Singlet oxygen (1O2) is formed by triplet-triplet energy transfer from triplet chlorophyll to O2 via Type II photosensitization reaction in photosystem II (PSII). Formation of triplet chlorophyll is associated with the change in spin state of the excited electron and recombination of triplet radical pair in the PSII antenna complex and reaction center, respectively. Here, we have provided evidence for the formation of 1O2 by decomposition of protein hydroperoxide in PSII membranes deprived of Mn4O5Ca complex. Protein hydroperoxide is formed by protein oxidation initiated by highly oxidizing chlorophyll cation radical and hydroxyl radical formed by Type I photosensitization reaction. Under highly oxidizing conditions, protein hydroperoxide is oxidized to protein peroxyl radical which either cyclizes to dioxetane or recombines with another protein peroxyl radical to tetroxide. These highly unstable intermediates decompose to triplet carbonyls which transfer energy to O2 forming 1O2. Data presented in this study show for the first time that 1O2 is formed by decomposition of protein hydroperoxide in PSII membranes deprived of Mn4O5Ca complex.

Department of Biophysics Centre of the Region Haná for Biotechnological and Agricultural Research Faculty of Science Palacký University Olomouc Czech Republic

Zobrazit více v PubMed

Vinyard DJ, Ananyev GM, Dismukes GC. Photosystem II: The Reaction Center of Oxygenic Photosynthesis. Annual Review of Biochemistry, Vol 82. 2013;82:577–606. doi: 10.1146/annurev-biochem-070511-100425 PubMed DOI

Shen JR. The Structure of Photosystem II and the Mechanism of Water Oxidation in Photosynthesis. In: Merchant SS, editor. Annu Rev Plant Biol. Annual Review of Plant Biology. 66 Palo Alto: Annual Reviews; 2015. p. 23–48. doi: 10.1146/annurev-arplant-050312-120129 PubMed DOI

Nelson N, Junge W. Structure and Energy Transfer in Photosystems of Oxygenic Photosynthesis. Annual Review of Biochemistry, Vol 84. 2015;84:659–83. doi: 10.1146/annurev-biochem-092914-041942 PubMed DOI

van Amerongen H, Croce R. Light harvesting in photosystem II. Photosynthesis Research. 2013;116(2–3):251–63. doi: 10.1007/s11120-013-9824-3 PubMed DOI PMC

Wobbe L, Bassi R, Kruse O. Multi-Level Light Capture Control in Plants and Green Algae. Trends in Plant Science. 2016;21(1):55–68. doi: 10.1016/j.tplants.2015.10.004 PubMed DOI

Rappaport F, Diner BA. Primary photochemistry and energetics leading to the oxidation of the (Mn)4Ca cluster and to the evolution of molecular oxygen in Photosystem II. Coordination Chemistry Reviews. 2008;252(3–4):259–72. doi: 10.1016/j.ccr.2007.07.016 DOI

Nadtochenko VA, Semenov AY, Shuvalov VA. Formation and decay of P680 (PD1–PD2)+PheoD1− radical ion pair in photosystem II core complexes. Biochimica et Biophysica Acta (BBA)—Bioenergetics. 2014;1837(9):1384–8. http://dx.doi.org/10.1016/j.bbabio.2014.01.026. PubMed DOI

Cardona T, Sedoud A, Cox N, Rutherford AW. Charge separation in Photosystem II: A comparative and evolutionary overview. Biochimica Et Biophysica Acta-Bioenergetics. 2012;1817(1):26–43. doi: 10.1016/j.bbabio.2011.07.012 PubMed DOI

Grundmeier A, Dau H. Structural models of the manganese complex of photosystem II and mechanistic implications. Biochimica Et Biophysica Acta-Bioenergetics. 2012;1817(1):88–105. doi: 10.1016/j.bbabio.2011.07.004 PubMed DOI

Perez-Navarro M, Neese F, Lubitz W, Pantazis DA, Cox N. Recent developments in biological water oxidation. Current Opinion in Chemical Biology. 2016;31:113–9. doi: 10.1016/j.cbpa.2016.02.007 PubMed DOI

Yano J, Yachandra V. Mn4Ca Cluster in Photosynthesis: Where and How Water is Oxidized to Dioxygen. Chemical reviews. 2014;114(8):4175–205. doi: 10.1021/cr4004874 PubMed DOI PMC

Chatterjee R, Han G, Kern J, Gul S, Fuller FD, Garachtchenko A, et al. Structural changes correlated with magnetic spin state isomorphism in the S2 state of the Mn4CaO5 cluster in the oxygen-evolving complex of photosystem II. Chemical Science. 2016;7(8):5236–48. doi: 10.1039/C6SC00512H PubMed DOI PMC

Bao H, Burnap RL. Photoactivation: The Light-Driven Assembly of the Water Oxidation Complex of Photosystem II. Frontiers in Plant Science. 2016;7:13. PubMed PMC

Tyystjarvi E. Photoinhibition of Photosystem II. In: Jeon KW, editor. Intenational Review of Cell and Molecular Biology, Vol 300 International Review of Cell and Molecular Biology. 300. San Diego: Elsevier Academic Press Inc; 2013. p. 243–303. PubMed

Yadav DK, Pospíšil P. Evidence on the Formation of Singlet Oxygen in the Donor Side Photoinhibition of Photosystem II: EPR Spin-Trapping Study. Plos One. 2012;7(9). doi: 10.1371/journal.pone.0045883 PubMed DOI PMC

Yanykin DV, Khorobrykh AA, Khorobrykh SA, Klimov VV. Photoconsumption of molecular oxygen on both donor and acceptor sides of photosystem II in Mn-depleted subchloroplast membrane fragments. Biochimica Et Biophysica Acta-Bioenergetics. 2010;1797(4):516–23. doi: 10.1016/j.bbabio.2010.01.014 PubMed DOI

Davies MJ. Protein oxidation and peroxidation. Biochemical Journal. 2016;473:805–25. doi: 10.1042/BJ20151227 PubMed DOI PMC

Farmer EE, Mueller MJ. ROS-Mediated Lipid Peroxidation and RES-Activated Signaling. Annu Rev Plant Biol. 2013;64:429–50. doi: 10.1146/annurev-arplant-050312-120132 PubMed DOI

Khorobrykh SA, Khorobrykh AA, Yanykin DV, Ivanov BN, Klimov VV, Mano J. Photoproduction of Catalase-Insensitive Peroxides on the Donor Side of Manganese-Depleted Photosystem II: Evidence with a Specific Fluorescent Probe. Biochemistry. 2011;50(49):10658–65. doi: 10.1021/bi200945v PubMed DOI

Khorobrykh AA, Klimov VV. Involvement of molecular oxygen in the donor-side photoinhibition of Mn-depleted photosystem II membranes. Photosynthesis Research. 2015;126(2–3):417–25. doi: 10.1007/s11120-015-0135-8 PubMed DOI

Triantaphylides C, Havaux M. Singlet oxygen in plants: production, detoxification and signaling. Trends Plant Sci. 2009;14(4):219–28. Epub 2009/03/24. S1360-1385(09)00072-7 [pii] doi: 10.1016/j.tplants.2009.01.008 . PubMed DOI

Pospíšil P. Molecular mechanisms of production and scavenging of reactive oxygen species by photosystem II. Biochim Biophys Acta. 2012;1817(1):218–31. doi: 10.1016/j.bbabio.2011.05.017 . PubMed DOI

Fischer BB, Hideg E, Krieger-Liszkay A. Production, Detection, and Signaling of Singlet Oxygen in Photosynthetic Organisms. Antioxidants & Redox Signaling. 2013;18(16):2145–62. doi: 10.1089/ars.2012.5124 PubMed DOI

Telfer A. Singlet Oxygen Production by PSII Under Light Stress: Mechanism, Detection and the Protective role of beta-Carotene. Plant and Cell Physiology. 2014;55(7):1216–23. doi: 10.1093/pcp/pcu040 PubMed DOI PMC

Havaux M, Triantaphylides C, Genty B. Autoluminescence imaging: a non-invasive tool for mapping oxidative stress. Trends in Plant Science. 2006;11(10):480–4. doi: 10.1016/j.tplants.2006.08.001 PubMed DOI

Pospíšil P, Prasad A. Formation of singlet oxygen and protection against its oxidative damage in Photosystem II under abiotic stress. Journal of Photochemistry and Photobiology B-Biology. 2014;137:39–48. doi: 10.1016/j.jphotobiol.2014.04.025 PubMed DOI

Pospíšil P, Yamamoto Y. Damage to photosystem II by lipid peroxidation products. Biochim Biophys Acta-Gen Subj. 2017;1861(2):457–66. doi: 10.1016/j.bbagen.2016.10.005 PubMed DOI

Russell GA. Deuterium-Isotope Effects in the Autoxidation of Aralkyl Hydrocarbons—Mechanism of the Interaction of Peroxy Radicals. Journal of the American Chemical Society. 1957;79(14):3871–7. doi: 10.1021/Ja01571a068 DOI

Birtic S, Ksas B, Genty B, Mueller MJ, Triantaphylides C, Havaux M. Using spontaneous photon emission to image lipid oxidation patterns in plant tissues. The Plant journal: for cell and molecular biology. 2011;67(6):1103–15. doi: 10.1111/j.1365-313X.2011.04646.x . PubMed DOI

Berthold DA, Babcock G.T., Yocum C.F. A highly resolved oxygen-evolving photosytem II preparation from spinach thylakoid membranes. FEBS Lett. 1981;134:231–4.

Caffarri S, Kouřil R, Kereïche S, Boekema EJ, Croce R. Functional architecture of higher plant photosystem II supercomplexes. The EMBO Journal. 2009;28(19):3052–63. doi: 10.1038/emboj.2009.232 PubMed DOI PMC

Schagger H. Tricine-SDS-PAGE. Nat Protoc. 2006;1(1):16–22. doi: 10.1038/nprot.2006.4 . PubMed DOI

Soh N, Ariyoshi T, Fukaminato T, Nakano K, Irie M, Imato T. Novel fluorescent probe for detecting hydroperoxides with strong emission in the visible range. Bioorganic & Medicinal Chemistry Letters. 2006;16(11):2943–6. http://dx.doi.org/10.1016/j.bmcl.2006.02.078. PubMed DOI

Soh N, Ariyoshi T, Fukaminato T, Nakajima H, Nakano K, Imato T. Swallow-tailed perylene derivative: a new tool for fluorescent imaging of lipid hydroperoxides. Organic & biomolecular chemistry. 2007;5(23):3762–8. Epub 2007/11/16. doi: 10.1039/b713223a . PubMed DOI

Prasad A, Pospíšil P. Towards the two-dimensional imaging of spontaneous ultra-weak photon emission from microbial, plant and animal cells. Scientific Reports. 2013;3:1211 doi: 10.1038/srep01211 PubMed DOI PMC

Zhang H, Joseph J, Vasquez-Vivar J, Karoui H, Nsanzumuhire C, Martasek P, et al. Detection of superoxide anion using an isotopically labeled nitrone spin trap: potential biological applications. Febs Letters. 2000;473(1):58–62. doi: 10.1016/s0014-5793(00)01498-8 PubMed DOI

Pou S, Ramos CL, Gladwell T, Renks E, Centra M, Young D, et al. A KINETIC APPROACH TO THE SELECTION OF A SENSITIVE SPIN-TRAPPING SYSTEM FOR THE DETECTION OF HYDROXYL RADICAL. Analytical biochemistry. 1994;217(1):76–83. doi: 10.1006/abio.1994.1085 PubMed DOI

Mason RP. Using anti-5,5-dimethyl-1-pyrroline N-oxide (anti-DMPO) to detect protein radicals in time and space with immuno-spin trapping. Free Radical Bio Med. 2004;36(10):1214–23. doi: 10.1016/j.freeradbiomed.2004.02.077 PubMed DOI

Moan J, Wold E. Detection of singlet oxygen production by ESR. Nature. 1979;279(5712):450–1. doi: 10.1038/279450a0 PubMed DOI

Miyamoto S, Ronsein GE, Prado FM, Uemi M, Correa TC, Toma IN, et al. Biological hydroperoxides and singlet molecular oxygen generation. IUBMB life. 2007;59(4–5):322–31. doi: 10.1080/15216540701242508 . PubMed DOI

Zabelin AA, Neverov KV, Krasnovsky AA, Shkuropatova VA, Shuvalov VA, Shkuropatov AY. Characterization of the low-temperature triplet state of chlorophyll in photosystem II core complexes: Application of phosphorescence measurements and Fourier transform infrared spectroscopy. Biochimica Et Biophysica Acta-Bioenergetics. 2016;1857(6):782–8. doi: 10.1016/j.bbabio.2016.03.029 PubMed DOI

Rinalducci S, Pedersen JZ, Zolla L. Generation of reactive oxygen species upon strong visible light irradiation of isolated phycobilisomes from Synechocystis PCC 6803. Biochimica Et Biophysica Acta-Bioenergetics. 2008;1777(5):417–24. doi: 10.1016/j.bbabio.2008.02.005 PubMed DOI

Kobayashi M, Ohashi S, Iwamoto K, Shiraiwa Y, Kato Y, Watanabe T. Redox potential of chlorophyll d in vitro. Biochimica Et Biophysica Acta-Bioenergetics. 2007;1767(6):596–602. doi: 10.1016/j.bbabio.2007.02.015 PubMed DOI

Schmitt F-J, Renger G, Friedrich T, Kreslavski VD, Zharmukhamedov SK, Los DA, et al. Reactive oxygen species: Re-evaluation of generation, monitoring and role in stress-signaling in phototrophic organisms. Biochimica et Biophysica Acta (BBA)—Bioenergetics. 2014;1837(6):835–48. https://doi.org/10.1016/j.bbabio.2014.02.005. PubMed DOI

Faller P, Debus RJ, Brettel K, Sugiura M, Rutherford AW, Boussac A. Rapid formation of the stable tyrosyl radical in photosystem II. P Natl Acad Sci USA. 2001;98(25):14368–73. doi: 10.1073/pnas.251382598 PubMed DOI PMC

Ananyev G, Renger G, Wacker U, Klimov V. The photoproduction of superoxide radicals and the superoxide-dismutase activity of photosystem-II—THE POSSIBLE INVOLVEMENT OF CYTOCHROME B559. Photosynthesis Research. 1994;41(2):327–38. doi: 10.1007/BF00019410 PubMed DOI

Murata N, Allakhverdiev SI, Nishiyama Y. The mechanism of photoinhibition in vivo: re-evaluation of the roles of catalase, alpha-tocopherol, non-photochemical quenching, and electron transport. Biochim Biophys Acta. 2012;1817(8):1127–33. Epub 2012/03/06. doi: 10.1016/j.bbabio.2012.02.020 . PubMed DOI

Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI. Photoinhibition of photosystem II under environmental stress. Biochimica et Biophysica Acta (BBA)—Bioenergetics. 2007;1767(6):414–21. https://doi.org/10.1016/j.bbabio.2006.11.019. PubMed DOI

Allakhverdiev SI, Murata N. Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage–repair cycle of Photosystem II in Synechocystis sp. PCC 6803. Biochimica et Biophysica Acta (BBA)—Bioenergetics. 2004;1657(1):23–32. https://doi.org/10.1016/j.bbabio.2004.03.003. PubMed DOI

Mori H, Yamashita Y, Akasaka T, Yamamoto Y. Further characterization of the loss of antenna chlorophyll-binding protein cp43 from photosystem-II during donor-side photoinhibition. Biochimica Et Biophysica Acta-Bioenergetics. 1995;1228(1):37–42. doi: 10.1016/0005-2728(94)00156-y DOI

Miyamoto S, Martinez GR, Rettori D, Augusto O, Medeiros MH, Di Mascio P. Linoleic acid hydroperoxide reacts with hypochlorous acid, generating peroxyl radical intermediates and singlet molecular oxygen. Proc Natl Acad Sci U S A. 2006;103(2):293–8. doi: 10.1073/pnas.0508170103 ; PubMed DOI PMC

Miyamoto S, Martinez GR, Medeiros MH, Di Mascio P. Singlet molecular oxygen generated from lipid hydroperoxides by the russell mechanism: studies using 18(O)-labeled linoleic acid hydroperoxide and monomol light emission measurements. J Am Chem Soc. 2003;125(20):6172–9. doi: 10.1021/ja029115o . PubMed DOI

Mano CM, Prado FM, Massari J, Ronsein GE, Martinez GR, Miyamoto S, et al. Excited singlet molecular O-2 ((1)Delta g) is generated enzymatically from excited carbonyls in the dark. Scientific Reports. 2014;4 doi: 10.1038/srep05938 PubMed DOI PMC

Foote CS. Definition of type-I and type-II photosensitized oxidation. Photochemistry and Photobiology. 1991;54(5):659- doi: 10.1111/j.1751-1097.1991.tb02071.x PubMed DOI

Modulation of pulsed electric field induced oxidative processes in protein solutions by pro- and antioxidants sensed by biochemiluminescence

Reactive oxygen species in photosystem II: relevance for oxidative signaling

Reactive Oxygen Species as a Response to Wounding: In Vivo Imaging in Arabidopsis thaliana