Mixed population hypothesis of the active and inactive PSII complexes opens a new door for photoinhibition and fluorescence studies: an ecophysiological perspective
Masaru Kono
A * , Kazunori Miyata A , Sae Matsuzawa A , Takaya Noguchi A , Riichi Oguchi A , Yoshihiro Suzuki B and Ichiro Terashima A
+ Author Affiliations
- Author Affiliations
A Department of Biological Sciences, Graduate School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan.
B Department of Biological Sciences, Faculty of Science, Kanagawa University, 2946 Tsuchiya, Hiratsuka-City, Kanagawa 259-1293, Japan.
Functional Plant Biology 49(10) 917-925 https://doi.org/10.1071/FP21355
Submitted: 27 July 2021 Accepted: 20 June 2022 Published: 13 July 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
The current hypotheses for the mechanisms of photosystem II (PSII) photodamage in vivo remain split on the primary damage site. However, most researchers have considered that PSII is inhibited by a sole mechanism and that the photoinhibited PSII consists of one population. In this perspective, we propose ‘the mixed population hypothesis’, in which there are four PSII populations: PSII with active/inactive Mn4CaO5 oxygen-evolving complex respectively with functional/damaged primary quinone (QA) reduction activity. This hypothesis provides a new insight into not only the PSII photoinhibition/photoprotection studies but also the repair process. We discuss our new data implying that the repair rate differs in the respective PSII populations.
Keywords: Mn4CaO5 oxygen-evolving complex, photodamage, photoinhibition, photoprotection, photosystem II, photon flux density, repair, the mixed population hypothesis.
References
Aro E-M, Virgin I, Andersson B (1993) Photoinhibition of Photosystem-II. Inactivation, protein damage and turnover. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1143, 113–134.| Photoinhibition of Photosystem-II. Inactivation, protein damage and turnover.Crossref | GoogleScholarGoogle Scholar |
Bailey S, Thompson E, Nixon PJ, Horton P, Mullineaux CW, Robinson C, Mann NH (2002) A critical role for the Var2 FtsH homologue of Arabidopsis thaliana in the photosystem II repair cycle in vivo. Journal of Biological Chemistry 277, 2006–2011.
| A critical role for the Var2 FtsH homologue of Arabidopsis thaliana in the photosystem II repair cycle in vivo.Crossref | GoogleScholarGoogle Scholar | 11717304PubMed |
Bao H, Burnap RL (2016) Photoactivation: the light-driven assembly of the water oxidation complex of photosystem II. Frontiers in Plant Science 7, 578
| Photoactivation: the light-driven assembly of the water oxidation complex of photosystem II.Crossref | GoogleScholarGoogle Scholar | 27200051PubMed |
Bergantino E, Brunetta A, Touloupakis E, Segalla A, Szabò I, Giacometti GM (2003) Role of the PSII-H subunit in photoprotection: novel aspects of D1 turnover in Synechocystis 6803. Journal of Biological Chemistry 278, 41820–41829.
| Role of the PSII-H subunit in photoprotection: novel aspects of D1 turnover in Synechocystis 6803.Crossref | GoogleScholarGoogle Scholar | 12909614PubMed |
Bodini ME, Willis LA, Riechel TL, Sawyer DT (1976) Electrochemical and spectroscopic studies of manganese(II), -(III), and -(IV) gluconate complexes. 1. Formulas and oxidation-reduction stoichiometry. Inorganic Chemistry 15, 1538–1543.
| Electrochemical and spectroscopic studies of manganese(II), -(III), and -(IV) gluconate complexes. 1. Formulas and oxidation-reduction stoichiometry.Crossref | GoogleScholarGoogle Scholar |
Demmig-Adams B, Adams WW, Barker DH, Logan BA, Bowling DR, Verhoeven AS (1996) Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation. Physiologia Plantarum 98, 253–264.
| Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation.Crossref | GoogleScholarGoogle Scholar |
Enami I, Kitamura M, Tomo T, Isokawa Y, Ohta H, Katoh S (1994) Is the primary cause of thermal inactivation of oxygen evolution in spinach PS-II membranes release of the extrinsic 33 kDa protein or of Mn. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1186, 52–58.
| Is the primary cause of thermal inactivation of oxygen evolution in spinach PS-II membranes release of the extrinsic 33 kDa protein or of Mn.Crossref | GoogleScholarGoogle Scholar |
Gururani MA, Venkatesh J, Tran LSP (2015) Regulation of photosynthesis during abiotic stress-induced photoinhibition. Molecular Plant 8, 1304–1320.
| Regulation of photosynthesis during abiotic stress-induced photoinhibition.Crossref | GoogleScholarGoogle Scholar | 25997389PubMed |
Hakala M, Tuominen I, Keränen M, Tyystjärvi T, Tyystjärvi E (2005) Evidence for the role of the oxygen-evolving manganese complex in photoinhibition of Photosystem II. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1706, 68–80.
| Evidence for the role of the oxygen-evolving manganese complex in photoinhibition of Photosystem II.Crossref | GoogleScholarGoogle Scholar |
He J, Chow WS (2003) The rate coefficient of repair of photosystem II after photoinactivation. Physiologia Plantarum 118, 297–304.
| The rate coefficient of repair of photosystem II after photoinactivation.Crossref | GoogleScholarGoogle Scholar |
Higuchi M, Noguchi T, Sonoike K (2003) Over-reduced states of the Mn-cluster in cucumber leaves induced by dark-chilling treatment. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1604, 151–158.
| Over-reduced states of the Mn-cluster in cucumber leaves induced by dark-chilling treatment.Crossref | GoogleScholarGoogle Scholar |
Hikosaka K, Kato MC, Hirose T (2004) Photosynthetic rates and partitioning of absorbed light energy in photoinhibited leaves. Physiologia Plantarum 121, 699–708.
| Photosynthetic rates and partitioning of absorbed light energy in photoinhibited leaves.Crossref | GoogleScholarGoogle Scholar |
Jansen MAK, Greenberg BM, Edelman M, Mattoo AK, Gaba V (1996) Accelerated degradation of the D2 protein of photosystem II under ultraviolet radiation. Photochemistry and Photobiology 63, 814–817.
| Accelerated degradation of the D2 protein of photosystem II under ultraviolet radiation.Crossref | GoogleScholarGoogle Scholar |
Johnson GN, Rutherford AW, Krieger A (1995) A change in the midpoint potential of the quinone QA in Photosystem II associated with photoactivation of oxygen evolution. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1229, 202–207.
| A change in the midpoint potential of the quinone QA in Photosystem II associated with photoactivation of oxygen evolution.Crossref | GoogleScholarGoogle Scholar |
Kato Y, Sakamoto W (2009) Protein quality control in chloroplasts: a current model of D1 protein degradation in the photosystem II repair cycle. Journal of Biochemistry 146, 463–469.
| Protein quality control in chloroplasts: a current model of D1 protein degradation in the photosystem II repair cycle.Crossref | GoogleScholarGoogle Scholar | 19451147PubMed |
Kato MC, Hikosaka K, Hirose T (2002) Photoinactivation and recovery of photosystem II in Chenopodium album leaves grown at different levels of irradiance and nitrogen availability. Functional Plant Biology 29, 787–795.
| Photoinactivation and recovery of photosystem II in Chenopodium album leaves grown at different levels of irradiance and nitrogen availability.Crossref | GoogleScholarGoogle Scholar | 32689526PubMed |
Kato Y, Sun X, Zhang L, Sakamoto W (2012) Cooperative D1 degradation in the photosystem II repair mediated by chloroplastic proteases in Arabidopsis. Plant Physiology 159, 1428–1439.
| Cooperative D1 degradation in the photosystem II repair mediated by chloroplastic proteases in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 22698923PubMed |
Kato Y, Ohira A, Nagao R, Noguchi T (2019) Does the water-oxidizing Mn4CaO5 cluster regulate the redox potential of the primary quinone electron acceptor QA in photosystem II? A study by Fourier transform infrared spectroelectrochemistry. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1860, 148082
| Does the water-oxidizing Mn4CaO5 cluster regulate the redox potential of the primary quinone electron acceptor QA in photosystem II? A study by Fourier transform infrared spectroelectrochemistry.Crossref | GoogleScholarGoogle Scholar |
Klughammer C, Schreiber U (2008) Complementary PS II quantum yields calculated from simple fluorescence parameters measured by PAM fluorometry and the saturation pulse method. PAM Application Notes 1, 27–35.
Kobayashi K, Endo K, Wada H (2016) Multiple impacts of loss of plastidic phosphatidylglycerol biosynthesis on photosynthesis during seedling growth of Arabidopsis. Frontiers in Plant Science 7, 336
| Multiple impacts of loss of plastidic phosphatidylglycerol biosynthesis on photosynthesis during seedling growth of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 27047516PubMed |
Kono M, Matsuzawa S, Noguchi T, Miyata K, Oguchi R, Terashima I (2022) A new method for separate evaluation of photosystem II with inactive oxygen evolving complex and active D1 by the pulse-amplitude modulated chlorophyll fluorometry. Functional Plant Biology 49, 542–553.
| A new method for separate evaluation of photosystem II with inactive oxygen evolving complex and active D1 by the pulse-amplitude modulated chlorophyll fluorometry.Crossref | GoogleScholarGoogle Scholar | 34511179PubMed |
Krieger A, Weis E (1993) The role of calcium in the pH-dependent control of Photosystem II. Photosynthesis Research 37, 117–130.
| The role of calcium in the pH-dependent control of Photosystem II.Crossref | GoogleScholarGoogle Scholar | 24317708PubMed |
Lavergne J, Briantais JM (1996) Photosystem II heterogeneity. In ‘Oxygenic photosynthesis: the light reactions.’ (Eds DR Ort, CF Yocum, IF Heichel) pp. 265–287. (Springer: Dordrecht)
Matsubara S, Chow WS (2004) Populations of photoinactivated photosystem II reaction centers characterized by chlorophyll a fluorescence lifetime in vivo. Proceedings of the National Academy of Sciences of the United States of America 101, 18234–18239.
| Crossref |
Miyata K, Noguchi K, Terashima I (2012) Cost and benefit of the repair of photodamaged photosystem II in spinach leaves: roles of acclimation to growth light. Photosynthesis Research 113, 165–180.
| Cost and benefit of the repair of photodamaged photosystem II in spinach leaves: roles of acclimation to growth light.Crossref | GoogleScholarGoogle Scholar | 22797856PubMed |
Miyata K, Ikeda H, Nakaji M, Kanel DR, Terashima I (2015) Rate constants of PSII photoinhibition and its repair, and PSII fluorescence parameters in field plants in relation to their growth light environments. Plant and Cell Physiology 56, 1841–1854.
| Rate constants of PSII photoinhibition and its repair, and PSII fluorescence parameters in field plants in relation to their growth light environments.Crossref | GoogleScholarGoogle Scholar | 26203120PubMed |
Murata N, Nishiyama Y (2018) ATP is a driving force in the repair of photosystem II during photoinhibition. Plant, Cell & Environment 41, 285–299.
| ATP is a driving force in the repair of photosystem II during photoinhibition.Crossref | GoogleScholarGoogle Scholar |
Nash D, Miyao M, Murata N (1985) Heat inactivation of oxygen evolution in Photosystem II particles and its acceleration by chloride depletion and exogenous manganese. Biochimica et Biophysica Acta (BBA) – Bioenergetics 807, 127–133.
| Heat inactivation of oxygen evolution in Photosystem II particles and its acceleration by chloride depletion and exogenous manganese.Crossref | GoogleScholarGoogle Scholar |
Nawrocki WJ, Liu X, Raber B, Hu C, de Vitry C, Bennett DIG, Croce R (2021) Molecular origins of induction and loss of photoinhibition-related energy dissipation qI. Science Advances 7, eabj0055
| Molecular origins of induction and loss of photoinhibition-related energy dissipation qI.Crossref | GoogleScholarGoogle Scholar | 34936440PubMed |
Oguchi R, Terashima I, Chow WS (2009) The involvement of dual mechanisms of photoinactivation of Photosystem II in Capsicum annuum L. plants. Plant and Cell Physiology 50, 1815–1825.
| The involvement of dual mechanisms of photoinactivation of Photosystem II in Capsicum annuum L. plants.Crossref | GoogleScholarGoogle Scholar | 19737797PubMed |
Ohnishi N, Allakhverdiev SI, Takahashi S, Higashi S, Watanabe M, Nishiyama Y, Murata N (2005) Two-step mechanism of photodamage to photosystem II: Step 1 occurs at the oxygen-evolving complex and step 2 occurs at the photochemical reaction center. Biochemistry 44, 8494–8499.
| Two-step mechanism of photodamage to photosystem II: Step 1 occurs at the oxygen-evolving complex and step 2 occurs at the photochemical reaction center.Crossref | GoogleScholarGoogle Scholar | 15938639PubMed |
Ono T (2001) Metallo-radical hypothesis for photoassembly of (Mn)(4)-cluster of photosynthetic oxygen evolving complex. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1503, 40–51.
| Metallo-radical hypothesis for photoassembly of (Mn)(4)-cluster of photosynthetic oxygen evolving complex.Crossref | GoogleScholarGoogle Scholar |
Ono T, Mino H (1999) Unique binding site for Mn2+ ion responsible for reducing an oxidized YZ tyrosine in manganese-depleted photosystem II membranes. Biochemistry 38, 8778–8785.
| Unique binding site for Mn2+ ion responsible for reducing an oxidized YZ tyrosine in manganese-depleted photosystem II membranes.Crossref | GoogleScholarGoogle Scholar | 10393553PubMed |
Radmer R, Cheniae GM (1971) Photoactivation of the manganese catalyst of O2 evolution II. A two-quantum mechanism. Biochimica et Biophysica Acta (BBA) – Bioenergetics 253, 182–186.
| Photoactivation of the manganese catalyst of O2 evolution II. A two-quantum mechanism.Crossref | GoogleScholarGoogle Scholar |
Renger G, Völker M, Eckert HJ, Fromme R, Hohm-veit S, Graber P (1989) On the mechanism of Photosystem-Ii deterioration by UV-B irradiation. Photochemistry and Photobiology 49, 97–105.
| On the mechanism of Photosystem-Ii deterioration by UV-B irradiation.Crossref | GoogleScholarGoogle Scholar |
Richter M, Goss R, Wagner B, Holzwarth AR (1999) Characterization of the fast and slow reversible components of non-photochemical quenching in isolated pea thylakoids by picosecond time-resolved chlorophyll fluorescence analysis. Biochemistry 38, 12718–12726.
| Characterization of the fast and slow reversible components of non-photochemical quenching in isolated pea thylakoids by picosecond time-resolved chlorophyll fluorescence analysis.Crossref | GoogleScholarGoogle Scholar | 10504242PubMed |
Sato A, Nakano Y, Nakamura S, Noguchi T (2021) Rapid-scan time-resolved ATR-FTIR study on the photoassembly of the water-oxidizing Mn4CaO5 cluster in Photosystem II. Journal of Physical Chemistry B 125, 4031–4045.
| Rapid-scan time-resolved ATR-FTIR study on the photoassembly of the water-oxidizing Mn4CaO5 cluster in Photosystem II.Crossref | GoogleScholarGoogle Scholar | 33861065PubMed |
Shen JR, Terashima I, Katoh S (1990) Cause for dark, chilling-induced inactivation of photosynthetic oxygen-evolving system in cucumber leaves. Plant Physiology 93, 1354–1357.
| Cause for dark, chilling-induced inactivation of photosynthetic oxygen-evolving system in cucumber leaves.Crossref | GoogleScholarGoogle Scholar | 16667624PubMed |
Sipka G, Magyar M, Mezzetti A, Akhtar P, Zhu QJ, Xiao YA, Han G, Santabarbara S, Shen J-R, Lambrev PH, Garab G (2021) Light-adapted charge-separated state of photosystem II: structural and functional dynamics of the closed reaction center. The Plant Cell 33, 1286–1302.
| Light-adapted charge-separated state of photosystem II: structural and functional dynamics of the closed reaction center.Crossref | GoogleScholarGoogle Scholar | 33793891PubMed |
Strasser RJ, Srivastava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. In ‘Probing photosynthesis: mechanisms, regulation and adaptation’. (Eds M Yunus, U Pathre, P Mohanty) pp. 445–483. (CRC Press)
Terashima I, Shen JR, Katoh S (1989) Chilling damage in cucumber (Cucumis sativus L.) thylakoids. In ‘Plant water relations and growth under stress’. (Eds M Tazawa, M Katsumi, Y Masuda, H Okamoto) pp. 470–472. (Yamada Science Foundation: Osaka and Myu K.K., Tokyo)
Terashima I, Kashino Y, Katoh S (1991) Exposure of leaves of Cucumis sativus L. to low-temperatures in the light causes uncoupling of thylakoids. 1. Studies with isolated thylakoids. Plant and Cell Physiology 32, 1267–1274.
Tóth SZ, Nagy V, Puthur JT, Kovacs L, Garab G (2011) The physiological role of ascorbate as photosystem II electron donor: protection against photoinactivation in heat-stressed leaves. Plant Physiology 156, 382–392.
| The physiological role of ascorbate as photosystem II electron donor: protection against photoinactivation in heat-stressed leaves.Crossref | GoogleScholarGoogle Scholar | 21357184PubMed |
Tyystjärvi E (2008) Photoinhibition of Photosystem II and photodamage of the oxygen evolving manganese cluster. Coordination Chemistry Reviews 252, 361–376.
| Photoinhibition of Photosystem II and photodamage of the oxygen evolving manganese cluster.Crossref | GoogleScholarGoogle Scholar |
Tyystjärvi E (2013) Photoinhibition of Photosystem II. International Review of Cell and Molecular Biology 300, 243–303.
| Photoinhibition of Photosystem II.Crossref | GoogleScholarGoogle Scholar | 23273864PubMed |
Vass I (2011) Role of charge recombination processes in photodamage and photoprotection of the photosystem II complex. Physiologia Plantarum 142, 6–16.
| Role of charge recombination processes in photodamage and photoprotection of the photosystem II complex.Crossref | GoogleScholarGoogle Scholar | 21288250PubMed |
Vass I, Gatzen G, Holzwarth AR (1993) Picosecond time-resolved fluorescence studies on photoinhibition and double reduction of QA in Photosystem II. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1183, 388–396.
| Picosecond time-resolved fluorescence studies on photoinhibition and double reduction of QA in Photosystem II.Crossref | GoogleScholarGoogle Scholar |
Vinyard DJ, Badshah SL, Riggio MR, Kaur D, Fanguy AR, Gunner MR (2019) Photosystem II oxygen-evolving complex photoassembly displays an inverse H/D solvent isotope effect under chloride-limiting conditions. Proceedings of the National Academy of Sciences of the United States of America 116, 18917–18922.
| Photosystem II oxygen-evolving complex photoassembly displays an inverse H/D solvent isotope effect under chloride-limiting conditions.Crossref | GoogleScholarGoogle Scholar | 31484762PubMed |
Zabret J, Bohn S, Schuller SK, Arnolds O, Möller M, Meier-Credo J, Liauw P, Chan A, Tajkhorshid E, Langer JD, Stoll R, Krieger-Liszkay A, Engel BD, Rudack T, Schuller JM, Nowaczyk MM (2021) Structural insights into photosystem II assembly. Nature Plants 7, 524–538.
| Structural insights into photosystem II assembly.Crossref | GoogleScholarGoogle Scholar | 33846594PubMed |
Zavafer A, Iermak I, Cheah MH, Chow WS (2019) Two quenchers formed during photodamage of phostosystem II and the role of one quencher in preemptive photoprotection. Scientific Reports 9, 17275
| Two quenchers formed during photodamage of phostosystem II and the role of one quencher in preemptive photoprotection.Crossref | GoogleScholarGoogle Scholar | 31754181PubMed |
Zhang L, Paakkarinen V, van Wijk KJ, Aro EM (1999) Co-translational assembly of the D1 protein into photosystem II. Journal of Biological Chemistry 274, 16062–16067.
| Co-translational assembly of the D1 protein into photosystem II.Crossref | GoogleScholarGoogle Scholar | 10347157PubMed |
