Singlet oxygen scavenging activity of tocopherol and plastochromanol in Arabidopsis thaliana: Relevance to photooxidative stress

Plant, Cell and Environment

Volumn 37, Issue 2, 2014, Pages 392-401

  Rastogi, Anshu ^a   Yadav, Deepak Kumar ^a   Szymańska, Renata ^b   Kruk, Jerzy ^b   Sedlářová, Michaela ^a   Pospíšil, Pavel ^a  

^a PALACKÝ UNIVERSITY   (Czech Republic)

^b JAGIELLONIAN UNIVERSITY   (Poland)

Author keywords

Chloroplast; EPR spin trapping

Indexed keywords

ANTIOXIDANT; BIOLOGICAL PRODUCTION; DICOTYLEDON; ENVIRONMENTAL STRESS; FUNCTIONAL ROLE; LIPID; MUTATION; OXYGEN; SCAVENGING (CHEMISTRY); TOLERANCE; VITAMIN;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

MUTASE; SCAVENGER; SINGLET OXYGEN; TOCOPHEROL; TOCOPHEROL CYCLASE;

ARABIDOPSIS; ARTICLE; CHLOROPLAST; EPR SPIN-TRAPPING; GENETICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; METABOLISM; OXIDATIVE STRESS; PLANT LEAF; RADIATION EXPOSURE; SPIN TRAPPING;

CHLOROPLAST; EPR SPIN-TRAPPING;

ARABIDOPSIS; CHLOROPLASTS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; FREE RADICAL SCAVENGERS; INTRAMOLECULAR TRANSFERASES; OXIDATIVE STRESS; PLANT LEAVES; SINGLET OXYGEN; SPIN TRAPPING; TOCOPHEROLS;

EID: 84891634558     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/pce.12161     Document Type: Article

References (106)

1. Alboresi A., Dall'Osto L., Aprile A., Carillo P., Roncaglia E., Cattivelli L. & Bassi R. (2011) Reactive oxygen species and transcript analysis upon excess light treatment in wild-type Arabidopsis thaliana vs a photosensitive mutant lacking zeaxanthin and lutein. BMC Plant Biology 11, 62-83.
2. Apel K. & Hirt H. (2004) Reactive oxygen species: metabolism, oxidative stress and signal transduction. Annual Review of Plant Biology 55, 373-399.
3. Arnoux P., Morosinotto T., Saga G., Bassi R. & Pignol D. (2009) A structural basis for the pH-dependent xanthophyll cycle in Arabidopsis thaliana. The Plant Cell 7, 2036-2044.
4. Aro E.-M., Virgin I. & Andersson B. (1993) Photoinhibition of photosystem II: inactivation, protein damage and turnover. Biochimica et Biophysica Acta 1143, 113-134.
5. Aronsson H. & Jarvis P. (2002) A simple method for isolating import-competent Arabidopsis chloroplasts. FEBS Letters 529, 215-220.
6. Asada K. (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiology 141, 391-396.
7. Austin J.R., Frost E., Vidi P.A., Kessler F. & Staehelin L.A. (2006) Plastoglobuls are lipoprotein subcompartments of the chloroplast that are permanently coupled to thylokoid membranes and contain biosynthetic enzymes. The Plant Cell 18, 1693-1703.
8. Bailey-Serres J. & Mittler R. (2006) The roles of reactive oxygen species in plant cells. Plant Physiology 141, 311.
9. Caliandro R., Nagel K.A., Kastenholz B., Bassi R., Li Z., Niyogi K.K., Pogson B.J., Schurr U. & Matsubara S. (2013) Effect of altered α- and β-branch carotenoid biosynthesis on photoprotection and whole-plant acclimation of Arabidopsis to photo-oxidative stress. Plant, Cell & Environment 36, 438-453.
10. Dall'Osto L., Fiore A., Cazzaniga S., Giuliano G. & Bassi R. (2007) Different roles of alpha- and beta-branch xanthophylls in photosystem assembly and photoprotection. Journal of Biological Chemistry 282, 35056-35068.
11. Dall'Osto L., Cazzaniga S., Havaux M. & Bassi R. (2010) Enhanced photoprotection by protein bound vs free chlorophyll pools: a comparative analysis of chlorophyll b and xanthophyll biosynthesis mutants. Molecular Plant 3, 576-593.
12. Del Rio D., Stewart A.J. & Pellegrini N. (2005) A review of recent studies on malondialdehyde as toxic molecule and biological marker of oxidative stress. Nutrition Metabolism and Cardiovascular Diseases 15, 316-328.
13. Dörmann P. (2007) Functional diversity of tocochromanols in plants. Planta 225, 269-276.
14. Driever S.M., Fryer M.J., Mullineaux P.M. & Baker N.R. (2009) Imaging of reactive oxygen species in vivo. Methods in Molecular Biology 479, 109-116.
15. Fischer B.B., Eggen R.I.L., Trebst A. & Krieger-Liszkay A. (2006) The glutathione peroxidase homologous gene Gpxh in Chlamydomonas reinhardtii is upregulated by singlet oxygen produced in photosystem II. Planta 223, 583-590.
16. Fischer B.B., Krieger-Liszkay A., Hideg E., Šnyrychová I., Wiesendanger M. & Eggen R.I.L. (2007) Role of singlet oxygen in chloroplast to nucleus retrograde signaling in Chlamydomonas reinhardtii. FEBS Letters 581, 5555-5560.
17. Fischer B.B., Eggen R.I.L. & Niyogi K.K. (2010) Characterization of singlet oxygen-accumulating mutants isolated in a screen for altered oxidative stress response in Chlamydomonas reinhardtii. BMC Plant Biology 10, 279-291.
18. Flors C., Fryer M.J., Waring J., Reeder B., Bechtold U., Mullineaux P.M., Nonell S., Wilson M.T. & Baker N.R. (2006) Imaging the production of singlet oxygen in vivo using a new fluorescent sensor, Singlet oxygen sensor green. Journal of Experimental Botany 57, 1725-1734.
19. Foreman J., Demidchik V., Bothwell J.H., etal. (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422, 442-446.
20. Foyer C.H. & Noctor G. (2003) Redox sensing and signaling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiologia Plantarum 119, 355-364.
21. Foyer C.H. & Noctor G. (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. The Plant Cell 17, 1866-1875.
22. Foyer C.H. & Shigeoka S. (2011) Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiology 155, 93-100.
23. Fukuzawa K., Matsuura K., Tokumura A., Suzuki A. & Terao J. (1997) Kinetics and dynamics of singlet oxygen scavenging by α-tocopherol in phospholipid model membranes. Free Radical Biology and Medicine 22, 923-930.
24. Gruszka J. & Kruk J. (2007) RP-LC for determination of plastochromanol, tocotrienols in plant oils. Chromatographia 66, 909-913.
25. Gruszka J., Pawlak A. & Kruk J. (2008) Tocochromanols, plastoquinol and other biological prenyllipids as singlet oxygen quenchers-determination of singlet oxygen quenching rate constants and oxidation products. Free Radical Biology and Medicine 45, 920-928.
26. Hakala-Yatkin M., Sarvika P., Paturi P., Mäntysaari M., MAttila H., Tyystjärvi T., Nedbal L. & Tyystjärvi E. (2011) Magnetic field protects plants against high light by slowing down production of singlet oxygen. Physiologia Plantarum 142, 26-34.
27. Havaux M. (2003) Spontaneous and thermoinduced photon emission: new methods to detect and quantify oxidative stress in plants. Trends in Plant Science 8, 409-413.
28. Havaux M., Eymery F., Porfirova S., Rey P. & Dörmann P. (2005) Vitamin E protects against photoinhibition and photooxidative stress in Arabidopsis thaliana. The Plant Cell 17, 3451-3469.
29. Havaux M., Triantaphylidès C. & Genty B. (2006) Autoluminescence imaging: a non-invasive tool for mapping oxidative stress. Trends in Plant Science 11, 480-484.
30. Henry M.F., McCabe T.C., de Bruxelles G.L. & Roberts M.R. (2004) Use of a highly sensitive two-dimensional luminescence imaging system to monitor endogenous bioluminescence in plant leaves. BMC Plant Biology 4, 19.
31. Hideg É., Spetea C. & Vass I. (1994) Singlet oxygen and free radical production during acceptor and donor side induced photoinhibition: studies with spin trapping EPR spectroscopy. Biochimica et Biophysica Acta 1186, 143-152.
32. Hideg É., Kálai T., Hideg K. & Vass I. (1998) Photoinhibition of photosynthesis in vivo results in singlet oxygen production detection via nitroxide-induced fluorescence quenching in broad bean leaves. Biochemistry 37, 11405-11411.
33. Hideg É., Kálai T., Kós P.B., Asada K. & Hideg K. (2006) Singlet oxygen in plants - its significance and possible detection with double (fluorescent and spin) indicator reagents. Photochemistry and Photobiology 82, 1211-1218.
34. Inoue S., Ejima K., Iwai E., Hayashi H., Apel J., Tyystjärvi E., Murata N. & Nishiyama Y. (2011) Protection of α-tocopherol of the repair of photosystem II during photoinhibition in Synechocystis Sp. PCC 6803. Biochimica et Biophysica Acta 1807, 236-241.
35. Kaiser S., DiMascio P., Murphy M.E. & Sies H. (1990) Physical and chemical scavenging of singlet molecular oxygen by tocopherols. Archives of Biochemistry and Biophysics 277, 101-108.
36. Kálai T., Hideg É., Vass I. & Hideg K. (1998) Double (fluorescent and spin) sensors for detection of reactive oxygen species in the thylakoid membranes. Free Radical Biology and Medicine 24, 649-652.
37. Kanwischer M., Porfirova S., Bergmüller E. & Dörmann P. (2005) Alterations in tocopherol cyclase activity in transgenic and mutant plant of Arabidopsis affect tocopherol content, tocopherol composition and oxidative stress. Plant Physiology 137, 713-123.
38. Kobayashi M., Sasaki K., Enomoto M. & Ehara Y. (2007) Highly sensitive determination of transient generation of biophotons during hypersensitive response to cucumber mosaic virus in cowpea. Journal of Experimental Botany 58, 465-472.
39. Komenda J., Sobotka R. & Nixon P.J. (2012) Assembling and maintaining the photosystem II complex in chloroplasts and cyanobacteria. Current Opinion in Plant Biology 15, 245-251.
40. Krieger-Liszkay A. (2005) Singlet oxygen production in photosynthesis. Journal of Experimental Botany 56, 337-346.
41. Krieger-Liszkay A. & Trebst A. (2006) Tocopherol is a scavenger of singlet oxygen produced by the triplet state of chlorophyll in the PSII reaction centre. Journal of Experimental Botany 57, 1677-1684.
42. Krieger-Liszkay A., Fufezan C. & Trebst A. (2008) Singlet oxygen production in photosystem II and related protection mechanism. Photosynthesis Research 98, 551-564.
43. Kruk J. & Trebst A. (2008) Plastoquinol as a singlet oxygen scavenger in photosystem II. Biochimica et Biophysica Acta 1777, 154-162.
44. Kruk J., Holländer-Czytko H., Oettmeier W. & Trebst A. (2005) Tocopherol as a singlet oxygen scavenger in photosystem II. Journal of Plant Physiology 162, 749-757.
45. Kruk J., Szymańska R. & Krupinska K. (2008) Tocopherol quinone content of green algae and higher plants revised by a new high-sensitive fluorescence detection method using HPLC - effects of high light stress and senescence. Journal of Plant Physiology 165, 1238-1247.
46. Kumar R., Raclaru M., Schüßeler T., etal. (2005) Characterisation of plant tocopherol cyclases and their overexpression in Brassica napus. FEBS Letters 579, 1357-1364.
47. Li Z., Ahn T.K., Avenson T.J., Ballottari M., Cruz J.A., Kramer D.M., Bassi R., Fleming G.R., Keasling J.D. & Niyogi K.K. (2009) Lutein accumulation in the absence of zeaxanthin restores nonphotochemical quenching in the Arabidopsis thaliana npq1 mutant. The Plant Cell 21, 1798-1812.
48. Lichtenthaler H.K. (2007) Biosynthesis, accumulation and emission of carotenoids, tocopherols, plastoquinone and isoprene in leaves under high photosynthetic irradiance. Photosynthesis Research 92, 163-179.
49. Liu X., Hua X., Guo J., Qi D., Wang L., Liu Z., Jin Z., Chen S. & Liu G. (2008) Enhanced tolerance to drought stress in transgenic tobacco plants overexpressing VTE1 for increased tocopherol production from Arabidopsis thaliana. Biotechnological Letters 30, 1275-1280.
50. Macpherson A.N., Telfer A., Barber J. & Truscott T.G. (1993) Direct detection of singlet oxygen from isolated photosystem II reaction centers. Biochimica et Biophysica Acta 114, 301-309.
51. Matringe M., Ksas B., Rey P. & Havaux M. (2008) Tocotrienols the unsaturated forms of vitamin E can function as antioxidants and lipid protectors in tobacco leaves. Plant Physiology 147, 764-778.
52. Mène-Saffrané L., Jones A.D. & DellaPenna D. (2010) Plastochromanol-8 and tocopherols are essential lipid-soluble antioxidants during seed desiccation and quiescence in Arabidopsis. Proceedings of the National Academy of Sciences USA 107, 17815-17820.
53. Miller G., Shulaev V. & Mittler R. (2008) Reactive oxygen signaling and abiotic stress. Physiologia Plantarum 133, 481-489.
54. Mittler R. (2002) Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science 7, 405-410.
55. Mittler R. (2006) Abiotic stress, the field environment and stress combination. Trends in Plant Science 11, 15-19.
56. Mittler R., Vanderauwera S., Gollery M. & Van Breusegem F. (2004) Reactive oxygen gene network of plants. Trends in Plant Science 9, 490-498.
57. Moan J. & Wold E. (1979) Detection of singlet oxygen production by ESR. Nature 279, 450-451.
58. Munné-Bosch S. & Alegre L. (2002) The function of tocopherols and tocotrienols in plants. Critical Reviews in Plant Sciences 21, 31-57.
59. Murata N., Takahashi S., Nishiyama Y. & Allakhverdiev S.I. (2007) Photoinhibition of photosystem II under environmental stress. Biochimica et Biophysica Acta 1767, 414-421.
60. Murata N., Allakhverdiev S.I. & Nishiyama Y. (2012) The mechanisms of photoinhibition in vivo: re-evaluations of the roles of catalase, α-tocopherol, non photochemical quenching and electron transport. Biochimica et Biophysica Acta 1817, 1127-1133.
61. Neely W.C., Martin J.M. & Barker S.A. (1988) Products and relative reaction rates of the oxidation of tocopherols with singlet molecular oxygen. Photochemistry and Photobiology 48, 423-428.
62. Nishiyama Y., Yamamoto H., Allakhverdiev S.I., Inaba M., Yokota A. & Murata N. (2001) Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery. The EMBO Journal 20, 5587-5594.
63. Nishiyama Y., Allakhverdiev S.I. & Murata N. (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochimica et Biophysica Acta 1757, 742-749.
64. Nishiyama Y., Allakhverdiev S.I. & Murata N. (2011) Protein synthesis is primary target of reactive oxygen species in the photoinhibition of photosystem II. Physiologia Plantarum 142, 35-46.
65. Nixon P.J., Michoux F., Yu J., Boehm M. & Komenda J. (2010) Recent advances in understanding the assembly and repair of photosystem II. Annals of Botany 106, 1-16.
66. Nowicka B. & Kruk J. (2012) Plastoquinol is more active than - tocopherol in singlet oxygen scavenging during high light stress of Chlamydomonas reinhardtii. Biochimica et Biophysica Acta 1817, 389-394.
67. Nowicka B., Gruszka J. & Kruk J. (2013) Function of plastochromanol and other biological prenyllipids in the inhibition of lipid peroxidation - a comparative study in model systems. Biochimica et Biophysica Acta Biomembrane 1828, 233-240.
68. Penuelas J. & Munné-Bosch S. (2005) Isoprenoids: an evolutionary pool for photoprotection. Trends in Plant Science 10, 166-169.
69. Piller L.E., Abraham A., Dörmann P., Kessler F. & Besagni C. (2012) Plastid lipid droplets at the crossroads of prenylquinone metabolism. Journal of Experimental Botany 63, 1609-1618.
70. Porfirova S., Bergmüller E., Tropf S., Lemke R. & Dörmann P. (2002) Isolation of an Arabidopsis mutant lacking vitamin E and identification of a cyclase essential for all tocopherol biosynthesis. Proceedings of the National Academy of Sciences USA 99, 12495-12500.
71. Pospíšil P. (2009) Production of reactive oxygen species by photosystem II. Biochimica et Biophysica Acta 1787, 1151-1160.
72. Pospíšil P. (2012) Molecular mechanism of production and scavenging of reactive oxygen species by photosystem II. Biochimica et Biophysica Acta 1817, 218-231.
73. Prasad A. & Pospíšil P. (2011) Linoleic acid-induced ultra weak photon emission from Chlamydomonas reinhardtii as a tool for monitoring of lipid peroxidation in the cell membranes. PLoS ONE 6, e22345.
74. Queval G. & Foyer C.H. (2012) Redox regulation of photosynthetic gene regulation. Philosophical Transactions of the Royal Sociaty B: Biological Sciences 367, 3475-3485.
75. Rastogi A. & Pospíšil P. (2010) Effect of exogenous hydrogen peroxide on biophoton emission from radish root cells. Plant Physiology and Biochemistry 48, 117-123.
76. Rastogi A. & Pospíšil P. (2012) Production of hydrogen peroxide and hydroxyl in potato tuber during the necrotrophic phase of hemibiotrophic pathogen Phytophthora infestans infection. Journal Photochemistry and Photobiology B: Biology 117, 202-206.
77. Rastogi A. & Pospíšil P. (2013) Ultra-weak photon emission as a non-invasive tool for the measurement of oxidative stress induced by UVA radiation in Arabidopsis thaliana. Journal of Photochemistry and Photobiology B: Biology 123, 59-64.
78. Sattler S.E., Cahoon E.B., Coughlan S.J. & DellaPenna D. (2003) Characterization of tocopherol cyclase from higher plants and cyanobacteria. Evolutionary implications for tocopherol synthesis and function. Plant Physiology 132, 2184-2195.
79. Sattler S.E., Gilliland L.U., Magallanes-Lundback M., Pollard M. & DellaPenna D. (2004) Vitamin E is essential for seed longevity and for preventing lipid peroxidation during germination. The Plant Cell 16, 1419-1432.
80. Sattler S.E., Mène-Saffrané L., Farmer E.E., Krischke M., Müller M.J. & DellaPenna D. (2006) Non-enzymatic lipid peroxidation reprograms gene expression and activates defense markers in Arabidopsis tocopherol-defficient mutants. The Plant Cell 18, 3706-3720.
81. Seigneurin-Berny D., Salvi D., Dorne A.-J., Joyard J. & Rolland N. (2008) Percoll-purified and photosynthetically active chloroplasts from Arabidopsis thaliana leaves. Plant Physiology and Biochemistry 46, 951-955.
82. Serbinova E., Kagan V., Han D. & Packer L. (1991) Free radical recycling and intramembrane mobility in the antioxidant properties of alpha-tocopherol and alpha-tocotrienol. Free Radical Biology and Medicine 10, 263-275.
83. Strzalka K., Szymańska R., Świezewska E., Skorupińska-Tudek K. & Suwalsky M. (2009) Tocochromnols, plastoquinone and polyprenols in selected plant species from Chilean Patagonia. Acta Biologica Cracoviensia series Botanica 51, 39-44.
84. Suzuki Y.J. (1993) Structural and dynamic membrane properties of -tocopherol and -tocotrienol: limitation to the molecular mechanism of their antioxidant potency. Biochemistry 32, 10692-10699.
85. Szymańska R. & Kruk J. (2010a) Plastoquinol is the main prenyllipid synthesized during acclimation to high light conditions in Arabidopsis and is converted to plastochromanol by tocopherol cyclase. Plant and Cell Physiology 51, 537-545.
86. Szymańska R. & Kruk J. (2010b) Identification of hydroxy-plastochromanol in Arabidopsis leaves. Acta Biochimica Polonica 57, 105-108.
87. Telfer A. (2002) What is β-carotene doing in the photosystem II reaction centre. Philosophical Transactions of the Royal Society B: Biological Sciences 357, 1431-1440.
88. Telfer A. (2005) Too much light? How beta-carotene protects the photosystem II reaction centre. Photochemical and Photobiological Sciences 4, 950-956.
89. Telfer A., Bishop S.M., 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. Journal of Biological Chemistry 269, 13244-13253.
90. Trebst A. (2003) Function of β-carotene and tocopherol in photosystem II. Z Naturforsch 58c, 609-620.
91. Trebst A. & Depka B. (1997) Role of carotene in the rapid turnover and assembly of photosystem II in Chlamydomonas reinhardtii. FEBS Letters 400, 359-362.
92. Trebst A., Depka B. & Holländer-Czytko H. (2002) A specific role for tocopherol and of chemical singlet oxygen quenchers in the maintenance of photosystem II structure and function in Chlamydomonas reinhardtii. FEBS Letters 516, 156-160.
93. Triantaphylidès C. & Havaux M. (2009) Singlet oxygen in plant, production, detoxification and signaling. Trends in Plant Science 14, 219-228.
94. Triantaphylidès C., Krischke M., Hoeberichts F.A., Ksas B., Gresser G., Havaux M., Van Breusegem F. & Mueller M.J. (2008) Singlet oxygen is the major reactive oxygen species involved in photooxidative damage to plants. Plant Physiology 148, 960-968.
95. Truscott T.G. (1990) The photophysics and photochemistry of the carotenoids. Journal Photochemistry and Photobiology B: Biology 6, 359-371.
96. Tyystjärvi E. (2008) Photoinhibition of photosystem II and the Photodamage of oxygen evolving cluster. Coordination Chemistry Reviews 252, 361-376.
97. Tyystjärvi E. (2013) Photoinhibition of photosystem II. International review of cell and molecular biology 300, 243-303.
98. Vass I. (2012) Molecular mechanism of Photodamage in the photosystem II complex. Biochimica et Biophysica Acta 1817, 209-217.
99. Wolf G. (2005) The discovery of the antioxidant function of vitamin E: the contribution of H.A. Mattill. Journal of Nutrition 135, 363-366.
100. Yadav D.K. & Pospíšil P. (2012) Evidence on the formation of singlet oxygen in the donor side of photoinhibition of photosystem II: EPR spin-trapping study. PLoS ONE 7, e45883.
101. Yadav D.K., Kruk J., Sinha R.K. & Pospíšil P. (2010) Singlet oxygen scavenging activity of plastoquinol in photosystem II of higher plants: electron paramagnetic resonance spin trapping study. Biochimica et Biophysica Acta 1797, 1807-1811.
102. Yamamoto Y. (2001) Quality control of photosystem II. Plant and cell Physiology 42, 121-128.
103. Yamauchi R. (2003) Oxidation products of vitamin E in the peroxidation of liposomal and biological systems. Journal of Clinical Biochemistry and Nutrition 34, 111-120.
104. Yamauchi R. (2007) Addition products of alpha-tocopherol with lipid derived free radicals. Vitamins and Hormones 76, 309-327.
105. Yoshida Y., Niki E. & Noguchi N. (2003) Comparative study on the action of tocopherols and tocotrienols as antioxidant: chemical and physical effects. Chemistry and Physics of Lipids 123, 63-75.
106. Zbierzak A.M., Kanwischer M., Wille C., etal. (2010) Intersection of the tocopherol and plastoquinol metabolic pathways at the plastoglobule. Biochemical Journal 425, 389-399.