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http://dx.doi.org/10.5322/JES.2010.19.12.1323

Protective Effect of Nitric Oxide against Oxidative Stress under UV-B Radiation in Maize Leaves  

Kim, Tae-Yun (Department of Biological Sciences, Pusan National University)
Jo, Myung-Hwan (Department of Biological Sciences, Pusan National University)
Hong, Jung-Hee (Department of Biological Sciences, Pusan National University)
Publication Information
Journal of Environmental Science International / v.19, no.12, 2010 , pp. 1323-1334 More about this Journal
Abstract
The effect of nitric oxide (NO) on antioxidant system and protective mechanism against oxidative stress under UV-B radiation was investigated in leaves of maize (Zea mays L.) seedlings during 3 days growth period. UV-B irradiation caused a decrease of leaf biomass including leaf length, width and weight during growth. Application of NO donor, sodium nitroprusside (SNP), significantly alleviated UV-B stress induced growth suppression. NO donor permitted the survival of more green leaf tissue preventing chlorophyll content reduction and of higher quantum yield for photosystem II than in non-treated controls under UV-B stress, suggesting that NO has protective effect on chloroplast membrane in maize leaves. Flavonoids and anthocyanin, UV-B absorbing compounds, were significantly accumulated in the maize leaves upon UV-B exposure. Moreover, the increase of these compounds was intensified in the NO treated seedlings. UV-B treatment resulted in lipid peroxidation and induced accumulation of hydrogen peroxide ($H_2O_2$) in maize leaves, while NO donor prevented UV-B induced increase in the contents of malondialdehyde (MDA) and $H_2O_2$. These results demonstrate that NO serves as antioxidant agent able to scavenge $H_2O_2$ to protect plant cells from oxidative damage. The activities of two antioxidant enzymes that scavenge reactive oxygen species, catalase (CAT) and ascorbate peroxidase (APX) in maize leaves in the presence of NO donor under UV-B stress were higher than those under UV-B stress alone. Application of 2-(4-carboxyphenyl)-4, 4, 5, 5-tetramethylimidazoline-1-oxyl-3- oxide (PTIO), a specific NO scavenger, to the maize leaves arrested NO donor mediated protective effect on leaf growth, photosynthetic pigment and free radical scavenging activity. However, PTIO had little effect on maize leaves under UV-B stress compared with that of UV-B stress alone. $N^{\omega}$-nitro-L-arginine (LNNA), an inhibitor of nitric oxide synthase (NOS), significantly increased $H_2O_2$ and MDA accumulation and decreased antioxidant enzyme activities in maize leaves under UV-B stress. This demonstrates that NOS inhibitor LNNA has opposite effects on oxidative resistance. From these results it is suggested that NO might act as a signal in activating active oxygen scavenging system that protects plants from oxidative stress induced by UV-B radiation and thus confer UV-B tolerance.
Keywords
Antioxidant enzymes; Nitric oxide; Oxidative stress; UV-B radiation; Zea mays;
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1 Yannarelli, G. G., Gallego, S. M., Tomaro, M., 2005, Effect of UV-B radiation on the activity and isoforms of enzymes with peroxidase activity in sunflower cotyledons, Environ. Exp. Bot., 56, 174-181.   DOI
2 Zhang, M., An, L., Feng, H., Chen, T., Chen, K., Liu, L., Tang, H., Chang, J., Wang, X., 2003a, The cascade mechanisms of nitric oxide as a second messenger of ultraviolet-B in inhibiting mesocotyl elongations, Photochem. Photobiol., 77, 219-225.   DOI
3 Zhang, H., Shen, M. B., Xu, L. L., 2003b, Effects of nitric oxide on the germination of wheat seeds and its reactive oxygen species metabolism under osmotic stress, Acta. Bot. Sin., 45, 901-905.
4 Zhang, L., Zhou, S., Xuan, Y., Sun, M., Zhao, L., 2009, Protective effect of nitric oxide against oxidative damage in Arabidopsis leaves under UV-B irradiation, J. Plant Biol., 52, 135-140.   DOI
5 Zhao, M. G., Zhao, X., Wu, Y. X., Zhang, L. X., 2007, Enhanced sensitivity to oxidative stress in Arabidopsis nitric oxide synthesis mutant, J. Plant Physiol., 164, 737-745.   DOI
6 hao, S. J., Xu, C. C., Zhou, Q., Meng, Q. W., 1994. Improvement of method for measurement of malondialdehyde in plant tissues, Plant Physiol. Comm., 30, 207-210.
7 Schreiber, U., Schliwa, U., Bilger, W., 1986, Continuous recording of photochemical and nonphotochemical chlorophyll fluorescence quencing with a new type of modulation fluorometer, Photosynth. Res., 10, 51-62.   DOI
8 Song, L., Ding, W., Zhao, M., Sun, B., Zhang, L., 2006, Nitric oxide protects against oxidative stress under heat stress in the calluses from two ecotypes of reed, Plant Sci., 171, 449-458.   DOI   ScienceOn
9 Tossi, V., Lamattina, L., Cassia, R., 2009, An increase in the concentration of abscisic acid is critical for nitric oxide-mediated plant adaptive responses to UV-B irradiation, New Phytol., 181, 871-879.   DOI
10 Tu, J., Shen, Y. B., Xu, L. L., 2003, Regulation of nitric acid on the aging process of wheat leaves, Acta. Bot. Sin., 45, 1055-1062.
11 Uchida, A., Jagendorf, A. T., Hibino, T., Takabe, T., Takabe, T., 2002, Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice, Plant Sci., 163, 515-523.   DOI
12 Veljovic-Jovanovic, S., Noctor, G., Foyer, C. H., 2002, Are leaf hydrogen peroxide concentration commonly overestimated? The potential influence of artefactual interference by tissue phenolics and ascorbate, Plant Physiol. Biochem., 40, 501-507.   DOI
13 Warren, J. M., Bassman, J. H., Mattinson, D. S., Fellman, J. K., Edwards, G. E., Robberecht, R., 2002, Alteration of foliar flavonoid chemistry induced by enhanced UV-B radiation in field-grown Pinus ponderosa, Quercus rubra and Pseudotsuga menziesii, Photochem. Photobiol., 66, 125-133.   DOI
14 Wendehenne, D., Pulgin, A., Klessing, D. F., Durner, J., 2001, Nitric acid : comparative synthesis and signaling in animal and plant cell, Trends Plant Sci., 6, 177-186.   DOI
15 Wilson, I. D., Neill, S. J., Hancock, J. T., 2008, Nitric oxide synthesis and signalling in plants, Plant, Cell & Environ. 31, 622-631.   DOI
16 Inskeep, W. P., Bloom, P. R., 1985, Extinction coefficients of chlorophyll a and b in N, N-dimethylformamide and 80% acetone, Plant Physiol., 77, 483-485.   DOI
17 Lamotte, O., Gould, K., Lecourieux, D., Sequeira-Legrand, A., Lebrun-Garcia, A., Durner, J., Pugin, A., Wendehenne, D., 2004, Analysis of nitric oxide signalling functions in tobacco cells challenged by the elicitor cryptogein, Plant Physiol., 135, 516-529.   DOI
18 Leshem, Y. Y., 1996, Nitric oxide in biological systems, Plant Growth Regul., 18, 155-159.   DOI
19 Leshem, Y. Y., Haramaty, E., 1996, The characterization and contrasting effects of the nitric oxide free radical in vegetative stress and senescence of Pisum sativum Linn. foliage, J. Plant Physiol., 148, 258-263.   DOI   ScienceOn
20 Mackerness, S. A. -H., 2000, Plant responses to ultraviolet-B (UV-B : 280-320 nm) stress : what are the key regulators?, Plant Growth Regul., 32, 27-39.   DOI
21 Mackerness, S. A. -H., John, C. F., Jordan, B., Thomas, B., 2001, Early signaling components in ultraviolet-B responses : distinct roles for different reactive oxygen species and nitric oxide, FEBS Lett., 489, 237-242.   DOI
22 Mirecki, R. M., Teramura, A. H., 1984, Effects of ultraviolet-B irradiance on soybean, Plant Physiol., 74, 475-480.   DOI
23 Mittler, R., 2002, Oxidative stress, antioxidants and stress tolerance, Trends Plant Sci., 7, 405-410.   DOI
24 Neill, S. J., Desikan, R., Hancock, J. T., 2003, Nitric oxide signaling in plants, New Phytol., 159, 11-35.   DOI
25 Qiao, W., Fan, L.-M., 2008, Nitric oxide signaling in plant response abiotic stresses, J. Int. Plant Biol., 50, 1238-1246.   DOI
26 Beligni, M. V., Lamattina, L., 2001, Nitric oxide in plants : the history is just beginning, Plant Cell Environ. 24, 267-278.   DOI
27 Brosche, M., Strid, A., 2003, Molecular events following perception of ultraviolet-B radiation by plants, Physiol. Plant., 117, 1-10.   DOI
28 Clark, D., Dunar, J., Navarre, D. A., Klessig, D. F., 2000, Nitric oxide inhibition of tobacco catalase and ascorbate peroxidase, Mol. Plant-Microbe Interact., 14, 1380-1384.   DOI
29 Durner, J., Klessing, D. F., 1996, Salicylic acid is a modulator of tobacco and mammalian catalases, J. Biol. Chem., 271, 28492-28502.   DOI
30 Frohnmeyer, H., Staiger, D., 2003, Ultraviolet-B radiation-mediated responses in plants : balancing damage and protection, Plant Physiol., 133, 1420-1428.   DOI
31 Greenberg, B. M., Wilson, M. I., Huang, X. D., Duxbury, C. L., Gerhardt, K. E., Gensemer, R. W., 1997, The effects of ultraviolet-B radiation on higher plants, In : Wang, W., Gorsuch, J. W., Hughes, J. S. (eds.), Plants for environmental studies, CRC Lewis Publishers, Boca Raton, N. Y., 1-35.
32 Harborne, J. B., Williams, C. A., 2000, Advances in flavonoid research since 1992, Phytochem., 55, 481-504.   DOI
33 Hsu, Y. T., Kao, C. H., 2004, Cadmium toxicity is reduced by nitric oxide in rice leaves, Plant Growth Regul., 42, 227-238.   DOI
34 Hung, K. T., Chang, C. J., Kao, C. H., 2002, Paraquat toxicity is reduced by nitric oxide in rice leaves, J. Plant Physiol., 159, 159-166.   DOI
35 Huang, X., Rad, U., Durner, J., 2002, Nitric oxide induces transcriptional activation of the nitric oxide-tolerant alternative oxidase in Arabidopsis suspension cells, Planta, 215, 914-923.   DOI
36 An, L., Liu, Y., Zhang, M., Chen, T., Wang, X., 2005, Effects of nitric oxide on growth of maize seedling leaves in the presence or absence of ultraviolet-B radiation, J. Plant. Physiol., 162, 317-326.   DOI   ScienceOn
37 Apel, K., Hirt, H., 2004, Reactive oxygen species : metabolism, oxidative stress, and signal transduction, Annu. Rev. Plant Biol., 55, 373-399.   DOI
38 Beligni, M. V., Lamattina, L., 2000, Nitric oxide stimulates seed germination and de-etiolation, and inhibits hypocotyl elongation, three light-inducible responses in plants, Planta, 210, 215-221.   DOI