle Scholar
  13. Ke B.: Photosynthesis photobiochemistry and photobiophysics.–In: {ieGovindjee, Sharkey T.D (ed.).: Advances in Photosynthesis and Respiration, Vol. 10. Kluwer Acad. Publ., Dordrecht 2001.Google Scholar
  14. Klughammer C., Siebke K., Schreiber U.: Continuous ECSindicated recording of the proton-motive charge flux in leaves.–Photosynth. Res. 117: 471–487, 2013.CrossRefPubMedPubMedCentralGoogle Scholar
  15. Kramer D.M., Crofts A.R.: Activation of the chloroplast ATPase measured by the electrochromic shift in leaves of intact plants.–BBA-Bioenergetics 976: 28–41, 1989.CrossRefGoogle Scholar
  16. Lazár D., Schansker G.: Modeling of chlorophyll a fluorescence transients.–In: Laisk A., Nedbal L., {ieGovindjee (ed.): Photosynthesis in Silico: Understanding Complexity from Molecules to Ecosystems. Pp. 85–123, Springer, Dordrecht 2009.CrossRefGoogle Scholar
  17. Lazár D.: Parameters of photosynthetic energy partitioning.–J. Plant Physiol. 175: 131–147, 2015.CrossRefPubMedGoogle Scholar
  18. Lill H., Junge W.: CF0, the proton channel of chloroplast ATP synthase.–Eur. J. Biochem. 179: 459–467, 1989.CrossRefPubMedGoogle Scholar
  19. Niyogi K.K., Li X.-P., Rosenberg V., Jung H.-S.: Is PsbS the site of nonphotochemical quenching in photosynthesis?–J. Exp. Bot. 56: 375–382, 2005.CrossRefPubMedGoogle Scholar
  20. Ort D.R., Oxborough K.: In situ regulation of chloroplast coupling factor activity.–Plant Physiol. 43: 269–291, 1992.Google Scholar
  21. Papageorgiou G.C., Govindjee: The nonphotochemical quenching of the electronically excited state of chlorophyll a in plants: definitions, timelines, viewpoints, open questions.–In: Demmig-Adams B., Garab G., Adams W.W., {ieGovindjee (ed.): Nonphotochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria. Advances in Photosynthesis and Respiration, Vol. 40, Pp. 1–44. Springer, Dordrecht 2014.Google Scholar
  22. Papageorgiou G.C., Govindjee (ed.): Chlorophyll a Fluorescence: a Signature of Photosynthesis, Advances in Photosynthesis and Respiration, Vol. 19, Springer, Dordrecht 2004.CrossRefGoogle Scholar
  23. Papageorgiou G.C., Tsimilli-Michael M., Stamatakis K.: The fast and slow kinetics of chlorophyll a fluorescence induction in plants, algae and cyanobacteria: a viewpoint.–Photosynth. Res. 94: 275–290, 2007.CrossRefPubMedGoogle Scholar
  24. Pascal A.A., Liu Z., Broess K., van Oort B. et al.: Molecular basis of photoprotection and control of photosynthetic lightharvesting.–Nature 436: 134–137, 2005.CrossRefPubMedGoogle Scholar
  25. Peters R.L.A., Bossen M., van Kooten O., Vredenberg W.J.: On the correlation between the activity of ATP-hydrolase and the kinetics of the flash-induced P515 electrochromic bandshift in spinach chloroplasts.–J. Bioenerg. Biomembr. 15: 335–346, 1983.CrossRefPubMedGoogle Scholar
  26. Peters R.L.A., van Kooten O., Vredenberg W.J.: The kinetics of the flash-induced P515 response in relation to the H+-permeability of the membrane bound ATPase in spinach chloroplasts.–J. Bioenerg. Biomembr. 17: 207–316, 1985.CrossRefPubMedGoogle Scholar
  27. Schreiber U., Klughammer C.: Analysis of photosystem I donor and acceptor sides with a new type of online-deconvoluting kinetic LED-array spectrophotometer.–Plant Cell Physiol. 57: 1454–1467, 2016.PubMedGoogle Scholar
  28. Shikanai T.: Regulatory network of proton motive force: contribution of cyclic transport around photosystem I.–Photosynth. Res. 129: 253–260, 2016.CrossRefPubMedGoogle Scholar
  29. Snellenburg J.J., Johnson M.P., Ruban A.V. et al: A four state parametric model for the kinetics of the nonphotochemical quenching in Photosystem II.–BBA-Bioenergetics 1858: 854–864, 2017.CrossRefPubMedGoogle Scholar
  30. Stirbet A., Govindjee: The slow phase of chlorophyll a fluorescence induction in silico: Origin of the slow S-M fluorescence rise.–Photosynth. Res. 130: 193–213, 2016.CrossRefPubMedGoogle Scholar
  31. Stirbet A., Govindjee, Strasser B.J., Strasser R.J.: Chlorophyll a fluorescence induction in higher plants: Modeling and numerical simulation.–J. Theor. Biol. 193: 131–151, 1998.CrossRefGoogle Scholar
  32. Strasser R.J., Srivastava A., Govindjee,: Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria.–Photochem. Photobiol. 61: 32–42, 1995.CrossRefGoogle Scholar
  33. Takizawa K., Kanazawa A., Kramer D.: Depletion of stromal Pi induces high’ energy-dependent’ antenna exciton’ quenching (qE) by decreasing proton conductivity at CF0-CF1 ATP synthase.–Plant Cell Environ. 31: 235–243, 2008.CrossRefPubMedGoogle Scholar
  34. Tikhonov A.N.: Induction events and short-term regulation of electron transport in chloroplasts: an overview.–Photosynth. Res. 125: 65–94 2015.CrossRefPubMedGoogle Scholar
  35. Tikkanen M., Aro E.A.: Integrative regulatory network of plant thylakoid energy transduction.–Trends Plant Sci. 19: 10–17, 2014.CrossRefPubMedGoogle Scholar
  36. van Grondelle R.: Excitation energy transfer, trapping and annihilation in photosynthetic systems.–BBA-Rev. Bioenerg. 811: 147–195, 1985.Google Scholar
  37. Vredenberg W.J.: A three-state model for energy trapping and chlorophyll fluorescence in photosystem II incorporating radical pair recombination.–Biophys. J. 79: 26–38, 2000.CrossRefPubMedPubMedCentralGoogle Scholar
  38. Vredenberg W.J.: Electrogenesis in the photosynthetic membrane: fields, facts and features.–Bioelectroch. Bioenerg. 44: 1–11, 1997.CrossRefGoogle Scholar
  39. Vredenberg W.J.: Kinetic analysis and mathematical modeling of primary photochemical and photoelectrochemical processes in plant photosystems.–Biosystems 103: 139–151, 2011.CrossRefGoogle Scholar
  40. Vredenberg W.J.: A simple routine for quantitative analysis of light and dark kinetics of photochemical and nonphotochemical quenching of chlorophyll fluorescence in intact leaves.–Photosynth. Res. 124: 87–106, 2015.CrossRefPubMedPubMedCentralGoogle Scholar
  41. Vredenberg W.J., Prášil O.: Modeling of chlorophyll a fluorescence kinetics in plant cells: derivation of a descriptive algorithm.–In: Laisk A, Nedbal L., {ieGovindjee (ed.): Photosynthesis in Silico: Understanding Complexity from Molecules to Ecosystems. Pp. 125–149. Springer, Dordrecht 2009.CrossRefGoogle Scholar
  42. Vredenberg W.J., Bulychev A.A.: Photoelectrochemical control of the balance between cyclic- and linear electron transport in photosystem I. Algorithm for P700+ induction kinetics.–BBABioenergetics 1797: 1521–1532, 2010.CrossRefGoogle Scholar
  43. Vredenberg W.J., Durchan M., Prášil O.: On the chlorophyll a fluorescence yield in chloroplasts upon excitation with twin turnover flashes (TTF) and high frequency flash trains.–Photosynth. Res. 93: 183–192, 2007.CrossRefPubMedGoogle Scholar
  44. Vredenberg W.J., Durchan M., Prášil O.: The analysis of PSII photochemical activity using single and multi-turnover excitations.–J. Photoch. Photobio. B 107: 45–54, 2012.CrossRefGoogle Scholar
  45. Witt H.T.: Energy conversion in the functional membrane of photosynthesis. Analysis by light pulse and electric pulse methods: The central role of the electric field.–BBA-Rev. Bioenerg. 505: 355–427, 1979.Google Scholar

Copyright information

© The Author(s) 2018

Open Access This article is distributed under the terms of the Creative Commons Attribution License which permits any use, distribution, and reproduction in any medium, provided the original author(s) and the source are credited.

Authors and Affiliations

  1. 1.Department of Plant PhysiologyWageningen UniversityWageningenThe Netherlands

Personalised recommendations