Photoinhibition of PSI and PSII in Nature and in the Laboratory: Ecological Approaches

Kono, Masaru; Oguchi, Riichi; Terashima, Ichiro

doi:10.1007/124_2022_67

Masaru Kono¹¹,
Riichi Oguchi¹² &
Ichiro Terashima¹¹

Part of the book series: Progress in Botany ((BOTANY,volume 84))

136 Accesses

Abstract

Light is indispensable for plants to photosynthesize organic matters. Almost all the organisms including animals on our planet eventually rely on this plant function for their energy as well as the materials forming their bodies. Paradoxically, light often damages the photosynthetic apparatus. This phenomenon is called photoinhibition and has been attracting attention of many photosynthesis researchers. Although the term photoinhibition had been used almost synonymously to refer to photoinhibition of photosystem II (PSII), it was recently shown that PSI is susceptible to fluctuating light. First, we compare two PSII photoinhibition hypotheses: the Mn/(Two-step) hypothesis and Excess-Y(NO) hypothesis. The former claims that the oxygen-evolving complex (OEC) is primarily damaged, while the latter claims excess excitation energy in PSII directly damages D1 function. Both can be induced in the laboratory and may parallelly occur in the same leaf. Because OEC is damaged by ultraviolet (UV) or blue light, UV screening substances in the leaf epidermis plays a crucial role. It is also indicated that the rate of PSII repair in PSII damaged by the Mn/(Two-step) mechanism is much slower than that by the Excess-Y(NO) mechanism. It appears then plants should avoid PSII photoinhibition by the Mn/(Two-step) hypothesis. Photoinhibition of photosystem I (PSI) in cucumber, a model chilling sensitive plant, and that in the mutant of PROTON GRADIENT 5 are compared. The effects of fluctuating light, which naturally occurs in the field, on PSI photoinhibition are also discussed. The PSI photoinhibition in these three cases can be explained by similar scenarios. When reduced P700 donates electrons to O₂, oxidative damage is induced. The mechanisms that protect PSI from photoinhibition all contribute to oxidation of P700 to P700⁺, a safe quencher. When a leaf is suddenly exposed to strong light, spillover of excitation energy from PSII to PSI protects both PSII and PSI from photoinhibition. In all these situations, far-red (FR) light plays essential roles in PSI protection. As FR light not only protects PSI but also enhances photosynthesis, especially in low light phases in the fluctuating light, the roles of FR light in photosynthesis should be fully examined. Other ecologically important problems that should be solved in the future are also pointed out.

Communicated by Ulrich Lüttge

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Abbreviations

APX:: Ascorbate peroxidase
CBB :: Calvin-Benson-Bassham (cycle)
CF₀ :: Membrane-embedded part of the thylakoid H⁺-ATPase
CF₁:: Catalytic component of the thylakoid H⁺-ATPase
Cyt b₆/f:: Cytochrome b₆/f complex
Cyt f :: Cytochrome f
DCIP:: Dichloro-indophenol
DCMU:: Dichlorophenyl dimethylurea
DPC:: Diphenylcarbazide
EPR:: Electron spin resonance
FA :: Iron-sulfur cluster A in PSI
FB :: Iron-sulfur cluster B in PSI
FL:: Fluctuating light
FR:: Far-red (light)
FX:: Iron-sulfur cluster X in PSI
K_pi:: Rate constant of PSI photoinhibition
k_pi:: Rate constant of PSII photoinhibition
k_rec:: Rate constant of PSII repair
LHCII :: Light-harvesting chlorophyll-protein complex of PSII
MAP:: Mehler ascorbate peroxidase (pathway)
MTSF:: Multiple turnover saturating flash
MV:: Methyl viologen
NDH :: NADH DEHYDROGENASE-LIKE complex
NPQ:: Non-photochemical quenching
OEC:: Oxygen-evolving complex
OJIP :: Analysis based on the fluorescence increasing pattern upon strong actinic light illumination
PAM:: Pulse-amplitude modulated (fluorometry)
PFD:: Photon flux density (mol m⁻² s⁻¹)
pgr5:: A mutant of PROTON GRADIENT 5/PROTON GRADIENT LIKE 1 cyclic electron transport system around PSI
PPFD :: Photosynthetically active photon flux density (400–700 nm, mol m⁻² s⁻¹)
PR:: Photorespiration (pathway)
PSI-CEF:: Cyclic electron transport around PSI
QA :: Quinone electron acceptor A
QB:: Quinone electron acceptor B
Y (NPQ):: Quantum yield of regulated thermal dissipation in PSII
RISE:: PQ reduction-induced suppression of electron flow
^SChl*:: Excited chlorophyll in the singlet state
STSF:: Single turnover saturating flash
^TChl*:: Excited chlorophyll in the triplet state
TyrZ:: A Tyr residue involving in electron transport in D1
UV-A :: Ultraviolet A, ranging from 315 or 320 nm to 400 nm
WWC:: Water to water cycle
Y(I):: Quantum yield of PSI photochemistry
Y(II) :: Quantum yield of PSII photochemistry
Y(NA):: Quantum yield of non-photochemical energy dissipation due to limitation of electron acceptors from PSI
Y(ND):: Quantum yield of non-photochemical energy dissipation due to limitation of electron donors to PSI
Y(NO):: Quantum yield of non-regulated energy dissipation in PSII

References

Adachi K, Oiwa K, Nishizaka T, Furuike S, Noji H, Itoh H, Yoshida M, Kinoshita K Jr (2007) Coupling of rotation and catalysis in F1-ATPase revealed by single-molecule imaging and manipulation. Cell 140:30–321. https://doi.org/10.1016/j.cell.2007.05.020
Article Google Scholar
Adams WW III, Terashima I (eds) (2018) The leaf: a platform for performing photosynthesis. Springer, Cham, p 575. https://doi.org/10.1007/978-3-319-93594-2
Book Google Scholar
Åkerlund H-E, Jansson C, Andersson B (1982) Reconstitution of photosynthetic water splitting in inside-put thylakoid vesicles and identification of a participating polypeptide. Biochim Biophys Acta 681:1–10
Google Scholar
Anderson JM (1986) Photoregulation of the composition, function, and structure of thylakoid membranes. Annu Rev Plant Physiol 37:93–136. https://doi.org/10.1146/annurev.pp.37.060186.000521
Article Google Scholar
Anderson JM, Aro EM (1993) Grana stacking and protection of photosystem II in thylakoid membranes of higher plant leaves under sustained high irradiance: an hypothesis. Photosynth Res 41:315–326. https://doi.org/10.1007/BF000.19409
Article Google Scholar
Anderson JM, Park Y-I, Chow WS (1997) Photoinactivation and photoprotection of photosystem II in nature. Physiol Plant 100:214–223
Google Scholar
Anderson JM, Park TI, Chow WX (1998) Unifying model for the photoinactivation of photosystem II in vivo under steady-state photosynthesis. Photosynth Res 56:1–13
Google Scholar
Anderson JM, Horton P, Kim EH, Chow WS (2012) Towards elucidation of dynamic structural changes of plant thylakoid architecture. Philos Trans R Soc B 367:3515–3524
Google Scholar
Andersson B, Anderson JM (1980) Lateral heterogeneity in the distribution of chlorophyll-protein complexes of the thylakoid membranes of spinach chloroplasts. Biochim Biophys Acta 583:427–440
Google Scholar
Armbruster U, Carrillo LR, Venema K, Pavlovic L, Schmidtmann E, Koenfeld A, Jahns P, Berry JA, Kramer DM, Jonikas MC (2014) Ion antiport accelerates photosynthetic acclimationin fluctuating light environments. Nat Commun 5:5439. https://doi.org/10.1038/ncomms6439
Article PubMed Google Scholar
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 50:601–640
PubMed Google Scholar
Bag P, Chukhutsina V, Zhang Z, Paul S, Ivanov AG, Shutova T, Croce R, Holzwarth AR, Jansson S (2020) Direct energy transfer from photosystem II to photosystem I confers winter sustainability in Scots pine. Nat Commun 11:6388. https://doi.org/10.1038/s41467-020-20137-9
Article PubMed PubMed Central Google Scholar
Baker N (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113. https://doi.org/10.1146/annurev.arplant.59.032607.092759
Article PubMed Google Scholar
Barth C, Krause GH, Winter K (2001) Responses of photosystem I compared with photosystem II to high-light stress in tropical shade and sun leaves. Plant Cell Environ 24:163–176. https://doi.org/10.1111/j.1365-3040.2001.00673.x
Article Google Scholar
Battchikova N, Eisenhut M, Aro E-M (2011) Cyanobacteril NDH-1 complexes: novel insights and remaining puzzles. Biochim Biophys Acta 1807:935–944
PubMed Google Scholar
Berthold DA, Babcock GT, Yocum CF (1981) A highly resolved, oxygen-evolving photosystem II preparation from spinach thylakoid membranes. FEBS Lett 134:231–234
Google Scholar
Bilger W, Björkman O (1990) Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynth Res 25:173–185
PubMed Google Scholar
Björkman O (1981) Responses to different quantum flux densities. In: Lange OK, Nobel PS, Osmond CB, Ziegler H (eds) Encyclopedia of plant physiology, new series, vol 12A. Springer, Berlin, pp 57–106
Google Scholar
Björkman O, Demmig B (1987) Photon yield of O₂ evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta 170:489–504
PubMed Google Scholar
Boardman NK (1977) Comparative photosynthesis of sun and shade plants. Annu Rev Plant Physiol 28:355–377. https://doi.org/10.1146/annurev.pp.28.060177.002035
Article Google Scholar
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. Inorg Chem 15:1538–1543
Google Scholar
Bos I, Bland KM, Tian L, Croce R, Frankeo LK, van Amerongen H, Bricker TM, Wientjes E (2017) Multiple LHCII antennae can transfer energy efficiently to a single photosystem I. Biochim Biophys Acta 1858:371–378. https://doi.org/10.1016/j.bbabio.2017.02.012
Article Google Scholar
Brody M, Emerson R (1959) The effect of wavelength intensity of light on the proportion of pigments in Porphyridium cruentum. Am J Bot 46:433
Google Scholar
Carraretto L, Formentin E, Teardo E, Checchetto V, Tomizioli M, Morosinotto T, Giacometti GM, Finazzi G, Szabó I (2013) A thylakoid-located two-pore K⁺ channel controls photosynthetic light utilization in plants. Science 342:114–118. https://doi.org/10.1126/science.1242113
Article PubMed Google Scholar
Cazzaniga S, Li Z, Niyogi KK, Bassi R, Dall’Osto L (2012) The Arabidopsis szl1 mutant reveals a critical role of β-carotene in photosystem I photoprotection. Plant Physiol 159: 1745–1758. doi: https://doi.org/10.1104/pp.112.201137
Chow WS, Hope AB (2004) Kinetics of reactions around the cytochrome bf complex studies in intact leaf disks. Photosynth Res 81:153–163
Google Scholar
Chow WS, Qian L, Goodchild DJ, Anderson JM (1988) Photosynthetic acclimation of Alocasia macrorrhiza (L.) G. Don. Aust J Plant Physiol 15:107–122. https://doi.org/10.1071/PP988.0107
Article Google Scholar
Chow WS, Hope AB, Anderson JM (1991) Further studies on quantifying photosystem II in vivo by flash-induced oxygen yield from leaf discs. Funct Plant Physiol 18:397–410. https://doi.org/10.1071/PP9910397
Article Google Scholar
Chow WS, Lee H-Y, He J, Hendrickson L, Hong Y-N, Matsubara S (2005) Photoinactivation of phososystem II in leaves. Photosynth Res 84:35–41
PubMed Google Scholar
Cleland RE, Melis A (1987) Probing the events of photoinhibition by altering electron -transport activity and light-harvesting capacity in chloroplast thylakoids. Plant Cell Environ 10:747–752
Google Scholar
Cox N, Pantzis DA, Lubitz W (2019) Current understanding of the mechanism of water oxidation in photosystem II and its relation to XFEL data. Annu Rev Biochem 89:795–820. https://doi.org/10.1146/annurev-biochem-011520
Article Google Scholar
Cruz JA, Avenson TJ, Kanazawa A, Takizawa K, Edwards GE, Kramer DM (2005) Plasticity in light reactions of photosynthesis for energy production and photoprotection. J Exp Bot 56:395–406. https://doi.org/10.1093/jxb/eri022
Article PubMed Google Scholar
Day TA, Martin G, Vogelmann TC (1993) Penetration of UV-B radiation in foliage: evidence that the epidermis behaves as a non-uniform filter. Plant Cell Environ 16:735–741
Google Scholar
Demmig-Adams B, Adams WW III, 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. Physiol Plant 98:253–264. https://doi.org/10.1034/j.1399-3054.1996.980206.x
Article Google Scholar
Emerson R, Lewis C (1943) The dependence of the quantum yield of chlorella photosynthesis on wavelength of light. Am J Bot 30:165–178
Google Scholar
Emerson R, Chalmers R, Cederstrand C (1957) Some factors influencing the long-wave limit of photosynthesis. Proc Natl Acad Sci U S A 43:133–143
PubMed PubMed Central Google Scholar
Flannery SE, Hepworth C, Wood WHJ, Pastorellli F, Hunter CN, Dickman MJ, Jackson PJ, Johnson MP (2021) Developmental acclimation of the thylakoid proteome to light intensity in Arabidopsis. Plant J 105:223–244
PubMed Google Scholar
Franck F, Juneau P, Popovic R (2002) Resolution of the photosystem I and photosystem II contributions to chlorophyll fluorescence of intact leaves at room temperature. Biochim Biophys Acta 1556:239–246
PubMed Google Scholar
Fujii T, Yokoyama E-I, Inoue K, Sakurai H (1990) The sites of electron donation of photosystem I to methyl viologen. Biochim Biophys Acta 1015:41–48. https://doi.org/10.1016/0005-2728(90)90213-N
Article Google Scholar
Furutani R, Ifuku K, Suzuki Y, Oguchi K, Shimakawa G, Wada S, Makino A, Sohtome T, Miyake C (2020) P700 oxidation suppresses the production of reactive oxygen species in photosystem I. Adv Bot Res 96:153–176. https://doi.org/10.1016/bs.abr.2020.08.001
Article Google Scholar
Furutani R, Ohnishi M, Mori Y, Wada S, Miyake C (2022) The difficulty of estimating the electron transport rate at photosystem I. J Plant Res 135:565–577. https://doi.org/10.1007/s10265-021-01357-6
Article PubMed Google Scholar
Gates DM (1980) Spectral characteristics of radiation and matter. In: Reichle DE (ed) Biophysical Ecology. Springer, New York, pp 181–267
Google Scholar
Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92. https://doi.org/10.1016/S0304-4165(89)80016-9
Article Google Scholar
Gray GR, Savitch LV, Ivanov AG, Huner NPA (1996) Photosystem II excitation pressure and development of resistance to photoinhibition. II. Adjustment of photosynthetic capacity in winter wheat and winter rye. Plant Physiol 107:687–694
Google Scholar
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. Biochim Biophys Acta 1706:68–80
PubMed Google Scholar
Hakala-Yatkin M, Mäntysaari M, Mattila H, Tyystjärvi E (2010) Contribution of visible and ultraviolet parts of sunlight to photoinhibition. Plant Cell Physiol 51:1745–1753. https://doi.org/10.1093/pcp/pcq133
Article PubMed Google Scholar
Havaux M, Davaud A (1994) Photoinhibition of photosynthesis in chilled potato leaves is not correalted with a loss of photosysytem-II activity: preferential inactivation of photosystem I. Photosynth Res 40:75–92. https://doi.org/10.1007/BF000.19047
Article PubMed Google Scholar
Havaux M, Strasser R, Greppin H (1991) A theoretical and experimental analysis of the q_P, and q_N coefficients of chlorophyll fluorescence quenching and their relation to photochemical and nonphotochemical events. Photosynth Res 27:41–55
PubMed Google Scholar
He J, Chow WS (2003) The rate coefficient of repair of photosystem II after photoinactivation. Physiol Plant 118:297–304
Google Scholar
He J, Yang W, Qin L, Fan D-Y, Chow WS (2015) Photoinactivation of photosystem II in wild-type and chlorophyll b-less barley leaves: which mechanisms dominates depends on experimental circumstances. Photosynth Res 126:399–407. https://doi.org/10.1007/s11120-015-0167-0
Article PubMed Google Scholar
Hendrickson L, Furbank RT, Chow WS (2004) A simple alternative approach to assessing the fate of absorbed light energy using chlorophyll fluorescence. Photosynth Res 82:73–81
PubMed Google Scholar
Higuchi M, Noguchi T, Sonoike K (2003) Over-reduced state of the Mn-cluster in cucumber leaves induced by dark-chilling treatment. Biochim Biophys Acta 1604:151–158
PubMed Google Scholar
Hikosaka K, Terashima I (1996) Nitrogen partitioning among photosynthetic components and its consequences in sun and shade plants. Funct Ecol 10:335–343. https://doi.org/10.2307/23902.81
Article Google Scholar
Hikosaka K, Tersahima I (1995) A model of the acclimation of photo- synthesis in the leaves of C3 plants to sun and shade with respect to nitrogen use. Plant Cell Environ 18:615–618. https://doi.org/10.1111/j.1365-3040.1995.tb005.62.x
Article Google Scholar
Hikosaka K, Kato M, Hirose T (2004) Photosynthetic rates and partitioning of absorbed light energy in photoinhibited leaves. Physiol Plant 121:699–708. https://doi.org/10.1111/j.1399-3054.2004.00364.x
Article Google Scholar
Hikosaka K, Niinemets Ü, Anten NPP (eds) (2015) Canopy photosynthesis: from basics to applications. Springer, Dordrecht, p 428. https://doi.org/10.1007/978-94-017-7291-4
Book Google Scholar
Höhner R, Galvis VC, Strand DD, Völkner C, Krämer M, Messer M, Dinc F, Sjuts I, Bölter B, Kramer DM, Armbruster U, Kunz HH (2019) Photosynthesis in Arabidopsis is unaffected by the function of the vacuolar K⁺ channel TPK3. Plant Physiol 180:1322–1335
PubMed PubMed Central Google Scholar
Ifuku K, Yamamoto Y, Ono TA, Ishihara S, Sato F (2005) PsbP protein, but not PsbQ protein, is essential for the regulation and stabilization of photosystem II in higher plants. Plant Physiol 139:1175–1184. https://doi.org/10.1104/pp.105.068643
Article PubMed PubMed Central Google Scholar
Inoue K, Sakurai H, Hiyama T (1986) Photoinactivation sites of photosystem I in isolated chloroplasts. Plant Cell Physiol 27:962–968. https://doi.org/10.1093/oxfordjournals.pcp.a0772.13
Article Google Scholar
Inoue K, Fujii T, Yokoyama E, Matsuura K, Hiyama T, Sakurai H (1989) The photoinhibition site of photosystem I in isolated chloroplasts under extremely reducing conditions. Plant Cell Physiol 30:65–71
Google Scholar
Ishida S, Morita KI, Kishine M, Takabayashi A, Murakami R. Takeda S. Shimamoto K, Sato F, Endo T (2011) Allocation of absorbed light energy in PSII to thermal dissipations in the presence or absence of PsbS subunits of rice. Plant Cell Physiol 52: 1822–1831
Google Scholar
Ishida S, Uebayashi N, Tazoe Y, Ikeuchi M, Homma K, Sato F, Endo T (2014) Diurnal and developmental changes in energy allocation of absorbed light at PSII in field-grown rice. Plant Cell Physiol 55:171–182
PubMed Google Scholar
Ivanov AG, Morgan RM, Gray GR, Welitchkova MY, Huner NPA (1998) Temperature/light dependent development of selective resistance to photoinhibition of photosystem I. FEBS Lett 430:288–292
PubMed Google Scholar
Ivanov AG, Rosso D, Savitch LV, Stachula P, Rosembert M, Öquist G, Hurry V, Huner NPA (2012) Implication of alternative electron sinks in increased resistance of PSII and PSI photochemistry to high light stress in cold-acclimated Arabidopsis thaliana. Photosynth Res 113:191–206. https://doi.org/10.1007/s11120-012-9769-y
Article PubMed Google Scholar
Iwai M, Yokono M, Kurokawa K, Ichihara A, Nakano A (2018) Live-cell visualization of excitation energy dynamics in chloroplast thylakoid structures. Sci Rep 6:29940. https://doi.org/10.1038/srep29940
Article Google Scholar
Izawa S (1980) Acceptors and donors and chloroplast electron transport. Methods Enzymol 69:413–434. https://doi.org/10.1016/S0076-6879(80)69041-7
Article Google Scholar
Järvi S, Suorsa M, Aro E-M (2015) Photosystem II repair in plant chloroplasts-regulation, assisting proteins and shared components with photosystem II biogenesis. Biochim Biophys Acta 1847:900–909. https://doi.org/10.1016/j.bbabio.2015.01.006
Article PubMed Google Scholar
Jegerschöld C, Virgin I, Styring S (1990) Light-dependent degradation of the D1 protein in photosystem II is accelerated after inhibition of the water splitting reaction. Biochem 29:6179–6186
Google Scholar
Jones LW, Kok B (1966) Photoinhibition of chloroplast reactions. I. Kinetics and action spectra. Plant Physiol 41:1037–1043. https://doi.org/10.1104/pp.41.6.1037
Article PubMed PubMed Central Google Scholar
Kaniuga Z, Michalski W (1978) Photosynthetic apparatus in chilling-sensitive plants. II. Changes in free fatty acid composition and photoperoxidation in chloroplasts following cold storage and illumination of leaves in relation to Hill reaction activity. Planta 140:129–136
PubMed Google Scholar
Kaniuga Z, Sochanowicz B, Ząbec J, Krzystyniak K (1978) Photosynthetic apparatus in chilling-sensitive plants. I. Reactivation of Hill reaction activity inhibited on the cold and dark storage of detached leaves and intact plants. Planta 140:121–128
PubMed Google Scholar
Karapetyan NN (2008) Protective dissipation of excess absorbed energy by photosynthetic apparatus of cyanobacteria: role of antenna terminal emitters. Photosynth Res 97:195–204
PubMed Google Scholar
Kasajima I, Takahara K, Kawai-Yamada M, Uchimiya H (2009) Estimation of the relative sizes of rate constants for chlorophyll de-excitation processes through comparison of inverse fluorescence intensities. Plant Cell Physiol 50:1600–1616. https://doi.org/10.1093/pcp/pcp102
Article PubMed Google Scholar
Kato N, Hikosaka K, Hirotsu N, Makino A, Hirose T (2003) The excess light energy that is neither utilized in photosynthesis nor dissipated by photoprotective mechanisms determines the rate of photoinactivation in photosystem II. Plant Cell Physiol 44:318–325
PubMed Google Scholar
Kato Y, Hyodo K, Sakamoto W (2018) The photosystem II repair cycle requires FtsH turnover through the EngA GTPase. Plant Physiol 178:596–611. https://doi.org/10.1104/pp.18.00652
Article PubMed PubMed Central Google Scholar
Katoh S, San Pietro A (1967) Ascorbate-supported NADP photoreduction by heated Euglena chloroplats. Arch Biochem Biophys 122:144–152
PubMed Google Scholar
Kim E, Watanabe A, Duffy CDP, Ruban AV, Minagawa J (2020) Multimeric and monomeric photosystem II supercomplexes represent structural adaptations to low-and high-light condi- tions. J Biol Chem 295:14537–14545. https://doi.org/10.1074/jbc.RA120.014198
Article PubMed PubMed Central Google Scholar
Kitajima M, Butler WL (1975a) Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone. Biochim Biophys Acta 376:105–115
PubMed Google Scholar
Kitajima M, Butler WL (1975b) Fluorescence quenching in photosystem II of chloroplasts. Biochim Biophys Acta 376:116–125
PubMed Google Scholar
Kitajima M, Butler WL (1975c) Excitation spectra for photosystem I and photosystem II in chloroplasts and the spectral characteristics of the distribution of quanta between the two photosystems. Biochim Biophys Acta 408:297–305
PubMed Google Scholar
Klughammer C, Schreiber U (1994) An improved method, using saturating light-pulses, for the determination of photosystem-I quantum yield via P700⁺-absorbency changes at 830 nm. Planta 192:261–268. https://doi.org/10.1007/BF001.94461
Article Google 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 Appl Notes 1:27–35
Google Scholar
Klughammer C, Siebke K, Schreiber U (2013) Continuous ECS-indicated recording of the proton-motive charge flux in leaves. Photosynth Res 117:471–487
PubMed PubMed Central Google Scholar
Kok B (1956) Kinetics of photosynthesis and photo-inhibition. Nature 177:135–136
Google Scholar
Kono M, Terashima I (2014) Long-term and short-term responses of the photosynthetic electron transport to fluctuating light. J Photochem Photobiol B 137:89–99. https://doi.org/10.1016/j.jphotobiol.2014.02.016
Article PubMed Google Scholar
Kono M, 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
Article PubMed Google Scholar
Kono M, Noguchi K, Terashima I (2014) Roles of the cyclic electron flow around PSI (CEF-PSI) and O -dependent alternative pathways in regulation of the photosynthetic electron flow in short-term fluctuating light in Arabidopsis thaliana. Plant Cell Physiol 55:990–1004. https://doi.org/10.1093/pcp/pcu033
Article PubMed Google Scholar
Kono M, Yamori W, Suzuki Y, Terashima I (2017) Photoprotection of PSI by far-red light against the fluctuating light-induced photoinhibition in Arabidopsis thaliana and field-grown plants. Plant Cell Physiol 58:35–45. https://doi.org/10.1093/pcp/pcw215
Article PubMed Google Scholar
Kono M, Kawaguchi H, Mizusawa N, Yamori W, Suzuki Y, Terashima I (2020) Far-red light accelerates photosynthesis in the low-light phases of fluctuating light. Plant Cell Physiol 61:192–202. https://doi.org/10.1093/pcp/pcz191
Article PubMed Google Scholar
Kono M, Matsuzawa S, Noguchi T, Miyata K, Oguchi R, Terashima I (2022a) A new method for separate evaluation of PSII with inactive oxygen evolving complex and active D1 by the pulse-ampplitude modulated chlorophyll fluorometry. Funct Plant Biol 49:542–553. https://doi.org/10.1071/FP21073
Article PubMed Google Scholar
Kono M, Miyata K, Matsuzawa S, Noguchi T, Oguchi R, Suzuki Y, Terashima I (2022b) Mixed population hypothesis of the active and inactive PSII complexes opens a new door for photoinhibition and fluorescence studies: an ecophysiological perspective. Funct Plant Biol. (published online 13 July 2022). https://doi.org/10.1071/FP21355
Körner C (2021) Tools shape paradigms of plant-environment interactions. Prog Bot 82:1–42. https://doi.org/10.1007/124_2020_41
Article Google Scholar
Kornyeyev D, Holaday S, Logan BA (2003a) Predicting the extent of photosystem II photoinactivation using chlorophyll a fluorescence parameter measured during illumination. Plant Cell Physiol 44:1064–1070. https://doi.org/10.1093/pcp/pcg129
Article PubMed Google Scholar
Kornyeyev D, Logan BA, Allen RD, Holaday AS (2003b) Effect of chloroplastic overproduction of ascorbate peroxidase on photosynthesis and photoprotection in cotton leaves subjected to low temperature photoinhibition. Plant Sci 165:10933–11041. https://doi.org/10.1016/S0168-9452(03)00294-2
Article Google Scholar
Kornyeyev D, Logan BA, Payton PR, Alle RD, Holaday AS (2003c) Elevated chloroplastic glutathione reductase activities decrease chilling-induced photoinhibition by increasing rates of photochemistry, but not thermal energy dissipation, in transgenic cotton. Funct Plant Biol 30:101–110. https://doi.org/10.1071/FP02144
Article PubMed Google Scholar
Kou J, Takahashi S, Oguchi R, Fan D-Y, Badger MR, Chow WS (2013) Estimation of the steady-state cyclic electron flux around PSI in spinach leaf discs in white light, CO₂-enriched air and other varied conditions. Funct Plant Biol 40:1018–1028. https://doi.org/10.1071/FP13010
Article PubMed Google Scholar
Kramer D, Evans JR (2011) The importance of energy balance in improving photosynthetic productivity. Plant Physiol 155:70–78. https://doi.org/10.1104/pp.110.166652
Article PubMed Google Scholar
Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of QA redox state and excitation fluxes. Photosynth Res 79:209–218
PubMed Google Scholar
Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Physiol Plant Mol Biol 42:313–349
Google Scholar
Krause GH, Winter K (2021) The photosynthetic system in tropical plants under high irradiance and temperature stress. Prog Bot 82:131–169
Google Scholar
Krieger A, Weis E, Demeter S (1993) Low-pH-induced Ca²⁺ ion release in the water-splitting system is accompanied by a shift in the midpoint redox potential of the primary quinone acceptor QA. Biochim Biophys Acta 1144:411–418
Google Scholar
Kudoh H, Sonoike K (2002) 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. https://doi.org/10.1007/s00425-002-0790-9
Article PubMed Google Scholar
Külheim C, Ågren J, Jansson S (2002) Rapid regulation of light harvesting and plant fitness in the field. Science 297:91–93. https://doi.org/10.1126/science.1072359
Article PubMed Google Scholar
Laisk A, Oja V (2020) Variable fluorescence of closed photochemical reaction centres. Photosynth Res 143:335–346. https://doi.org/10.1007/s11120-020-00712-3
Article PubMed Google Scholar
Lazár D (2015) Parameters of photosynthetic energy partitioning. J Plant Physiol 175:131–147. https://doi.org/10.1016/j.jplph.2014.10.021
Article PubMed Google Scholar
Li L, Aro EM, Miller AH (2018) Mechanisms of photodamage and protein turnover in photoinhibition. Trends Plant Sci 23:667–676. https://doi.org/10.1016/j.tplants.2018.05.004
Article PubMed Google Scholar
Lois R (1994) Accumulation of UV-absorbing flavonoids induced by in Arabidopsis thaliana L. I. Mechanisms of UV-resistance in Arabidopsis UV-B radiation. Planta 194:498–503
Google Scholar
Malone LA, Proctor MS, Hitchcock A, Huner CN, Johnson MP (2021) Cytochrome b₆f – orchestrator of photosynthetic electron transfer. Biochim Biophys Acta 1862:148380. https://doi.org/10.1016/j.bbabio.2021.148380
Article Google Scholar
Margulies MM (1972) Effects of cold-storage of bean leaves on photosynthetic reactions of isolated chloroplasts. Inability to donate electron to photosystem II and reactions to manganese content. Biochim Biophys Acta 267:96–103
PubMed Google Scholar
Matsubara S, Chow WS (2004) Populations of photoinactivated photosystem II reaction centres characterized by chlorophyll a fluorescence life time in vivo. Proc Natl Acad Sci U S A 101:18234–18239. https://doi.org/10.1073/pnas.0403857102
Article PubMed PubMed Central Google Scholar
Mattila H, Khorobrykh S, Hakala-Yatkin M, Havyrubbe V, Kuusisto I, Antal T, Tyystjärvi T, Tyystjärvi T (2020a) Action spectrum of the redox state of the plastoquinone pool defines its function in plant acclimation. Plant J 104:1088–1104. https://doi.org/10.1111/tpj.14983
Article PubMed Google Scholar
Mattila H, Misra KB, Kuusisto I, Mishra A, Novotná K, Šebela D, Tyystjäevi T (2020b) Effects of low temperature on photoinhibition and singlet oxygen production in four natural accessions of Arabidopsis. Planta 252:19. https://doi.org/10.1007/s00425-020-03423-0
Article PubMed PubMed Central Google Scholar
Maxwell DP, Falk S, Huner NPA (1995) Photosystem II excitation pressure and development of resistance to photoinhibition: I. Light-harvesting complex II abundance and zeaxanthin content in Chlorella vulgaris. Plant Physiol 107:687–694. https://doi.org/10.1104/pp.107.3.687
Article PubMed PubMed Central Google Scholar
Miyake C (2010) Alternative electron flows (water-water cycle and cyclic electron flow around PSI) in photosynthesis: molecular mechanisms and physiological functions. Plant Cell Physiol 51:1951–1963
PubMed Google Scholar
Miyake C (2020) Molecular mechanisms of oxidation of P700 and suppression of ROS production in photosystem I in response to electron-sink limitations in C3 plants. Antioxidants 9:230. https://doi.org/10.3390/antiox9030.230
Article PubMed PubMed Central Google Scholar
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. Photosynth Res 113:165–180. https://doi.org/10.1007/s11120-012-9767-0
Article PubMed Google Scholar
Miyata K, Ikeda H, Nakaji M, Kanel DR, Terashima I (2015) Rate constants of PSII photoinhibition and its repair, and PSII fluorescence parameters in the field plants in relation to their growth light environments. Plant Cell Physiol 56:1841–1854. https://doi.org/10.1093/pcp/pcv107
Article PubMed Google Scholar
Munekage Y, Hojo M, Meurer J, Endo T, Tsak M, 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
Article PubMed Google Scholar
Murata N, Nishiyama Y (2018) ATP is a driving force in the repair of photosystem II during photoinhibition. Plant Cell Environ 41:285–299. https://doi.org/10.1111/pce.13108
Article PubMed Google Scholar
Nawrocki WJ, Liu X, Raber B, Hu C, de Vitry C, Bennett DIG, Groce R (2021) Molecular origins of induction and loss of photoinhibition-related energy dissipation qI. Sci Adv 7:eabj0055
PubMed PubMed Central Google Scholar
Nellaepalli S, Kim RG, Grossman AR, Takahashi Y (2021) Interplay of four auxiliary factors is required for the assembly of photosystem I reaction centre subcomplex. Plant J 106:1075–1086. https://doi.org/10.1111/tpj.15220
Article PubMed Google Scholar
Nickelsen J, Rengstl B (2013) Photosystem II assembly: from cyanobacteria to plants. Annu Rev Plant Biol 64:609–635. https://doi.org/10.1146/annurev-arplant-050312-120124
Article PubMed Google Scholar
Noji H, Ueno H, McMillan DGG (2017) Catalytic robustness and torque generation of the F1-ATPase. Biophys Rev 9:103–118. https://doi.org/10.1007/s12551-017-0262-x
Article PubMed PubMed Central Google Scholar
Ogawa T, Mi H (2007) Cyanobacterial NADPH dehydrogenase complexes. Photosynth Res 93:69–77. https://doi.org/10.1007/s11120-006-9128-y
Article PubMed Google Scholar
Oguchi R, Terashima I, Chow WS (2009) The involvement of dual mechanisms of photoinactivation of photosystem II in Capsicum annuum L. plants. Plant Cell Physiol 50:1815–1825
PubMed Google Scholar
Oguchi R, Douwstra P, Fujita T, Chow WS, Terashima I (2011a) Intra-leaf gradients of photoinhibition induced by different color lights: implications for the dual mechanisms of photoinhibition and for the application of conventional chlorophyll fluorometers. New Phytol 191:146–159
PubMed Google Scholar
Oguchi R, Terashima I, Kou J, Chow WS (2011b) Operation of dual mechanisms that both lead to photoinactivation of Photosystem II in leaves by visible light. Physiol Plant 142: 47–55. doi:https://doi.org/10.1111/j.1399-3054.2011.01452.x
Oguchi R, Terashima I, Chow WS (2021) The effect of different spectral light quality on the photoinhibition of photosystem I in intact leaves. Photosynth Res 149:83–92. https://doi.org/10.1007/s11120-020-00805-z
Article PubMed Google Scholar
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 centre. Biochemistry 44:8494–8499. https://doi.org/10.1021/bi047518q
Article PubMed Google Scholar
Okada K, Satoh K, Katoh S (1991) Chloramphenicol is an inhibitor of photosynthesis. FEBS Lett 295:155–158
PubMed Google Scholar
Öquist G, Greer DH, Ögren E (1987) Light stress at low temperature. In: Kyle DJ, Osmond CB, Arntzen CJ (eds) Photoinhibition. Elsevier, Amsterdam, pp 67–87. ISBN-13: 978-0444808905
Google Scholar
Öquist G, Anderson JM, McCaffery S, Chow WS (1992) Mechanistic differences in photoinhibition of sun and shade plants. Planta 188:422–431
PubMed Google Scholar
Oxborough K, Baker NR (1997) Resolving chlorophyll a fluorescence of photosynthetic efficiency into photochemical components – calculation of qP and Fv’/Fm’ without measuring Fo’. Photosynth Res 54:135–142
Google Scholar
Oxborough K, Ort DR (1995) In situ evidence that chilling in the light does not cause uncoupling of photophosphorylation or detachment of coupling factor in chilling-sensitive plants. Photosynth Res 43:93–105
PubMed Google Scholar
Papageorgiou GC, Govindjee eds (2004) Chlorophyll a fluorescence: a signature of photosynthesis. pp. XXIV+818, Springer, Dordrecht. doi:https://doi.org/10.1007/978-1-4020-3218-9
Pearcy RW (1990) Sunflecks and photosynthesis in plant canopies. Annu Rev Plant Physiol Plant Mol Biol 41:421–453. https://doi.org/10.1146/annurev.pp.41.060190.002225
Article Google Scholar
Pfündel EE, Ghozlen NB, Meyer S, Cerobic ZG (2007) Investigating UV screening in leaves by two different types of portable UV fluorimeters reveals in vivo screening by anthocyanins and carotenoids. Phootsynth Res 93:205–221. https://doi.org/10.1007/s11120-007-9135-7
Article Google Scholar
Powles SB (1984) Photoinhibition of photosynthesis induced by visible light. Annu Rev Plant Physiol 35:15–44
Google Scholar
Roach T (2020) Lhcsr3-type npq prevents photoinhibition and slowed growth under fluctuating light in Chlamydomonas reinhardtii. Plan Theory 9:1604. https://doi.org/10.3390/plants9111604
Article Google Scholar
Rozak PR, Seiser RM, Wacholtz WF, Wise RR (2002) Rapid, reversible alterations in spinach thylakoid appression upon changes in light intensity. Plant Cell Environ 25:421–429
Google Scholar
Rutherford AW, Osyczka A, Rappaport F (2012) Back-reactions, short-circuits, leaks and other energy wasteful reactions in biological electron transfer: redox tuning to survive life in O. FEBS Lett 586:603–616. https://doi.org/10.1016/j.febsl.et.2011.12.039
Article PubMed Google Scholar
Sarvikas P, Tyystjärvi T, Tyystjärvi E (2010) Kinetics of prolonged photoinhibition revisited: photoinhibited photosystem II centres do not protect the active ones against loss of oxygen evolution. Photosynth Res 103:7–17. https://doi.org/10.1007/s11120-009-9496-1
Article PubMed Google Scholar
Sato A, Nakano Y, Nakamura S, Noguchi T (2021) Rapid-scan time-resolved ATR-FTIR study on the photoassembly of the aater-oxidizing Mn₄CaO₅ cluster in photosystem II. J Phys Chem B 125:4031–4045
PubMed Google Scholar
Satoh K (1970a) Mechanisms of photoinactivation in photosynthetic systems. I. The dark reaction in photoinactivation. Plant Cell Physiol 11:15–27. https://doi.org/10.1093/oxfordjournals.pcp.a0744.87
Article Google Scholar
Satoh K (1970b) Mechanisms of photoinactivation in photosynthetic systems. II. The occurrence and properties of two different types of photoinactivation. Plant Cell Physiol 11:29–38. https://doi.org/10.1093/oxfordjournals.pcp.a0744.93
Article Google Scholar
Satoh K (1970c) Mechanisms of photoinactivation in photosynthetic systems. III. Site and mode of phoinactivation in photosystem I. Plant Cell Physiol 11:187–197. https://doi.org/10.1093/oxfordjournals.pcp.a074500
Article Google Scholar
Schansker G, Tóth SZ, Holzwarth AR, Garab G (2014) Chlorophyll a fluorescence: beyond the limits of the QA model. Photosynth Res 120:43–58. https://doi.org/10.1007/s11120-013-9806-5
Article PubMed Google Scholar
Schöttler MA, Tóth SZ (2014) Photosynthetic complex stoichiometry dynamics in higher plants: environmental acclimation and photosynthetic flux control. Front Plant Sci 5:188. https://doi.org/10.3389/fpls.2014.00188
Article PubMed PubMed Central Google Scholar
Schreiber U, Klughammer C (2013) Wavelength-dependent photodamage to Chlorella investigated with a new type of multi-color PAM chlorophyll fluorometer. Photosynth Res 114:165–177. https://doi.org/10.1007/s11120-013-9801-x
Article PubMed Google Scholar
Searle GFW, Tredwell CJ, Barber J, Porter G (1979) Picosecond time-resolved fluorescence study of chlorophyll organization and excitation-energy distribution in chloroplasts from wild-type barley and a mutant lacking chlorophyll-b. Biochim Biophys Acta 545:496–507
PubMed Google Scholar
Sejima T, Takag D, Fukayama H, Makino A, 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
Article PubMed Google Scholar
Şener M, Strumpfer J, Hsin J, Chandler D, Scheuring S, Hunter N, Schulten K (2011) Förster energy transfer theory as reflected in the structures of photosynthetic light harvesting systems. Chem Phys Chem 12:518–531. https://doi.org/10.1002/cphc.201000944
Article PubMed Google Scholar
Shaku K, Shimakawa G, Hashiguchi M, Miyake C (2016) Reduction-induced suppression of electron flow (RISE) in the photosynthetic electron transport system of Synechococcus elongatus PCC 7942. Plant Cell Physiol 57:1443–1453. https://doi.org/10.1093/pcp/pcv198
Article PubMed Google Scholar
Shen J-R, Terashima I, Katoh S (1990) Cause for dark, chilling-induced inactivation of photosynthetic oxygen-evolving system in cucumber leaves. Plant Physiol 93:1354–1357
PubMed PubMed Central Google Scholar
Shimakawa G, Miyake C (2018a) Oxidation of P700 ensures robust photosynthesis. Front Plant Sci 9:1617. https://doi.org/10.3389/fpls.2018.01617
Article PubMed PubMed Central Google Scholar
Shimakawa G, Miyake C (2018b) Reduction-induced suppression of electron flow (RISE) is relieved by non-ATP-consuming electron flow in Synechococcus elongatus PCC 7942. Front Microbiol 9:886. https://doi.org/10.3389/fmicb.2018.00886
Article PubMed PubMed Central Google Scholar
Sipka G, Magyar M, Mezzetti A, Akhtar P, Zhu Q, Xiao Y, Han G, Santabarbara S, Shen JR, Lambrev PH, Garab G (2021) Light-adapted charge-separated state of photosystem II: structural and functional dynamics of the closed reaction centre. Plant Cell 33:1286–1302. https://doi.org/10.1093/plcell/koab008
Article PubMed PubMed Central Google Scholar
Smith H (1982) Light quality, photoperception, and plant strategy. Annu Rev Plant Physiol 33:481–518
Google Scholar
Sonoike K (1996) Degradation of psaB gene product, the reaction centre 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
Article Google Scholar
Sonoike K (1999) The different roles of chilling temperatures in the photoinhibition of photosystem I and photosystem II. J Photochem Photobiol B Biology 48:136–141
Google Scholar
Sonoike K (2011) Photoinhibition of photosystem I. Physiol Plant 142:56–64. https://doi.org/10.1111/j.1399-3054.2010.01437.x
Article PubMed Google Scholar
Sonoike K, Terashima I (1994) Mechanism of photosystem-I photoinhibition in leaves of Cucumis sativus L. Planta 194:287–293. https://doi.org/10.1007/BF011.01690
Article Google Scholar
Sonoike K, Terashima I, Iwaki M, Itoh S (1995) Destruction of photosystem iron-sulfur centres 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
Article PubMed Google Scholar
Stefanov D, Terashima I (2008) Non-photochemical loss in PSII in high- and low-light-grown leaves of Vicia faba quantified by several fluorescence parameters including LNP, a novel parameter. Physiol Plant 133:327–338. https://doi.org/10.1111/j.1399-3054.rev2008.01077.x
Article PubMed Google Scholar
Steigmiller S, Turina P, Gräber P (2008) The thermodynamic H/ATP ratios of the H-ATP synthases from chloroplasts and Escherichia coli. Proc Natl Acad Sci U S A 105:3745–3750. https://doi.org/10.1073/pnas.0708356105
Article PubMed PubMed Central Google Scholar
Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transient. In: Papgeorgiou GC, Govindjee (eds) Chlorophyll fluorescence: a signature of photosynthesis. Springer, Dordrecht, pp 321–362. https://doi.org/10.1007/978-1-4020-3218-9_12
Chapter Google Scholar
Suorsa M, Jarvi S, Grieco M, Nurmi M, Pietrzykowska M, Rantala M, Kangasjarvi S, Paakkarinen V, Tikkanen M, Jansson S, 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
Article PubMed PubMed Central Google Scholar
Takagi D, Takumi S, Hashiguchi M, Sejima T, 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
Article PubMed PubMed Central Google Scholar
Takagi D, Ihara H, Takumi S, Miyake C (2019) Growth light environment changes the sensitivity of photosystem I photoinhibition depending on common wheat cultivars. Front Plant Sci 10:686. https://doi.org/10.3389/fpls.2019.00686
Article PubMed PubMed Central Google Scholar
Takahashi S, Badger MR (2010) Photoprotection in plants: a new light on photosystem II damage. Trends Plant Sci 16:53–60. https://doi.org/10.1016/j.tplants.2010.10.001
Article PubMed Google Scholar
Takeuchi K, Che Y, Nakano T, Miyake C, Ifuku K (2022) The ability of P700 oxidation in photosystem I reflects chilling stress tolerance in cucumber. J Plant Res. (Published online on 29 June 2022). https://doi.org/10.1007/s10265-022-01404-w
Tasker R, Smith H (1977) The function of phytochrome in the natural environment V. Seasonal changes in radiant energy quality in woodlands. Photochem Photobiol 26:487–491
Google Scholar
Teicher HB, Møller BL, Scheller HV (2000) Photoinhibition of photosystem I in field-grown barley (Hordeum vulgare L.): induction, recovery and acclimation. Photosynth Res 64:53–61
Google Scholar
Terashima I, Hikosaka K (1995) Comparative ecophysiology of leaf and canopy photosynthesis. Plant Cell Environ 18:1111–1128
Google Scholar
Terashima I, Huang L-K, Osmond CB (1989) Effects of leaf chilling on thylakoid functions, measured at room temperature, in Cucumis sativus L. and Oryza sativa L. Plant Cell Physiol 30:841–850
Google Scholar
Terashima I, Kashino Y, Katoh S (1991a) Exposure of leaves of Cucumis sativus L. to low temperatures in the light causes uncoupling of thylakoids I. Studies with isolated thylakoids. Plant Cell Physiol 32:1267–1274
Google Scholar
Terashima I, Sonoike K, Kawazu T, Katoh S (1991b) Exposure of leaves of Cucumis sativus L. to low temperatures in the light causes uncoupling of thylakoids II. Non-destructive measurements with intact leaves. Plant Cell Physiol 32:1275–1283
Google Scholar
Terashima I, Funayama S, 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/BF001.92544
Article Google Scholar
Terashima I, Noguchi K, Itoh-Nemoto T, Park Y-M, Kubo A, Tanaka K (1998) The cause of PSI photoinhibition at low temperatures in leaves of Cucumis sativus, a chilling-sensitive plant. Physiol Plant 103:295–303
Google Scholar
Terashima I, Ooeda H, Fujita T, Oguchi R (2016) Light environment within a leaf. II. Progress in the past one-third century. J Plant Res 129:353–363. https://doi.org/10.1007/s10265-016-0808-1
Article Google Scholar
Terashima I, Matsuo M, Suzuki Y, Yamori W, Kono M (2021) Photosystem I in low light-grown leaves of Alocasia odora, a shade-tolerant plant, is resistant to fluctuating light-induced photoinhibition. Photosynth Res 149:69–82. https://doi.org/10.1007/s11120-021-00832-4
Article PubMed Google Scholar
Tester M, Blatt MR (1989) Direct measurement of K⁺ channels in thylakoid membranes by incorporation of vesicles into planar lipid bilayers. Plant Physiol 91:249–252
PubMed PubMed Central Google Scholar
Tikkanen M, Makala NR, Aro EM (2014) Photosystem II photoinhibition-repair cycle protects Photosystem I from irreversible damage. Biochim Biophys Acta 1837:210–215
PubMed Google Scholar
Tikhonov AN (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
Article PubMed Google Scholar
Tikkanen M, Grebe S (2018) Switching off photoprotection of photosystem I- a novel tool for gradual PSI photoinhibition. Phsiol Plant 162:156–161. https://doi.org/10.1111/ppl.12618
Article Google Scholar
Tikkanen M, Griecon M, Kangasjärvi S, Aro EM (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
Article PubMed PubMed Central Google Scholar
Tiwari A, Mamedov F, Grieco M, Soursa M, Jajoo A, Styring S, Tikkanen M, Aro EM (2016) Photodamage of iron-sulphur clusters in photosystem I induces non-photochemical energy dissipation. Nat Plants 2:1–9. https://doi.org/10.1038/NPLANTS.2016.35
Article Google Scholar
Tjus SE, Møller BL, Scheller HV (1998) Photosystem I is an early target of photoinhibition in barley illuminated at chilling temperatures. Plant Physiol 116:755–764
PubMed Google Scholar
Trebst A (2007) Inhibitors in the functional dissection of the photosynthetic electron transport system. Photosynth Res 92:217–224. https://doi.org/10.1007/s11120-007-9213-x
Article PubMed Google Scholar
Trissl HW (1997) Determination of the quenching efficiency of the oxidized primary donor of photosystem I, P700: implications for the trapping mechanisms. Photosynth Res 54:237–240. https://doi.org/10.1023/A:10059.81016.835
Article Google Scholar
Tsonev TD, Hikosaka K (2003) Contribution of photosynthetic electron transport, heat dissipation, and recovery of photoinactivated photosystem II to photoprotection at different temperatures in Chenopodium album leaves. Plant Cell Physiol 44:828–835
PubMed Google Scholar
Tsuyama M, Kobayashi Y (2009) Reduction of the primary donor P700 of photosystem I during steady-state photosynthesis under low light in Arabidopsis. Photosynth Res 99:37–47. https://doi.org/10.1007/s11120-008-9379-x
Article PubMed Google Scholar
Tyystjärvi E (2013) Photoinhibition of photosystem II. Int Rev Cell Mol Biol 300:243–303. https://doi.org/10.1016/B978-0-12-405210-9.00007-2
Article PubMed Google Scholar
Tyystjärvi E, Aro E-M (1996) The rate constant of photoinhibition, measured in lincomycin-treated leaves, is directly proportional to light intensity. Proc Natl Acad Sci U S A 93:2213–2218
PubMed PubMed Central Google Scholar
Uniacke J, Zerges A (2007) Photosystem II assembly and repair are differentially localized in Chlamydomonas. Plant Cell 19:3640–3654. https://doi.org/10.1105/tpc.107.054882
Article PubMed PubMed Central Google Scholar
Vass I (2011) Role of charge recombination processes in photodamage and photoprotection of the photosystem II complex. Physiol Plant 142:6–16. https://doi.org/10.1111/j.1399-3054.2011.01454.x
Article PubMed Google Scholar
West KR, Wiskish JT (1968) Photosynthetic control by isolated pea chloroplasts. Biochem J 109:527–532
PubMed PubMed Central Google Scholar
Wise RR, Terashima I, Ort D (1990) The effect of chilling in the light on photophosphorylation analysis of discrepancies between in vitro and in vivo results. Photosynth Res 25:137–139
PubMed Google Scholar
Wood WHJ, Barnett SFH, Flannery S, Hunter CN, Johnson MP (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
Article PubMed Central Google Scholar
Yamashita T, Butler WL (1969) Photooxidation by photosystem II of tris-washed chloroplasts. Plant Physiol 44:1342–1346
PubMed PubMed Central Google Scholar
Yamori W (2016) Photosynthetic response to fluctuating environments and photoprotective strategies under abiotic stress. J Plant Res 129:379–395. https://doi.org/10.1007/s10265-016-0816-1
Article PubMed Google Scholar
Yi X-P, Yao H-S, Fan D-Y, Zhu X-G, Losciale P, Zhang Y-L, Zhang W-F, Chow WS (2022) The energy cost of repairing photoinactivated photosystem II: an experimental determination in cotton leaf discs. New Phytol. https://doi.org/10.1111/nph.18165
Yokono M, Murakami A, Akinomot S (2015) A mega-complex composed of both photosystem reaction centres in higher plants. Nat Commun 6:6675. https://doi.org/10.1038/ncomm.s7675
Article PubMed Google Scholar
Yokono M, Takabayashi A, Kishimoto J, Fujita T, Iwai M, Murakami A, Akimoto S, Tanaka A (2019) The PSI-PSII megacomplex in green plants. Plant Cell Physiol 60:1098–1108. https://doi.org/10.1093/pcp/pcz026
Article PubMed Google Scholar
Yordanov I, Velikova V (2000) Photoinhibition of photosystem I. Burg J Plant Physiol 26:70–92
Google Scholar
Zabret J, Bohn S, Schuller SK, Arnold 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, Nwoaczyk MM (2021) Structural insights into photosystem II assembly. Nat Plant 7:524–538. https://doi.org/10.1038/s41477-021-00895-0
Article Google Scholar
Zavafer A, Cheah MH, Hillier W, Chow WS, Takahashi S (2015) Photodamage to the oxygen evolving complex of photosystem II by visible light. Sci Rep 5:16363. https://doi.org/10.1038/srep16363
Article PubMed PubMed Central Google Scholar
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. Sci Rep 9:17275. https://doi.org/10.1038/s41598-019-53030-7
Article PubMed PubMed Central Google Scholar
Zhang S, Scheller HV (2004) Photoinhibition of photosystem I at chilling temperature and subsequent recovery in Arabidopsis thaliana. Plant Cell Physiol 45:1595–1602. https://doi.org/10.1093/pcp/pch180
Article PubMed Google Scholar
Zhang M-M, Fan D-Y, Sun G-Y, Chow WS (2018) Optimizing the linear electron transport rate measured by chlorophyll a fluorescence to empirically match the gross rate of oxygen evolution in white light: towards improved estimation of the cyclic electron flux around photosystem I in leaves. Funct Plant Biol 45:1138–1148. https://doi.org/10.1071/FP18039
Article PubMed Google Scholar
Zivcak M, Brestic M, Kunderlikova K, Sytar O, Allakhverdiev SI (2015) Repetitive light pulse-induced photoinhibition of photo- system I severely affects CO₂ assimilation and photoprotection in wheat leaves. Photosynth Res 126:449–463. https://doi.org/10.1007/s11120-015-0121-1
Article PubMed Google Scholar

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Professor Barry Osmond recommended us as potential authors of a Progress in Botany article to Professor Ulrich Lüttge, who then kindly invited us to write this review and closely edit our drafts. We are grateful to both. We thank two reviewers Professors W.S. Chow and E. Tyystjärvi for critical reviews and useful suggestions. We incorporate their useful suggestions to this review, acknowledging their contributions. We also thank many colleagues for collaborations, discussions, and encouragements. Our photoinhibition studies have been only sporadically supported by the grants from the Japan Society for Promotion of Science (JSPS) and the Ministry of Education, Culture, Sports, and Technology (MEXT). Thus, two recent grants from MEXT (17H05718 and 19H04718) are appreciated. More importantly, we highly appreciate Continuous Ordinary Operating/Management Expenses Grants from our universities. Without these ordinary grants, our studies might have been interrupted or severely delayed. It is regrettable that the amount of such ordinary operating grants is gradually decreasing in Japan. This is due to the governmental policy to concentrate research grants to selected scientists, which obviously suppresses ordinary operations of ordinary scientists like us.

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Authors and Affiliations

Department of Biological Sciences, School of Science, The University of Tokyo, Tokyo, Japan
Masaru Kono & Ichiro Terashima
Botanical Gardens, Osaka Metropolitan University, Osaka, Japan
Riichi Oguchi

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Masaru Kono
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Riichi Oguchi
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Ichiro Terashima
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Correspondence to Masaru Kono or Ichiro Terashima .

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Department of Biology, Technical University of Darmstadt, Darmstadt, Germany
Ulrich Lüttge
Department of Molecular Biology and Biochemistry, University of Málaga, Málaga, Spain
Francisco M. Cánovas
Pollen Biotechnology of Crop Plants Group, Centro de Investigaciones Biologicas “Margarita Salas” (CIB) CSIC, Madrid, Madrid, Spain
María-Carmen Risueño
Plant Ecology, University of Göttingen, Göttingen, Germany
Christoph Leuschner
Chair for Forest Growth and Yield Science, School of Life Sciences Weihenstephan, Technical University of Munich, Freising, Bayern, Germany
Hans Pretzsch

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Kono, M., Oguchi, R., Terashima, I. (2022). Photoinhibition of PSI and PSII in Nature and in the Laboratory: Ecological Approaches. In: Lüttge, U., Cánovas, F.M., Risueño, MC., Leuschner, C., Pretzsch, H. (eds) Progress in Botany Vol. 84. Progress in Botany, vol 84. Springer, Cham. https://doi.org/10.1007/124_2022_67

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DOI: https://doi.org/10.1007/124_2022_67
Published: 29 September 2022
Publisher Name: Springer, Cham
Print ISBN: 978-3-031-45753-1
Online ISBN: 978-3-031-45754-8
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