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Influence of Ca2+ on the thylakoid lumen violaxanthin de-epoxidase activity through Ca2+ gating of H+ flux at the CFo H+ channel

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Abstract

Part of the chloroplast photoprotection response to excess light absorption involves formation of zeaxanthin (and antheraxanthin) via the violaxanthin deepoxidase enzyme, the activity of which requires lumen acidity near or below pH 6.0. Clearly, the violaxanthin de-epoxidase activity is strongly regulated because at equivalent energization levels (including the parameters of H+ accumulation and ATP formation rates), there can be either low or high violaxanthin de-epoxidase enzyme activity. This work shows that the factor or factors responsible for regulating the violaxanthin deepoxidase correlate directly with those which regulate the expression of membrane-localized or delocalized proton gradient (Δ~μH+) energy coupling. The most clearly identified factor regulating switching between localized and delocalized energy coupling modes is Ca2+ binding to the lumen side of the thylakoid membrane; in particular, Ca2+ binding to the 8 kDA subunit III of the CFo H+ channel. The activity of violaxanthin deepoxidase in pea (Pisum sativa) and spinach (Spinacea oleracea) thylakoids is shown here to be strongly correlated with conditions known from previous work to displace Ca2+ from the CFo H+ channel and thus to modulate the extent of lumenal acidification while maintaining a fairly constant rate of ATP formation.

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References

  • Allnutt FCT, Ewy R, Renganathan M, Pan RS and Dilley RA (1991) Nigericin and hexlamine effects on localized proton gradients in thylakoids. Biochim Biophys Acta (1059) 28-36

    CAS  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidases in Beta vulgaris. Plant Physiol 24: 1-15

    Article  PubMed  CAS  Google Scholar 

  • Beard WA and Dilley RA (1986) A shift in chloroplast energy coupling by KCl from localized to bulk phase delocalized proton gradients. FEBS Lett 201: 57-62

    Article  CAS  Google Scholar 

  • Beard WA and Dilley RA (1988) ATP formation onset lag and postillumination phosphorylation initiated with single-turnover flashes. III. Characterization of the ATP formation onset lag and postillumination phosphorylation for thylakoids exhibiting localized or bulk-phase delocalized energy coupling. J Bioenerg Biomembr 20: 129-154

    Article  PubMed  CAS  Google Scholar 

  • Blumenfeld LA, Davydov RM and Tikhonov AN (1989) Molecular dynamics and energy transduction in chloroplasts and mitochondria. J Mol Liquids 42: 231-253

    Article  CAS  Google Scholar 

  • Chiang GG and Dilley RA (1987) Evidence for Ca2+-gated proton fluxes in chloroplast thylakoid membranes: Ca2+ controls a localized to delocalized proton gradient switch. Biochemistry 26: 4911-4916

    Article  CAS  Google Scholar 

  • Chiang GG and Dilley RA (1989) Intact chloroplasts show Ca2+-gated switching between localized and delocalized proton gradient energy coupling. Plant Physiol 90: 1513-1523

    PubMed  CAS  Google Scholar 

  • Chiang GG, Wooten DC and Dilley RA (1992) Calcium dependent interaction of chlorpromazine with the chloroplast 8-kilodalton CF0 protein and calcium gating of II+ fluxes between thylakoid membrane domains and the lumen. Biochemistry 31: 5808-5819

    Article  PubMed  CAS  Google Scholar 

  • Demmig-Adams B (1990) Carotenoids and photoprotection in plants: A role for the xanthophyll zeaxanthin. Biochim Biophys Acta 1020: 1-24

    Article  CAS  Google Scholar 

  • Demmig-Adams B and Adams III WW (1992) Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol 43: 599-626

    Article  CAS  Google Scholar 

  • Demmig B, Winter K, Krüger A and Czygan FC (1987) Photoinhibition and zeaxanthin formation in intact leaves. A possible role of the xanthophyll cycle in the dissipation of excess light energy. Plant Physiol 84: 218-224

    PubMed  CAS  Google Scholar 

  • Dilley RA (1991) Energy coupling in chloroplasts: A calcium-gated switch controls proton fluxes between localized and delocalized proton gradients. Curr Topics Bioenerg 16: 265-318

    CAS  Google Scholar 

  • Dilley RA and Vernon LP (1965) Ion and water transport processes related to the light-dependent shrinkage of chloroplasts. Arch Biochem Biophys 111: 365-375

    Article  PubMed  CAS  Google Scholar 

  • Dilley RA, Theg SM and Beard WA (1987) Membrane-proton interactions in chloroplast bioenergetics: Localized proton domains. Ann Rev Plant Physiol 38: 347-389

    Article  CAS  Google Scholar 

  • Ehrenheim AM, Forti G and Finazzi G (1991) The influence of membrane localized protons on energy utilization at the reaction centres of photosystem II in isolated thylakoids. Biochim Biophys Acta 1059: 106-110

    CAS  Google Scholar 

  • Enz C, Steinkkanp T and Wagner R (1993) Ion channels in the thylakoid membrane (a patch-clamp study). Biochim Biophys Acta 1143: 67-76

    Article  CAS  Google Scholar 

  • Ettinger WF, Clear AM, Fanning KJ and Peck ML (1999) Identification of a Ca++/H+ antiport in the plant chloroplast thylakoid membrane. Plant Physiol 119: 1379-1385

    Article  PubMed  CAS  Google Scholar 

  • Ewy RG (1997) Delineation between sequestered domain and lumen buffering in the chloroplast thylakoid membrane. PhD Thesis, Purdue University, Ch 5.

  • Frank HA, Cua A, Chynwat V, Young A, Gosztola D and Wasielewski PMR (1994) Photophysics of the carotenoids associated with the xanthophyll cycle in photosynthesis. Photosynth Res 41: 389-395

    Article  CAS  Google Scholar 

  • Frank HA, Bautista JA, Josue JS and Young AJ (2000) Mechanism of nonphoto chemical quenching in green plants: energies of the lowest excited siglet states of violaxanthin and zeaxanthin. Biochemistry 39: 2831-2837

    Article  PubMed  CAS  Google Scholar 

  • Giersch C (1983) Nigericin-induced stimulation of photophosphorylation in chloroplasts. Biochim Biophys Acta 725: 309-319

    Article  CAS  Google Scholar 

  • Gilmore AM (1997) Mechanistic aspects of xanthophyll cycle-dependent photoprotection in higher plant chloroplasts and leaves. Physiol Plant 99: 197-209

    Article  CAS  Google Scholar 

  • Gilmore AM and Yamamoto HY (1991a) Resolution of lutein and zeaxanthin using a non-endcapped, lightly carbon-loaded C18 high-performance liquid chromatographic column. J Chromatogr 543: 137-145

    Article  CAS  Google Scholar 

  • Gilmore AM and Yamamoto HY (1991b) Zeaxanthin formation and energy-dependent fluorescence quenching in pea chloroplasts under artificially mediated linear and cyclic electron transport. Plant Physiol 96: 635-643

    PubMed  CAS  Google Scholar 

  • Gilmore AM and Yamamoto HY (1993) Linear models relating xanthophylls and lumen acidity to non-photochemical fluorescence quenching. Evidence that antheraxanthin explains zeaxanthin-independent quenching. Photosynth Res 35: 67-78

    Article  CAS  Google Scholar 

  • Graan T, Flores S and Ort DR (1981) The nature of ATP formation associated with single turnovers of the electron transport carriers in chloroplasts. In: Selman BR and Selman-Reimer S (eds) Energy Coupling in Photosynthesis, Developments in Biochemistry, 20: 25-34. Elsevier-North Holland, New York

    Google Scholar 

  • Günther G, Thiele A and Laasch H (1994) A new method for the determination of the transthylakoid pH gradient in isolated chloroplasts: The pH-dependent activity of violaxanthin depoxidase. Plant Sci 102: 19-30

    Article  Google Scholar 

  • Hager A (1969) Lichtbedingte pH-Erniedrigung in einem Chloroplastenkompartiment als Ursache der enzymatischen Violaxanthin → Zeaxanthin-Umwandlung: Beziehungen zur Photophosphorylierung. Planta 89: 224-243

    Article  CAS  Google Scholar 

  • Hangarter RP and Good NE (1982) Energy thresholds for ATP synthesis in chloroplasts. Biochim Biophys Acta 681: 397-404

    Article  CAS  Google Scholar 

  • Heldt HW, Werdan K, Milovancev M and Geller G (1973) Alkalization of the chloroplast stroma caused by light-dependent proton flux into the thylakoid space. Biochim Biophys Acta 314: 224-241

    Article  PubMed  CAS  Google Scholar 

  • Hind G, Nakatani HY and Izawa S (1974) Light-dependent redistribution of ions in suspensions of chloroplast thylakoid membranes. Proc Natl Acad Sci USA 71: 1484-1488

    Article  PubMed  CAS  Google Scholar 

  • Horner RD and Moudrianakis EN (1986) Effects of permeant buffers on the initiation of photosynchronous phosphorylation and postillumination phosphorylation in chloroplasts. J Biol Chem 261: 13408-13414

    PubMed  CAS  Google Scholar 

  • Kramer DM, Sacksteder CA and Crus JA (1999) How acidic is the lumen? Photosynthesis Res 60: 151-163

    Article  CAS  Google Scholar 

  • Kreimer G, Melkonian M, Holtum JAM and Latzko E (1988) Stromal free calcium concentration and light mediated activation of chloroplast fructose 1,6-bisphosphate. Plant Physiol 86: 423-428

    PubMed  CAS  Google Scholar 

  • Krieger A and Weis E (1992) Energy-dependent quenching of chlorophyll a fluorescence: The involvement of proton-calcium exchange at Photosystem 2. Photosynthetica 27: 89-98

    CAS  Google Scholar 

  • Krieger A and Weis E (1993) The role of calcium in the pH dependent control of Photosystem II. Photosynth Res 37: 117-130

    Article  CAS  Google Scholar 

  • Krieger A, Weis E and Demeter S (1993) Low pH-induced Ca2+ ion release in the water-splitting system is accompanied by a shift in the midpoint potential of the primary quinone acceptor QA. Biochim Biophys Acta 1144: 411-418

    Article  CAS  Google Scholar 

  • Mohanty N and Yamamoto HY (1995) Mechanism of non-photochemical chlorophyll fluorescence quenching. I. The role of de-epoxidized xanthophylls and sequestered thylakoid membrane protons as probed by dibucaine. Aust J Plant Physiol 22: 231-238

    Article  CAS  Google Scholar 

  • Neubauer C and Yamamoto HY (1994) Membrane barriers and Mehler-peroxidase reaction limit the ascorbate available for violaxanthin de-epoxidase activity in intact chloroplasts. Photosynth Res 39: 137-147

    Article  CAS  Google Scholar 

  • Opanasenko V, Semenova G and Agafonov A (1999) Changes in the structure and the functional state of thylakoids under the conditions of osmotic shock. Photosynth Res 62: 281-290

    Article  CAS  Google Scholar 

  • Ort DR and Izawa S (1973) Studies on the energy-coupling sites of photophosphorylation. II. Treatment of chloroplasts with NH2OH plus ethylenediaminetetraacetate to inhibit water oxidation while maintaining energy-coupling efficiencies. Plant Physiol 52: 595-600

    PubMed  CAS  Google Scholar 

  • Ort DR Dilley RA and Good NE (1976) Photophosphorylation as a function of illumination time. II. Effects of permanent buffers. Biochim Biophys Acta 449: 108-124

    Article  PubMed  CAS  Google Scholar 

  • Owens TG (1994) Excitation energy transfer between chlorophylls and carotenoids. A proposed molecular mechanism for non-photochemical quenching. In: Baker NR and Bowyer JR (eds) Photoinhibition of Photosynthesis, pp 95-107. Bios Scientific Publishers, Oxford

    Google Scholar 

  • Pfündel EE, Renganathan M, Gilmore AM, Yamamoto HY and Dilley RA (1994) Intrathylakoid pH in isolated pea chloroplasts as probed by violaxanthin de-epoxidation. Plant Physiol 106: 1647-1658

    PubMed  Google Scholar 

  • Pfündel E and Bilger W (1994) Regulation and possible function of the violaxanthin cycle. Photosyn Res 42: 89-100

    Article  Google Scholar 

  • Pfündel E and Dilley RA (1993) The pH dependence of violaxanthin deepoxidation in isolated pea chloroplasts. Plant Physiol 101: 65-71

    PubMed  Google Scholar 

  • Pick U, Weiss M and Rottenberg H (1987) Anomalous uncoupling of photophosphorylation by palmitic acid and by gramicidin D. Biochemistry 26: 8295-8302

    Article  PubMed  CAS  Google Scholar 

  • Pottosin II and Schönknecht G (1996) Ion channel permeability for divalent and monovalent cations in native spinach thylakoid membranes. J Membr Biol 152: 223-233

    Article  PubMed  CAS  Google Scholar 

  • Powles SB (1984) Photoinhibition of photosynthesis induced by visible light. Annu Rev Plant Physiol 35: 14-44

    Article  Google Scholar 

  • Renganathan M, Pan R-S, Ewy RG, Theg SM, Allnutt FCT and Dilley RA (1991) Evidence that localized energy coupling in thylakoids can continue beyond the energetic threshold onset into steady illumination. Biochim Biophys Acta 1059: 16-27

    PubMed  CAS  Google Scholar 

  • Renganathan M, Pfündel E and Dilley RA (1993) Thylakoid lumenal pH determination using a fluorescent dye: Correlation of lumen pH and gating between localized and delocalized energy coupling. Biochim Biophys Acta 1142: 277-292

    Article  CAS  Google Scholar 

  • Rottenberg H (1985) Proton-coupled energy conversion: Chemiosmotic and intramembrane coupling. Modern Cell Biol 4: 47-83

    CAS  Google Scholar 

  • Ruban AV and Horton P (1999) The xanthophyll cycle modulates the kinetics of nonphotochemical energy dissipation in isolated light-harvesting complexes, intact chloroplasts and leaves of spinach. Plant Physiol 119: 531-542

    Article  PubMed  CAS  Google Scholar 

  • Schuldiner S, Rottenberg H and Avron M (1972) Determination of ΔpH in chloroplasts. 2. Fluorescent amines as a probe for the determination of ΔpH in chloroplasts. Eur J Biochem 25: 64-70

    Article  PubMed  CAS  Google Scholar 

  • Siefermann D and Yamamoto HY (1974) Light-induced de-epoxidation of violaxanthin in lettuce chloroplasts. III. Reaction kinetics and effect of light intensity on de-epoxidase activity and substrate availability. Biochim Biophys Acta 357: 144-150 Siefermann D and Yamamoto HY (1975b) Light-induced de-epoxidation of violaxanthin in lettuce chloroplasts. IV. The effects of electron-transport conditions on violaxanthin availability. Biochim Biophys Acta 387: 149–158

    Article  PubMed  CAS  Google Scholar 

  • Sigalat C, Haraux F, De Kouchkovsky F, Hung S and De Kouchkovsky Y (1985) Adjustable microchemiosmotic character of the proton gradient generated by systems I and II for photosynthetic phosphorylation in thylakoids. Biochim Biophys Acta 809: 403-413

    Article  CAS  Google Scholar 

  • Tikhonov AN and Shevyakova AV (1985) Electron transport, proton translocation and their relation to photophosphorylation in chloroplasts. 3. Metabolic state effects on the proton transport in chloroplasts. Biol Membranes (USSR) 2(8): 776-788

    CAS  Google Scholar 

  • Theg SM, Chiang G and Dilley RA (1988) Protons in the thylakoid membrane-sequestered domains can directly pass through the coupling factor during ATP synthesis in flashing light. J Biol Chem 63: 673-681

    Google Scholar 

  • Trewavas AJ and Malho R (1998) Ca2+ signalling in plant cells: The big network! Curr Opin Plant Biol 1: 428-433

    Article  PubMed  CAS  Google Scholar 

  • Van Walraven HS, Strotmann H, Schwarz O and Rumberg B (1996) The H+/ATP coupling ratio of the ATP synthase from thiolmodulated chloroplasts and two cynobacterial strains is four. FEBS Lett 379: 309-313

    Article  PubMed  CAS  Google Scholar 

  • Van Walraven HS, Hollander EE, Scholts MJC and Kraayenhof R (1997) The H+/ATP ratio of the ATP synthase from the cyanobacterium Synechococcus 6716 varies with growth temperature and light intensity. Biochim Biophys Acta 1318: 217-224

    Article  CAS  Google Scholar 

  • Wooten DC and Dilley RA (1993) Calcium gating of H+ fluxes in chloroplasts affects acid-base-driven ATP formation. J Bioenerg Biomembr 25: 557-567

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto HY and Higashi RM (1978) Violaxanthin de-epoxidase: Lipid composition and substrate specificity. Arch Biochem Biophys 190: 514-522

    Article  PubMed  CAS  Google Scholar 

  • Zakharov SD, Ewy RG and Dilley RA (1993) Subunit III of the chloroplast ATP-synthase can form a Ca2+-binding site on the lumenal side of the thylakoid membrane. FEBS 1379 336: 95-99

    Article  CAS  Google Scholar 

  • Zakharov SD, Ewy RG and Dilley RA (1995) Calcium binding to the chloroplast and E. coli (CF0) F0 subunit (III) c of the ATP-synthase. Protoplasma 184: 42-49

    Article  CAS  Google Scholar 

  • Zakharov SD, Li X, Red'ko TP and Dilley RA (1996) Calcium binding to the subunit c of E. coli ATP-synthase and possible functional implications in energy coupling. J Bioenerg Biomembr 28: 483-493

    Article  PubMed  CAS  Google Scholar 

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  1. Department of Biological Sciences, Purdue University, West Lafayette, IN, 47907-1392, USA

    Run-Sun Pan

  2. Department of Biological Sciences, Purdue University, West Lafayette, IN, 47907-1392, USA

    Richard A. Dilley

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  1. Run-Sun Pan
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Pan, RS., Dilley, R.A. Influence of Ca2+ on the thylakoid lumen violaxanthin de-epoxidase activity through Ca2+ gating of H+ flux at the CFo H+ channel. Photosynthesis Research 65, 141–154 (2000). https://doi.org/10.1023/A:1006496719927

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