Abstract
We have measured, under Cu (II) toxicity conditions, the oxygen-evolving capacity of spinach PS II particles in the Hill reactions H2O→SiMo (in the presence and absence of DCMU) and H2O→PPBQ, as well as the fluorescence induction curve of Tris-washed spinach PS II particles. Cu (II) inhibits both Hill reactions and, in the first case, the DCMU-insensitive H2O → SiMo activity. In addition, the variable fluorescence is lowered by Cu (II). We have interpreted our results in terms of a donor side inhibition close to the reaction center. The same polarographic and fluorescence measurements carried out at different pHs indicate that Cu (II) could bind to amino acid residues that can be protonated and deprotonated. In order to reverse the Cu (II) inhibition by a posterior EDTA treatment, in experiments of preincubation of PS II particles with Cu (II) in light we have demonstrated that light is essential for the damage due to Cu (II) and that this furthermore is irreversible.
Similar content being viewed by others
Abbreviations
- DCMU:
-
3-(3,4-dichlorophenyl)-1, 1-dimethyl urea
- DCIP:
-
2,6-dichlorophenolindophenol
- DPC:
-
1,5-diphenilcarbazide
- Fo :
-
initial non-variable fluorescence
- FI :
-
intermediate fluorescence yield
- Fm :
-
maximum fluorescence yield
- Fv :
-
variable fluorescence yield
- Mes:
-
2,-(N-morpholino)ethanosulfonic acid
- OEC:
-
oxygen-evolving complex
- P680:
-
Primary electron donor chlorophyll
- Pheo:
-
pheophytin
- PPBQ:
-
phenyl-p-benzo-quinone
- PS II:
-
Photosystem II
- SiMo:
-
Silicomolybdate
- QB :
-
secondary quinone acceptor
- QA :
-
primary quinone aceptor
- Tris:
-
N-tris(hydroxymethyl)amino ethane
- Tyrz :
-
electron carrier functioning between P680 and the Mn cluster
References
Arellano JB, Schröder WP, Sandmann G, Chueca A and Barón M (1994) Removal of nuclear contaminants and of non-specifically Photosystem II-bound copper from Photosystem II preparations. Physiol Plant 91: 369–373
Barber J, Chapman DJ and Telfer A (1987) Characterization of a PS II reaction center isolated from the chloroplasts of Pisum sativum. FEBS Lett 251: 147–154
Barón M, Arellano JB, Schröder WP, Lachica M and Chueca A (1993) Copper binding sites associated with Photosystem II preparations. Photosynthetica 28: 195–204.
Barón M, Arellano JB and López Gorgé J (1995) Copper and Photosystem II: A controversial relationship. Physiol Plant 94: 174–180.
Berthold DA, Babcock GT and Yocum CA (1981) A highly resolved, oxygen-evolving Photosystem II preparation from spinach thylakoid membranes. FEBS Lett 134: 231–234
Böger P (1982) Replacement of photosynthetic electron transport inhibitors by silicomolybdate. Physiol Plant 54: 221–224
Briantais JM, Cornic G and Hodges M (1988) The modification of chlorophyll fluorescence of Chlamydomonas reinhardtii by photoinhibition and chloramphenicol addition suggests a form of Photosystem II less susceptible to degradation. FEBS Lett 236: 226–230
Butler WL (1972) Primary nature of fluorescence yield changes associated with photosynthesis. Proc Natl Acad Sci 69: 3420–3422
Cao J and Govinjee (1990) Chlorophyll a fluorescence transient as an indicator of active and inactive Photosystem II in thylakoid membranes. Biochim Biophys Acta 1015, 180–188
Cedeño-Maldonado A and Swader JA (1972) The cupric ion as an inhibitor of photosynthetic electron transport in isolated chloroplasts. Plant Physiol 50: 698–701
Conjeaud H and Mathis P (1980) The effect of pH on the reduction kinetics of P680 in Tris-treated chloroplasts. Biochim Biophys Acta 590: 353–369
Droppa M and Horvath G (1990) The role of copper in photosynthesis. Crit Rev Plant Sci 9: 111–123
Falkowski PG, Fujita Y, Ley A and Mauzerall D (1986) Evidence for cyclic electron flow around Photosystem II in Chlorella pyrenoidosa. Plant Physiol 81: 310–312
Govindjee (1990) Photosystem II heterogeneity: the acceptor side. Photosynth Res 25: 151–160
Graan T (1986) The interaction of silicomolybdate with the Photosystem II herbicide-binding site. FEBS Lett 206: 9–14
Gross RE, Rugno P and Dugger M (1970) Observations on the mechanism of copper damage in Chlorella. Plant Physiol 46: 183–185
Gupta (1986) Copper uptake and inhibition of growth, photosynthetic pigments and macromolecules in the cyanobacterium Anacystis nidulans. Photosynthetica 20: 447–453
Habermann HM (1969) Reversal of copper inhibition in chloroplast reactions by manganese. Plant Physiol 44: 331–336
Hsu BD and Lee JY (1988) Toxic effects of copper on Photosystem II of spinach chloroplasts. Plant Physiol 87: 116–119
Hsu BD and Lee JY (1991) Characterization of the Photosystem II centers inactive in plastoquinone reduction by fluorescence induction. Photosynth Res 27: 143–150
Jegerschöld C, Arellano JB, Schröder WP, van Kan PJ, Barón M and Styring S (1995) Cu (II) inhibition of the electron transfer through Photosystem II studied by EPR spectroscopy. Biochemistry (in press)
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
Lapointe L, Huner NPA, Leblanc RM and Carpentier R (1993) Possible photoacustic detection of cyclic electron transport around Photosystem II in photoinhibited thylakoid preparations. Biochim Biophys Acta 1142: 43–48
Lavergne J (1982) Two types of primary acceptors in chloroplast PS II. Photobiochem Photobiophys 3: 257–285
Ljungberg U, Åkerlund HE and Andersson B (1986) Isolation and caracterization of the 10 kDa and 22 kDa polypeptides from higher plant Photosystem II. Eur J Biochem 158: 477–482
Mäenpää P, Andersson B and Sundby C (1987) Difference in sensitivity to photoinhibition between Photosystem II in the appressed and non-appressed thylakoid regions. FEBS Lett 215: 31–36
Melis A (1991) Dynamics of photosynthetic membrane composition and function. Biochim Biophys Acta 1058: 87–106
Melis A (1995) Functional properties of Photosystem IIβ in spinach chloroplasts. Biochim Biophys Acta 808: 334–342
Mohanty N, Vass I and Demeter S (1989) Copper toxicity affects Photosystem II electron transport at the secondary quinone acceptor (QB). Plant Physiol 90: 175–179
Neale PN and Melis A (1990) Activation of a reserve pool of Photosystem II in Chlamydomonas reinhardii counteracts photoinhibition. Plant Physiol 92: 1196–1204
Renganathan M and Bose S (1989) Inhibition of primary photochemistry of Photosystem II by copper in isolated pea chloroplasts. Biochim Biophys Acta 974: 247–253
Renganathan M and Bose S (1990) Inhibition of Photosystem II activity by Cu (II) (II) ion. Choice of buffer and reagent is critical. Photosynth Res 23: 95–99
Renger G, Gleiter HM, Haag E and Reifart F (1993) Photosystem II: thermodynamics and kinetics of electron transport from QA - to QB (QB -) and deleterious effects of copper (II). Z Naturforsch 48: 234–240
Samson G, Morissette JC and Popovic R (1988) Copper quenching of the variable fluorescence in Dunaliella tertiolecta. New evidence for a copper inhibition effect on PS II photochemistry. Photochem Photobiol 48: 329–332
Samuelsson G and Öquist G (1980) Effects of copper chloride on photosynthetic electron transport and chlorophyll-protein complexes of Spinacea oleracea. Plant Cell Physiol 21: 445–454
Schlodder E and Meyer B (1987) pH dependence of oxygen evolution and reduction kinetics of photooxidized chlorophyll a II (P680) in Photosystem II particles of Synechococus sp. Biochim Biophys Acta 890: 23–31
Schreiber U and Neubauer C (1987) The polyphasic rise of chlorophyll fluorescence upon onset of strong continuous illumination: II. Partial control by the Photosystem II donor side and possible ways of interpretation. Z Naturforsch 42: 1255–1264
Schreiber U, Schliwa U and Bilger W (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth Res 10: 51–62
Schröder WP, Arellano JB, Bittner T, Eckert JH, Barón M and Renger G (1994) Flash induced absorption spectroscopy studies of copper interaction with Photosystem II in higher plants. J Biol Chem 269: 32865–32870
Shioi Y, Tamai H and Sasa T (1978a) Effects of copper on photosynthetic electron transport systems in spinach chloroplasts. Plant Cell Physiol 19: 203–209
Shioi Y, Tamai H and Sasa T (1978b) Inhibition of Photosystem II in green alga Ankistrodesmus falcatus by copper. Physiol Plant 44: 434–438
Singh DP and Singh SP (1987) Action of heavy metals on Hill activity and O2 evolution in Anacystis nidulans. Plant Physiol 83: 12–14
Steemann-Nielsen E, Kamp-Nielsen L, and Wium-Andersen S (1969) The effect of deleterious concentrations of copper on the photosynthesis of Chlorella pyrenoidosa. Physiol Plant 22: 1121–1333
Takahashi Y, Hansson Ö, Mathis P and Satoh K (1987) Primary radical pair in the Photosystem II reaction center. Biochim Biophys Acta 893: 49–59
Vierke G and Struckmeier P (1977) Binding of copper (II) to protein of the photosynthetic membrane and its correlation with inhibition of electron transport in class II chloroplasts of spinach. Z Naturforsch 32: 605–610
Vierke G and Struckmeier P (1978): Inhibition of millisecond luminescence by copper (II) in spinach chloroplasts. Z Naturforsch 33: 266–270
Yruela I, Montoya G, Alonso PJ and Picorel R (1991) Identification of the pheophytin-QA-Fe domain of the reducing side of the Photosystem II as the Cu (II)-inhibitory binding site. J Biol Chem 266: 22847–22850
Yruela I, Montoya G and Picorel R (1992) The inhibitory mechanism of Cu (II) on the Photosystem II electron transport from higher plants. Photosynth Res 33: 227–233
Yruela I, Alfonso M, Ortizde Zárate I, Montoya G and Picorel R (1993) Precise Location of the Cu (II)-inhibitory binding site in higher plant and bacterial photosynthetic reaction centers as probed by light-induced absortion changes. J Biol Chem 268: 1684–1689
Author information
Authors and Affiliations
Additional information
This article is dedicated to Prof. Dr. Harmut Lichtenthaler on the occasion of his 60th birthday.
Rights and permissions
About this article
Cite this article
Arellano, J.B., Lázaro, J.J., López-Gorgé, J. et al. The donor side of Photosystem II as the copper-inhibitory binding site. Photosynth Res 45, 127–134 (1995). https://doi.org/10.1007/BF00032584
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00032584