Abstract
Oxygen reduction in chloroplasts in the light was discovered by (Mehler Arch Biochem Biophys 33:65–77, 1951) as production of hydrogen peroxide. Later, it was shown that the primary product of the oxygen reduction is superoxide radical produced in thylakoids by one-electron transfer from reduced components of photosynthetic electron transport chain to O2 molecule. For a long time, the formation of hydrogen peroxide was considered to be a result of disproportionation of superoxide radicals in chloroplast stroma. Here, we overview a growing number of evidence indicating on another one, additional to disproportionation, pathway of hydrogen peroxide formation in chloroplasts, namely its formation in thylakoid membrane due to reaction of superoxide radical generated in the membrane with the reduced plastoquinone molecule, plastohydroquinone. Since various components of photosynthetic electron transport chain (primarily photosystem I) can supply superoxide radicals to this reaction, we refer this two-step O2 photoreduction to H2O2 as a cooperative process. The significance of hydrogen peroxide production via this pathway for redox signaling and scavenging of reactive oxygen species is discussed.
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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. https://doi.org/10.1038/256599a0
Allen JF, Hall DO (1974) The relationship of oxygen uptake to electron transport in photosystem I of isolated chloroplasts: the role of superoxide and ascorbate. Biochem Biophys Res Commun 58:579–585. https://doi.org/10.1016/S0006-291X(74)80459-6
Allen JF, de Paula WBM, Puthiyaveetil S, Nield J (2011) A structural phylogenetic map for chloroplast photosynthesis. Trends Plant Science 16:645–655. https://doi.org/10.1016/j.tplants.2011.10.004
Anderson JM (1986) Photoregulation of the composition, function, and structure of thylakoid membranes. Annu Rev Plant Biol 37:93–136. https://doi.org/10.1146/annurev.pp.37.060186.000521
Asada K (1994) Production and action of active oxygen species in photosynthesis tissues. In: Foyer CH, Mullineaux PM (ed) Causes of photo-oxidative stress and amelioration of defense systems in plants. CRC Press, Boca Raton, pp 77–104
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 50:601–639. https://doi.org/10.1146/annurev.arplant.50.1.601
Asada K (2000) The water-water cycle as alternative photon and electron sinks. Philos Trans R Soc Lond B Biol Sci 355:1419–1431. https://doi.org/10.1098/rstb.2000.0703
Asada K, Kiso K (1973a) Initiation of aerobic oxidation of sulfite by illuminated spinach chloroplasts. Eur J Biochem 33:253–257. https://doi.org/10.1111/j.1432-1033.1973.tb02677.x
Asada K, Kiso K (1973b) The photo-oxidation of epinephrine by spinach chloroplasts and its inhibition by superoxide dismutase: evidence for the formation of superoxide radicals in chloroplasts. Agric Biol Chem 37:453–454. https://doi.org/10.1080/00021369.1973.10860693
Asada K, Nakano Y (1978) Affinity for oxygen in photoreduction of molecular oxygen and scavenging of hydrogen peroxide in spinach chloroplasts. Photochem Photobiol 28:917–920. https://doi.org/10.1111/j.1751-1097.1978.tb07040.x
Asada K, Takahashi M (1987) Production and scavenging of active oxygen in photosynthesis. In: Kyle DJ, Osmond CB, Arntzen CJ (eds) Photoinhibition. Elsevier, Amsterdam, The Netherlands, pp 227–287
Asada K, Kiso K, Yoshikawa K (1974) Univalent reduction of molecular oxygen by spinach chloroplasts on illumination. J Biol Chem 249:2175–2181. https://doi.org/10.1016/S0021-9258(19)42815-9
Asada K, Takahashi M, Hayakawa T 1983 Photoreduction of superoxide in membranes of chloroplast thylakoids and intrachloroplast distribution of superoxide dismutase. In: Cohen G, Greenwald (eds) Oxy radicals and their scavenger systems, Elsevier, Amsterdam, pp 240–245
Badger MR (1985) Photosynthetic oxygen exchange. Annu Rev Plant Physiology 36:27–53. https://doi.org/10.1146/annurev.pp.36.060185.000331
Bakh A, Shoda R (1902) Untersuchungen uber die Rolle der Peroxyde in der Chemie der lebenden Zelle. II. Ueber Peroxydbildung in der lebenden Zelle. Ber Dtsch Chem Ges 35:2466–2469
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. Biochim Biophys Acta 1817:1314–1321. https://doi.org/10.1016/j.bbabio.2012.02.036
Borisova-Mubarakshina MM, Ivanov BN, Vetoshkina DV, Lubimov VY, Fedorchuk TP, Naydov IA, Kozuleva MA, Rudenko NN, DallʹOsto L, Cazzaniga S, Bassi R (2015) Long-term acclimatory response to excess excitation energy: evidence for a role of hydrogen peroxide in the regulation of photosystem II antenna size. J Exp Bot 66:7151–7164. https://doi.org/10.1093/jxb/erv410
Borisova-Mubarakshina MM, Naydov IA, Ivanov BN (2018) Oxidation of the plastoquinone pool in chloroplast thylakoid membranes by superoxide anion radicals. FEBS Lett 592:3221–3228. https://doi.org/10.1002/1873-3468.13237
Borisova-Mubarakshina MM, Vetoshkina DV, Naydov IA, Rudenko NN, Zhurikova EM, Balashov NV, Ignatova LK, Fedorchuk TP, Ivanov BN (2020) Regulation of the size of photosystem II light harvesting antenna represents a universal mechanism of higher plant acclimation to stress conditions. Func Plant Biol 47:959–969. https://doi.org/10.1071/FP19362
Breeze E, Mullineaux PM (2022) The passage of H2O2 from chloroplasts to their associated nucleus during retrograde signalling: reflections on the role of the nuclearenvelope. Plants 11:552. https://doi.org/10.3390/plants11040552
Borisova-Mubarakshina, M. M., Naydov, I. A., Vetoshkina, D. V., Kozuleva, M. A., Vilyanen, D. V., Rudenko, N. N., & Ivanov, B. N. 2021 Photosynthetic antenna size regulation as an essential mechanism of higher plants acclimation to biotic and abiotic factors: the role of the chloroplast plastoquinone pool and hydrogen peroxide. In Vegetation index and dynamics. Intech Open doi: https://doi.org/10.5772/intechopen.97664
Cohen J, Arkhipov A, Braun R, Schulten K (2006) Imaging the migration pathways for O2, CO, NO, and Xe inside myoglobin. Biophys J 91:1844–1857. https://doi.org/10.1529/biophysj.106.085746
Crofts AR, Robinson HH, Snozzi M (1984) Reactions of quinols at catalytic sites: a diffusion role in H-transfer. In Sybesma C (ed) Advances in photosynthesis research. MNijhoff/Dr W Junk Publishers, The Hague, pp. 1.461–1.468.
Elstner EF, Kramer R (1973) Role of the superoxide free radical ion in photosynthetic ascorbate oxidation and ascorbate-mediated photophosphorylation. Biochim Biophys Acta 314:340–353. https://doi.org/10.1016/0005-2728(73)90118-7
Eskling M, Akerlund HE (1998) Changes in the quantities of violaxanthin de-epoxidase, xanthophylls and ascorbate in spinach upon shift from low to high light. Photosynth Res 57:41–50. https://doi.org/10.1023/A:1006015630167
Escoubas J-M, Lomas MW, Laroche J, Falkowski P (1995) Light intensity regulation of cab gene transcription is signaled by the redox state of the plastoquinone pool. PNAS USA 92:10237–10241. https://doi.org/10.1073/pnas.92.22.10237
Yan’shole VV, Kirilyuk IA, Grigor’ev IA, Morozov SV, Tsentalovich YuP (2010) Antioxidative properties of nitroxyl radicals and hydroxyamines in reactions with triplet and deaminated kynurenine. Russ Chem Bull 59:66–74. https://doi.org/10.1007/s11172-010-0046-y
Fantuzzi A, Allgower F, Baker H, McGuire G, Teh WK, Gamiz-Hernandez AP, Kaila VRI, Rutherford AW (2022) Bicarbonate-controlled reduction of oxygen by the QA semiquinone in photosystem II in membranes. PNAS 119:e2116063119. https://doi.org/10.1073/pnas.2116063119
Fey V, Wagner R, Braütigam K, Wirtz M, Hell R, Dietzmann A, Leister D, Oelmüller R, Pfannschmidt T (2005) Retrograde plastid redox signals in the expression of nuclear genes for chloroplast proteins of Arabidopsis thaliana. J Biol Chem 280:5318–5328. https://doi.org/10.1074/jbc.M406358200
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. J Biol Chem 281:38459–38465. https://doi.org/10.1074/jbc.M605119200
Foyer CH, Noctor GD (2009) Redox regulation in photosynthetic organisms: signalling, acclimation, and practical implications. Antioxidants Redox Signal 11:861–905. https://doi.org/10.1089/ars.2008.2177
Foyer CH, Rowell H, Walker DF (1983) Measurement of the ascorbate content of spinach leaves protoplasts and chloroplasts during illumination. Planta 157:239–244. https://doi.org/10.1007/BF00405188
Frigerio S, Campoli C, Zorzan S, Fantoni LI, Crosatti C, Drepper F, Haehnel W, Cattivelli L, Morosinotto T, Bassi R (2007) Photosynthetic antenna size in higher plants is controlled by the plastoquinone redox state at the post-transcriptional rather than transcriptional level. J Biol Chem 282:29457–29469. https://doi.org/10.1074/jbc.M705132200
Furbank RT, Badger MR (1983) Oxygen exchange associated with electron transport and photophosphorylation in spinach thylakoids. Biochim Biophys Acta 723:400–409. https://doi.org/10.1016/0005-2728(83)90047-6
Goetze DC, Carpentier R (1994) Ferredoxin–NADP+ reductase is the site of oxygen reduction in pseudocyclic electron transport. Can J Bot 72:256–260. https://doi.org/10.1139/b94-034
Golbeck JH, Kok B (1979) Redox titration of electron acceptor Q and the plastoquinone pool in Photosystem II. Biochim Biophys Acta 547:347–360. https://doi.org/10.1016/0005-2728(79)90016-1
Gotoh N, Niki E (1992) Rates of interactions of superoxide with vitamin E, vitamin C and related compounds as measured by chemiluminescence. Biochim Biophys Acta 1115:201–207. https://doi.org/10.1016/0304-4165(92)90054-x
Golbeck J, Radmer R (1984) Is the rate of oxygen uptake by reduced ferredoxin sufficient to account for photosystem I-mediated O2 reduction? In In Sybesma C (ed) Advances in photosynthesis research. M Nijhoff/Dr W Junk Publishers, The Hague, pp. 1.4.561–1.4.564
Greenstock CL, Miller RW (1975) Oxidation of Tiron by superoxide anion: kinetics of reaction in aqueous solution and in chloroplasts. Biochim Biophys Acta 396:11–16. https://doi.org/10.1016/0005-2728(75)90184-x
Harbour JR, Bolton JR (1975) Superoxide formation in spinach chloroplasts: electron spin resonance detection by spin trapping. Biochem Biophys Res Commun 64:803–807. https://doi.org/10.1016/0006-291X(75)90118-7
Hauska G, Hurt E, Gabellini N, Lockau W (1983) Comparative aspects of quinol-cytochrome c/plastocyanin oxidoreductases. Biochim Biophys Acta 726:97–133. https://doi.org/10.1016/0304-4173(83)90002-2
Heber U, French CS (1968) Effects of oxygen on the electron transport chain of photosynthesis. Planta 79:99–112. https://doi.org/10.1007/BF00390153
Ivanov BN, Red’ko TP, Shmeleva VL, Mukhin EN (1980) The role of ferredoxin in pseudocyclic electron transport in isolated pea chloroplasts. Biochem Mosc 45:1425–1432
Ivanov B, Mubarakshina M, Khorobrykh S (2007) Kinetics of the plastoquinone pool oxidation following illumination. Oxygen incorporation into photosynthetic electron transport chain. FEBS Lett 581:1342–1346. https://doi.org/10.1016/j.febslet.2007.02.044
Ivanov BN, Borisova-Mubarakshina MM, Kozuleva MA (2018) Formation mechanisms of superoxide radical and hydrogen peroxide in chloroplasts, and factors determining the signalling by hydrogen peroxide. Funct Plant Biol 45:102–110. https://doi.org/10.1071/FP16322
Ivanov B, Khorobrykh S (2003) Participation of photosynthetic electron transport in production and scavenging of reactive oxygen species. Antiox Redox Signal 5:43–54. https://doi.org/10.1089/152308603321223531
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. J Biol Chem 280:21295–21312. https://doi.org/10.1074/jbc.M501527200
Jung HS, Mockler TC (2014) A new alternative in plant retrograde signaling. Genome Biol 15:117. https://doi.org/10.1186/gb4178
Kaiser W (1976) The effect of hydrogen peroxide on CO2-fixation of isolated chloroplasts. Biochim Biophys Acta 440:476–482. https://doi.org/10.1016/0005-2728(76)90035-9
Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen G, Mullineaux P (1999) Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284:654–657. https://doi.org/10.1126/science.284.5414.654
Khorobrykh A (2019) Hydrogen peroxide and superoxide anion radical photoproduction in PSII preparations at various modifications of the water oxidizing complex. Plants 8:329. https://doi.org/10.3390/plants8090329
Khorobrykh SA, Ivanov BN (2002) Oxygen reduction in a plastoquinone pool of isolated pea thylakoids. Photosynth Res 71:209–219. https://doi.org/10.1023/A:1015583502345
Khorobrykh S, Tyystjärvi E (2018) Plastoquinol generates and scavenges reactive oxygen species in organic solvent: potential relevance for thylakoids. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1859:1119–1131. https://doi.org/10.1016/j.bbabio.2018.07.003
Konig J, Baier M, Horling F, Kahmann U, Harris G, Schurmann P, Dietz KJ (2002) The plant-specific function of 2-Cys peroxiredoxin-mediated detoxification of peroxides in the redox-hierarchy of photosynthetic electron flux. Proc Natl Acad Sci USA 99:5738–5743. https://doi.org/10.1073/pnas.072644999
Kozuleva MA, Ivanov BN (2010) Evaluation of the participation of ferredoxin in oxygen reduction in the photosynthetic electron transport chain of isolated pea thylakoids. Photosynth Res 105:51–61. https://doi.org/10.1007/s11120-010-9565-5
Kozuleva MA, Ivanov BN (2016) The mechanisms of oxygen reduction in the terminal reducing segment of the chloroplast photosynthetic electron transport chain. Plant Cell Physiol 57:1397–1404. https://doi.org/10.1093/pcp/pcw035
Kozuleva MA, Naidov IA, Mubarakshina MM, Ivanov BN (2007) Participation of ferredoxin in oxygen reduction by the photosynthetic electron transport chain. Biophysics 52:393–397. https://doi.org/10.1134/S0006350907040069
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 Lett 585:1067–1071. https://doi.org/10.1016/j.febslet.2011.03.004
Kozuleva MA, Petrova AA, Mamedov MD, Semenov AYu, Ivanov BN (2014) O2 reduction by photosystem I involves phylloquinone under steady-state illumination. FEBS Lett 588:4364–4368. https://doi.org/10.1016/j.febslet.2014.10.003
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 Rad Biol Med 89:1014–1023. https://doi.org/10.1016/j.freeradbiomed.2015.08.016
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 Physiol 172:1480–1493. https://doi.org/10.1104/pp.16.01084
Kozuleva M, Petrova A, Milrad Y, Semenov A, Ivanov B, Redding KE, Yacoby I (2021) Phylloquinone is the principal Mehler reaction site within photosystem I in high light. Plant Physiol 186:1848–1858. https://doi.org/10.1093/plphys/kiab221
Kruk J, Karpinski S (2006) An HPLC-based method of estimation of the total redox state of plastoquinone in chloroplasts, the size of the photochemically active plastoquinone pool and its redox state in thylakoids of Arabidopsis. Biochim Biophys Acta 1757:1669–1675. https://doi.org/10.1016/j.bbabio.2006.08.004
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. Photosynth Res 62:273–279. https://doi.org/10.1023/A:1006374319191
Kruk J, Jemioła-Rzemińska M, Burda K et al (2003) Scavenging of superoxide generated in photosystem I by plastoquinol and other prenyllipids in thylakoid membranes. Biochemistry 42:8501–8505. https://doi.org/10.1021/bi034036q
Leo A, Hansch C, Elkins D (1971) Partition coefficients and their uses. Chem Revs 71:525–616. https://doi.org/10.1021/cr60274a001
Lindahl M, Yang D-H, Andersson B (1995) Regulatory proteolysis of the major light-harvesting chlorophyll a/b protein of photosystem II by a light-induced membrane-associated enzymic system. Eur J Biochem 231:503–509. https://doi.org/10.1111/j.1432-1033.1995.tb20725.x
McCauley SW, Melis A (1986) Quantitation of plastoquinone photoreduction in spinach chloroplasts. Photosynth Res 8:3–16. https://doi.org/10.1007/BF00028472
Mehler AH (1951) Studies on reactions of illuminated chloroplasts: I. Mechanism of the reduction of oxygen and other hill reagents. Arch Biochem Biophys 33:65–77
Melis A, Brown JS (1980) Stoichiometry of system I and system II reaction centers and of plastoquinone in different photosynthetic membranes. Proc Natl Acad Sci USA 77:4712–4716. https://doi.org/10.1073/pnas.77.8.4712
Milanovsky GE, Petrova AA, Cherepanov DA, Semenov AYu (2017) Kinetic modeling of electron transfer reactions in photosystem I complexes of various structures with substituted quinone acceptors. Photosynth Res 133:185–199. https://doi.org/10.1007/s11120-017-0366-y
Misra HP, Fridovich I (1971) The generation of superoixide radical during the autoxidation of ferredoxins. J Biol Chem 246:6886–6890
Miyake C, Schreiber U, Hormann H et al (1998) The FAD-enzyme monodehydroascorbate radical reductase mediates photoproduction of superoxide radicals in spinach thylakoid membranes. Plant Cell Physiol 39:821–829. https://doi.org/10.1093/oxfordjournals.pcp.a029440
Mubarakshina MM, Khorobrykh SA, Kozuleva MA, Ivanov BN (2006a) Intramembrane hydrogen peroxide production in the course of oxygen reduction in higher plant thylakoids. Doklady Biochem and Biophys 408:118–121
Mubarakshina M, Khorobrykh S, Ivanov B (2006b) Oxygen reduction in chloroplast thylakoids results in production of hydrogen peroxide inside the membrane. Biochim Biophys Acta 1757:1496–1503. https://doi.org/10.1016/j.bbabio.2006.09.004
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. J Exp Bot 61:3577–3587. https://doi.org/10.1093/jxb/erq171
Mullineaux PM, Karpinski S, Baker NR (2006) Spatial dependence for hydrogen peroxide-directed signalling in light-stressed plants. Plant Physiol 141:346–350. https://doi.org/10.1104/pp.106.078162
Naydov IA, Mudrik VA, Ivanov BN (2010) Lightinduced hydrogen peroxide dynamics in protoplasts from leaves of both wildtype Arabidopsis and its mutant deficient in ascorbate biosynthesis. Doklady Biochem Biophys 432:137–140. https://doi.org/10.1134/S1607672910030129
Naydov IA, Mubarakshina MM, Ivanov BN (2012) Formation kinetics and H2O2 distribution in chloroplasts and protoplasts of photosynthetic leaf cells of higher plants under illumination. Biochem Mosc 77:143–151. https://doi.org/10.1134/S0006297912020046
Nixon PJ, Rich PR (2006) Chlororespiratory pathways and their physiological significance. In: Wise RR, Hoober JK (eds) The structure and function of plastids. Springer, The Netherlands, pp 237–251
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 Cchloroplasts: detection by immuno-gold labeling after rapid freezing and substitution method. Plant Cell Physiol 36:565–573. https://doi.org/10.1093/oxfordjournals.pcp.a078795
Pfalz J, Liebers M, Hirth M, Grubler B, Holtzegel U, Schroter Y, Dietzel L, Pfannschmidt T (2012) Environmental control of plant nuclear gene expression by chloroplast redox signals. Front Plant Sci 3:257. https://doi.org/10.3389/fpls.2012.00257
Piippo M, Allahverdiyeva Y, Paakkarinen V, Suoranta UM, Battchikova N, Aro EM (2006) Chloroplast-mediated regulation of nuclear genes in Arabidopsis thaliana in the absence of light stress. Physiol Genomics 25:142–152. https://doi.org/10.1152/physiolgenomics.00256.2005
Pospíšil P (2012) Molecular mechanisms of production and scavenging of reactive oxygen species by photosystem II. Biochim Biophys Acta 1817:218–231. https://doi.org/10.1016/j.bbabio.2011.05.017
Ptushenko VV, Cherepanov DA, Krishtalik LI, Semenov AY (2008) Semi-continuum electrostatic calculations of redox potentials in photosystem I. Photosynth Res 97:55–74. https://doi.org/10.1007/s11120-008-9309-y
Rich PR, Harper R (1990) Partition coefficients of quinones and hydroquinones and their relation to biochemical reactivity. FEBS Lett 269:139–144. https://doi.org/10.1016/0014-5793(90)81139-F
Robinson JM (1988) Does O2 photoreduction occur within chloroplasts in vivo? Physiol. Plantarum 72:666–680. https://doi.org/10.1111/j.1399-3054.1988.tb09181.x
Santabarbara S, Bullock B, Rappaport F, Redding KE (2015) Controlling electron transfer between the two cofactor chains of photosystem I by the redox state of one of their components. Biophys J 108:1537–1547. https://doi.org/10.1016/j.bpj.2015.01.009
Semenov AY, Mamedov MD, Chamorovsky SK (2003) Photoelectric studies of the transmembrane charge transfer reactions in photosystem I pigment–protein complexes. FEBS Lett 553:223–228. https://doi.org/10.1016/S0014-5793(03)01032-9
Semenov AY, Mamedov MD, Chamorovsky SK (2006) Electrogenic reactions associated with electron transfer in photosystem I. In: Golbeck JH (ed) The light-driven plastocyanin. Springer, Netherlands, pp 319–338
Sewelam N, Jaspert N, Van Der Kelen K, Tognetti VB, Schmitz J, Frerigmann H, Stahl E, Zeier J, Van Breusegem F, Maurino VG (2014) Spatial H2O2 signaling specificity: H2O2 from chloroplasts and peroxisomes modulates the plant transcriptome differentially. Mol Plant 7:1191–1210. https://doi.org/10.1093/mp/ssu070
Shibamoto T, Kato Y, Nagao R, Yamazaki T, Tomo T, Watanabe T (2010) Species-dependence of the redox potential of the primary quinone electron acceptor QA in photosystem II verified by spectroelectrochemistry. FEBS Lett 584:1526–1530. https://doi.org/10.1016/j.febslet.2010.03.002
Shuvalov VA, Krasnovskii AA (1975) Study of photoreduction of oxygen by chloroplasts by method of luminol and chlorophyll chemiluminescence. Biochem Mosc 40:301–308
Suzuki N, Koussevitzky S, Mittler R, Miller G (2011) ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ 35:259–270. https://doi.org/10.1111/j.1365-3040.2011.02336.x
Tagawa K, Arnon DI (1962) Ferredoxins as electron carriers in photosynthesis and in the biological production and consumption of hydrogen gas. Nature 195:537–543. https://doi.org/10.1038/195537a0
Tagawa K, Arnon DI (1968) Oxidation-reduction potentials and stoichiometry of electron transfer in ferredoxins. Biochim Biophys Acta 153:602–613. https://doi.org/10.1016/0005-2728(68)90188-6
Takahashi M, Asada K (1982) Dependence of oxygen affinity for Mehler reaction on photochemical activity of chloroplast thylakoids. Plant Cell Physiol 23:1457–1461. https://doi.org/10.1093/oxfordjournals.pcp.a076495
Takahashi M, Asada K (1988) Superoxide production in aprotic interior of chloroplast thylakoids. Arch Biochem Biophys 267:714–722. https://doi.org/10.1016/0003-9861(88)90080-x
Trebst A, Wietoska H, Draber W, Knops HJ (1978) The inhibition of photosynthetic electron flow in chloroplasts by the dinitrophenylether of bromo-or iodo-nitrothymol. Zeitschrift Naturforsch C 33:919–927. https://doi.org/10.1515/znc-1978-11-1220
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. J Biol Life Sci 6:50–60. https://doi.org/10.5296/jbls.v6i2.7277
Vetoshkina DV, Ivanov BN, Khorobrykh SA, Proskuryakov II, Borisova-Mubarakshina MM (2017) Involvement of the chloroplast plastoquinone pool in the Mehler reaction. Physiol Plantarum 161:45–55. https://doi.org/10.1111/ppl.12560
Vetoshkina DV, Kozuleva MA, Terentyev VV, Zhurikova EM, Borisova-Mubarakshina MM, Ivanov BN (2019) Comparison of state transitions of the photosynthetic antennae in Arabidopsis and barley plants upon illumination with light of various intensity. Biochemistry (Moscow) 84:1065–1073. https://doi.org/10.1134/S0006297919090098
Vilyanen D, Naydov I, Ivanov B, Borisova-Mubarakshina M, Kozuleva M (2022) Inhibition of plastoquinol oxidation at the cytochrome b6f complex by dinitrophenylether of iodonitrothymol (DNP-INT) depends on irradiance and H+ uptake by thylakoid membranes. Biochim Biophys Acta. https://doi.org/10.1016/j.bbabio.2021.148506
Wardman P (1990) Bioreactive activation of quinones: redox properties and thiol reactivity. Free Radical Research Communs 8:219–229. https://doi.org/10.3109/10715769009053355
Wei Y, Dang X, Hu Sh (2004) Electrochemical properties of superoxide ion in aprotic media. Russian J Electrochem 40:400–404. https://doi.org/10.1023/B:RUEL.0000023930.50615.ab
Winterbourn CC, Metodiewa D (1994) The reaction of superoxide with reduced glutathione. Arch Biochem Biophys 314:284–290. https://doi.org/10.1006/abbi.1994.1444
Yang D-H, Andersson B, Aro E-M, Ohad I (2001) The redox state of the plastoquinone pool controls the level of the light-harvesting chlorophyll a/b binding protein complex II (LHC II) during photoacclimation. Photosynth Res 68:163–174. https://doi.org/10.1023/A:1011849919438
Yang J, Dungrawala H, Hua H, Manukyan A, Abraham L, Lane W, Mead H, Wright J, Schneider BL (2011) Cell size and growth rate are major determinants of replicative lifespan. Cell Cycle 10:144–55. https://doi.org/10.4161/cc.10.1.14455
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This work was supported by the State Scientific Program No. FMRM-2022–0015.
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Ivanov, B., Borisova-Mubarakshina, M., Vilyanen, D. et al. Cooperative pathway of O2 reduction to H2O2 in chloroplast thylakoid membrane: new insight into the Mehler reaction. Biophys Rev 14, 857–869 (2022). https://doi.org/10.1007/s12551-022-00980-4
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DOI: https://doi.org/10.1007/s12551-022-00980-4