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Interaction of Terbium Cations with the Donor Side of Photosystem II in Higher Plants

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Abstract

Photosystem II (PSII) of higher plants provides photoinduced water oxidation and produces molecular oxygen as a by-product of this reaction followed by its release into the atmosphere. The oxygen-evolving complex (OEC) is located on the donor side of PSII and contains an Mn4CaO5 cluster catalyzing water oxidation. A cofactor of this reaction is a Ca2+ cation. Lanthanide ions are similar to Ca2+ ions in relation to some physical and chemical properties, such as the ionic radius and coordination number. In the case of calcium-binding proteins, Ca2+ substitution with these cations is possible. Some representatives of this group of cations are able to bind to the Ca-binding site of PSII. In this study, we investigated an interaction between the donor side of PSII and terbium, one of the least studied lanthanides. According to the obtained results, the incubation of native PSII preparations with Tb3+ cations caused an irreversible inhibition (by ~75% for 2 mM of Tb3+) of the oxygen evolving function. At the same time, changes in the electron transport at the acceptor side of PSII remained rather insignificant. Supplementation of an incubation buffer with 30 mM Ca2+ reduced the inhibiting effect of terbium almost two times. The obtained results agree with the fluorescence induction kinetics measurement in PSII preparations in the presence of exogenous Ca2+ and Tb3+ and allow for the supposition that terbium cations displace Ca2+ ions from OEC. This terbium-induced release of calcium from the catalytic center results in incomplete water oxidation producing H2O2 instead of molecular oxygen as it has been shown earlier for PSII in the absence of Ca2+ in OEC.

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REFERENCES

  1. Umena, Y., Kawakami, K., Shen, J.-R., and Kamiya, N., Crystal structure of oxygen evolving photosystem II at a resolution of 1.9 Å, Nature, 2011, vol. 473, no. 7345, pp. 55–60.

    Article  CAS  PubMed  Google Scholar 

  2. Yocum, C.F., Calcium activation of photosynthetic water oxidation, Biochim. Biophys. Acta, 1991, vol. 1059, no. 1, pp. 1–15.

    Article  CAS  Google Scholar 

  3. Shamsipur, M. and Pashabadi, A., Latest advances in PSII features and mechanism of water oxidation, Coordin. Chem. Rev., 2018, vol. 374, pp. 153–172.

    Article  CAS  Google Scholar 

  4. McEvoy, J.P. and Brudvig, G.W., Water-splitting chemistry of photosystem II, Chem. Rev., 2006, vol. 106, no. 11, pp. 4455–4483.

    Article  CAS  PubMed  Google Scholar 

  5. Yocum, C.F., The calcium and chloride requirements of the O2 evolving complex, Coordin. Chem. Rev., 2008, vol. 252, nos. 3–4, pp. 296–305.

    Article  CAS  Google Scholar 

  6. Wang, L., Zhou, Q., and Huang, X., Photosynthetic responses to heavy metal terbium stress in horseradish leaves, Chemosphere, 2009, vol. 77, no. 7, pp. 1019–1025.

    Article  CAS  PubMed  Google Scholar 

  7. Ono, T., Effects of lanthanide substitution at Ca2+-site on the properties of the oxygen evolving center of photosystem II, J. Inorg. Biochem., 2000, vol. 82, nos. 1–4, pp. 85–91.

    Article  CAS  PubMed  Google Scholar 

  8. Popovic, R., Carpentier, R., and Morin, L., Determination of fluorescence inductions in a PSII submembrane fraction affected by additives, J. Plant Physiol., 1988, vol. 132, no. 6, pp. 754–757.

    Article  CAS  Google Scholar 

  9. Ghanotakis, D.F., Babcock, G.T., and Yocum, C.F., Structure of the oxygen-evolving complex of Photosystem II: Calcium and lanthanum compete for sites on the oxidizing side of Photosystem II which control the binding of water-soluble polypeptides and regulate the activity of the manganese complex, Biochim. Biophys. Acta, 1985, vol. 809, no. 2, pp. 173–180.

    Article  CAS  Google Scholar 

  10. Ghanotakis, D.F., Babcock, G.T., and Yocum, C.F., Calcium reconstitutes high rates of oxygen evolution in polypeptide depleted photosystem II preparations, FEBS Lett., 1984, vol. 167, no. 1, pp. 127–130.

    Article  CAS  Google Scholar 

  11. Porra, R.J., Thompson, W.A., and Kriedemann, P.E., Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: Verification of the concentration of chlorophyll standards by atomic absorption spectroscopy, Biochim. Biophys. Acta, 1989, vol. 975, no. 3, pp. 384–394.

    Article  CAS  Google Scholar 

  12. Pospisil, P. and Dau, H., Chlorophyll fluorescence transients of photosystem II membrane particles as a tool for studying photosynthetic oxygen evolution, Photosynth. Res., 2000, vol. 65, no. 1, pp. 41–52.

    Article  CAS  PubMed  Google Scholar 

  13. Strasser, R.J. and Govindjee, On the O-J-I-P fluorescence transients in leaves and D1 mutants of Chlamydomonas reinhardtii, in Research in Photosynthesis, Murata, M., Ed., Dordrecht: Kluwer Academic Publ., 1992, vol. 2, pp. 29–32.

    Google Scholar 

  14. Strasser, B.J., Donor side capacity of photosystem II probed by chlorophyll a fluorescence transients, Photosynth. Res., 1997, vol. 52, no. 2, pp. 147–155.

    Article  CAS  Google Scholar 

  15. Semin, B.K. and Seibert, M., Substituting Fe for two of the four Mn ions in photosystem II—effects on water-oxidation, J. Bioenerg. Biomembr., 2016, vol. 48, no. 3, pp. 227–240.

    Article  CAS  PubMed  Google Scholar 

  16. Johnson, G.N., Rutherford, A.W., and Krieger, A., A change in the midpoint potential of the quinone QA in photosystem II associated with photoactivation of oxygen evolution, Biochim. Biophys. Acta, 1995, vol. 1229, no. 2, pp. 202–207.

    Article  Google Scholar 

  17. Loktyushkin, A.V., Lovyagina, E.R., and Semin, B.K., Inhibition of the electron-transport chain of the photosystem II with terbium cations, Akt. Vopr. Biol. Fiz. Khim., 2018, vol. 3, no. 2, pp. 250–255.

    Google Scholar 

  18. Semin, B.K., Davletshina, L.N., Ivanov, I.I., Rubin, A.B., and Seibert, M., Decoupling of the processes of molecular oxygen synthesis and electron transport in Ca2+-depleted PSII membranes, Photosynth. Res., 2008, vol. 98, nos. 1–3, pp. 235–249.

    Article  CAS  PubMed  Google Scholar 

  19. Lovyagina, E.R. and Semin, B.K., Mechanism of inhibition and decoupling of oxygen evolution from electron transfer in photosystem II by fluoride, ammonia and acetate, J. Photochem. Photobiol. B, 2016, vol. 158, pp. 145–153.

    Article  CAS  PubMed  Google Scholar 

  20. Pospíšil, P. and Dau H., Valinomycin sensitivity proves that light-induced thylakoid voltages result in millisecond phase of chlorophyll fluorescence transients, Biochim. Biophys. Acta, 2002, vol. 1554, nos. 1–2, pp. 94–100.

    Article  PubMed  Google Scholar 

  21. Semin, K., Davletshina, L.N., Timofeev, K.N., Ivanov, I.I., Rubin, A.B., and Seibert, M., Production of reactive oxygen species in decoupled, Ca2+-depleted PSII and their use in assigning a function to chloride on both sides of PSII, Photosynth. Res., 2013, vol. 117, nos. 1–3, pp. 385–399.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Biophysics, Faculty of Biology, Moscow State University, 119234, Moscow, Russia

    A. V. Loktyushkin, E. R. Lovyagina & B. K. Semin

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  1. A. V. Loktyushkin
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  2. E. R. Lovyagina
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  3. B. K. Semin
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Correspondence to A. V. Loktyushkin.

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The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

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Translated by N. Statsyuk

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Loktyushkin, A.V., Lovyagina, E.R. & Semin, B.K. Interaction of Terbium Cations with the Donor Side of Photosystem II in Higher Plants. Moscow Univ. Biol.Sci. Bull. 74, 81–85 (2019). https://doi.org/10.3103/S009639251902007X

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  • DOI: https://doi.org/10.3103/S009639251902007X

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