Evidence on the formation of singlet oxygen in the donor side photoinhibition of photosystem II: EPR spin-trapping study
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
23049883
PubMed Central
PMC3458798
DOI
10.1371/journal.pone.0045883
PII: PONE-D-12-13720
Knihovny.cz E-zdroje
- MeSH
- chemické modely MeSH
- elektronová paramagnetická rezonance metody MeSH
- fotochemie metody MeSH
- fotosystém II - proteinový komplex fyziologie MeSH
- koncentrace vodíkových iontů MeSH
- kyslík chemie MeSH
- propylgalan chemie MeSH
- singletový kyslík * MeSH
- spin trapping metody MeSH
- Spinacia oleracea MeSH
- světlo MeSH
- Synechococcus metabolismus MeSH
- uhlík chemie MeSH
- volné radikály MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- fotosystém II - proteinový komplex MeSH
- kyslík MeSH
- propylgalan MeSH
- singletový kyslík * MeSH
- uhlík MeSH
- volné radikály MeSH
When photosystem II (PSII) is exposed to excess light, singlet oxygen ((1)O(2)) formed by the interaction of molecular oxygen with triplet chlorophyll. Triplet chlorophyll is formed by the charge recombination of triplet radical pair (3)[P680(•+)Pheo(•-)] in the acceptor-side photoinhibition of PSII. Here, we provide evidence on the formation of (1)O(2) in the donor side photoinhibition of PSII. Light-induced (1)O(2) production in Tris-treated PSII membranes was studied by electron paramagnetic resonance (EPR) spin-trapping spectroscopy, as monitored by TEMPONE EPR signal. Light-induced formation of carbon-centered radicals (R(•)) was observed by POBN-R adduct EPR signal. Increased oxidation of organic molecules at high pH enhanced the formation of TEMPONE and POBN-R adduct EPR signals in Tris-treated PSII membranes. Interestingly, the scavenging of R(•) by propyl gallate significantly suppressed (1)O(2). Based on our results, it is concluded that (1)O(2) formation correlates with R(•) formation on the donor side of PSII due to oxidation of organic molecules (lipids and proteins) by long-lived P680(•+)/TyrZ(•). It is proposed here that the Russell mechanism for the recombination of two peroxyl radicals formed by the interaction of R(•) with molecular oxygen is a plausible mechanism for (1)O(2) formation in the donor side photoinhibition of PSII.
Zobrazit více v PubMed
Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303: 1831–1838. PubMed
Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W (2009) Cynobacterial photosystem II at 2.9 Å resolution and the role of quinones, lipids, channels and chloride. Nat Struct Mol Biol 16: 334–342. PubMed
Umena Y, Kawakami K, Shen J-R, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473: 55–61. PubMed
Renger G, Holzwarth AR (2005) Primary electron transfer. In: Wydrzynski TJ, Satoh K, Eds. Photosystem II: The Light-Driven Water: Plastoquinone Oxidoreductase. Springer Dordrecht pp. 139–175.
Rappaport F, Diner BA (2008) Primary photochemistry and energetics leading to the oxidation of the (Mn)4Ca cluster and to the evolution of molecular oxygen in photosystem II. Coord Chem Rev 252: 259–272.
Brudvig GW (2008) Water oxidation chemistry of photosystem II. Phil Trans R Soc B 363: 1211–1219. PubMed PMC
Cardona T, Sedoud A, Cox N, Rutherford AW (2012) Charge separation in photosystem II: a comparative and evolutionary overview. Biochim Biophys Acta 1817: 26–43. PubMed
Rutherford AW, Boussac (2004) A Water photolysis in biology. Science 303: 1782–1784. PubMed
McEvoy JP, Brudvig GW (2006) Water-splitting chemistry of photosystem II. Chem Rev 106: 4455–4483. PubMed
Dau H, Haumann M (2008) The manganese complex of photosystem II in its reaction cycle-basic framework and possible realization at the atomic level. Coord Chem Rev 252: 273–295.
Zein S, Kilik LV, Yano J, Kern J, Pushkar Y, Zouni A, Yachandra VK, Lubitz W, Neese F, Messigner J (2008) Focusing the view on nature's water-splitting catalyst. Phil Trans R Soc B 363: 167–1177. PubMed PMC
Grundmeier A, Dau H (2012) Structural models of the magnese complex of photosystem II and mechanistic implications. Biochim Biophys Acta 1817: 88–105. PubMed
Chow WS, Aro E-M (2005) Photoinactivation and mechanisms of repair. In: Wydrzynski TJ, Satoh K, Eds. Photosystem II: The Light-Driven Water: Plastoquinone Oxidoreductase. Springer Dordrecht pp. 627–648.
Vass I, Aro E-M (2007) Photoinhibition of photosynthetic electron transport. In: Renger G, Eds. Primary processes in photosynthesis, basic principles and apparatus. The Royal Society of Chemistry Cambridge pp. 393–425.
Takahashi S, Murata N (2008) How do environmental stresses accelerate photoinhibition?. Trends Plant Sci 13: 178–182. PubMed
Tyystjärvi E (2008) Photoinhibition of photosystem II and photodamage of the oxygen evolving manganese cluster. Coord Chem Rev 252: 361–376.
Takahashi S, Badger MR (2011) Photoprotection in plants: a new light on photosystem II damage. Trends Plant Sci 16: 53–60. PubMed
Vass I (2012) Molecular mechanism of Photodamage in the photosystem II complex. Biochim Biophys Acta 1817: 209–217. PubMed
Aro E-M, Virgin I, Andersson B (1993) Photoinhibition of photosystem II: inactivation, protein damage and turnover. Biochim Biophys Acta 1143: 113–134. PubMed
Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 1767: 414–421. PubMed
Yamamoto Y, Aminaka R, Yoshioka M, Khatoon M, Komayama K, Takenaka D, Yamashita A, Nijo N, Inagawa K, Morita N, Sasaki T, Yamamoto Y (2008) Quality control of photosystem II: impact of light and heat stresses. Photosynth Res 98: 589–608. PubMed
Kato Y, Sakamoto W (2009) Protein quality control in chloroplasts: a current model of D1 protein degradation in the photosystem II repair cycle. J Biochem 146: 463–469. PubMed
Yamamoto Y (2001) Quality control of photosystem II. Plant cell Physiol 42: 121–128. PubMed
Ohira S, Morita N, Suh HJ, Jung J, Yamamoto Y (2005) Quality control of photosystem II under light stress-turnover of aggregates of the D1 protein in vivo . Photosynth Res 84: 29–33. PubMed
Vass I, Styring S, Hundal T, Koivuniemi A, Aro E-M, Anderson B (1992) Reversible and irreversible intermediates during photoinhibition of photosystem II: stable reduced QA species promote chlorophyll triplet formation. Proc Natl Acad Sci USA 89: 1408–1412. PubMed PMC
Van Mieghem F, Brettel K, Hillmann B, Kamlowski A, Rutherford AW, Schlodder E (1995) Charge recombination reaction in photosystem II. 1. yields, recombination pathways, and kinetics of the primary pair. Biochemistry 34: 4798–4813. PubMed
Vass I (2011) Role of charge recombination processes in photodamage and photoprotection of the photosystem II complex. Physiol Plant 142: 6–16. PubMed
Krieger-Liszkay A, Fufezan C, Trebst A (2008) Singlet oxygen production in photosystem II and related protection mechanism. Photosynth Res 98: 551–564. PubMed
Pospíšil P (2009) Production of reactive oxygen species by photosystem II. Biochim. Biophys. Acta 1787: 1151–1160. PubMed
Pospíšil P (2012) Molecular mechanism of production and scavenging of reactive oxygen species by photosystem II. Biochim Biophys Acta 1817: 218–231. PubMed
Rappaport F, Guergova-Kuras M, Nixon PJ, Diner BA, Lavergne J (2002) Kinetics and pathway of charge recombination in photosystem II. Biochemistry 41: 8518–8527. PubMed
Hideg E, Spetea C, Vass I (1994) Singlet oxygen and free radical production during acceptor and donor side induced photoinhibition: studies with spin trapping EPR spectroscopy. Biochim Biophys Acta 1186: 143–152.
Fischer BB, Krieger-Liszkay A, Hideg E, Šnyrychová I, Wiesendanger M, Eggen RIL (2007) Role of singlet oxygen in chloroplast to nucleus retrograde signaling in chlamydomonas reinhardtii . FEBS Lett 581: 5555–5560. PubMed
Yadav DK, Kruk J, Sinha RK, Pospíšil P (2010) Singlet oxygen scavenging activity of plastoquinol in photosystem II of higher plants: electron paramagnetic resonance spin trapping study. Biochim Biophys Acta 1797: 1807–1811. PubMed
Telfer A, Bishop SM, Phillips D, Barber J (1994) Isolated photosynthetic reaction center of photosystem II as a sensitizer for the formation of singlet oxygen, detection and quantum yield determination using a chemical trapping technique. J Biol Chem 269: 13244–13253. PubMed
Macpherson AN, Telfer A, Barber J, Truscott TG (1993) Direct detection of singlet oxygen from isolated photosystem II reaction centers. Biochim Biophys Acta 114: 301–309.
Santabarbara S, Neverov KV, Garlaschi FM, Zucchelli G, Jennings RC (2001) Involvement of uncoupled antenna chlorophylls in photoinhibition in thylakoids. FEBS Lett 491: 109–113. PubMed
Santabarbara S, Cazzalini I, Rivadossi A, Garlaschi FM, Zucchelli G, Jennings RC (2002) Photoinhibition in vivo and in vitro involves weakly coupled chlorophyll protein complexes. Photochem Photobiol 75: 613–618. PubMed
Zolla L, Rinalducci S (2002) Involvement of active oxygen species in degradation of light harvesting proteins under light stresses. Biochemistry 42: 14391–14402. PubMed
Rinalducci S, Pedersen JZ, Zolla L (2004) Formation of radicals from singlet oxygen produced during photoinhibition of isolated light harvesting proteins of photosystem II,. Biochim Biophys Acta 1608: 63–73. PubMed
Pospíšil P, Arató A, Krieger-Liszkay A, Rutherford AW (2004) Hydroxyl radical generation by photosystem II. Biochemistry 43: 6783–6792. PubMed
Pospíšil P, Šnyrychová E, Kruk J, Strzalka K, Nauš J (2006) Evidence that cytochrome b559 is involved in superoxide production in photosystem II: effect of synthetic short-chain plastoquinones in a cytochrome b559 tobacco mutant. Biochem J 397: 321–327. PubMed PMC
Arató A, Bondrava N, Krieger-Liszkay A (2004) Production of reactive oxygen species in chloride- and calcium-depleted photosystem II and their involvement in photoinhibition. Biochim Biophys Acta 1608: 171–180. PubMed
Yanykin DV, Khorobrykh AA, Khorobrykh SS, Klimov VV (2010) Photoconsumption of molecular oxygen on both donor and acceptor sides of photosystem II in Mn-depleted subchloroplast membrane fragments. Biochim Biophys Acta 1797: 516–523. PubMed
Khorobrykh SA, Khorobrykh AA, Yanykin DV, Ivanov BN, Klimov VV, Mano J (2011) Photoproduction of catalase insensitive peroxides on the donor side of manganese-depleted photosystem II, evidence with a specific fluorescent probe. Biochemistry 50: 10658–10665. PubMed
Khorobrykh SA, Khorobrykh AA, Klimov VV, Ivanov BN (2002) Photoconsumption of oxygen in photosystem II preparations under impairment of the water oxidizing complex. Biochemistry (Moscow) 67: 683–688. PubMed
Ivanov B, Khorobrykh S (2003) Participation of photosynthetic electron transport in production and scavenging of reactive oxygen species. Antioxid Redox Signal 5: 43–53. PubMed
Hakala M, Tuominen I, Keränen M, Tyystjärvi T, Tyystjärvi E (2005) Evidence for the role of the oxygen-evolving manganese complex in photoinhibition of photosystem II. Biochim Biophys Acta 1706: 68–80. PubMed
Anderson JM, Park Y-I, Chow WS (1998) Unifying model for the photoinactivation of photosystem II in vivo under study state photosynthesis. Photosynth Res 56: 1–13.
Anderson JM, Chow WS (2002) Structural and functional dynamics of plant photosystem II. Phil Trans R Soc Lond B 357: 1421–1430. PubMed PMC
Angelin M, Hermansson M, Dong H, Ramström O (2006) Direct, mild and selective synthesis of unprotected dialdo-glycosides. Eur J Org Chem 19: 4323–4326.
Nixon PJ, Michoux F, Yu J, Boehm M, Komenda J (2010) Recent advances in understanding the assembly and repair of photosystem II. Ann Bot 106: 1–16. PubMed PMC
Telfer A (2005) Too much light? How beta-carotene protects the photosystem II reaction centre. Photochem Photobiol Sci 4: 950–956. PubMed
Krieger-Liszkay A, Rutherford AW, Vass I, Hideg E (1998) Relationship between activity, D1 loss and Mn binding in photoinhibition of photosystem II. Biochemistry 37: 16262–16269. PubMed
Russell GA (1957) Deuterium-isotope effects in the autooxidation of aralkyl hydrocorbons- mechanism of interaction of peroxy radicals. J Am Chem Soc 79: 3871–3877.
Howard JA, Ingold KU (1968) Self reaction of sec-butylperoxy radicals. confirmation of Russell mechanism. J Am Chem Soc 90: 1056–1058.
Dean RT, Fu S, Stocker R, Davies MJ (1997) Biochemistry and pathology of radical-mediated protein oxidation. Biochem J 324: 1–18. PubMed PMC
Miyamoto S, Ronsein GE, Prado FM, Uemi M, Correa TC, Toma IN, Bertolucci A, Oliveira MCB, Motta FD, Medeiros MHG, Mascio PD (2007) Biological hydroperoxides and singlet molecular oxygen generation. IUBMB Life 59: 322–331. PubMed
Miyamoto S, Martinez GR, Medeiros MHG, Mascio PD (2003) Singlet molecular oxygen generated from lipid hydroperoxide by the Russell mechanism: studies using 18O-labeled linoleic acid hydroperoxide and monomol light emission measurements. J Am Chem Soc 125: 6172–6179. PubMed
Sun S, Bao Z, Ma H, Zhang D, Zheng X (2007) Singlet oxygen generation from the decomposition of α–linolenic acid hydroperoxide by cytochrome c and lactoperoxidase. Biochemistry 46: 6668–6673. PubMed
Mendenhall GD, Sheng XC, Wilson T (1991) Yields of excited carbonyl species from alkoxyl and from alkylperoxyl radical dismutations. J Am Chem Soc 113: 8976–8977.
Niu QJ, Mendenhall GD (1992) Yields of singlet molecular oxygen from peroxyl radical termination. J Am Chem Soc 114: 165–172.
Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2007) Lipids in photosystem II: interactions with protein and cofactors. Biochim Biophys Acta 1767: 509–519. PubMed
Kern J, Guskov A (2011) Lipids in photosystem II: multifunctional cofactors. J Photochem Photobiol B Biology 104: 19–34. PubMed
Mizusawa N, Wada H (2012) The role of lipids in photosystem II. Biochim Biophys Acta 1817: 194–208. PubMed
Ishikita H, Loll B, Biesiadka J, Saenger W, Knapp EW (2005) Redox potentials of chlorophylls in the photosystem II reaction center. Biochemistry 44: 4118–4124. PubMed
Allakhverdiev SI, Tomo T, Shimada Y, Kindo H, Nagao R, Klimov VV, Mimuro M (2010) Redox potential of pheophytin a in photosystem II of two cyanobacteria having the different special pair chlorophylls. Proc Natl Acad Sci USA 107: 3924–3929. PubMed PMC
Berthold DA, Babcock GT, Yocum CF (1981) A highly resolved oxygen evolving photosystem II preparation from spinach thylakoid membranes. FEBS Lett 134: 231–234.
Ford RC, Evans MCW (1983) Isolation of a photosystem II from higher plants with highly enriched oxygen evolution activity. FEBS Lett 160: 159–164.
Moan J, Wold E (1979) Detection of singlet oxygen production by ESR. Nature 279: 450–451. PubMed
Sinha RK, Komenda J, Knoppová J, Sedláŕová M, Pospíšil P (2012) Small CAB-like proteins prevent formation of singlet oxygen in the damaged photosystem II complex of the cyanobacterium synechocystis sp. PCC 6803. Plant Cell Environ 35: 806–818. PubMed
North JA, Spector AA, Buettner GR (1992) Detection of lipid radicals by electron paramagnetic resonance spin trapping using intact cells enriched with polyunsaturated fatty acid. J Biol Chem 267: 5743–5746. PubMed
Stolze K, Udilova N, Rosenau T, Hofinger A, Nohl H (2005) Spin adduct formation from lipophilic EMPO-derived spin traps with various oxygen- and carbon-centered radicals. Biochem Pharm 69: 297–305. PubMed
Reactive Oxygen Species as a Response to Wounding: In Vivo Imaging in Arabidopsis thaliana
Formation of singlet oxygen by decomposition of protein hydroperoxide in photosystem II