In vivo modulation of nonphotochemical exciton quenching (NPQ) by regulation of the chloroplast ATP synthase

Nonphotochemical quenching (NPQ) of excitation energy, which protects higher plant photosynthetic machinery from photodamage, is triggered by acidification of the thylakoid lumen as a result of light-induced proton pumping, which also drives the synthesis of ATP. It is clear that the sensitivity of NPQ is modulated in response to changing physiological conditions, but the mechanism for this modulation has remained unclear. Evidence is presented that, in intact tobacco or Arabidopsis leaves, NPQ modulation in response to changing CO2 levels occurs predominantly by alterations in the conductivity of the CFO-CF1 ATP synthase to protons (g\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \setlength{\oddsidemargin}{-69pt} \begin{document} \begin{equation*}{\mathrm{_{H}^{+}}}\end{equation*}\end{document}). At a given proton flux, decreasing g\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \setlength{\oddsidemargin}{-69pt} \begin{document} \begin{equation*}{\mathrm{_{H}^{+}}}\end{equation*}\end{document} will increase transthylakoid proton motive force (pmf), thus lowering lumen pH and contributing to the activation of NPQ. It was found that an ≈5-fold decrease in g\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \setlength{\oddsidemargin}{-69pt} \begin{document} \begin{equation*}{\mathrm{_{H}^{+}}}\end{equation*}\end{document} could account for the majority of NPQ modulation as atmospheric CO2 was decreased from 2,000 ppm to 0 ppm. Data are presented that g\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \setlength{\oddsidemargin}{-69pt} \begin{document} \begin{equation*}{\mathrm{_{H}^{+}}}\end{equation*}\end{document} is kinetically controlled, rather than imposed thermodynamically by buildup of ΔGATP. Further results suggest that the redox state of the ATP synthase γ-subunit thiols is not responsible for altering g\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \setlength{\oddsidemargin}{-69pt} \begin{document} \begin{equation*}{\mathrm{_{H}^{+}}}\end{equation*}\end{document}. A working model is proposed wherein g\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \setlength{\oddsidemargin}{-69pt} \begin{document} \begin{equation*}{\mathrm{_{H}^{+}}}\end{equation*}\end{document} is modulated by stromal metabolite levels, possibly by inorganic phosphate.

[1]  D. Ort,et al.  Initial events in the regulation of electron transfer in chloroplasts. The role of the membrane potential. , 1983, Journal of Biological Chemistry.

[2]  S. Robinson.  The involvement of stromal ATP in maintaining the pH gradient across the chloroplast envelope in the light , 1985 .

[3]  A. Crofts,et al.  Regulation of coupling factor in field-grown sunflower: A Redox model relating coupling factor activity to the activities of other thioredoxin-dependent chloroplast enzymes , 1990, Photosynthesis Research.

[4]  H. Inokuchi,et al.  Nucleotide Sequences of cDNA Clones Encoding Ferrochelatase from Barley and Cucumber , 1994, Plant physiology.

[5]  K. Niyogi,et al.  Non-photochemical quenching. A response to excess light energy. , 2001, Plant physiology.

[6]  G. Johnson,et al.  Regulation of the photosynthetic electron transport chain , 1999, Planta.

[7]  D. Walker,et al.  PHOTOSYNTHESIS IN VIVO CAN BE LIMITED BY PHOSPHATE SUPPLY , 1986 .

[8]  P. Fromme,et al.  KINETICS OF PROTON-TRANSPORT-COUPLED ATP SYNTHESIS CATALYZED BY THE CHLOROPLAST ATP SYNTHASE. , 1986 .

[9]  K. Niyogi,et al.  Altered xanthophyll compositions adversely affect chlorophyll accumulation and nonphotochemical quenching in Arabidopsis mutants. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[10]  I. Vass,et al.  Characterization of chlorophyll triplet promoting states in photosystem II sequentially induced during photoinhibition. , 1993, Biochemistry.

[11]  P. Horton,et al.  A study of the regulation and function of energy-dependent quenching in pea chloroplasts , 1988 .

[12]  U. Heber,et al.  Chloroplast pH values and buffer capacities in darkened leaves as revealed by CO2 solubilization in vivo , 1995, Planta.

[13]  K. Werdan,et al.  Alkalization of the chloroplast stroma caused by light-dependent proton flux into the thylakoid space. , 1973, Biochimica et biophysica acta.

[14]  D. Kramer,et al.  How acidic is the lumen? , 1999, Photosynthesis Research.

[15]  U. Heber,et al.  Oxygen reduction in the Mehler reaction is insufficient to protect photosystems I and II of leaves against photoinactivation , 1998 .

[16]  G. Edwards,et al.  Relationship between photosystem II activity and CO2 fixation in leaves , 1992 .

[17]  K. Niyogi,et al.  The roles of specific xanthophylls in photoprotection. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[18]  P. Horton,et al.  Regulation of Photosystem II , 1992, Photosynthesis Research.

[19]  J. Briantais,et al.  The relationship between non-photochemical quenching of chlorophyll fluorescence and the rate of photosystem 2 photochemistry in leaves , 1990, Photosynthesis Research.

[20]  D. Cooke.  Oxygenic Photosynthesis: The Light Reactions. Edited by Donald R. Ort and Charles F. Yocum , 1998, Plant Growth Regulation.

[21]  D. Kramer,et al.  Dark-interval relaxation kinetics (DIRK) of absorbance changes as a quantitative probe of steady-state electron transfer , 2004, Photosynthesis Research.

[22]  D. Kramer,et al.  The proton to electron stoichiometry of steady-state photosynthesis in living plants: A proton-pumping Q cycle is continuously engaged. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[23]  A. Crofts,et al.  Mutants of Chloroplast Coupling Factor Reduction in Arabidopsis , 1994, Plant physiology.

[24]  K. Asada.  The water-water cycle as alternative photon and electron sinks. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[25]  D. Kramer,et al.  A diffused-optics flash kinetic spectrophotometer (DOFS) for measurements of absorbance changes in intact plants in the steady-state , 1998, Photosynthesis Research.

[26]  T. Sharkey,et al.  Low oxygen inhibition of photosynthesis is caused by inhibition of starch synthesis. , 1989, Plant physiology.

[27]  Ulrich Heber,et al.  ATP and NADPH as the driving force of carbon reduction in leaves in relation to thylakoid energization by light , 1994, Planta.

[28]  I. E. Woodrow,et al.  Enzymatic Regulation of Photosynthetic CO2, Fixation in C3 Plants , 1988 .

[29]  A. Young,et al.  Modulation of chlorophyll fluorescence quenching in isolated light harvesting complex of Photosystem II , 1994 .

[30]  G. Berkowitz,et al.  Stromal pH and Photosynthesis Are Affected by Electroneutral K and H Exchange through Chloroplast Envelope Ion Channels. , 1992, Plant physiology.

[31]  C. Foyer,et al.  Homeostasis of adenylate status during photosynthesis in a fluctuating environment. , 2000, Journal of experimental botany.

[32]  H. Witt,et al.  Relations between the electrical potential, pH gradient, proton flux and phosphorylation in the photosynthetic membrane. , 1976, Biochimica et biophysica acta.

[33]  Govindjee,et al.  Advances in Photosynthesis and Respiration: Focus on Plant Respiration , 2005, Photosynthesis Research.

[34]  P. Horton,et al.  Chlorophyll fluorescence quenching in isolated light harvesting complexes induced by zeaxanthin , 2000, FEBS letters.

[35]  K. Niyogi,et al.  Chlamydomonas Xanthophyll Cycle Mutants Identified by Video Imaging of Chlorophyll Fluorescence Quenching. , 1997, The Plant cell.

[36]  U. Heber,et al.  Stimulation by Light of Rapid pH Regulation in the Chloroplast Stroma in Vivo as Indicated by CO2 Solubilization in Leaves , 1995, Plant physiology.

[37]  K. Sonoike.  Photoinhibition of Photosystem I: Its Physiological Significance in the Chilling Sensitivity of Plants , 1996 .

[38]  K. Niyogi,et al.  The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[39]  É. Hideg,et al.  Photoinhibition of photosynthesis in vivo results in singlet oxygen production detection via nitroxide-induced fluorescence quenching in broad bean leaves. , 1998, Biochemistry.

[40]  U. Heber,et al.  Relationship between photosynthetic electron transport and pH gradient across the thylakoid membrane in intact leaves. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[41]  J. Briantais,et al.  The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence , 1989 .

[42]  B. Genty,et al.  Relative quantum efficiencies of the two photosystems of leaves in photorespiratory and non-respiratory conditions. , 1990 .

[43]  P. Horton,et al.  REGULATION OF LIGHT HARVESTING IN GREEN PLANTS. , 1996, Annual review of plant physiology and plant molecular biology.

[44]  C. Foyer,et al.  Relationships between the Efficiencies of Photosystems I and II and Stromal Redox State in CO(2)-Free Air : Evidence for Cyclic Electron Flow in Vivo. , 1991, Plant physiology.

[45]  D. Kramer,et al.  Contribution of electric field (Δψ) to steady-state transthylakoid proton motive force (pmf) in vitro and in vivo. Control of pmf parsing into Δψ and ΔpH by ionic strength , 2001 .

[46]  Berry,et al.  Proton to electron stoichiometry in electron transport of spinach thylakoids , 1999, Biochimica et biophysica acta.

[47]  N. Baker.  Photosynthesis and the Environment , 1996, Advances in Photosynthesis and Respiration.

[48]  S. Ruuska,et al.  Electron flow to oxygen in higher plants and algae: rates and control of direct photoreduction (Mehler reaction) and rubisco oxygenase. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[49]  C. Cobbett,et al.  Cadmium-Sensitive, cad1 Mutants of Arabidopsis thaliana Are Phytochelatin Deficient , 1995, Plant physiology.

[50]  K Maxwell,et al.  Chlorophyll fluorescence--a practical guide. , 2000, Journal of experimental botany.

[51]  D. Kramer,et al.  A portable, non-focusing optics spectrophotometer (NoFOSpec) for measurements of steady-state absorbance changes in intact plants , 2004, Photosynthesis Research.

[52]  A. Crofts,et al.  Activation of the chloroplast atpase measured by the electrochromic change in leaves of intact plants , 1989 .

[53]  K. Dietz,et al.  Rate-limiting factors in leaf photosynthesis. I. Carbon fluxes in the calvin cycle , 1984 .

[54]  H. Stahlberg,et al.  ATP synthase: constrained stoichiometry of the transmembrane rotor , 2001, FEBS letters.

[55]  R. Furbank,et al.  Stimulation of photosynthesis by 2% oxygen at low temperatures is restored by phosphate , 1986, Planta.

[56]  E. Pfundel,et al.  The pH Dependence of Violaxanthin Deepoxidation in Isolated Pea Chloroplasts , 1993, Plant physiology.

[57]  U. Heber,et al.  Concerning a dual function of coupled cyclic electron transport in leaves. , 1992, Plant physiology.