Skip to main content
SpringerLink
Log in

Oxygenic photosynthesis: EPR study of photosynthetic electron transport and oxygen-exchange, an overview

  • Original Paper
  • Published:
Cell Biochemistry and Biophysics Aims and scope Submit manuscript

Abstract

In this review, we consider the applications of electron paramagnetic resonance (EPR) methods to the study of the relationships between the electron transport and oxygen-exchange processes in photosynthetic systems of oxygenic type. One of the purposes of this article is to encourage scientists to use the advantageous EPR oximetry approaches to study oxygen-related electron transport processes in photosynthetic systems. The structural organization of the photosynthetic electron transfer chain and the EPR approaches to the measurements of molecular oxygen (O2) with O2-sensitive species (nitroxide spin labels and solid paramagnetic particles) are briefly reviewed. In solution, the collision of O2 with spin probes causes the broadening of their EPR spectra and the reduction of their spin-lattice relaxation times. Based on these effects, tools for measuring O2 concentration and O2 diffusion in biological systems have been developed. These methods, named “spin-label oximetry,” include not only nitroxide spin labels, but also other stable-free radicals with narrow EPR lines, as well as particulate probes with EPR spectra sensitive to molecular oxygen (lithium phthalocyanine, coals, and India ink). Applications of EPR approaches for measuring O2 evolution and consumption are illustrated using examples of photosynthetic systems of oxygenic type, chloroplasts in situ (green leaves), and cyanobacteria.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  1. Edwards, G. E., & Walker, D. A. (1983). C3, C4: Mechanisms, and cellular and environmental regulation of photosynthesis. Oxford: Blackwell.

    Google Scholar 

  2. Witt, H. T. (1979). Energy conversion in the functional membrane of photosynthesis. Analysis by light pulse and electric pulse methods. Biochimica et Biophysica Acta, 505, 355–427.

    Article  CAS  PubMed  Google Scholar 

  3. Blankenship, R. E. (2002). Molecular mechanisms of photosynthesis. Oxford: Blackwell Science.

    Book  Google Scholar 

  4. Jordan, P., Fromme, P., Witt, H. T., Klukas, O., Saenger, W., & Krauss, N. (2001). Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution. Nature, 411, 909–917.

    Article  CAS  PubMed  Google Scholar 

  5. Nelson, N., & Yocum, C. (2006). Structure and function of photosystems I and II. Annual Review of Plant Biology, 57, 521–565.

    Article  CAS  PubMed  Google Scholar 

  6. Umena, Y., Kawakami, K., Shen, J. R., & Kamiya, N. (2011). Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 A. Nature, 473, 55–60.

    Article  CAS  PubMed  Google Scholar 

  7. Daum, B., & Kuhlbrandt, W. (2011). Electron tomography of plant thylakoid membranes. Journal of Experimental Botany, 62, 2393–2402.

    Article  CAS  PubMed  Google Scholar 

  8. Skulachev, V. P., Bogachev, A. V., & Kasparinsky, F. O. (2012). Principles of bioenergetics. Berlin: Springer.

    Google Scholar 

  9. Ruban, A. V. (2012). The photosynthetic membrane: Molecular mechanisms and biophysics of light harvesting. Oxford: Wiley-Blackwell.

    Book  Google Scholar 

  10. Kirchhoff, H. (2013). Architectural switches in plant thylakoid membranes. Photosynthesis Research, 116, 481–487.

    Article  CAS  PubMed  Google Scholar 

  11. Mamedov, M., Govindjee, Nadtochenko, V., & Semenov, A. (2015). Primary electron transfer processes in photosynthetic reaction centers from oxygenic organisms. Photosynthesis Research, 125, 51–63.

    Article  CAS  PubMed  Google Scholar 

  12. Nelson, N., & Junge, W. (2015). Structure and energy transfer in photosystems of oxygenic photosynthesis. Annual Review of Biochemistry, 84, 659–683.

    Article  CAS  PubMed  Google Scholar 

  13. Mitchell, P. (1966). Chemiosmotic coupling in oxidative and photosynthetic phosphorylation. Biological Review, 41, 445–502.

    Article  CAS  Google Scholar 

  14. Junge, W., & Nelson, N. (2015). ATP synthase. Annual Review of Biochemistry, 83, 631–657.

    Article  CAS  Google Scholar 

  15. Shikanai, T. (2007). Cyclic electron transport around photosystem I: genetic approaches. Annual Review of Plant Biology, 58, 199–217.

    Article  CAS  PubMed  Google Scholar 

  16. Iwai, M., Takizawa, K., Tokutsu, R., Okamuro, A., Takahashi, Y., & Minagawa, J. (2010). Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis. Nature, 464, 1210–1213.

    Article  CAS  PubMed  Google Scholar 

  17. Asada, K. (1999). The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annual Review of Plant Physiology and Plant Molecular Biology, 50, 601–639.

    Article  CAS  PubMed  Google Scholar 

  18. Foyer, C. H., & Noctor, G. (2000). Oxygen processing in photosynthesis: regulation and signalling. New Phytologist, 146, 359–388.

    Article  CAS  Google Scholar 

  19. Bennoun, P. (1982). Evidence for a respiratory chain in the chloroplast. Proceedings of the National Academy of Sciences of the United States of America, 79, 4352–4356.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Peltier, G., & Cournac, L. (2002). Chlororespiration. Annual Review of Plant Biology, 53, 523–550.

    Article  CAS  PubMed  Google Scholar 

  21. Andersson, I. (2008). Catalysis and regulation in Rubisco. Journal of Experimental Botany, 59, 1555–1568.

    Article  CAS  PubMed  Google Scholar 

  22. McDonald, A. E., Ivanov, A. G., Bode., R., Maxwell, D. P., Rodermel, S. R., & Huner, N. P. A. (2011). Flexibility in photosynthetic electron transport: The physiological role of plastoquinol terminal oxidase (PTOX). Biochimica et Biophysica Acta, 1807, 954–967.

    Article  CAS  PubMed  Google Scholar 

  23. Cherepanov, D. A., Milanovski, G. E., Petrova, A. A., Tikhonov, A. N., & Semenov, A. Yu. (2017). Electron transport through the acceptor side of photosystem I: Interaction with exogenous acceptors and molecular oxygen. Biochemistry (Moscow), 82, 1249–1268.

    Article  CAS  Google Scholar 

  24. Kuvykin, I. V., Vershubskii, A. V., Ptushenko, V. V., & Tikhonov, A. N. (2008). Oxygen as an alternative electron acceptor in the photosynthetic electron transport chain of C3 plants. Biochemistry, 73, 1063–1075.

    CAS  PubMed  Google Scholar 

  25. Kuvykin, I. V., Ptushenko, V. V., Vershubskii, A. V., & Tikhonov, A. N. (2011). Regulation of electron transport in C3 plant chloroplasts in situ and in silico: short-term effects of atmospheric CO2 and O2. Biochimica et Biophysica Acta, 1807, 336–347.

    Article  CAS  PubMed  Google Scholar 

  26. Ryzhikov, S. B., & Tikhonov, A. N. (1988). Regulation of electron transfer in photosynthetic membranes of higher plants. Biophysics, 33, 642–646.

    CAS  Google Scholar 

  27. Tikhonov, A. N., & Subczynski, W. K. (2005). Application of spin labels to membrane bioenergetics (photosynthetic systems of higher plants). In S. S. Eaton, G. R. Eaton, & L. J. Berliner (Eds.), Biomedical EPR—Part A: Free radicals, metals, medicine, and physiology, Vol. 23 (pp. 147–194). Boston, MA: Kluwer Academic/Plenum Publishers.

  28. Webber, A. N., & Lubitz, W. (2001). P700: The primary electron donor of photosystem I. Biochimica et Biophysica Acta, 1507, 61–79.

    Article  CAS  PubMed  Google Scholar 

  29. Tikhonov, A. N. (2015). Induction events and short-term regulation of electron transport in chloroplasts: an overview. Photosynthesis Research, 125, 65–94.

    Article  CAS  PubMed  Google Scholar 

  30. Tikhonov, A. N. (2012). Energetic and regulatory role of proton potential in chloroplasts. Biochemistry (Moscow), 77, 956–974.

    Article  CAS  Google Scholar 

  31. Tikhonov, A. N. (2013). pH-Dependent regulation of electron transport and ATP synthesis in chloroplasts. Photosynthesis Research, 116, 511–534.

    Article  CAS  PubMed  Google Scholar 

  32. Joliot, P., & Joliot, A. (2006). Cyclic electron flow in C3 plants. Biochimica et Biophysica Acta, 1757, 362–368.

    Article  CAS  PubMed  Google Scholar 

  33. Bulychev, A. A., & Vredenberg, W. J. (2010). Induction kinetics of photosystem I-activated P700 oxidation in plant leaves and their dependence on pre-energization. Russian Journal of Plant Physiology, 57, 599–608.

    Article  CAS  Google Scholar 

  34. Bulychev, A. A., Cherkashin, A. A., & Rubin, A. B. (2010). Dependence of chlorophyll P700 redox transients during induction period on the transmembrane distribution of protons in chloroplasts of pea leaves. Russian Journal of Plant Physiology, 57, 23–31.

    Google Scholar 

  35. Buchanan, B. B. (1980). Role of light in the regulation of chloroplast enzymes. Annual Review of Plant Physiology, 31, 341–374.

    Article  CAS  Google Scholar 

  36. Foyer, C. H., Furban, R. T., Harbinson, J., & Horton, P. (1990). The mechanisms contributing to photosynthetic control of electron transport by carbon assimilation in leaves. Photosynthesis Research, 25, 83–100.

    Article  CAS  PubMed  Google Scholar 

  37. Buchanan, B. B. (1991). Regulation of CO2 assimilation in oxygenic photosynthesis: the ferredoxin/thioredoxin system. Perspective on its discovery, present status, and future development. Archives of Biochemistry and Biophysics, 288, 1–9.

    Article  CAS  PubMed  Google Scholar 

  38. Foyer, C. H., Lelandais, M., & Harbinson, J. (1992). Control of the quantum efficiencies of photosystems I and II, electron flow, and enzyme activation following dark-to-light transitions in pea leaves. Plant Physiology, 99, 979–986.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Demmig-Adams, B., Cohu, C. M., Muller, O., & Adams, W. W. (2012). Modulation of photosynthetic energy conversion efficiency in nature: from seconds to seasons. Photosynthesis Research, 113, 75–88.

    Article  CAS  PubMed  Google Scholar 

  40. Jahns, P., & Holzwarth, A. R. (2012). The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochimica et Biophysica Acta, 1817, 182–193.

    Article  CAS  PubMed  Google Scholar 

  41. Tikhonov, A. N. (2014). The cytochrome b 6 f complex at the crossroad of photosynthetic electron transport pathways. Plant Physiology and Biochemistry, 81, 163–183.

    Article  CAS  PubMed  Google Scholar 

  42. Jarvi, S., Gollan, P. J. & Aro, E.-M. (2013). Understanding the roles of the thylakoid lumen in photosynthetic regulation. Frontiers in Plant Science. https://doi.org/10.3389/fpls.2013.00434.

  43. Tikhonov A. N. (2018). The cytochrome b 6 f complex: biophysical aspects of its functioning in chloroplasts. In J. R. Harris & E. J. Boekema (Eds.), Membrane protein complexes: structure and function, subcellular biochemistry. Vol. 87 (pp. 287–328). New York: Springer Nature Singapore Pte Ltd.

  44. Lemeille, S., & Rochaix, J.-D. (2010). State transitions at the crossroad of thylakoid signaling pathways. Photosynthesis Research, 106, 33–46.

    Article  CAS  PubMed  Google Scholar 

  45. Allen, J. F. (2003). Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain. Trends in Plant Sciences, 8, 15–19.

    Article  CAS  Google Scholar 

  46. Laisk, A., Talts, E., Oja, V., Eichelmann, H., & Peterson, R. B. (2010). Fast cyclic electron transport around photosystem I in leaves under far-red light: a proton-uncoupled pathway? Photosynthesis Research, 103, 79–95.

    Article  CAS  PubMed  Google Scholar 

  47. Ptushenko, V. V., Zhigalova, T. V. Avercheva, O. V., & Tikhonov A. N. (2018). Three phases of energy-dependent induction of P + 700 and Chl a fluorescence in Tradescantia fluminensis leaves. Photosynthesis Research. https://doi.org/10.1007/s11120-018-0494-z.

  48. Trubitsin, B. V., Vershubskii, A. V., Priklonskii, V. I., & Tikhonov, A. N. (2015). Short-term regulation and alternative pathways of photosynthetic electron transport in Hibiscus rosa-sinensis leaves. Journal of Photochemistry and Photobiology B, 152, 400–415.

    Article  CAS  Google Scholar 

  49. Foyer, C. H., & Noctor, G. (2011). Ascorbate and glutathione: The heart of the redox hub. Plant Physiology, 155, 2–18.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Trubitsin, B. V., Mamedov, M. D., Vitukhnovskaya, L. A., Semenov, A., Yu., & Tikhonov, A. N. (2003). EPR study of light-induced regulation of photosynthetic electron transport in photosystem I complexes. FEBS Letters, 544, 15–20.

    Article  CAS  PubMed  Google Scholar 

  51. Trubitsin, B. V., Ptushenko, V. V., Koksharova, O. A., Mamedov, M. D., Vitukhnovskaya, L. A., Grigor’ev, I. A., Semenov, A., Yu., & Tikhonov, A. N. (2005). EPR study of electron transport in the cyanobacterium Synechocystis sp. PCC 6803. Oxygen-dependent interrelations between photosynthetic and respiratory electron transport chains. Biochimica et Biophysica Acta, 1708, 238–249.

    Article  CAS  PubMed  Google Scholar 

  52. Peschek, G. A. (1987). Respiratory electron transport. In P. Fay & C. Van Baalen (Eds.), The Cyanobacteria (pp. 119–161). Amsterdam, The Netherlands: Elsevier.

  53. Schmetterer, G. (1994). Cyanobacterial respiration. In D. A. Bryant (Ed.), The molecular biology of Cyanobacteria (pp. 409–435). Dordrecht, The Netherlands: Kluwer.

  54. Howitt, C. A., & Vermaas, W. F. J. (1998). Quinol and cytochrome oxidases in the cyanobacterium Synechocystis sp. PCC 6803. Biochemistry, 37, 17944–17951.

    Article  CAS  PubMed  Google Scholar 

  55. Ort, D. R., & Baker, N. R. (2002). A photoprotective role for O2 as an alternative electron sink in photosynthesis? Current Opinion in Plant Biology, 5, 193–198.

    Article  CAS  PubMed  Google Scholar 

  56. Murata, N., Takahashi, S., Nishiyama, Y., & Allakhverdiev, S. I. (2007). Photoinhibition of photosystem II under environmental stress. Biochimica et Biophysica Acta, 1767, 414–421.

    Article  CAS  PubMed  Google Scholar 

  57. Li, Z., Wakao, S., Fischer, B. B., & Niyogi, K. K. (2009). Sensing and responding to excess light. Annual Review of Plant Biology, 60, 239–260.

    Article  CAS  PubMed  Google Scholar 

  58. Asada, K. (2006). Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiology, 141, 391–396.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Backer, J. M., Budker, V. G., Eremenko, S. I., & Molin, Y. N. (1977). Detection of the kinetics of biochemical reactions with oxygen using exchange broadening in the ESR spectra of nitroxide radicals. Biochimica et Biophysica Acta, 460, 152–156.

    Article  CAS  PubMed  Google Scholar 

  60. Popp, C. A., & Hyde, J. S. (1981). Effects of oxygen on EPR spectra of nitroxide spin-labels probes of model membranes. Journal of Magnetic Resonance, 43, 249–258.

    CAS  Google Scholar 

  61. Pajak, S., Cieszka, K., Gurbiel, R., Subczynski, W. K., & Lukiewicz, S. J. (1978). EPR measurements of the oxygen consumption by tumor cells. Third meeting of the Polish Biophysical Society, Wroclaw-Olesnica, Book of Abstracts, p. 70.

  62. Lai, C. S., Hopwood, L. E., Hyde, J. S., & Lukiewicz, S. (1982). ESR studies of O2 uptake by Chinese hamster ovary cells during the cell cycle. Proceedings of the National Academy of Sciences of the United States of America, 79, 1166–1170.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Sarna, T., Duleba, A., Korytowski, W., & Swartz, H. M. (1980). Interaction of melanin with oxygen. Archives of Biochemistry and Biophysics, 200, 140–148.

    Article  CAS  PubMed  Google Scholar 

  64. Froncisz, W., Lai, C. S., & Hyde, J. S. (1985). Spin-label oximetry: kinetic study of cell respiration using a rapid-passage T1-sensitive electron spin resonance display. Proceedings of the National Academy of Sciences of the United States of America, 82, 411–415.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Kalyanaraman, B., Feix, J. B., Sieber, F., Thomas, J. P., & Girotti, A. W. (1987). Photodynamic action of merocyanine 540 on artificial and natural cell membranes: Involvement of singlet molecular oxygen. Proceedings of the National Academy of Sciences of the United States of America, 84, 2999–3003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Strzalka, K., Sarna, T., & Hyde, J. S. (1986). ESR oximetry: measurement of photosynthetic oxygen evolution by spin-probe technique. Photobiochemistry and Photobiophysics, 12, 67–71.

    CAS  Google Scholar 

  67. Strzalka, K., Walczak, T., Sarna, T., & Swartz, H. M. (1990). Measurements of time-resolved oxygen concentration changes in photosynthetic systems by nitroxide based ESR oximetry. Archives of Biochemistry and Biophysics, 281, 312–318.

    Article  CAS  PubMed  Google Scholar 

  68. Subczynski, W. K., Cieslikowska, D., & Tikhonov, A. N. (1990). Light-induced oxygen uptake in chloroplasts: ESR spin-label oximetry. Photosynthetica, 24, 75–84.

    Article  Google Scholar 

  69. Ligeza, A., Swartz, H. M., & Subczynski, W. K. (1994). Spin-label oximetry in dense cell suspensions: Problems in closed- and open-chambered methods. Current Topics in Biophysics, 18, 29–38.

    CAS  Google Scholar 

  70. Kusumi, A., Subczynski, W. K., & Hyde, J. S. (1982). Oxygen transport parameter in membranes as deduced by saturation recovery measurements of spin-lattice relaxation times of spin labels. Proceedings of the National Academy of Sciences of the United States of America, 79, 1854–1858.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Yin, J.-J., & Hyde, J. S. (1987). Spin-label saturation-recovery electron spin resonance measurements of oxygen transport in membranes. Zeitschrift für Physikalische Chemie, 153, 57–65.

    Article  CAS  Google Scholar 

  72. Subczynski, W. K., Hyde, J. S., & Kusumi, A. (1989). Oxygen permeability of phosphatidylcholine-cholesterol membranes. Proceedings of the National Academy of Sciences of the United States of America, 86, 4474–4478.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Subczynski, W. K., & Hyde, J. S. (1981). The diffusion-concentration product of oxygen in lipid bilayers using the spin-label T1 method. Biochimica et Biophysica Acta, 643, 283–291.

    Article  CAS  PubMed  Google Scholar 

  74. Altenbach, C., Froncisz, W., Hyde, J. S., & Hubbell, W. L. (1989). Conformation of spin-labeled melittin at membrane surfaces investigated by pulse saturation recovery and continuous wave power saturation electron paramagnetic resonance. Biophysical Journal, 56, 1183–1191.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Jajic, I., Wisniewska-Becker, A., Sarna, T., Jemiola-Rzeminska, M., & Strzalka, K. (2014). EPR spin labeling measurements of thylakoid membrane fluidity during barley leaf senescence. Journal of Plant Physiology, 171, 1046–1053.

    Article  CAS  PubMed  Google Scholar 

  76. Hyde, J. S., & Subczynski, W. K. (1984). Simulation of EPR spectra of the oxygen-sensitive spin-label probe CTPO. Journal of Magnetic Resonance, 56, 125–130.

    CAS  Google Scholar 

  77. Subczynski, W. K., & Hyde, J. S. (1984). Diffusion of oxygen in water and hydrocarbons using an electron spin resonance spin-label technique. Biophysical Journal, 45, 743–748.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Hyde, J. S., & Subczynski, W. K. (1989). Spin-label oximetry. In L. J. Berliner & J. Reuben (Eds.), Biological magnetic resonance. Vol. 8 (pp. 399–425). New York: Plenum Press.

  79. Feix, J. B., & Klug, C. S. (1998). Site-directed spin labeling of membrane proteins and peptide-membrane interaction. In L. J. Berliner (Ed.), Biological magnetic resonance. Spin labeling: the next millennium. Vol. 14 (pp. 251–281). New York: Plenum Press.

  80. Ligeza, A., Tikhonov, A. N., Hyde, J. S., & Subczynski, W. K. (1998). Oxygen permeability of thylakoid membranes: EPR spin labeling study. Biochimica et Biophysica Acta, 1365, 453–463.

    Article  CAS  PubMed  Google Scholar 

  81. Halpern, H. J., Perik, M., Nguyen, T.-D., Spencer, D. P., Teicher, B. A., & Lin, Y. J. (1990). Selective isotopic labeling of a nitroxide spin label to enhance sensitivity for T2 oximetry. Journal of Magnetic Resonance, 90, 40–51.

    CAS  Google Scholar 

  82. Ardenkjaer-Larsen, J. H., Laursen, I., Leunbach, I., Ehnholm, G., Wistrand, L.-G., Petersson, J. S., & Golman, K. (1998). EPR and DNP properties of certain novel single electron contrast agents intended for oximetric imaging. Journal of Magnetic Resonance, 133, 1–12.

    Article  CAS  PubMed  Google Scholar 

  83. Halpern, H. J., Chandramouli, G. V. R., Williams, B. B., Barth, E. D., & Galtsev, V. (1998). Challenge of 3- and 4-dimensional in vivo spectral spatial EPR imaging at radiofrequency with narrow line spin resonance. Twenty first International EPR Symposium, Denver, Abstract No. 124.

  84. Kocherginsky, N., & Swartz, H. M. (1995). Nitroxide spin labels: Reactions in biology and chemistry. Boca Raton: CRC Press.

  85. Ligeza, A., Wisniewska, A., & Subczynski, W. K. (1992). Paraffin oil particles as microscopic probes for oxygen measurement in biological systems: ESR spin-label oximetry. Current Topics in Biophysics, 16, 92–98.

    CAS  Google Scholar 

  86. Ligeza, A., Wisniewska, A., Subczynski, W. K., & Tikhonov, A. N. (1994). Oxygen production and consumption by chloroplasts in situ and in vitro as studied with microscopic spin label probes. Biochimica et Biophysica Acta, 1186, 201–208.

    Article  CAS  PubMed  Google Scholar 

  87. Liu, K. J., Grinstaff, M. W., Jiang, J. J., Suslick, K. S., Swartz, H. M., & Wang, W. (1994). In vivo measurement of oxygen concentration using sonochemically synthesized microspheres. Biophysical Journal, 67, 896–901.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Mainali, L., Vasquez-Vivar, J., Hyde, J. S., & Subczynski, W. K. (2015). Spin-labeled small unilamellar vesicles with the T1-sensitive saturation-recovery EPR display as an oxygen sensitive analyte for measurement of cellular respiration. Applied Magnetic Resonance, 46, 885–895.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Linke, W. F. (1965). Solubilities: Inorganic and metal organic compounds II. 4th ed. (pp. 1233–1236). Washington, DC: American Chemical Society.

  90. Vahidi, N., Clarkson, R. B., Liu, K. J., Norby, S. W., Wu, M., & Swartz, H. M. (1994). In Vivo and In Vitro EPR oximetry with fusinite: A new coal-derived, particulate EPR probe. Magnetic Resonance in Medicine, 31, 139–146.

    Article  CAS  PubMed  Google Scholar 

  91. Subczynski, W. K., & Swartz, H. M. (2005). EPR oximetry in biological and model samples. In S. S. Eaton, G. R. Eaton, & L. J. Berliner (Eds.), Biological magnetic resonance. In biomedical ESR–Part A: free radicals, metals, medicine, and physiology, Vol. 23 (pp. 229–282). Boston: Kluwer.

  92. Liu, K. J., Gast, P., Moussavi, M., Norby, S. W., Vahidi, N., Walczak, T., Wu, M., & Swartz, H. M. (1993). Lithium phtalocyanide: a probe for electron paramagnetic resonance oximetry in viable biological systems. Proceedings of the National Academy of Sciences of the United States of America, 90, 5438–5442.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Swartz, H. M. (2003). The measurement of oxygen in vivo using EPR techniques. In L. J. Berliner, (Ed.), Biological magnetic resonance 18: in vivo EPR (ESR): theory and applications (pp. 404–440). New York: Plenum Publishing Co.

  94. James, P. E., Grinberg, O. Y., Goda, F., Panz, T., O’Hara, J. A., & Swartz, H. M. (1997). Gloxy: an oxygen-sensitive coal for accurate measurement of low oxygen tensions in biological systems. Magnetic Resonance in Medicine, 37, 48–58.

    Article  Google Scholar 

  95. Ligeza, A., Tikhonov, A. N., & Subczynski, W. K. (1997). In situ measurements of oxygen production and consumption using paramagnetic fusinite particles injected into a bean leaf. Biochimica et Biophysica Acta, 1319, 133–137.

    Article  CAS  Google Scholar 

  96. Laureau, C., De Paepe, R., Latouche, G., Moreno-Chacon, M., Finazzi, G., Kuntz, M., Cornic, G., & Streb, P. (2013). Plastid terminal oxidase (PTOX) has the potential to act as a safety valve for excess excitation energy in the alpine plant species Ranunculus glacialis L. Plant, Cell and Environment, 36, 1296–1310.

    Article  CAS  PubMed  Google Scholar 

  97. Krieger-Liszkay, A., Fufezan, C., & Trebst, A. (2008). Singlet oxygen production in PS II and related protection mechanism. Photosynthesis Research, 98, 551–564.

    Article  CAS  PubMed  Google Scholar 

  98. Foyer, C. H., Neukermans, J., Queval, G., Noctor, G., & Harbinson, J. (2012). Photosynthetic control of electron transport and the regulation of gene expression. Journal of Experimental Botany, 63, 1637–1661.

    Article  CAS  PubMed  Google Scholar 

  99. Kozuleva, M. A., Petrova, A. A., Mamedov, M. D., Semenov, A. Y., & Ivanov, B. N. (2014). O2 reduction by photosystem I involves phylloquinone under steady-state illumination. FEBS Letters, 588, 4364–4368.

    Article  CAS  PubMed  Google Scholar 

  100. Daisuke, T., Takumi, S., Hashiguchi, M., Sejima, T., & Miyake, C. (2016). Superoxide and singlet oxygen produced within the thylakoid membranes both cause Photosystem I photoinhibition. Plant Physiology, 171, 1626–1634.

    Article  CAS  Google Scholar 

  101. Trubitsin, B. V., & Tikhonov, A. N. (2003). Determination of a transmembrane pH difference in chloroplasts with a spin label Tempamine. Journal of Magnetic Resonance, 163, 257–269.

    Article  CAS  PubMed  Google Scholar 

  102. Vershubskii, A. V., Trubitsin, B. V., Priklonskii, V. I., & Tikhonov, A. N. (2017). Lateral heterogeneity of the proton potential along the thylakoid membranes of chloroplasts. Biochimica et Biophysics Acta, 1859, 388–401.

    Article  CAS  Google Scholar 

  103. Tikhonov, A. N. (2017). Photosynthetic electron and proton transport in chloroplasts: EPR study of ΔpH generation, an overview. Cell Biochemistry and Biophysics, 75, 421–432.

    Article  CAS  PubMed  Google Scholar 

  104. Ptushenko, V. V., Ikryannikova, L. N., Grigor’ev, I. A., Kirilyuk, I. A., Trubitsin, B. V., & Tikhonov, A. N. (2006). Interaction of imidazoline and imidazolidin-based derivatives of nitroxide radicals with chloroplasts. Applied Magnetic Resonance, 30, 329–343.

    Article  CAS  Google Scholar 

  105. Ahmad, R., & Kuppusamy, P. (2010). Theory, instrumentation, and applications of EPR oximetry. Chemical Reviews, 110, 3212–3236.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Meenakshisundaram, G., Eteshola, E., Pandian, R. P., Bratasz, A., Lee, S. C., & Kuppusamy, P. (2009). Fabrication and physical evaluation of a polymer-encapsulated paramagnetic probe for biomedical oximetry. Biomedical Microdevices, 11, 773–782.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Hou, H., Khan, N., & Kuppusamy, P. (2017). Measurement of pO2 in a pre-clinical model of rabbit tumor using OxyChip, a paramagnetic oxygen sensor. Advances in Experimental Medicine and Biology, 977, 313–318.

    Article  CAS  PubMed  Google Scholar 

  108. Hou, H., Khan, N., Gohain, S., Kuppusamy, M. L., & Kuppusamy, P. (2018). Pre-clinical evaluation of OxyChip for long-term EPR oximetry. Biomed Microdevices 6, 20(2), 29. https://doi.org/10.1007/s10544-018-0272-x.

    Article  CAS  Google Scholar 

  109. Epel, B., Redler, G., & Halpern, H. J. (2014). How in vivo EPR measures and images oxygen. Advances in Experimental Medicine and Biology, 812, 113–119.

    Article  PubMed  PubMed Central  Google Scholar 

  110. Swartz, H. M., Hou, H., Khan, N., Jarvis, L. A., Chen, E. Y., Williams, B. B., & Kuppusamy, P. (2014). Advances in probes and methods for clinical EPR oximetry. Advances in Experimental Medicine and Biology, 812, 73–79.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Epel, B., & Halpern, H. J. (2015). In vivo pO2 imaging of tumors: oxymetry with very low-frequency electron paramagnetic resonance. Methods in Enzymology, 564, 501–527.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Khramtsov, V. V., Grigor’ev, I. A., Foster, M. A., Lurie, D. J., & Nicholson, I. (2000). Biological applications of spin pH probes. Cellular and Molecular Biology, 46, 1361–1374.

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported in part by the Russian Foundation for Basic Researches, Projects 15-04-03790 and 18-04-00214 (A. N. Tikhonov) and by the National Institutes of Health, USA, Grants EY015526 and EB001980 (W. K. Subczynski).

Author information

Authors and Affiliations

  1. Department of Biophysics, Faculty of Physics, M. V. Lomonosov Moscow State University, Moscow, Russia

    Alexander N. Tikhonov

  2. Department of Biophysics, Medical College of Wisconsin, Milwaukee, WI, USA

    Witold K. Subczynski

Authors
  1. Alexander N. Tikhonov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Witold K. Subczynski
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alexander N. Tikhonov.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tikhonov, A.N., Subczynski, W.K. Oxygenic photosynthesis: EPR study of photosynthetic electron transport and oxygen-exchange, an overview. Cell Biochem Biophys 77, 47–59 (2019). https://doi.org/10.1007/s12013-018-0861-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12013-018-0861-6

Keywords

Search

Navigation