Фотосинтетический контроль и его участие в защите фотосистемы I от фотоингибирования

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В обзоре поднимается вопрос о фотосинтетическом контроле как о защитном механизме, предотвращающем фотоингибирование фотосистемы I в условиях дисбаланса между ассимиляцией CO2 в ходе цикла Кальвина–Бенсона–Бассама и световыми реакциями в фотосинтетическом аппарате тилакоидов. Рассмотрены пути фотоингибирования фотосистемы I и описаны защитные механизмы, предотвращающие её повреждение на свету. Проанализирована pH-чувствительность окисления пластохинола в хинол-окисляющем сайте цитохромного b6f-комплекса и описано функционирование двух каналов, выводящих протоны в люмен тилакоида из цитохромного b6f-комплекса. Рассмотрено влияние активации фотосинтетического контроля на функционирование самого цитохромного b6f-комплекса и предложена гипотеза о влиянии фотосинтетического контроля на образование активных форм кислорода в фотосистеме I.

Об авторах

Д. В. Вильянен

Институт фундаментальных проблем биологии РАН Федерального исследовательского центра "Пущинский научный центр биологических исследований РАН"

Автор, ответственный за переписку.
Email: marina.kozuleva@pbcras.ru
Пущино

М. А. Козулева

Институт фундаментальных проблем биологии РАН Федерального исследовательского центра "Пущинский научный центр биологических исследований РАН"

Email: marina.kozuleva@pbcras.ru
Пущино

Список литературы

  1. Terashima, I., Funayama, S., and Sonoike, K. (1994) The site of photoinhibition in leaves of Cucumis sativus L. at low temperatures is photosystem I, not photosystem II, Planta, 193, 300-306, https://doi.org/10.1007/BF00192544.
  2. Kono, M., Oguchi, R., and Terashima, I. (2022) Photoinhibition of PSI and PSII in nature and in the laboratory: ecological approaches, in Progress in Botany (Lüttge, U., Cánovas, F. M., Risueño, M.-C., Leuschner, C., and Pretzsch, H., eds), Vol. 84, Springer Nature Switzerland, pp. 241-292, https://doi.org/10.1007/124_2022_67.
  3. Tikkanen, M., Grieco, M., Kangasjärvi, S., and Aro, E.-M. (2010) Thylakoid protein phosphorylation in higher plant chloroplasts optimizes electron transfer under fluctuating light, Plant Physiol., 152, 723-735, https://doi.org/10.1104/pp.109.150250.
  4. Sejima, T., Takagi, D., Fukayama, H., Makino, A., and Miyake, C. (2014) Repetitive short-pulse light mainly inactivates photosystem I in sunflower leaves, Plant Cell Physiol., 55, 1184-1193, https://doi.org/10.1093/pcp/pcu061.
  5. Lempiäinen, T., Rintamäki, E., Aro, E.-M., and Tikkanen, M. (2022) Plants acclimate to Photosystem I photoinhibition by readjusting the photosynthetic machinery, Plant Cell Environ., 45, 2954-2971, https://doi.org/10.1111/pce.14400.
  6. Lima-Melo, Y., Kılıç, M., Aro, E.-M., and Gollan, P. J. (2021) Photosystem I inhibition, protection and signalling: knowns and unknowns, Front. Plant Sci., 12, 791124, https://doi.org/10.3389/fpls.2021.791124.
  7. Shimakawa, G., and Miyake, C. (2018) Oxidation of P700 ensures robust photosynthesis, Front. Plant Sci., 9, 1617, https://doi.org/10.3389/fpls.2018.01617.
  8. Suorsa, M., Järvi, S., Grieco, M., Nurmi, M., Pietrzykowska, M., Rantala, M., Kangasjärvi, S., Paakkarinen, V., Tikkanen, M., Jansson, S., and Aro, E.-M. (2012) PROTON GRADIENT REGULATION5 is essential for proper acclimation of Arabidopsis photosystem I to naturally and artificially fluctuating light conditions, Plant Cell, 24, 2934-2948, https://doi.org/10.1105/tpc.112.097162.
  9. Munekage, Y., Hojo, M., Meurer, J., Endo, T., Tasaka, M., and Shikanai, T. (2002) PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis, Cell, 110, 361-371, https://doi.org/10.1016/S0092-8674(02)00867-X.
  10. Yamamoto, H., and Shikanai, T. (2019) PGR5-dependent cyclic electron flow protects photosystem I under fluctuating light at donor and acceptor sides, Plant Physiol., 179, 588-600, https://doi.org/10.1104/pp.18.01343.
  11. Shikanai, T. (2024) Molecular genetic dissection of the regulatory network of proton motive force in chloroplasts, Plant Cell Physiol., 65, 537-550, https://doi.org/10.1093/pcp/pcad157.
  12. Degen, G. E., and Johnson, M. P. (2024) Photosynthetic control at the cytochrome b6f complex, Plant Cell, 36, 4065-4079, https://doi.org/10.1093/plcell/koae133.
  13. Hanke, G., Mulo, P. (2013) Plant type ferredoxins and ferredoxin-dependent metabolism, Plant Cell Environ., 36, 1071-1084, https://doi.org/10.1111/pce.12046.
  14. Davis, G. A., Rutherford, A. W., and Kramer, D. M. (2017) Hacking the thylakoid proton motive force for improved photosynthesis: modulating ion flux rates that control proton motive force partitioning into Δψ and ΔpH, Philos. Trans. R. Soc. B Biol. Sci., 372, 20160381, https://doi.org/10.1098/rstb.2016.0381.
  15. Allen, J. F. (2002) Photosynthesis of ATP – electrons, proton pumps, rotors, and poise, Cell, 110, 273-276, https://doi.org/10.1016/S0092-8674(02)00870-X.
  16. Munekage, Y., Hashimoto, M., Miyake, C., Tomizawa, K.-I., Endo, T., Tasaka, M., and Shikanai, T. (2004) Cyclic electron flow around photosystem I is essential for photosynthesis, Nature, 429, 579-582, https://doi.org/10.1038/nature02598.
  17. Takabayashi, A., Kishine, M., Asada, K., Endo, T., and Sato, F. (2005) Differential use of two cyclic electron flows around photosystem I for driving CO2-concentration mechanism in C4 photosynthesis, Proc. Natl. Acad. Sci. USA, 102, 16898-16903, https://doi.org/10.1073/pnas.0507095102.
  18. 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.
  19. Sarewicz, M., Pintscher, S., Pietras, R., Borek, A., Bujnowicz, Ł., Hanke, G., Cramer, W. A., Finazzi, J., 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.
  20. 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.
  21. 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.
  22. Ilík, P., Pavlovič, A., Kouřil, R., Alboresi, A., Morosinotto, T., Allahverdiyeva, Y., Aro, E.-M., Yamamoto, H., and Shikanai, T. (2017) Alternative electron transport mediated by flavodiiron proteins is operational in organisms from cyanobacteria up to gymnosperms, New Phytol., 214, 967-972, https://doi.org/10.1111/nph.14536.
  23. Wietrzynski, W., Lamm, L., Wood, W. H., Loukeri, M.-J., Malone, L., Peng, T., Johnson, M. P., and Engel, B. D. (2025) Molecular architecture of thylakoid membranes within intact spinach chloroplasts, eLife, 14, RP105496, https://doi.org/10.7554/eLife.105496.1.
  24. Höhner, R., Pribil, M., Herbstová, M., Lopez, L. S., Kunz, H.-H., Li, M., Wood, M., Svoboda, V., Puthiyaveetil, S., Leister, D., and Kirchhoff, H. (2020) Plastocyanin is the long-range electron carrier between photosystem II and photosystem I in plants, Proc. Natl. Acad. Sci. USA, 117, 15354-15362, https://doi.org/10.1073/pnas.2005832117.
  25. Kozuleva, M., Petrova, A., Milrad, Y., Semenov, A., Ivanov, B., Redding, K. E., and Yacoby, I. (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.
  26. 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.
  27. 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.
  28. Takagi, D., Takumi, S., Hashiguchi, M., Sejima, T., and Miyake, C. (2016) Superoxide and singlet oxygen produced within the thylakoid membranes both cause photosystem I photoinhibition, Plant Physiol., 171, 1626-1634, https://doi.org/10.1104/pp.16.00246.
  29. 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.
  30. Mathis, P., and Setif, P. (1981) Near infra-red absorption spectra of the chlorophyll a cations and triplet state in vitro and in vivo, Isr. J. Chem., 21, 316-320, https://doi.org/10.1002/ijch.198100057.
  31. Caspy, I., Borovikova-Sheinker, A., Klaiman, D., Shkolnisky, Y., and Nelson, N. (2020) The structure of a triple complex of plant photosystem I with ferredoxin and plastocyanin, Nat. Plants, 6, 1300-1305, https://doi.org/10.1038/s41477-020-00779-9.
  32. Sonoike, K., Terashima, I., Iwaki, M., and Itoh, S. (1995) Destruction of photosystem I iron-sulfur centers in leaves of Cucumis sativus L. by weak illumination at chilling temperatures, FEBS Lett., 362, 235-238, https://doi.org/10.1016/0014-5793(95)00254-7.
  33. Shimakawa, G., Müller, P., Miyake, C., Krieger-Liszkay, A., and Sétif, P. (2024) Photo-oxidative damage of photosystem I by repetitive flashes and chilling stress in cucumber leaves, Biochim. Biophys. Acta Bioenerg., 1865, 149490, https://doi.org/10.1016/j.bbabio.2024.149490.
  34. Sonoike, K. (1996) Degradation of psaB gene product, the reaction center subunit of photosystem I, is caused during photoinhibition of photosystem I: possible involvement of active oxygen species, Plant Sci., 115, 157-164, https://doi.org/10.1016/0168-9452(96)04341-5.
  35. Sonoike, K., Kamo, M., Hihara, Y., Hiyama, T., and Enami, I. (1997) The mechanism of the degradation of psaB gene product, one of the photosynthetic reaction center subunits of Photosystem I, upon photoinhibition, Photosynth. Res., 53, 55-63, https://doi.org/10.1023/A:1005852330671.
  36. Sonoike, K. (2011) Photoinhibition of photosystem I, Physiol. Plant., 142, 56-64, https://doi.org/10.1111/j.1399-3054.2010.01437.x.
  37. Tiwari, A., Mamedov, F., Grieco, M., Suorsa, M., Jajoo, A., Styring, S., Tikkanen, M., and Aro, E.-M. (2016) Photodamage of iron-sulphur clusters in photosystem I induces non-photochemical energy dissipation, Nat. Plants, 2, 16035, https://doi.org/10.1038/nplants.2016.35.
  38. Tiwari, A., Mamedov, F., Fitzpatrick, D., Gunell, S., Tikkanen, M., and Aro, E.-M. (2024) Differential FeS cluster photodamage plays a critical role in regulating excess electron flow through photosystem I, Nat. Plants, 10, 1592-1603, https://doi.org/10.1038/s41477-024-01780-2.
  39. Furutani, R., Wada, S., Ifuku, K., Maekawa, S., and Miyake, C. (2023) Higher reduced state of Fe/S-signals, with the suppressed oxidation of P700, causes PSI inactivation in Arabidopsis thaliana, Antioxidants, 12, 21, https://doi.org/10.3390/antiox12010021.
  40. Subramanyam, R., Joly, D., Gauthier, A., Beauregard, M., and Carpentier, R. (2005) Protective effect of active oxygen scavengers on protein degradation and photochemical function in photosystem I submembrane fractions during light stress, FEBS J., 272, https://doi.org/10.1111/j.1742-4658.2004.04512.x.
  41. Petrova, A. A., Boskhomdzhieva, B. K., Milanovsky, G. E., Koksharova, O. A., Mamedov, M. D., Cherepanov, D. A., and Semenov, A. Yu. (2017) Interaction of various types of photosystem I complexes with exogenous electron acceptors, Photosynth. Res., 133, 175-184, https://doi.org/10.1007/s11120-017-0371-1.
  42. Shi, Q., Sun, H., Timm, S., Zhang, S., and Huang, W. (2022) Photorespiration alleviates photoinhibition of photosystem I under fluctuating light in tomato, Plants, 11, 195, https://doi.org/10.3390/plants11020195.
  43. Yamamoto, H., Takahashi, S., Badger, M. R., and Shikanai, T. (2016) Artificial remodelling of alternative electron flow by flavodiiron proteins in Arabidopsis, Nat. Plants, 2, 16012, https://doi.org/10.1038/nplants.2016.12.
  44. Tan, S.-L., Huang, X., Li, W.-Q., Zhang, S.-B., and Huang, W. (2021) Elevated CO2 concentration alters photosynthetic performances under fluctuating light in Arabidopsis thaliana, Cells, 10, 2329, https://doi.org/10.3390/cells10092329.
  45. Tikkanen, M., Mekala, N. R., and Aro, E.-M. (2014) Photosystem II photoinhibition-repair cycle protects Photosystem I from irreversible damage, Biochim. Biophys. Acta Bioenerg., 1837, 210-215, https://doi.org/10.1016/j.bbabio.2013.10.001.
  46. Messant, M., Hani, U., Lai, T.-L., Wilson, A., Shimakawa, G., and Krieger-Liszkay, A. (2024) Plastid terminal oxidase (PTOX) protects photosystem I and not photosystem II against photoinhibition in Arabidopsis thaliana and Marchantia polymorpha, Plant J., 117, 669-678, https://doi.org/10.1111/tpj.16520.
  47. Kozuleva, M. A., and Ivanov, B. N. (2023) Superoxide anion radical generation in photosynthetic electron transport chain, Biochemistry (Moscow), 88, 1045-1060, https://doi.org/10.1134/S0006297923080011.
  48. Naydov, I., Kozuleva, M., Ivanov, B., Borisova-Mubarakshina, M., and Vilyanen, D. (2024) Pathways of oxygen-dependent oxidation of the plastoquinone pool in the dark after illumination, Plants, 13, 3479, https://doi.org/10.3390/plants13243479.
  49. Zhou, Q., Yamamoto, H., and Shikanai, T. (2022) Distinct contribution of two cyclic electron transport pathways to P700 oxidation, Plant Physiol., 192, 326-341, https://doi.org/10.1093/plphys/kiac557.
  50. Kono, M., and Terashima, I. (2016) Elucidation of photoprotective mechanisms of PSI against fluctuating light photoinhibition, Plant Cell Physiol., 57, 1405-1414, https://doi.org/10.1093/pcp/pcw103.
  51. Kramer, M., Rodriguez-Heredia, M., Saccon, F., Mosebach, L., Twachtmann, M., Krieger-Liszkay, A., Duffy, C., Knell, R. J., Finazzi, J., 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.
  52. Rodriguez-Heredia, M., Saccon, F., Wilson, S., Finazzi, G., Ruban, A. V., and Hanke, G. T. (2022) Protection of photosystem I during sudden light stress depends on ferredoxin:NADP(H) reductase abundance and interactions, Plant Physiol., 188, 1028-1042, https://doi.org/10.1093/plphys/kiab550.
  53. Tikhonov, A. N. (2024) The cytochrome b6f complex: plastoquinol oxidation and regulation of electron transport in chloroplasts, Photosynth. Res., 159, 203-227, https://doi.org/10.1007/s11120-023-01034-w.
  54. Kurisu, G., Zhang, H., Smith, J. L., and Cramer, W. A. (2003) Structure of the cytochrome b6f complex of oxygenic photosynthesis: tuning the cavity, Science, 302, 1009-1014, https://doi.org/10.1126/science.1090165.
  55. Malone, L. A., Qian, P., Mayneord, G. E., Hitchcock, A., Farmer, D. A., Thompson, R. F., Swainsbury, D. J. K., Ranson, N. A., Hunter, C. N., and Johnson, M. P. (2019) Cryo-EM structure of the spinach cytochrome b6 f complex at 3.6 Å resolution, Nature, 575, 535-539, https://doi.org/10.1038/s41586-019-1746-6.
  56. Pintscher, S., Pietras, R., Mielecki, B., Szwalec, M., Wójcik-Augustyn, A., Indyka, P., Rawski, M., Koziej, L., Jaciuk, M., Ważny, G., Glatt, S., and Osyczka, A. (2024) Molecular basis of plastoquinone reduction in plant cytochrome b6f, Nat. Plants, 10, 1814-1825, https://doi.org/10.1038/s41477-024-01804-x.
  57. Martinez, S. E., Huang, D., Ponomarev, M., Cramer, W. A., and Smith, J. L. (1996) The heme redox center of chloroplast cytochrome f is linked to a buried five-water chain, Protein Sci., 5, 1081-1092, https://doi.org/10.1002/pro.5560050610.
  58. Ponamarev, M. V., and Cramer, W. A. (1998) Perturbation of the internal water chain in cytochrome f of oxygenic photosynthesis: loss of the concerted reduction of cytochromes f and b6, Biochemistry, 37, 17199-17208, https://doi.org/10.1021/bi981814j.
  59. Sainz, G., Carrell, C. J., Ponamarev, M. V., Soriano, G. M., Cramer, W. A., and Smith, J. L. (2000) Interruption of the internal water chain of cytochrome f impairs photosynthetic function, Biochemistry, 39, 9164-9173, https://doi.org/10.1021/bi0004596.
  60. Hasan, S. S., Yamashita, E., Baniulis, D., and Cramer, W. A. (2013) Quinone-dependent proton transfer pathways in the photosynthetic cytochrome b6f complex, Proc. Natl. Acad. Sci. USA, 110, 4297-4302, https://doi.org/10.1073/pnas.1222248110.
  61. Crofts, A. R., Hong, S., Wilson, C., Burton, R., Victoria, D., Harrison, C., and Schulten, K. (2013) The mechanism of ubihydroquinone oxidation at the Qo-site of the cytochrome bc1 complex, Biochim. Biophys. Acta Bioenerg., 1827, 1362-1377, https://doi.org/10.1016/j.bbabio.2013.01.009.
  62. 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.
  63. Zito, F., Finazzi, G., Joliot, P., and Wollman, F. A. (1998) Glu78, from the conserved PEWY sequence of subunit IV, has a key function in cytochrome b6f turnover, Biochemistry, 37, 10395-10403, https://doi.org/10.1021/bi980238o.
  64. Szwalec, M., Bujnowicz, Ł., Sarewicz, M., and Osyczka, A. (2022) Unexpected heme redox potential values implicate an uphill step in cytochrome b6f, J. Phys. Chem. B, 126, 9771-9780, https://doi.org/10.1021/acs.jpcb.2c05729.
  65. Hope, A. B. (1993) The chloroplast cytochrome bf complex A critical focus on function, Biochim. Biophys. Acta Bioenerg., 1143, 1-22, https://doi.org/10.1016/0005-2728(93)90210-7.
  66. Ustynyuk, L. Y., and Tikhonov, A. N. (2022) Plastoquinol oxidation: rate-limiting stage in the electron transport chain of chloroplasts, Biochemistry (Moscow), 87, 1084-1097, https://doi.org/10.1134/S0006297922100029.
  67. Sarewicz, M., Szwalec, M., Pintscher, S., Indyka, P., Rawski, M., Pietras, R., Mielecki, B., Koziej, Ł., Jaciuk, M., Glatt, S., and Osyczka, A. (2023) High-resolution cryo-EM structures of plant cytochrome b6f at work, Sci. Adv., 9, eadd9688, https://doi.org/10.1126/sciadv.add9688.
  68. Finazzi, G. (2002) Redox-coupled proton pumping activity in cytochrome b6f, as evidenced by the pH dependence of electron transfer in whole cells of Chlamydomonas reinhardtii, Biochemistry, 41, 7475-7482, https://doi.org/10.1021/bi025714w.
  69. Soriano, G. M., Guo, L.-W., de Vitry, C., Kallas, T., and Cramer, W. A. (2002) Electron transfer from the Rieske iron-sulfur Protein (ISP) to cytochrome f in vitro, J. Biol. Chem., 277, 41865-41871, https://doi.org/10.1074/jbc.M205772200.
  70. Arantes, G. M. (2025) Redox-activated proton transfer through a redundant network in the Qo site of cytochrome bc1, J. Chem. Inf. Model, 65, 2660-2669, https://doi.org/10.1021/acs.jcim.4c02361.
  71. Soriano, G. M., Ponamarev, M. V., Carrell, C. J., Xia, D., Smith, J. L., and Cramer, W. A. (1999) Comparison of the cytochrome bc1 complex with the anticipated structure of the cytochrome b6f complex: De Plus Ça Change de Plus C’est la Même Chose, J. Bioenerg. Biomembr., 31, 201-214, https://doi.org/10.1023/A:1005463527752.
  72. Rumberg, B., and Siggel, U. (1969) pH changes in the inner phase of the thylakoids during photosynthesis, Naturwissenschaften, 56, 130-132, https://doi.org/10.1007/BF00601025.
  73. Tikhonov, A. N., Khomutov, G. B., Ruuge, E. K., and Blumenfeld, L. A. (1981) Electron transport control in chloroplasts. Effects of photosynthetic control monitored by the intrathylakoid pH, Biochim. Biophys. Acta Bioenerg., 637, 321-333, https://doi.org/10.1016/0005-2728(81)90171-7.
  74. Hope, A. B., Valente, P., and Matthews, D. B. (1994) Effects of pH on the kinetics of redox reactions in and around the cytochrome bf complex in an isolated system, Photosynth. Res., 42, 111-120, https://doi.org/10.1007/BF02187122.
  75. Finazzi, G., and Rappaport, F. (1998) In vivo characterization of the electrochemical proton gradient generated in darkness in green algae and its kinetic effects on cytochrome b6f turnover, Biochemistry, 37, 9999-10005, https://doi.org/10.1021/bi980320j.
  76. Tikhonov, A. N. (2015) Induction events and short-term regulation of electron transport in chloroplasts: an overview, Photosynth. Res., 125, 65-94, https://doi.org/10.1007/s11120-015-0094-0.
  77. Finazzi, G., Minagawa, J., and Johnson, G. N. (2016) The cytochrome b6f complex: a regulatory hub controlling electron flow and the dynamics of photosynthesis? in Cytochrome Complexes: Evolution, Structures, Energy Transduction, and Signaling (Cramer, W. A., and Kallas, T., eds), Springer Netherlands, pp. 437-452, https://doi.org/10.1007/978-94-017-7481-9_22.
  78. Genty, B., and Harbinson, J. (1996) Regulation of light utilization for photosynthetic electron transport, in Photosynthesis and the Environment (Baker, N. R., eds), Springer Netherlands, pp. 67-99, https://doi.org/10.1007/0-306-48135-9_3.
  79. Kramer, D. M., Sacksteder, C. A., and Cruz, J. A. (1999) How acidic is the lumen? Photosynth. Res., 60, 151-163, https://doi.org/10.1023/A:1006212014787.
  80. Cooley, J. W. (2013) Protein conformational changes involved in the cytochrome bc1 complex catalytic cycle, Biochim. Biophys. Acta Bioenerg., 1827, 1340-1345, https://doi.org/10.1016/j.bbabio.2013.07.007.
  81. Schoepp, B., Brugna, M., Riedel, A., Nitschke, W., and Kramer, D. M. (1999) The Qo-site inhibitor DBMIB favours the proximal position of the chloroplast Rieske protein and induces a pK-shift of the redox-linked proton, FEBS Lett., 450, 245-250, https://doi.org/10.1016/s0014-5793(99)00511-6.
  82. Roberts, A. G., Bowman, M. K., and Kramer, D. M. (2004) The inhibitor DBMIB provides insight into the functional architecture of the Qo site in the cytochrome b6f complex, Biochemistry., 43, 7707-7716, https://doi.org/10.1021/bi049521f.
  83. Vilyanen, D., Pavlov, I., Naydov, I., Ivanov, B., and Kozuleva, M. (2024) Peculiarities of DNP-INT and DBMIB as inhibitors of the photosynthetic electron transport, Photosynth. Res., 161, 79-92, https://doi.org/10.1007/s11120-023-01063-5.
  84. Jahns, P., Graf, M., Munekage, Y., and Shikanai, T. (2002) Single point mutation in the Rieske iron-sulfur subunit of cytochrome b6/f leads to an altered pH dependence of plastoquinol oxidation in Arabidopsis, FEBS Lett., 519, 99-102, https://doi.org/10.1016/s0014-5793(02)02719-9.
  85. 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.
  86. Ivanov, B. N. (1993) Stoichiometry of proton uptake by thylakoids during electron transport in chloroplasts, in Photosynthesis: Photoreactions to Plant Productivity (Abrol, Y. P., Mohanty, P., and Govindjee, eds), Springer Netherlands, pp. 109-128, https://doi.org/10.1007/978-94-011-2708-0_4.
  87. Schansker, G. (2022) Determining photosynthetic control, a probe for the balance between electron transport and Calvin-Benson cycle activity, with the DUAL-KLAS-NIR, Photosynth. Res., 153, 191-204, https://doi.org/10.1007/s11120-022-00934-7.
  88. Joliot, P., and Johnson, G. N. (2011) Regulation of cyclic and linear electron flow in higher plants, Proc. Natl. Acad. Sci. USA, 108, 13317-13322, https://doi.org/10.1073/pnas.1110189108.
  89. Ott, T., Clarke, J., Birks, K., and Johnson, G. (1999) Regulation of the photosynthetic electron transport chain, Planta, 209, 250-258, https://doi.org/10.1007/s004250050629.
  90. Harbinson, J., and Hedley, C. L. (1989) The kinetics of P-700+ reduction in leaves: a novel in situ probe of thylakoid functioning, Plant Cell Environ., 12, 357-369, https://doi.org/10.1111/j.1365-3040.1989.tb01952.x.
  91. Laisk, A., and Oja, V. (1994) Range of photosynthetic control of postillumination P700+ reduction rate in sunflower leaves, Photosynth. Res., 39, 39-50, https://doi.org/10.1007/BF00027141.
  92. Kanazawa, A., Ostendorf, E., Kohzuma, K., Hoh, D., Strand, D. D., Sato-Cruz, M., Savage, L., Cruz, J. A., Fisher, N., Froehlich, J. E., and Kramer, D. M. (2017) Chloroplast ATP synthase modulation of the thylakoid proton motive force: implications for photosystem I and photosystem II photoprotection, Front. Plant Sci., 8, 719, https://doi.org/10.3389/fpls.2017.00719.
  93. Takagi, D., Amako, K., Hashiguchi, M., Fukaki, H., Ishizaki, K., Goh, T., Fukao, Y., Sano, R., Kurata, T., Demura, T., Sawa, S., and Miyake, C. (2017) Chloroplastic ATP synthase builds up a proton motive force preventing production of reactive oxygen species in photosystem I, Plant J., 91, 306-324, https://doi.org/10.1111/tpj.13566.
  94. Wang, C., and Shikanai, T. (2019) Modification of activity of the thylakoid H+/K+ antiporter KEA3 disturbs ∆pH-­dependent regulation of photosynthesis, Plant Physiol., 181, 762-773, https://doi.org/10.1104/pp.19.00766.
  95. Wu, G., Ortiz-Flores, G., Ortiz-Lopez, A., and Ort, D. R. (2007) A point mutation in atpC1 raises the redox potential of the Arabidopsis chloroplast ATP synthase γ-subunit regulatory disulfide above the range of thioredoxin modulation, JBC, 282, 36782-36789, https://doi.org/10.1074/jbc.M707007200.
  96. Degen, G. E., Jackson, P. J., Proctor, M. S., Zoulias, N., Casson, S. A., and Johnson, M. P. (2023) High cyclic electron transfer via the PGR5 pathway in the absence of photosynthetic control, Plant Physiol., 192, 370-386, https://doi.org/10.1093/plphys/kiad084.
  97. Nandha, B., Finazzi, G., Joliot, P., Hald, S., and Johnson, G. N. (2007) The role of PGR5 in the redox poising of photosynthetic electron transport, Biochim. Biophys. Acta Bioenerg., 1767, 1252-1259, https://doi.org/10.1016/j.bbabio.2007.07.007.
  98. Penzler, J.-F., Naranjo, B., Walz, S., Marino, G., Kleine, T., and Leister, D. (2024) A pgr5 suppressor screen uncovers two distinct suppression mechanisms and links cytochrome b6f complex stability to PGR5, Plant Cell, 36, 4245-4266, https://doi.org/10.1093/plcell/koae098.
  99. Degen, G. E., Pastorelli, F., and Johnson, M. P. (2024) Proton Gradient Regulation 5 is required to avoid photosynthetic oscillations during light transitions, J. Exp. Bot., 75, 947-961, https://doi.org/10.1093/jxb/erad428.
  100. Avenson, T. J., Cruz, J. A., Kanazawa, A., and Kramer, D. M. (2005) Regulating the proton budget of higher plant photosynthesis, Proc. Natl. Acad. Sci. USA, 102, 9709-9713, https://doi.org/10.1073/pnas.0503952102.
  101. 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.
  102. Kozuleva, M., Goss, T., Twachtmann, M., Rudi, K., Trapka, J., Selinski, J., Ivanov, B., Garapati, P., Steinhoff, H., 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.
  103. 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.
  104. Sang, M., Ma, F., Xie, J., Chen, X.-B., Wang, K.-B., Qin, X.-C., Wang, W.-D., Zhao, J.-Q., Li, L.-B., Zhang, J.-P., and Kuang, T.-Y. (2010) High-light induced singlet oxygen formation in cytochrome b6f complex from Bryopsis corticulans as detected by EPR spectroscopy, Biophys. Chem., 146, 7-12, https://doi.org/10.1016/j.bpc.2009.09.012.
  105. 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, Biochem., 52, 8975-8983, https://doi.org/10.1021/bi4013534.
  106. Sarewicz, M., Bujnowicz, Ł., Bhaduri, S., Singh, S. K., Cramer, W. A., and Osyczka, A. (2017) Metastable radical state, nonreactive with oxygen, is inherent to catalysis by respiratory and photosynthetic cytochromes bc1/b6f, Proc. Natl. Acad. Sci. USA, 114, 1323-1328, https://doi.org/10.1073/pnas.1618840114.
  107. Borisova-Mubarakshina, M. M., Naydov, I. A., and Ivanov, B. N. (2018) Oxidation of the plastoquinone pool in chloroplast thylakoid membranes by superoxide anion radicals, FEBS Lett., 592, 3221-3228, https://doi.org/10.1002/1873-3468.13237.
  108. 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.
  109. Pesaresi, P., Pribil, M., Wunder, T., and Leister, D. (2011) Dynamics of reversible protein phosphorylation in thylakoids of flowering plants: the roles of STN7, STN8 and TAP38, Biochim. Biophys. Acta Bioenerg., 1807, 887-896, https://doi.org/10.1016/j.bbabio.2010.08.002.
  110. Schönberg, A., Rödiger, A., Mehwald, W., Galonska, J., Christ, G., Helm, S., Thieme, D., Majovsky, P., Hoehenwarter, W., and Baginsky, S. (2017) Identification of STN7/STN8 kinase targets reveals connections between electron transport, metabolism and gene expression, Plant J., 90, 1176-1186, https://doi.org/10.1111/tpj.13536.
  111. Grieco, M., Tikkanen, M., Paakkarinen, V., Kangasjärvi, S., and Aro, E.-M. (2012) Steady-state phosphorylation of light-harvesting complex II proteins preserves photosystem I under fluctuating white light, Plant Physiol., 160, 1896-1910, https://doi.org/10.1104/pp.112.206466.
  112. Shapiguzov, A., Chai, X., Fucile, G., Longoni, P., Zhang, L., and Rochaix, J.-D. (2016) Activation of the Stt7/STN7 kinase through dynamic interactions with the cytochrome b6f complex, Plant Physiol., 171, 82-92, https://doi.org/10.1104/pp.15.01893.
  113. Hoh, D., Froehlich, J. E., and Kramer, D. M. (2024) Redox regulation in chloroplast thylakoid lumen: the pmf changes everything, again, Plant Cell Environ., 47, 2749-2765, https://doi.org/10.1111/pce.14789.
  114. Балашов Н.В., Борисова-Мубаракшина М.М., Ветошкина Д.В. (2025) Влияние пероксида водорода на перераспределение антенных комплексов между фотосистемами у высших растений, Биохимия, 90, 1028-1042, https://doi.org/10.31857/S0320972525070112.
  115. Fernyhough, P., Horton, P., and Foyer, C. (1984) Regulation of light harvesting chlorophyll a/b binding protein (LHCP) phosphorylation in intact maize mesophyll chloroplasts, in Advances in Photosynthesis Research, Springer, Dordrecht, pp. 299-302, https://doi.org/10.1007/978-94-017-4973-2_68.
  116. Vershubskii, A. V., Trubitsin, B. V., Priklonskii, V. I., and Tikhonov, A. N. (2017) Lateral heterogeneity of the proton potential along the thylakoid membranes of chloroplasts, Biochim. Biophys. Acta Bioenerg., 1859, 388-401, https://doi.org/10.1016/j.bbamem.2016.11.016.

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