Skip to main content
Log in

Superoxide Anion Radical Generation in Photosynthetic Electron Transport Chain

  • REVIEW
  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

Abstract

This review analyzes data available in the literature on the rates, characteristics, and mechanisms of oxygen reduction to a superoxide anion radical at the sites of photosynthetic electron transport chain where this reduction has been established. The existing assumptions about the role of the components of these sites in this process are critically examined using thermodynamic approaches and results of the recent studies. The process of O2 reduction at the acceptor side of PSI, which is considered the main site of this process taking place in the photosynthetic chain, is described in detail. Evolution of photosynthetic apparatus in the context of controlling the leakage of electrons to O2 is explored. The reasons limiting application of the results obtained with the isolated segments of the photosynthetic chain to estimate the rates of O2 reduction at the corresponding sites in the intact thylakoid membrane are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

Fd:

ferredoxin

FNR:

ferredoxin:NADP+ oxidoreductase

DCPIP:

2,6-dichlorophenolindophenol

DNP-INT:

dinitrophenyl ether 2-iodine-4-nitrotimol

Em :

midpoint redox potential

PETC:

photosynthetic electron transport chain

PhQ:

phylloquinone

PQ:

plastoquinone

PSI:

photosystem I

PSII:

photosystem II

QA and QB :

primary and secondary quinone acceptors of photosystem II, respectively

QO and QR :

quinol-oxidizing (QO site) and quinol-reducing (QR site) sites of the b6f complex, respectively

ROS:

reactive oxygen species

References

  1. Mehler, A. H. (1951) Studies on reactions of illuminated chloroplasts: I. Mechanism of the reduction of oxygen and other hill reagents, Arch. Biochem. Biophys., 33, 65-77, https://doi.org/10.1016/0003-9861(51)90082-3.

    Article  CAS  PubMed  Google Scholar 

  2. Ivanov, B. N., Khorobrykh, S. A., Kozuleva, M. A., and Borisova-Mubarakshina, M. M. (2013) The role of oxygen and its reactive species in photosynthesis, in Photosynthesis: Questions to Answer and What We Know Today (Allakhverdiev, S. I., Rubin, A. B., and Shuvalov, V. A., eds) [in Russian], Institute of Computer-Aided Studies, Izhevsk, Vol. 1, pp. 407-460.

  3. Mubarakshina, M. M., and Ivanov, B. N. (2010) The production and scavenging of reactive oxygen species in the plastoquinone pool of chloroplast thylakoid membranes, Physiol. Plant., 140, 103-110, https://doi.org/10.1111/j.1399-3054.2010.01391.x.

    Article  CAS  PubMed  Google Scholar 

  4. Pospíšil, P. (2012) Molecular mechanisms of production and scavenging of reactive oxygen species by photosystem II, Biochim. Biophys. Acta, 1817, 218-231, https://doi.org/10.1016/j.bbabio.2011.05.017.

    Article  CAS  PubMed  Google Scholar 

  5. Kozuleva, M. A., and Ivanov, B. N. (2016) The mechanisms of oxygen reduction in the terminal reducing segment of the chloroplast photosynthetic electron transport chain, Plant Cell Physiol., 57, 1397-1404, https://doi.org/10.1093/pcp/pcw035.

    Article  CAS  PubMed  Google Scholar 

  6. Kozuleva, M. A., Ivanov, B. N., Vetoshkina, D. V., and Borisova-Mubarakshina, M. M. (2020) Minimizing an electron flow to molecular oxygen in photosynthetic electron transfer chain: an evolutionary view, Front. Plant Sci., 11, 211, https://doi.org/10.3389/fpls.2020.00211.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Sarewicz, M., Pintscher, S., Pietras, R., Borek, A., Bujnowicz, Ł., Hanke, G., Cramer, W. A., Finazzi, G., and Osyczka, A. (2021) Catalytic reactions and energy conservation in the cytochrome bc1 and b6f complexes of energy-transducing membranes, Chem. Rev., 121, 2020-2108, https://doi.org/10.1021/acs.chemrev.0c00712.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Allen, J. F., and Hall, D. O. (1973) Superoxide reduction as a mechanism of ascorbate-stimulated oxygen uptake by isolated chloroplasts, Biochem. Biophys. Res. Commun., 52, 856-862, https://doi.org/10.1016/0006-291X(73)91016-4.

    Article  CAS  PubMed  Google Scholar 

  9. Asada, K., Kiso, K., and Yoshikawa, K. (1974) Univalent reduction of molecular oxygen by spinach chloroplasts on illumination, J. Biol. Chem., 249, 2175-2181, https://doi.org/10.1016/S0021-9258(19)42815-9.

    Article  CAS  PubMed  Google Scholar 

  10. Wardman, P. (1990) Bioreductive activation of quinones: redox properties and thiol reactivity, Free Radic. Res. Commun., 8, 219-229, https://doi.org/10.3109/10715769009053355.

    Article  CAS  PubMed  Google Scholar 

  11. Takahashi, M., and Asada, K. (1988) Superoxide production in aprotic interior of chloroplast thylakoids, Arch. Biochem. Biophys., 267, 714-722, https://doi.org/10.1016/0003-9861(88)90080-X.

    Article  CAS  PubMed  Google Scholar 

  12. Kozuleva, M., Klenina, I., Proskuryakov, I., Kirilyuk, I., and Ivanov, B. (2011) Production of superoxide in chloroplast thylakoid membranes: ESR study with cyclic hydroxylamines of different lipophilicity, FEBS Lett., 585, 1067-1071, https://doi.org/10.1016/j.febslet.2011.03.004.

    Article  CAS  PubMed  Google Scholar 

  13. Kozuleva, M., Klenina, I., Mysin, I., Kirilyuk, I., Opanasenko, V., Proskuryakov, I., and Ivanov, B. (2015) Quantification of superoxide radical production in thylakoid membrane using cyclic hydroxylamines, Free Radic. Biol. Med., 89, 1014-1023, https://doi.org/10.1016/j.freeradbiomed.2015.08.016.

    Article  CAS  PubMed  Google Scholar 

  14. Kozuleva, M., Goss, T., Twachtmann, M., Rudi, K., Trapka, J., Selinski, J., Ivanov, B., Garapati, P., Steinhoff, H. J., Hase, T., Scheibe, R., Klare, J. P., and Hanke, G. T. (2016) Ferredoxin:NADP(H) oxidoreductase abundance and location influences redox poise and stress tolerance, Plant Physiol., 172, 1480-1493, https://doi.org/10.1104/pp.16.01084.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Fantuzzi, A., Allgöwer, F., Baker, H., McGuire, G., Teh, W. K., Gamiz-Hernandez, A. P., Kaila, V. R. I., and Rutherford, A. W. (2022) Bicarbonate-controlled reduction of oxygen by the QA semiquinone in Photosystem II in membranes, Proc. Natl. Acad. Sci. USA, 119, e2116063119, https://doi.org/10.1073/pnas.2116063119.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Khorobrykh, S. A., and Ivanov, B. N. (2002) Oxygen reduction in a plastoquinone pool of isolated pea thylakoids, Photosynth. Res., 71, 209-219, https://doi.org/10.1023/A:1015583502345.

    Article  CAS  PubMed  Google Scholar 

  17. 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, https://doi.org/10.1016/0014-5793(83)80957-0.

    Article  CAS  Google Scholar 

  18. Fan, D.-Y., Hope, A. B., Smith, P. J., Jia, H., Pace, R. J., Anderson, J. M., and Chow, W. S. (2007) The stoichiometry of the two photosystems in higher plants revisited, Biochim. Biophys. Acta Bioenerg., 1767, 1064-1072, https://doi.org/10.1016/j.bbabio.2007.06.001.

    Article  CAS  Google Scholar 

  19. Baniulis, D., Hasan, S. S., Stofleth, J. T., and Cramer, W. A. (2013) Mechanism of enhanced superoxide production in the cytochrome b6f complex of oxygenic photosynthesis, Biochemistry, 52, 8975-8983, https://doi.org/10.1021/bi4013534.

    Article  CAS  PubMed  Google Scholar 

  20. Kozuleva, M., Petrova, A., Milrad, Y., Semenov, A., Ivanov, B., Redding, K. E., and Iftach, Y. (2021) Phylloquinone is the principal Mehler reaction site within photosystem I in high light, Plant Physiol., 186, 1848-1858, https://doi.org/10.1093/plphys/kiab221.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Hosein, B., and Palmer, G. (1983) The kinetics and mechanism of oxidation of reduced spinach ferredoxin by molecular oxygen and its reduced products, Biochim. Biophys. Acta Bioenerg., 723, 383-390, https://doi.org/10.1016/0005-2728(83)90045-2.

    Article  CAS  Google Scholar 

  22. Golbeck, J., and Radmer, R. (1984) Is the rate of oxygen uptake by reduced ferredoxin sufficient to account for photosystem I-mediated O2 reduction, Adv. Photosynth. Res., 1, 561.

    CAS  Google Scholar 

  23. Böhme, H. (1978) Quantitative determination of ferredoxin, ferredoxin-NADP+ reductase and plastocyanin in spinach chloroplasts, Eur. J. Biochem., 83, 137-141, https://doi.org/10.1111/j.1432-1033.1978.tb12077.x.

    Article  PubMed  Google Scholar 

  24. McKenzie, S. D., Ibrahim, I. M., Aryal, U. K., and Puthiyaveetil, S. (2020) Stoichiometry of protein complexes in plant photosynthetic membranes, Biochim. Biophys. Acta Bioenerg., 1861, 148141, https://doi.org/10.1016/j.bbabio.2019.148141.

    Article  CAS  PubMed  Google Scholar 

  25. Frankel, L. K., Sallans, L., Limbach, P. A., and Bricker, T. M. (2013) Oxidized amino acid residues in the vicinity of QA and PheoD1 of the photosystem II reaction center: putative generation sites of reducing-side reactive oxygen species, PLoS One, 8, e58042, https://doi.org/10.1371/journal.pone.0058042.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Kale, R., Hebert, A. E., Frankel, L. K., Sallans, L., Bricker, T. M., and Pospíšil, P. (2017) Amino acid oxidation of the D1 and D2 proteins by oxygen radicals during photoinhibition of Photosystem II, Proc. Natl. Acad. Sci. USA, 114, 2988-2993, https://doi.org/10.1073/pnas.1618922114.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Kumar, A., Prasad, A., Sedlářová, M., Kale, R., Frankel, L. K., Sallans, L., Bricker, T. M., and Pospíšil, P. (2021) Tocopherol controls D1 amino acid oxidation by oxygen radicals in Photosystem II, Proc. Natl. Acad. Sci. USA, 118, e2019246118, https://doi.org/10.1073/pnas.2019246118.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Taylor, R. M., Sallans, L., Frankel, L. K., and Bricker, T. M. (2018) Natively oxidized amino acid residues in the spinach cytochrome b6f complex, Photosynth. Res., 137, 141-151, https://doi.org/10.1007/s11120-018-0485-0.

    Article  CAS  PubMed  Google Scholar 

  29. Ananyev, G., Renger, G., Wacker, U., and Klimov, V. (1994) The photoproduction of superoxide radicals and the superoxide dismutase activity of Photosystem II. The possible involvement of cytochrome b559, Photosynth. Res., 41, 327-338, https://doi.org/10.1007/BF00019410.

    Article  CAS  PubMed  Google Scholar 

  30. Cleland, R. E., and Grace, S. C. (1999) Voltammetric detection of superoxide production by photosystem II, FEBS Lett., 457, 348-352, https://doi.org/10.1016/S0014-5793(99)01067-4.

    Article  CAS  PubMed  Google Scholar 

  31. Brinkert, K., Causmaecker, S. D., Krieger-Liszkay, A., Fantuzzi, A., and Rutherford, A. W. (2016) Bicarbonate-induced redox tuning in Photosystem II for regulation and protection, Proc. Natl. Acad. Sci. USA, 113, 12144-12149, https://doi.org/10.1073/pnas.1608862113.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Linke, K., and Ho, F. M. (2014) Water in photosystem II: structural, functional and mechanistic considerations, Biochim. Biophys. Acta Bioenerg., 1837, 14-32, https://doi.org/10.1016/j.bbabio.2013.08.003.

    Article  CAS  Google Scholar 

  33. Causmaecker, S. D., Douglass, J. S., Fantuzzi, A., Nitschke, W., and Rutherford, A. W. (2019) Energetics of the exchangeable quinone, QB, in Photosystem II, Proc. Natl. Acad. Sci. USA, 116, 19458-19463, https://doi.org/10.1073/pnas.1910675116.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Kruk, J., and Strzałka, K. (1999) Dark reoxidation of the plastoquinone-pool is mediated by the low-potential form of cytochrome b-559 in spinach thylakoids, Photosynth. Res., 62, 273-279, https://doi.org/10.1023/A:1006374319191.

    Article  CAS  Google Scholar 

  35. Pospíšil, P., Šnyrychová, I., Kruk, J., Strzałka, K., and Nauš, J. (2006) Evidence that cytochrome b559 is involved in superoxide production in photosystem II: effect of synthetic short-chain plastoquinones in a cytochrome b559 tobacco mutant, Biochem. J., 397, 321-327, https://doi.org/10.1042/BJ20060068.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Müh, F., and Zouni, A. (2016) Cytochrome b 559 in Photosystem II, in Adv. Photosynth. Respir. Springer, Dordrecht, 41, 143-175, https://doi.org/10.1007/978-94-017-7481-9_8.

  37. Shuvalov, V. A., Schreiber, U., and Heber, U. (1994) Spectral and thermodynamic properties of the two hemes of the D1D2cytochrome b-559 complex of spinach, FEBS Lett., 337, 226-230, https://doi.org/10.1016/0014-5793(94)80196-7.

    Article  CAS  PubMed  Google Scholar 

  38. Yadav, D. K., Prasad, A., Kruk, J., and Pospíšil, P. (2014) Evidence for the involvement of loosely bound plastosemiquinones in superoxide anion radical production in photosystem II, PLoS One, 9, e115466, https://doi.org/10.1371/journal.pone.0115466.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Khorobrykh, A. (2019) Hydrogen peroxide and superoxide anion radical photoproduction in PSII preparations at various modifications of the water-oxidizing complex, Plants, 8, 329, https://doi.org/10.3390/plants8090329.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Mubarakshina, M., Khorobrykh, S., and Ivanov, B. (2006) Oxygen reduction in chloroplast thylakoids results in production of hydrogen peroxide inside the membrane, Biochim. Biophys. Acta Bioenerg., 1757, 1496-1503, https://doi.org/10.1016/j.bbabio.2006.09.004.

    Article  CAS  Google Scholar 

  41. McCauley, S. W., and Melis, A. (1986) Quantitation of plastoquinone photoreduction in spinach chloroplasts, Photosynth. Res., 8, 3-16, https://doi.org/10.1007/BF00028472.

    Article  CAS  PubMed  Google Scholar 

  42. Khorobrykh, S., Mubarakshina, M., and Ivanov, B. (2004) Photosystem I is not solely responsible for oxygen reduction in isolated thylakoids, Biochim. Biophys. Acta Bioenerg., 1657, 164-167, https://doi.org/10.1016/j.bbabio.2004.04.009.

    Article  CAS  Google Scholar 

  43. Forquer, I., Covian, R., Bowman, M. K., Trumpower, B. L., and Kramer, D. M. (2006) Similar transition states mediate the Q-cycle and superoxide production by the cytochrome bc1 complex, J. Biol. Chem., 281, 38459-38465, https://doi.org/10.1074/jbc.M605119200.

    Article  CAS  PubMed  Google Scholar 

  44. Vetoshkina, D. V., Ivanov, B. N., Khorobrykh, S. A., Proskuryakov, I. I., and Borisova-Mubarakshina, M. M. (2017) Involvement of the chloroplast plastoquinone pool in the Mehler reaction, Physiol. Plant., 161, 45-55, https://doi.org/10.1111/ppl.12560.

    Article  CAS  PubMed  Google Scholar 

  45. Tikhonov, A. N. (2014) The cytochrome b6f complex at the crossroad of photosynthetic electron transport pathways, Plant Physiol. Biochem., 81, 163-183, https://doi.org/10.1016/j.plaphy.2013.12.011.

    Article  CAS  PubMed  Google Scholar 

  46. Kramer, D. M., Crofts, A. R. (1994) Re-examination of the properties and function of the b cytochromes of the thylakoid cytochrome bf complex, Biochim. Biophys. Acta Bioenerg., 1184, 193-201, https://doi.org/10.1016/0005-2728(94)90223-2.

    Article  CAS  Google Scholar 

  47. Sang, M., Qin, X. C., Wang, W. D., Xie, J., Chen, X. B., Wang, K. B., Zhang, J. P., Li, L. B., Kuang, T. Y. (2011) High-light-induced superoxide anion radical formation in cytochrome b6f complex from spinach as detected by EPR spectroscopy, Photosynthetica, 49, 48-54, https://doi.org/10.1007/s11099-011-0008-0.

    Article  CAS  Google Scholar 

  48. Šnyrychová, I., Pospíšil, P., and Nauš, J. (2006) Reaction pathways involved in the production of hydroxyl radicals in thylakoid membrane: EPR spin-trapping study, Photochem. Photobiol. Sci., 5, 472-476, https://doi.org/10.1039/B514394B.

    Article  PubMed  Google Scholar 

  49. Kozuleva, M. A., Naidov, I. A., Mubarakshina, M. M., and Ivanov, B. N. (2007) Participation of ferredoxin in oxygen reduction by the photosynthetic electron transport chain, Biophysics, 52, 393-397, https://doi.org/10.1134/S0006350907040069.

    Article  Google Scholar 

  50. Badger, M. R. (1985) Photosynthetic oxygen exchange, Annu. Rev. Plant. Physiol., 36, 27-53, https://doi.org/10.1146/annurev.pp.36.060185.000331.

    Article  CAS  Google Scholar 

  51. Allen, J. F. (1975) Oxygen reduction and optimum production of ATP in photosynthesis, Nature, 256, 599-600, https://doi.org/10.1038/256599a0.

    Article  CAS  Google Scholar 

  52. Furbank, R. T., and Badger, M. R. (1983) Oxygen exchange associated with electron transport and photophosphorylation in spinach thylakoids, Biochim. Biophys. Acta Bioenerg., 723, 400-409, https://doi.org/10.1016/0005-2728(83)90047-6.

    Article  CAS  Google Scholar 

  53. Kozuleva, M. A., and Ivanov, B. N. (2010) Evaluation of the participation of ferredoxin in oxygen reduction in the photosynthetic electron transport chain of isolated pea thylakoids, Photosynth. Res., 105, 51-61, https://doi.org/10.1007/s11120-010-9565-5.

    Article  CAS  PubMed  Google Scholar 

  54. Asada, K. (1999) The water–water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons, Annu. Rev. Plant. Physiol. Plant. Mol. Biol., 50, 601-639, https://doi.org/10.1146/annurev.arplant.50.1.601.

    Article  CAS  PubMed  Google Scholar 

  55. Asada, K., and Nakano, Y. (1978) Affinity for oxygen in photoreduction of molecular oxygen and scavenging of hydrogen peroxide in spinach chloroplasts, Photochem. Photobiol., 28, 917-920, https://doi.org/10.1111/j.1751-1097.1978.tb07040.x.

    Article  CAS  Google Scholar 

  56. Petrova, A., Mamedov, M., Ivanov, B., Semenov, A., and Kozuleva, M. (2018) Effect of artificial redox mediators on the photoinduced oxygen reduction by photosystem I complexes, Photosynth. Res., 137, 421-429, https://doi.org/10.1007/s11120-018-0514-z.

    Article  CAS  PubMed  Google Scholar 

  57. Robinson, J. M. (1988) Does O2 photoreduction occur within chloroplasts in vivo? Physiol. Plant., 72, 666-680, https://doi.org/10.1111/j.1399-3054.1988.tb09181.x.

    Article  CAS  Google Scholar 

  58. Miyake, C., Schreiber, U., Hormann, H., Sano, S., and Asada, K. (1998) The FAD-enzyme monodehydroascorbate radical reductase mediates photoproduction of superoxide radicals in spinach thylakoid membranes, Plant Cell Physiol., 39, 821-829, https://doi.org/10.1093/oxfordjournals.pcp.a029440.

    Article  CAS  Google Scholar 

  59. Hanke, G. T., Endo, T., Satoh, F., and Hase, T. (2008) Altered photosynthetic electron channelling into cyclic electron flow and nitrite assimilation in a mutant of ferredoxin:NADP(H) reductase, Plant Cell Environ., 31, 1017-1028, https://doi.org/10.1111/j.1365-3040.2008.01814.x.

    Article  CAS  PubMed  Google Scholar 

  60. Kramer, M., Rodriguez-Heredia, M., Saccon, F., Mosebach, L., Twachtmann, M., Krieger-Liszkay, A., Duffy, C., Knell, R. J., Finazzi, G., and Hanke, G. T. (2021) Regulation of photosynthetic electron flow on dark to light transition by ferredoxin:NADP(H) oxidoreductase interactions, ELife, 10, e56088, https://doi.org/10.7554/eLife.56088.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Buchert, F., Mosebach, L., Gäbelein, P., and Hippler, M. (2020) PGR5 is required for efficient Q cycle in the cytochrome b6f complex during cyclic electron flow, Biochem. J., 477, 1631-1650, https://doi.org/10.1042/BCJ20190914.

    Article  CAS  PubMed  Google Scholar 

  62. Malone, L. A., Proctor, M. S., Hitchcock, A., Hunter, C. N., and Johnson, M. P. (2021) Cytochrome b6f – orchestrator of photosynthetic electron transfer, Biochim. Biophys. Acta Bioenerg., 1862, 148380, https://doi.org/10.1016/j.bbabio.2021.148380.

    Article  CAS  PubMed  Google Scholar 

  63. Kozuleva, M. (2022) Recent advances in the understanding of superoxide anion radical formation in the photosynthetic electron transport chain, Acta Physiol. Plant., 44, 92, https://doi.org/10.1007/s11738-022-03428-0.

    Article  CAS  Google Scholar 

  64. Hiyama, T., and Ke, B. (1971) A new photosynthetic pigment, “P430”: its possible role as the primary electron acceptor of photosystem I, Proc. Natl. Acad. Sci. USA, 68, 1010-1013, https://doi.org/10.1073/pnas.68.5.1010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Kozuleva, M. A., Vetoshkina, D. V., Petrova, A. A., Borisova-Mubarakshina, M. M., and Ivanov, B. N. (2015) The study of oxygen reduction in photosystem I of higher plants using electron donors for this photosystem in intact thylakoids, Biochemistry (Moscow) Suppl. Ser. A Membr. Cell Biol., 9, 246-251, https://doi.org/10.1134/S1990747814060026.

    Article  Google Scholar 

  66. Khorobrykh, S., and Tyystjärvi, E. (2018) Plastoquinol generates and scavenges reactive oxygen species in organic solvent: potential relevance for thylakoids, Biochim. Biophys. Acta Bioenerg., 1859, 1119-1131, https://doi.org/10.1016/j.bbabio.2018.07.003.

    Article  CAS  PubMed  Google Scholar 

  67. Takahashi, M., and Asada, K. (1982) Dependence of oxygen affinity for Mehler reaction on photochemical activity of chloroplast thylakoids, Plant Cell Physiol., 23, 1457-1461, https://doi.org/10.1093/oxfordjournals.pcp.a076495.

    Article  CAS  Google Scholar 

  68. Kruk, J., Jemioła-Rzemińska, M., Burda, K., Schmid, G. H., and Strzałka, K. (2003) Scavenging of superoxide generated in photosystem I by plastoquinol and other prenyllipids in thylakoid membranes, Biochemistry, 42, 8501-8505, https://doi.org/10.1021/bi034036q.

    Article  CAS  PubMed  Google Scholar 

  69. Kozuleva, M. A., Petrova, A. A., Mamedov, M. D., Semenov, A. Yu., and Ivanov, B. N. (2014) O2 reduction by photosystem I involves phylloquinone under steady-state illumination, FEBS Lett., 588, 4364-4368, https://doi.org/10.1016/j.febslet.2014.10.003.

    Article  CAS  PubMed  Google Scholar 

  70. Semenov, A. Y., Vassiliev, I. R., van der Est, A., Mamedov, M. D., Zybailov, B., Shen, G., Stehlik, D., Diner, B. A., Chitnis, P. R., and Golbeck, J. H. (2000) Recruitment of a foreign quinone into the A1 site of Photosystem I: altered kinetics of electron transfer in phylloquinone biosynthetic pathway mutants studied by time-resolved optical, EPR, and electrometric techniques, J. Biol. Chem., 275, 23429-23438, https://doi.org/10.1074/jbc.M000508200.

    Article  CAS  PubMed  Google Scholar 

  71. Santabarbara, S., Bullock, B., Rappaport, F., and Redding, K. E. (2015) Controlling electron transfer between the two cofactor chains of photosystem I by the redox state of one of their components, Biophys. J., 108, 1537-1547, https://doi.org/10.1016/j.bpj.2015.01.009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Kale, R., Sallans, L., Frankel, L. K., and Bricker, T. M. (2020) Natively oxidized amino acid residues in the spinach PS I-LHC I supercomplex, Photosynth. Res., 143, 263-273, https://doi.org/10.1007/s11120-019-00698-7.

    Article  CAS  PubMed  Google Scholar 

  73. Milanovsky, G. E., Petrova, A. A., Cherepanov, D. A., and Semenov, A. Yu. (2017) Kinetic modeling of electron transfer reactions in photosystem I complexes of various structures with substituted quinone acceptors, Photosynth. Res., 133, 185-199, https://doi.org/10.1007/s11120-017-0366-y.

    Article  CAS  PubMed  Google Scholar 

  74. Ivanov, B. (2000) The competition between methyl viologen and monodehydroascorbate radical as electron acceptors in spinach thylakoids and intact chloroplasts, Free Radic. Res., 33, 217-227, https://doi.org/10.1080/10715760000301391.

    Article  CAS  PubMed  Google Scholar 

  75. Bukhov, N. G., Govindachary, S., Egorova, E. A., Joly, D., and Carpentier, R. (2003) N,N,N′,N′-tetramethyl-p-phenylenediamine initiates the appearance of a well-resolved I peak in the kinetics of chlorophyll fluorescence rise in isolated thylakoids, Biochim. Biophys. Acta Bioenerg., 1607, 91-96, https://doi.org/10.1016/j.bbabio.2003.09.002.

    Article  CAS  Google Scholar 

  76. Trubitsin, B. V., Mamedov, M. D., Semenov, A. Yu., and Tikhonov, A. N. (2014) Interaction of ascorbate with photosystem I, Photosynth. Res., 122, 215-231, https://doi.org/10.1007/s11120-014-0023-7.

    Article  CAS  PubMed  Google Scholar 

  77. Michelet, L., and Krieger-Liszkay, A. (2012) Reactive oxygen intermediates produced by photosynthetic electron transport are enhanced in short-day grown plants, Biochim. Biophys. Acta Bioenerg., 1817, 1306-1313, https://doi.org/10.1016/j.bbabio.2011.11.014.

    Article  CAS  Google Scholar 

  78. Krieger-Liszkay, A., Shimakawa, G., and Sétif, P. (2020) Role of the two PsaE isoforms on O2 reduction at photosystem I in Arabidopsis thaliana, Biochim. Biophys. Acta Bioenerg., 1861, 148089, https://doi.org/10.1016/j.bbabio.2019.148089.

    Article  CAS  PubMed  Google Scholar 

  79. Marco, P., Elman, T., and Yacoby, I. (2019) Binding of ferredoxin NADP+ oxidoreductase (FNR) to plant photosystem I, Biochim. Biophys. Acta Bioenerg., 1860, 689-698, https://doi.org/10.1016/j.bbabio.2019.07.007.

    Article  CAS  PubMed  Google Scholar 

  80. Andersen, B., Scheller, H. V., and Møller, B. L. (1992) The PSI-E subunit of photosystem I binds ferredoxin:NADP+ oxidoreductase, FEBS Lett., 311, 169-173, https://doi.org/10.1016/0014-5793(92)81391-X.

    Article  CAS  PubMed  Google Scholar 

  81. Benz, J. P., Stengel, A., Lintala, M., Lee, Y.-H., Weber, A., Philippar, K., Gügel, I. L., Kaieda, S., Ikegami, T., Mulo, P., Soll, J., and Bölter, B. (2009) Arabidopsis Tic62 and ferredoxin-NADP(H) oxidoreductase form light-regulated complexes that are integrated into the chloroplast redox poise, Plant Cell, 21, 3965-3983, https://doi.org/10.1105/tpc.109.069815.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Jurić, S., Hazler-Pilepić, K., Tomašić, A., Lepeduš, H., Jeličić, B., Puthiyaveetil, S., Bionda, T., Vojta, L., Allen, J. F., Schleiff, E., and Fulgosi, H. (2009) Tethering of ferredoxin:NADP+ oxidoreductase to thylakoid membranes is mediated by novel chloroplast protein TROL, Plant J., 60, 783-794, https://doi.org/10.1111/j.1365-313X.2009.03999.x.

    Article  CAS  PubMed  Google Scholar 

  83. Jagannathan, B., Shen, G., and Golbeck, J. H. (2012) The evolution of type I reaction centers: the response to oxygenic photosynthesis, in Functional Genomics and Evolution of Photosynthetic Systems, Springer, Dordrecht, pp. 285-316, https://doi.org/10.1007/978-94-007-1533-2_12.

  84. Rutherford, A. W., Osyczka, A., and Rappaport, F. (2012) Back-reactions, short-circuits, leaks and other energy wasteful reactions in biological electron transfer: Redox tuning to survive life in O2, FEBS Lett., 586, 603-616, https://doi.org/10.1016/j.febslet.2011.12.039.

    Article  CAS  PubMed  Google Scholar 

  85. Pierella Karlusich, J. J., and Carrillo, N. (2017) Evolution of the acceptor side of photosystem I: ferredoxin, flavodoxin, and ferredoxin-NADP+ oxidoreductase, Photosyn. Res., 134, 235-250, https://doi.org/10.1007/s11120-017-0338-2.

    Article  CAS  Google Scholar 

  86. Orf, G. S., Gisriel, C., and Redding, K. E. (2018) Evolution of photosynthetic reaction centers: insights from the structure of the heliobacterial reaction center, Photosynth. Res., 138, 11-37, https://doi.org/10.1007/s11120-018-0503-2.

    Article  CAS  PubMed  Google Scholar 

  87. Hanke, G., and Mulo, P. (2013) Plant type ferredoxins and ferredoxin-dependent metabolism, Plant Cell Environ., 36, 1071-1084, https://doi.org/10.1111/pce.12046.

    Article  CAS  PubMed  Google Scholar 

  88. Fischer, N., Sétif, P., and Rochaix, J.-D. (1997) Targeted mutations in the psaC gene of Chlamydomonas reinhardtii: preferential reduction of FB at low temperature is not accompanied by altered electron flow from photosystem I to ferredoxin, Biochemistry, 36, 93-102, https://doi.org/10.1021/bi962244v.

    Article  CAS  PubMed  Google Scholar 

  89. Shinkarev, V. P., Vassiliev, I. R., and Golbeck, J. H. (2000) A kinetic assessment of the sequence of electron transfer from F(X) to F(A) and further to F(B) in photosystem I: the value of the equilibrium constant between F(X) and F(A), Biophys. J., 78, 363-372, https://doi.org/10.1016/S0006-3495(00)76599-4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Ptushenko, V. V., Cherepanov, D. A., Krishtalik, L. I., and Semenov, A. Y. (2008) Semi-continuum electrostatic calculations of redox potentials in photosystem I, Photosynth. Res., 97, 55-74, https://doi.org/10.1007/s11120-008-9309-y.

    Article  CAS  PubMed  Google Scholar 

  91. Schoepp-Cothenet, B., van Lis, R., Atteia, A., Baymann, F., Capowiez, L., Ducluzeau, A.-L., Duval, S., Brink, F., Russell, M. J., and Nitschke, W. (2013) On the universal core of bioenergetics, Biochim. Biophys. Acta Bioenerg., 1827, 79-93, https://doi.org/10.1016/j.bbabio.2012.09.005.

    Article  CAS  Google Scholar 

  92. Massey, V. (1994) Activation of molecular oxygen by flavins and flavoproteins, J. Biol. Chem., 269, 22459-22462, https://doi.org/10.1016/S0021-9258(17)31664-2.

    Article  CAS  PubMed  Google Scholar 

  93. Ceccarelli, E. A., Arakaki, A. K., Cortez, N., and Carrillo, N. (2004) Functional plasticity and catalytic efficiency in plant and bacterial ferredoxin-NADP(H) reductases, Biochim. Biophys. Acta Proteins Proteomics, 1698, 155-165, https://doi.org/10.1016/j.bbapap.2003.12.005.

    Article  CAS  Google Scholar 

  94. Carrillo, N., and Ceccarelli, E. A. (2003) Open questions in ferredoxin-NADP+ reductase catalytic mechanism, Eur. J. Biochem., 270, 1900-1915, https://doi.org/10.1046/j.1432-1033.2003.03566.x.

    Article  CAS  PubMed  Google Scholar 

  95. Batie, C. J., and Kamin, H. (1984) Ferredoxin:NADP+ oxidoreductase. Equilibria in binary and ternary complexes with NADP+ and ferredoxin, J. Biol. Chem., 259, 8832-8839, https://doi.org/10.1016/S0021-9258(17)47229-2.

    Article  CAS  PubMed  Google Scholar 

  96. Mulo, P., and Medina, M. (2017) Interaction and electron transfer between ferredoxin-NADP+ oxidoreductase and its partners: structural, functional, and physiological implications, Photosynth. Res., 134, 265-280, https://doi.org/10.1007/s11120-017-0372-0.

    Article  CAS  PubMed  Google Scholar 

  97. Drachev, L. A., Kaurov, B. S., Mamedov, M. D., Mulkidjanian, A. Y., Semenov, A. Yu, Shinkarev, V. P., Skulachev, V. P., and Verkgovsky, M. I. (1989) Flash-induced electrogenic events in the photosynthetic reaction center and bc1 complexes of Rhodobacter sphaeroides chromatophores, Biochim. Biophys. Acta, 973, 189-197, https://doi.org/10.1016/S0005-2728(89)80421-9.

    Article  CAS  Google Scholar 

  98. De Vries, S., Berden, J. A., and Slater, E. C. (1980) Properties of a semiquinone anion located in the QH2:cytochrome c oxidoreductase segment of the mitochondrial respiratory chain, FEBS Lett., 122, 143-148, https://doi.org/10.1016/0014-5793(80)80422-4.

    Article  PubMed  Google Scholar 

  99. Stroebel, D., Choquet, Y., Popot, J.-L., and Picot, D. (2003) An atypical haem in the cytochrome b(6)f complex, Nature, 426, 413-418, https://doi.org/10.1038/nature02155.

    Article  CAS  PubMed  Google Scholar 

  100. Vilyanen, D., Naydov, I., Ivanov, B., Borisova-Mubarakshina, M., and Kozuleva, M. (2022) Inhibition of plastoquinol oxidation at the cytochrome b6f complex by dinitrophenyl ether of iodonitrothymol (DNP-INT) depends on irradiance and H+ uptake by thylakoid membranes, Biochim. Biophys. Acta Bioenerg., 1863, 148506, https://doi.org/10.1016/j.bbabio.2021.148506.

    Article  CAS  PubMed  Google Scholar 

  101. Schoepp-Cothenet, B., Lieutaud, C., Baymann, F., Verméglio, A., Friedrich, T., Kramer, D. M., and Nitschke, W. (2009) Menaquinone as pool quinone in a purple bacterium, Proc. Natl. Acad. Sci. USA, 106, 8549-8554, https://doi.org/10.1073/pnas.0813173106.

    Article  PubMed  PubMed Central  Google Scholar 

  102. Bergdoll, L., ten Brink, F., Nitschke, W., Picot, D., and Baymann, F. (2016) From low- to high-potential bioenergetic chains: thermodynamic constraints of Q-cycle function, Biochim. Biophys. Acta Bioenerg., 1857, 1569-1579, https://doi.org/10.1016/j.bbabio.2016.06.006.

    Article  CAS  Google Scholar 

  103. Alric, J., Pierre, Y., Picot, D., Lavergne, J., and Rappaport, F. (2005) Spectral and redox characterization of the heme ci of the cytochrome bf complex, Proc. Natl. Acad. Sci. USA, 102, 15860-15865, https://doi.org/10.1073/pnas.0508102102.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Gisriel, C., Sarrou, I., Ferlez, B., Golbeck, J. H., Redding, K. E., and Fromme, R. (2017) Structure of a symmetric photosynthetic reaction center-photosystem, Science, 357, 1021-1025, https://doi.org/10.1126/science.aan5611.

    Article  CAS  PubMed  Google Scholar 

  105. He, Z., Ferlez, B., Kurashov, V., Tank, M., Golbeck, J. H., and Bryant, D. A. (2019) Reaction centers of the thermophilic microaerophile, Chloracidobacterium thermophilum (Acidobacteria) I: biochemical and biophysical characterization, Photosynth. Res., 142, 87-103, https://doi.org/10.1007/s11120-019-00650-9.

    Article  CAS  PubMed  Google Scholar 

  106. Su, X., Ma, J., Pan, X., Zhao, X., Chang, W., Liu, Z., Zhang, X., and Li, M. (2019) Antenna arrangement and energy transfer pathways of a green algal photosystem-I-LHCI supercomplex, Nat. Plants, 5, 273-281, https://doi.org/10.1038/s41477-019-0380-5.

    Article  CAS  PubMed  Google Scholar 

  107. Kashey, T. S., Luu, D. D., Cowgill, J. C., Baker, P. L., and Redding, K. E. (2018) Light-driven quinone reduction in heliobacterial membranes, Photosynth. Res., 138, 1-9, https://doi.org/10.1007/s11120-018-0496-x.

    Article  CAS  PubMed  Google Scholar 

  108. McConnell, M. D., Cowgill, J. B., Baker, P. L., Rappaport, F., and Redding, K. E. (2011) Double reduction of plastoquinone to plastoquinol in photosystem 1, Biochemistry, 50, 11034-11046, https://doi.org/10.1021/bi201131r.

    Article  CAS  PubMed  Google Scholar 

  109. Guergova-Kuras, M., Boudreaux, B., Joliot, A., Joliot, P., and Redding, K. (2001) Evidence for two active branches for electron transfer in photosystem I, Proc. Natl. Acad. Sci. USA, 98, 4437-4442, https://doi.org/10.1073/pnas.081078898.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Ksas, B., Alric, J., Caffarri, S., and Havaux, M. (2022) Plastoquinone homeostasis in plant acclimation to light intensity, Photosynth. Res., 152, 43-54, https://doi.org/10.1007/s11120-021-00889-1.

    Article  CAS  PubMed  Google Scholar 

  111. Suslichenko, I. S., and Tikhonov, A. N. (2019) Photo-reducible plastoquinone pools in chloroplasts of Tradescentia plants acclimated to high and low light, FEBS Lett., 593, 788-798, https://doi.org/10.1002/1873-3468.13366.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Dr. M. M. Borisova for valuable discussions during preparation of the review.

Funding

This work was financially supported by the Russian Science Foundation, grant no. 22-24-01074.

Author information

Authors and Affiliations

Authors

Contributions

M.A.K. – writing the text; B.N.I. – editing the article.

Corresponding author

Correspondence to Marina A. Kozuleva.

Ethics declarations

The authors declare no conflict of interest in financial or any other sphere. This article does not contain descriptions of any research involving human or animal subjects performed by any of the authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kozuleva, M.A., Ivanov, B.N. Superoxide Anion Radical Generation in Photosynthetic Electron Transport Chain. Biochemistry Moscow 88, 1045–1060 (2023). https://doi.org/10.1134/S0006297923080011

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006297923080011

Keywords

Navigation