Impact of hydrogen peroxide on the redistribution of antenna complexes between photosystems in higher plants

Мұқаба

Дәйексөз келтіру

Толық мәтін

Ашық рұқсат Ашық рұқсат
Рұқсат жабық Рұқсат берілді
Рұқсат жабық Тек жазылушылар үшін

Аннотация

One of the acclimatory mechanisms of photosynthetic organisms to changing light conditions is the redistribution of antenna complexes between photosystems, the process known as state transitions. This process allows the amount of light energy absorbed by each photosystem to be regulated. Numerous studies have demonstrated that state transitions are inhibited under high light intensity; however, the exact mechanism of this inhibition remains unclear. In the present study, the effect of H2O2 at various concentrations on the state transition process was investigated using functionally active thylakoids isolated from Arabidopsis leaves. Additionally, the specific stage of this process affected by H2O2 was evaluated. To assess state transitions, low-temperature chlorophyll a fluorescence spectra (F, from 650 to 780 nm) were measured, and the F745/F685 ratio was calculated as an indicator of state transition activity. It was shown that the addition of H2O2 led to the inhibition of state transitions in low light. The addition of H2O2 to thylakoids under low light conditions resulted in a decreased accumulation of phosphorylated Lhcb1 and Lhcb2 proteins, which are involved in state transitions. This indicates that the inhibition of state transitions is likely a consequence of inhibited activity of the STN7 kinase. It is important to note that H2O2 at the concentrations used did not affect the rate of electron transport, indicating that the inhibition of STN7 kinase activity is not associated with a suppression of the photosynthetic electron transport chain functioning. Moreover, the study demonstrates the selective effect of H2O2 on the activity of the STN7 kinase: no decrease in the level of the phosphorylated photosystem II D1 protein, the substrate of the STN8 kinase, was observed upon H2O2 treatment. Thus, this work provides the first evidence of the H2O2-dependent inhibitory mechanism of STN7 kinase activity and, consequently, of the state transition process.

Авторлар туралы

N. Balashov

Institute of Basic Biological Problems of the Russian Academy of Sciences, Federal Research Center, Pushchino Scientific Center for Biological Research of the Russian Academy of Sciences

Хат алмасуға жауапты Автор.
Email: vetoshkina_d@mail.ru
Pushchino, Moscow Region

M. Borisova-Mubarakshina

Institute of Basic Biological Problems of the Russian Academy of Sciences, Federal Research Center, Pushchino Scientific Center for Biological Research of the Russian Academy of Sciences

Email: vetoshkina_d@mail.ru
Pushchino, Moscow Region

D. Vetoshkina

Institute of Basic Biological Problems of the Russian Academy of Sciences, Federal Research Center, Pushchino Scientific Center for Biological Research of the Russian Academy of Sciences

Email: vetoshkina_d@mail.ru
Pushchino, Moscow Region

Әдебиет тізімі

  1. Wientjes, E., van Amerongen, H., and Croce, R. (2013) LHCII is an antenna of both photosystems after long-term acclimation, Biochim. Biophys. Acta, 1827, 420-426, https://doi.org/10.1016/j.bbabio.2012.12.009.
  2. Crepin, A., and Caffarri, S. (2015) The specific localizations of phosphorylated Lhcb1 and Lhcb2 isoforms reveal the role of Lhcb2 in the formation of the PSI-LHCII supercomplex in Arabidopsis during state transitions, Biochim. Biophys. Acta Bioenergetics, 1847, 1539-1548, https://doi.org/10.1016/j.bbabio.2015.09.005.
  3. Longoni, P., Douchi, D., Cariti, F., Fucile, G., and Goldschmidt-Clermont, M. (2015) Phosphorylation of the light-harvesting complex II isoform Lhcb2 is central to state transitions, Plant Physiol., 169, 2874-2883, https://doi.org/10.1104/pp.15.01498.
  4. Pietrzykowska, M., Suorsa, M., Semchonok, D. A., Tikkanen, M., Boekema, E. J., Aro, E.-M., and Jansson, S. (2014) The light-harvesting chlorophyll a/b binding proteins Lhcb1 and Lhcb2 play complementary roles during state transitions in Arabidopsis, Plant Cell, 26, 3646-3660, https://doi.org/10.1105/tpc.114.127373.
  5. Wood, W. H. J., Barnett, S. F. H., Flannery, S., Hunter, C. N., and Johnson, M. P. (2019) Dynamic thylakoid stacking is regulated by LHCII phosphorylation but not its interaction with PSI, Plant Physiol., 180, 2152-2166, https://doi.org/10.1104/pp.19.00503.
  6. Rintamaki, E., Salonen, M., Suoranta, U. M., Carlberg, I., Andersson, B., and Aro, E. M. (1997) Phosphorylation of light-harvesting complex II and photosystem II core proteins shows different irradiance-dependent regulation in vivo. Application of phosphothreonine antibodies to analysis of thylakoid phosphoproteins, J. Biol. Chem., 272, 30476-30482, https://doi.org/10.1074/jbc.272.48.30476.
  7. Lemeille, S., and Rochaix, J.-D. (2010) State transitions at the crossroad of thylakoid signalling pathways, Photosynth Res., 106, 33-46, https://doi.org/10.1007/s11120-010-9538-8.
  8. Mekala, N. R., Suorsa, M., Rantala, M., Aro, E.-M., and Tikkanen, M. (2015) Plants actively avoid state transitions upon changes in light intensity: role of light-harvesting complex II protein dephosphorylation in high light, Plant Physiol., 168, 721-734, https://doi.org/10.1104/pp.15.00488.
  9. Lemeille, S., Willig, A., Depege-Fargeix, N., Delessert, C., Bassi, R., and Rochaix, J.-D. (2009) Analysis of the chloroplast protein kinase Stt7 during state transitions, PLoS Biol., 7, e1000045, https://doi.org/10.1371/journal.pbio.1000045.
  10. Depege, N., Bellafiore, S., and Rochaix, J.-D. (2003) Role of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas, Science, 299, 1572-1575, https://doi.org/10.1126/science.1081397.
  11. 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 complex1, Plant Physiol., 171, 82-92, https://doi.org/10.1104/pp.15.01893.
  12. Zito, F., Finazzi, G., Delosme, R., Nitschke, W., Picot, D., and Wollman, F. A. (1999) The Qo site of cytochrome b6f complexes controls the activation of the LHCII kinase, EMBO J., 18, 2961-2969, https://doi.org/10.1093/emboj/18.11.2961.
  13. Bellafiore, S., Barneche, F., Peltier, G., and Rochaix, J.-D. (2005) State transitions and light adaptation require chloroplast thylakoid protein kinase STN7, Nature, 433, 892-895, https://doi.org/10.1038/nature03286.
  14. Wu, J., Rong, L., Lin, W., Kong, L., Wei, D., Zhang, L., Rochaix, J.-D., and Xu, X. (2021) Functional redox links between lumen thiol oxidoreductase1 and serine/threonine-protein kinase STN7, Plant Physiol., 186, 964-976, https://doi.org/10.1093/plphys/kiab091.
  15. Singh, S. K., Hasan, S. S., Zakharov, S. D., Naurin, S., Cohn, W., Ma, J., Whitelegge, J.P., and Cramer, W. A. (2016) Trans-membrane signaling in photosynthetic state transitions: redox- and structure-dependent interaction in vitro between STT7 kinase and the cytochrome b6f complex, J. Biol. Chem., 291, 21740-21750, https://doi.org/10.1074/jbc.M116.732545.
  16. Puthiyaveetil, S. (2011) A mechanism for regulation of chloroplast LHC II kinase by plastoquinol and thioredoxin, FEBS Lett., 585, 1717-1721, https://doi.org/10.1016/j.febslet.2011.04.076.
  17. Rintamaki, E., Martinsuo, P., Pursiheimo, S., and Aro, E. M. (2000) Cooperative regulation of light-harvesting complex II phosphorylation via the plastoquinol and ferredoxin-thioredoxin system in chloroplasts, Proc. Natl. Acad. Sci. USA, 97, 11644-11649, https://doi.org/10.1073/pnas.180054297.
  18. Ancin, M., Fernandez-San Millan, A., Larraya, L., Morales, F., Veramendi, J., Aranjuelo, I., and Farran, I. (2019) Overexpression of thioredoxin m in tobacco chloroplasts inhibits the protein kinase STN7 and alters photosynthetic performance, J. Exp. Bot., 70, 1005-1016, https://doi.org/10.1093/jxb/ery415.
  19. Calvo, I. A., Boronat, S., Domenech, A., Garcia-Santamarina, S., Ayte, J., and Hidalgo, E. (2013) Dissection of a redox relay: H2O2-dependent activation of the transcription factor Pap1 through the peroxidatic Tpx1-thioredoxin cycle, Cell Rep., 5, 1413-1424, https://doi.org/10.1016/j.celrep.2013.11.027.
  20. Kim, J.-R., Yoon, H. W., Kwon, K.-S., Lee, S.-R., and Rhee, S. G. (2000) Identification of proteins containing cysteine residues that are sensitive to oxidation by hydrogen peroxide at neutral pH, Anal. Biochem., 283, 214-221, https://doi.org/10.1006/abio.2000.4623.
  21. Chen, K., Vita, J. A., Berk, B. C., and Keaney, J. J. (2001) c-Jun N-terminal kinase activation by hydrogen peroxide in endothelial cells involves SRC-dependent epidermal growth factor receptor transactivation, J. Biol. Chem., 276, 16045-16050, https://doi.org/10.1074/jbc.M011766200.
  22. Guyton, K. Z., Liu, Y., Gorospe, M., Xu, Q., and Holbrook, N. J. (1996) Activation of mitogen-activated protein kinase by HO role in cell survival following oxidant injury, J. Biol. Chem., 271, 4138-4142, https://doi.org/10.1074/jbc.271.8.4138.
  23. Khorobrykh, S. A., Karonen, M., and Tyystjarvi, E. (2015) Experimental evidence suggesting that H2O2 is produced within the thylakoid membrane in a reaction between plastoquinol and singlet oxygen, FEBS Lett., 589, 779-786, https://doi.org/10.1016/j.febslet.2015.02.011.
  24. Roach, T., Na, C. S., and Krieger-Liszkay, A. (2015) High light-induced hydrogen peroxide production in Chlamydomonas reinhardtii is increased by high CO2 availability, Plant J., 81, 759-766, https://doi.org/10.1111/tpj.12768.
  25. Casazza, A. P., Tarantino, D., and Soave, C. (2001) Preparation and functional characterization of thylakoids from Arabidopsis thaliana, Photosynth. Res., 68, 175-180, https://doi.org/10.1023/A:1011818021875.
  26. Lichtenthaler, H. K. (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes, in Methods in Enzymology, Academic Press, vol. 148, pp. 350-382, https://doi.org/10.1016/0076-6879(87)48036-1.
  27. McCormac, D. J., Bruce, D., and Greenberg, B. M. (1994) State transitions, light-harvesting antenna phosphorylation and light-harvesting antenna migration in vivo in the higher plant Spirodela oligorrhiza, Biochim. Biophys. Acta Bioenergetics, 1187, 301-312, https://doi.org/10.1016/0005-2728(94)90004-3.
  28. Mubarakshina, M. M., Ivanov, B. N., Naydov, I. A., Hillier, W., Badger, M. R., and Krieger-Liszkay, A. (2010) Production and diffusion of chloroplastic H2O2 and its implication to signalling, J. Exp. Bot., 61, 3577-3587, https://doi.org/10.1093/jxb/erq171.
  29. Bonardi, V., Pesaresi, P., Becker, T., Schleiff, E., Wagner, R., Pfannschmidt, T., Jahns, P., and Leister, D. (2005) Photo system II core phosphorylation and photosynthetic acclimation require two different protein kinases, Nature, 437, 1179-1182, https://doi.org/10.1038/nature04016.
  30. Vainonen, J. P., Hansson, M., and Vener, A. V. (2005) STN8 Protein kinase in Arabidopsis thaliana is specific in phosphorylation of photosystem II core proteins, J. Biol. Chem., 280, 33679-33686, https://doi.org/10.1074/jbc.M505729200.
  31. Hommel, E., Liebers, M., Offermann, S., and Pfannschmidt, T. (2021) Effectiveness of light-quality and dark-white growth light shifts in short-term light acclimation of photosynthesis in Arabidopsis, Front. Plant Sci., 12, 615253, https://doi.org/10.3389/fpls.2021.615253.
  32. Oung, H. M. O., Koochak, H., Krysiak, M., Svoboda, V., and Kirchhoff, H. (2024) A holistic quantitative understanding of state transition in plant photosynthesis, bioRxiv, 2024.06.21.600050, https://doi.org/10.1101/2024.06.21.600050.
  33. Saito, A., Shimizu, M., Nakamura, H., Maeno, S., Katase, R., Miwa, E., Higuchi, K., and Sonoike, K. (2014) Fe deficiency induces phosphorylation and translocation of Lhcb1 in barley thylakoid membranes, FEBS Lett., 588, 2042-2048, https://doi.org/10.1016/j.febslet.2014.04.031.
  34. Nellaepalli, S., Mekala, N. R., Zsiros, O., Mohanty, P., and Subramanyam, R. (2011) Moderate heat stress induces state transitions in Arabidopsis thaliana, Biochim. Biophys. Acta Bioenergetics, 1807, 1177-1184, https://doi.org/10.1016/j.bbabio.2011.05.016.
  35. Vener, A. V., van Kan, P. J. M., Rich, P. R., Ohad, I., and Andersson, B. (1997) Plastoquinol at the quinol oxidation site of reduced cytochrome bf mediates signal transduction between light and protein phosphorylation: thylakoid protein kinase deactivation by a single-turnover flash, Proc. Natl. Acad. Sci. USA, 94, 1585-1590, https://doi.org/10.1073/pnas.94.4.1585.
  36. Reiland, S., Messerli, G., Baerenfaller, K., Gerrits, B., Endler, A., Grossmann, J., Gruissem, W., and Baginsky, S. (2009) Large-scale Arabidopsis phosphoproteome profiling reveals novel chloroplast kinase substrates and phosphorylation networks, Plant Physiol., 150, 889-903, https://doi.org/10.1104/pp.109.138677.
  37. Trotta, A., Suorsa, M., Rantala, M., Lundin, B., and Aro, E.-M. (2016) Serine and threonine residues of plant STN7 kinase are differentially phosphorylated upon changing light conditions and specifically influence the activity and stability of the kinase, Plant J., 87, 484-494, https://doi.org/10.1111/tpj.13213.
  38. Willig, A., Shapiguzov, A., Goldschmidt-Clermont, M., and Rochaix, J.-D. (2011) The phosphorylation status of the chloroplast protein kinase STN7 of Arabidopsis affects its turnover, Plant Physiol., 157, 2102-2107, https://doi.org/10.1104/pp.111.187328.
  39. Nellaepalli, S., Kodru, S., Malavath, T., Subramanyam, R. (2013) Change in fast Chl a fluorescence transients, 2 dimensional protein profile and pigment protein interactions during state transitions in Arabidopsis thaliana, J. Photochem. Photobiol. B, 128, 27-34, https://doi.org/10.1016/j.jphotobiol.2013.07.028.
  40. Cutolo, E. A., Caferri, R., Guardini, Z., Dall'Osto, L., and Bassi, R. (2023) Analysis of state 1 - state 2 transitions by genome editing and complementation reveals a quenching component independent from the formation of PSI-LHCI-LHCII supercomplex in Arabidopsis thaliana, Biol. Direct, 18, 49, https://doi.org/10.1186/s13062-023-00406-5.
  41. 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 Bioenergetics, 1757, 1496-1503, https://doi.org/10.1016/j.bbabio.2006.09.004.
  42. Borisova, M. M., Kozuleva, M. A., Rudenko, N. N., Naydov, I. A., Klenina, I. B., and Ivanov, B. N. (2012) Photosynthetic electron flow to oxygen and diffusion of hydrogen peroxide through the chloroplast envelope via aquaporins, Biochim. Biophys. Acta Bioenergetics, 1817, 1314-1321, https://doi.org/10.1016/j.bbabio.2012.02.036.
  43. Liu, X., Chai, J., Ou, X., Li, M., and Liu, Z. (2019) Structural insights into substrate selectivity, catalytic mechanism, and redox regulation of rice photosystem ii core phosphatase, Mol. Plant, 12, 86-98, https://doi.org/10.1016/j.molp.2018.11.006.
  44. Tikkanen, M., Piippo, M., Suorsa, M., Sirpio, S., Mulo, P., Vainonen, J., Vener, A. V., Allahverdiyeva, Y., and Aro, E.-M. (2006) State transitions revisited-a buffering system for dynamic low light acclimation of Arabidopsis, Plant Mol. Biol., 62, 779-793, https://doi.org/10.1007/s11103-006-9044-8.
  45. Pursiheimo, S., Mulo, P., Rintamaki, E., and Aro, E. M. (2001) Coregulation of light-harvesting complex II phosphorylation and lhcb mRNA accumulation in winter rye, Plant J., 26, 317-327, https://doi.org/10.1046/j.1365-313x.2001.01033.x.
  46. Nellaepalli, S., Kodru, S., and Subramanyam, R. (2012) Effect of cold temperature on regulation of state transitions in Arabidopsis thaliana, J. Photochem. Photobiol. B Biol., 112, 23-30, https://doi.org/10.1016/j.jphotobiol.2012.04.003.
  47. Chen, Y., and Hoehenwarter, W. (2015) Changes in the phosphoproteome and metabolome link early signaling events to rearrangement of photosynthesis and central metabolism in salinity and oxidative stress response in Arabidopsis, Plant Physiol., 169, 3021-3033, https://doi.org/10.1104/pp.15.01486.

Қосымша файлдар

Қосымша файлдар
Әрекет
1. JATS XML
Жүктеу

© Russian Academy of Sciences, 2025

Согласие на обработку персональных данных с помощью сервиса «Яндекс.Метрика»

1. Я (далее – «Пользователь» или «Субъект персональных данных»), осуществляя использование сайта https://journals.rcsi.science/ (далее – «Сайт»), подтверждая свою полную дееспособность даю согласие на обработку персональных данных с использованием средств автоматизации Оператору - федеральному государственному бюджетному учреждению «Российский центр научной информации» (РЦНИ), далее – «Оператор», расположенному по адресу: 119991, г. Москва, Ленинский просп., д.32А, со следующими условиями.

2. Категории обрабатываемых данных: файлы «cookies» (куки-файлы). Файлы «cookie» – это небольшой текстовый файл, который веб-сервер может хранить в браузере Пользователя. Данные файлы веб-сервер загружает на устройство Пользователя при посещении им Сайта. При каждом следующем посещении Пользователем Сайта «cookie» файлы отправляются на Сайт Оператора. Данные файлы позволяют Сайту распознавать устройство Пользователя. Содержимое такого файла может как относиться, так и не относиться к персональным данным, в зависимости от того, содержит ли такой файл персональные данные или содержит обезличенные технические данные.

3. Цель обработки персональных данных: анализ пользовательской активности с помощью сервиса «Яндекс.Метрика».

4. Категории субъектов персональных данных: все Пользователи Сайта, которые дали согласие на обработку файлов «cookie».

5. Способы обработки: сбор, запись, систематизация, накопление, хранение, уточнение (обновление, изменение), извлечение, использование, передача (доступ, предоставление), блокирование, удаление, уничтожение персональных данных.

6. Срок обработки и хранения: до получения от Субъекта персональных данных требования о прекращении обработки/отзыва согласия.

7. Способ отзыва: заявление об отзыве в письменном виде путём его направления на адрес электронной почты Оператора: info@rcsi.science или путем письменного обращения по юридическому адресу: 119991, г. Москва, Ленинский просп., д.32А

8. Субъект персональных данных вправе запретить своему оборудованию прием этих данных или ограничить прием этих данных. При отказе от получения таких данных или при ограничении приема данных некоторые функции Сайта могут работать некорректно. Субъект персональных данных обязуется сам настроить свое оборудование таким способом, чтобы оно обеспечивало адекватный его желаниям режим работы и уровень защиты данных файлов «cookie», Оператор не предоставляет технологических и правовых консультаций на темы подобного характера.

9. Порядок уничтожения персональных данных при достижении цели их обработки или при наступлении иных законных оснований определяется Оператором в соответствии с законодательством Российской Федерации.

10. Я согласен/согласна квалифицировать в качестве своей простой электронной подписи под настоящим Согласием и под Политикой обработки персональных данных выполнение мною следующего действия на сайте: https://journals.rcsi.science/ нажатие мною на интерфейсе с текстом: «Сайт использует сервис «Яндекс.Метрика» (который использует файлы «cookie») на элемент с текстом «Принять и продолжить».