Chloroplasts and strong photoprotective mechanisms

Current Chemical Biology

Volumn 6, Issue 3, 2012, Pages 254-264

  Szymanska, Renata ^a   Latowski, Dariusz ^a   Strzalka, Kazimierz ^a  

^a JAGIELLONIAN UNIVERSITY   (Poland)

Author keywords

Carotene; Chloroplast; Photoinhibition; Photoprotection; Plastoquinone; Reactive oxygen species; Tocopherols; Xantophyll cycle

Indexed keywords

ANTIOXIDANT; CAROTENOID; CHLOROPHYLL; LIPID; PIGMENT; REACTIVE OXYGEN METABOLITE; XANTHINE DERIVATIVE; XANTHOPHYLL;

BIOTRANSFORMATION; BLEACHING; CHLOROPLAST; LIGHT DAMAGE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVIEW; THYLAKOID MEMBRANE; WATER CYCLE;

EID: 84874903155     PISSN: 22127968     EISSN: 18723136     Source Type: Journal    
DOI: 10.2174/2212796811206030008     Document Type: Review

References (116)

1. Barber J, Rivas JD. A functional model for the role of cytochrome b-559 in the protection against donor and acceptor side photoinhibition. Proc Natl Acad Sci USA 1993; 90: 10942-6.
2. Yamamoto Y. Quality control of photosystem II. Plant Cell Physiol 2001; 42: 121-8.
3. Renger G (2008) Functional pattern of photosystem II. In: Renger G Eds. Primary processes in photosynthesis, RSC Publishing Cambridge, UK (part 2) 2008; 237-290.
4. Ferreira KN, Iverson TM, Maghlaoui K, et al. Architecture of the photosynthetic oxygen-evolving centre. Science 2004; 303: 1831-183.
5. Loll B, Kern J, Saenger W, et al. Towards complete cofactor arrangement in the 3.0 Å resolution a structure of photosystem II. Nature 2005; 438: 1040-4.
6. Adir N, Zer H, Shochat S, Ohad I. Photoinhibition-a historical perspective. Photosynth Res 2003; 76: 343-70.
7. Kok B. On the inhibition of photosynthesis by intense light. Biochim Biophys Acta 1956; 21: 234-44.
8. Ewart AJ. On assimilatory inhibition in plants. J Linnean Soc Bot 1986; 31: 364-461.
9. Nishiyama Y, Yamamoto H, Allakhverdiev SI, et al. Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery. EMBO J 2001; 20: 5587-94.
10. Aro E-M, Virgin I, Andersson B. Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1993; 1143: 113-34.
11. Allakhverdiev SI, Murata N. Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage-repair cycle of photosystem II in Synechocysts sp. PCC 6803. Biochim Biophys Acta 2004; 1657: 23-32.
12. Takahashi S, Murata N. How do environmental stresss accelerate photoinhibition? Trends Plant Sci 2008; 13: 178-82.
13. Raven JA. The cost of photoinhibition. Physiologia Plantarum 2011; 142: 87-104.
14. Yoshioka M, Yamamoto Y. Quality control of photosystem II: Where and how does the degradation of the D1 protein by FtsH proteases start under light stress? Fact and hypotheses. J. Photochem Photobiol B Biology 2011; 104: 229-35.
15. Kyle DJ, Ohad I, Arntzen CJ. Membrane protein damage and repair: selective loss of quinine-protein function in chloroplast membrane. Proc Natl Acad Sci USA 1984; 181: 4070-4.
16. Aro E-M, Suorsa M, Rokka A, et al. Dynamics of photosystem II: a proteomic approach to thylakoid protein complexes. J Exp Bot 2005; 56: 347-56.
17. A species promote chlorophyll triplet formation. Proc Natl Acad Sci USA 1992; 89: 1408-12.
18. Kruk J, Trebst A. Plastoquinol as a singlet oxygen scavenger in photosystem II. Biochim Biophys Acta 2008; 1777: 154-62.
19. Vavilin D, Vermaas W. Continuous chlorophyll degradation accompanied by chlorophyllide and phytol reutilization for chlorophyll synthesis in Synechococystis sp. 6803. Biochim Biophys Acta 2007; 1767: 14831-8.
20. Krieger-Liszkay A, Fufezan C, Trebst A. Singlet oxygen production in photosystem II and related protection mechanism. Photosynth Res 2008; 98: 551-64.
21. Keren N, Berg A, van Kan PJM, et al. Mechanism of photosystem II photoinactivation and D1 protein degradation at low light: The role of back electron flow. Proc Natl Acad Sci USA 1997; 94: 1579-84.
22. Van Gorkom HJ, Schelvis JPM. Kok's oxygen clock: what makes it tick? The structure of P680 and consequences of its oxidizing power. Photosynth Res 1993; 38: 297-301.
23. Edelman M, Mattoo AK. D1-protein dynamics in photosystem II: the lingering enigma. Photosynth Res 2008; 98: 609-20.
24. Vass I. Molecular mechanisms of photodamage in the photosystem II complex. Biochim Biophys Acta 2012; 1817: 209-17.
25. Tyystjarvi E. Photoinhibition of photosystem II and photodamage of the oxygen evolving manganese cluster. Coord Chem Rev 2008; 252: 361-76.
26. Hakala M, Tuominen I, Keranen M, et al. Evidence for the role of the oxygen-evolving manganese complex in photoinhibition of photosystem II. Biochim Biophys Acta 2005; 1706, 68-80.
27. Ohnishi N, Allakhverdiev SI, Takahashi S, et al. 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. Biochem 2005; 44: 8494-9.
28. Jegerschold C, Virgin I, Styring S. Light-dependent degradation of the D1 protein in photosystem II is accelerated after inhibition of the water splitting reaction. Biochem 1990; 29: 6179-86.
29. Kasahara M, Kagawa T, Oikawa K, Suetsugu, N Miyao M, Wada M. Chloroplast avoidance movement reduces photodamage in plants. Nature 2002; 420: 69: 829-32.
30. Sztatelman O, Waloszek A, Banas AK, Gabrys H. Photoprotective function of chloroplast avoidance movement: In vivo chlorophyll fluorescence study. J Plant Physiol 2010; 167: 709-16.
31. Munne-Bosch S. [-Tocopherol: A multifaceted molecule in plants. Vitamins and Hormones 2007; 76: 375-92.
32. Pospisil P. Molecular mechanisms of production and scavenging of reactive oxygen species by photosystem II. Biochim Biophys Acta 2012; 1817: 218-31.
33. Asada K. Production and scavenging of reactive oxygen species in chloroplasts and their function. Plant Physiol 2006; 141: 391-6.
34. Krieger-Liszkay A. Singlet oxygen production in photosynthesis. J Exp Bot 2005; 56: 337-46.
35. 6f complex protects photosystem II from photoinfibition. FEBS Lett 2000; 486: 191-4.
36. Tjus SE, Scheller HV, Andersson B, et al. Active oxygen produced during selective excitation of photosystem I is damaging not only to photosystem I, but also to photosystem II. Plant Physiol 2001; 125: 2007-15.
37. Prasil O, Adir N, Ohad I. Dynamics of photosystem II: mechanism of photoinhibition and recovery process. In: Barber J; Eds. Topics in photosynthesis, the photosystems: structure, function and molecular biology. Elsevier, Amsterdam 1992; 220-50.
38. Nishuyama Y, Allakhverdiev SI, Murata N. A new paradigm for the action of reactive species in the photoinhibition of photosystem II. Biochim Biophys Acta 2006; 1757: 742-9.
39. Logan BA, Kornyeyev D, Hardison J, et al. The role of antioxidant enzymes in photoprotection. Photosynth Res 2006; 88: 119-32.
40. Asada K. The Water-Water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 1999; 50: 601-39.
41. rd ed). Oxford Universisty Press, Oxford 1999.
42. 559 in photosystem II. Biochim Biophys Acta 2009; 1787: 985-94.
43. Zhang Y, Ding S, Lu Q, et al. Characterization of photosystem II in transgenic tobacco plants with decreased iron superoxide dismutase. Biochim Biophys Acta 2011; 1807: 391-403.
44. Sheptovitsky YG, Brudvig GW. Isolation and characterization of spinach photosystem II membrane-associated catalase and polyphenols oxidase. Biochem 1996; 35: 16255-63.
45. Munne-Bosch S, Alegre L. The function of tocopherols and tocotrienols in plants. Crit Rev Plant Sci 2002; 21: 31-57.
46. Szymanska R, Kruk J. Tocopherol content and isomers' composition in selected plant species. Plant Physiol Biochem 2008; 46: 29-33.
47. Nowicka B, Kruk J. Occurrence, biosynthesis and function of isoprenoid quinones. Biochim Biophys Acta 2010; 1797: 1587-1605.
48. Szymanska R, Kruk J. Plastoquinol is the main prenyllipid synthesized during acclimation to high-light conditions in Arabidopsis and is converted to plastochromanol by tocopherol cyclase. Plant Cell Physiol 2010; 51: 537-45.
49. Szymanska R, Kruk J. Identification of hydroxy-plastochromanol in Arabidopsis leaves. Acta Biochim Pol 2010; 57: 105-8.
50. Kruk J, Pisarski A, Szymanska R. Novel vitamin E forms in leaves of Kalanchoe daigremontiana and Phaseolus coccineus. J Plant Physiol 2011; 168: 2021-7.
51. Maeda H, DellaPenna D. Tocopherol function in photosynthetic organisms. Curr Opin Plant Biol 2007; 10: 260-5.
52. Trebst A, Depka B, Holländer-Czytko H. A specific role for tocopherol and of chemical singlet oxygen quenchers in the maintenance of photosystem II structure and function in Chlamydomonas reinhardtii. FEBS Lett 2002; 516: 156-60.
53. Havaux M, Lutz C, Grimm B. Chloroplast membrane photostability in chlP transgenic tobacco plants deficient in tocopherols. Plant Physiol 2003; 132: 300-10.
54. Havaux M, Eymery F, Porfirova S, et al. Vitamin E protects against photoinhibition and photooxidative stress in Arabidopsis thaliana. Plant Cell 2005; 17: 3451-69.
55. Kruk J, Hollander-Czytko H, Oettmeier W, et al. Tocopherol as a singlet oxygen scavenger in photosystem II. J Plant Physiol 2005; 162: 749-57.
56. Gruszka J, Pawlak A, Kruk J. Tocochromanols, plastoquinol and other biological prenyllipids as singlet oxygen quenchers-determination of singlet oxygen quenching rate constants and oxidation products. Free Rad Biol Med 2008; 45: 920-8.
57. Kruk J, Burda K, Schmid GH, et al. Function of plastoquinones B and C as an electron acceptors in photosystem II and fatty acid analysis of plastoquinone B. Z Naturforsch 1998; 52c: 766-74.
58. 559 in the presence of plastoquinones. J Biol Chem 2001; 276: 86-91.
59. Inoue S, Ejima K, Iwai E, et al. Protection by α-tocopherol of the repair of photosystem II during photoinhibition in Synechocystis sp. PCC 6803. Biochim Biophys Acta 2011; 1807: 236-41.
60. Hakala-Yatkin M, Sarvikas P, Paturi P, et al. Magnetic field protects plants against high light by slowing down production of singlet oxygen. Physiol Plant 2011; 142: 26-34.
61. Yadav DK, Kruk J, Sinha RK, et al. Singlet oxygen scavenging activity of plastoquinol in photosystem II of higher plants: electron paramagnetic resonance spin-trapping study. Biochim Biophys Acta 2010; 1797: 1807-11.
62. Telfer A. What is beta-carotene doing in the photosystem II reaction centre? Phil Trans R Soc London, Ser B 2002; 357: 1431-9.
63. Li ZR, Wakao S, Fischer BB, et al. Sensing and responding to excess light. Annu Rev Plant Biol 2009; 60: 239-60.
64. Horton P, Wentworth M, Ruban A. Control of the light harvesting function of chloroplast membranes: the LHCII-aggregation model for non-photochemical quenching. FEBS Lett 2005; 579: 4201-6.
65. Jahns P, Holzwarth AR. The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim Biophys Acta 2012; 1817: 182-93.
66. Latowski D, Kuczynska P, Strzalka K. Xanthophyll cycle-a mechanism protecting plants against oxidative stress. Redox Report 2011; 16: 78-90.
67. Van Dorssen RJ, Breton J, Plijter JJ, et al. Spectroscopic properties of the reaction center and of the 47 kDa chlorophyll protein of photosystem II. Biochim Biophys Acta 1987; 893: 267-74.
68. Breton J, Duranton J, Satoh K. Orientation of pigments in the reaction center and the core antenna of photosystem II. In: H. Scheer, S. Schneider Eds. Photosynthetic light-harvesting systems: organization and function. Walter de Gruyter 1998; 375-86.
69. Kwa SLS, Newell WR, Van Grondelle R, et al. The reaction center of photosystem II studied by polarized fluorescence spectroscopy. Biochim Biophys Acta 1992; 1099: 193-202.
70. Tomo T, Mimuro M, Iwaki M, et al. Topology of pigments in the isolated photosystem II reaction center studied by selective extraction. Biochim Biophys Acta 1997; 1321: 21-30.
71. Telfer A, Barber J. Evidence for the photo-induced oxidation of the primary electron donor P680 in the isolated photosystem II reaction centre. FEBS Lett 1989; 246: 223-8.
72. de Las Rivas J, Telfer A, Barber J. Two coupled [-carotene molecules protect P680 from photodamage in isolated photosystem II reaction centers. Biochim Biophys Acta 1993; 1142: 155-64.
73. Telfer A, Barber J. Role of carotenoid bound to the photosystem II reaction centre. In: Mathis P. Eds. Photosynthesis: from light to the biosphere. Vol. IV Dordrecht, The Netherlands: Kluwer 1995; 15-20.
74. Hanley J, Deligiannakis Y, Pascal A, et al. Carotenoid oxidation in photosystem II. Biochem 1999; 38: 8189-95.
75. Faller P, Maly T, Rutherford AW, et al. Chlorophyll and carotenoid radicals in photosystem II studied by pulsed ENDOR. Biochem 2001; 40: 320-6.
76. Stewart DH, Cua A, Chisholm DA, et al. Identification of histidine 118 in the D1 polypeptide of photosystem II as the axial ligand to chlorophyll Z. Biochem 1998; 37: 10040-6.
77. Shigemori K, Hara H, Kawamori A, et al. Determination of the distances from tyrosine D to QA and chlorophyll Z in photosystem II studied by '2 + 1' pulsed EPR. Biochim Biophys Acta 1998; 1363: 187-98.
78. Ruffle SV, Wang J, Johnston HG, et al. Photosystem II peripheral chlorophyll mutants in Chlamydomonas reinhardtii. Biochemical characterization and sensitivity to photo-inhibition. Plant Physiol 2001; 127, 633-44.
79. Wang J, Gosztola D, Ruffle SV, et. al. Functional asymmetry of photosystem II D1 and D2 peripheral chlorophyll mutants of Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 2002; 99: 4091-6.
80. 559 may function to protect photosystem II from photoinhibition. Biochem 1988; 27: 6653-8.
81. Edge R, McGarvey DJ, Truscott TG. The carotenoids as antioxidants. J Photochem Photobiol B: Biol 1997; 41:189-200.
82. Garcia-Plazaola JI, Matsubara S, Osmond CB. The lutein epoxide cycle in higher plants: its relationships to other xanthophyll cycles and possible functions. Funct Plant Biol 2007; 34: 759-73.
83. Latowski D, Grzyb J, Strzalka K. The xanthophyll cycle-molecular mechanism and physiological significance. Acta Physiol Plant 2004; 26: 197-212.
84. Muller P, Li XP, Niyogi KK. Non-photochemical quenching. A response to excess light energy. Plant Physiol 2001; 125: 1558-66.
85. Niyogi KK. Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 1999; 50: 333-59.
86. Horton P, Ruban AV, Walters RG. Regulation of light harvesting in green plants. Annu Rev Plant Physiol Plant Mol Biol 1996; 47: 655-84.
87. de Bianchia S, Ballottaria M, Dall'Ostoa L, Bassi R. Regulation of plant light harvesting by thermal dissipation of excess energy. Biochem Soc Trans 2010; 38: 651-60.
88. Sapozhnikov DI, Krasovskaya TA, Maevskaya AN. Change in the interrelationship of the basic carotenoids of the plastids of green leaves under the action of light. Dokl Akad Nauk USSR 1957; 113: 465-7.
89. Yamamoto HY, Nakayama TOM, Chichester CO. Studies on the light and dark interconversions of leaf xanthophylls. Arch Biochem Biophys 1962; 97: 168-73.
90. Jahns P, Latowski D, Strzalka K. Mechanism and regulation of the violaxanthin cycle: the role of antenna proteins and membrane lipids. Biochim Biophys Acta 2009; 1787: 3-14.
91. Adams WW, Demmig-Adams B, Verhoeven AS, Baker DH. Photoinhibition during winter stress: involvement of sustained xanthophyll cycle-dependent energy dissipation. Plant Physiol 1995; 22: 261-76.
92. Ruban AV, Horton P. The xanthophyll cycle modulates the kinetics of non-photochemical energy dissipation in isolated lightharvesting complexes, intact chloroplasts, and leaves of spinach. Plant Physiol 1999; 119: 531-42.
93. Nilkens M, Kress E, Lambrev PH, et al. Identification of a slowly inducible zeaxanthin-dependent component of nonphotochemical quenching of chlorophyll fluorescence generated under steady state conditions in Arabidopsis. Biochim Biophys Acta 2010; 1797: 466-75.
94. Lavaud J, Rosseau B, Etienne AL. In diatoms, a transthylakoid proton gradient alone is not sufficient to induce a nonphotochemical fluorescence quenching. FEBS Lett 2002; 523:163-6.
95. Lavaud J, Rosseau B, van Gorkom HJ, Etienne AL. Influence of the diadinoxanthin pool size on photoprotection in the marine planktonic diatom Phaeodactylum tricornutum. Plant Physiol 2002; 129: 1398-406.
96. Grouneva I, Jakob T, Wilhelm C, Goss R. A new multicomponent NPQ mechanism in the diatom Cyclotella meneghiniana. Plant Cell Physiol 2008; 49:1217-25.
97. Grouneva I, Jakob T, Wilhelm C, Goss R. The regulation of xanthophyll cycle activity and of non-photochemical fluorescence quenching by two alternative electron flows in the diatoms Phaeodactylum tricornutum and Cyclotella meneghiniana. Biochim Biophys Acta 2009; 1787: 929-38.
98. Zudaire L, Roy S. Photoprotection and long-term acclimation to UV radiation in the marine diatom Thalassiosira weissflogii. J Photochem Photobiol B Bio. 2001; 62: 26-34.
99. Niyogi KK, Björkman O, Grossman AR. Chlamydomonas xanthophyll cycle mutants identified by video imaging of chlorophyll fluorescence quenching. Plant Cell 1997; 9: 1369-80.
100. Llorens L, Aranda X, Abad́i{dotless}a A, Fleck I. Variations in Quercus ilex chloroplast pigment content during summer stress: involvement in photoprotection according to principal component analysis. Funct Plant Biol 2002; 29: 81-8.
101. Matsubara S, Naumann M, Martin R, et al. Slowly reversible deepoxidation of lutein-epoxide in deep shade leaves of a tropical tree legume may 'lock-in' lutein-based photoprotection during acclimation to strong light. J Exp Bot 2005; 56: 461-8.
102. Frank HA, Bautista JA, Josue SJ, Young AJ Mechanism of nonphotochemical quenching in green plants: energies of the lowest excited singlet states of violaxanthin and zeaxanthin. Biochem 2000; 39: 2831-7.
103. Polivka T, Sundstrom V Ultrafast dynamics of carotenoid excited states-from solution to natural and artificial systems. Chem Rev 2004; 104: 2021-71.
104. Mueller MG, Lambrev P, Reus M, Wientjes E, Croce R, Holzwarth AR. Singlet energy dissipation in the photosystem II lightharvesting complex does not involve energy transfer to carotenoids. ChemPhysChem 2010; 11: 1289-1296.
105. Liao PN, Holleboom CP, Wilk L, Kuehlbrandt W, Walla PJ. Correlation of Car S1 β Chl with Chl β Car S1 energy transfer supports the excitonic model in quenched light harvesting Complex II. J Phys Chem B. 2010; 114: 15650-5.
106. Bode S, Quentmeier CC, Liao PN, et al. On the regulation of photosynthesis by excitonic interactions between carotenoids and chlorophylls. Proc Nat Acad Sci USA 2009; 106: 12311-6.
107. Ruban AV, Johnson MP, Duffy CDP. The photoprotective molecular switch in the photosystem II antenna. Biochim Biophys Acta 2012; 1817: 167-81.
108. Berera R, van Stokkum IH, Kodis G, et al. Energy transfer, excited-state deactivation, and exciplex formation in artificial caroteno-phthalocyanine light-harvesting antennas. J Phys Chem B 2007; 111: 6868-6877.
109. Ruban AV, Berera R, Ilioaia C, et al. Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 2007; 450: 575-8.
110. Miloslavina Y, Wehner A, Lambrev PH, et al. Far-red fluorescence: a direct spectroscopic marker for LHCII oligomer formation in non-photochemical quenching. FEBS Lett 2008; 582: 3625-31.
111. Holzwarth AR, Miloslavina Y, Nilkens M, Jahns P. Identification of two quenching sites active in the regulation of photosynthetic light-harvesting studied by time-resolved fluorescence. Chem Phys Lett 2009; 483: 262-7.
112. Betterle N, Ballottari M, Zorzan S, et al. Light-induced dissociation of an antenna hetero-oligomer is needed for non-photochemical quenching induction. J Biol Chem 2009; 284: 15255-66.
113. Caffarri S, Croce R, Breton J, Bassi R. The major antenna complex of photosystem II has a xanthophyll binding site not involved in light harvesting. J Biol Chem 2001; 276: 35924-33.
114. Holt NE, Zigmantas D, Valkunas L, Li XP, Niyogi KK, Fleming GR. Carotenoid cation formation and the regulation of photosynthetic light harvesting. Science 2005; 307: 433-6.
115. Avenson TJ, Ahn TK, Zigmantas D, et al. Zeaxanthin radical cation formation in minor light-harvesting complexes of higher plant antenna. J Biol Chem 2008; 283: 3550-8.
116. Avenson TJ, Ahn TK, Niyogi KK, et al. Lutein can act as a switchable charge transfer quencher in the CP26 light-harvesting complex. J Biol Chem 2009; 284: 2830-5.