Photosynthetica 2023, 61(2):250-263 | DOI: 10.32615/ps.2023.021
Photosystems under high light stress: throwing light on mechanism and adaptation
- 1 Department of Basic Sciences, College of Forestry, Dr. Y.S. Parmar University of Horticulture and Forestry, Nauni, 173230 Solan, India
- 2 Division of Plant Physiology, ICAR-Indian Agricultural Research Institute, 110012 New Delhi, India
- 3 Department of Basic Sciences, College of Horticulture and Forestry, Dr. Y.S. Parmar University of Horticulture and Forestry, Neri, 177001 Hamirpur, India
- 4 School of Biochemistry, Devi Ahilya University, 452001 Indore, Madhya Pradesh, India
- 5 Division of Crop Sciences, Central Research Institute for Dryland Agriculture, Hyderabad, Telangana, India
- 6 Department of Agriculture, Food and Environment, University of Pisa, Pisa, Italy
High light stress decreases the photosynthetic rate in plants due to photooxidative damage to photosynthetic apparatus, photoinhibition of PSII, and/or damage to PSI. The dissipation of excess energy by nonphotochemical quenching and degradation of the D1 protein of PSII and its repair cycle help against photooxidative damage. Light stress also activates stress-responsive nuclear genes through the accumulation of phosphonucleotide-3'-phosphoadenosine- 5'-phosphate, methylerythritol cyclodiphosphate, and reactive oxygen species which comprise the chloroplast retrograde signaling pathway. Additionally, hormones, such as abscisic acid, cytokinin, brassinosteroids, and gibberellins, play a role in acclimation to light fluctuations. Several alternate electron flow mechanisms, which offset the excess of electrons, include activation of plastid or plastoquinol terminal oxidase, cytochrome b6/f complex, cyclic electron flow through PSI, Mehler ascorbate peroxidase pathway or water-water cycle, mitochondrial alternative oxidase pathway, and photorespiration. In this review, we provided insights into high light stress-mediated damage to photosynthetic apparatus and strategies to mitigate the damage by decreasing antennae size, enhancing NPQ through the introduction of mutants, expression of algal proteins to improve photosynthetic rates and engineering ATP synthase.
Additional key words: light stress; nonphotochemical quenching; photodamage; photosystem; reactive oxygen species; signaling.
Received: January 31, 2023; Revised: May 13, 2023; Accepted: May 15, 2023; Prepublished online: May 30, 2023; Published: June 6, 2023 Show citation
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References
- Ahmad N., Khan M.O., Islam E. et al.: Contrasting responses to stress displayed by tobacco overexpressing an algal plastid terminal oxidase in the chloroplast. - Front. Plant Sci. 11: 501, 2020.
Go to original source... - Alboresi A., Storti M., Cendron L., Morosinotto T.: Role and regulation of class-C flavodiiron proteins in photosynthetic organisms. - Biochem. J. 476: 2487-2498, 2019.
Go to original source... - Allen J.F., Forsberg J.: Molecular recognition in thylakoid structure and function. - Trends Plant Sci. 6: 317-326, 2001.
Go to original source... - Andersson B., Styring S.: Photosystem II: molecular organization, function, and acclimation. - Curr. Top. Bioenerg. 16: 1-81, 1991.
Go to original source... - Aro E.-M., Suorsa M., Rokka A. et al.: Dynamics of photosystem II: a proteomic approach to thylakoid protein complexes. - J. Exp. Bot. 56: 347-356, 2005.
Go to original source... - Aro E.-M., Virgin I., Andersson B.: Photoinhibition of photosystem II. Inactivation, protein damage and turnover. - BBA-Bioenergetics 1143: 113-134, 1993.
Go to original source... - Asada K.: 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, 1999.
Go to original source... - Baena-González E., Aro E.-M.: Biogenesis, assembly and turnover of photosystem II units. - Philos. T. Roy. Soc. B 357: 1451-1460, 2002.
Go to original source... - Benn G., Bjornson M., Ke H. et al.: Plastidial metabolite MEcPP induces a transcriptionally centered stress-response hub via the transcription factor CAMTA3. - PNAS 113: 8855-8860, 2016.
Go to original source... - Blubaugh D.J., Atamian M., Babcock G.T. et al.: Photoinhibition of hydroxylamine-extracted photosystem II membranes: identification of the sites of photodamage. - Biochemistry 30: 7586-7597, 1991.
Go to original source... - Bolte S., Marcon E., Jaunario M. et al.: Dynamics of the localization of the plastid terminal oxidase inside the chloroplast. - J. Exp. Bot. 71: 2661-2669, 2020.
Go to original source... - Burlacot A., Sawyer A., Cuiné S. et al.: Flavodiiron-mediated O2 photoreduction links H2 production with CO2 fixation during the anaerobic induction of photosynthesis. - Plant Physiol. 177: 1639-1649, 2018.
Go to original source... - Cardona T., Shao S., Nixon P.J.: Enhancing photosynthesis in plants: the light reactions. - Essays Biochem. 62: 85-94, 2018.
Go to original source... - Cazzaniga S., Li Z., Niyogi K.K. et al.: The Arabidopsis szl1 mutant reveals a critical role of β-carotene in photosystem I photoprotection. - Plant Physiol. 159: 1745-1758, 2012.
Go to original source... - Chang C.C.C., Ślesak I., Jordá L. et al.: Arabidopsis chloroplastic glutathione peroxidases play a role in cross-talk between photooxidative stress and immune responses. - Plant Physiol. 150: 670-683, 2009.
Go to original source... - Chaux F., Peltier G., Johnson X.: A security network in PSI photoprotection: regulation of photosynthetic control, NPQ and O2 photoreduction by cyclic electron flow. - Front. Plant Sci. 6: 875, 2015.
Go to original source... - Chen Z., Gallie D.R.: Ethylene regulates energy-dependent non-photochemical quenching in Arabidopsis through repression of the xanthophyll cycle. - PLoS ONE 10: e0144209, 2015.
Go to original source... - Chida H., Nakazawa A., Akazaki H. et al.: Expression of the algal cytochrome c6 gene in Arabidopsis enhances photosynthesis and growth. - Plant Cell Physiol. 48: 948-957, 2007.
Go to original source... - Colombo M., Suorsa M., Rossi F. et al.: Photosynthesis control: An underrated short-term regulatory mechanism essential for plant viability. - Plant Signal. Behav. 11: e1165382, 2016.
Go to original source... - Cortleven A., Nitschke S., Klaumunzer M. et al.: A novel protective function for cytokinin in the light stress response is mediated by the ARABIDOPSIS HISTIDINE KINASE2 and ARABIDOPSIS HISTIDINE KINASE3 receptors. - Plant Physiol. 164: 1470-1483, 2014.
Go to original source... - Czégény G., Mátai A., Hideg É.: UV-B effects on leaves - Oxidative stress and acclimation in controlled environments. -Plant Sci. 248: 57-63, 2016.
Go to original source... - Damkjaer J.T., Kereïche S., Johnson M.P. et al.: The photosystem II light-harvesting protein Lhcb3 affects the macrostructure of photosystem II and the rate of state transitions in Arabidopsis. - Plant Cell 21: 3245-3256, 2009.
Go to original source... - De Souza A.P., Burgess S.J., Doran L. et al.: Soybean photosynthesis and crop yield are improved by accelerating recovery from photoprotection. - Science 377: 851-854, 2022.
Go to original source... - Derks A., Schaven K., Bruce D.: Diverse mechanisms for photoprotection in photosynthesis. Dynamic regulation of photosystem II excitation in response to rapid environmental change. - BBA-Bioenergetics 1847: 468-485, 2015.
Go to original source... - Dietz K.-J.: Efficient high light acclimation involves rapid processes at multiple mechanistic levels. - J. Exp. Bot. 66: 2401-2414, 2015.
Go to original source... - Dietz K.-J.: Thiol-based peroxidases and ascorbate peroxidases: Why plants rely on multiple peroxidase systems in the photosynthesizing chloroplast? - Mol. Cells 39: 20-25, 2016.
Go to original source... - Dobrikova A.G., Krasteva V., Apostolova E.L.: Damage and protection of the photosynthetic apparatus from UV-B radiation. I. Effect of ascorbate. - J. Plant Physiol. 170: 251-257, 2013.
Go to original source... - Edelman M., Mattoo A.K.: D1-protein dynamics in photosystem II: the lingering enigma. - Photosynth. Res. 98: 609-620, 2008.
Go to original source... - Fagerlund R.D., Forsman J.A., Biswas S. et al.: Stabilization of Photosystem II by the PsbT protein impacts photodamage, repair and biogenesis. - BBA-Bioenergetics 1861: 148234, 2020.
Go to original source... - Feilke K., Streb P., Cornic G. et al.: Effect of Chlamydomonas plastid terminal oxidase 1 expressed in tobacco on photosynthetic electron transfer. - Plant J. 85: 219-228, 2016.
Go to original source... - Fiorucci A.-S., Fankhauser C.: Plant strategies for enhancing access to sunlight. - Curr. Biol. 27: R931-R940, 2017.
Go to original source... - Friedland N., Negi S., Vinogradova-Shah T. et al.: Fine-tuning the photosynthetic light harvesting apparatus for improved photosynthetic efficiency and biomass yield. - Sci. Rep.-UK 9: 13028, 2019.
Go to original source... - Ghosh D., Mohapatra S., Dogra V.: Improving photosynthetic efficiency by modulating non-photochemical quenching. - Trends Plant Sci. 28: 264-266, 2023.
Go to original source... - Gollan P.J., Aro E.-M.: Photosynthetic signalling during high light stress and recovery: targets and dynamics. - Philos. T. Roy. Soc. B 375: 20190406, 2020.
Go to original source... - Gómez R., Carrillo N., Morelli M.P. et al.: Faster photosynthetic induction in tobacco by expressing cyanobacterial flavodiiron proteins in chloroplasts. - Photosynth. Res. 136: 129-138, 2018.
Go to original source... - González-Pérez S., Gutiérrez J., García-García F. et al.: Early transcriptional defense responses in Arabidopsis cell suspension culture under high-light conditions. - Plant Physiol. 156: 1439-1456, 2011.
Go to original source... - Gu J., Zhou Z., Li Z. et al.: Rice (Oryza sativa L.) with reduced chlorophyll content exhibit higher photosynthetic rate and efficiency, improved canopy light distribution, and greater yields than normally pigmented plants. - Field Crop. Res. 200: 58-70, 2017.
Go to original source... - Huang W., Sun H., Tan S.-L., Zhang S.-B.: The water-water cycle is not a major alternative sink in fluctuating light at chilling temperature. - Plant Sci. 305: 110828, 2021.
Go to original source... - Huang W., Yang Y.J., Hu H., Zhang S.-B.: Moderate photoinhibition of photosystem II protects Photosystem I from photodamage at chilling stress in tobacco leaves. - Front. Plant Sci. 7: 182, 2016.
Go to original source... - Huang W., Yang Y.-J., Zhang S.-B.: Specific roles of cyclic electron flow around photosystem I in photosynthetic regulation in immature and mature leaves. - J. Plant Physiol. 209: 76-83, 2017.
Go to original source... - Huang W., Yang Y.-J., Zhang S.-B.: The role of water-water cycle in regulating the redox state of photosystem I under fluctuating light. - BBA-Bioenergetics 1860: 383-390, 2019.
Go to original source... - Ilík P., Pavlovič A., Kouřil R. et al.: Alternative electron transport mediated by flavodiiron proteins is operational in organisms from cyanobacteria up to gymnosperms. - New Phytol. 214: 967-972, 2017.
Go to original source... - Ivanov A.G., Morgan R.M., Gray G.R. et al.: Temperature/light dependent development of selective resistance to photoinhibition of photosystem I. - FEBS Lett. 430: 288-292, 1998.
Go to original source... - Ivanov A.G., Sane P.V., Krol M. et al.: Acclimation to temperature and irradiance modulates PSII charge recombination. - FEBS Lett. 580: 2797-2802, 2006.
Go to original source... - Janečková H., Husičková A., Ferretti U. et al.: The interplay between cytokinins and light during senescence in detached Arabidopsis leaves. - Plant Cell Environ. 41: 1870-1885, 2018.
Go to original source... - Jegerschoeld C., Arellano J.B., Schroder W.P. et al.: Copper (II) inhibition of electron transport through photosystem II studied by EPR spectroscopy. - Biochemistry 34: 12747-12754, 1995.
Go to original source... - Jin H., Li M., Duan S. et al.: Optimization of light-harvesting pigment improves photosynthetic efficiency. - Plant Physiol. 172: 1720-1731, 2016.
Go to original source... - Josse E.-M., Alcaraz J.-P., Labouré A.-M., Kuntz M.: In vitro characterization of a plastid terminal oxidase (PTOX). - Eur. J. Biochem. 270: 3787-3794, 2003.
Go to original source... - Jung J., Kim H.-S.: The chromophores as endogenous sensitizers involved in the photogeneration of singlet oxygen in spinach thylakoids. - Photochem. Photobiol. 52: 1003-1009, 1990.
Go to original source... - Kataria S., Jajoo A., Guruprasad K.N.: Impact of increasing ultraviolet-B (UV-B) radiation on photosynthetic processes. -J. Photoch. Photobio. B 137: 55-66, 2014.
Go to original source... - Kato Y., Ozawa S., Takahashi Y., Sakamoto W.: D1 fragmentation in photosystem II repair caused by photo-damage of a two-step model. - Photosynth. Res. 126: 409-416, 2015.
Go to original source... - Kirst H., Gabilly S.T., Niyogi K.K. et al.: Photosynthetic antenna engineering to improve crop yields. - Planta 245: 1009-1020, 2017.
Go to original source... - Kono M., Noguchi K., Terashima I.: Roles of the cyclic electron flow around PSI (CEF-PSI) and O2-dependent alternative pathways in regulation of the photosynthetic electron flow in short-term fluctuating light in Arabidopsis thaliana. - Plant Cell Physiol. 55: 990-1004, 2014.
Go to original source... - Kozaki A., Takeba G.: Photorespiration protects C3 plants from photooxidation. - Nature 384: 557-560, 1996.
Go to original source... - Kozuleva M.A., Ivanov B.N.: Evaluation of the participation of ferredoxin in oxygen reduction in the photosynthetic electron transport chain of isolated pea thylakoids. - Photosynth. Res. 105: 51-61, 2010.
Go to original source... - Kozuleva M.A., Ivanov B.N., Vetoshkina D.V., Borisova-Mubarakshina M.M.: Minimizing an electron flow to molecular oxygen in photosynthetic electron transfer chain: an evolutionary view. - Front. Plant Sci 11: 211, 2020.
Go to original source... - Kozuleva M.A., Petrova A.A., Mamedov M.D. et al.: O2 reduction by photosystem I involves phylloquinone under steady-state illumination. - FEBS Lett. 588: 4364-4368, 2014.
Go to original source... - Krieger A., Weis E.: The role of calcium in the pH-dependent control of Photosystem II. - Photosynth. Res. 37: 117-130, 1993.
Go to original source... - Kromdijk J., Głowacka K., Leonelli L. et al.: Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. - Science 354: 857-861, 2016.
Go to original source... - Kudoh H., Sonoike K.: Irreversible damage to photosystem I by chilling in the light: cause of the degradation of chlorophyll after returning to normal growth temperature. - Planta 215: 541-548, 2002.
Go to original source... - Külheim C., Ågren, J., Jansson S.: Rapid regulation of light harvesting and plant fitness in the field. - Science 297: 91-93, 2002.
Go to original source... - Larkum A.W.D., Karge M., Reifarth F. et al.: Effect of monochromatic UV-B radiation on electron transfer reactions of Photosystem II. - Photosynth. Res. 68: 49-60, 2001.
Go to original source... - Laureau C., de Paepe R., Latouche G. et al.: Plastid terminal oxidase (PTOX) has the potential to act as a safety valve for excess excitation energy in the alpine plant species Ranunculus glacialis L. - Plant Cell Environ. 36: 1296-1310, 2013.
Go to original source... - Li L., Aro E.-M., Millar A.H.: Mechanisms of photodamage and protein turnover in photoinhibition. - Trends Plant Sci. 23: 667-676, 2018.
Go to original source... - Li X.-P., Björkman O., Shih C. et al.: A pigment-binding protein essential for regulation of photosynthetic light harvesting. - Nature 403: 391-395, 2000.
Go to original source... - Li X.-P., Müller-Moulé P., Gilmore A.M., Niyogi K.K.: PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition. - PNAS 99: 15222-15227, 2002.
Go to original source... - Lima-Melo Y., Alencar V.T.C.B., Lobo A.K.M. et al.: Photoinhibition of photosystem I provides oxidative protection during imbalanced photosynthetic electron transport in Arabidopsis thaliana. - Front. Plant Sci. 10: 916, 2019.
Go to original source... - López-Calcagno P.E., Brown K.L., Simkin A.J. et al.: Stimulating photosynthetic processes increases productivity and water-use efficiency in the field. - Nat. Plants 6: 1054-1063, 2020.
Go to original source... - Lu Y., Hall D.A., Last R.L.: A small zinc finger thylakoid protein plays a role in maintenance of photosystem II in Arabidopsis thaliana. - Plant Cell 23: 1861-1875, 2011.
Go to original source... - Malnoë A., Schultink A., Shahrasbi S. et al.: The plastid lipocalin LCNP is required for sustained photoprotective energy dissipation in Arabidopsis. - Plant Cell 30: 196-208, 2018.
- Mekala N.R., Suorsa M., Rantala M. et al.: 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, 2015.
Go to original source... - Merilo E., Jalakas P., Kollist H., Brosché M.: The role of ABA recycling and transporter proteins in rapid stomatal responses to reduced air humidity, elevated CO2, and exogenous ABA. - Mol. Plant 8: 657-659, 2015.
Go to original source... - Messinger J., Renger G.: Photosynthetic water splitting. - In: Renger G. (ed.): Primary Processes of Photosynthesis: Basic Principles and Apparatus. Part II. Pp. 295-353. Royal Society Chemistry, Cambridge 2008.
- Minagawa J.: State transitions - the molecular remodeling of photosynthetic supercomplexes that controls energy flow in the chloroplast. - BBA-Bioenergetics 1807: 897-905, 2011.
Go to original source... - Morales A., Kaiser E.: Photosynthetic acclimation to fluctuating irradiance in plants. - Front. Plant Sci. 11: 268, 2020.
Go to original source... - Muh F., Zouni A.: Light-induced water oxidation in photosystem II. - Front. Biosci.-Landmark 16: 3072-3132, 2011.
Go to original source... - Mullineaux C.W.: Photosynthesis: Rewiring an angiosperm. - Nat. Plants 2: 16018, 2016.
Go to original source... - Mulo P., Sakurai I., Aro E.-M.: Strategies for psbA gene expression in cyanobacteria, green algae and higher plants: from transcription to PSII repair. - BBA-Bioenergetics 1817: 247-257, 2012.
Go to original source... - Munekage Y., Hojo M., Meurer J. et al.: PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. - Cell 110: 361-371, 2002.
Go to original source... - Murata N., Allakhverdiev S.I., Nishiyama Y.: The mechanism of photoinhibition in vivo: re-evaluation of the roles of catalase, α-tocopherol, non-photochemical quenching, and electron transport. - BBA-Bioenergetics 1817: 1127-1133, 2012.
Go to original source... - Murata N., Nishiyama Y.: ATP is a driving force in the repair of photosystem II during photoinhibition. - Plant Cell Environ. 41: 285-299, 2018.
Go to original source... - Murata N., Takahashi S., Nishiyama Y., Allakhverdiev S.I.: Photoinhibition of photosystem II under environmental stress. - BBA-Bioenergetics 1767: 414-421, 2007.
Go to original source... - Naranjo B., Penzler J.-F., Rühle T., Leister D.: NTRC effects on non-photochemical quenching depends on PGR5. - Antioxidants 10: 900, 2021.
Go to original source... - Nath K., Jajoo A., Poudyal R.S. et al.: Towards a critical understanding of the photosystem II repair mechanism and its regulation during stress conditions. - FEBS Lett. 587: 3372-3381, 2013.
Go to original source... - Nawrocki W.J., Bailleul B., Picot D. et al.: The mechanism of cyclic electron flow. - BBA-Bioenergetics 1860: 433-438, 2019.
Go to original source... - Nelson C.J., Alexova R., Jacoby R.P., Millar A.H.: Proteins with high turnover rate in barley leaves estimated by proteome analysis combined with in planta isotope labeling. - Plant Physiol. 166: 91-108, 2014.
Go to original source... - Nicol L., Croce R.: The PsbS protein and low pH are necessary and sufficient to induce quenching in the light-harvesting complex of plants LHCII. - Sci. Rep.-UK 11: 7415, 2021.
Go to original source... - Nicol L., Nawrocki W.J., Croce R.: Disentangling the sites of non-photochemical quenching in vascular plants. - Nat. Plants 5: 1177-1183, 2019.
Go to original source... - Nosalewicz A., Okoń K., Skorupka M.: Non-photochemical quenching under drought and fluctuating light. - Int. J. Mol. Sci. 23: 5182, 2022.
Go to original source... - Pfannschmidt T., Nilsson A., Allen J.F.: Photosynthetic control of chloroplast gene expression. - Nature 397: 625-628, 1999.
Go to original source... - Pietrzykowska M., Suorsa M., Semchonok D.A. et al.: The light-harvesting chlorophyll a/b binding proteins Lhcb1 and Lhcb2 play complementary roles during state transitions in Arabidopsis. - Plant Cell 26: 3646-3660, 2014.
Go to original source... - Powles S.B.: Photoinhibition of photosynthesis induced by visible light. - Annu. Rev. Plant Physiol. 35: 15-44, 1984.
Go to original source... - Rantala M., Tikkanen M., Aro E.-M.: Proteomic characterization of hierarchical megacomplex formation in Arabidopsis thylakoid membrane. - Plant J. 92: 951-962, 2017.
Go to original source... - Raven J.A.: Speedy small stomata? - J. Exp. Bot. 65: 1415-1424, 2014.
Go to original source... - Ribas-Carbo M., Berry J.A., Yakir D. et al.: Electron partitioning between the cytochrome and alternative pathways in plant mitochondria. - Plant Physiol. 109: 829-837, 1995.
Go to original source... - Roach T., Krieger-Liszkay A.: The role of the PsbS protein in the protection of photosystems I and II against high light in Arabidopsis thaliana. - BBA-Bioenergetics 1817: 2158-2165, 2012.
Go to original source... - Rochaix J.D.: Regulation and dynamics of the light-harvesting system. - Annu. Rev. Plant Biol. 65: 287-309, 2014.
Go to original source... - Rog I., Chaturvedi A.K., Tiwari V., Danon A.: Low light-regulated intramolecular disulfide fine-tunes the role of PTOX in Arabidopsis. - Plant J. 109: 585-597, 2022.
Go to original source... - Rott M., Martins N.F., Thiele W. et al.: ATP synthase repression in tobacco restricts photosynthetic electron transport, CO2 assimilation, and plant growth by overacidification of the thylakoid lumen. - Plant Cell 23: 304-321, 2011.
Go to original source... - Ruban A.V.: Nonphotochemical chlorophyll fluorescence quenching: mechanism and effectiveness in protecting plants from photodamage. - Plant Physiol. 170: 1903-1916, 2016.
Go to original source... - Ruban A.V., Johnson M.P., Duffy C.D.P.: The photoprotective molecular switch in the photosystem II antenna. - BBA-Bioenergetics 1817: 167-181, 2012.
Go to original source... - Ruban A.V., Wilson S.: The mechanism of non-photochemical quenching in plants: localization and driving forces. - Plant Cell Physiol. 62: 1063-1072, 2021.
Go to original source... - Rutherford A.W., Osyczka A., Rappaport F.: 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, 2012.
Go to original source... - Sarvikas P., Hakala M., Pätsikkä E. et al.: Action spectrum of photoinhibition in leaves of wild type and npq1-2 and npq4-1 mutants of Arabidopsis thaliana. - Plant Cell Physiol. 47: 391-400, 2006.
Go to original source... - Schuster M., Gao Y., Schöttler M.A. et al.: Limited responsiveness of chloroplast gene expression during acclimation to high light in tobacco. - Plant Physiol. 182: 424-435, 2020.
Go to original source... - Shahinnia F., Tula S., Hensel G. et al.: Plastid-targeted cyanobacterial flavodiiron proteins maintain carbohydrate turnover and enhance drought stress tolerance in barley. - Front. Plant Sci. 11: 613731, 2021.
Go to original source... - Shin M., Tagawa K., Arnon D.: Crystallization of Ferredoxin-Tpn reductase and its role in the photosynthetic apparatus of chloroplasts. - Biochem. Z. 338: 84-93, 1963.
- Shumbe L., Chevalier A., Legeret B. et al.: Singlet oxygen-induced cell death in Arabidopsis under high-light stress is controlled by OXI1 kinase. - Plant Physiol. 170: 1757-1771, 2016.
Go to original source... - Simkin A.J., Kapoor L., Doss G.P.C. et al.: The role of photosynthesis related pigments in light harvesting, photoprotection and enhancement of photosynthetic yield in planta. - Photosynth. Res. 152: 23-42, 2022.
Go to original source... - Slavov C., Schrameyer V., Reus M. et al.: "Super-quenching" state protects Symbiodinium from thermal stress - implications for coral bleaching. - BBA-Bioenergetics 1857: 840-847, 2016.
Go to original source... - Song Y., Feng L., Alyafei M.A.M. et al.: Function of chloroplasts in plant stress responses. - Int. J. Mol. Sci. 22: 13464, 2021.
Go to original source... - Sonoike K.: Photoinhibition of photosystem I. - Physiol. Plantarum 142: 56-64, 2011.
Go to original source... - Sonoike K., Terashima I., Iwaki M., Itoh S.: Destruction of photosystem I iron-sulfur centers in leaves of Cucumis sativus L. by weak illumination at chilling temperatures. - FEBS Lett. 362: 235-238, 1995.
Go to original source... - Spetea C., Rintamäki E., Schoefs B.: Changing the light environment: chloroplast signalling and response mechanisms. - Philos. T. Roy. Soc. B 369: 20130220, 2014.
Go to original source... - Strodtkötter I., Padmasree K., Dinakar C. et al.: Induction of the AOX1D isoform of alternative oxidase in A. thaliana T-DNA insertion lines lacking isoform AOX1A is insufficient to optimize photosynthesis when treated with antimycin A. - Mol. Plant 2: 284-297, 2009.
Go to original source... - Suh H.J., Kim C.S., Jung J.: Cytochrome b6/f complex as an indigenous photodynamic generator of singlet oxygen in thylakoid membranes. - Photochem. Photobiol. 71: 103-109, 2000.
Go to original source... - Sun H., Shi Q., Zhang S.B., Huang W.: Coordination of cyclic electron flow and water-water cycle facilitates photoprotection under fluctuating light and temperature stress in the epiphytic orchid Dendrobium officinale. - Plants-Basel 10: 606, 2021.
Go to original source... - Sun H., Yang Y.J., Huang W.: The water-water cycle is more effective in regulating redox state of photosystem I under fluctuating light than cyclic electron transport. - BBA-Bioenergetics 1861: 148235, 2020.
Go to original source... - Suorsa M., Järvi S., Grieco M. et al.: PROTON GRADIENT REGULATION5 is essential for proper acclimation of Arabidopsis photosystem I to naturally and artificially fluctuating light conditions. - Plant Cell 24: 2934-2948, 2012.
Go to original source... - Suorsa M., Rantala M., Danielsson R. et al.: Dark-adapted spinach thylakoid protein heterogeneity offers insights into the photosystem II repair cycle. - BBA-Bioenergetics 1837: 1463-1471, 2014.
Go to original source... - Suzuki N., Miller G., Salazar C. et al.: Temporal-spatial interaction between reactive oxygen species and abscisic acid regulates rapid systemic acclimation in plants. - Plant Cell 25: 3553-3569, 2013.
Go to original source... - Szilárd A., Sass L., Deák Z., Vass I.: The sensitivity of Photosystem II to damage by UV-B radiation depends on the oxidation state of the water-splitting complex. - BBA-Bioenergetics 1767: 876-882, 2007.
Go to original source... - Takagi D., Takumi S., Hashiguchi M. et al.: Superoxide and singlet oxygen produced within the thylakoid membranes both cause photosystem I photoinhibition. - Plant Physiol. 171: 1626-1634, 2016.
Go to original source... - Takahashi S., Bauwe H., Badger M.: Impairment of the photorespiratory pathway accelerates photoinhibition of photosystem II by suppression of repair but not acceleration of damage processes in Arabidopsis. - Plant Physiol. 144: 487-494, 2007.
Go to original source... - Telfer W.H., Kunkel J.G.: The function and evolution of insect storage hexamers. - Annu. Rev. Entomol. 36: 205-228, 1991.
Go to original source... - Tian Y.-N., Zhong R.-H., Wei J.-B. et al.: Arabidopsis CHLOROPHYLLASE 1 protects young leaves from long-term photodamage by facilitating FtsH-mediated D1 degradation in photosystem II repair. - Mol. Plant 14: 1149-1167, 2021.
Go to original source... - Tikkanen M., Mekala N.R., Aro E.-M.: Photosystem II photoinhibition-repair cycle protects Photosystem I from irreversible damage. - BBA-Bioenergetics 1837: 210-215, 2014.
Go to original source... - Tikkanen M., Rantala S., Aro E.-M.: Electron flow from PSII to PSI under high light is controlled by PGR5 but not by PSBS. -Front. Plant Sci. 6: 521, 2015.
Go to original source... - Townsend A.J., Ware M.A., Ruban A.V.: Dynamic interplay between photodamage and photoprotection in photosystem II. - Plant Cell Environ. 41: 1098-1112, 2018.
Go to original source... - Tula S., Shahinnia F., Melzer M. et al.: Providing an additional electron sink by the introduction of cyanobacterial flavodiirons enhances growth of A. thaliana under various light intensities. - Front. Plant Sci. 11: 902, 2020.
Go to original source... - Tyystjärvi E., Aro E.-M.: The rate constant of photoinhibition, measured in lincomycin-treated leaves, is directly proportional to light intensity. - PNAS 93: 2213-2218, 1996.
Go to original source... - Vass I.: Molecular mechanisms of photodamage in the Photosystem II complex. - BBA-Bioenergetics 1817: 209-217, 2012.
Go to original source... - Vass I., Aro E.-M.: Photoinhibition of photosynthetic electron transport. - In: Renger G. (ed.): Primary Processes of Photosynthesis: Principles and Apparatus. Part 1. Pp. 393-425. RSC Publishing, 2008.
Go to original source... - Vass I., Kirilovsky D., Etienne A.-L.: UV-B radiation-induced donor- and acceptor-side modifications of photosystem II in the cyanobacterium Synechocystis sp. PCC 6803. - Biochemistry 38: 12786-12794, 1999.
Go to original source... - Vass I., Styring S., Hundal T. et al.: Reversible and irreversible intermediates during photoinhibition of photosystem II: Stable reduced QA species promote chlorophyll triplet formation. - PNAS 89: 1408-1412, 1992.
Go to original source... - Vass I., Szilárd A., Sicora C.: Adverse effects of UV-B light on the structure and function of the photosynthetic apparatus. -In: Pessarakli M. (ed.): Handbook of Photosynthesis. 2nd Edition. Pp. 827-843. CRC Press, Boca Raton 2005.
- Vicino P., Carrillo J., Gómez R. et al.: Expression of flavodiiron proteins Flv2-Flv4 in chloroplasts of Arabidopsis and tobacco plants provides multiple stress tolerance. - Int. J. Mol. Sci. 22: 1178, 2021.
Go to original source... - Vishwakarma A., Tetali S.D., Selinski J. et al.: Importance of the alternative oxidase (AOX) pathway in regulating cellular redox and ROS homeostasis to optimize photosynthesis during restriction of the cytochrome oxidase pathway in Arabidopsis thaliana. - Ann. Bot.-London 116: 555-569, 2015.
Go to original source... - Wada S., Yamamoto H., Suzuki Y. et al.: Flavodiiron protein substitutes for cyclic electron flow without competing CO2 assimilation in rice. - Plant Physiol. 176: 1509-1518, 2018.
Go to original source... - Walker J.E.: The ATP synthase: the understood, the uncertain and the unknown. - Biochem. Soc. T. 41: 1-16, 2013.
Go to original source... - Wang F., Sun H., Rong L. et al.: Genotypic-dependent alternation in D1 protein turnover and PSII repair cycle in psf mutant rice (Oryza sativa L.), as well as its relation to light-induced leaf senescence. - Plant Growth Regul. 95: 121-136, 2021.
Go to original source... - Wang L., Kim C., Xu X. et al.: Singlet oxygen- and EXECUTER1-mediated signaling is initiated in grana margins and depends on the protease FtsH2. - PNAS 113: E3792-E3800, 2016.
Go to original source... - Watson S.J., Sowden R.G., Jarvis P.: Abiotic stress-induced chloroplast proteome remodelling: a mechanistic overview. - J. Exp. Bot. 69: 2773-2781, 2018.
Go to original source... - Wei Z., Cady C.W., Brudvig G.W., Hou H.J.M.: Photodamage of a Mn (III/IV)-oxo mixed-valence compound and photosystem II: evidence that a high-valent manganese species is responsible for UV-induced photodamage of the oxygen-evolving complex in photosystem II. - J. Photoch. Photobio. B 104: 118-125, 2011.
Go to original source... - Welc R., Luchowski R., Kluczyk D. et al.: Mechanisms shaping the synergism of zeaxanthin and PsbS in photoprotective energy dissipation in the photosynthetic apparatus of plants. -Plant J. 107: 418-433, 2021.
Go to original source... - Werner C., Correia O., Beyschlag W.: Characteristic patterns of chronic and dynamic photoinhibition of different functional groups in a Mediterranean ecosystem. - Funct. Plant Biol. 29: 999-1011, 2002.
Go to original source... - Woodson J.D.: Chloroplast quality control - balancing energy production and stress. - New Phytol. 212: 36-41, 2016.
Go to original source... - Wu J., Rong L., Lin W. et al.: Functional redox links between lumen thiol oxidoreductase1 and serine/threonine-protein kinase STN7. - Plant Physiol. 186: 964-976, 2021.
Go to original source... - Xiao Y., Savchenko T., Baidoo E.E.K. et al.: Retrograde signaling by the plastidial metabolite MEcPP regulates expression of nuclear stress-response genes. - Cell 149: 1525-1535, 2012.
Go to original source... - Yadav S.K., Khatri K., Rathore M.S., Jha B.: Introgression of Ufcyt c6, a thylakoid lumen protein from a green seaweed Ulva fasciata Delile enhanced photosynthesis and growth in tobacco. - Mol. Biol. Rep. 45: 1745-1758, 2018.
Go to original source... - Yokono M.A., Takabayashi S., Akimoto S., Tanaka A.: A megacomplex composed of both photosystem reaction centres in higher plants. - Nat. Commun. 6: 6675, 2015.
Go to original source... - Zavafer A., Chow W.S., Cheah M.H.: The action spectrum of Photosystem II photoinactivation in visible light. - J. Photoch. Photobio. B 152: 247-260, 2015.
Go to original source... - Zavafer A., Mancilla C.: Concepts of photochemical damage of Photosystem II and the role of excessive excitation. - J. Photoch. Photobio. C 47: 100421, 2021.
Go to original source... - Zhang D.W., Xu F., Zhang Z.W. et al.: Effects of light on cyanide-resistant respiration and alternative oxidase function in Arabidopsis seedlings. - Plant Cell Environ. 33: 2121-2131, 2010.
Go to original source... - Zhang M., Zeng Y., Peng R. et al.: N6-methyladenosine RNA modification regulates photosynthesis during photodamage in plants. - Nat. Commun. 13: 7441, 2022.
Go to original source... - Zulfugarov I.S., Tovuu A., Eu Y.-J. et al.: Production of superoxide from Photosystem II in a rice (Oryza sativa L.) mutant lacking PsbS. - BMC Plant Biol. 14: 242, 2014.
Go to original source...




