Skip to main content
SpringerLink
Log in

The role of calcium in the pH-dependent control of Photosystem II

  • Regular Paper
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

pH-dependent inactivation of Photosystem (PS) II and related quenching of chlorophyll-a-fluorescence have been investigated in isolated thylakoids and PS II-particles and related to calcium release at the donor side of PS II. The capacity of oxygen evolution (measured under light saturation) decreases when the ΔpH is high and the pH in the thylakoid lumen decreases below 5.5. Oxygen evolution recovers upon uncoupling. The pH-response of inactivation can be described by a 1 H+-transition with an apparent pK-value of about 4.7. The yield of variable fluorescence decreases in parallel to the inactivation of oxygen evolution. pH-dependent quenching requires light and can be inhibited by DCMU. In PS II-particles, inactivation is accompanied by a reversible release of Ca2+-ions (one Ca2+ released per 200 Chl). In isolated thylakoids, where a ΔpH was created by ATP-hydrolysis, both inactivation of oxygen evolution (and related fluorescence quenching) by internal acidification and the recovery of that inactivation can be suppressed by calcium-channel blockers. In the presence of the Ca2+-ionophore A23187, recovery of Chl-fluorescence (after relaxation of the ΔpH) is stimulated by external Ca2+ and retarded by EGTA. As shown previously (Krieger and Weis 1993), inactivation of oxygen evolution at low pH is accompanied by an upward shift of the midpoint redox-potential, Em, of QA. Here, we show that in isolated PS II particles the pH-dependent redox-shift (about 160 mV, as measured from redox titration of Chl-fluorescence) is suppressed by Ca2+-channel blockers and DCMU. When a redox potential of −80 to −120mV was established in a suspension of isolated thylakoids, the primary quinone acceptor, QA, was largely reduced in presence of a ΔpH (created by ATP-hydrolysis) but oxidized in presence of an uncoupler. Ca2+-binding at the lumen side seems to control redox processes at the lumen- and stroma-side of PS II. We discuss Ca2+-release to be involved in the physiological process of ‘high energy quenching’.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

Chl:

Chlorophyll

DCMU:

3-(3′,4′-dichloro-phenyl)-1,1-dimethylurea

DMBQ:

2,5-dimethylbenzoquinone

EGTA:

ethylengylcol bis(β-aminoethylether)-N,N,N′,N′-tetra-acetate

HEPES:

4-(2-hydroxyethyl)-1-piperazineethanesulfonic acid

MES:

4-morpholino ethanesulfonic acid

MOPS:

4-morpholine-propanesulfonic acid

P680 :

reaction center chlorophyll in Photosystem II

Pheo:

pheophytin

QA, QB :

primary and secondary quinone acceptor of Photosystem II

tyrZ :

redox actie tyrosine (electron donor)

References

  • Bertold DA, Babcock GT and Yocum CF (1981) A highly resolved, oxygen-evolving Photosystem II preparation from spinach thylakoid membranes. FEBS Lett 134: 231–234

    Google Scholar 

  • Bilger W, Björkman O and Thayer SS (1989) Light-induced spectral absorbance changes in relation to photosynthesis and the epoxidation state of xanthophyll cycle components in cotton leaves. Plant Physiol 91: 542–551

    Google Scholar 

  • Blubaugh D, Atamian M, Babcock GT, Goldbeck JH and Cheniae GM (1991) Photoinhibition of hydroxylamin-extracted Photosystem II membranes: Identification of the sites of photodamage. Biochemistry 30: 7586–7597

    PubMed  Google Scholar 

  • Boussac A and Rutherford AW (1988) Ca2+-binding to the oxygen evolving enzyme varies with the redox state of the Mn cluster. FEBS Lett 236: 432–436

    Google Scholar 

  • Boussac A and Rutherford AW (1992) The involvement of Ca2+ in the Ca2+-effect on Photosystem II oxygen evolution. Photosynth Res 33: 208–209

    Google Scholar 

  • Boussac A, Maison-Peteri B, Etienne A-L and Vernotte C (1985) Reactivation of oxygen evolution of NaCl-washed Photosystem II particles by Ca2+ and/or the 24kDa protein, Biochim Biophys Acta 808: 225–230

    Google Scholar 

  • Boussac A, Zimmermann J-L, Rutherford AW and Lavergne J (1990) Histidine oxidation in the oxygen-evolving Photosystem II enzme. Nature 347, No 6290: 303–306

    Google Scholar 

  • Boussac A, Sétif P and Rutherford AW (1992) Inhibition of Tyrosine Z photooxidation after formation of the S3-state in Ca2+-depleted and Cl−-depleted Photosystem II. Biochemistry 31: 1224–1233

    PubMed  Google Scholar 

  • Briantais J-M, Vernotte C, Picaud M and Krause GH (1979) A quantitative study of the slow decline of chlorophylla fluorescence in isolated chloroplasts. Biochim Biophys Acta 548: 128–138

    PubMed  Google Scholar 

  • Carpentier R and Nakatani HY (1985) Inhibitors affecting the oxidizing side of Photosystem II at the Ca2+- and Cl−-sensitive sites. Biochim Biophys Acta 808: 288–292

    Google Scholar 

  • Crofts J and Horton P (1991) Dissipation of excess energy by Photosystem II particles at low pH. Biochim Biophys Acta 1058: 187–193

    Google Scholar 

  • Debus JD (1992) The manganese and calcium ions of photosynthetic oxygen evolution. Biochim Biophys Acta 1102: 269–352

    PubMed  Google Scholar 

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

    Google Scholar 

  • Dietz KJ, Schreiber U and Heber U (1985) The relationship between the redox state of QA and photosynthesis in leaves at various carbon dioxide, oxygen and light regimes. Planta 166: 219–226

    Google Scholar 

  • Diner BA and Delosme R (1983) Oxidation-reduction properties of the electron acceptors of Photosystem II, II. Redox titrations at various pH values of the flash-induced formation of C550 inChlamydomonas Photosystem II particles lacking the secondary quinone electron acceptor. Biochim Biophys Acta 722: 452–459

    Google Scholar 

  • Eckert H-J, Geiken B, Bernarding J, Napiwotzki A, Eichler H-J and Renger G (1991) Two sites of photoinhibition of the electron transfer in oxygen evolving and Tris-treated PS II membrane fragments from spinach. Photosynth Res 27: 97–108

    Google Scholar 

  • Genty B, Briantais J-M and Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990: 87–92

    Google Scholar 

  • Gilmore AU and Yamamoto HY (1992) Dark induction of zeaxanthin-dependent nonphotochemical quenching mediated by ATP. Proc Natl Acad Sci USA 89: 1899–1903

    PubMed  Google Scholar 

  • Grynkiewicz G, Poenie M and Tsien RY (1985) A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem 260(6): 3440–3450

    PubMed  Google Scholar 

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

    Google Scholar 

  • Heber U, Neimanis S, Siebke K, Schönknecht G and Katona E (1992) Chloroplast energization and oxidation of P700/ plastocyanin in illuminated leaves at reduced levels of CO2 or oxygen. Photosynth Res 34: 433–447

    Google Scholar 

  • Homann PH (1988) The chloride and calcium requirement of photosynthetic water oxidation: Effects of pH. Biochim Biophys Acta 934: 1–13

    Google Scholar 

  • Horton P and Hague A (1988) Studies on the induction of chlorophyll fluorescence in isolated barley protoplasts. IV. Resolution of non-photochemical quenching. Biochim Biophys Acta 932: 107–115

    Google Scholar 

  • Horton P, Oxborough K, Rees D and Scholes JD (1988) Regulation of the photochemical efficiency of Photosystem II; consequences for the light response of field photosynthesis. Plant Physiol Biochim 26: 453–460

    Google Scholar 

  • Horton P, Ruban AV, Rees D, Pascal AA, Noctor G and Young AJ (1991) Control of the light-harvesting function of chloroplast membranes by aggregation of the LHC II chlorophyll-protein complex. FEBS Lett 292: 1–4

    PubMed  Google Scholar 

  • Jegerschöld C, Virgin I and Styring S (1990) Light-dependent degradation of the D1-protein in Photosystem II is accelerated after inhibition of the water splitting reaction. Biochemistry 29: 6170–6186

    Google Scholar 

  • Krause GH and Weis E (1991) Chlorophyll fluorescence and photosynthesis: The basics. Ann Rev Plant Physiol Plant Mol Biol 42: 313–349

    Google Scholar 

  • Krause GH, Laasch H and Weis E (1988) Regulation of thermal dissipation of absorbed light energy in chloroplasts indicated by energy-dependent fluorescence quenching. Plant Physiol Biochem 26: 445–452

    Google Scholar 

  • Krieger A and Weis E (1993) Energy-dependent quenching of chlorophyll-a-fluorescence: The involvement of protoncalcium exchange at Photosystem II. Photosynthetica 27(1–2): 89–98

    Google Scholar 

  • Krieger A, Moya I and Weis E (1992) Energy-dependent quenching of chlorophyll-a-fluorescence: Effect of pH on stationary fluorescence and picosecond-relaxation kinetics in thylakoid membranes and Photosystem II preparations. Biochim Biophys Acta 1102: 167–176

    Google Scholar 

  • Krieger A, Weis E and Demeter S (1993) Low pH-induced Ca ion release in the water-splitting system is accompanied with a shift in the midpoint redox potential of the primary quinone aceptor, QA. Biochim Biophys Acta (in press)

  • Laasch H (1987) Non-photochemical quenching of Chlorophyll-a-fluorescence in isolated chloroplasts under conditions of stressed photosynthesis. Planta 171: 220–226

    Google Scholar 

  • Laisk A, Kiirats O, Oja V, Weis E and Heber U (1992) Analysis of oxygen evolution during photosynthetic induction and in multiple-turnover flashes in sunflower leaves. Planta 186: 434–441

    Google Scholar 

  • Onishi ST (1987) Characterization of the murexid method: Dual-wavelength spectrometry of cations under physiological conditions. Analyt Biochem 85: 165–179

    Google Scholar 

  • Ono T and Inoue Y (1988) Discrete extraction of Ca atom functional for O2-evolution in higher plant Photosystem II by a simple low pH treatment. FEBS Lett 227: 147–152

    Google Scholar 

  • Ono T and Inoue Y (1989) Removal of Ca by pH3.0 treatment inhibits S2 to S3 transition in photosynthetic oxygen evolution system. Biochim Biophys Acta 973: 443–449

    Google Scholar 

  • Oxborough K and Horton P (1987) Characterization of the effects of Antimycin A upon high energy state quenching of chlorophyll fluorescence (qE) in spinach and pea chloroplasts. Photosynthe Res 12: 119–128

    Google Scholar 

  • Rees D, Noctor G, Ruban AV, Crofts J, Young A and Horton P (1992) pH-dependent chlorophyll fluorescence quenching in spinach thylakoids from light treated or dark-adapted leaves. Photosynth Res 31: 11–19

    Google Scholar 

  • Rutherford AW, Zimmermann J-L and Boussac A (1992) Oxygen evolution. In: Barber J (ed) The Photosystems: Structure, Function and Molecular Biology, pp 179–230. Elsevier, Amsterdam

    Google Scholar 

  • Schlodder E and Meyer B (1987) pH-dependence of oxygen evolution and reduction kinetics of photooxidized chlorophylla II (P-680) in Photosystem II particles fromSynechococcus sp. Biochim Biophys Acta 890: 23–31

    Google Scholar 

  • Schreiber U and Avron M (1979) Properties of ATP-driven reverse electron flow in chloroplasts. Biochim Biophys Acta 546: 436–447

    PubMed  Google Scholar 

  • Schreiber U and Neubauer C (1989) Correlation between dissipative fluorescence quenching at Photosystem II and 50 μ s recombination luminescence. FEBS Lett 258: 339–342

    Google Scholar 

  • Schreiber U and Neubauer C (1990) O2-dependent electron flow, membrane energization and the mechanism of non-photochemical quenching of chlorophyll fluorescence. Photosynth Res 25: 279–293

    Google Scholar 

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

    PubMed  Google Scholar 

  • Semin BK, Ivanov II and Rubin AB (1989) Effects of calcium-channel blockers and activators on electron transport in pea chloroplasts. Biochim Biophys Acta 975: 239–243

    Google Scholar 

  • Styring S, Virgin I, Ehrenberg A and Andersson B (1990) Strong light photoinhibition of electron transport in Photosystem II. Impairment of the function of the first quinone acceptor, QA. Biochim Biophys Acta 1015: 269–278

    Google Scholar 

  • Thielen APG and van Gorkom HJ (1981) Redox potentials of electron acceptors in Photosystem IIα and IIβ. FEBS Lett 129: 205–209

    Google Scholar 

  • Vass I, Styring S, Hundal T, Koivuniemi A, Aro E-M and Andersson B (1992) Reversible and irreversible intermediates during photoinhibition of Photosystem II. Stable reduced QA species promote chlorophyll triplet formation. Proc Natl Acad Sci USA 89: 1408–1412

    PubMed  Google Scholar 

  • Vernotte C, Etienne A-L and Briantais J-M (1979) Quenching of the Photosystem II chlorophyll fluorescence by the plastoquinone pool. Biochim Biophys Acta 545: 519–527

    PubMed  Google Scholar 

  • Walker D (1992) Transley Review No. 36, Excited leaves. New Phytol 121: 325–345

    Google Scholar 

  • Weis E and Berry JA (1987) Quantum efficiency of Photosystem II in relation to energy-dependent quenching of chlorophyll fluorescence. Biochim Biophys Acta 894: 198–208

    Google Scholar 

  • Weis E and Lechtenberg D (1989) Fluorescence analysis during steady state photosynthesis. Phil Trans R Soc London B 323: 253–268

    Google Scholar 

  • van Wijk KJ and van Hasselt PR (1993) Photoinhibition of Photosystem II in vivo is preceded by down-regulation through light-induced acidification of the lumen: Consequences for the mechanism of photoinhibition in vivo. Planta 189: 359–368

    Google Scholar 

  • Yocum CF (1991) Calcium activation of photosynthetic water oxidation. Biochim Biophys Acta 1059: 1–15

    Google Scholar 

Download references

Author information

Author notes

  1. Anja Krieger

    Present address: Centre d'Etudes Nucléaire de Saclay, DBCM, SBE, Bât 532, F-91191, Gif-sur-Yvette, France

Authors and Affiliations

  1. Institute of Botany, University of Münster, Schlossgarten 3, D-48149, Münster, Germany

    Anja Krieger & Engelbert Weis

Authors
  1. Anja Krieger
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Engelbert Weis
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Krieger, A., Weis, E. The role of calcium in the pH-dependent control of Photosystem II. Photosynth Res 37, 117–130 (1993). https://doi.org/10.1007/BF02187470

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02187470

Key words

Search

Navigation