Abstract
This study deals with effects of oxygen on the kinetics of P700 photoinduced redox transitions and on induction transients of chlorophyll fluorescence in leaves of C3 plants Hibiscus rosa-sinensis and Vicia faba. It is shown that the removal of oxygen from the leaf environment has a conspicuous effect on photosynthetic electron transport. Under anaerobic conditions, the concentration of oxidized P700 centers in continuous white light was substantially lower than under aerobic conditions. The deficiency of oxygen released non-photochemical quenching of chlorophyll fluorescence, thus indicating a decrease in the trans-thylakoid pH gradient (ΔpH). Quantitative analysis of experimental data within the framework of an original mathematical model has shown that the steady-state electron flux toward oxygen in Chinese hibiscus leaves makes up to ∼40% of the total electron flow passing through photosystem 1 (PS1). The decrease in P +700 content under anaerobic conditions can be due to two causes: i) the retardation of electron outflow from PS1, and ii) the release of photosynthetic control (acceleration of electron flow from PS2 to P +700 ) owing to lower acidification of the intra-thylakoid space. At the same time, cyclic electron transport around PS1 was not stimulated in the oxygen-free medium, although such stimulation seemed likely in view of possible rearrangement of electron flows on the acceptor side of PS1. This conclusion stems from observations that the rates of P +700 reduction in DCMU-poisoned samples, both under aerobic and anaerobic conditions, were negligibly small compared to rates of electron flow from PS2 toward P +700 in untreated samples.
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Abbreviations
- DCMU:
-
3-(3,4-dichlorophenyl)-1,1-dimethylurea (diuron)
- EPR:
-
electron paramagnetic resonance
- Fd:
-
ferredoxin
- NDH:
-
NAD(P)H-dehydrogenase
- PAM:
-
pulse amplitude modulated (fluorometry)
- PS1 and PS2:
-
photosystems 1 and 2
- Q and QH2 :
-
oxidized and reduced plastoquinone forms, respectively
References
Bendall, D. S., and Manasse, R. S. (1995) Biochim. Biophys. Acta, 1229, 23–38.
Allen, J. (2003) Trends Plant Sci., 8, 15–19.
Munekage, Y., Hashimoto, M., Miyake, C., Tomizawa, K.-I., Endo, T., Tasaka, M., and Shikanai, T. (2004) Nature, 429, 579–582.
Joet, T., Cournac, L., Peltier, G., and Havaux, M. (2002) Plant Physiol., 128, 760–769.
Joliot, P., and Joliot, A. (2002) Proc. Natl. Acad. Sci. USA, 99, 10209–10214.
Joliot, P., and Joliot, A. (2005) Proc. Natl. Acad. Sci. USA, 102, 4913–4918.
Johnson, G. N. (2005) J. Exp. Bot., 56, 407–416.
Breyton, C., Nandha, B., Johnson, G., Joliot, P., and Finazzi, G. (2006) Biochemistry 45, 13465–13475.
Golding, A. J., and Johnson, G. N. (2003) Planta, 218, 107–114.
Talts, E., Oja, V., Ramma, H., Rasulov, B., Anijalg, A., and Laisk, A. (2007) Photosynth. Res., 94, 109–120.
Mehler, A. H. (1951) Arch. Biochem. Biophys., 33, 65–77.
Asada, K. (1999) Annu. Rev. Plant Physiol. Plant Mol. Biol., 50, 601–639.
Heber, U. (2002) Photosynth. Res., 73, 223–231.
Peltier, G., and Cournac, L. (2002) Annu. Rev. Plant Biol., 53, 523–550.
Badger, M. R., von Caemmerer, S., Ruuska, S., and Nakano, H. (2000) Philos. Trans. R. Soc. Lond. B, 355, 1433–1446.
Backhausen, J. E., Kitzmann, C., Horton, P., and Scheibe, R. (2000) Photosynth. Res., 64, 1–13.
Foyer, C. H., and Noctor, G. (2000) J. Exp. Bot., 51, 15–19.
Allen, J., and Fosberg, J. (2001) Trends Plant Sci., 6, 317–326.
Kramer, D. M., Sacksteder, C. A., and Cruz, J. A. (2003) Trends Plant Sci., 8, 27–32.
Kramer, D. M., Avenson, T. J., and Edwards, G. E. (2004) Trends Plant Sci., 9, 349–357.
Ruuska, S. A., Badger, M. R., Andrews, T. J., and von Caemmerer, S. (2000) J. Exp. Bot., 51, 357–368.
Sage, F. R., Cen, Y.-P., and Li, M. (2002) Photosynth. Res., 71, 241–250.
Miyake, C., and Yokota, A. (2000) Plant Cell. Physiol., 41, 335–343.
Makino, A., Miyake, C., and Yokota, A. (2002) Plant Cell. Physiol., 43, 1017–1026.
Osmond, C. B., and Grace, S. C. (1995) J. Exp. Bot., 46, 1351–1362.
Ziem-Hanck, U., and Heber, U. (1980) Biochim. Biophys. Acta, 591, 266–274.
Ivanov, B., Kobayashi, Y., and Heber, U. (1998) Photosynth. Res., 57, 61–70.
Cornic, G., and Briantais, J.-M. (1991) Planta, 183, 178–184.
Vishnyakova, E. A., Trubitsin, B. V., and Tikhonov, A. N. (2000) Biofizika, 45, 899–904.
Chow, W. S., and Hope, A. B. (2002) Photosynth. Res., 81, 77–89.
Joliot, P., and Joliot, A. (2006) Biochim. Biophys. Acta, 1757, 362–368.
Maxwell, P. C., and Biggins, J. (1977) Biochim. Biophys. Acta, 459, 442–450.
Trubitsin, B. V., Mamedov, M. D., Vitukhnovskaya, L. A., Semenov, A. Yu., and Tikhonov, A. N. (2003) FEBS Lett., 544, 15–20.
Trubitsin, B. V., Ptushenko, V. V., Koksharova, O. A., Mamedov, M. D., Vitukhnovskaya, L. A., Grigor’ev, I. A., Semenov, A. Yu., and Tikhonov, A. N. (2005) Biochim. Biophys. Acta, 1708, 238–249.
Edwards, G. E., and Walker, D. A. (1983) C3, C4: Mechanisms and Cellular and Environmental Regulation of Photosynthesis, Blackwell Scientific, Oxford.
Allen, J. F. (1992) Biochim. Biophys. Acta, 1098, 275–335.
Rumberg, B., and Siggel, U. (1969) Naturwissenschaften, 56, 130–132.
Stiehl, H. H., and Witt, H. T. (1969) Z. Naturforsch. Teil B, 24, 1588–1598.
Tikhonov, A. N., Khomutov, G. B., Ruuge, E. K., and Blumenfeld, L. A. (1981) Biochim. Biophys. Acta, 637, 321–333.
Haehnel, W. (1984) Annu. Rev. Plant Physiol. Plant Mol. Biol., 35, 659–693.
Blumenfeld, L. A., and Tikhonov, A. N. (1994) Biophysical Thermodynamics of Intracellular Processes. Molecular Machines of the Living Cell, Spinger Verlag, N. Y.
Kramer, D. M., Sacksteder, C. A., and Cruz, J. A. (1999) Photosynth. Res., 60, 151–163.
Horton, P., Ruban, A. V., and Walters, R. G. (1996) Annu. Rev. Plant Physiol. Plant Mol. Biol., 47, 655–684.
Niyogi, K. (1999) Ann. Rev. Plant Physiol. Plant Mol. Biol., 50, 333–359.
Maxwell, K., and Johnson, G. N. (2000) J. Exp. Bot., 51, 659–668.
Mueller, P., Li, X. P., and Niyogi, K. K. (2001) Plant Physiol., 125, 1558–1566.
Niyogi, K. K., Li, X. P., Rosenberg, V., and Jung, H. S. (2004) J. Exp. Bot., 56, 375–382.
Karapetyan, N. V. (2007) Biochemistry (Moscow), 72, 1127–1135.
Rabinowitch, E. (1956) Photosynthesis, Vol. 3, Interscience Publishers, New York.
Webber, A. N., and Lubitz, W. (2001) Biochim. Biophys. Acta, 1507, 61–79.
Heber, U., Neimanis, S., Siebke, K., Schonknecht, G., and Katona, E. (1992) Photosynth. Res., 34, 443–447.
Savitsky, A., Trubitsin, B. V., Mobius, K., Semenov, A. Yu., and Tikhonov, A. N. (2007) Appl. Magn. Reson., 31, 221–236.
Tagawa, K., Tsujimoto, H. Y., and Arnon, D. (1963) Nature, 199, 1247–1252.
Kobayashi, Y., and Heber, U. (1994) Photosynth. Res., 41, 419–428.
Lazar, D. (1999) Biochim. Biophys. Acta, 1412, 1–28.
Khorobrykh, S. A., and Ivanov, B. N. (2002) Photosynth. Res., 71, 209–219.
Toth, S. Z., Schansker, G., and Strasser, R. J. (2007) Photosynth. Res., 93, 193–203.
Nandha, B., Finazzi, G., Joliot, P., Hald, S., and Johnson, G. N. (2007) Biochim. Biophys. Acta, 1767, 1252–1259.
Karavaev, V. K., and Kukushkin, A. K. (1975) Biofizika, 20, 88–92.
Burrows, P. A., Sazanov, L. F., Svab, Z., Maliga, P., and Nixon, P. J. (1998) EMBO J., 17, 868–876.
Kanazawa, A., and Kramer, D. M. (2002) Proc. Natl. Acad. Sci. USA, 99, 12789–12794.
Avenson, T. J., Cruz, J. A., and Kramer, D. M. (2004) Proc. Natl. Acad. Sci. USA, 101, 5530–5535.
Takizawa, K., Cruz, J. A., Kanazawa, A., and Kramer, D. M. (2007) Biochim. Biophys. Acta, 1767, 1233–1244.
Vershubskii, A. V., Priklonskii, V. I., and Tikhonov, A. N. (2004) Biochemistry (Moscow), 69, 1016–1024.
Vershubskii, A. V., Priklonskii, V. I., and Tikhonov, A. N. (2006) Fiz. Khim., 80, 552–559.
Vershubskii, A. V., Priklonskii, V. I., and Tikhonov, A. N. (2007) Khim. Fiz., 26, 54–64.
Dubinskii, A. Yu., and Tikhonov, A. N. (1994) Biofizika, 39, 652–665.
Dubinskii, A. Yu., and Tikhonov, A. N. (1995) Biofizika, 40, 365–371.
Frolov, A. E., and Tikhonov, A. N. (2007) Biofizika, 52, 656–666.
Ivanov, B. N. (2008) Biochemistry (Moscow), 73, 112–117.
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Original Russian Text © I. V. Kuvykin, A. V. Vershubskii, V. V. Ptushenko, A. N. Tikhonov, 2008, published in Biokhimiya, 2008, Vol. 73, No. 10, pp. 1329–1343.
Originally published in Biochemistry (Moscow) On-Line Papers in Press, as Manuscript BM08-016, September 14, 2008.
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Kuvykin, I.V., Vershubskii, A.V., Ptushenko, V.V. et al. Oxygen as an alternative electron acceptor in the photosynthetic electron transport chain of C3 plants. Biochemistry Moscow 73, 1063–1075 (2008). https://doi.org/10.1134/S0006297908100027
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DOI: https://doi.org/10.1134/S0006297908100027