Nonenzymic carotenoid oxidation and photooxidative stress signalling in plants

Journal of Experimental Botany

Volumn 64, Issue 3, 2013, Pages 799-805

  Ramel, Fanny ^a,b,c   Mialoundama, Alexis S ^d   Havaux, Michel ^a,b,c  

^a IRFM   (France)

^b CNRS   (France)

^c AIX MARSEILLE UNIVERSITY   (France)

^d UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

Carotenoid; Carotenoid cleavage dioxygenase; Photooxidative stress; Reactive oxygen species; Signalling; Singlet oxygen

Indexed keywords

CAROTENOID;

GENETICS; METABOLISM; OXIDATIVE STRESS; PHOTOSYNTHESIS; PLANT; RADIATION EXPOSURE; REVIEW; SIGNAL TRANSDUCTION;

CAROTENOIDS; OXIDATIVE STRESS; PHOTOSYNTHESIS; PLANTS; SIGNAL TRANSDUCTION;

EID: 84875765519     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ers223     Document Type: Review

References (69)

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.
2. Alméras E, Stolz S, Vollenweider S, Reymond P, Mène-Saffrané L, Farmer EE. 2003. Reactive electrophile species activate defense gene expression in Arabidopsis. The Plant Journal 34, 205-216.
3. Amengual J, Lobo GP, Golczak M, Li HN, Klimova T, Hoppel CL, Wyss A, Palczewski K, von Lintig J. 2011. A mitochondrial enzyme degrades carotenoids and protects against oxidative stress. FASEB Journal 25, 948-959.
4. Auldridge ME, McCarty DR, Klee HJ. 2006. Plant carotenoid cleavage oxygenases and their apocarotenoid products. Current Opinion in Plant Biology 9, 315-321.
5. Bando N, Hayashi H, Wakamatsu S, Inakuma T, Miyoshi M, Nagao A, Yamauchi R, Terao J. 2004. Participation of singlet oxygen in ultraviolet-A-induced lipid peroxidation in mouse skin and its inhibition by dietary ß-carotene: An ex vivo study. Free Radical in Biology and Medecine 37, 1854-1863.
6. Bernstein PS, Khachik F, Carvalho LS, Muir GJ, Zho DY, Katz NB. 2001. Identification and quantitation of carotenoids and their metabolites in the tissues of the human eye. Experimental Eye Research 72, 215-223.
7. Bhosale P, Bernstein PS. 2005. Quantitative measurement of 3'-oxolutein from human retina by normal-phase high-performance liquid chromatography coupled to atmospheric pressure chemical ionization mass spectrometry. Analytical Chemistry 345, 296-301.
8. Bouvier F, Isner JC, Dogbo O, Camara B. 2005. Oxidative tailoring of carotenoids: A prospect towards novel functions in plants. Trends in Plant Science 10, 187-194.
9. Davoine C, Douki T, Iacazio G, Montillet JL, Triantaphylidès C. 2005. Conjugation of keto fatty acids to glutathione in plant tissues. Characterization and quantification by HPLC-tandem mass spectrometry. Analytical Chemistry 77, 7366-7372.
10. Dueckershoff K, Mueller S, Mueller MJ, Reinders J. 2008. Impact of cyclopentenone-oxylipins on the proteome of Arabidopsis thaliana. Biochimica et Biophysica Acta 1784, 1975-1985.
11. Edge R, Mcgarvey DJ, Truscott TG. 1997. The carotenoids as anti-oxidants-a review. Journal of Photochemistry and Photobiology B 41, 189-200.
12. Eroglu A, Hruszkewycz DP, Dela Sena C, Narayanasamy S, Riedl KM, Kopec RE, Scwartz SJ, Curley RW Jr, Harrison EH. 2012. Naturally-occurring eccentric cleavage products of provitamin A ß-carotene function as antagonists of retinoic acid receptors. Journal of Biological Chemistry 287, 15886-15895.
13. Farmer EE, Davoine C. 2007. Reactive electrophile species. Current Opinion in Plant Biology 10, 380-386.
14. Fiedor J, Fiedor L, Winkler J, Scherz A, Scheer H. 2001. Photodynamics of the bacteriochlorophyll-carotenoid system. 1. Bacteriochlorophyll- photosensitized oxygenation of ß-carotene in acetone. Photochemistry and Photobiology 74, 64-71.
15. Fiedor J, Fiedor L, Haessner R, Scheer H. 2005. Cyclic endoperoxides of ß-carotene, potential pro-oxidants, as products of chemical quenching of singlet oxygen. Biochimica et Biophysica Acta 1709, 1-4.
16. Fischer BB, Ledford HK, Wakao S, Huang SG, Casero D, Pellegrini M, Merchant SS, Koller A, Eggen RI, Niyogi KK. 2012. SINGLET OXYGEN RESISTANT 1 links reactive electrophile signalling to singlet oxygen acclimation in Chlamydomonas reinhardtii. Proceedings of the National Academy of Sciences, USA 109, E1302-E1311.
17. Floss DS, Walter MH. 2009. Role of carotenoid cleavage dioxygenase 1 (CCD1) in apocarotenoid biogenesis revisited. Plant Signaling and Behavior 4, 172-175.
18. Gomez-Roldan V, Fermas S, Brewer PB, et al. 2008. Strigolactone inhibition of shoot branching. Nature 455, 189-194.
19. González-Pérez S, Gutiérrez J, García- García F, Osuna D, Dopazo J, Lorenzo Ó, Revuelta JL, Arellano JB. 2011. Early transcriptional defense responses in Arabidopsis cell suspension culture under high-light conditions. Plant Physiology 156, 1439-1456.
20. Gouranton E, Aydemir G, Reynaud E, Marcotorchino J, Malezet C, Caris-Veyrat C, Blomhoff R, Landrier JF, Rühl R. 2011. Apo-10'-lycopenoic acid impacts adipose tissue biology via the retinoic acid receptors. Biochimica et Biophysica Acta 1811, 1105-1114.
21. Havaux M. 1998. Carotenoids as membrane stabilizers in chloroplasts. Trends in Plant Science 3, 147-151.
22. Heddad M, Adamska I. 2002. The evolution of light stress proteins in photosynthetic organisms. Comparative Functional Genomics 3, 504-510.
23. Heintzen C. 2012. Plant and fungal photopigments. WIREs Membrane Transport and Signaling 1, 411-432.
24. Horton P, Ruban AV. 2005. Molecular design of photosystem II light-harvesting antenna: Photosynthesis and photoprotection. Journal of Experimental Botany 56, 365-373.
25. Hurst JS, Saini MK, Jin G-F, Awasthi YC, van Kuijk FJGM. 2005. Toxicity of oxidized ß-carotene to cultured human cells. Experimental Eye Research 81, 239-243.
26. Jahns P, Holzwarth AR. 2012. The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochimica et Biophysica Acta 1817, 182-193.
27. Janakiram NB, Cooma I, Mahammed A, Steele VE, Rao CV. 2008. ß-Ionone inhibits colonic aberrant crypt foci formation in rats, suppresses cell growth, and induces retinoid X receptor-a in human colon cancer cells. Molecular Cancer Therapeutics 7, 181-190.
28. Jeong TC, Gu HK, Chun YJ, Yun CH, Han SS, Roh JK. 1998. Effects of beta-ionone on the expression of cytochrome P450s and NADPH-cytochrome P450 reductase in Sprague Dawley rats. Chemico-biological Interactions 114, 97-107.
29. Johnson M, Havaux M, Triantaphylidès C, Ksas B, Pascal AA, Robert B, Davison PA, Ruban AV, Horton P. 2007. Elevated zeaxanthin bound to oligomeric LHCII enhances the resistance of Arabidopsis to photooxidative stress by a lipid-protective, antioxidant mechanism. Journal of Biological Chemistry 282, 22605-22618.
30. Jüttner F, Watson SB, von Elert E, Köster O. 2010. ß-Cyclocitral, a grazer defence signal unique to the cyanobacterium Microcystis. Chemical Ecology 36, 1387-1397.
31. Kato-Noguchi H. 1994. Occurrence of a growth inhibitor, 3-hydroxy-ß-ionone, in seven cultivars of Phaseolus vulgaris and its role in light-induced growth inhibition. Phytochemistry 36, 273-276.
32. Kato-Noguchi H, Seki T. 2010. Allelopathy of the moss Rhunchostegium pallidifolium and 3-hydroxy-ß-ionone. Plant Signaling and Behavior 5, 702-704.
33. Kalariya NM, Ramana KV, Srivastava SK, van Kuijk FJGM. 2008. Carotenoid derived aldehydes-induced oxidative stress causes apoptotic cell death in human retinal epithelial cells. Experimental Eye Research 86, 70-80.
34. Kalariya NM, Ramana KV, Srivastava SK, van Kuijk FJGM. 2009. Genotoxic effects of carotenoid breakdown products in human retinal pigment epithelial cells. Current Eye Research 34, 737-747.
35. Klein M, Burla B, Martinoia E. 2006. The multidrug resistance-associated protein (MRP/ABCC) subfamily of ATP-binding cassette transporters in plants. FEBS Letters 580, 1112-1122.
36. Kuntz E, Hoeller U, Greatrix B, et al. 2006. ß-Carotene and apocarotenals promote retinoid signaling in BEAS-2B human bronchioepithelial cells. Archives of Biochemistry and Biophysics 455, 48-60.
37. Lakshminarayana R, Sathish UV, Dhrmash SM, Baskaran V. 2010. Antioxidant and cytotoxic effect of oxidized lutein in human cervical carcinoma cells (HeLa). Food Chemistry and Toxicology 48, 1811-1816.
38. Ledford HK, Chin BL, Niyogi KK. 2007. Acclimation to singlet oxygen stress in Chlamydomonas reinhardtii. Eukaryotic Cell 6, 919-930.
39. Levonen AL, Landar A, Ramachandran A, Ceaser EK, Dickinson DA, Zanoni G, Morrow JD, Darley-Usmar VM. 2004. Cellular mechanisms of redox cell signalling: Role of cysteine modification in controlling antioxidant defences in response to electrophilic lipid oxidation products. The Biochemical Journal 378, 373-382.
40. Li Z, Wakao S, Fischer BB, Niyogi KK. 2009. Sensing and responding to excess light. Annual Review of Plant Biology 60, 239-260.
41. Lim BP, Nagao A, Terao J, Tanaka K, Suzuki T, Takama K. 1992. Antioxidant activity of xanthophylls on peroxyl radical-mediated phospholipid peroxidation. Biochimica et Biophysica Acta 1126, 178-184.
42. Linnewiel K, Ernst H, Caris-Veyrat C, Ben-Dor A, Kampf A, Salman H, Danilenko M, Levy J, Sharoni Y. 2009. Structure activity relationship of carotenoid derivatives in activation of the electrophile/antioxidant response element transcription system. Free Radical Biology and Medicine 47, 659-667.
43. Liu J-R, Sun X-R, Dong H-W, Sun C-H, Sun W-G, Chen B-Q, Song Y-Q, Yang B-F. 2008. ß-Ionone suppresses mammary carcinogenesis, proliferative activity and induces apoptosis in the mammary gland of the Sprague-Sawley rat. International Journal of Cancer 122, 2689-2698.
44. Loeffler C, Berger S, Guy A, Durand T, Bringmann G, Dreyer M, von Rad U, Durner J, Mueller MJ. 2005. B1-phytoprostanes trigger plant defense and detoxification responses. Plant Physiology 137, 328-340.
45. Montenegro MA, Nazareno MA, Durantini EN, Borsarelli CD. 2002. Singlet molecular oxygen quenching ability of carotenoids in a reverse-micelle membrane mimetic system. Photochemistry and Photobiology 75, 353-361.
46. Mozzo M, Dall'Osto L, Hienerwadel R, Bassi R, Croce R. 2008. Photoprotection in the antenna complexes of Photosystem II. Role of individual xanthophylls in chlorophyll triplet quenching. Journal of Biological Chemistry 283, 6184-6192.
47. Mueller MJ, Berger S. 2009. Reactive electrophilic oxylipins: Pattern recognition and signalling. Phytochemistry 70, 1511-1521.
48. Mueller S, Hilbert B, Dueckershoff K, Roitsch T, Krischke M, Mueller MJ, Berger S. 2008. General detoxification and stress responses are mediated by oxidized lipids through TGA transcription factors in Arabidopsis. The Plant Cell 20, 768-785.
49. Ouchane S, Picaud M, Vernotte C, Astier C. 1997. Photooxidative stress stimulates illegitimate recombination and mutability in carotenoid-less mutants of Rubrivivax gelatinosus. The EMBO Journal 16, 4777-4787.
50. Ramel F, Birtic S, Cuiné S, Triantaphylidès C, Ravanat JL, Havaux M. 2012a. Chemical quenching of singlet oxygen by carotenoids in plants. Plant Physiology 158, 1267-1278.
51. Ramel F, Birtic S, Ginies C, Soubigou-Taconnat L, Triantaphylidès C, Havaux M. 2012b. Carotenoid oxidation products are stress signals that mediate gene responses to singlet oxygen in plants. Proceedings of the National Academy of Sciences, USA 109, 5535-5540.
52. Reynaud E, Aydemir G, Rühl R, Dangles O, Caris-Veyrat C. 2011. Organic synthesis of new putative lycopene metabolites and preliminary investigation of their cell-signaling effects. Journal of Agricultural and Food Chemistry 59, 1457-1463.
53. Rocca JR, Tumlinson JH, Glancey BM, Lofgren CS. 1983. Synthesis and stereochemistry of tetrahydro-3,5-dimethyl-6-(1-methylbutyl)-2H-pyran-2-one, a component of the queen recognition pheromone of Solenopsis invicta. Tetrahedron Letters 24, 1893-1896.
54. Salt SD, Tuzun S, Kuc J. 1986. Effect of ß-ionone and abscisic acid on the growth of tobacco and resistance to blue mold: Mimicry of effects of stem infection by Peronospora tabacina Adam. Physiological Molecular Plant Pathology 28, 287-297.
55. Scherzinger D, Al-Babili S. 2008. In vitro characterization of a carotenoid cleavage dioxygenase from Nostoc sp. PCC 7120 reveals a novel cleavage pattern, cytosolic localization and induction by highlight. Molecular Microbiology 69, 231-244.
56. Shao J, Xu Y, Wang Z, Jiang Y, Yu G, Peng X, Li R. 2011. Elucidating the toxicity targets of ß-ionone on photosynthetic system of Microcystis aeruginosa NIES-843 (Cyanobacteria). Aquatic Toxicology 104, 48-55.
57. Siefermann-Harms D. 1985. Carotenoids in photosynthesis. I. Location in photosynthetic membranes and light-harvesting function. Biochimica et Biophysica Acta 811, 325-355.
58. Siems WG, Sommerburg O, Hurst JS, van Kuijk FJGM. 2000. Carotenoid oxidative degradation products inhibit Na+-K+-ATPase. Free Radical Research 33, 427-435.
59. Siems W, Sommerburg O, Schild L, Augustin W, Langhans C-D, Wiswedel I. 2002. ß-Carotene cleavage products induce oxidative stress in vitro by impairing mitochondrial respiration. FASEB Journal 16, 1289-1291.
60. Strack D, Fester T. 2006. Isoprenoid metabolism and plastid reorganization in arbuscular mycorrhizal roots. New Phytologist 172, 22-34.
61. Stratton SP, Schaefer WH, Liebler DC. 1993. Isolation and identification of singlet oxygen oxidation products of ßcarotene. Chemical Research in Toxicology 6, 542-547.
62. Telfer A. 2005. Too much light? How ß-carotene protects the photosystem II reaction centre. Photochemical and Photobiological Sciences 4, 950-956.
63. Triantaphylidès C, Havaux M. 2009. Singlet oxygen in plants: Production, detoxification and signaling. Trends in Plant Science 14, 219-228.
64. Triantaphylidès C, Krischke M, Hoeberichts FA, Ksas B, Gresser G, Havaux M, van Breusegem F, Mueller MJ. 2008. Singlet oxygen is the major reactive oxygen species involved in photooxidative damage to plants. Plant Physiology 148, 960-968.
65. Wagner D, Przybyla D, Op den Camp R, et al. 2004. The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana. Science 306, 1183-1185.
66. Walsh K, Jones GJ, Dunstan RH. 1998. Effect of high irradiance and iron on volatile odour compounds in the cyanobacterium Microcystis aeruginosa. Phytochemistry 49, 1227-1239.
67. Weber H, Chélatat A, Reymond P, Farmer EE. 2004. Selective and powerful stress gene expression in Arabidopsis in response to malondialdehyde. The Plant Journal 37, 877-888.
68. Yamauchi R, Tsuchihashi K, Kato K. 1998. Oxidation products of ß-carotene during the peroxidation of methyl linoleate in the bulk phase. Bioscience, Biotechnology and Biochemistry 62, 1301-1306.
69. Yeh SL, Wu SH. 2006. Effects of quercetin on beta-apo-8'-carotenal- induced DNA damage and cytochrome P1A2 expression in A549 cells. Chemico-Biological Interactions 163, 199-206.