Experimental evidence suggesting that H2O2 is produced within the thylakoid membrane in a reaction between plastoquinol and singlet oxygen

FEBS Letters

Volumn 589, Issue 6, 2015, Pages 779-786

  Khorobrykh, Sergey A ^a   Karonen, Maarit ^a   Tyystjärvi, Esa ^a  

^a UNIVERSITY OF TURKU   (Finland)

Author keywords

Hydrogen peroxide; Photosystem II; Plastoquinone; Singlet oxygen; Thylakoid membrane

Indexed keywords

HYDROGEN PEROXIDE; PLASTOQUINOL; PLASTOQUINONE; SINGLET OXYGEN; UNCLASSIFIED DRUG;

ARTICLE; CHEMICAL REACTION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ELECTRON TRANSPORT; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LIPOPHILICITY; OXIDATION; PRIORITY JOURNAL; THYLAKOID MEMBRANE; ANALOGS AND DERIVATIVES; CYTOLOGY; METABOLISM; OXIDATION REDUCTION REACTION; PLANT LEAF; SQUASH; THYLAKOID;

CUCURBITA; HYDROGEN PEROXIDE; OXIDATION-REDUCTION; PLANT LEAVES; PLASTOQUINONE; SINGLET OXYGEN; THYLAKOIDS;

EID: 84923576570     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2015.02.011     Document Type: Article

References (56)

1. C.H. Foyer, and G. Noctor Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses Plant Cell 17 2005 1866 1875
2. K. Apel, and H. Hirt Reactive oxygen species: metabolism, oxidative stress, and signal transduction Annu. Rev. Plant Biol. 5 2004 373 399
3. Frank. Van Breusegem, J. Bailey-Serres, and R. Mittler Unraveling the tapestry of networks involving reactive oxygen species in plants Plant Physiol. 147 2008 978 984
4. D.M. Rhoads, A.L. Umbach, C.C. Subbaiah, and J.N. Siedow Mitochondrial reactive oxygen species. Contribution to oxidative stress and interorganellar signaling Plant Physiol. 141 2006 357 366
5. K. Asada Production and scavenging of reactive oxygen species in chloroplasts and their functions Plant Physiol. 141 2006 391 396
6. M.A. Torres, J.D.G. Jones, and J.L. Dang Reactive oxygen species signaling in response to pathogens Plant Physiol. 141 2006 373 378
7. S. Santabarbara, G. Agostini, A.P. Casazza, C.D. Syme, P. Heathcote, F. Böhles, M.C. Evans, R.C. Jennings, and D. Carbonera Chlorophyll triplet states associated with photosystem I and photosystem II in thylakoids of the green alga Chlamydomonas reinhardtii Biochim. Biophys. Acta 1767 2007 88 105
8. P. Pospíšil Molecular mechanisms of production and scavenging of reactive oxygen species by photosystem II Biochim. Biophys. Acta 1817 2012 218 231
9. É. Hideg, and I. Vass Singlet oxygen is not produced in photosystem I under photoinhibitory conditions Photochem. Photobiol. 62 1995 949 952
10. A. Krieger-Liszkay, C. Fufezan, and A. Trebst Singlet oxygen production in photosystem II and related protection mechanism Photosynth. Res. 98 2008 551 564
11. A.J. Hoff, H. Rademaker, R. van Grondelle, and L.N.M. Duysens On the magnetic field dependence of the yield of the triplet state in reaction centers of photosynthetic bacteria Biochim. Biophys. Acta 460 1977 547 554
12. P. Di Mascio, T.P.A. Devasagayam, S. Kaiser, and H. Sies Carotenoids, tocopherols and thiols as biological singlet molecular oxygen quenchers Biochem. Soc. Trans. 18 1990 1054 1056
13. E. Tyystjärvi Photoinhibition of photosystem II Int. Rev. Cell Mol. Biol. 300 2013 243 303
14. B. Loll, J. Kern, W. Saenger, A. Zouni, and J. Biesiadka Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II Nature 438 2005 1040 1044
15. Y. Umena, K. Kawakami, J.-R. Shen, and N. Kamiya Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å Nature 473 2011 55 60
16. K. Asada, K. Kiso, and K. Yoshikawa Univalent reduction of molecular oxygen by spinach chloroplasts on illumination J. Biol. Chem. 249 1974 2175 2181
17. J. Kruk, M. Jemioła-Rzemińska, K. Burda, G.H. Schmid, and K. Strzałka Scavenging of superoxide generated in photosystem I by plastoquinol and other prenyllipids in thylakoid membranes Biochemistry 42 2003 8501 8505
18. 2 reduction by photosystem I involves phylloquinone under steady-state illumination FEBS Lett. 588 2014 4364 4368
19. R.E. Cleland, and S.C. Grace Voltametric detection of superoxide production by photosystem II FEBS Lett. 457 1999 348 352
20. P. Pospíšil, A. Arató, A. Krieger-Liszkay, and A.W. Rutherford Hydroxyl radical generation by photosystem II Biochemistry 43 2004 6783 6792
21. S.A. Khorobrykh, and B.N. Ivanov Oxygen reduction in a plastoquinone pool of isolated pea thylakoids Photosynth. Res. 71 2002 209 219
22. M. Mubarakshina, S. Khorobrykh, and B. Ivanov Oxygen reduction in chloroplast thylakoids results in production of hydrogen peroxide inside the membrane Biochim. Biophys. Acta 1757 2006 1496 1503
23. S. Khorobrykh, M. Mubarakshina, and B. Ivanov Photosystem I is not solely responsible for oxygen reduction in isolated thylakoids Biochim. Biophys. Acta 1657 2004 164 167
24. J. Kruk, and A. Trebst Plastoquinol as a singlet oxygen scavenger in photosystem II Biochim. Biophys. Acta 1777 2008 154 162
25. D.K. Yadav, J. Kruk, R.K. Sinha, and P. Pospíšil Singlet oxygen scavenging activity of plastoquinol in photosystem II of higher plants: electron paramagnetic resonance spin-trapping study Biochim. Biophys. Acta 1797 2010 1807 1811
26. B. Nowicka, and J. Kruk Plastoquinol is more active than α-tocopherol in singlet oxygen scavenging during high light stress of Chlamydomonas reinhardtii Biochim. Biophys. Acta 1817 2012 389 394
27. J. Gruszka, A. Pawlak, and J. Kruk Tocochromanols, plastoquinol, and other biological prenyllipids as singlet oxygen quenchers - determination of singlet oxygen quenching rate constants and oxidation products Free Radic. Biol. Med. 45 2008 920 928
28. C. Triantaphylidès, M. Krischke, F.A. Hoeberichts, B. Ksas, G. Gresser, M. Havaux, Frank. Van Breusegem, and M.J. Mueller Singlet oxygen is the major reactive oxygen species involved in photooxidative damage to plants Plant Physiol. 148 2008 960 968
29. J. Kruk, and S. Karpinski 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 2006 1669 1675
30. V. Klimov, G. Ananyev, O. Zastryzhnaya, T. Wydrzynski, and G. Renger Photoproduction of hydrogen peroxide in photosystem II membrane fragments: a comparison of four signals Photosynth. Res. 38 1987 409 416
31. E. Tyystjärvi, S. Rantamäki, and J. Tyystjärvi Connectivity of photosystem II is the physical basis of retrapping in photosynthetic thermoluminescence Biophys. J. 96 2009 3735 3743
32. E. Gasteiger, C. Hoogland, A. Gattiker, S. Duvaud, M.R. Wilkins, R.D. Appel, and A. Bairoch Protein identification and analysis tools on the ExPASy server J.M. Walker, The Proteomics Protocols Handbook 2005 Humana Press 571 607
33. J. Kyte, and R.F. Doolittle A simple method for displaying the hydropathic character of a protein J. Mol. Biol. 157 1982 105 132
34. J. Kruk, K. Strzałka, and R.M. Leblanc Fluorescence properties of plastoquinol, ubiquinol and alpha-tocopherol quinol in solution and liposome membranes J. Photochem. Photobiol. B Biol. 19 1993 33 38
35. J. Kruk Charge-transfer complexes of plastoquinone and alpha-tocopherol quinone in vitro Biophys. Chem. 30 1988 143 149
36. E. Tyystjärvi Phototoxicity L.D. Noodén, Plant Cell Death Processes 2004 Academic Press San Diego 271 283
37. 2) by azide anion in solvent mixtures Photochem. Photobiol. 74 2001 760 764
38. C.R. Lambert, and I.E. Kochevar Electron transfer quenching of the Rose Bengal triplet state Photochem. Photobiol. 66 1997 15 25
39. D.B. Min, and J.M. Boff Chemistry and reaction of singlet oxygen in foods Compr. Rev. Food Sci. F 1 2002 58 72
40. G.H.G. Thorpe, L.J. Kricka, S.B. Moseley, and T.P. Whitehead Phenols as enhancers of the chemiluminescent horseradish peroxidase-luminol-hydrogen peroxide reaction: application in luminescence-monitored enzyme immunoassays Clin. Chem. 31 1985 1335 1341
41. C.R. Lambert, and I.E. Kochevar Does rose bengal triplet generate superoxide anion? J. Am. Chem. Soc. 118 1996 3297 3298
42. Y. Fu, and J.R. Kanofsky Singlet oxygen generation from liposomes: a comparison of time-resolved 1270 nm emission with singlet-oxygen kinetics calculated from a one dimensional model of singlet-oxygen diffusion and quenching Photochem. Photobiol. 62 1995 692 702
43. C. Schweitzer, and R. Schmidt Physical mechanisms of generation and deactivation of singlet oxygen Chem. Rev. 103 2003 1685 1757
44. J. Kruk, and R. Szymańska Singlet oxygen and non-photochemical quenching contribute to oxidation of the plastoquinone-pool under high light stress in Arabidopsis Biochim. Biophys. Acta 1817 2012 705 710
45. G.G. Kramarenko, S.G. Hummel, S.M. Martin, and G.R. Buettner Ascorbate reacts with singlet oxygen to produce hydrogen peroxide Photochem. Photobiol. 82 2006 1634 1637
46. J. Kruk, and K. Strzałka Dark reoxidation of the plastoquinone-pool is mediated by the low-potential form of cytochrome b-559 in spinach thylakoids Photosynth. Res. 62 1999 273 279
47. P.R. Rich Electron transfer reactions between quinols and quinines in aqueous and aprotic media Biochim. Biophys. Acta 637 1981 28 33
48. K. Asada, and M. Takahashi Production and scavenging of active oxygen in photosynthesis D.J. Kyle, C.B. Osmond, C.J. Arntzen, Photoinhibition 1987 Elsevier Amsterdam, The Netherlands 227 287
49. P. Wardman Bioreactive activation of quinones: redox properties and thiol reactivity Free Radic. Res. Commun. 8 1990 219 229
50. I.B. Afanas'ev Superoxide Ion: Chemistry and Biological Implications 1989 CRC Press Boca Raton, Florida, USA
51. M.M. Mubarakshina, and B.N. Ivanov The production and scavenging of reactive oxygen species in the plastoquinone pool of chloroplast thylakoid membranes Physiologia Plantarum. 140 2010 103 110
52. C.P. Kelly, C.J. Cramer, and D.G. Truhlar Aqueous solvation free energies of ions and ion-water clusters based on an accurate value for the absolute aqueous solvation free energy of the proton J. Phys. Chem. B 110 2006 16066 16081
53. T.K. Antal, I.B. Kovalenko, A.B. Rubin, and E. Tyystjärvi Photosynthesis-related quantities for education and modeling Photosynth. Res. 117 2013 1 30
54. J.D. Rochaix, S. Lemeille, A. Shapiguzov, I. Samol, G. Fucile, A. Willig, and M. Goldschmidt-Clermont Protein kinases and phosphatases involved in the acclimation of the photosynthetic apparatus to a changing light environment Philos. Trans. R. Soc. Lond. B Biol. Sci. 367 2012 3466 3474
55. T. Wunder, Q. Liu, E. Aseeva, V. Bonardi, D. Leister, and M. Pribil Control of STN7 transcript abundance and transient STN7 dimerisation are involved in the regulation of STN7 activity Planta 237 2013 541 558
56. K. Apel, and H. Hirt Reactive oxygen species: metabolism, oxidative stress and signal transduction Annu. Rev. Plant Biol. 55 2004 373 399