Biologia plantarum 53:670-676, 2009 | DOI: 10.1007/s10535-009-0121-0
Effects of ozone on wild type and transgenic tobacco
- 1 Institute of Botany, Chinese Academy of Sciences, Beijing, P.R. China
- 2 Graduate School of the Chinese Academy of Sciences, Beijing, P.R. China
- 3 Department of Biology, University of Antwerp, Wilrijk, Belgium
Tocopherol cyclase (TC, encoded by gene VTE1) catalyzes the penultimate step of tocopherol synthesis. In this study we used wild type and transgenic tobacco plants overexpressing VTE1 from Arabidopsis to examine the role of tocopherol in ozone sensitivity. Wild type plants responded to an 4-h exposure to 300 nmol mol-1 ozone by severe leaf necrosis while the transgenic lines exhibited limited injury. Compared with the wild type, VTE1-overexpressing plants had lower increase in hydrogen peroxide, malondialdehyde contents and ion leakage, and lower decrease of net photosynthetic rate 48 h following the ozone exposure. Transgenic plants also better maintained the structural integrity of the photosynthetic apparatus.
Keywords: hydrogen peroxide; malondialdehyde; ion leakage; photosynthetic rate; tocopherol; ultrastructure
Subjects: chloroplast; electrolyte leakage; hydrogen peroxide; malondialdehyde; Nicotiana tabacum; ozone; photosynthetic rate; stomatal conductance; tobacco; tocopherol; tocopherol cyclase; transgenic plants; transpiration rate; ultrastructure
Received: October 24, 2008; Accepted: September 20, 2009; Published: December 1, 2009 Show citation
References
- Abbasi, A.R., Hajirezaei, M., Hofius, D., Sonnewald, U., Voll, L.M.: Specific roles of α- and γ-tocopherol in abiotic stress responses of transgenic tobacco. - Plant Physiol. 143: 1720-1738, 2007.
Go to original source... - Alscher, R.G., Erturk, N., Heath, L.S.: Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. - J. exp. Bot. 53: 1331-1341, 2002.
Go to original source... - Asada, K.: The water-water cycle as alternative photon and electron sinks. - Phil. Trans. roy. Soc. London B 355: 1419-1431. 2000.
Go to original source... - Bergmüller, E., Porfirova, S., Dörmann, P.: Characterization of an Arabidopsis mutant deficient in γ-tocopherol methyltransferase. - Plant mol. Biol. 52: 1181-1190, 2003.
Go to original source... - Bhargava, P., Atri, N., Srivastava, A.K., Rai, L.C.: Cadmium mitigates ultraviolet-B stress in Anabaena doliolum: enzymatic and non-enzymatic antioxidants. - Biol. Plant. 51: 546-550, 2007.
Go to original source... - Chen, S., Li, H., Liu, G.: Progress of vitamin E metabolic engineering in plants. - Transgenic Res. 15: 655-665, 2006.
Go to original source... - Chen, Z., Gallie, D.R.: Increasing tolerance to ozone by elevating foliar ascorbic acid confers greater protection against ozone than increasing avoidance. - Plant Physiol. 138: 1673-1689, 2005.
Go to original source... - Cheng, Z., Sattler, S., Maeda, H., Sakuragi, Y., Bryant, D.A., Della Penna, D.: Highly divergent methyltransferases catalyze a conserved reaction in tocopherol and plastoquinone synthesis in Cyanobacteria and photosynthetic eukaryotes. - Plant Cell 15: 2343-2356, 2003.
Go to original source... - Chun, J., Lee, J., Ye, L., Exler, J., Eitenmiller, R.R.: Tocopherol and tocotrienol contents of raw and processed fruits and vegetables in the United States diet. - J. Food Comp. Anal. 19: 196-204, 2006.
Go to original source... - Collakova, E., Della Penna, D.: The role of homogentisate phytyltransferase and other tocopherol pathway enzymes in the regulation of tocopherol synthesis during abiotic stress. - Plant Physiol. 133: 930-940, 2003.
Go to original source... - Collin, V.C., Eymery, F., Genty, B., Rey, P., Havaux, M.: Vitamin E is essential for the tolerance of Arabidopsis thaliana to metal-induced oxidative stress. - Plant Cell Environ. 31: 244-257, 2008.
Go to original source... - Conklin, P.L., Barth, C.: Ascorbic acid, a familiar small molecule intertwined in the response of plants to ozone, pathogens, and the onset of senescence. - Plant Cell Environ. 27: 959-970, 2004.
Go to original source... - Dat, J., Vandenabeele, S., Vranová, E., Van Montagu, M., Inzé, D., Van Breusegem, F.: Dual action of the active oxygen species during plant stress responses. - Cell. Mol. Life Sci. 57: 779-795, 2000.
Go to original source... - Della Penna, D.: A decade of progress in understanding vitamin E synthesis in plants. - J. Plant Physiol. 162: 729-737, 2005.
Go to original source... - Della Penna, D., Last, R.L.: Progress in the dissection and manipulation of plant vitamin E biosynthesis. - Physiol. Plant. 126: 356-368, 2006.
Go to original source... - Della Penna, D., Pogson, B.J.: Vitamin synthesis in plants: tocopherols and carotenoids. - Annu. Rev. Plant Biol. 57: 711-738, 2006.
Go to original source... - Fryer, M.J.: The antioxidant effects of thylakoid vitamin E (alpha;-tocopherol). - Plant Cell Environ. 15: 381-392, 1992.
Go to original source... - Foyer, C.H., Noctor, G.: Oxidant and antioxidant signaling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. - Plant Cell Environ. 28: 1056-1071, 2005.
Go to original source... - Guo, J., Liu, X., Li, X., Chen, S., Jin, Z., Liu, G.: Overexpression of VTE1 from Arabidopsis resulting in high vitamin E accumulation and salt stress tolerance increase in tobacco plant. - Chin. J. appl. Environ. Biol. 12: 468-471, 2006.
- Havaux, M., Enmery, F., Porfirova, S., Rey, P., Dörmann, P.: Vitamin E protects against photoinhibition and photooxidative stress in Arabidopsis thaliana. - Plant Cell 17: 3451-3469, 2005.
Go to original source... - Hodges, D.M., DeLong, J.M., Forney, C.F., Prange, R.K.: Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissue containing anthocyanin and other interfering compounds. - Planta 207: 604-611, 1999.
Go to original source... - Hofius, D., Hajirezaei, M.R., Geiger, M., Tschiersch, H., Melzer, M., Sonnewald, U.: RNAi-mediated tocopherol deficiency impairs photoassimilate export in transgenic potato plants. - Plant Physiol. 135: 1256-1268, 2004.
Go to original source... - Kanwischer, M., Porfirova, S., Bergmüller, E., Dörmann, P.: 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, 2005.
Go to original source... - Keen, N.T.: The molecular biology of disease resistance. - Plant mol. Biol. 19: 109-122, 1992.
Go to original source... - Kumar, R., Raclaru, M., Schüβeler, T., Gruber, J., Sadre, R., Lühs, W., Zarhloul, K.M., Friedt, W., Enders, D., Frentzen, M., Weier, D.: Characterization of plant tocopherol cyclases and their overexpression in transgenic Brassica napus seeds.-FEBS Lett. 579: 1357-1364, 2005.
Go to original source... - Lee, K., Lee, S.M., Park, S.R., Jung, J., Moon, J.K., Cheong, J.J., Kim, M.: Overexpression of Arabidopsis homogentisate phytyltransferase or tocopherol cyclase elevates vitamin E content by increasing γ-tocopherol level in lettuce (Lactuca sativa L.). - Mol. Cells 24: 301-306, 2007.
- Li, X.-M., He, X.-Y., Zhang, L.-H., Chen, W., Chen, Q.: Influence of elevated CO2 and O3 on IAA, IAA oxidase and peroxidase in the leaves of ginkgo trees. - Biol. Plant. 53: 339-342, 2009.
Go to original source... - Liu, X., Hua, X., Guo, J., Qi, D., Wang, L., Liu, Z., Jin, Z., Chen, S., Liu, G.: Enhanced tolerance to drought stress in transgenic tobacco plants overexpressing VTE1 for increased tocopherol production from Arabidopsis thaliana. - Biotechnol. Lett. 30: 1275-1280, 2008.
Go to original source... - Maeda, H., Sakuragi, Y., Bryant, D.A., Della Penna, D.: Tocopherols protect Synechocystis sp. strain PCC 6803 from lipid peroxidation. - Plant Physiol. 138: 1422-1435, 2005.
Go to original source... - Maeda, H., Song, W., Sage, T.L., Della Penna, D.: Tocopherols play a crucial role in low-temperature adaptation and phloem loading in Arabidopsis. - Plant Cell 18: 2710-2732, 2006.
Go to original source... - Mehdy, M.C.: Active oxygen species in plant defense against pathogens. - Plant Physiol. 105: 467-472, 1994.
Go to original source... - Munné-Bosch, S.: The role of α-tocopherol in plant stress tolerance. - J. Plant Physiol. 162: 743-748, 2005.
Go to original source... - Munné-Bosch, S., Alegre, L.: The function of tocopherols and tocotrienols in plants. - Crit. Rev. Plant Sci. 21: 31-57, 2002.
Go to original source... - Munné-Bosch, S., Schwarz, K., Alegre, L.: Enhanced formation of α-tocopherol and highly oxidized abietane diterpenes in water-stressed rosemary plants. - Plant Physiol. 121: 1047-1052, 1999.
Go to original source... - Nakajima, N., Itoh, T., Takikawa, S., Asai, N., Tamaoki, M., Aono, M., Kubo, A., Azumi, Y., Kamada, H., Saji, H.: Improvement in ozone tolerance of tobacco plants with an antisense DNA for 1-aminocyclopropane-1-carboxylate synthase. - Plant Cell Environ. 25: 727-735, 2002.
Go to original source... - Pasqualini, S., Piccioni, C., Reale, L., Ederli, L., Torre, G.D., Ferranti, F.: Ozone-induced cell death in tobacco cultivar Bel W3 plants. The role of programmed cell death in lesion formation. - Plant Physiol. 133: 1122-1134, 2003.
Go to original source... - Pell, E.J., Eckardt, N.A., Glick, R.E.: Biochemical and molecular basis for impairment of photosynthetic potential. - Photosynth. Res. 39: 453-462, 1994.
Go to original source... - Pellinen, R.I., Korhonen, M.S., Tauriainen, A.A., Palva E.T., Kangasjărvi, J.: Hydrogen peroxide activates cell death and defense gene expression in birch. - Plant Physiol. 130: 549-560, 2002.
Go to original source... - Porfirova, S., Bergmüller, E., Tropf, S., Lemke, R., Dörmann, P.: Isolation of an Arabidopsis mutant lacking vitamin E and identification of a cyclase essential for all tocopherol biosynthesis. - Proc. nat. Acad. Sci. USA 99: 12495-12500, 2002.
Go to original source... - Rippert, P., Scimemi, C., Dubald, M., Matringe, M.: Engineering plant shikimate pathway for production of tocotrienol and improving herbicide resistance. - Plant Physiol. 134: 92-100, 2004.
Go to original source... - Rizhsky, L., Hallak-Herr, E., Van Breusegem, F., Rachmilevitch, S., Barr, J.E., Rodermel, S., Inzé, D., Mittler, R.: Double antisense plants lacking ascorbate peroxidase and catalase are less sensitive to oxidative stress than single antisense plants lacking ascorbate peroxidase or catalase. - Plant J. 32: 329-342, 2002.
Go to original source... - Sattler, S.E., Gillilant, L.U., Magallanes-Lundback, M., Pollard, M., Della Penna, D.: Vitamin E is essential for seed longevity and for preventing lipid peroxidation during germination. - Plant Cell 16: 1419-1432, 2004.
Go to original source... - Sattler, S.E., Mène-Saffrané, L., Farmer, E.E., Krischke, M., Mueller, M.J., Della Penna, D.: Nonenzymatic lipid peroxidation reprograms gene expression and activates defense markers in Arabidopsis tocopherol-deficient mutants. - Plant Cell 18: 3706-3720, 2006.
Go to original source... - Schneider, C.: Chemistry and biology of vitamin E. - Mol. Nutr. Food Res. 49: 7-30, 2005.
Go to original source... - Shintani, D.K., Zigang, C., Della Penna, D.: The role of 2-methyl-6-phytylbenzoquinone methyltransferases in determining tocopherol composition in Synechocystis sp. PCC6803. - FEBS Lett. 511: 1-5, 2002.
Go to original source... - Soldatini, G.F., Nali, C., Guidi, L., Lorenzini, G.: Photosynthesis of Hedera canariensis var. azorica variegated leaves as affected by ozone. - Photosynthetica 35: 248-253, 1998.
Go to original source... - Trebst, A., Depka, B., Höllander-Czytko, H.: A specific role for tocopherol and of chemical singlet oxygen quenchers in the maintenance of photosystem Π structure and function in Chlamydomonas reinhardtii. - FEBS Lett. 516: 156-160, 2002.
Go to original source... - Uprety, D.C.: Carbon dioxide enrichment technology: Open Top Chambers a new tool for global climate research. - J. Sci. Ind. Res. 57: 266-270, 1998.
- Vidi, P.A., Kanwischer, M., Baginsky, S., Austin, J.R., Csucs, G., Dörmann, P., Kessler, F., Bréhélin, C.: Tocopherol cyclase (VTE1) localization and vitamin E accumulation in chloroplast plastoglobule lipoprotein particles. - J. biol. Chem. 281: 11225-11234, 2006.
Go to original source... - Von Caemmerer, S. Farquhar, G.D.: Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. - Planta 153: 376-387, 1981.
Go to original source... - Wagner, J.G., Jiang, Q., Harkema, J.R., Illek, B., Patel, D.D., Ames, B.N., Peden, D.B.: Ozone enhancement of lower airway allergic inflammation is prevented by γ-tocopherol. - Free Radical Biol. Med. 4: 1176-1188, 2007.
Go to original source... - Wang, X., Quinn, P.J.: The location and function of vitamin E in membranes (review). - Mol. Membr. Biol. 17: 143-156, 2000.
Go to original source... - Weber, H., Chételat, A., Reymond, P., Farmer, E.E.: Selective and powerful stress gene expression in Arabidopsis in response to malondialdehyde. - Plant J. 37: 877-888, 2004.
Go to original source...



