Abstract
The physiological significance of photosystem II (PSII) core protein phosphorylation has been suggested to facilitate the migration of oxidative damaged D1 and D2 proteins, but meanwhile the phosphorylation seems to be associated with the suppression of reactive oxygen species (ROS) production, and it also relates to the degradation of PSII reaction center proteins. To more clearly elucidate the possible protecting effect of the phosphorylation on oxidative damage of D1 protein, the degradation of oxidized D1 protein and the production of superoxide anion in the non-phosphorylated and phosphorylated PSII membranes were comparatively detected using the Western blotting and electron spin resonance spin-trapping technique, respectively. Obviously, all of three ROS components, including superoxide anion, hydrogen peroxide and hydroxyl radical are responsible for the degradation of oxidized D1 protein, and the protection of the D1 protein degradation by phosphorylation is accompanied by the inhibition of superoxide anion production. Furthermore, the inhibiting effect of 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU), a competitor to QB, on superoxide anion production and its protecting effect on D1 protein degradation are even more obvious than those of phosphorylation. Both DCMU effects are independent of whether PSII membranes are phosphorylated or not, which reasonably implies that the herbicide DCMU and D1 protein phosphorylation probably share the same target site in D1 protein of PSII. So, altogether it can be concluded that the phosphorylation of D1 protein reduces the oxidative damage of D1 protein by decreasing the production of superoxide anion in PSII membranes under high light.
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Abbreviations
- PSII:
-
Photosystem II
- ROS:
-
Reactive oxygen species
- QB :
-
Secondary quinone electron acceptor
- DCMU:
-
3-(3,4-Dichlorophenyl)-1,1-dimethylurea
- ESR:
-
Electron spin resonance
- Mes:
-
4-Morpholineethanesulfonic acid
- Chl:
-
Chlorophyll
- SOD:
-
Superoxide dismutase
- DMSO:
-
Dimethyl sulfoxide
- TCNE:
-
Tetracyanoethylene
- SDS-PAGE:
-
Sodium dodecyl sulfate-polyacrylamide gel electrophoresis
- BMPO:
-
5-Tert-butoxycarbonyl-5-methyl-1-pyrroline N-oxide
- DTPA:
-
Diethylene-triaminepentaacetic acid
- XOD:
-
Xanthine oxidase
- HX:
-
Hypoxanthine
- LHCII:
-
Light-harvesting complex II
- Pheo:
-
Pheophytin-primary electron acceptor
- QA :
-
Primary quinone electron acceptor
References
Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics Int 11:36–42
Allakhverdiev SI, Nishiyama Y, Takahashi S, Miyairi S, Suzuki I, Murata N (2005) Systematic analysis of the relation of electron transport and ATP synthesis to the photodamage and repair of photosystem II in synechocystis. Plant Physiol 137:263–273
Ananyev GM, Renger G, Wacker U, Klimov VV (1994) The photoproduction of superoxide radicals and the superoxide dismutase activity of photosystem II. The possible involvement of cytochrome b559. Photosynth Res 41:327–338
Arató A, Bondarava 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
Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15
Aro EM, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134
Aro EM, Rokka A, Vener AV (2004) Determination of phosphoproteins in higher plant thylakoids. In: Carpentier R (ed) Photosynthesis research protocols. Methods in molecular biology. Humana Press, Totowa, pp 177–193
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
Berthold DA, Babcock GT, Yocum CF (1981) A highly resolved, oxygen-evolving photosystem II preparation from spinach thylakoid membranes. EPR and electron-transport properties. FEBS Lett 134:231–234
Chen LB, Jia HY, Du LB, Tian Q, Gao YL, Liu Y (2011) Release of the oxygen-evolving complex subunits from photosystem II membranes in phosphorylation condition under light stress. Chin J Chem 29:2631–2636
Chiang HM, Yin JJ, Xia QS, Zhao YW, Fu PP, Wen KC, Yu HT (2010) Photoirradiation of azulene and guaiazulene-formation of reactive oxygen species and induction of lipid peroxidation. J Photochem Photobiol A 211:123–128
Cleland RE, Grace SC (1999) Voltammetric detection of superoxide production by photosystem II. FEBS Lett 457:348–352
Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–1838
Fufezan C, Rutherford AW, Krieger-Liszkay A (2002) Singlet oxygen production in herbicide-treated photosystem II. FEBS Lett 532:407–410
Giardi MT, Rigoni F, Barbato R (1992) Photosystem II core phosphorylation heterogeneity, differential herbicide binding, and regulation of electron transfer in photosystem II preparations from spinach. Plant Physiol 100:1948–1954
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
Henmi T, Miyao M, Yamamoto Y (2004) Release and reactive-oxygen-mediated damage of the oxygen-evolving complex subunits of PSII during photoinhibition. Plant Cell Physiol 45:243–250
Hodges M, Boussac A, Briantais JM (1987) Thylakoid membrane protein phosphorylation modifies the equilibrium between photosystem II quinone electron acceptors. Biochim Biophys Acta 894:138–145
Jung J, Kim HS (1990) The chromophores as endogenous sensitizers involved in the photogeneration of singlet oxygen in spinach thylakoids. Photochem Photobiol 52:1003–1009
Koivuniemi A, Aro EM, Andersson B (1995) Degradation of the D1- and D2-proteins of photosystem II in higher plants is regulated by reversible phosphorylation. Biochemistry 34:16022–16029
Kyle DJ (1987) The biochemical basis for photoinhibition of photosystem II. In: Kyle DJ, Osmond CB, Arntzen CJ (eds) Topics in photosynthesis: photoinhibition. Elsevier, Amsterdam, pp 197–226
Kyle DJ, Ohad I, Arntzen CJ (1984) Membrane protein damage and repair: selective loss of a quinone-protein function in chloroplast membranes. Proc Natl Acad Sci USA 81:4070–4074
Liu K, Sun J, Song YG, Liu B, Xu YK, Zhang SX, Tian Q, Liu Y (2004) Superoxide, hydrogen peroxide and hydroxyl radical in D1/D2/cytochrome b-559 photosystem II reaction center complex. Photosynth Res 81:41–47
Mattoo AK, Hoffman-Falk H, Marder JB, Edelman M (1984) Regulation of protein metabolism: coupling of photosynthetic electron transport to in vivo degradation of the rapidly metabolized 32-kilodalton protein of the chloroplast membranes. Proc Natl Acad Sci USA 81:1380–1384
Michael AH, John FA (1991) Light-dependent phosphorylation of photosystem II polypeptides maintains electron transport at high light intensity: separation from effects of phosphorylation of LHC-II. Biochim Biophys Acta 1058:289–296
Michel H, Deisenhofer J (1988) Relevance of the photosynthetic reaction center from purple bacteria to the structure of photosystem II. Biochemistry 27:1–7
Miyao M (1994) Involvement of active oxygen species in degradation of the D1 protein under strong illumination in isolated subcomplexes of photosystem II. Biochemistry 33:9722–9730
Miyao M, Ikeuchi M, Yamamoto N, Ono T (1995) Specific degradation of the D1 protein of photosystem II by treatment with hydrogen peroxide in darkness: implications for the mechanism of degradation of the D1 protein under illumination. Biochemistry 34:10019–10026
Mizusawa N, Yamamoto N, Miyao M (1999) Characterization of damage to the D1 protein of photosystem II under photoinhibitory illumination in non-phosphorylated and phosphorylated thylakoid membranes. J Photochem Photobiol B Biol 48:97–103
Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 1767:414–421
Murata N, Allakhverdiev SI, Nishiyama Y (2012) The mechanism of photoinhibition in vivo: re-evaluation of the roles of catalase, α-tocopherol, non-photochemical quenching, and electron transport. Biochim Biophys Acta. doi:10.1016/j.bbabio.2012.02.020
Nishiyama Y, Allakhverdiev SI, Murata N (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim Biophys Acta 1757:742–749
Nishiyama Y, Allakhverdiev SI, Murata N (2011) Protein synthesis is the primary target of reactive oxygen species in the photoinhibition of photosystem II. Physiol Plant 142:35–46
Ohad I, Kyle DJ, Arntzen CJ (1984) Membrane protein damage and repair: removal and replacement of inactivated 32-kilodalton polypeptides in chloroplast membranes. J Cell Biol 99:481–485
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
Pospísil P (2009) Production of reactive oxygen species by photosystem II. Biochim Biophys Acta 1787:1151–1160
Pospísil P, Arató A, Krieger-Liszkay A, Rutherford AW (2004) Hydroxyl radical generation by photosystem II. Biochemistry 43:6783–6792
Pospísil P, Snyrychová I, Kruk J, Strzałka K, Naus 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
Robinson HH, Yocum CF (1980) Cyclic photophosphorylation reactions catalyzed by ferredoxin, methyl viologen and anthraquinone sulfonate. Use of photochemical reactions to optimize redox poising. Biochim Biophys Acta 590:97–106
Sahni M, Locke BR (2006) Quantification of hydroxyl radicals produced in aqueous phase pulsed electrical discharge reactors. Ind Eng Chem Res 45:5819–5825
Scaduto RC (1995) Oxidation of DMSO and methanesulfinic acid by the hydroxyl radical. Free Radic Biol Med 18:271–277
Shimmura S, Masumizu T, Nakai Y, Urayama K, Shimazaki J, Bissen-Miyajima H, Kohno M, Tsubota K (1999) Excimer laser-induced hydroxyl radical formation and keratocyte death in vitro. Invest Ophthalmol Vis Sci 40:1245–1249
Song YG, Liu B, Wang LF, Li MH, Liu Y (2006) Damage to the oxygen-evolving complex by superoxide anion, hydrogen peroxide, and hydroxyl radical in photoinhibition of photosystem II. Photosynth Res 90:67–78
Takahashi R, Hasegawa K, Takano A, Noguchi T (2010) Structures and binding sites of phenolic herbicides in the QB pocket of photosystem II. Biochemistry 49:5445–5454
Tikkanen M, Nurmi M, Kangasjärvi S, Aro EM (2008) Core protein phosphorylation facilitates the repair of photodamaged photosystem II at high light. Biochim Biophys Acta 1777:1432–1437
Tikkanen M, Grieco M, Aro EM (2011) Novel insights into plant light-harvesting complex II phosphorylation and ‘state transitions’. Trends Plant Sci 16:126–131
Tiwari A, Pospísil P (2009) Superoxide oxidase and reductase activity of cytochrome b559 in photosystem II. Biochim Biophys Acta 1787:985–994
Tsai P, Ichikawa K, Mailer C, Pou S, Halpern HJ, Robinson BH, Nielsen R, Rosen GM (2003) Esters of 5-carboxyl-5-methyl-1-pyrroline N-oxide: a family of spin traps for superoxide. J Org Chem 68:7811–7817
Yamamoto Y (2001) Quality control of photosystem II. Plant Cell Physiol 42:121–128
Yruela I, Montoya G, Alonso PJ, Picorel R (1991) Identification of the pheophytin-QA-Fe domain of the reducing side of the photosystem II as the Cu(II)-inhibitory binding site. J Biol Chem 266:22847–22850
Zhang S, Weng J, Pan J, Tu T, Yao S, Xu C (2003) Study on the photo-generation of superoxide radicals in photosystem II with EPR spin trapping techniques. Photosynth Res 75:41–48
Acknowledgments
This research was supported by the National Natural Science Foundation of China (Nos. 20875093 and 90813021) and the Pilot Project of Knowledge Innovation Program of the Chinese Academy of Sciences (KGCX2-EW-308-1’). The authors are very grateful to Dr. Ronald Charles Kurtenbach for the careful reading and the correction of the manuscript.
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Chen, L., Jia, H., Tian, Q. et al. Protecting effect of phosphorylation on oxidative damage of D1 protein by down-regulating the production of superoxide anion in photosystem II membranes under high light. Photosynth Res 112, 141–148 (2012). https://doi.org/10.1007/s11120-012-9750-9
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DOI: https://doi.org/10.1007/s11120-012-9750-9