Xanthophyll cycle – a mechanism protecting plants against oxidative stress

References

• Schafer FQ, Buettner GR. Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic Biol Med 2001;30(11):1191–212. doi: 10.1016/S0891-5849(01)00480-4. PMID 11368918.
   PubMed Web of Science ®Google Scholar
• Lennon SV, Martin SJ, Cotter TG. Dose-dependent induction of apoptosis in human tumour cell lines by widely diverging stimuli. Cell Prolif 1991;24(2):203–14. doi: 10.1111/j.1365-2184.1991.tb01150.x. PMID 2009322.
   PubMed Web of Science ®Google Scholar
• Valko M, Morris H, Cronin MT. Metals, toxicity and oxidative stress. Curr Med Chem 2005;12(10):1161–208. doi: 10.2174/0929867053764635. PMID 15892631.
   PubMed Web of Science ®Google Scholar
• Puddu P, Puddu GM, Cravero E, Rosati M, Muscari A. The molecular sources of reactive oxygen species in hypertension. Blood Press 2008;17(2):70–7.
   PubMed Web of Science ®Google Scholar
• Rodriguez-Pallares J, Parga JA, Joglar B, Guerra MJ, Labandeira-Garcia JL. The mitochondrial ATP-sensitive potassium channel blocker 5-hydroxydecanoate inhibits toxicity of 6-hydroxydopamine on dopaminergic neurons. Neurotox Res 2009;15(1):82–95. Epub 2009 Feb 24.
   PubMed Web of Science ®Google Scholar
• Callaway JK, Lawrence AJ, Jarrott B. AM-36, a novel neuroprotective agent, profoundly reduces reactive oxygen species formation and dopamine release in the striatum of conscious rats after endothelin-1-induced middle cerebral artery occlusion. Neuropharmacology 2003;44:787–800.
   PubMed Web of Science ®Google Scholar
• Starkov AA. The role of mitochondria in reactive oxygen species metabolism and signaling. Ann N Y Acad Sci 2008;1147:37–52.
   PubMed Web of Science ®Google Scholar
• Parvaiz A, Maryam S, Satyawati S. Reactive oxygen species, antioxidants and signaling in plants. J Plant Biol 2008;51(3):167–73.
   Web of Science ®Google Scholar
• Slesak I, Libik M, Karpinska B, Karpinski S, Miszalski Z. The role of hydrogen peroxide in regulation of plant metabolism and cellular signalling in response to environmental stresses. Acta Biochim Pol 2007;54:39–50.
   PubMed Web of Science ®Google Scholar
• Alscher RG, Erturk N, Heath LS. Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 2002;53:1331–41.
   PubMed Web of Science ®Google Scholar
• Asada K, Takahashi M. Production and scavenging of active oxygen in chloroplasts. In: , Kyle DJ, Osmond CB, Arntzen CJ (eds) Photoinhibition. Amsterdam: Elsevier; 1987. pp.227–87.
   Google Scholar
• Wise RR, Naylor AW. Chilling-enhanced photooxidation: evidence for the role of singlet oxygen and superoxide in the breakdown of pigments and endogenous antioxidants. Plant Physiol 1987;83:278–82.
   PubMed Web of Science ®Google Scholar
• Osmond CB. What is photoinhibition? Some insights from comparisons of shade and sun plants. , Baker NR, Bowyer JR (eds) Photoinhibition of photosynthesis: from molecular mechanisms to the field. Oxford: Bios. Sci. Pub.; 1994. pp. 1–24.
   Google Scholar
• Dall'Osto L, Fiore A, Cazzaniga S, Giuliano G, Bassi R. Different roles of alpha- and beta-branch xanthophylls in photosystem assembly and photoprotection. J Biol Chem 2007;282:35056–68.
   PubMed Web of Science ®Google Scholar
• Liu Z, Yan H, Wang K, Kuang T, Zhang J, Gui L, et al. Crystal structure of spinach major light-harvesting complex at 2.72 A resolution. Nature 2004;428:287–92.
   PubMed Web of Science ®Google Scholar
• Latowski D, Grzyb J, Strzalka K. The xanthophyll cycle – molecular mechanism and physiological significance. Acta Physiol Plant 2004;26:197–212. doi: 10.1007/s11738-004-0009-8.
   Web of Science ®Google Scholar
• Gruszecki WI, Grudzinski W, Gospodarek M, Patyra M, Maksymiec W. Xanthophyll-induced aggregation of LHCII as a switch between light-harvesting and energy dissipation systems. Biochim Biophys Acta 2006;1757:1504–11.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Muller P, Li XP, Niyogi KK. Non-photochemical quenching. A response to excess light energy. Plant Physiol 2001;125:1558–66. doi: 10.1104/pp. 125.4.1558.
   PubMed Web of Science ®Google Scholar
• Niyogi KK. Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 1999;50:333–59.
   PubMed Web of Science ®Google Scholar
• Horton P, Ruban AV, Walters RG. Regulation of light harvesting in green plants. Annu Rev Plant Physiol Plant Mol Biol 1996;47:655–84.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Ma YZ, Holt NE, Li XP, Niyogi KK, Fleming GR. Proc Natl Acad Sci USA 2003;100(8):4377–82. Epub 2003 Apr 03.
   PubMed Web of Science ®Google Scholar
• Adams WW, Demmig-Adams B, Verhoeven AS, Baker DH, Aust J. Photoinhibition during winter stress: involvement of sustained xanthophyll cycle-dependent energy dissipation. Plant Physiol 1995;22:261–76.
   Web of Science ®Google Scholar
• Ruban AV, Horton P. The xanthophyll cycle modulates the kinetics of non-photochemical energy dissipation in isolated light-harvesting complexes, intact chloroplasts, and leaves of spinach. Plant Physiol 1999;119:531–42.
   PubMed Web of Science ®Google Scholar
• Lavaud J, Rosseau B, Etienne AL. In diatoms, a transthylakoid proton gradient alone is not sufficient to induce a non-photochemical fluorescence quenching. FEBS Lett 2002;523:163–6.
   PubMed Web of Science ®Google Scholar
• 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;129:1398–1406.
   PubMed Web of Science ®Google Scholar
• Young AJ, Frank HA. Energy transfer reactions involving carotenoids: quenching of chlorophyll fluorescence. J Photochem Photobiol B: Biol 1996;36:3–15.
   PubMed Web of Science ®Google Scholar
• Hudson B, Kohler BE. Electronic structure and spectra of finite linear polyenes. Synth Metals 1984;9:241–53.
   Web of Science ®Google Scholar
• Shrevea AP, Trautmana JK, Owensb TG, Albrechta AC. Two-photon excitation spectroscopy of thylakoid membranes from Phaeodactylum tricornutum: Evidence for an in vivo two-photon-allowed carotenoid state. Chem Phys Lett 1990;170(1):51–6.
   Web of Science ®Google Scholar
• 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. Biochemistry 2000;39:2831–7.
   PubMed Web of Science ®Google Scholar
• Demmig-Adamsa B. Carotenoids and photoprotection in plants: a role for the xanthophyll zeaxanthin. Biochimic Biophys Acta (BBA) – Bioenerg 1990;1020(1):1–24.
   Web of Science ®Google Scholar
• Frank HA, Cua A, Chynwat V, Young A, Gosztola D, Wasielewski MR. Photophysics of the carotenoids associated with the xanthophyll cycle in photosynthesis. Photosynth Res 1994;41:389–95.
   PubMed Web of Science ®Google Scholar
• Gruszecki WI, Matuła M, Myśliwa-Kurdziel B, Kernem P, Krupa Z, Strzałka K. Effect of xanthophyll pigments on fluorescencje of chlorophyll a in LHC II embedded to liposomes. J Photochem Photobiol, B: Biol 1997;37:84–90.
   Web of Science ®Google Scholar
• Avital S, Brumfeld V, Malkin S. A micellar model system for the role of zeaxanthin in the non-photochemical quenching process of photosynthesis – chlorophyll fluorescence quenching by the xanthophylls. Biochim Biophys Acta 2006;1757:798–810.
   PubMed Web of Science ®Google Scholar
• Polivka T, Sundstrom V. Ultrafast dynamics of carotenoid excited states – from solution to natural and artificial systems. Chem Rev 2004;104:2021–71.
   PubMed Web of Science ®Google Scholar
• Lokstein H, Tian L, Polle JEW, DellaPenna D. Xanthophyll biosynthetic mutants of Arabidopsis thaliana: altered nonphotochemical quenching of chlorophyll fluorescence is due to changes in Photosystem II antenna size and stability. Biochim Biophys Acta 2002;1553:309–19.
   PubMed Web of Science ®Google Scholar
• Polivka T, Herek JL, Zigmantas D, Akerlund H, Sundstrom V. Direct observation of the (forbidden) S1 state in carotenoids. Proc Natl Acad Sci USA 1999;96:4914.
   PubMed Web of Science ®Google Scholar
• Berera R, van Stokkum IH, Kodis G, Keirstead AE, Pillai S, Herrero C, et al. Energy transfer, excited-state deactivation, and exciplex formation in artificial caroteno-phthalocyanine light-harvesting antennas. J Phys Chem B 2007;111:6868–77.
   PubMed Web of Science ®Google Scholar
• Ruban AV, Berera R, Ilioaia C, van Stokkum IH, Kennis JT, Pascal AA, et al. Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 2007;450:575–8.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Croce R, Cinque G, Holzwarth AR, Bassi R. The soret absorption properties of carotenoids and chlorophylls in antenna complexes of higher plants. Photosynth Res 2000;64:221–31.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Wehner A, Storf S, Jahns P, Schmid VH. De-epoxidation of violaxanthin in light-harvesting complex I proteins. J Biol Chem 2004;279:26823–9.
   PubMed Web of Science ®Google Scholar
• Miloslavina Y, Wehner A, Lambrev PH, Wientjes E, Reus M, Garab G, et al. Far-red fluorescence: a direct spectroscopic marker for LHCII oligomer formation in nonphotochemical quenching. FEBS Lett 2008;582:3625–31.
   PubMed Web of Science ®Google Scholar
• Ilioaia C, Johnson MP, Horton P, Ruban AV. Induction of efficient energy dissipation in the isolated light-harvesting complex of photosystem II in the absence of protein aggregation. J Biol Chem 2008;283:29505–12.
   PubMed Web of Science ®Google Scholar
• Bode S, Quentmeier CC, Liao PN, Hafi N, Barros T, Wilk L, et al. On the regulation of photosynthesis by excitonic interactions between carotenoids and chlorophylls. Proc Nat Acad Sci USA 2009;106:12311–6.
   PubMed Web of Science ®Google Scholar
• Andersson J, Wentworth M, Walters RG, Howard CA, Ruban AV, Horton P, et al. Absence of the Lhcb1 and Lhcb2 proteins of the light-harvesting complex of photosystem II – effects on photosynthesis, grana stacking and fitness. Plant J 2003;35:350–61.
   PubMed Web of Science ®Google Scholar
• Damkjaer JT, Kereiche S, Johnson MP, Kovacs L, Kiss AZ, Boekema EJ, et al. The photosystem II light-harvesting protein Lhcb3 affects the macrostructure of photosystem II and the rate of state transitions in Arabidopsis. Plant Cell 2009;21(10):3245–56.
   PubMed Web of Science ®Google Scholar
• Mozzo M, Passarini F, Bassi R, van Amerongen H, Croce R. Photoprotection in higher plants: the putative quenching site is conserved in all outer light-harvesting complexes of photosystem II. Biochim Biophys Acta 2008;1777:1263–7.
   PubMed Web of Science ®Google Scholar
• Garab G, Cseh Z, Kovacs L, Rajagopal S, Varkonyi Z, Wentworth M, et al. Light-induced trimer to monomer transition in the main light- harvesting antenna complex of plants: thermo-optic mechanism. Biochemistry 2002;41:15121–9.
   PubMed Web of Science ®Google Scholar
• Grudziński W, Matula M, Sielewiesiuk J, Kernem P, Krupa Z, Gruszecki WI. Effect of 13-cis violaxanthin on organization of light harvesting complex II in monomolecular layers. Biochim Biophys Acta 2001;1503:291–302.
   PubMed Web of Science ®Google Scholar
• Yamamoto HY, Higashi RM. Violaxanthin de-epoxidase. Lipid composition and substrate specificity. Arch Biochem Biophys 1978;190:514–22.
   PubMed Web of Science ®Google Scholar
• Niedzwiedzki D, Krupa Z, Gruszecki WI. Temperature-induced isomerization of violaxanthin in organic solvents and in light-harvesting complex II. J Photochem Photobiol B, Biol 2005;78:109–14.
   PubMed Web of Science ®Google Scholar
• Schiffer R, Neis M, Holler D, Rodriguez F, Geier A, Gartung C, et al. Active influx transport is mediated by members of the organic anion transporting polypeptide family in human epidermal keratinocytes. J Invest Dermatol 2003;120:285–91.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Avenson TJ, Ahn TK, Zigmantas D, Niyogi KK, Li Z, Ballottari M, et al. Zeaxanthin radical cation formation in minor light-harvesting complexes of higher plant antenna. J Biol Chem 2008;283:3550–8.
   PubMed Web of Science ®Google Scholar
• Ahn TK, Avenson TJ, Ballottari M, Cheng YC, Niyogi KK, Bassi R, et al. Architecture of a charge transfer state regulating light harvesting in a plant antenna protein. Science 2008;320:794–7.
   PubMed Web of Science ®Google Scholar
• Avenson TJ, Ahn TK, Niyogi KK, Ballottari M, Bassi R, Fleming GR. Lutein can act as a switchable charge transfer quencher in the CP26 light-harvesting complex. J Biol Chem 2009;284:2830–5.
   PubMed Web of Science ®Google Scholar
• Li Z, Ahn TK, Avenson TJ, Ballottari M, Cruz JA, Kramer DM, et al. Lutein accumulation in the absence of zeaxanthin restores nonphotochemical quenching in the Arabidopsis thaliana npq1 mutant. Plant Cell 2009;21:1798–812.
   PubMed Web of Science ®Google Scholar
• Bonente G, Howes BD, Caffarri S, Smulevich G, Bassi R. Interactions between the photosystem II subunit PsbS and xanthophylls studied in vivo and in vitro. J Biol Chem 2008;283:8434–45.
   PubMed Web of Science ®Google Scholar
• Gruszecki WI, Strzalka K. Does the xanthophyll cycle take part in the regulation of fluidity of the thylakoid membrane? Biochim Biophys Acta 1991;1060:310–14.
   Web of Science ®Google Scholar
• Latowski D, Akerlund HE, Strzalka K. Violaxanthin de-epoxidase, the xanthophyll cycle enzyme, requires lipid inverted hexagonal structures for its activity. Biochemistry 2004;43:4417–20.
   PubMed Web of Science ®Google Scholar
• Havaux M, Gruszecki WI, Dupont I, Leblanc RM. Increased heat emission and its relationship to the xanthophyll cycle in pea leaves exposed to strong light stress. J. Photochem Photobiol B Biol 1991;8:361–70.
   Web of Science ®Google Scholar
• Havaux M, Niyogi KK. The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. Proc Nat Acad Sci USA 1999;96:8762–7.
   PubMed Web of Science ®Google Scholar
• Sarry JE, Montillet JL, Sauvaire Y, Havaux M. The protective function of the xanthophyll cycle in photosynthesis. FEBS Lett 1994;353:147–50.
   PubMed Web of Science ®Google Scholar
• Woodall AA, Britton G, Jackson MJ. Carotenoids and protection of phospholipids in solution or in liposomes against oxidation by peroxyl radicals: Relationship between carotenoid structure and protective ability. Biochim Biophys Acta 1997;1336:575–86.
   PubMed Web of Science ®Google Scholar
• Woodall AA, Lee SW-M, Weesie RJ, Jackson MJ, Britton G. Oxidation of carotenoids by free radicals: relationship between structure and reactivity Biochim. Biophys Acta 1997;1336:33–42.
   PubMed Web of Science ®Google Scholar
• Schaller S, Latowski D, Jemioła-Rzemińska M, Wilhelm C, Strzałka K, Goss R. The main thylakoid membrane lipid monogalactosyldiacylglycerol (MGDG) promotes the de-epoxidation of violaxanthin associated with the light-harvesting complex of photosystem II (LHCII). Biochim Biophys Acta-Bioenerg 2010;1797(3):414–24.
   PubMed Web of Science ®Google Scholar
• Munne-Bosch S, Alegre L. Plant aging increases oxidative stress in chloroplasts. Planta 2002;214:608–15.
   PubMed Web of Science ®Google Scholar
• Misra AN, Latowski D, Strzałka K. Photosynthetic excitation pressure causes violaxanthin de-epoxidation in aging cabbage (Brassica oleracea L.) leaves. J Life Sci 2011;5:182–91.
   Google Scholar
• Krinsky NI. Carotenoid protection against oxidation. Pure Appl Chem 1979;51:649–60.
   Web of Science ®Google Scholar
• Lim BP, Nagao A, Terao J, Tanaka T, Takama K. Antioxidant activity of xanthophylls on peroxyl radical-mediated phospholipid membrane. Biochem Biophys Acta 1992;1126:178–84.
   PubMed Web of Science ®Google Scholar
• Peguero-Pina JJ, Morales F, Flexas J, Gil-Pelegrín E, Moya I. Photochemistry, remotely sensed physiological reflectance index and de-epoxidation state of the xanthophyll cycle in Quercus coccifera under intense drought. Conference Information: 3rd International Workshop on Remote Sensing of Vegetation Fluorescence; 2007; Florence, Italy. Oecologia 2008; 156(1):1–11.
   Google Scholar
• Lu CM, Qiu NW, Lu QT. Photoinhibition and the xanthophyll cycle are not enhanced in the salt-acclimated halophyte Artimisia anethifolia. Physiol Planta 2003;118(4):532–7.
   Web of Science ®Google Scholar
• Sui N, Li M, Liu XY, Wang N, Fang W, Meng QW. Response of xanthophyll cycle and chloroplastic antioxidant enzymes to chilling stress in tomato over-expressing glycerol-3-phosphate acyltransferase gene. Photosynthetica 2007;45(3):447–54.
   Web of Science ®Google Scholar
• Pasqualini S, Batini P, Ederli L, Antonielli M. Responses of the xanthophyll cycle pool and ascorbate-glutathione cycle to ozone stress in two tobacco cultivars. Free Rad Res 1999;31 (Suppl):67–73.
   PubMedGoogle Scholar
• Ederli L, Pasqualini S, Batini P, Antonielli M. Photoinhibition and oxidative stress: effects on xanthophyll cycle, scavenger enzymes and ABA content in tobacco plants. J Plant Physiol 1997;151(4):422–8.
   Web of Science ®Google Scholar
• Audran C, Borel C, Frey A, Sotta B, Meyer C, Simonneau T, et al. Expression studies of the zeaxanthin epoxidase gene in Nicotiana plumbaginifolia. Plant Physiol 1998;118:1021–8.
   PubMed Web of Science ®Google Scholar
• Ivanov AG, Krol M, Maxwell D, Huner NP. Abscisic acid induced protection against photoinhibition of PSII correlates with enhanced activity of the xanthophyll cycle. FEBS Lett 1995;371:61–4.
   PubMed Web of Science ®Google Scholar