Cell Biochemistry and Biophysics

, Volume 77, Issue 1, pp 47–59 | Cite as

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

  • Alexander N. TikhonovEmail author
  • Witold K. Subczynski
Original Paper


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.


Photosynthesis Chloroplasts Cyanobacteria Electron transport EPR Spin-label oximetry Oxygen exchange 



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).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. 1.
    Edwards, G. E., & Walker, D. A. (1983). C3, C4: Mechanisms, and cellular and environmental regulation of photosynthesis. Oxford: Blackwell.Google Scholar
  2. 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.CrossRefGoogle Scholar
  3. 3.
    Blankenship, R. E. (2002). Molecular mechanisms of photosynthesis. Oxford: Blackwell Science.CrossRefGoogle Scholar
  4. 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.CrossRefGoogle Scholar
  5. 5.
    Nelson, N., & Yocum, C. (2006). Structure and function of photosystems I and II. Annual Review of Plant Biology, 57, 521–565.CrossRefGoogle Scholar
  6. 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.CrossRefGoogle Scholar
  7. 7.
    Daum, B., & Kuhlbrandt, W. (2011). Electron tomography of plant thylakoid membranes. Journal of Experimental Botany, 62, 2393–2402.CrossRefGoogle Scholar
  8. 8.
    Skulachev, V. P., Bogachev, A. V., & Kasparinsky, F. O. (2012). Principles of bioenergetics. Berlin: Springer.Google Scholar
  9. 9.
    Ruban, A. V. (2012). The photosynthetic membrane: Molecular mechanisms and biophysics of light harvesting. Oxford: Wiley-Blackwell.CrossRefGoogle Scholar
  10. 10.
    Kirchhoff, H. (2013). Architectural switches in plant thylakoid membranes. Photosynthesis Research, 116, 481–487.CrossRefGoogle Scholar
  11. 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.CrossRefGoogle Scholar
  12. 12.
    Nelson, N., & Junge, W. (2015). Structure and energy transfer in photosystems of oxygenic photosynthesis. Annual Review of Biochemistry, 84, 659–683.CrossRefGoogle Scholar
  13. 13.
    Mitchell, P. (1966). Chemiosmotic coupling in oxidative and photosynthetic phosphorylation. Biological Review, 41, 445–502.CrossRefGoogle Scholar
  14. 14.
    Junge, W., & Nelson, N. (2015). ATP synthase. Annual Review of Biochemistry, 83, 631–657.CrossRefGoogle Scholar
  15. 15.
    Shikanai, T. (2007). Cyclic electron transport around photosystem I: genetic approaches. Annual Review of Plant Biology, 58, 199–217.CrossRefGoogle Scholar
  16. 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.CrossRefGoogle Scholar
  17. 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.CrossRefGoogle Scholar
  18. 18.
    Foyer, C. H., & Noctor, G. (2000). Oxygen processing in photosynthesis: regulation and signalling. New Phytologist, 146, 359–388.CrossRefGoogle Scholar
  19. 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.CrossRefGoogle Scholar
  20. 20.
    Peltier, G., & Cournac, L. (2002). Chlororespiration. Annual Review of Plant Biology, 53, 523–550.CrossRefGoogle Scholar
  21. 21.
    Andersson, I. (2008). Catalysis and regulation in Rubisco. Journal of Experimental Botany, 59, 1555–1568.CrossRefGoogle Scholar
  22. 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.CrossRefGoogle Scholar
  23. 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.CrossRefGoogle Scholar
  24. 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.Google Scholar
  25. 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.CrossRefGoogle Scholar
  26. 26.
    Ryzhikov, S. B., & Tikhonov, A. N. (1988). Regulation of electron transfer in photosynthetic membranes of higher plants. Biophysics, 33, 642–646.Google Scholar
  27. 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.Google Scholar
  28. 28.
    Webber, A. N., & Lubitz, W. (2001). P700: The primary electron donor of photosystem I. Biochimica et Biophysica Acta, 1507, 61–79.CrossRefGoogle Scholar
  29. 29.
    Tikhonov, A. N. (2015). Induction events and short-term regulation of electron transport in chloroplasts: an overview. Photosynthesis Research, 125, 65–94.CrossRefGoogle Scholar
  30. 30.
    Tikhonov, A. N. (2012). Energetic and regulatory role of proton potential in chloroplasts. Biochemistry (Moscow), 77, 956–974.CrossRefGoogle Scholar
  31. 31.
    Tikhonov, A. N. (2013). pH-Dependent regulation of electron transport and ATP synthesis in chloroplasts. Photosynthesis Research, 116, 511–534.CrossRefGoogle Scholar
  32. 32.
    Joliot, P., & Joliot, A. (2006). Cyclic electron flow in C3 plants. Biochimica et Biophysica Acta, 1757, 362–368.CrossRefGoogle Scholar
  33. 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.CrossRefGoogle Scholar
  34. 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. 35.
    Buchanan, B. B. (1980). Role of light in the regulation of chloroplast enzymes. Annual Review of Plant Physiology, 31, 341–374.CrossRefGoogle Scholar
  36. 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.CrossRefGoogle Scholar
  37. 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.CrossRefGoogle Scholar
  38. 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.CrossRefGoogle Scholar
  39. 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.CrossRefGoogle Scholar
  40. 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.CrossRefGoogle Scholar
  41. 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.CrossRefGoogle Scholar
  42. 42.
    Jarvi, S., Gollan, P. J. & Aro, E.-M. (2013). Understanding the roles of the thylakoid lumen in photosynthetic regulation. Frontiers in Plant Science.
  43. 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.Google Scholar
  44. 44.
    Lemeille, S., & Rochaix, J.-D. (2010). State transitions at the crossroad of thylakoid signaling pathways. Photosynthesis Research, 106, 33–46.CrossRefGoogle Scholar
  45. 45.
    Allen, J. F. (2003). Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain. Trends in Plant Sciences, 8, 15–19.CrossRefGoogle Scholar
  46. 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.CrossRefGoogle Scholar
  47. 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.
  48. 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.CrossRefGoogle Scholar
  49. 49.
    Foyer, C. H., & Noctor, G. (2011). Ascorbate and glutathione: The heart of the redox hub. Plant Physiology, 155, 2–18.CrossRefGoogle Scholar
  50. 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.CrossRefGoogle Scholar
  51. 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.CrossRefGoogle Scholar
  52. 52.
    Peschek, G. A. (1987). Respiratory electron transport. In P. Fay & C. Van Baalen (Eds.), The Cyanobacteria (pp. 119–161). Amsterdam, The Netherlands: Elsevier.Google Scholar
  53. 53.
    Schmetterer, G. (1994). Cyanobacterial respiration. In D. A. Bryant (Ed.), The molecular biology of Cyanobacteria (pp. 409–435). Dordrecht, The Netherlands: Kluwer.Google Scholar
  54. 54.
    Howitt, C. A., & Vermaas, W. F. J. (1998). Quinol and cytochrome oxidases in the cyanobacterium Synechocystis sp. PCC 6803. Biochemistry, 37, 17944–17951.CrossRefGoogle Scholar
  55. 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.CrossRefGoogle Scholar
  56. 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.CrossRefGoogle Scholar
  57. 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.CrossRefGoogle Scholar
  58. 58.
    Asada, K. (2006). Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiology, 141, 391–396.CrossRefGoogle Scholar
  59. 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.CrossRefGoogle Scholar
  60. 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.Google Scholar
  61. 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.Google Scholar
  62. 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.CrossRefGoogle Scholar
  63. 63.
    Sarna, T., Duleba, A., Korytowski, W., & Swartz, H. M. (1980). Interaction of melanin with oxygen. Archives of Biochemistry and Biophysics, 200, 140–148.CrossRefGoogle Scholar
  64. 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.CrossRefGoogle Scholar
  65. 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.CrossRefGoogle Scholar
  66. 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.Google Scholar
  67. 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.CrossRefGoogle Scholar
  68. 68.
    Subczynski, W. K., Cieslikowska, D., & Tikhonov, A. N. (1990). Light-induced oxygen uptake in chloroplasts: ESR spin-label oximetry. Photosynthetica, 24, 75–84.CrossRefGoogle Scholar
  69. 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.Google Scholar
  70. 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.CrossRefGoogle Scholar
  71. 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.CrossRefGoogle Scholar
  72. 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.CrossRefGoogle Scholar
  73. 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.CrossRefGoogle Scholar
  74. 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.CrossRefGoogle Scholar
  75. 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.CrossRefGoogle Scholar
  76. 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.Google Scholar
  77. 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.CrossRefGoogle Scholar
  78. 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.Google Scholar
  79. 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.Google Scholar
  80. 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.CrossRefGoogle Scholar
  81. 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.Google Scholar
  82. 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.CrossRefGoogle Scholar
  83. 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.Google Scholar
  84. 84.
    Kocherginsky, N., & Swartz, H. M. (1995). Nitroxide spin labels: Reactions in biology and chemistry. Boca Raton: CRC Press.Google Scholar
  85. 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.Google Scholar
  86. 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.CrossRefGoogle Scholar
  87. 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.CrossRefGoogle Scholar
  88. 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.CrossRefGoogle Scholar
  89. 89.
    Linke, W. F. (1965). Solubilities: Inorganic and metal organic compounds II. 4th ed. (pp. 1233–1236). Washington, DC: American Chemical Society.Google Scholar
  90. 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.CrossRefGoogle Scholar
  91. 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.Google Scholar
  92. 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.CrossRefGoogle Scholar
  93. 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.Google Scholar
  94. 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.CrossRefGoogle Scholar
  95. 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.CrossRefGoogle Scholar
  96. 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.CrossRefGoogle Scholar
  97. 97.
    Krieger-Liszkay, A., Fufezan, C., & Trebst, A. (2008). Singlet oxygen production in PS II and related protection mechanism. Photosynthesis Research, 98, 551–564.CrossRefGoogle Scholar
  98. 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.CrossRefGoogle Scholar
  99. 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.CrossRefGoogle Scholar
  100. 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.CrossRefGoogle Scholar
  101. 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.CrossRefGoogle Scholar
  102. 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.CrossRefGoogle Scholar
  103. 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.CrossRefGoogle Scholar
  104. 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.CrossRefGoogle Scholar
  105. 105.
    Ahmad, R., & Kuppusamy, P. (2010). Theory, instrumentation, and applications of EPR oximetry. Chemical Reviews, 110, 3212–3236.CrossRefGoogle Scholar
  106. 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.CrossRefGoogle Scholar
  107. 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.CrossRefGoogle Scholar
  108. 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. Scholar
  109. 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.CrossRefGoogle Scholar
  110. 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.CrossRefGoogle Scholar
  111. 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.CrossRefGoogle Scholar
  112. 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.Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Biophysics, Faculty of PhysicsM. V. Lomonosov Moscow State UniversityMoscowRussia
  2. 2.Department of BiophysicsMedical College of WisconsinMilwaukeeUSA

Personalised recommendations