Formation mechanisms of superoxide radical and hydrogen peroxide in chloroplasts, and factors determining the signalling by hydrogen peroxide
Boris N. Ivanov A B , Maria M. Borisova-Mubarakshina A and Marina A. Kozuleva A
+ Author Affiliations
- Author Affiliations
A Institute of Basic Biological Problems, Russian Academy of Sciences, Pushchino, 142290, Russia.
B Corresponding author. Email: ivboni@rambler.ru
This paper originates from a presentation at the Fourth International Symposium on Plant Signaling and Behavior, Komarov Botanical Institute RAS/Russian Science Foundation, Saint Petersburg, Russia, 19–23 June 2016.
Functional Plant Biology 45(2) 102-110 https://doi.org/10.1071/FP16322
Submitted: 18 September 2016 Accepted: 13 December 2016 Published: 3 February 2017
Abstract
Reduction of O2 molecule to superoxide radical, O2•−, in the photosynthetic electron transport chain is the first step of hydrogen peroxide, H2O2, production in chloroplasts in the light. The mechanisms of O2 reduction by ferredoxin, by the components of the plastoquinone pool, and by the electron transfer cofactors in PSI are analysed. The data indicating that O2•− and H2O2 can be produced both outside and within thylakoid membrane are presented. The H2O2 production in the chloroplast stroma is described as a result of either dismutation of O2•− or its reduction by stromal reductants. Formation of H2O2 within thylakoid membrane in the reaction of O2•− with plastohydroquinone is examined. The significance of both ways of H2O2 formation for specificity of the signal being sent by photosynthetic electron transport chain to cell adaptation systems is discussed.
Additional keywords: adaptation, photosynthesis, photosynthetic electron transport chain, reactive oxygen species.
References
Afanas’ev IB (1989) ‘Superoxide ion: chemistry and biological implications.’ (CRC Press: Boca Raton, FL, USA)Allen JF (1975) Oxygen reduction and optimum production of ATP in photosynthesis. Nature 256, 599–600.
| Oxygen reduction and optimum production of ATP in photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2MXls1SqsrY%3D&md5=b6ba6e06d74c589718bb3ddf0ae7a1c4CAS |
Allen JF (2002) Plastoquinone redox control of chloroplast thylakoid protein phosphorylation and distribution of excitation energy between photosystems: discovery, background, implications. Photosynthesis Research 73, 139–148.
| Plastoquinone redox control of chloroplast thylakoid protein phosphorylation and distribution of excitation energy between photosystems: discovery, background, implications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnsVGltb4%3D&md5=43556a8b3617905fb1a31e514224cc5fCAS |
Allen JF, Hall DO (1973) Superoxide reduction as a mechanism of ascorbate-stimulated oxygen-uptake by isolated chloroplasts. Biochemical and Biophysical Research Communications 52, 856–862.
| Superoxide reduction as a mechanism of ascorbate-stimulated oxygen-uptake by isolated chloroplasts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3sXks1elsr0%3D&md5=536d47cd399552e90d057ec7b9fea086CAS |
Allen JF, de Paula WBM, Puthiyaveetil S, Nield J (2011) A structural phylogenetic map for chloroplast photosynthesis. Trends in Plant Science 16, 645–655.
| A structural phylogenetic map for chloroplast photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFOhu7%2FK&md5=53eef47593715b8690bf45e4f5dc3ba1CAS |
Asada K (1994) Production and action of active oxygen species in photosynthesis tissues. In ‘Causes of photo-oxidative stress and amelioration of defense systems in plants’. (Eds CH Foyer, PM Mullineaux) pp. 77–104. (CRC Press: Boca Raton, FL, USA)
Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annual Review of Plant Physiology and Plant Molecular Biology 50, 601–639.
| The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXkt1yktr0%3D&md5=0a882839acf99e081c96a6c5c55c9ef4CAS |
Asada K, Kiso K (1973) The photo-oxidation of epinephrine by spinach chloroplasts and its inhibition by superoxide dismutase: evidence for the formation of superoxide radicals in chloroplasts. Agricultural and Biological Chemistry 37, 453–454.
| The photo-oxidation of epinephrine by spinach chloroplasts and its inhibition by superoxide dismutase: evidence for the formation of superoxide radicals in chloroplasts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3sXhsVGgsLo%3D&md5=8fa7f95e719d0a59906e2dff00479fa5CAS |
Asada K, Kiso K, Yoshikawa K (1974) Univalent reduction of molecular oxygen by spinach chloroplasts on illumination. Journal of Biological Chemistry 249, 2175–2181.
Badger MR (1985) Photosynthetic oxygen exchange. Annual Review of Plant Physiology 36, 27–53.
| Photosynthetic oxygen exchange.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXktlCrsbc%3D&md5=781e0dd279761e73207ecccbf508e4afCAS |
Badger MR, von Caemmerer S, Ruuska S, Nakano H (2000) Electron flow to oxygen in higher plants and algae: rates and control of direct photoreduction (Mehler reaction) and rubisco oxygenase. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 355, 1433–1446.
| Electron flow to oxygen in higher plants and algae: rates and control of direct photoreduction (Mehler reaction) and rubisco oxygenase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXovFKgsbg%3D&md5=4e85bbf40df3bb0f478c7d9f17f5aaa0CAS |
Baruah A, Simkova K, Apel K, Laloi C (2009) Arabidopsis mutants reveal multiple singlet oxygen signaling pathways involved in stress response and development. Plant Molecular Biology 70, 547–563.
| Arabidopsis mutants reveal multiple singlet oxygen signaling pathways involved in stress response and development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnt12nurc%3D&md5=678979e7dac7fb6009c83ad29e06b94dCAS |
Bode R, Ivanov AG, Hüner NPA (2016) Global transcriptome analyses provide evidence that chloroplast redox state contributes to intracellular as well as long-distance signalling in response to stress and acclimation in Arabidopsis. Photosynthesis Research 128, 287–312.
| Global transcriptome analyses provide evidence that chloroplast redox state contributes to intracellular as well as long-distance signalling in response to stress and acclimation in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XkvFGlt7k%3D&md5=f948f40371ee66182bb6d4bb72e76c9aCAS |
Borisova-Mubarakshina MM, Kozuleva MA, Rudenko NN, Naydov IA, Klenina IB, Ivanov BN (2012) Photosynthetic electron flow to oxygen and diffusion of hydrogen peroxide through the chloroplast envelope via aquaporins. Biochimica et Biophysica Acta 1817, 1314–1321.
| Photosynthetic electron flow to oxygen and diffusion of hydrogen peroxide through the chloroplast envelope via aquaporins.Crossref | GoogleScholarGoogle Scholar |
Borisova-Mubarakshina MM, Ivanov BN, Vetoshkina DV, Lubimov VY, Fedorchuk TP, Naydov IA, Kozuleva MA, Rudenko NN, Dall’Osto L, Cazzaniga S, Bassi R (2015) Long-term acclamatory response to excess excitation energy: evidence for a role of hydrogen peroxide in the regulation of photosystem II antenna size. Journal of Experimental Botany 66, 7151–7164.
| Long-term acclamatory response to excess excitation energy: evidence for a role of hydrogen peroxide in the regulation of photosystem II antenna size.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhtlWnt7nF&md5=7eda7e73e9339a825808211422820922CAS |
Dietz K-J, Turkan I, Krieger-Liszkay A (2016) Redox- and reactive oxygen species-dependent signaling into and out of the photosynthesizing chloroplast. Plant Physiology 171, 1541–1550.
| Redox- and reactive oxygen species-dependent signaling into and out of the photosynthesizing chloroplast.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhvVGlt7bK&md5=9a236ccebc1cb2d8cef6f28d495aa82fCAS |
Ding MQ, Hou PC, Shen X, Wang MJ, Deng SR, Sun J, Xiao F, Wang R, Zhou X, Lu C, Zhang D, Zheng X, Hu Z, Chen S (2010) Salt-induced expression of genes related to Na+/K+ and ROS homeostasis in leaves of salt-resistant and salt-sensitive poplar species. Plant Molecular Biology 73, 251–269.
| Salt-induced expression of genes related to Na+/K+ and ROS homeostasis in leaves of salt-resistant and salt-sensitive poplar species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXkvFKqsbs%3D&md5=d5b09e426d18f19e5643efa1b5a30936CAS |
Fork DC, Heber UW (1968) Studies on electron-transport reactions of photosynthesis in plastome mutants of Oenothera. Plant Physiology 43, 606–612.
| Studies on electron-transport reactions of photosynthesis in plastome mutants of Oenothera.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF1cXktFKrurc%3D&md5=61a3181be8e932c74aa85ee80a91f16fCAS |
Forquer I, Covian R, Bowman MK, Trumpower BL, Kramer DM (2006) Similar transition states mediate the Q-cycle and superoxide production by the cytochrome bc1 complex. Journal of Biological Chemistry 281, 38459–38465.
| Similar transition states mediate the Q-cycle and superoxide production by the cytochrome bc1 complex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht12msr%2FM&md5=d27c2054e78be3922a0718ba2f4f358dCAS |
Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxidants & Redox Signalling 11, 861–905.
| Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXitlWhsr0%3D&md5=edff1e61eb09d385c483b1131a201038CAS |
Furbank R, Badger M (1983) Oxygen exchange associated with electron transport and photophosphorilation in spinach thylakoids. Biochimica et Biophysica Acta 723, 400–409.
| Oxygen exchange associated with electron transport and photophosphorilation in spinach thylakoids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXks1Oksr8%3D&md5=6beccade4295b3e09b2a1cef42983a58CAS |
Golbeck J, Radmer R (1984) Is the rate of oxygen uptake by reduced ferredoxin sufficient to account for photosystem I-mediated O2 reduction? In ‘Advances in photosynthesis research’. (Ed. C Sybesma) pp. 1.4.561–1.4.564. (Dr W Junk Publishers: The Hague)
Gus’kova RA, Ivanov II, Kol’tover VK, Akhobadze VV, Rubin AB (1984) Permeability of bilayer lipid membranes for superoxide (O2 •–) radicals. Biochimica et Biophysica Acta 778, 579–585.
| Permeability of bilayer lipid membranes for superoxide (O2 •–) radicals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXhvFyjsw%3D%3D&md5=b7091a01a2dd7d169b8c9f3f1f0c4807CAS |
Heber U, Heldt HW (1981) The chloroplast envelope: structure, function, and role in leaf metabolism. Annual Review of Plant Physiology 32, 139–168.
| The chloroplast envelope: structure, function, and role in leaf metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXkt1WhsL8%3D&md5=7a2bd9aa678d555fd8e1ed9258d5cc28CAS |
Hofmann NR (2010) A new thioredoxin is involved in plastid gene expression. The Plant Cell 22, 1423
| A new thioredoxin is involved in plastid gene expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXptVegtLc%3D&md5=45371aa35e9edd354b7d5abd925f5f4fCAS |
Inoue K (2007) The chloroplast outer envelope membrane: the edge of light and excitement. Journal of Integrative Plant Biology 49, 1100–1111.
| The chloroplast outer envelope membrane: the edge of light and excitement.Crossref | GoogleScholarGoogle Scholar |
Ivanov BN (2008) Cooperation of photosystem I with the plastoquinone pool in oxygen reduction in higher plant chloroplasts. Biochemistry (Moscow) 73, 112–118.
| Cooperation of photosystem I with the plastoquinone pool in oxygen reduction in higher plant chloroplasts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXitFKgur0%3D&md5=ef3c50d0e2099f28f4592da2e34adff7CAS |
Ivanov BN (2014) Role of ascorbic acid in photosynthesis. Biochemistry (Moscow) 79, 282–289.
| Role of ascorbic acid in photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXksF2isrc%3D&md5=82e1887ca214e363c923059226f22b29CAS |
Ivanov BN, Red’ko TP, Shmeleva VL, Mukhin EN (1980) The role of ferredoxin in pseudocyclic electron transport in isolated pea chloroplasts. Biochemistry (Moscow) 45, 1425–1432.
Ivanov BN, Mubarakshina MM, Khorobrykh SA (2007) Kinetics of the plastoquinone pool oxidation following illumination. Oxygen incorporation into photosynthetic electron transport chain. FEBS Letters 581, 1342–1346.
| Kinetics of the plastoquinone pool oxidation following illumination. Oxygen incorporation into photosynthetic electron transport chain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjsVWns7w%3D&md5=ea4cbb9bd1705f37c9a4fd9bc038b34eCAS |
James AM, Cocheme HM, Smith RAJ, Murphy MP (2005) Interactions of mitochondria-targeted and untargeted ubiquinones with the mitochondrial respiratory chain and reactive oxygen species. Journal of Biological Chemistry 280, 21295–21312.
| Interactions of mitochondria-targeted and untargeted ubiquinones with the mitochondrial respiratory chain and reactive oxygen species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXks1elsLo%3D&md5=4a5851d968f05627f9186dcc9280e0d0CAS |
Khorobrykh SA, Ivanov BN (2002) Oxygen reduction in a plastoquinone pool of isolated pea thylakoids. Photosynthesis Research 71, 209–219.
| Oxygen reduction in a plastoquinone pool of isolated pea thylakoids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlslWjtbw%3D&md5=201286c8e669580e6c07955dc6b59faaCAS |
Khorobrykh S, Mubarakshina M, Ivanov B (2004) Photosystem I is not solely responsible for oxygen reduction in isolated thylakoids. Biochimica et Biophysica Acta 1657, 164–167.
| Photosystem I is not solely responsible for oxygen reduction in isolated thylakoids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltl2htLw%3D&md5=d8a5c4ed1c0ffad8108b26e1038bcb78CAS |
Khorobrykh S, Karonen M, Tyystjärvi E (2016) Reactions of reactive oxygen species with plastoquinone pool. In ‘17th International congress on photosynthesis research. Maastricht, The Netherlands. Abstract book’. p. 241.
Kozuleva MA, Ivanov BN (2010) Evaluation of the participation of ferredoxin in oxygen reduction in the photosynthetic electron transport chain of isolated pea thylakoids. Photosynthesis Research 105, 51–61.
| Evaluation of the participation of ferredoxin in oxygen reduction in the photosynthetic electron transport chain of isolated pea thylakoids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXntlGitLc%3D&md5=eea5a40fd7158d48a1a997070c977078CAS |
Kozuleva M, Ivanov B (2016) The mechanisms of oxygen reduction in the terminal reducing segment of the chloroplast photosynthetic electron transport chain. Plant & Cell Physiology 57, 1397–1404.
Kozuleva M, Klenina I, Proskuryakov I, Kirilyuk I, Ivanov B (2011) Production of superoxide in chloroplast thylakoid membranes: ESR study with cyclic hydroxylamines of different lipophilicity. FEBS Letters 585, 1067–1071.
| Production of superoxide in chloroplast thylakoid membranes: ESR study with cyclic hydroxylamines of different lipophilicity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXktF2gu7k%3D&md5=0c1d423228272ec83ede29ed109a10adCAS |
Kozuleva MA, Petrova AA, Mamedov MD, Semenov AYu, Ivanov BN (2014) O2 reduction by photosystem I involves phylloquinone under steady-state illumination. FEBS Letters 588, 4364–4368.
| O2 reduction by photosystem I involves phylloquinone under steady-state illumination.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhslCisbjM&md5=5b44084f9e0efff309adba939faa68d9CAS |
Kozuleva M, Klenina I, Mysin I, Kirilyuk I, Opanasenko V, Proskuryakov I, Ivanov B (2015) Quantification of superoxide radical production in thylakoid membrane using cyclic hydroxylamine. Free Radical Biology & Medicine 89, 1014–1023.
| Quantification of superoxide radical production in thylakoid membrane using cyclic hydroxylamine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhs1CqtLzN&md5=f65937e7f70c89b12951ca05bf0fd3e8CAS |
Kozuleva M, Goss T, Twachtmann M, Rudi K, Trapka J, Selinski J, Ivanov B, Garapathi P, Steinhoff H-J, Hase T, Scheibe R, Klare J, Hanke G (2016) Ferredoxin: NADP (H) oxidoreductase abundance and location influences redox poise and stress tolerance. Plant Physiology 172, 1480–1493.
| Ferredoxin: NADP (H) oxidoreductase abundance and location influences redox poise and stress tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXhs1Oqsr0%3D&md5=a54d525ce09ab59cbc27bc08f7c9580aCAS |
Krieger-Liszkay A (2005) Singlet oxygen production in photosynthesis. Journal of Experimental Botany 56, 337–346.
| Singlet oxygen production in photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXovVymsg%3D%3D&md5=0f7a8874b5132e8e640bee5a025ff9d0CAS |
Kruk J, Strzalka K (1999) Dark reoxidation of the plastoquinone pool is mediated by the low-potential form of cytochrome b-559 in spinach thylakoids. Photosynthesis Research 62, 273–279.
| Dark reoxidation of the plastoquinone pool is mediated by the low-potential form of cytochrome b-559 in spinach thylakoids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXivVKrs7s%3D&md5=9851369147afc6dbb8ba3997fd63ba85CAS |
Kruk J, Jemiola-Rzeminska M, Burda K, Schmid G, Strzalka K (2003) Scavenging of superoxide generated in photosystem I by plastoquinol and other prenyllipids in thylakoid membranes. Biochemistry 42, 8501–8505.
| Scavenging of superoxide generated in photosystem I by plastoquinol and other prenyllipids in thylakoid membranes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXks12nurs%3D&md5=5e6f7cd7779774bc74b602f3a84dfcbcCAS |
Leo A, Hansch C, Elkins D (1971) Partition coefficients and their uses. Chemical Reviews 71, 525–616.
| Partition coefficients and their uses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE38XivVansw%3D%3D&md5=b37a67b610b6a6798901d9b9c3204c67CAS |
Maroz A, Anderson RF, Smith RAJ, Murphy MP (2009) Reactivity of ubiquinone and ubiquinol with superoxide and the hydroperoxyl radical: implications for in vivo antioxidant activity. Free Radical Biology & Medicine 46, 105–109.
| Reactivity of ubiquinone and ubiquinol with superoxide and the hydroperoxyl radical: implications for in vivo antioxidant activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFamsbnJ&md5=a135692af0514e5bd972ec43d75c7588CAS |
McCauley SW, Melis A (1986) Quantitation of plastoquinone photoreduction in spinach chloroplasts. Photosynthesis Research 8, 3–16.
| Quantitation of plastoquinone photoreduction in spinach chloroplasts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28Xit1ait7k%3D&md5=e5bdf2abc68c5c0d4520f0317c88199bCAS |
Mehler AH (1951) Studies on reactivity of illuminated chloroplasts. Mechanism of the reduction of oxygen and other Hill reagents. Archives of Biochemistry and Biophysics 33, 65–77.
| Studies on reactivity of illuminated chloroplasts. Mechanism of the reduction of oxygen and other Hill reagents.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG38XovFGg&md5=10fb295fc35bd26aa0588e9f427d4be5CAS |
Miyake C, Asada K (1992) Thylakoid-bound ascorbate peroxidase in spinach chloroplasts and photoreduction of its primary oxidation product monodehydroascorbate radicals in thylakoids. Plant & Cell Physiology 33, 541–553.
Mubarakshina MM, Ivanov BN (2010) The production and scavenging of reactive oxygen species in the plastoquinone pool of chloroplast thylakoid membranes. Physiologia Plantarum 140, 103–110.
| The production and scavenging of reactive oxygen species in the plastoquinone pool of chloroplast thylakoid membranes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1ejurnM&md5=c5844d40f99946f0eb4f07ad8c26acb8CAS |
Mubarakshina M, Khorobrykh S, Ivanov B (2006) Oxygen reduction in chloroplast thylakoids results in production of hydrogen peroxide inside the membrane. Biochimica et Biophysica Acta 1757, 1496–1503.
| Oxygen reduction in chloroplast thylakoids results in production of hydrogen peroxide inside the membrane.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFKmtL3E&md5=f83ddd6db768c2345d24cb2164f66336CAS |
Mubarakshina MM, Ivanov BN, Naydov IA, Hillier W, Badger MR, Krieger-Liszkay A (2010) Production and diffusion of chloroplastic H2O2 and its implication to signalling. Journal of Experimental Botany 61, 3577–3587.
| Production and diffusion of chloroplastic H2O2 and its implication to signalling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVert7jI&md5=5f735be960966543f5a9323759b3d69fCAS |
Mullineaux PM (2009) ROS in retrograde signalling from the chloroplast to the nucleus. In ‘Reactive oxygen species in plant signaling. Signaling and communication in plants’. (Eds LA Rio, A Puppo) pp. 221–240. (Springer-Verlag: Berlin)
Netto LES, Antunes F (2016) The roles of peroxiredoxin and thioredoxin in hydrogen peroxide sensing and in signal transduction. Molecules and Cells 39, 65–71.
| The roles of peroxiredoxin and thioredoxin in hydrogen peroxide sensing and in signal transduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XmvFGksLc%3D&md5=5ec9af34d002faa9b7f074e0b5a01114CAS |
Nilsson J, Erikson L, Laaksonen A (2001) Molecular dynamics simulations of plastoquinone in solution. Molecular Physics 99, 247–253.
| Molecular dynamics simulations of plastoquinone in solution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhs1KjtrY%3D&md5=92071802d5ce608d6d655c6ac8f9ab7fCAS |
Nishiyama Y, Allakhverdiev SI, Murata N (2011) Protein synthesis is the primary target of reactive oxygen species in the photoinhibition of photosystem II. Physiologia Plantarum 142, 35–46.
| Protein synthesis is the primary target of reactive oxygen species in the photoinhibition of photosystem II.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlsFWhsL8%3D&md5=9eb5a13f97f6fb38a6915cc17bb52f11CAS |
Nixon PJ, Rich PR (2006) Chlororespiratory pathways and their physiological significance. In ‘The structure and function of plastids’. (Eds RR Wise, JK Hoober) pp. 237–251. (Springer: Dordrecht, The Netherlands)
Ogawa K, Kanematsu S, Takabe K, Asada K (1995) Attachment of CuZn-superoxide dismutase to thylakoid membranes at the site of superoxide generation (PSI) in spinach chloroplasts: detection by immuno-gold labelling after rapid freezing and substitution method. Plant & Cell Physiology 36, 565–573.
Pfannschmidt T, Nilsson A, Allen JF (1999) Photosynthetic control of chloroplast gene expression. Nature 397, 625–628.
| Photosynthetic control of chloroplast gene expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhtlyiur4%3D&md5=0ebfbdc107c92daad496240e5933dbb3CAS |
Pospíšil P (2012) Molecular mechanisms of production and scavenging of reactive oxygen species by photosystem II. Biochimica et Biophysica Acta 1817, 218–231.
| Molecular mechanisms of production and scavenging of reactive oxygen species by photosystem II.Crossref | GoogleScholarGoogle Scholar |
Ptushenko VV, Cherepanov DA, Krishtalik LI, Semenov AY (2008) Semi-continuum electrostatic calculations of redox potentials in photosystem I. Photosynthesis Research 97, 55–74.
| Semi-continuum electrostatic calculations of redox potentials in photosystem I.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXptVKlsLk%3D&md5=32d651395b67535f232cee1e0c4ca1eaCAS |
Rich PR, Harper R (1990) Partition coefficients of quinones and hydroquinones and their relation to biochemical reactivity. FEBS Letters 269, 139–144.
| Partition coefficients of quinones and hydroquinones and their relation to biochemical reactivity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXmt1KksLY%3D&md5=6b4ec67ced8cdcc0ad02efb01acc2133CAS |
Scarpeci TE, Zanor MI, Carrillo N, Mueller-Roeber B, Valle EM (2008) Generation of superoxide anion in chloroplasts of Arabidopsis thaliana during active photosynthesis: a focus on rapidly induced genes. Plant Molecular Biology 66, 361–378.
| Generation of superoxide anion in chloroplasts of Arabidopsis thaliana during active photosynthesis: a focus on rapidly induced genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsl2msbg%3D&md5=3524c1e13ed154d4de7e81914b56df07CAS |
Scheibe R, Dietz K-J (2012) Reduction–oxidation network for flexible adjustment of cellular metabolism in photoautotrophic cells. Plant, Cell & Environment 35, 202–216.
| Reduction–oxidation network for flexible adjustment of cellular metabolism in photoautotrophic cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjtVKns7g%3D&md5=d114d49f9ab80d7a74fafcb10fe05dc1CAS |
Semenov AY, Vassiliev IR, van der Est A, Mamedov MD, Zybailov B, Shen G, Stehlik D, Diner BA, Chitnis PR, Golbeck JH (2000) Recruitment of a foreign quinone into the A1 site of photosystem I. Altered kinetics of electron transfer in phylloquinone biosynthetic pathway mutants studied by time-resolved optical, EPR, and electrometric techniques. Journal of Biological Chemistry 275, 23429–23438.
| Recruitment of a foreign quinone into the A1 site of photosystem I. Altered kinetics of electron transfer in phylloquinone biosynthetic pathway mutants studied by time-resolved optical, EPR, and electrometric techniques.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXls12mtrs%3D&md5=49b35be7d304e1dbd964d2d0db32317fCAS |
Shinkarev VP, Vassiliev IR, Golbeck JH (2000) A kinetic assessment of the sequence of electron transfer from F X to F A and further to F B in photosystem I: the value of the equilibrium constant between F X and F A. Biophysical Journal 78, 363–372.
| A kinetic assessment of the sequence of electron transfer from F X to F A and further to F B in photosystem I: the value of the equilibrium constant between F X and F A.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXktFeqsg%3D%3D&md5=709d2e88acf9edefc5626f044e2863abCAS |
Suzuki N, Koussevitzky S, Mittler R, Miller G (2012) ROS and redox signalling in the response of plants to abiotic stress. Plant, Cell & Environment 35, 259–270.
| ROS and redox signalling in the response of plants to abiotic stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjtVKnsL0%3D&md5=b63f29478270ca5abb4b2cca2c3ff07eCAS |
Svintitskikh VA, Andrianov VK, Bulychev AA (1985) Photo-induced H+ transport between chloroplasts and the cytoplasm in a protoplasmic droplet of characeae. Journal of Experimental Botany 36, 1414–1429.
| Photo-induced H+ transport between chloroplasts and the cytoplasm in a protoplasmic droplet of characeae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXlslGlsr0%3D&md5=5851a67760515c5a435a8e3c3e04fc59CAS |
Takahashi M, Asada K (1983) Superoxide anion permeability of phospholipids membranes and chloroplast thylakoids. Archives of Biochemistry and Biophysics 226, 558–566.
| Superoxide anion permeability of phospholipids membranes and chloroplast thylakoids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXlslWltLo%3D&md5=093e4a8d702664c472db73431ff1928dCAS |
Takahashi M, Asada K (1988) Superoxide production in aprotic interior of chloroplast thylakoids. Archives of Biochemistry and Biophysics 267, 714–722.
| Superoxide production in aprotic interior of chloroplast thylakoids.Crossref | GoogleScholarGoogle Scholar |
Turrens JF, Alexandre A, Lehninger AL (1985) Ubisemiquinone is the electron donor for superoxide formation by complex III of heart mitochondria. Archives of Biochemistry and Biophysics 237, 408–414.
| Ubisemiquinone is the electron donor for superoxide formation by complex III of heart mitochondria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXht1Ontrg%3D&md5=d8dff25091bb1014800275c131adab6aCAS |
Vetoshkina DV, Borisova-Mubarakshina MM, Naydov IA, Kozuleva MA, Ivanov BN (2015) Impact of high light on reactive oxygen species production within photosynthetic biological membranes. Journal of Biology and Life Science 6, 50–60.
| Impact of high light on reactive oxygen species production within photosynthetic biological membranes.Crossref | GoogleScholarGoogle Scholar |
Wardman P (1990) Bioreactive activation of quinones: redox properties and thiol reactivity. Free Radical Research Communications 8, 219–229.
| Bioreactive activation of quinones: redox properties and thiol reactivity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXktVais7g%3D&md5=71782bb97f19169439fd61ad48592b8cCAS |
