The antioxidative function of lutein: electron spin resonance studies and chemical detection
Chang-Lian Peng A B D , Zhi-Fang Lin B , Yue-Zeng Su C , Gui-Zhu Lin B , Hong-Yan Dou C and Cheng-Xue Zhao CA College of Life Science, South China Normal University, Guangzhou 510631, China.
B South China Institute of Botany, Chinese Academy of Sciences, Guangdong Key Laboratory of Digital Botanical Garden, Guangzhou 510650, China.
C Department of Chemistry, Shanghai Jiaotong University, Shanghai 200240, China.
D Corresponding author. Email: pengchl@scib.ac.cn
Functional Plant Biology 33(9) 839-846 https://doi.org/10.1071/FP06013
Submitted: 17 January 2006 Accepted: 15 May 2006 Published: 1 September 2006
Abstract
In the present study, both electron spin resonance (ESR) and chemical detection confirmed that lutein [extracted from alfalfa (Medicago sativa L.)], the most abundant xanthophyll in thylakoids of chloroplasts, could serve as an antioxidant to scavenge reactive oxygen species (ROS) in vitro. Lutein exhibited a greater capacity for scavenging hydroxyl (OH·) and superoxide (O2·–) radicals than β-carotene at the same concentration, whereas the opposite trend was observed in the capacity for scavenging singlet oxygen (1O2). The capacity of lutein for scavenging ROS from high to low is OH· > O2·– > 1O2. We hypothesise that lutein plays an important photoprotective role in scavenging O2·– and OH· under severe stress. This hypothesis is consistent with our previous report that the lut2 (lutein-deficient) Arabidopsis mutant is more susceptible to damage than the npq1 (lutein-replete but violaxanthin de-epoxidase-deficient) Arabidopsis mutant under severe stress during exposure to high light intensity at low temperature (Peng and Gilmore 2003).
Keywords: antioxidant, chemical detection, electron spin resonance, lutein, reactive oxygen species, scavenging capacity.
Acknowledgments
This work was supported by the National Natural Science Foundation of China (30270125, 30470282), Guangdong Natural Science Foundation (04002309), and Project of CAS Knowledge Innovation Program (KSCX2-SW-130).
Alscher RG,
Donahue JL, Cramer CL
(1997) Reactive oxygen species and antioxidants: relationships in green cells. Physiologia Plantarum 100, 224–233.
| Crossref | GoogleScholarGoogle Scholar |
Asada K
(2000) The water–water cycle as alternative photon and electron sinks. Philosophical Transactions of the Royal Society London — Series B. Biological Sciences 355, 1419–1430.
| Crossref | GoogleScholarGoogle Scholar |
Baroli I,
Do DA,
Yamane T, Niyogi KK
(2003) Zeaxanthin accumulation in the absence of a functional xanthophylls cycle protects Chlamydomonas reinhardtii from photooxidative stress. The Plant Cell 15, 992–1008.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Chakraborty N, Tripathy BC
(1992) Involvement of singlet oxygen in 5-amino-levalinic acid-induced photodynamic damage of cucumber (Cucumis sativus L.) chloroplasts. Plant Physiology 98, 7–11.
| PubMed |
Cogdell RJ, Frank HA
(1987) How carotenoids function in photosynthetic bacteria. Biochimica et Biophysica Acta 895, 63–79.
| PubMed |
Demmig-Adams B,
Adams WW,
Logan BA, Verhoeven AS
(1995) Xanthophyll cycle-dependent energy dissipation and flexible photosystem. II. Efficiency in plants acclimated to light stress. Australian Journal of Plant Physiology 22, 249–260.
Di Mascio P,
Devasagayam TPA,
Kaiser S, Sies H
(1990) Carotenoids, tocopherols and thids as biological singlet molecular oxygen quenchers. Biochemical Society Transactions 18, 1054–1056.
| PubMed |
Foyer CH,
Lelandais M, Kunert KJ
(1994) Photooxidative stress in plants. Physiologia Plantarum 92, 696–717.
| Crossref | GoogleScholarGoogle Scholar |
Frank HA, Cogdell RJ
(1996) Carotenoids in photosynthesis. Photochemistry and Photobiology 63, 257–264.
| PubMed |
García-Plazaola JI,
Hernandez A,
Olano JM, Becerril JM
(2003) The operation of the lutein epoxide cycle correlates with energy dissipation. Functional Plant Biology 30, 319–324.
| Crossref | GoogleScholarGoogle Scholar |
García-Plazaola JI,
Hormaetxe K,
Hernandez A,
Olano JM, Becerril JM
(2004) The lutein epoxide cycle in vegetative buds of woody plants. Functional Plant Biology 31, 815–823.
| Crossref | GoogleScholarGoogle Scholar |
Gilmore AM, Yamamoto HY
(1993) Linear models relating xanthophylls and lumen acidity to non-photochemical fluorescence quenching. Evidence that antheraxanthin explains zeaxanthin-independent quenching. Photosynthesis Research 35, 67–78.
| Crossref | GoogleScholarGoogle Scholar |
Gilmore AM,
Shinkarev VP,
Hazlett TL, Govindjee
(1998) Quantitative analysis of the effects intrathylakoid pH and xanthophylls cycle pigments on chlorophyll a fluorescence lifetime distributions and intensity in thylakoids. Biochemistry 37, 13582–13593.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Havaux M, Niyogi KK
(1999) The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. Proceedings of the National Academy of Sciences USA 96, 8762–8767.
| Crossref | GoogleScholarGoogle Scholar |
Havaux M,
Bonfils JP,
Lutz C, Niyogi KK
(2000) Photodamage of the photosynthetic apparatus and its dependence on leaf developmental stage in npq1 Arabidopsis mutant deficient in the xanthophylls cycle enzyme violaxanthin de-epoxidase. Plant Physiology 124, 273–284.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Iannone A,
Rota C,
Bergansini S,
Tomasi A, Canfield LM
(1998) Antioxidant activity of carotenoids: an electron spin resonance study on β-carotene and lutein interaction with free radicals generation in a chemical system. Journal of Biochemical and Molecular Toxicology 12, 299–304.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Krishna CM,
Liefmann JE,
Kaufman D,
Degraff W,
Hahn SM,
McMurry T,
Mitchell JB, Russo A
(1992) The catecholic metal sequestering agent 1,2-dihydroxybenzene-3,5-disulfonate confers protection against oxidative cell damage. Archives of Biochemistry and Biophysics 294, 98–106.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kühlbrandt W,
Wang DN, Fujiyoshi Y
(1994) Atomic model of plant light-harvesting complex by electronic biology crystallography. Nature 367, 614–627.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lee ALC, Thornber JP
(1995) Analysis of the pigment stoichiometry of pigment–protein complexes from barley (Hordeum vulgare). The xanthophylls cycle intermediates occur mainly in the light-harvesting complexes of photosystem I and photosystem II. Plant Physiology 107, 565–574.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lin ZF,
Lin GZ,
Li SS, Zhao CX
(1988) Changes of concentration of superoxide anion and organic radical in senescent leaves and chloroplasts. Acta Phytophysiolgia Sinica 14, 238–243.
Lin ZF,
Peng CL,
Lin GZ,
Ou ZY,
Yang CW, Zhang JL
(2003) Photosynthetic characteristics of two new chlorophyll b-less rice mutants. Photosynthetica 41, 61–67.
| Crossref | GoogleScholarGoogle Scholar |
Lion Y,
Delmelle M, Vorst A
(1976) New method of detecting singlet oxygen production. Nature 263, 442–443.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Liu ZF,
Yan HC,
Wang KB,
Kuang TY,
Zhang JP,
Gui LL,
An XM, Chang WR
(2004) Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution. Nature 428, 287–292.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lokstein H,
Tian L,
Polle JEW, DellaPenna D
(2002) Xanthophyll biosynthetic mutants of Arabidopsis thaliana: altered nonphotochemical quenching of chlorophyll fluorescence is due to changes in photosystem II antenna size and stability. Biochimica et Biophysica Acta 1553, 309–319.
| PubMed |
Markgraf T, Oelmüller R
(1991) Evidences that carotenoids are required for the accumulation of a functional photosystem II, but not photosystem I in the cotyledon of mustard seedlings. Planta 185, 97–104.
| Crossref |
Marklund S, Marklund G
(1974) Involvement of the superoxide anion radical in the autoxidation of pyrogallal and a convenient assay for superoxide dismutase. European Journal of Biochemistry 47, 469–474.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Matsubara S,
Naumann M,
Martin R,
Nichol C,
Rascher U,
Morosinotto T,
Bassi R, Osmond B
(2005) Slowly reversible de-epoxidation of lutein-epoxide in deep shade leaves of a tropical tree legume may ‘lock-in’ lutein-based photoprotection during acclimation to strong light. Journal of Experimental Botany 56, 461–468.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Mortensen A, Skibsted LH
(1997) Important of carotenoid structure in radical scavenging. Journal of Agricultural and Food Chemistry 45, 2970–2977.
| Crossref | GoogleScholarGoogle Scholar |
Niyogi KK,
Grossman AR, Björkman O
(1998) Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. The Plant Cell 10, 1121–1134.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Niyogi KK,
Björkman O, Grossman AR
(1997) The roles of specific xanthophylls in photoprotection. Proceedings of the National Academy of Sciences USA 94, 14 162–14 167.
| Crossref | GoogleScholarGoogle Scholar |
Peng CL, Gilmore AM
(2003) Contrasting changes of photosystem 2 efficiency in Arabidopsis xanthophylls mutants at room or low temperature under high irradiance stress. Photosynthetica 41, 233–239.
| Crossref | GoogleScholarGoogle Scholar |
Pogson BJ,
Niyogi KK,
Björkman O, Dellapenna D
(1998) Altered xanthophyll compositions adversely affect chlorophyll accumulation and nonphotochemical quenching in Arabidopsis mutants. Proceedings of the National Academy of Sciences USA 95, 13 324–13 329.
| Crossref | GoogleScholarGoogle Scholar |
Roubaud V,
Sankarapandis S,
Kuppusdmy P,
Tardo P, Zweier JL
(1997) Quantitative measurement of superoxide generation using the spin trap 5-(diethoxyphasphoryl)-5-methyl-1-pyrnoline-N-oxide. Analytical Biochemistry 247, 404–411.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Schweikert C,
Liszkay A, Schopfer P
(2000) Scission of polysaccharides by peroxidase-generated hydroxyl radicals. Phytochemistry 53, 565–570.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Shen QY, Shen QY
(2001) Study on the resisting oxygen free radical and hydroxyl free radical effect of Cordyceps militaris. Guihaia 21, 252–254.
Siefermann-Harms D
(1987) The light-harvesting and protective functions of carotenoids in photosynthetic membranes. Physiologia Plantarum 69, 561–568.
Sonoike K
(1999) The different roles of chilling temperatures in the photoinhibition of photosystem I and photosystem II. Journal of Photochemistry and Photobiology B: Biology 48, 136–141.
| Crossref | GoogleScholarGoogle Scholar |
Standfuss R,
van Scheltinga ACT,
Lamborghini M, Kühlbrandt W
(2005) Mechanisms of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2.5 Å resolution. EMBO Journal 24, 919–928.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Terashima I,
Funnayama S, Sonoike K
(1994) The site of photoinhibition in leaves of Cucumis sativus L. at low temperatures is photosystem I, not photosystem II. Planta 193, 300–306.
| Crossref | GoogleScholarGoogle Scholar |
Thayer SS, Björkman O
(1990) Leaf xanthophylls content and composition in sun and shade determined by HPLC. Photosynthesis Research 23, 331–343.
| Crossref | GoogleScholarGoogle Scholar |
Van Breusegem F,
Vranová E,
Dat JF, Inzé D
(2001) The role of reactive oxygen species in plant signal transduction. Plant Science 161, 405–414.
| Crossref | GoogleScholarGoogle Scholar |
Woodall AA,
Lee SWM,
Weesie RJ,
Jackson MJ, Britton G
(1997) Oxidation of carotenoids by free radicals: relationship between structure and reactivity. Biochimica et Biophysica Acta 136, 33–42.
Zhao HY, Zou Q
(2002) Protective effects of exogenous antioxidants and phenolic compounds on photosynthesis of wheat leaves under high irradiance and oxidative stress. Photosynthetica 40, 523–527.
| Crossref | GoogleScholarGoogle Scholar |
