Abstract
The pigment-protein complex of photosystem 2 (PS 2) catalyzes the light-driven oxidation of water molecule and the reduction of plastoquinone. In this work, we studied the effect of the disaccharide trehalose, which is unique in its physicochemical properties, on isolated PS 2 complex. It was found that trehalose significantly stimulated the steady-state rate of oxygen evolution. The study of single flash-induced fluorescence decay kinetics demonstrated that trehalose did not affect the rate of Q −A oxidation, although it led to an increase in the relative fractions of PS 2 reaction centers capable of Q −A oxidation. Trehalose also prevented PS 2 complexes from being inactivated on prolonged storage. We propose that in the presence of trehalose, which affects the extent of hydration, the protein can preferentially exist in a more optimal conformation for effective functioning.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Abbreviations
- DCBQ:
-
2,6-dichloro-p-benzoquinone
- DCMU:
-
3-(3,4-dichlorophenyl)-1,1-dimethylurea
- P680:
-
primary electron donor
- PS 2:
-
photosystem 2
- QA and QB :
-
primary and secondary quinone acceptors
- RC:
-
reaction center
- WOC:
-
water-oxidizing complex
- YZ :
-
redox-active tyrosine 161 of D1 protein
References
Goussias, C., Boussac, A., and Rutherford, A. W. (2002) Photosystem II and photosynthetic oxidation of water: an overview, Philos. Trans. R. Soc. London, Ser. B, 357, 1369–1381.
Wydrzynski, T. J., and Satoh K. (2005) in Photosystem II: The Light-Driven Water:Plastoquinone Oxidoreductase, Springer, New York.
Kok, B., Forbush, B., and McGloin, M. (1970) Cooperation of charges in photosynthetic O2 evolution. I. A linear four-step mechanism, Photochem. Photobiol., 11, 467–475.
Shinkarev, V. P. (2004) in Photosystem II: Oxygen Evolution and Chlorophyll a Fluorescence Induced by Multiple Flashes (Papageorgiou, G. C., ed.) Kluwer Academic Publishers, Dordrecht, pp. 197–229.
Renger, G., and Kuhn, P. (2007) Reaction pattern and mechanism of light induced oxidative water splitting in photosynthesis, Biochim. Biophys. Acta, 1767, 458–471.
Dau, H., and Haumann, M. (2007) Eight steps preceding O-O bond formation in oxygenic photosynthesis — a basic reaction cycle of the photosystem II manganese complex, Biochim. Biophys. Acta, 1767, 472–483.
Barber, J. (2008) Photosynthetic generation of oxygen, Trans. R. Soc. B, 363, 2665–2674.
Crowe, J. H., Crowe, L. M., and Jackson, S. A. (1983) Preservation of structural and functional activity in lyophilized sarcoplasmic reticulum, Arch. Biochem. Biophys., 220, 477–484.
Sun, W. Q., and Davidson, P. (1998) Protein inactivation in amorphous sucrose and trehalose matrices: effects of phase separation and crystallization, Biochim. Biophys. Acta, 1425, 235–244.
Francia, F., Dezi, M., Mallardi, A., Palazzo, G., Cordone, L., and Venturoli, G. (2008) Protein-matrix coupling/uncoupling in “dry” systems of photosynthetic reaction center embedded in trehalose/sucrose: the origin of trehalose peculiarity, J. Am. Chem. Soc., 130, 10240–10246.
Jain, N. K., and Roy, I. (2009) Effect of trehalose on protein structure, Protein Sci., 18, 24–36.
Allakhverdiev, S. I., Los, D. A., Mohanty, P., Nishiyama, Y., and Murata, N. (2007) Glycinebetaine alleviates the inhibitory effect of moderate heat stress on the repair of photosystem II during photoinhibition, Biochim. Biophys. Acta, 1767, 1363–1371.
Chen, T. H., and Murata, N. (2011) Glycinebetaine protects plants against abiotic stress: mechanisms and biotechnological applications, Plant Cell Environ., 34, 1–20.
Fernandez, O., Bethencourt, L., Quero, A., Sangwan, R. S., and Clement, C. (2010) Trehalose and plant stress responses: friend or foe? Trend Plant Sci., 15, 409–417.
Ohtake, S., and Wang, Y. J. (2011) Trehalose: current use and future applications, J. Pharm. Sci., 100, 2020–2053.
Jun, S.-S., Choi, H. J., Lee, H. Y., and Hong, Y-N. (2008) Altered physiology in trehalose-producing transgenic tobacco plants: enhanced tolerance to drought and salinity stresses, J. Plant Biol., 51, 327–336.
Garg, A. K., Kim, J.-K., Owens, T. G., Ranwala, A. P., Choi, Y. D., Kochian, L. V., and Ray, J. Wu. (2002) Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses, Proc. Natl. Acad. Sci. USA, 99, 15898–15903.
Hincha, D. K., Hofner, R., Schwab, K. B., Heber, U., and Schmitt, J. M. (1987) Membrane rupture is the common cause of damage to chloroplast membranes in leaves injured by freezing or excessive wilting, Plant Physiol., 83, 251–253.
Apostolova, E., Bushova, M., and Tenchov, B. (2005) in Research Photosynthesis (Murata, N., ed.) Vol. IV, Kluwer Academic Publishers, pp. 165–168.
Francia, E., Malferrari, M., Sacquin-Mora, S., and Venturoli, G. (2009) Charge recombination kinetics and protein dynamics in wild type and carotenoid-less bacterial reaction centers: studies in trehalose glasses, J. Phys. Chem., 113, 10389–10398.
Haag, E., Irrgang, K. D., Boekema, E. J., and Renger, G. (1990) Functional and structural analysis of photosystem II core complexes from spinach with high oxygen evolution capacity, Eur. J. Biochem., 189, 47–53.
Ford, R. C., and Evans, M. C. W. (1983) Isolation of a photosystem 2 preparation from higher plants with highly enriched oxygen evolution activity, FEBS Lett., 160, 159–164.
Lerbret, A., Bordat, P., Affouard, F., Descamps, M., and Migliardo, F. (2005) How homogeneous are the trehalose, maltose, and sucrose water solutions? An insight from molecular dynamics simulations, J. Phys. Chem. B, 109, 11046–11057.
Govindjee (1995) Sixty-three years since Kautsky: chlorophyll a fluorescence, Aust. J. Plant Physiol., 22, 131–160.
Pospisil, P., and Dau, H. (2000) Chlorophyll fluorescence transients of photosystem II membrane particles as a tool for studying photosynthetic oxygen evolution, Photosynth. Res., 65, 41–52.
Bukhov, N. G., Egorova, E. A., Govindacharya, S., and Carpentier, R. (2004) Changes in polyphasic chlorophyll a fluorescence induction curve upon inhibition of donor or acceptor side of photosystem II in isolated thylakoids, Biochim. Biophys. Acta, 1657, 121–130.
Zhu X-G., Govindjee Baker N. R., deSturler E., Ort D. R., and Long S. P. (2005) Chlorophyll a fluorescence induction kinetics in leaves predicted from a model describing each discrete step of excitation energy and electron transfer associated with photosystem II, Planta, 223, 114–133.
Petrova, I. O., Kurashov, V. N., Semenov, A. Yu., and Mamedov, M. D. (2011) Manganese-depleted/reconstituted photosystem II core complexes in solution and liposomes, J. Photochem. Photobiol. B: Biol., 104, 372–376.
Krieger, A., Rutherford, A. W., and Johnson, G. N. (1995) On the determination of redox midpoint potential of the primary quinone electron acceptor, QA, in photosystem II, Biochim. Biophys. Acta, 1229, 193–201.
Allakhverdiev, S. I., Hayashi, H., Nishiyama, Y., Ivanov, A. G., Aliev, J. A., Klimov, V. V., Murata, N., and Carpentier, R. (2003) Glycinebetaine protects the D1/D2/Cyt b559 complex of photosystem II against photo-induced and heat-induced inactivation, J. Plant Physiol., 160, 41–49.
Bowes, J. M., and Crofts, A. R. (1980) Binary oscillations in the rate of reoxidation of the primary acceptor of photo-system II, Biochim. Biophys. Acta, 590, 373–384.
Eaton-Rye, J. J., and Govindjee (1988) Electron-transfer through the quinone acceptor complex of photosystem II after one or two actinic flashes in bicarbonate-depleted spinach thylakoid membranes, Biochim. Biophys. Acta, 935, 248–257.
De Wijn, R., and van Gorkom, H. J. (2001) Kinetics of electron transfer from Q(a) to Q(b) in photosystem II, Biochemistry, 40, 11912–11922.
Rova M., Mamedov F., Magnuson A., Fredriksson P.-O., and Styring S. (1998) Coupled activation of the donor and the acceptor side of photosystem II during photoactivation of the oxygen evolving cluster, Biochemistry, 37, 11039–11045.
Halverson, K. M., and Barry, B. A. (2003) Sucrose and glycerol effects on photosystem II, Biophys. J., 85, 1317–1325.
Sigfridsson, K. G. V., Bernat, G., Mamedov, F., and Styring, S. (2004) Molecular interference of Cd(2+) with photosystem II, Biochim. Biophys. Acta, 1659, 19–31.
Roose J. L., Frankel L. K., and Bricker T. M. (2010) Documentation of significant electron transport defects on the reducing side of photosystem II upon removal of the PsbP and PsbQ extrinsic proteins, Biochemistry, 49, 36–41.
Muh, F., Glockner, C., Hellmich, J., and Zouni, A. (2012) Light-induced quinone reduction in photosystem II, Biochim. Biophys. Acta, 1817, 44–65.
Renger, G. (1999) in Concepts in Photobiology: Photosynthesis and Photomorphogenesis, Molecular Mechanism of Water Oxidation (Singhal, G. S., Renger, G., Govindjee, Irrgang, K.-D., and Sopory, S. K., eds.) Kluwer Academic Publishers, Dordrecht, Narosa Publishing Co., Delhi, pp. 292–329.
Rappaport F., Guergova-Kuras M., Nixon P. J., Diner B. A., and Lavergne J. (2002) Kinetics and pathways of charge recombination in photosystem II, Biochemistry, 41, 8518–8527.
Mamedov, F., Rintamaki, E., Aro, E.-M., Andersons, B., and Styring, S. (2002) Influence of protein phosphorylation on the electron-transport properties of photosystem II, Photosynth. Res., 74, 61–72.
Malferrari, M., Francia, F., and Venturoli, G. (2011) Coupling between electron transfer and protein-solvent dynamics: FTIR and laser-flash spectroscopy studies in photosynthetic reaction center films at different hydration levels, J. Phys. Chem., 115, 14732–14750.
Polander, P. C., and Barry, B. A. (2012) A hydrogen-bonding network plays a catalytic role in photosynthetic oxygen evolution, Proc. Natl. Acad. Sci. USA, 109, 6112–6117.
Author information
Authors and Affiliations
Corresponding author
Additional information
Published in Russian in Biokhimiya, 2015, Vol. 80, No. 1, pp. 79–86.
Originally published in Biochemistry (Moscow) On-Line Papers in Press, as Manuscript BM14-208, December 28, 2014.
Rights and permissions
About this article
Cite this article
Mamedov, M.D., Petrova, I.O., Yanykin, D.V. et al. Effect of trehalose on oxygen evolution and electron transfer in photosystem 2 complexes. Biochemistry Moscow 80, 61–66 (2015). https://doi.org/10.1134/S0006297915010071
Received:
Revised:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S0006297915010071