БИОХИМИЯ, 2023, том 88, вып. 8, с. 1283–1301

УДК 577.1

Генерация супероксидного анион-радикала в фотосинтетической электрон-транспортной цепи

Обзор

© 2023 М.А. Козулева *kozuleva@gmail.com, Б.Н. Иванов

Федеральный исследовательский центр «Пущинский научный центр биологических исследований Российской академии наук», Институт фундаментальных проблем биологии РАН, 142290 Пущино, Московская обл., Россия

Поступила в редакцию 09.05.2023
После доработки 16.06.2023
Принята к публикации 18.06.2023

DOI: 10.31857/S0320972523080018

КЛЮЧЕВЫЕ СЛОВА: фотосинтез, фотосинтетическая электрон-транспортная цепь, восстановление кислорода, супероксидный радикал.

Аннотация

В обзоре проанализированы имеющиеся в литературе данные о скоростях, характеристиках и механизмах восстановления молекул O2 до супероксидного анион-радикала на участках фотосинтетической электрон-транспортной цепи, на которых это восстановление было установлено. С использованием термодинамических расчетов и результатов недавних работ критически рассмотрены имеющиеся предположения о роли компонентов этих участков в данном процессе. Детально описан процесс восстановления молекул O2 на акцепторной стороне фотосистемы 1, считающейся основным местом этого процесса в фотосинтетической цепи. Рассмотрены аспекты эволюции фотосинтетического аппарата в контексте контроля утечки электронов к молекуле O2. Обсуждены причины, ограничивающие применение результатов, полученных с использованием фрагментов тилакоидных мембран, содержащих отдельные участки фотосинтетической цепи, для оценки скорости восстановления молекул O2 на этих участках в интактной тилакоидной мембране.

Текст статьи

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Сноски

* Адресат для корреспонденции.

Финансирование

Работа выполнена при поддержке Российского научного фонда (грант № 22‑24‑01074).

Благодарности

Авторы благодарят д.б.н. М.М. Борисову за полезные дискуссии при подготовке обзора.

Вклад авторов

М.А. Козулева – написание текста; Б.Н. Иванов – редактирование текста статьи.

Конфликт интересов

Авторы заявляют об отсутствии конфликта интересов.

Соблюдение этических норм

Настоящая статья не содержит описания каких-либо исследований с участием людей или животных в качестве объектов.

Список литературы

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, doi: 10.1016/0003-9861(51)90082-3.

2. Иванов Б., Хоробрых С., Козулева М., Борисова-Мубаракшина М. (2014) Роль кислорода и его активных форм в фотосинтезе, Современные Проблемы Фотосинтеза/Под Ред. Аллахвердиева С. И., Рубина А. Б., Шувалова В. А., Ижевский Институт Компьютерных Исследований, Ижевск-Москва, 1, 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, doi: 10.1111/j.1399-3054.2010.01391.x.

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

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, doi: 10.1093/pcp/pcw035.

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, doi: 10.3389/fpls.2020.00211.

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, doi: 10.1021/acs.chemrev.0c00712.

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, doi: 10.1016/0006-291X(73)91016-4.

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, doi: 10.1016/S0021-9258(19)42815-9.

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

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

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, doi: 10.1016/j.febslet.2011.03.004.

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, doi: 10.1016/j.freeradbiomed.2015.08.016.

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, doi: 10.1104/pp.16.01084.

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, doi: 10.1073/pnas.2116063119.

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

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, doi: 10.1016/0014-5793(83)80957-0.

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, doi: 10.1016/j.bbabio.2007.06.001.

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, doi: 10.1021/bi4013534.

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, doi: 10.1093/plphys/kiab221.

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, doi: 10.1016/0005-2728(83)90045-2.

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.

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

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, doi: 10.1016/j.bbabio.2019.148141.

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, doi: 10.1371/journal.pone.0058042.

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, doi: 10.1073/pnas.1618922114.

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, doi: 10.1073/pnas.2019246118.

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, doi: 10.1007/s11120-018-0485-0.

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, doi: 10.1007/BF00019410.

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

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, doi: 10.1073/pnas.1608862113.

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

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, doi: 10.1073/pnas.1910675116.

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, doi: 10.1023/A:1006374319191.

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, doi: 10.1042/BJ20060068.

36. Müh, F., and Zouni, A. (2016) Cytochrome b 559 in Photosystem II, in Adv. Photosynth. Respir. Springer, Dordrecht, 41, 143-175, doi: 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, doi: 10.1016/0014-5793(94)80196-7.

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, doi: 10.1371/journal.pone.0115466.

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, doi: 10.3390/plants8090329.

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, doi: 10.1016/j.bbabio.2006.09.004.

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

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, doi: 10.1016/j.bbabio.2004.04.009.

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, doi: 10.1074/jbc.M605119200.

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, doi: 10.1111/ppl.12560.

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

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, doi: 10.1016/0005-2728(94)90223-2.

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, doi: 10.1007/s11099-011-0008-0.

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, doi: 10.1039/B514394B.

49. Козулева М. А., Найдов И. А., Мубаракшина М. М., Иванов Б. Н. (2007) Участие ферредоксина в восстановлении кислорода в фотосинтетической электрон-транспортной цепи, Биофизика, 52, 650-655.

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

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

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, doi: 10.1016/0005-2728(83)90047-6.

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, doi: 10.1007/s11120-010-9565-5.

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, doi: 10.1146/annurev.arplant.50.1.601.

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, doi: 10.1111/j.1751-1097.1978.tb07040.x.

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, doi: 10.1007/s11120-018-0514-z.

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

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, doi: 10.1093/oxfordjournals.pcp.a029440.

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, doi: 10.1111/j.1365-3040.2008.01814.x.

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, doi: 10.7554/eLife.56088.

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, doi: 10.1042/BCJ20190914.

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, doi: 10.1016/j.bbabio.2021.148380.

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, doi: 10.1007/s11738-022-03428-0.

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, doi: 10.1073/pnas.68.5.1010.

65. Козулева М. А., Ветошкина Д. В., Петрова А. А., Борисова М. М., Иванов Б. Н. (2014) Исследование восстановления кислорода в фотосистеме 1 высших растений с применением доноров электронов для этой фотосистемы в целых тилакоидах, Биол. Мембр., 31, 427-434, doi: 10.7868/S0233475514060024.

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, doi: 10.1016/j.bbabio.2018.07.003.

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, doi: 10.1093/oxfordjournals.pcp.a076495.

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, doi: 10.1021/bi034036q.

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, doi: 10.1016/j.febslet.2014.10.003.

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, doi: 10.1074/jbc.M000508200.

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, doi: 10.1016/j.bpj.2015.01.009.

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, doi: 10.1007/s11120-019-00698-7.

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, doi: 10.1007/s11120-017-0366-y.

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, doi: 10.1080/10715760000301391.

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, doi: 10.1016/j.bbabio.2003.09.002.

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, doi: 10.1007/s11120-014-0023-7.

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, doi: 10.1016/j.bbabio.2011.11.014.

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, doi: 10.1016/j.bbabio.2019.148089.

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, doi: 10.1016/j.bbabio.2019.07.007.

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, doi: 10.1016/0014-5793(92)81391-X.

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, doi: 10.1105/tpc.109.069815.

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, doi: 10.1111/j.1365-313X.2009.03999.x.

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, doi: 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, doi: 10.1016/j.febslet.2011.12.039.

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, doi: 10.1007/s11120-017-0338-2.

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, doi: 10.1007/s11120-018-0503-2.

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

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, doi: 10.1021/bi962244v.

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, doi: 10.1016/S0006-3495(00)76599-4.

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, doi: 10.1007/s11120-008-9309-y.

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, doi: 10.1016/j.bbabio.2012.09.005.

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

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, doi: 10.1016/j.bbapap.2003.12.005.

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

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, doi: 10.1016/S0021-9258(17)47229-2.

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, doi: 10.1007/s11120-017-0372-0.

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, doi: 10.1016/S0005-2728(89)80421-9.

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, doi: 10.1016/0014-5793(80)80422-4.

99. Stroebel, D., Choquet, Y., Popot, J.-L., and Picot, D. (2003) An atypical haem in the cytochrome b6f complex, Nature, 426, 413-418, doi: 10.1038/nature02155.

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, doi: 10.1016/j.bbabio.2021.148506.

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, doi: 10.1073/pnas.0813173106.

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, doi: 10.1016/j.bbabio.2016.06.006.

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, doi: 10.1073/pnas.0508102102.

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, doi: 10.1126/science.aan5611.

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, doi: 10.1007/s11120-019-00650-9.

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, doi: 10.1038/s41477-019-0380-5.

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, doi: 10.1007/s11120-018-0496-x.

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, doi: 10.1021/bi201131r.

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, doi: 10.1073/pnas.081078898.

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

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, doi: 10.1002/1873-3468.13366.