Fred Chow: the contributions of a quiet giant of photoinhibition and photoprotection
Alonso Zavafer
A B D and Douglas A. Campbell C
+ Author Affiliations
- Author Affiliations
A Research School of Biology, the Australian National University, Canberra, ACT 2600, Australia.
B Climate Change Cluster, University of Technology Sydney, Ultimo, NSW 2001, Australia.
C Mount Allison University, Sackville, NB E4L 1E2, New Brunswick, Canada.
D Corresponding author. Email: alonso.zavaleta@anu.edu.au
Functional Plant Biology - https://doi.org/10.1071/FP20337
Submitted: 29 October 2020 Accepted: 28 January 2021 Published online: 23 February 2021
Abstract
Wah Soon (Fred) Chow has been a major contributor to photosynthesis research since the late 20th century. Fred, a quiet, gentle, smart and prolific writer, has contributed to our understanding of thylakoid structure, cyclic electron flow and the development of novel methods for phenotyping plants. However, a third of his productivity centres on the understanding of photoinhibition and photoprotection, which we honour herein. We give a brief biographical account of his academic trajectory, followed by a chronological and conceptual summary of his contributions to the field of photodamage and photoprotection. We thereby hope to introduce the work of Fred to young readers and non-experts in the field of photoinhibition.
Keywords: photoinhibition, photosystem II, photodamage, P700, photosystem I.
References
Adams WW, III, Zarter CR, Mueh KE, Demmig-Adams B (2008) Energy dissipation and photoinhibition: a continuum of photoprotection. In ‘Photoprotection, photoinhibition, gene regulation, and environment. Vol. 21’. (Eds Demmig-Adams B, Adams, WW, III, Mattoo AK) pp. 49–64. (Springer: Dordrecht, Netherlands)Anderson JM, Park YI, Chow WS (1997) Photoinactivation and photoprotection of photosystem II in nature. Physiologia Plantarum 100, 214–223.
| Photoinactivation and photoprotection of photosystem II in nature.Crossref | GoogleScholarGoogle Scholar |
Anderson JM, Park Y-I, Chow WS (1998a) Is P680+ the dominant cause of photoinactivation of photosystem II in plants? In ‘Photosynthesis: mechanisms and effects. Vols I–V’. (Ed. Garab G) pp. 2115–2118. (Springer: Dordrecht, Netherlands)
Anderson JM, Park Y-I, Chow WS (1998b) Unifying model for the photoinactivation of Photosystem II in vivo under steady-state photosynthesis. Photosynthesis Research 56, 1–13.
| Unifying model for the photoinactivation of Photosystem II in vivo under steady-state photosynthesis.Crossref | GoogleScholarGoogle Scholar |
Aro EM, 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 |
Baena-González E, Aro EM (2002) Biogenesis, assembly and turnover of photosystem II units. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 357, 1451–1460.
| Biogenesis, assembly and turnover of photosystem II units.Crossref | GoogleScholarGoogle Scholar | 12437884PubMed |
Callahan FE, Cheniae GM (1985) Studies on the photoactivation of the water-oxidizing enzyme: I. Processes limiting photoactivation in hydroxylamine-extracted leaf segments. Plant Physiology 79, 777–786.
| Studies on the photoactivation of the water-oxidizing enzyme: I. Processes limiting photoactivation in hydroxylamine-extracted leaf segments.Crossref | GoogleScholarGoogle Scholar | 16664491PubMed |
Campbell DA, Serôdio J (2020) Photoinhibition of photosystem II in phytoplankton: processes and patterns. In ‘Photosynthesis in algae: biochemical and physiological mechanisms (including bioenergy and related processes. Vol. 45’. (Eds Larkum A, Grossman A, Raven J.) pp. 329–365. (Springer: Cham, Germany)
Campbell DA, Tyystjarvi E (2012) Parameterization of photosystem II photoinactivation and repair. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1817, 258–265.
| Parameterization of photosystem II photoinactivation and repair.Crossref | GoogleScholarGoogle Scholar |
Chow W (1994) Photoprotection and photoinhibitory damage. In ‘Advances in molecular and cell biology. Vol. 10’. (Eds Bittar EE, Barber J.) pp. 151–196. (Elsevier: Greenwich, CT)
Chow W, Hope A (1998a) Redox reactions in photoinhibited tobacco leaf segments. In ‘Photosynthesis: mechanisms and effects. Vols I–V’. (Ed. Garab G.) pp. 2123–2126. (Springer: Dordrecht, Netherlands)
Chow WS, Hope AB (1998b) The electrochromic signal, redox reactions in the cytochrome bf complex and photosystem functionality in photoinhibited tobacco leaf segments. Functional Plant Biology 25, 775–784.
| The electrochromic signal, redox reactions in the cytochrome bf complex and photosystem functionality in photoinhibited tobacco leaf segments.Crossref | GoogleScholarGoogle Scholar |
Chow WS, Osmond CB, Huang LK (1989) Photosystem II function and herbicide binding sites during photoinhibition of spinach chloroplasts in-vivo and in-vitro. Photosynthesis Research 21, 17–26.
Demmig-Adams B, Adams WW (1996) The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends in Plant Science 1, 21–26.
| The role of xanthophyll cycle carotenoids in the protection of photosynthesis.Crossref | GoogleScholarGoogle Scholar |
Demmig-Adams B, Adams WW, Heber U, Neimanis S, Winter K, Kruger A, Czygan FC, Bilger W, Bjorkman O (1990) Inhibition of zeaxanthin formation and of rapid changes in radiationless energy dissipation by dithiothreitol in spinach leaves and chloroplasts. Plant Physiology 92, 293–301.
| Inhibition of zeaxanthin formation and of rapid changes in radiationless energy dissipation by dithiothreitol in spinach leaves and chloroplasts.Crossref | GoogleScholarGoogle Scholar | 16667274PubMed |
Du Ysens LN (1989) The discovery of the two photosynthetic systems: a personal account. Photosynthesis Research 21, 61–79.
| The discovery of the two photosynthetic systems: a personal account.Crossref | GoogleScholarGoogle Scholar | 24424526PubMed |
Fan DY, Ye ZP, Wang SC, Chow WS (2016) Multiple roles of oxygen in the photoinactivation and dynamic repair of Photosystem II in spinach leaves. Photosynthesis Research 127, 307–319.
| Multiple roles of oxygen in the photoinactivation and dynamic repair of Photosystem II in spinach leaves.Crossref | GoogleScholarGoogle Scholar | 26297354PubMed |
Flexas J, Hendrickson L, Chow WS (2001) Photoinactivation of photosystem II in high light-acclimated grapevines. Functional Plant Biology 28, 755–764.
| Photoinactivation of photosystem II in high light-acclimated grapevines.Crossref | GoogleScholarGoogle Scholar |
Goltsev V, Yordanov I, Gurmanova M, Kouzmanova M, Dambov S, Apostolova S, Savova G, Strasser R (2010) Multifunctional plant efficiency analyzer mPEA used to describe the physiological states of the photosynthetic apparatus. Agrarni Nauki 2, 15–25.
| Multifunctional plant efficiency analyzer mPEA used to describe the physiological states of the photosynthetic apparatus.Crossref | GoogleScholarGoogle Scholar |
Hakala M, Tuominen I, Keranen M, Tyystjarvi T, Tyystjarvi 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 |
He J, Yang W, Qin L, Fan DY, Chow WS (2015) Photoinactivation of Photosystem II in wild-type and chlorophyll b-less barley leaves: which mechanism dominates depends on experimental circumstances. Photosynthesis Research 126, 399–407.
| Photoinactivation of Photosystem II in wild-type and chlorophyll b-less barley leaves: which mechanism dominates depends on experimental circumstances.Crossref | GoogleScholarGoogle Scholar | 26101037PubMed |
Hendrickson L, Ball MC, Osmond CB, Furbank RT, Chow WS (2003) Assessment of photoprotection mechanisms of grapevines at low temperature. Functional Plant Biology 30, 631–642.
| Assessment of photoprotection mechanisms of grapevines at low temperature.Crossref | GoogleScholarGoogle Scholar | 32689048PubMed |
Hendrickson L, Förster B, Furbank RT, Chow WS (2004) Processes contributing to photoprotection of grapevine leaves illuminated at low temperature. Physiologia Plantarum 121, 272–281.
| Processes contributing to photoprotection of grapevine leaves illuminated at low temperature.Crossref | GoogleScholarGoogle Scholar | 15153195PubMed |
Hendrickson L, Förster B, Pogson BJ, Chow WS (2005) A simple chlorophyll fluorescence parameter that correlates with the rate coefficient of photoinactivation of photosystem II. Photosynthesis Research 84, 43–49.
| A simple chlorophyll fluorescence parameter that correlates with the rate coefficient of photoinactivation of photosystem II.Crossref | GoogleScholarGoogle Scholar | 16049753PubMed |
Idedan I, Tomo T, Noguchi T (2011) Herbicide effect on the photodamage process of photosystem II: fourier transform infrared study. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1807, 1214–1220.
| Herbicide effect on the photodamage process of photosystem II: fourier transform infrared study.Crossref | GoogleScholarGoogle Scholar |
Iermak I, Szabo M, Zavafer A (2020) Special issue in honour of Prof. Reto J. Strasser–Analysis of OJIP transients during photoinactivation of photosystem II indicates the presence of multiple photosensitizers in vivo and in vitro. Photosynthetica 58, 497–506.
| Special issue in honour of Prof. Reto J. Strasser–Analysis of OJIP transients during photoinactivation of photosystem II indicates the presence of multiple photosensitizers in vivo and in vitro.Crossref | GoogleScholarGoogle Scholar |
Joliot P, Barbieri G, Chabaud R (1969) Un nouveau modele des centres photochimiques du systeme II. Photochemistry and Photobiology 10, 309–329.
| Un nouveau modele des centres photochimiques du systeme II.Crossref | GoogleScholarGoogle Scholar |
Jones LW, Kok B (1966) Photoinhibition of chloroplast reactions. I. Kinetics and action spectra. Plant Physiology 41, 1037–1043.
| Photoinhibition of chloroplast reactions. I. Kinetics and action spectra.Crossref | GoogleScholarGoogle Scholar | 16656345PubMed |
Key T, McCarthy A, Campbell DA, Six C, Roy S, Finkel ZV (2010) Cell size trade-offs govern light exploitation strategies in marine phytoplankton. Environmental Microbiology 12, 95–104.
| Cell size trade-offs govern light exploitation strategies in marine phytoplankton.Crossref | GoogleScholarGoogle Scholar | 19735282PubMed |
Kok B (1956) On the inhibition of photosynthesis by intense light. Biochimica et Biophysica Acta 21, 234–244.
| On the inhibition of photosynthesis by intense light.Crossref | GoogleScholarGoogle Scholar | 13363902PubMed |
Kok B, Forbush B, McGloin M (1970) Cooperation of charges in photosynthetic O2 evolution-I. A linear four step mechanism. Photochemistry and Photobiology 11, 457–475.
| Cooperation of charges in photosynthetic O2 evolution-I. A linear four step mechanism.Crossref | GoogleScholarGoogle Scholar | 5456273PubMed |
Kyle DJ, Ohad I, Arntzen CJ (1984) Membrane protein damage and repair: Selective loss of a quinone-protein function in chloroplast membranes. Proceedings of the National Academy of Sciences of the United States of America 81, 4070–4074.
| Membrane protein damage and repair: Selective loss of a quinone-protein function in chloroplast membranes.Crossref | GoogleScholarGoogle Scholar | 16593483PubMed |
Lee HY, Chow WS, Hong YN (1999) Photoinactivation of photosystem II in leaves of Capsicum annuum. Physiologia Plantarum 105, 376–383.
| Photoinactivation of photosystem II in leaves of Capsicum annuum.Crossref | GoogleScholarGoogle Scholar |
Lee HY, Hong YN, Chow WS (2001) Photoinactivation of photosystem II complexes and photoprotection by non-functional neighbours in Capsicum annuum L. leaves. Planta 212, 332–342.
| Photoinactivation of photosystem II complexes and photoprotection by non-functional neighbours in Capsicum annuum L. leaves.Crossref | GoogleScholarGoogle Scholar | 11289597PubMed |
Lee HY, Hong YN, Chow WS (2002) Putative effects of pH in intra-chloroplast compartments on photoprotection of functional photosystem II complexes by photoinactivated neighbours and on recovery from photoinactivation in Capsicum annuum leaves. Functional Plant Biology 29, 607–619.
| Putative effects of pH in intra-chloroplast compartments on photoprotection of functional photosystem II complexes by photoinactivated neighbours and on recovery from photoinactivation in Capsicum annuum leaves.Crossref | GoogleScholarGoogle Scholar | 32689506PubMed |
Liu L-X, Chow WS, Anderson JM (1993) Light quality during growth of Tradescantia albiflora regulates photosystem stoichiometry, photosynthetic function and susceptibility to photoinhibition. Physiologia Plantarum 89, 854–860.
| Light quality during growth of Tradescantia albiflora regulates photosystem stoichiometry, photosynthetic function and susceptibility to photoinhibition.Crossref | GoogleScholarGoogle Scholar |
Losciale P, Oguchi R, Hendrickson L, Hope AB, Corelli-Grappadelli L, Chow WS (2008) A rapid, whole-tissue determination of the functional fraction of PSII after photoinhibition of leaves based on flash-induced P700 redox kinetics. Physiologia Plantarum 132, 23–32.
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.
| Populations of photoinactivated photosystem II reaction centers characterized by chlorophyll a fluorescence lifetime in vivo.Crossref | GoogleScholarGoogle Scholar | 15601775PubMed |
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 & 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 |
Murphy CD, Roodvoets MS, Austen EJ, Dolan A, Barnett A, Campbell DA (2017) Photoinactivation of Photosystem II in Prochlorococcus and Synechococcus. PLoS One 12, e0168991
| Photoinactivation of Photosystem II in Prochlorococcus and Synechococcus.Crossref | GoogleScholarGoogle Scholar | 28129341PubMed |
Neale P, Pritchard A, Ihnacik R (2014) UV effects on the primary productivity of picophytoplankton: biological weighting functions and exposure response curves of Synechococcus. Biogeosciences 11, 2883
| UV effects on the primary productivity of picophytoplankton: biological weighting functions and exposure response curves of Synechococcus.Crossref | GoogleScholarGoogle Scholar |
Neilson JA, Durnford DG (2010) Structural and functional diversification of the light-harvesting complexes in photosynthetic eukaryotes. Photosynthesis Research 106, 57–71.
| Structural and functional diversification of the light-harvesting complexes in photosynthetic eukaryotes.Crossref | GoogleScholarGoogle Scholar | 20596891PubMed |
Nishiyama Y, Murata N (2014) Revised scheme for the mechanism of photoinhibition and its application to enhance the abiotic stress tolerance of the photosynthetic machinery. Applied Microbiology and Biotechnology 98, 8777–8796.
| Revised scheme for the mechanism of photoinhibition and its application to enhance the abiotic stress tolerance of the photosynthetic machinery.Crossref | GoogleScholarGoogle Scholar | 25139449PubMed |
Nishiyama Y, Allakhverdiev SI, Yamamoto H, Hayashi H, Murata N (2004) Singlet oxygen inhibits the repair of photosystem II by suppressing the translation elongation of the D1 protein in Synechocystis sp. PCC 6803. Biochemistry 43, 11321–11330.
| Singlet oxygen inhibits the repair of photosystem II by suppressing the translation elongation of the D1 protein in Synechocystis sp. PCC 6803.Crossref | GoogleScholarGoogle Scholar | 15366942PubMed |
Nishiyama Y, Allakhverdiev SI, Murata N (2005) Inhibition of the repair of photosystem II by oxidative stress in cyanobacteria. Photosynthesis Research 84, 1–7.
| Inhibition of the repair of photosystem II by oxidative stress in cyanobacteria.Crossref | GoogleScholarGoogle Scholar | 16049747PubMed |
Nishiyama Y, Allakhverdiev SI, Murata N (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1757, 742–749.
| A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II.Crossref | GoogleScholarGoogle 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 Physiology 50, 1815–1825.
| The involvement of dual mechanisms of photoinactivation of photosystem II in Capsicum annuum L. Plants.Crossref | GoogleScholarGoogle 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 Phytologist 191, 146–159.
| 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.Crossref | GoogleScholarGoogle 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. Physiologia Plantarum 142, 47–55.
| Operation of dual mechanisms that both lead to photoinactivation of Photosystem II in leaves by visible light.Crossref | GoogleScholarGoogle Scholar | 21288248PubMed |
Ohad I, Berg A, Berkowicz SM, Kaplan A, Keren N (2011) Photoinactivation of photosystem II: is there more than one way to skin a cat? Physiologia Plantarum 142, 79–86.
| Photoinactivation of photosystem II: is there more than one way to skin a cat?Crossref | GoogleScholarGoogle Scholar | 21382038PubMed |
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 |
Öquist G, Chow WS (1992) On the relationship between the quantum yield of Photosystem II electron transport, as determined by chlorophyll fluorescence and the quantum yield of CO2-dependent O 2 evolution. Photosynthesis Research 33, 51–62.
| On the relationship between the quantum yield of Photosystem II electron transport, as determined by chlorophyll fluorescence and the quantum yield of CO2-dependent O 2 evolution.Crossref | GoogleScholarGoogle Scholar | 24408447PubMed |
Öquist G, Anderson JM, McCaffery S, Chow WS (1992a) Mechanistic differences in photoinhibition of sun and shade plants. Planta 188, 422–431.
| Mechanistic differences in photoinhibition of sun and shade plants.Crossref | GoogleScholarGoogle Scholar | 24178333PubMed |
Öquist G, Chow WS, Anderson JM (1992b) Photoinhibition of photosynthesis represents a mechanism for the long-term regulation of photosystem II. Planta 186, 450–460.
| Photoinhibition of photosynthesis represents a mechanism for the long-term regulation of photosystem II.Crossref | GoogleScholarGoogle Scholar | 24186743PubMed |
Osmond C, Chow WS (1988) Ecology of photosynthesis in the sun and shade: summary and prognostications. Functional Plant Biology 15, 1–9.
| Ecology of photosynthesis in the sun and shade: summary and prognostications.Crossref | GoogleScholarGoogle Scholar |
Park Y-I, Chow WS, Anderson J (1995a) Light inactivation of functional photosystem II in leaves of peas grown in moderate light depends on photon exposure. Planta 196, 401–411.
| Light inactivation of functional photosystem II in leaves of peas grown in moderate light depends on photon exposure.Crossref | GoogleScholarGoogle Scholar |
Park Y, Chow WS, Anderson JM (1995b) The quantum yield of photoinactivation of photosystem II in pea leaves is greater at low than high photon exposure. Plant & Cell Physiology 36, 1163–1167.
| The quantum yield of photoinactivation of photosystem II in pea leaves is greater at low than high photon exposure.Crossref | GoogleScholarGoogle Scholar |
Park YI, Chow WS, Anderson JM (1996a) Chloroplast movement in the shade plant Tradescantia albiflora helps protect photosystem ii against light stress. Plant Physiology 111, 867–875.
| Chloroplast movement in the shade plant Tradescantia albiflora helps protect photosystem ii against light stress.Crossref | GoogleScholarGoogle Scholar | 12226333PubMed |
Park YI, Chow WS, Anderson JM, Hurry VM (1996b) Differential susceptibility of Photosystem II to light stress in light-acclimated pea leaves depends on the capacity for photochemical and non-radiative dissipation of light. Plant Science 115, 137–149.
| Differential susceptibility of Photosystem II to light stress in light-acclimated pea leaves depends on the capacity for photochemical and non-radiative dissipation of light.Crossref | GoogleScholarGoogle Scholar |
Park YI, Chow WS, Osmond CB, Anderson JM (1996c) Electron transport to oxygen mitigates against the photoinactivation of Photosystem II in vivo. Photosynthesis Research 50, 23–32.
| Electron transport to oxygen mitigates against the photoinactivation of Photosystem II in vivo.Crossref | GoogleScholarGoogle Scholar | 24271819PubMed |
Pfündel E, Klughammer C, Schreiber U (2008) Monitoring the effects of reduced PS II antenna size on quantum yields of photosystems I and II using the Dual-PAM-100 measuring system. PAM Application Notes 1, 21–24.
Platt T, Gallegos C, Harrison WG (1980) Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. Journal of Marine Research 38, 103–111.
Ragni M, Airs RL, Leonardos N, Geider RJ (2008) Photoinhibition of PSII in Emiliania huxleyi (Haptophyta) under high light stress: the roles of photoacclimation, photoprotection, and photorepair. Journal of Phycology 44, 670–683.
| Photoinhibition of PSII in Emiliania huxleyi (Haptophyta) under high light stress: the roles of photoacclimation, photoprotection, and photorepair.Crossref | GoogleScholarGoogle Scholar | 27041425PubMed |
Ragni M, Airs RL, Hennige SJ, Suggett DJ, Warner ME, Geider RJ (2010) PSII photoinhibition and photorepair in Symbiodinium (Pyrrhophyta) differs between thermally tolerant and sensitive phylotypes. Marine Ecology Progress Series 406, 57–70.
| PSII photoinhibition and photorepair in Symbiodinium (Pyrrhophyta) differs between thermally tolerant and sensitive phylotypes.Crossref | GoogleScholarGoogle Scholar |
Rast A, Heinz S, Nickelsen J (2015) Biogenesis of thylakoid membranes. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1847, 821–830.
| Biogenesis of thylakoid membranes.Crossref | GoogleScholarGoogle Scholar |
Raven JA (2011) The cost of photoinhibition. Physiologia Plantarum 142, 87–104.
| The cost of photoinhibition.Crossref | GoogleScholarGoogle Scholar | 21382037PubMed |
Rutherford AW, Heathcote P (1985) Primary photochemistry in photosystem-I. Photosynthesis Research 6, 295–316.
| Primary photochemistry in photosystem-I.Crossref | GoogleScholarGoogle Scholar | 24442951PubMed |
Shen YK, Chow WS, Park YI, Anderson JM (1996) Photoinactivation of photosystem II by cumulative exposure to short light pulses during the induction period of photosynthesis. Photosynthesis Research 47, 51–59.
| Photoinactivation of photosystem II by cumulative exposure to short light pulses during the induction period of photosynthesis.Crossref | GoogleScholarGoogle Scholar | 24301707PubMed |
Sinclair J, Park YI, Chow WS, Anderson JM (1996) Target theory and the photoinactivation of Photosystem II. Photosynthesis Research 50, 33–40.
| Target theory and the photoinactivation of Photosystem II.Crossref | GoogleScholarGoogle Scholar | 24271820PubMed |
Six C, Finkel ZV, Irwin AJ, Campbell DA (2007) Light variability illuminates niche-partitioning among marine picocyanobacteria. PLoS One 2, e1341
| Light variability illuminates niche-partitioning among marine picocyanobacteria.Crossref | GoogleScholarGoogle Scholar | 18092006PubMed |
Soitamo A, Havurinne V, Tyystjarvi E (2017) Photoinhibition in marine picocyanobacteria. Physiologia Plantarum 161, 97–108.
| Photoinhibition in marine picocyanobacteria.Crossref | GoogleScholarGoogle Scholar | 28370227PubMed |
Sun ZL, Lee HY, Matsubara S, Hope AB, Pogson BJ, Hong YN, Chow WS (2006) Photoprotection of residual functional photosystem II units that survive illumination in the absence of repair, and their critical role in subsequent recovery. Physiologia Plantarum 128, 415–424.
| Photoprotection of residual functional photosystem II units that survive illumination in the absence of repair, and their critical role in subsequent recovery.Crossref | GoogleScholarGoogle Scholar |
Sundby C, Chow WS, Anderson JM (1993) Effects on Photosystem II Function, Photoinhibition, and Plant Performance of the Spontaneous Mutation of Serine-264 in the Photosystem II Reaction Center D1 Protein in Triazine-Resistant Brassica napus L. Plant Physiology 103, 105–113.
| Effects on Photosystem II Function, Photoinhibition, and Plant Performance of the Spontaneous Mutation of Serine-264 in the Photosystem II Reaction Center D1 Protein in Triazine-Resistant Brassica napus L.Crossref | GoogleScholarGoogle Scholar | 12231917PubMed |
Szabó M, Larkum AW, Suggett DJ, Vass I, Sass L, Osmond B, Zavafer A, Ralph PJ, Chow WS (2017) Non-intrusive assessment of Photosystem II and Photosystem I in whole coral tissues. Frontiers in Marine Science 4, 269
| Non-intrusive assessment of Photosystem II and Photosystem I in whole coral tissues.Crossref | GoogleScholarGoogle Scholar |
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. In ‘International review of cell and molecular biology. Vol. 300’. (Ed. Jeon KW.) pp. 243–303. (Elsevier: Cambridge, MA)
Tyystjärvi E, Aro E-M (1996) The rate constant of photoinhibition, measured in lincomycin-treated leaves, is directly proportional to light intensity. Proceedings of the National Academy of Sciences of the United States of America 93, 2213–2218.
| The rate constant of photoinhibition, measured in lincomycin-treated leaves, is directly proportional to light intensity.Crossref | GoogleScholarGoogle Scholar | 11607639PubMed |
Vass I (2012) Molecular mechanisms of photodamage in the Photosystem II complex. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1817, 209–217.
| Molecular mechanisms of photodamage in the Photosystem II complex.Crossref | GoogleScholarGoogle Scholar |
Vass I, Styring S, Hundal T, Koivuniemi A, Aro E, Andersson B (1992) Reversible and irreversible intermediates during photoinhibition of photosystem II: stable reduced QA species promote chlorophyll triplet formation. Proceedings of the National Academy of Sciences of the United States of America 89, 1408–1412.
| Reversible and irreversible intermediates during photoinhibition of photosystem II: stable reduced QA species promote chlorophyll triplet formation.Crossref | GoogleScholarGoogle Scholar | 11607279PubMed |
Zavafer A, Cheah MH, Hillier W, Chow WS, Takahashi S (2015a) Photodamage to the oxygen evolving complex of photosystem II by visible light. Scientific Reports 5, 16363
| Photodamage to the oxygen evolving complex of photosystem II by visible light.Crossref | GoogleScholarGoogle Scholar | 26560020PubMed |
Zavafer A, Chow WS, Cheah MH (2015b) The action spectrum of Photosystem II photoinactivation in visible light. Journal of Photochemistry and Photobiology. B, Biology 152, 247–260.
| The action spectrum of Photosystem II photoinactivation in visible light.Crossref | GoogleScholarGoogle Scholar | 26298696PubMed |
Zavafer A, Koinuma W, Chow WS, Cheah MH, Mino H (2017) Mechanism of Photodamage of the Scientific Reports Oxygen Evolving Mn Cluster of Photosystem II by Excessive Light Energy. Scientific Reports 7, 7604
| Mechanism of Photodamage of the Scientific Reports Oxygen Evolving Mn Cluster of Photosystem II by Excessive Light Energy.Crossref | GoogleScholarGoogle Scholar | 28790352PubMed |
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 |
