Study of the Effect of Ion Channel Modulators on Photosynthetic Oxygen Evolution

Various ion channel activities can be recorded by electrophysiological methods in the outer and inner envelope membranes of chloroplasts as well as in the thylakoid membrane. However, most of these channels are poorly characterized from a pharmacological point of view. Furthermore, the molecular identity has been determined only for a few of them, preventing an understanding of their role in plant physiology. By allowing specific ion fluxes across plastidial membranes, these ion channels may either directly or indirectly regulate photosynthesis, as has been hypothesized earlier. We have determined the effect of various ion channel modulators [indole-3-acetic acid, 5-nitro-2-(3-phenylpropylamino)-benzoate, (-)-epigallocatechin-3-gallate, p-chlorophenoxyacetic acid, Konig's polyanion, Cs+, Gd3+, 4-aminopyridine, tetraethylammonium chloride, charybdotoxin, nimodipine, and cyclosporin A] on the efficiency of photosynthetic oxygen evolution in intact chloroplasts, broken chloroplasts, and isolated thylakoids. The data may improve our understanding of chloroplast ion channels and identifies inhibitors which may be exploited for electrophysiological studies.

[1]  A. Bulychev,et al.  Patch-clamp studies of light-induced currents across the thylakoid membrane of isolated chloroplasts , 1992 .

[2]  Michael Pennington,et al.  K+ channels as targets for specific immunomodulation. , 2004, Trends in pharmacological sciences.

[3]  B. Fuks,et al.  A Voltage-dependent Porin-like Channel in the Inner Envelope Membrane of Plant Chloroplasts (*) , 1995, The Journal of Biological Chemistry.

[4]  Influences of the N- and C-Termini of the Distal Nephron Inward Rectifier, ROMK , 2001, Kidney and Blood Pressure Research.

[5]  G. Ananyev,et al.  Remarkable affinity and selectivity for Cs+ and uranyl (UO22+) binding to the manganese site of the apo-water oxidation complex of photosystem II. , 1999, Biochemistry.

[6]  F. L. Crane,et al.  Ca2+ and calmodulin antagonists inhibit the proton gradients associated with non-cyclic and cyclic photophosphorylation in spinach chloroplasts. , 1982, Biochemical and biophysical research communications.

[7]  G. Ben-Hayyim.  Mg2+ translocation across the thylakoid membrane: studies using the ionophore A 23187. , 1978, European journal of biochemistry.

[8]  I. Pottosin,et al.  Patch-clamp study of vascular plant chloroplasts: Ion channels and photocurrents , 1995, Journal of bioenergetics and biomembranes.

[9]  A. Bock,et al.  Cl- channel inhibitors of the arylaminobenzoate type act as photosystem II herbicides: a functional and structural study. , 2001, Biochemistry.

[10]  A. Bulychev,et al.  Micro-electrode Measurements of the Transmembrane Potential of Chloroplasts and its Photoinduced Changes , 1972, Nature.

[11]  S. Campello,et al.  Plant polyphenols inhibit VacA, a toxin secreted by the gastric pathogen Helicobacter pylori , 2003, FEBS letters.

[12]  J. Jackson,et al.  The Development of Electrochemical Potential Gradients across Photosynthetic Membranes , 1982 .

[13]  D. Arnon.  COPPER ENZYMES IN ISOLATED CHLOROPLASTS. POLYPHENOLOXIDASE IN BETA VULGARIS. , 1949, Plant physiology.

[14]  W. Junge,et al.  The slow rise of the flash-light-induced alkalization by Photosystem II of the suspending medium of thylakoids is reversibly related to thylakoid stacking , 1986 .

[15]  K. Walsh,et al.  Structural and ionic determinants of 5‐nitro‐2‐(3‐phenylpropylamino)‐benzoic acid block of the CFTR chloride channel , 1999, British journal of pharmacology.

[16]  Keiji Naruse,et al.  Molecular identification of a eukaryotic, stretch-activated nonselective cation channel. , 1999, Science.

[17]  A. Rubin,et al.  Effects of calcium-channel blockers and activator on electron transport in pea chloroplasts , 1989 .

[18]  R. Heath,et al.  The stimulation of CO2-supported O2 evolution in intact spinach chloroplasts by ammonium ion. , 1978, Archives of biochemistry and biophysics.

[19]  M. Goldsmith,et al.  Rapid response of the plasma-membrane potential in oat coleoptiles to auxin and other weak acids , 1983, Planta.

[20]  G. Berkowitz,et al.  Characterization of a Chloroplast Inner Envelope K+ Channel , 1994, Plant physiology.

[21]  R. Hedrich,et al.  A voltage-dependent chloride channel in the photosynthetic membrane of a higher plant , 1988, Nature.

[22]  G. Schönknecht,et al.  Patch clamp study of the voltage-dependent anion channel in the thylakoid membrane , 1995, The Journal of Membrane Biology.

[23]  R. Rappuoli,et al.  Formation of anion‐selective channels in the cell plasma membrane by the toxin VacA of Helicobacter pylori is required for its biological activity , 1999, The EMBO journal.

[24]  R. Wagner,et al.  Ion channels in the thylakoid membrane (a patch-clamp study) , 1993 .

[25]  V. Vambutas.  Ion Fluxes across Nonenergized Membranes of Chloroplasts a , 1984 .

[26]  W. Downton,et al.  Potassium, sodium, and chloride content of isolated intact chloroplasts in relation to ionic compartmentation in leaves. , 1984, Archives of biochemistry and biophysics.

[27]  M. Zoratti,et al.  Gadolinium ion inhibits loss of metabolites induced by osmotic shock and large stretch-activated channels in bacteria. , 1992, European journal of biochemistry.

[28]  A. Messina,et al.  Novel aspects of the electrophysiology of mitochondrial porin. , 1998, Biochemical and biophysical research communications.

[29]  M. Blatt,et al.  K+ channels of stomatal guard cells: bimodal control of the K+ inward-rectifier evoked by auxin. , 1994, The Plant journal : for cell and molecular biology.

[30]  F. Orallo,et al.  (−)-Epigallocatechin-3-gallate induces contraction of the rat aorta by a calcium influx-dependent mechanism , 2004, Naunyn-Schmiedeberg's Archives of Pharmacology.

[31]  M. Zoratti,et al.  The inner mitochondrial membrane contains ion‐conducting channels similar to those found in bacteria , 1989, FEBS letters.

[32]  M. Zoratti,et al.  The giant channel of the inner mitochondrial membrane is inhibited by cyclosporin A. , 1991, The Journal of biological chemistry.

[33]  N. Murata.  Effects of monovalent cations on light energy distribution between two pigment systems of photosynthesis in isolated spinach chloroplasts. , 1971, Biochimica et biophysica acta.

[34]  R. Hedrich,et al.  Plant growth hormones control voltage-dependent activity of anion channels in plasma membrane of guard cells , 1991, Nature.

[35]  C. Gasser,et al.  Cloning and characterization of chloroplast and cytosolic forms of cyclophilin from Arabidopsis thaliana. , 1994, The Journal of biological chemistry.

[36]  R. Wagner,et al.  Thylakoid membranes contain a high-conductance channel. , 1998, European journal of biochemistry.

[37]  I. Szabó,et al.  Localization of a putative ClC chloride channel in spinach chloroplasts , 2005, FEBS letters.

[38]  J. Barber,et al.  Structure of photosystem II and molecular architecture of the oxygen-evolving centre. , 2004, Current opinion in structural biology.

[39]  E. Bergantino,et al.  Light- and pH-dependent structural changes in the PsbS subunit of photosystem II , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[40]  R. Carpentier,et al.  Inhibitors affecting the oxidizing side of photosystem II at the Ca2+- and Cl−-sensitive sites , 1985 .

[41]  James Barber,et al.  Architecture of the Photosynthetic Oxygen-Evolving Center , 2004, Science.

[42]  C. Andreo,et al.  Divalent‐cation ionophores and Ca2+ transport in spinach chloroplasts , 1975, FEBS letters.

[43]  Charles R. Yang,et al.  Dopamine D1/D5 Receptor Modulates State-Dependent Switching of Soma-Dendritic Ca2+ Potentials via Differential Protein Kinase A and C Activation in Rat Prefrontal Cortical Neurons , 2004, The Journal of Neuroscience.

[44]  D. Deamer,et al.  Light-dependent anion transport in isolated spinach chloroplasts. , 1969, Biochimica et biophysica acta.

[45]  P. Bernardi,et al.  Properties of the Permeability Transition Pore in Mitochondria Devoid of Cyclophilin D* , 2005, Journal of Biological Chemistry.

[46]  D. Walker,et al.  CO2-dependent Oxygen Evolution by Envelope-free Chloroplasts , 1971, Nature.

[47]  E. Gross.  Divalent cation binding to chloroplast membranes and its relationship to reversal of quaternary ammonium salt uncoupling of photophosphorylation. , 1972, Archives of biochemistry and biophysics.

[48]  P. Wangemann,et al.  Cl−-channel blockers in the thick ascending limb of the loop of Henle Structure activity relationship , 2004, Pflügers Archiv.

[49]  J. Soll,et al.  A High-Conductance Solute Channel in the Chloroplastic Outer Envelope from Pea , 1998, Plant Cell.

[50]  T. Ehrhardt,et al.  Ion channels in plant signaling , 1999, Cellular and Molecular Life Sciences CMLS.

[51]  A. Weber,et al.  Ion channels in the chloroplast envelope membrane. , 1995, Biochemistry.

[52]  R. Carpentier,et al.  Protective effect of active oxygen scavengers on protein degradation and photochemical function in photosystem I submembrane fractions during light stress , 2005, The FEBS journal.

[53]  W. Vredenberg,et al.  A 50-Picosiemens Anion Channel of the Chloroplast Envelope Is Involved in Chloroplast Protein Import* , 1997, The Journal of Biological Chemistry.

[54]  M. Schwarz,et al.  Inhibition of chloroplast ATPase by the K+ channel blocker α‐dendrotoxin , 1992 .

[55]  A. Krieger.  Effect of the Ca2+ channel activator CGP 28392 on reactivation of oxygen evolution of Ca2+‐depleted photosystem II , 1995, FEBS letters.

[56]  Vener,et al.  A cyclophilin-regulated PP2A-like protein phosphatase in thylakoid membranes of plant chloroplasts , 1999, Biochemistry.

[57]  L. Altschmied,et al.  A novel multi‐functional chloroplast protein: identification of a 40 kDa immunophilin‐like protein located in the thylakoid lumen , 1998, The EMBO journal.

[58]  J. Soll,et al.  Ion channels in the outer membranes of chloroplasts and mitochondria: open doors or regulated gates? , 2001, The EMBO journal.

[59]  H. Lichtenthaler,et al.  Hill-Activity and P700 Concentration of Chloroplasts Isolated from Radish Seedlings Treated with -Indoleacetic Acid, Kinetin or Gibberellic Acid , 1977, Zeitschrift fur Naturforschung. Section C, Biosciences.

[60]  J. Schroeder,et al.  Identification of High-Affinity Slow Anion Channel Blockers and Evidence for Stomatal Regulation by Slow Anion Channels in Guard Cells. , 1993, The Plant cell.

[61]  M. Pusch,et al.  Molecular modeling of p-chlorophenoxyacetic acid binding to the CLC-0 channel. , 2003, Biochemistry.

[62]  G. Schönknecht,et al.  Ion Channel Permeable for Divalent and Monovalent Cations in Native Spinach Thylakoid Membranes , 1996, The Journal of Membrane Biology.

[63]  A. Weber,et al.  Solute transporters of the plastid envelope membrane. , 2005, Annual review of plant biology.

[64]  Jeffrey Robbins,et al.  Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death , 2005, Nature.

[65]  Enrico Schleiff,et al.  Protein import into chloroplasts , 2004, Nature Reviews Molecular Cell Biology.

[66]  S. Izawa,et al.  Light-dependent redistribution of ions in suspensions of chloroplast thylakoid membranes. , 1974, Proceedings of the National Academy of Sciences of the United States of America.

[67]  D. Min,et al.  Effects of (-)-epigallocatechin-3-gallate, the main component of green tea, on the cloned rat brain Kv1.5 potassium channels. , 2001, Biochemical pharmacology.