Current opinions on the functions of tocopherol based on the genetic manipulation of tocopherol biosynthesis in plants

Journal of Integrative Plant Biology

Volumn 50, Issue 9, 2008, Pages 1057-1069

  Li, Yin ^a   Wang, Zinan ^a   Sun, Xiaofen ^a   Tang, Kexuan ^a,b  

^a FUDAN UNIVERSITY   (China)

^b SHANGHAI JIAO TONG UNIVERSITY   (China)

Author keywords

Antioxidant; Carbohydrate metabolism; Genetic dissection; Programmed cell death; Redox homeostasis; Signal molecule; Tocopherol

Indexed keywords

REACTIVE OXYGEN METABOLITE; TOCOPHEROL;

ANTIOXIDANT; CARBOHYDRATE; GENOMICS; HOMEOSTASIS; LIPID; PLANT; REDOX CONDITIONS;

CYANOBACTERIUM; GENETICS; METABOLISM; PLANT; REVIEW;

CYANOBACTERIA; PLANTS; REACTIVE OXYGEN SPECIES; TOCOPHEROLS;

ANIMALIA; ARABIDOPSIS; ARABIDOPSIS THALIANA; SYNECHOCYSTIS; SYNECHOCYSTIS SP. PCC 6803;

EID: 51349112342     PISSN: 16729072     EISSN: 17447909     Source Type: Journal    
DOI: 10.1111/j.1744-7909.2008.00689.x     Document Type: Review

References (97)

1. Abbasi AR, Hajirezaei M, Hofius D, Sonnewald U, Voll LM (2007). Specific roles of α- and γ-Tocopherol in abiotic stress responses of transgenic tobacco. Plant Physiol. 143, 1720-1738.
2. Apel K, Hirt H (2004). Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55, 373-399.
3. Asada K (1999). The water-water cycle in chloroplasts: Scavenging of active oxygens and dissipation of excess photons. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 601-639.
4. Azzi A, Gysin R, KempnáP, Munteanu A, Negis Y, Villacorta L et al. (2004). Vitamin E mediates cell signaling and regulation of gene expression. Ann. NY Acad. Sci. 1031, 86-95.
5. Ball L, Accotto G, Bechtold U, Creissen G, Funck D, Jiménez A et al. (2004). Evidence for a direct link between glutathione biosynthesis and stress defense gene expression in Arabidopsis. Plant Cell 16, 2448-2462.
6. Bergmüller E, Porfirova S, Dörmann P (2003). Characterization of an Arabidopsis mutant deficient in γ-tocopherol methyltransferase. Plant Mol. Biol. 52, 1181-1190.
7. Bernier G, Havelange A, Houssa C, Petitjean A, Lejeune P (1993). Physiological signals that induce flowering. Plant Cell 5, 1147-1155.
8. Bramley PM, Elmadfa I, Kafatos A, Kelly FJ, Manios Y, Roxborough HE et al. (2000). Vitamin E. J. Sci. Food Agric. 80, 913-938.
9. Cahoon EB, Hall SH, Ripp KG, Ganzke TS, Hitz WD, Coughlan SJ (2003). Metabolic redesign of vitamin E biosynthesis in plants for tocotrienol production and increased antioxidant content. Nat. Biotechnol. 21, 1082-1087.
10. Caretto S, Paradiso A, D'Amico L, Gara LD (2002). Ascorbate and glutathione metabolism in two sunflower cell lines of differing α-tocopherol biosynthetic capability. Plant Physiol. Biochem. 40, 509-513.
11. Chen Z, Gallie DR (2004). The ascorbic acid redox state controls guard cell signaling and stomatal movement. Plant Cell 16, 1143-1162.
12. Cheng Z, Sattler S, Maeda H, Sakuragi Y, Bryant DA, DellaPenna D (2003). Highly divergent methyltransferases catalyze a conserved reaction in tocopherol and plastoquinone synthesis in cyanobacteria and photosynthetic eukaryotes. Plant Cell 15, 2343-2356.
13. Collakova E, DellaPenna D (2001). Isolation and functional analysis of homogentisate phytyltransferase from Synechocystis sp. PCC 6803 and Arabidopsis. Plant Physiol. 127, 1113-1124.
14. Collakova E, DellaPenna D (2003a). The role of homogentisate phytyltransferase and other tocopherol pathway enzymes in regulation of tocopherol biosynthesifcs during abiotic stress. Plant Physiol. 133, 930-940.
15. Collakova E, DellaPenna D (2003b). Homogentisate phytyltransferase activity is limiting for tocopherol biosynthesis in Arabidopsis. Plant Physiol. 131, 632-642.
16. Coruzzi M, Zhou L (2001). Carbon and nitrogen sensing and signaling in plants: Emerging "matrix effect". Curr. Opin. Plant Biol. 4, 247-253.
17. Creelman A, Mullet E (1997). Biosynthesis and action of jasmonates in plants. Annu. Rev. Plant Mol. Biol. 48, 255-381.
18. Dähnhardt D, Falk J, Appel J, Van Der Kooij TA, Schulz-Friedrich R, Krupinska K (2002). The hydroxyphenylpyruvate dioxygenase from Synechocystis sp. PCC 6803 is not required for plastoquinone biosynthesis. FEBS Lett. 523, 177-181.
19. Dat JF, Foyer CH, Scott IM (1998). Changes in salicylic acid and antioxidants during induction of thermotolerance in mustard seedings. Plant Physiol. 118, 1455-1461.
20. DellaPenna D (2005a). A decade of progress in understanding vitamin E synthesis in plants. J. Plant Physiol. 162, 729-737.
21. DellaPenna D (2005b). Progress in the dissection and manipulation of vitamin E synthesis. Trends Plant Sci. 10, 574-579.
22. DellaPenna D, Last RL (2006). Progress in the dissection and manipulation of plant vitamin E biosynthesis. Physiol. Plant. 126, 356-368.
23. DellaPenna D, Pogson BJ (2006). Vitamin synthesis in plants: Tocopherols and carotenoids. Annu. Rev. Plant Biol. 57, 711-738.
24. van Eenennaam A, Valentin HE, Karunanandaa B, Hao M, Aasen E, Levering C (2003a). Methyltransferase genes and uses of thereof. International Patent Application WO 30/16482.
25. van Eenennaam A, Lincoln K, Durrett TP, Valentin HE, Shewmaker CK, Thorne GM et al. (2003b). Engineering vitamin E content: From Arabidopsis mutant to soy oil. Plant Cell 15, 3007-3019.
26. Evans HM, Bishop KS (1922). On the existence of a hitherto unrecognized dietary factor essential for reproduction. Science 56, 650-651.
27. Evans NH, McAinsh MR, Hetherington AM, Knight MR (2005). ROS perception in Arabidopsis thaliana: The ozone-induced calcium response. Plant J. 41, 615-626.
28. Falk J, Brosch M, Schafer A, Braun S, Krupinska K (2005). Characterization of transplastomic tobacco plants with a plastid localized barley 4-hydroxyphenylpyruvate dioxygenase. J. Plant Physiol. 162, 738-742.
29. Falk J, Krauß N, Dähnhardt D, Krupinska K (2002). The senescence associated gene of barley encoding 4-hydroxyphenylpyruvate dioxygenase is expressed during oxidative stress. J. Plant Physiol. 159, 1245-1253.
30. Foyer CH, Noctor G (2005). Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17, 1866-1875.
31. Foyer CH, Vanacker H, Gomez LD, Harbinson J (2002). Regulation of photosynthesis and antioxidant metabolism in maize leaves at optimal and chilling temperatures: Review. Plant Physiol. Biochem. 40, 659-668.
32. Gibson SI (2005). Control of plant development and gene expression by sugar signaling. Curr. Opin. Plant Biol. 8, 93-102.
33. Grusak MA (1999). Genomics-assisted plant improvement to benefit human nutrition and health. Trends Plant Sci. 4, 164-166.
34. Havaux M, Eymery F, Porfirova S, Rey P, Dörmann P (2005). Vitamin E protects against photoinhibition and photooxidative stress in Arabidopsis thaliana. Plant Cell 17, 3451-3469.
35. Havaux M, Lütz C, Grimm B (2003). Chloroplast membrane stability in chlP transgenic tobacco plants deficient in tocopherols. Plant Physiol. 132, 300-310.
36. Hofius D, Hajirezaei M, Geiger M, Tschiersch H, Melzer M, Sonnewald U (2004). RNAi-mediated tocopherol deficiency impairs photo assimilate export in transgenic potato plants. Plant Physiol. 135, 1256-1268.
37. Hunter SC, Cahoon EB (2007). Enhancing vitamin E in oilseeds: Unraveling tocopherol and tocotrienol biosynthesis. Lipids 42, 97-108.
38. Kanwischer M, Porfirova S, Bergmüller E, Dörmann P (2005). Alterations in tocopherol cyclase activity in transgenic and mutant plants of Arabidopsis affect tocopherol content, tocopherol composition, and oxidative stress. Plant Physiol. 137, 713-723.
39. Karunanandaa B, Qi Q, Hao M, Baszis S, Jensen P, Wong Y-HH et al. (2005). Metabolically engineered oilseed crops with enhanced seed tocopherol. Metab. Eng. 7, 384-400.
40. Kruk J, Schmid GH, Strzalka K (2000). Interaction of α-tocopherol quinone, α-tocopherol and other prenyllipids with photosystem II. Plant Physiol. Biochem. 38, 271-277.
41. Kruk J, Strzalka K (1995). Occurrence and function of quinone in plants. J. Plant Physiol. 145, 405-409.
42. Kumar R, Raclaru M, Schüßeler T, Gruber J, Sadre R, Lühs W et al. (2005). Characterisation of plant tocopherol cyclases and their overexpression in transgenic Brassica napus seeds. FEBS Lett. 579, 1357-1364.
43. Léon P, Sheen J (2003). Sugar and hormone connections. Trends Plant Sci. 8, 110-116.
44. Liebler DC, Burr JA (1992). Oxidation of vitamin E during iron-catalyzed lipid peroxidation: Evidence for electron-transfer reactions of the tocopheroxyl radical. Biochemistry 8, 8278-8284.
45. Lloyd JC, Zakhleniuk OV (2004). Responses of primary and secondary metabolism to sugar accumulation revealed by microarray expression analysis of the Arabidopsis mutant, pho3. J. Exp. Bot. 55, 1221-1230.
46. Maeda H, DellaPenna D (2007). Tocopherol functions in photosynthetic organisms. Curr. Opin. Plant Biol. 10, 260-265.
47. Maeda H, Sakuragi Y, Bryant DA, DellaPenna D (2005). Tocopherols protect Synechocystis sp. Strain PCC 6803 from lipid peroxidation. Plant Physiol. 138, 1422-1435.
48. Maeda H, Song W, Sage TL, DellaPenna D (2006). Tocopherols play a crucial role in low-temperature adaptation and phloem loading in Arabidopsis. Plant Cell 18, 2710-2732.
49. Mateo A, Mühlenbock P, Rustéchal P, Keryer E, Miginiac-Maslow M, Decottignies P (2004). LESION SIMULATING DISEASE 1 is required for acclimation to conditions that promote excess excitation energy. Plant Physiol. 136, 2818-2834.
50. Maxwell DP, Nickels R, Mclntosh L (2002). Evidence of mitochondrial involvement in the transduction of signals required for the induction of genes associated with pathogen attack and senescence. Plant J. 29, 269-279.
51. Müller M, Hernández I, Alegre L, Munné-Bosch S (2006). Enhanced α-tocopherol quinine levels and xanthophyll cycle de-epoxidation in rosemary plants exposed to water deficit during a Mediterranean winter. J. Plant Physiol. 163, 601-606.
52. Munné-Bosch S (2005a). Linking tocopherols with cellular signaling in plants. New Phytol. 166, 363-366.
53. Munné-Bosch S (2005b). The role of α-tocopherol in plant stress tolerance. J. Plant Physiol. 162, 743-748.
54. Munné-Bosch S (2007). Alpha-tocopherol: A multifaceted molecule in plants. Vitam. Horm. 76, 375-392.
55. Munné-Bosch S, Alegre L (2002). The function of tocopherols and tocotrienols in plants. Crit. Rev. Plant Sci. 21, 31-57.
56. Munné-Bosch S, Alegre L (2003). Drought-induced changes in the redox state of α-tocopherol, ascorbate, and the diterpene carnosic acid in chloroplasts of Labiatae plants differing in carnosic acid contents. Plant Physiol. 131, 1816-1825.
57. Munné-Bosch S, Falk J (2004). New insights into the function of tocopherols in plants. Planta 218, 323-326.
58. Munné-Bosch S, Peñuelas J (2004). Drought-induced oxidative stress in strawberry tree (Arbutus unedo L.) growing in Mediterranean field conditions. Plant Sci. 166, 1105-1110.
59. Munné-Bosch S, Weiler EW, Alegre L, Müller M, Düchting P, Falk J (2007). α-Tocopherol may influence cellular signaling by modulating jasmonic acid levels in plants. Planta 225, 1039-1049.
60. Norris SR, Barette TR, DellaPenna D (1995). Genetic dissection of carotenoid synthesis in Arabidopsis defines plastoquinone as an essential component of phytone desaturation. Plant Cell 7, 2139-2149.
61. Norris SR, Shen X, DellaPenna D (1998). Complementation of the Arabidopsis pds1 mutation with the gene encoding p -hydroxyphenylpuruvate dioxygenase. Plant Physiol. 117, 1317-1323.
62. Pascoe GA, Fariss MW, Olafsdottir K, Reed DJ (1987). A role of vitamin E in protection against cell injury. Eur. J. Biochem. 166, 241-247.
63. Pastori GM, Foyer CH (2002). Common components, networks, and pathways of cross-tolerance to stress. The central role of "Redox" and abscisic acid-mediated controls. Plant Physiol. 129, 460-468.
64. Paul MJ, Pellny TK (2003). Carbon metabolite feedback regulation of leaf photosynthesis and development. J. Exp. Bot. 54, 539-547.
65. Price J, Laxmi A, St Martin SK, Jang JC (2004). Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis. Plant Cell 16, 2128-2150.
66. Price J, Li T C, Kang SG, Na JK, Jang JC (2003). Mechanisms of glucose signaling during germination of Arabidopsis. Plant Physiol. 132, 1424-1438.
67. Provencher LM, Miao L, Sinha N, Lucas WJ (2001). Sucrose export defective1 encodes a novel protein implicated in chloroplast-to-nucleus signaling. Plant Cell 13, 1127-1141.
68. Porfirova S, Bergmüller E, Tropf S, Lemke R, Dörmann P (2002). Isolation of an Arbidopsis mutant lacking vitamin E and identification of a cyclase essential for tocopherol biosynthesis. Proc. Natl. Acad. Sci. USA 99, 12495-12500.
69. 2-metabolizing enzymes. Plant Physiol. 115, 137-149.
70. Rippert P, Scimemi C, Dubald M, Matringe M (2004). Engineering plant shikimate pathway for production of tocotrienol and improving herbicide resistance. Plant Physiol. 134, 92-100.
71. Rohmer M (2003). Mevalonate-independent methylerythritol phosphate pathway for isoprenoid biosynthesis. Elucidation and distribution. Pure Appl. Chem. 75, 375-387.
72. Rolland F, Moore B, Sheen J (2002). Sugar sensing and signaling in plants. Plant Cell 14, S185-S205.
73. Sakuragi Y, Maeda H, DellaPenna D, Bryant DA (2006). α-Tocopherol plays a role in photosynthesis and macronutrient homeostasis of the Cyanobacterium Synechocystis sp. PCC 6803 that is independent of its antioxidant function. Plant Physiol. 141, 508-521.
74. Sandorf I, Holländer-Czytko H (2002). Jasmonate is involved in the induction of tyrosine aminotransferase and tocopherol biosynthesis in Arabidopsis thaliana. Planta 216, 149-173.
75. Sattler SE, Cahoon EB, Coughlan SJ, DellaPenna D (2003). Characterization of tocopherol cyclases from higher plants and cyanobacteria. Evolutionary implications for tocopherol synthesis and function. Plant Physiol. 132, 2184-2195.
76. Sattler SE, Gilliland LU, Magallanes-Lundback M, Pollard M, DellaPenna D (2004). Vitamin E is essential for seed longevity and for preventing lipid peroxidation during germination. Plant Cell 16, 1419-1432.
77. Sattler SE, Mène-Saffrané L, Farmer EE, Krischke M, Mueller MJ, DellaPenna D (2006). Nonenzymatic lipid peroxidation reprograms gene expression and activates defense markers in Arabidopsis tocopherol-deficient mutants. Plant Cell 18, 3706-3720.
78. Savidge B, Weiss JD, Wong YHH, Lassner MW, Mitsky TA, Shewmaker CK et al. (2002). Isolation and characterization of homogentisate phytyltransferase genes from Synechocystis sp PCC6803 and Arabidopsis. Plant Physiol. 129, 321-332.
79. Schaller F (2001). Enzymes of the biosynthesis of octadecanoid-derived signaling molecules. J. Exp. Bot. 52, 11-23.
80. Schledz M, Seidler A, Beyer P, Neuhaus G (2001). A novel phytyltransferase from Synechocystis sp. PCC 6803 involved in tocopherol biosynthesis. FEBS Lett. 499, 15-20.
81. Schneider C (2005). Chemistry and biology of vitamin E. Mol. Nutr. Food Res. 49, 7-30.
82. Sen CK, Khanna S, Roy S (2006). Tocotrienols: Vitamin E beyond tocopherols. Life Sci. 78, 2088-2098.
83. Shintani D, DellaPenna D (1998). Elevating the vitamin E content of plants through metabolic engineering. Science 282, 2098-2100.
84. Shintani DK, Cheng Z, DellaPenna D (2002). The role of 2-methyl-6-phytylbenzoquinone methyltransferase in determining tocopherol composition in Synechocystis sp. PCC 6803. FEBS Lett. 511, 1-5.
85. Soll J, Schultz G (1979). Comparison of geranylgeranyl and phytyl substituted methylquinols in the tocopherol synthesis of spinach chloroplasts. Biochem. Biophys. Res. Commun. 91, 715-720.
86. Subramanniam S, Slater S, Karberg K, Chen R, Valentin HE, Wong Y-HH (2001). Nucleic acid sequences to proteins involved in tocopherol synthesis. International Patent Application WO 01/79472.
87. Theriault A, Chao JT, Wang Q, Gapor A, Adeli K (1999). Tocotrienol: A review of its therapeutic potential. Clin. Biochem. 32, 309-319.
88. Thum KE, Shin MJ, Palenchar PM, Kouranov A, Coruzzi GM (2004). Genome-wide investigation of light and carbon signaling interactions in Arabidopsis. Genom. Biol. 5, R10.
89. Tokunaga T, Miyahara K, Tabata K, Esaka M (2005). Generation and properties of ascorbic acid-overrproducing transgenic tobacco cells expressing sense RNA for L-galactono-1,4-lactone dehydrogenase. Planta 220, 854-863.
90. 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 Lett. 516, 156-160.
91. Tsegaye Y, Shintani DK, DellaPenna D (2002). Overexpression of the enzyme p-hydroxyphenylpyruvate dioxygenase in Arabidopsis and its relation to tocopherol biosynthesis. Plant Physiol. Biochem. 40, 913-920.
92. Valentin HE, Lincoln K, Moshiri F, Jensen PK, Qi Q, Venkatesh TV et al. (2006). The Arabidopsis vitamin E pathway gene5-1 mutant reveals a critical role for phytol kinase in seed tocopherol biosynthesis. Plant Cell 18, 212-224.
93. Valentin HE, Qi Q (2005). Biotechnological production and application of vitamin E: Current state and prospects. Appl. Microbiol. Biotechnol. 68, 436-444.
94. Vidi PA, Kanwischer M, Baginsky S, Austin JR, Csucs G, Dörmann P et al. (2006). Tocopherol cyclase (VTE1) localization and vitamin E accumulation in chloroplast plastoglobule lipoprotein particles. J. Biol. Chem. 281, 11225-11234.
95. Welsch R, Medina J, Giuliano G, Beyer P, von Litig J (2003). Structural and functional characterization of the phytoene synthase promoter from Arabidopsis thaliana. Planta 216, 523-534.
96. Weschke W, Panitz R, Gubatz S, Wang Q, Radchuk R, Weber H et al. (2003). The role of invertases and hexose transporters in controlling sugar ratios in maternal and filial tissues of barley caryopses during early development. Plant J. 33, 395-411.
97. Welsch R, Medina J, Giuliano G, Beyer P, von Litig J (2003). Structural and functional characterization of the phytoene synthase promoter from Arabidopsis thaliana. Planta 216, 523-534.