Abstract
Ionic environment is important in regulating photosynthetic reactions. The roles of cations, Mn2+, Mg2+, Ca2+, Na+, and K+ as cofactors in electron transport, energy transfer, phosphorylation, and carbon assimilation are better known than the roles of anions, except for chloride and bicarbonate. Only a limited information exists on the roles and effects of nitri formate, sulphate, and phosphate. In this review, we evaluate and highlight the roles of some specific anions on electron transport as well as on excitation energy transfer processes in photosynthesis. Anions exert significant effects on thyla membrane conformation and membrane fluidity, possibly by redistributing the thylakoid membrane surface charges. The anion/cation induced phase transitions in the hydrophilic domains of the thylakoid membranes are probably responsible for the various structural and co-related functional changes under stress. Anions are also important in regulation of energy distribution between the two photosystems. Anions do not only divert more energy from photosystem (PS) 2 to PS1, but can also reverse the effect of cations on energy distribution in a valence-dependent manner. Anions affect also the structure of the photosynthetic apparatus and excitation energy distribution between the two photosystems.
Similar content being viewed by others
References
Allakhverdiev, S.I., Yruela, I., Picorel, R., Klimov, V.V.: Bicarbonate is an essential constituent of the water oxidizing complex of photosystem II.-Proc. nat. Acad. Sci. USA 94: 5050-5054, 1997.
Andersson, B., Larsson, U.K., Sundby, C., Mäenpää, P., Bingsmark, S., Hundal, T.: Subfractional analysis of thylakoid membrane organisation and adaptation.-In: Barber, J., Malkin, R. (ed.): Techniques and New Developments in Photosynthesis Research. Pp. 511-521. Plenum Press, New York-London 1989.
Baranov, S.V., Ananyev, G.M., Klimov, V.V., Dismukes, G.C.: Bicarbonate accelerates assembly of the inorganic core of the water oxidising complex in manganese-depleted PSII: a proposed biogeochemical role for atmospheric carbon dioxide in oxygenic photosynthesis.-Biochemistry 39: 6060-6065, 2000.
Barber, J.: Ionic regulation in intact chloroplasts and its effect on primary photosynthetic processes.-In: Barber, J. (ed.): The Intact Chloroplast. Vol. 1. Pp. 89-134. Elsevier, Amsterdam-New York-Oxford 1976.
Barber, J.: An explanation for the relationship between salt-induced thylakoid stacking and the chlorophyll fluorescence changes associated with changes in spillover of energy from photosystem II to photosystem I.-FEBS Lett. 118: 1-10, 1980.
Barber, J.: Influence of surface charges on thylakoid structure and function.-Annu. Rev. Plant Physiol. 33: 261-295, 1982.
Barber, J.: Regulation of thylakoid membrane structure and function by surface transfer electrical charge.-In: Barber, J., Malkin, R. (ed.): Techniques and New Developments in Photosynthesis Research. Pp. 159-171. Plenum Press, New York-London 1989.
Barber, J., Chow, W.S.: A mechanism for controlling the stacking and unstacking of chloroplasts thylakoid membranes.-FEBS Lett. 105: 5-10, 1979.
Barber, J., Chow, W.S., Scoufflaire, C., Lannoye, R.: The relationship between thylakoid stacking and salt induced chlorophyll fluorescence changes.-Biochim. biophys. Acta 591: 92-103, 1980.
Barber, J., Telfer, A., Nicolson, J.: Evidence for divalent cation movement within isolated whole chloroplasts from studies with ionophore A23187.-Biochim. biophys. Acta 357: 161-165, 1974.
Bennett, J.: Regulation of photosynthesis by reversible phosphorylation of the light-harvesting chlorophyll a/b protein.-Biochem. J. 212: 1-13, 1983.
Bonaventura, C., Myers, J.: Fluorescence and oxygen evolution from Chlorella pyrenoidosa.-Biochim. biophys. Acta 189: 366-383, 1969.
Bose, S., Ramanujam, P.: Heterogeneity in Photosystem I. Evidence from cation-induced decrease in Photosystem I electron transport.-Biochim. biophys. Acta 764: 40-45, 1984.
Boucher, N., Harnois, J., Carpentier, R.: Heat stress stimulation of electron flow in a photosystem I submembrane fraction.-Biochem. Cell Biol. 68: 999-1004, 1990.
Braun, G., Malkin, S.: Regulation of the imbalance in light excitation between Photosystem II and Photosystem I by cations and by the energized state of the thylakoid membrane.-Biochim. biophys. Acta 1017: 79-90, 1990.
Cao, J., Ohad, N., Hirschberg, J., Xiong, J., Govindjee: Binding affinity of bicarbonate and formate in herbicide-resistant D1 mutants of Synechococcus sp. PCC 7942.-Photosynth. Res. 34: 397-408, 1992.
Cappellini, P., Turina, P., Fregni, V., Melandri, B.A.: Sulfite stimulates the ATP hydrolysis activity of but not proton translocation by the ATP synthase of Rhodobacter capsulatus and interferes with its activation by delta muH+.-Eur. J. Biochem. 248: 496-506, 1997.
Coleman, W.J., Baianu, I.C., Gutowsky, H.S., Govindjee: The effect of chloride and other anions on the thermal inactivation of oxygen evolution in spinach thylakoids.-In: Sybesma, C. (ed.): Advances in Photosynthesis Research. Vol. I. Pp. 283-286. Martinus Nijhoff/Dr W. Junk Publ., The Hague-Boston-Lancaster 1984.
Critchley, C.: The role of chloride in Photosystem II.-Biochim. biophys. Acta 811: 33-46, 1985.
Critchley, C., Baianu, I.C., Govindjee, Gutowsky, H.S.: The role of chloride in O2 evolution by thylakoids from salt-tolerant higher plants.-Biochim. biophys. Acta 682: 436-445, 1982.
Debus, R.J.: The manganese and calcium ions in photosynthetic oxygen evolution.-Biochim. biophys. Acta 1102: 269-352, 1992.
Diner, B., Petropeas, V., Wendoloski, J.J.: The iron-quinone electron-acceptor complex of photosystem II.-Physiol. Plant. 81: 423-436, 1991.
Diner, B.A., Petrouleas, V.: Formation by NO of nitrosyl adducts of redox components of the Photosystem II reaction center. II. Evidence that HCO3 −/CO2 binds to the acceptor-side non-heme iron.-Biochim. biophys. Acta 1015: 141-149, 1990.
Eaton Rye, J.J., Blubaugh, D.J., Govindjee: Action of bicarbonate on photosynthetic electron transport in the presence and absence of inhibitory anions.-In: Papageorgiou, G.C., Barber, J., Papa, S. (ed.): Ion Interactions in Energy Transfer Biomembranes. Pp. 263-278. Plenum Press, New York-London 1986.
El-Shintinawy, F., Govindjee: Bicarbonate effects in leaf discs from spinach.-Photosynth. Res. 24: 189-200, 1990.
El-Shintinawy, F., Xu, C., Govindjee: A dual bicarbonate-reversible formate effect in Chlamydomonas cells.-J. Plant Physiol. 136: 421-428, 1990.
Franzén, L.-G., Andréasson, L.-E.: Studies on manganese binding by selective solubilization of photosystem-II polypeptides.-Biochim. biophys. Acta 765: 166-170, 1984.
Good. N.E.: Uncoupling of the Hill reaction from photophosphorylation by anions.-Arch. Biochem. Biophys. 96: 653-661, 1962.
Good, N.E.: Carbon dioxide and the Hill reaction.-Plant Physiol. 38: 298-304, 1963.
Govindjee: Bicarbonate-reversible inhibition of plastoquinone reductase in photosystem II.-Z. Naturforsch. 48c: 251-258, 1993.
Govindjee: Sixty-three years since Kautsky: Chlorophyll a fluorescence.-Aust. J. Plant Physiol. 22: 131-160, 1995.
Govindjee, Baianu, I.C., Critchley, C., Gutowsky, H.S.: Comments on the possible roles of bicarbonate and chloride ions in PS II.-In: Inoue, Y., Crofts, A.R., Govindjee, Murata, N., Renger, G., Satoh, S. (ed.): The Oxygen Evolving System of Photosynthesis. Pp. 303-315. Academic Press, Tokyo 1983.
Govindjee, Pulles, M.P.J., Govindjee, R., van Gorkom, H.J., Duysens, L.N.M.: Inhibition of the reoxidation of the secondary electron acceptor of photosystem II by bicarbonate depletion.-Biochim. biophys. Acta 449: 602-605, 1976.
Govindjee, Robinson, H., Crofts, A.R., Van Rensen, J.J.S.: Bicarbonate does not influence electron transfer to the reaction center chlorophyll a of photosystem II. Measurement of chlorophyll a fluorescence rise in microseconds.-Naturwissenschaften 76: 119-121, 1989.
Govindjee, Van Rensen, J.J.S.: Bicarbonate effects on the electron flow in isolated broken chloroplasts.-Biochim. biophys. Acta 505: 183-213, 1978.
Govindjee, Weger, H.G., Turpin, D.H., Van Rensen, J.J.S., de Vos, O.J., Snel, J.F.H.: Formate releases carbon dioxide/bicarbonate from thylakoid membrane. Measurements by mass spectroscopy and infrared gas analyzer.-Naturwissenschaften 78: 168-170, 1991.
Gross, E.L.: Cation-induced increases in the rate of P700 recovery in Photosystem I particles.-Arch. Biochem. Biophys. 195: 198-204, 1979.
Gross, E.L., Hess, S.C.: Monovalent cation-induced inhibition of chlorophyll a fluorescence: Antagonism by divalent cations.-Arch. Biochem. Biophys. 159: 832-836, 1973.
Gross, E.L., Prasher, S.H.: Correlation between monovalent cation-induced decreases in chlorophyll a fluorescence and chloroplast structural changes.-Arch. Biochem. Biophys. 164: 460-468, 1974.
Haehnel, W., Hesse, V., Propper, A.: Electron transfer from plastocyanin to P700. Function of a subunit of photosystem I reaction center.-FEBS Lett. 111: 79-82, 1980.
Hind, G., Nakatani, H.Y., Izawa, S.: The role of Cl− ion in photosynthesis. I. The Cl− requirement of electron transport.-Biochim. biophys. Acta 172: 277-289, 1969.
Homann, P.H.: Cation effects on the fluorescence of isolated chloroplasts.-Plant Physiol. 44: 932-936, 1969.
Homann, P.H.: The association of functional anions with the oxygen-evolving center of chloroplasts.-Biochim. biophys. Acta 809: 311-319, 1985.
Homann, P.H.: The relations between the chloride, calcium and polypeptide requirements of photosynthetic water oxidation.-J. Bioenerg. Biomembr. 19: 105-123, 1987a.
Homann, P.H.: Cl− dependent binding of the extrinsic 23 kDa polypeptide at the water oxidizing site of chloroplast photosystem II.-In: Biggins, J. (ed.): Progress in Photosynthesis Research. Vol. 1. Pp. 657-660. Martinus Nijhoff Publ., Dordrecht-Boston-Lancaster 1987b.
Homann, P.H.: Structural effects of Cl− and other anions on the water oxidizing complex of chloroplast photosystem II.-Plant Physiol. 88: 194-199, 1988.
Homann, P.H.: Thermoluminiscence properties of the S2-state in chloride-depleted water oxidizing complexes after reconstituting treatments with various monovalent anions.-Photosynth. Res. 38: 395-400, 1993.
Homann, P.H., Inoue, Y.: The anion and calcium requirement of the photosynthetic water splitting complex.-In: Papageorgiou, G.C., Barber, J., Papa, S. (ed.): Ion Interactions in Energy Transfer Biomembranes. Pp. 279-290. Plenum Press, New York-London 1985.
Homann, P.H., Johnson, J.D., Pfister, V.R.: Interactions of protons with PS II.-In: Inoue, Y., Crofts, A.R., Govindjee, Murata, N., Renger, G., Satoh, K. (ed.): The Oxygen Evolving System of Photosynthesis. Pp. 283-292. Academic Press, Tokyo 1983.
Hutchison, R.S., Xiong, J., Sayre, R.T., Govindjee: Construction and characterization of a photosystem II mutant (argininew-269-glycine) of Chlamydomonas reinhardtii.-Biochim. biophys. Acta 1277: 83-92, 1996.
Inoue, H., Kitamura, T., Noguchi, M.: Heat inactivation of electron transport reactions in photosystem II particles.-Physiol. Plant. 71: 441-447, 1987.
Itoh, S.: Membrane surface potential and the reactivity of the system II primary electron acceptor to charged electron carriers in the medium.-Biochim. biophys. Acta 504: 324-340, 1978.
Itoh, S.: Surface potential and reaction of the membrane-bound electron transfer components. I. Reaction of P-700 in sonicated chloroplasts with redox reagents.-Biochim. biophys. Acta 548: 579-595, 1979a.
Itoh, S.: Surface potential and reaction of the membrane-bound electron transfer components. II. Integrity of the chloroplasts membrane and reaction of P-700.-Biochim. biophys. Acta 548: 596-607, 1979b.
Itoh, S., Uwano, S.: Characteristics of the Cl− action site in the O2 evolution reaction in PS II particles: electrostatic interaction with ions.-Plant Cell Physiol. 27: 25-36, 1986.
Ivanov, A.G., Velitchkova, M.Y.: Heat-induced changes in the efficiency of P700 photooxidation in pea chloroplast membranes.-J. Photochem. Photobiol. B4: 307-320, 1990.
Izawa, S., Good, N.E.: Effect of salts and electron transport on the conformation of isolated chloroplasts. I. Light-scattering and volume changes.-Plant Physiol. 41: 533-543, 1966a.
Izawa, S., Good, N.E.: Effect of salts and electron transport on the conformation of isolated chloroplasts. II. Electron microscopy.-Plant Physiol. 41: 544-552, 1966b.
Izawa, S., Muallem, A., Ramaswamy, N.K.: Chloride ion sensitive inactivation of oxygen evolving centres.-In: Inoue, Y., Crofts, A.R., Govindjee, Murata, N., Renger, G., Satoh, S. (ed.): The Oxygen Evolving System of Photosynthesis. Pp. 303-315. Academic Press, Tokyo 1983.
Jajoo, A., Bharti, S.: Effects of anions on photosystem 1-mediated electron transport in spinach chloroplasts.-J. exp. Bot. 44: 785-790, 1993.
Jajoo, A., Bharti, S.: On the participation of chloride in bicarbonate-induced reversal of anion inhibition of photosystem II electron transport in spinach thylakoids.-Physiol. Plant. 88: 78-84, 1993.
Jajoo, A., Bharti, S.: Possible role of anions in the regulation of energy distribution between the two photosystems.-Indian J. exp. Biol. 33: 67-72, 1995.
Jajoo, A., Bharti, S.: Interaction of anions and cations in regulating energy distribution between the two photosystems.-Photosynthetica 37: 529-535, 1999.
Jajoo, A., Bharti, S., Govindjee: Inorganic anions induce state changes in spinach thylakoid membrane.-FEBS Lett. 434: 193-196, 1998.
Jajoo, A., Dube, A., Bharti, S.: Mg2+-induced lipid phase transition in thylakoid membranes is reversed by anions.-Biochem. biophys. Res. Commun. 202: 1724-1730, 1994.
Jennings, R.C., Garlaschi, F.M., Gerola, P.D., Etzion-Katz, R., Forti, G.: Proton-induced grana formation in chloroplasts. Distribution of chlorophyll-protein complexes and photosystem II photochemistry.-Biochim. biophys. Acta 638: 100-107, 1981.
Jennings, R.C., Gerola, P.D., Forti, G., Garlaschi, F.M.: The influence of proton-induced grana formation on partial electron transport reactions in chloroplasts.-FEBS Lett. 106: 247-250, 1979.
Jursinic, P., Stemler, A.: Multiple anion effects on photosystem II in chloroplast membranes.-Photosynth. Res. 15: 41-56, 1988.
Jursinic, P.A., Stemler, A.: High rates of Photosystem II electron flow occur in maize thylakoids when the high-affinity binding site for bicarbonate is empty of all monovalent anions or has bicarbonate bound.-Biochim. biophys. Acta 1098: 359-367, 1992.
Jursinic, P., Warden, J., Govindjee: A major site of bicarbonate effect in System II reaction. Evidence from EST signal IIvf; fast fluorescence yield changes and delayed light emission.-Biochim. biophys. Acta 440: 322-330, 1976.
Katoh, S., San Pietro, A.: Ascorbate-supported NADP photoreduction by heated Euglena chloroplasts.-Arch. Biochem. Biophys. 122: 144-152, 1967.
Kelley, P.M., Izawa, S.: The role of chloride ion in photosystem II. I. Effects of chloride ion on photosystem II electron transport and on hydroxylamine inhibition.-Biochim. biophys. Acta 502: 198-210, 1978.
Khanna, R., Pfister, K., Keresztes, Á., Van Rensen, J.J.S., Govindjee: Evidence for a close spatial location of the binding sites for CO2 and for photosystem II inhibitions.-Biochim. biophys. Acta 634: 105-116, 1981.
Klimov, V.V., Baranov, S.V.: Bicarbonate requirement for the water-oxidising complex of photosystem II.-Biochim. Biophys. Acta 1475: 1-10, 2000.
Klimov, V.V., Baranov, S.V., Allakhverdiev, S.I.: Bicarbonate protects the donor side of PS II against photoinhibition and thermoinactivation.-FEBS Lett. 418: 243-246, 1997.
Klimov, V.V., Krasnovskiï, A.A.: Pheophytin as the primary electron acceptor in photosystem 2 reaction centres.-Photosynthetica 15: 592-609, 1981.
Krasnovsky, A.A.: The models of photosynthetic electron transfer.-Physiol. vég. 23: 611-618, 1985.
Krishnan, M., Mohanty, P.: Reactivation by chloride of Hill activity in heat-and tris-treated thylakoid membrane from Beta vulgaris.-Photosynth. Res. 5: 185-198, 1984.
Kuwabara, T., Murata, N.: Inactivation of photosynthetic oxygen evolution and concomitant release of three polypeptides in the photosystem II particles of spinach chloroplasts.-Plant Cell Physiol. 23: 533-539, 1982.
Lindberg, K., Andreasson, L.E.: A one-site, two-state model for the binding of anions in photosystem II.-Biochemistry 35: 14259-14267, 1996.
Makarova, V.V., Kukarskikh, G.P., Nizovskaya, N.V., Lavrukhina, O.G., Krendeleva, T.E.: Effect of nitrite on přimary photosynthetic processes in isolated chloroplasts of wheat grown under various conditions of nitrogen supply.-Biochemistry (Moscow) 63: 1414-1418, 1998.
Mano, J., Kawamoto, K., Dismukes, G.C., Asada, K.: Inhibition of the catalase reaction of Photosystem II by anions.-Photosynth. Res. 38: 433-440, 1993.
Marsho, T.V., Kok, B.: Photosynthetic regulation by cations in spinach chloroplasts.-Biochim. biophys. Acta 333: 353-365, 1974.
Mc Swain, B.D., Tsujimoto, H.Y., Arnon, D.I.: Effects of magnesium and chloride ions on light-induced electron transport in membrane fragments from a blue-green alga.-Biochim. biophys. Acta 423: 313-322, 1976.
Mohanty, P., Braun, B.Z., Zilinskas, Govindjee: Light-induced slow changes in chlorophyll a fluorescence in isolated chloroplasts: Effects of magnesium and phenazine methosulfate.-Biochim. biophys. Acta 292: 459-476, 1973.
Mohanty, P., Govindjee, Wydrzynski, T.: Salt-induced alterations of the fluorescence yield and of emission spectra in Chlorella pyrenoidosa.-Plant Cell Physiol. 15: 213-224. 1974.
Murai, T., Katoh, T.: Photosystem I-dependent oxidation of organic acids in blue-green alga, Anabaena variabilis.-Plant Cell Physiol. 16: 789-797, 1975.
Murakami, S., Packer, L.: The role of cations in the organization of chloroplast membranes.-Arch. Biochim. Biophys. 146: 337-347, 1971.
Murata, N.: Control of excitation transfer in photosynthesis. II. Magnesium ion-dependent distribution of excitation energy between two pigment systems in spinach chloroplasts.-Biochim. biophys. Acta 189: 171-181, 1969.
Murata, N.: Effects of monovalent cations on light energy distribution between two pigment systems of photosynthesis in isolated spinach chloroplasts.-Biochim. biophys. Acta 226: 422-432, 1971.
Nash, D., Miyao, M., Murata, N.: Heat inactivation of oxygen evolution in Photosystem II particles and its acceleration by chloride depletion and exogenous manganese.-Biochim. biophys. Acta 807: 127-133, 1985.
Papageorgiou, G.C.: Permeabilized cyanobacteria: A model system for photosynthetic and biotechnological studies.-In: Barber, J., Malkin, R. (ed.): Techniques and New Developments in Photosynthesis Research. Pp. 449-467. Plenum Press, New York-London 1989.
Papahadjopoulos, D., Vail, W.J., Newton, C., Nir, S., Jacobson, K., Poste, G., Lazo, R.: Studies on membrane fusion. III. The role of calcium-induced phase changes.-Biochim. biophys. Acta 465: 579-598, 1977.
Pick, U., Avron, M.: Inorganic sulfate and selenate as energy transfer inhibitors of photophosphorylation.-Biochim. biophys. Acta 325: 297-303, 1973.
Radda, G.K.: Dynamic aspects of membrane structure.-In: Parsons, D.S. (ed.): Biological Membranes. Pp. 81-95. Clarendon Press, Oxford 1975.
Ramanujam, P., Bose, S.: Correlation between thylakoid stacking and cation-induced decrease in photosystem I electron transport at saturating light intensity.-Arch. Biochem. Biophys. 221: 238-242, 1983.
Rashid, A., Homann, P.H.: Properties of iodide-activated photosynthetic water-oxidizing complexes.-Biochim. biophys. Acta 1101: 303-310, 1992.
Renger, G.: Mechanism of photosynthetic water cleavage.-In: Singhal, G.S., Renger, G., Sopory, S.K., Irrgang, K.-D., Govindjee (ed.): Concepts in Photobiology. Pp. 292-329. Narosa Publishing House, New Delhi-Madras-Bombay-Calcutta-London 1999.
Richter, M.L., Homann, P.H.: The involvement of amino groups in electron transfer between plastocyanin and P700 in Photosystem 1 subchloroplast particles.-Photobiochem. Photobiophys. 8: 125-131, 1984.
Robinson, H.H., Eaton Rye, J.J., Van Rensen, J.J.S., Govindjee: The effects of bicarbonate depletion and formate incubation on the kinetics of oxidation-reduction reactions of the PS II quinone acceptor complex.-Z. Naturforsch. 39c: 382-385, 1984.
Rutherford, A.W., Zimmermann, J.-L., Boussac, A.: Oxygen evolution.-In: Barber, J. (ed.): The Photosystems: Structure, Function and Molecular Biology. Pp. 179-229. Elsevier, Amsterdam-London-New York-Tokyo 1992.
Sabat, S.C., Mohanty, P.: Characterisation of heat stress induced stimulation of photosystem I electron transport activity in Amaranthus chloroplasts: effect of cations.-J. Plant Physiol. 133: 686-691, 1989.
Sinclair, J.: The influence of anions on oxygen evolution by isolated spinach chloroplast.-Biochim. biophys. Acta 764: 247-252, 1984.
Sinclair, J.: Changes in spinach thylakoid activity due to nitrite ions.-Photosynth. Res. 12: 255-263, 1987.
Snel, J.F.H., Van Rensen, J.J.S.: Reevaluation of the role of bicarbonate and formate in the regulation of photosynthetic electron flow in broken chloroplasts.-Plant Physiol. 75: 146-150, 1984.
Spiller, H., Böger, P.: Photosynthetic nitrite reduction by dithioerythritol and the effect of nitrite on electron transport in isolated chloroplasts.-Photochem. Photobiol. 26: 397-402, 1977.
Stemler, A.: Inhibition of Photosystem II by formate. Possible evidence for a direct role of bicarbonate in photosynthetic oxygen evolution.-Biochim. biophys. Acta 593: 103-112, 1980.
Stemler, A.: The functional role of bicarbonate in photosynthetic light reaction II.-In: Govindjee (ed.): Photosynthesis. Vol. II. Pp. 513-538. Academic Press, New York-London-Paris-San Diego-San Francisco-São Paulo-Sydney-Tokyo-Toronto 1982.
Stemler, A.: Carbonic anhydrase: molecular insights applied to photosystem II research in thylakoid membranes.-In: Lucas, W.J., Berry, J.A. (ed.): Inorganic Carbon Uptake by Aquatic Photosynthetic Organisms. Pp. 377-387. Amer. Soc. Plant Physiologists, Rockville 1985.
Stemler, A., Govindjee: Effect of bicarbonate ion on chlorophyll a fluorescence transients and delayed light emission from maize chloroplasts.-Photochem. Photobiol. 19: 227-232, 1973.
Stemler, A., Jursinic, P.: The effects of carbonic anhydrase inhibitors formate, bicarbonate, acetazolamide and imidozole on photosystem II in maize chloroplasts.-Arch. Biochem. Biophys. 221: 227-237, 1983.
Stemler, A., Murphy, J.: Determination of the binding constant of H14CO3 − to the photosystem II complex in maize chloroplasts: effects of inhibitors and light.-Photochem. Photobiol. 38: 701-707, 1983.
Stemler, A., Murphy, J.B.: Bicarbonate reversible and irreversible inhibition of PS II by monovalent anions.-Plant Physiol. 77: 974-977, 1985.
Stemler, A.J.: Bicarbonate and photosynthetic oxygen evolution: An unwelcome legacy of Otto Warburg.-Indian J. exp. Biol. 36: 841-848, 1998.
Sundby, C., Andersson, B.: Temperature-induced reversible migration along the thylakoid membrane of photosystem II regulates its association with LHC-II.-FEBS Lett. 191: 24-28, 1985.
Tamura, N., Yamamoto, Y., Nishimura, M.: Effect of surface potential on P-700 reduction in chloroplasts.-Biochim. biophys. Acta 592: 536-545, 1980.
Telfer, A., Barber, J., Nicolson, J.: Availability of monovalent and divalent cations within intact chloroplast for the action of ionophores nigercin and A23187.-Biochim. biophys. Acta 396: 301-309, 1975.
Thomas, P.G., Quinn, P.J., Williams, W.P.: The origin of photosystem I-mediated electron transport stimulation in heat stressed chloroplasts.-Planta 167: 133-139, 1986.
Tripathy, B.C., Draheim, J.E., Anderson, G.P., Gross, E.L.: Variable fluorescence of photosystem I particles and its application to the study of the structure and function of photosystem I.-Arch. Biochem. Biophys. 235: 449-60, 1984.
Vandermeulen, D.L., Govindjee: Relation of membrane structural changes to energy spillover in oat and spinach chloroplasts: Use of fluorescence probes and light scattering.-Biochim. biophys. Acta 368: 61-70, 1974.
Van Rensen, J.J.S., Xu, C., Govindjee: Role of bicarbonate in photosystem II, the water-plastoquinone oxido-reductase of plant photosynthesis.-Physiol. Plant. 105: 585-592, 1999.
Velthuys, B.R.: Electron-dependent competition between plastoquinone and inhibitor for binding to photosystem II.-FEBS Lett. 126: 277-281, 1981.
Warburg, O.: Schwerelemente als Wirkungsgruppen von Fermenten. 2nd Ed.-W. Saenger, Berlin 1948.
Warburg, O., Krippahl, G.: Hill-Reaktionen.-Z. Naturforsch. 13b: 509-514, 1958.
Warburg, O., Krippahl, G.: Notwendigkeit der Kohlensäure für die Chinon und Ferricyanid-Reaktionen in grünen Grana.-Z. Naturforsch. 15b: 367-369, 1960.
Warburg, O., Lüttgens, W.: Experiment zur Assimilation der Kohlensäure.-Naturwissenschaften 32: 161, 301, 1944.
Warburg, O., Lüttgens, W.: Fotokhimicheskoe vosstanevlenie khinona v zelenykh granulakh. [Photochemical reduction of quinone in green granules.]-Biokhimiya 11: 303-322, 1946. [In R.]
Wavare, R.A., Mohanty, P.: Cation-induced changes in fluorescence yield and emission of Synechococcus spheroplasts: Effects of monovalent, divalent and trivalent cations.-Proc. Indian nat. Sci. Acad. B51: 110-116, 1985.
Weis, E.: Light-and temperature-induced changes in the distribution of excitation energy between Photosystem I and Photosystem II in spinach leaves.-Biochim. biophys. Acta 807: 118-126, 1985.
Whitmarsh, J., Govindjee: The photosynthetic process.-In: Singhal, G.S., Renger, G., Sopory, S.K., Irrgang, K.-D., Govindjee (ed.): Concepts in Photobiology. Pp. 11-51. Narosa Publishing House, New Delhi-Madras-Bombay-Calcutta-London 1999.
Wincencjusz, H., Van Gorkom, H.J., Yocum, C.F.: The photosynthetic oxygen evolving complex requires chloride for its redox state S2→S3 and S3→S0 transitions but not for S0→S1 or S1→S2 transitions.-Biochemistry 36: 3663-3670, 1997.
Wong, D., Govindjee: Antagonistic effects of mono-and divalent cations on polarization of chlorophyll fluorescence in thylakoids and changes in excitation energy transfer.-FEBS Lett. 97: 373-377, 1979.
Wong, D., Govindjee, Merkelo, H.: Effects of bulk pH and of monovalent and divalent cations on Chl a fluorescence and electron tranport in pea thylakoid.-Biochim. biophys. Acta 592: 546-558, 1980.
Wong, D., Merkelo, H., Govindjee: Regulation of excitation transfer by cations: Wavelengths-resolved fluorescence life-times and intensities at 77 K in thylakoid membranes of pea chloroplasts.-FEBS Lett. 104: 223-226, 1979.
Wydrzynski, T., Govindjee: A new site for bicarbonate effect in photosystem II of photosynthesis: Evidence from chlorophyll fluorescence transients in spinach chloroplasts.-Biochim. biophys. Acta 387: 403-408, 1975.
Xiong, J., Hutchison, R.S., Sayre, R.T., Govindjee: Modification of the photosystem II acceptor side function in a D1 mutant (argininew-269-glycine) of Chlamydomonas reinhardtii.-Biochim. biophys. Acta 1322: 60-76, 1996.
Xiong, J., Minagawa, J., Crofts, A., Govindjee: Loss of inhibition by formate in newly constructed photosystem II D1 mutants, D1-R257E and D1-R257M, of Chlamydomonas reinhardtii.-Biochim. biophys. Acta 1365: 473-491, 1998.
Yamamoto, Y., Nishimura, M.: Organisation of the oxygen evolving enzyme complex in highly active oxygen evolving PS II preparation.-In: Inoue, Y., Crofts, A.R., Govindjee, Murata, N., Renger, G., Satoh, S. (ed.): The Oxygen Evolving System of Photosynthesis. Pp. 303-315. Academic Press, Tokyo 1983.
Yamashita, T., Butler, W.L.: Inhibition of chloroplasts by UV-irradiation and heat treatment.-Plant Physiol. 43: 2037-2040, 1968.
Yocum, C.F.: The calcium and chloride requirements for photosynthetic water oxidation.-In: Pecoraro, V.L. (ed.): Manganese Redox Enzymes. Pp. 71-83. VCH, NewYork 1992.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Jajoo, A., Bharti, S. & Mohanty, P. Evaluation of the Specific Roles of Anions in Electron Transport and Energy Transfer Reactions in Photosynthesis. Photosynthetica 39, 321–337 (2001). https://doi.org/10.1023/A:1015125008028
Issue Date:
DOI: https://doi.org/10.1023/A:1015125008028