, Volume 52, Issue 4, pp 636–640 | Cite as

Proton concentration in the thylakoid membranes can regulate energy distribution between the two photosystems

  • T. Tongra
  • S. Bharti
  • A. Jajoo
Brief Communication


The aim of our study was to investigate the role of protons in regulating energy distribution between the two photosystems in the thylakoid membranes. Low pH-induced changes were monitored in the presence of a proton blocker, N,N′-dicyclohexylcarbodiimide (DCCD). When thylakoid membranes were suspended in a low-pH reaction mixture and incubated with DCCD, then a decrease in the fluorescence intensity of photosystem II (PSII) was observed, while no change in the intensity of photosystem I (PSI) fluorescence occurred according to the measured fluorescence emission spectra at 77 K. Since low pH induced distribution of energy from PSII to PSI was inhibited in the presence of DCCD, we concluded that pH/proton concentration of the thylakoid membranes plays an important role in regulating the distribution of the absorbed excitation energy between both photosystems.

Additional key words

light-harvesting complex luminal pH nonphotochemical quenching oxygen consumption oxygen evolution spinach 





nonphotochemical quenching


energy-dependent quenching


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Allen, J.F., Forsberg, J.: Molecular recognition in thylakoid structure and function.? Trends Plant Sci. 6: 317–326, 2001.PubMedCrossRefGoogle Scholar
  2. Azzi, A., Casey, R.P., Nalecz, M.J.: The effect of N,N′-dicyclohexylcarbodiimide on enzymes of bioenergetic relevance. — Biochim. Biophys. Acta 768: 209–226, 1984.PubMedCrossRefGoogle Scholar
  3. Bergantino, E., Segalla, A., Brunetta, A. et al.: Light and pH dependent structural changes in PsbS subunit of photosystem II. — P. Natl. Acad. Sci. USA 100: 15265–15270, 2003.CrossRefGoogle Scholar
  4. Cardol, P., Gloire, G., Havaux, M. et al.: Photosynthesis and state transitions in mitochondrial mutants of Chlamydomonas reinhardtii affected in respiration. — Plant Physiol. 133: 2010–2020, 2003.PubMedCentralPubMedCrossRefGoogle Scholar
  5. Horton, P., Johnson, M.P., Perez-Bueno, M.L. et al.: Photosynthetic acclimation: Does the dynamic structure and macroorganisation of photosystem II in higher plant grana membranes regulate light harvesting states? − FEBS J. 275: 1069–1079, 2008.PubMedCrossRefGoogle Scholar
  6. 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
  7. Horton, P., Wentworth, M., Ruban, A.: Control of the light harvesting function of chloroplast membranes: the LHCII-aggregation model for non-photochemical quenching II. — FEBS Lett. 579: 4201–4206, 2005.PubMedCrossRefGoogle Scholar
  8. Iwai, M., Yokono, M., Inada, N. et al.: Live-cell imaging of photosystem II antenna dissociation during state transitions. — P. Natl. Acad. Sci. USA 107: 2337–2342, 2010.CrossRefGoogle Scholar
  9. Jahns, P., Heyde, S.: Dicyclohexylcarbodiimide alters the pH dependence of violaxanthin de-epoxidation. — Planta 207: 393–400, 1999.CrossRefGoogle Scholar
  10. Jahns, P., Polle, A., Junge, W.: The photosynthetic water oxidase: its proton pumping activity is short-circuited within the protein by DCCD. — EMBO J. 7: 589–594, 1988.PubMedCentralPubMedGoogle Scholar
  11. Jajoo, A., Bharti, S., Govindjee.: Inorganic anions induce state changes in spinach thylakoid membranes. — FEBS Lett. 434: 193–196, 1998.PubMedCrossRefGoogle Scholar
  12. Jajoo, A., Szabom, M., Zsiros, O. et al.: Low pH induced structural reorganizations in thylakoid membranes of higher plants. — BBA-Bioenergetics 1817: 1388–1391, 2012.PubMedCrossRefGoogle Scholar
  13. Jajoo, A., Mekala, N.R., Tongra, T. et al.: Low pH-induced regulation of excitation energy between the two photosystems. — FEBS Lett. 588: 970–974,, 2014.PubMedCrossRefGoogle Scholar
  14. Johnson, M.P., Ruban, A.V.: Restoration of rapidly reversible photoprotective energy dissipation in the absence of PsbS protein by enhanced ΔpH. — J. Biol. Chem. 286: 19973–19981, 2011.PubMedCentralPubMedCrossRefGoogle Scholar
  15. Kereiche, S., Kiss, A.Z., Kouřil, R. et al.: The PsbS protein controls the macro-organisation of photosystem II complexes in the grana membranes of higher plant chloroplasts. — FEBS Lett. 584: 759–764, 2010.PubMedCrossRefGoogle Scholar
  16. Kiss, A.Z., Ruban, A.V., Horton, P.: The PsbS protein controls the organization of the photosystem II antenna in higher plant thylakoid membranes. — J. Biol. Chem. 283: 3972–3978, 2008.PubMedCrossRefGoogle Scholar
  17. Kramer, D.M., Sacksteder, C.A., Cruz, J.A.: How acidic is the lumen? — Photosynth. Res. 60: 151–163, 1999.CrossRefGoogle Scholar
  18. Lambrev, P.H., Nilkens, M., Miloslavina, Y. et al.: Kinetic and spectral resolution of multiple nonphotochemical quenching components in Arabidopsis leaves. — Plant Physiol. 152: 1611–1624, 2010.PubMedCentralPubMedCrossRefGoogle Scholar
  19. Li, X.P., Gilmore, A.M., Caffari, S. et al.: Regulation of photosynthetic light harvesting involves intra-thylakoid lumen pH sensing by the PsbS protein. — J. Biol. Chem. 279: 22866–22874, 2004.PubMedCrossRefGoogle Scholar
  20. Liu, C., Zhang, Y.J., Cao, D.R. et al.: Structural and functional analysis of the antiparallel strands in the lumenal loop of the major light-harvesting chlorophyll a/b complex of photosystem II (LHCII b) by site-directed mutagenesis. — J. Biol. Chem. 283: 487–495, 2008.PubMedCrossRefGoogle Scholar
  21. Minagawa, J.: State transitions-The molecular remodelling of photosynthetic super complexes that control energy flow in the chloroplasts. — BBA-Bioenergetics 1807: 897–905, 2011.PubMedCrossRefGoogle Scholar
  22. Mizutani, K., Yamamoto, M., Suzuki, K. et al.: Structure of the rotor ring modified with N,N′-dicyclohexylcarbodiimide of the Na+transporting vacuolar ATPase. — P. Natl. Acad. Sci. USA 108: 13474–13479, 2012.CrossRefGoogle Scholar
  23. Niyogi, K.K., Björkman, O., Grossman, A.R.: The roles of specific xanthophylls in photoprotection. — P. Natl. Acad. Sci. USA 94: 14162–14167, 1997.CrossRefGoogle Scholar
  24. Niyogi, K.K., Li, X.P., Rosenberg, V. et al.: Is PsbS the site of non-photochemical quenching in photosynthesis? — J. Exp. Bot. 56: 375–382, 2005.PubMedCrossRefGoogle Scholar
  25. Pogoryelov, D., Yildiz, O., Faraldo-Gomez, J.D. et al.: Highresolution structure of the rotor ring of a proton-dependent ATP synthase. — Nat. Struct. Mol. Biol. 16: 1068–1073, 2009.PubMedCrossRefGoogle Scholar
  26. Porra, R.J., Thompson, W.A., Kriedemann, P.E.: Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectrometry. — BBA-Bioenergetics 975: 384–394, 1989.CrossRefGoogle Scholar
  27. Roach, T., Krieger-Liszkay A.: The role of the PsbS protein in the protection of photosystems I and II against high light in Arabidopsis thaliana. — BBA-Bioenergetics 1817: 2158–2165, 2012.PubMedCrossRefGoogle Scholar
  28. Ruban, A.V., Pesaresi, P., Wacker, U. et al.: The relationship between the binding of dicyclohexylcarbodiimide and quenching of chlorophyll fluorescence in the light-harvesting proteins of photosystem II. — Biochemistry 37: 11586–11591, 1998.PubMedCrossRefGoogle Scholar
  29. Singh-Rawal, P., Jajoo, A., Mathur, S. et al.: Evidence that pH can drive state transitions in isolated thylakoid membranes from spinach. — Photoch. Photobio. Sci. 9: 830–837, 2010.CrossRefGoogle Scholar
  30. Tikkanen, M., Gollan, P.J., Suorsa, M. et al.: STN7 operates in retrograde signaling through controlling redox balance in the electron transfer chain. — Front. Plant Sci. 3: 1–11, 2012.CrossRefGoogle Scholar
  31. Tokutsu, R., Minagawa, J.: Energy-dissipative supercomplex of photosystem II associated with LHCSR3 in Chlamydomonas reinhardtii. — P. Natl. Acad. Sci. USA 110: 10016–10021, 2013.CrossRefGoogle Scholar
  32. Waloszek, A., Wieckowski, S.: Effects of pH on the kinetics of light-dependent proton flux in thylakoids isolated from lettuce leaves. — Plant Sci. 166: 479–483, 2004.CrossRefGoogle Scholar
  33. Walters, R.G., Ruban, A.V., Horton, P.: Identification of proton active residues in a higher plant light-harvesting complex. — P. Natl. Acad. Sci. USA 93: 14204–14209, 1996.CrossRefGoogle Scholar
  34. Wilk, L., Grunwald, M., Liao, P.N. et al.: Direct interaction of the major light-harvesting complex II and PsbS in nonphotochemical quenching. — P. Natl. Acad. Sci. USA 110: 5452–5456, 2013.CrossRefGoogle Scholar
  35. Wollman, F.A.: State transitions reveal the dynamics and flexibility of the photosynthetic apparatus. — EMBO J. 20: 3623–3630, 2001.PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© The Institute of Experimental Botany 2014

Authors and Affiliations

  1. 1.School of Life ScienceDevi Ahilya UniversityIndoreIndia

Personalised recommendations