Abstract
Nitric oxide (NO) is a key molecule involved in many physiological processes. To characterize its roles in the tolerance of Arabidopsis thaliana to ultraviolet-B (UV-B), we investigated the effect of a reduced endogenous NO level on oxidative damage to wild-type and mutant (Atnoa1) plants. Under irradiation, hydrogen peroxide was accumulated more in mutant leaves than in the wild type. However, the amounts of UV-B-absorbing compounds (flavonoids and anthocyanin) and the activities of two antioxidant enzymes—catalase (CAT, EC 1.11.1.6) and ascorbate peroxidase (APX, EC 1.11.1.11)—were lower in leaves of the former. Supplementing with sodium nitroprusside, an NO donor, could alleviate the oxidative damage to mutant leaves by increasing flavonoid and anthocyanin contents and enzyme activities. In comparison, \({\text{N}}^{\text{ $ \omega $ }} - {\text{nitro}} - l - {\text{arginine}}\), an inhibitor of nitric oxide synthase, had the opposite effects on oxidation resistance in wild-type leaves. All these results suggest that nitric oxide acts as a signal for an active oxygen-scavenging system that protects plants from oxidative stress induced by UV-B irradiation.
Similar content being viewed by others
Abbreviations
- APX:
-
ascorbate peroxidase
- CAT:
-
catalase
- H2O2 :
-
hydrogen peroxide
- LNNA:
-
\({\text{N}}^{\text{ $ \omega $ }} - {\text{nitro}} - l - {\text{arginine}}\)
- MP:
-
membrane permeability
- NO:
-
nitric oxide
- NOS:
-
nitric oxide synthase
- SNP:
-
sodium nitroprusside
- UV-B:
-
ultraviolet-B
References
Beligni MV, Lamattina L (2001) Nitric oxide: a non-traditional regulator of plant growth. Trends Plant Sci 11:508–509
Boullerne AI, Nedelkoska L, Benjamins JA (1999) Synergism of nitric oxide and iron in killing the transformed murine oligodendrocyte cell line N20.1. J Neurochem 72:1050–1060
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantity of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Meth Enzymol 52:302–310
Crawford NM, Galli M, Tischner R, Heimer YM, Okamoto M, Mack A (2006) Response to Zemojtel et al. Plant nitric oxide synthase: back to square one. Trend Plant Sci 11:526–527
Day TA, Vogelmann TC (1995) Alteration in photosynthesis and pigment distribution in pea leaves following UV-B exposure. Physiol Plant 94:433–440
Durner J, Klessing DF (1996) Salicylic acid is a modulator of tobacco and mammalian catalases. J Biol Chem 271:28492–28502
Durner J, Klessing DF (1999) Nitric oxide as a signal in plants. Curr Opin Plant Biol 2:369–374
Foresi NP, Laxalt AM, Tonón CV, Casalongué CA, Lamattina L (2007) Extracellular ATP induces nitric oxide production in tomato cell suspensions. Plant Physiol 145:589–592
Guo FQ (2006) Response to Zemojtel et al. Plant nitric oxide synthase: AtNOS1 is just the beginning. Trend Plant Sci 11:527–528
Guo FQ, Okamoto M, Crawford NM (2003) Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science 302:100–103
Leshem YY, Wills RBH, Ku VV (1998) Evidence for the function of the free radical gas-nitric oxide (NO) as an endogenous maturation and senescence regulating factor in higher plants. Plant Physiol Biochem 36:825–833
Mackerness SAH, John CF, 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
Mata CG, Lamattina L (2001) Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress. Plant Physiol 126:1196–1204
McCord JM, Fridovich I (1969) The utility of superoxide dismutase in studying free radical reactions. I. Radicals generated by the interaction of sulfite, dimethyl sulfoxide, and oxygen. J Biol Chem 244:6056–6063
Mirecki RM, Teramura AH (1984) Effects of ultraviolet-B irradiance on soybean. Plant Physiol 74:475–480
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880
Ninnemann H, Maier J (1996) Indications for occurrence of nitric oxide synthases in fungi and plants and involvement in photoconidiation of Neurospora crassa. Photochem Photobiol 64:393–398
Pedroso MC, Durzan DJ (2000) Effects of different gravity environments on DNA fragmentation and cell death in Kalanchoe leaves. Ann Bot 86:983–994
Pedroso MC, Magalhaes JR, Durzan DJ (2000) A nitric oxide burst precedes apoptosis in angiosperm and gymnosperm and foliar tissues. J Exp Bot 51:1027–1036
Rao MV, Davis KR (2001) The physiology of ozone induced cell death. Planta 213:682–690
Sairam RK, Srivastava GC (2002) Changes in antioxidant activity in subcellular fraction of tolerant and susceptible wheat genotypes in response to long term salt stress. Plant Sci 162:897–904
Vega MP, Pizarro RA (2000) Oxidative stress and defence mechanisms of the freshwater cladoceran Daphnia longispina exposed to UV-B radiation. J Photochem Photobiol 54:121–125
Veljovic-Jovanovic S, Noctor G, Foyer CH (2002) Are leaf hydrogen peroxide concentrations commonly overestimated? The potential influence of artefactual interference by tissue phenolics and ascorbate. Plant Physiol Biochem 40:501–507
Wu CH, Tewari RK, Hahn EJ, Pa KY (2007) Nitric oxide elicitation induces the accumulation of secondary metabolites and antioxidant defense in adventitious roots of Echinacea purpurea. J Plant Biol 50:636–643
Zhang L, Zhao L (2008) Production of nitric oxide under ultraviolet-B irradiation is mediated by hydrogen peroxide through activation of nitric oxide synthase. J Plant Biol 51:395–400
Zhang MX, An LZ, Feng HY, Chen T, Chen K, Liu YH, Tang HG, Chang JF, Wang XL (2003) The cascade mechanism of nitric oxide as second messenger of ultraviolet-B in inhibiting mesocotyl elongations. Photochem Photobiol 77:219–225
Zhao L, Zhang F, Guo J, Yang Y, Li B, Zhang L (2004) Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed. Plant Physiol 134:849–857
Zhao MG, Tian QY, Zhang WH (2007) Nitric oxide synthase-dependent nitric oxide production is associated with salt tolerance in Arabidopsis. Plant Physiol 144:206–217
Acknowledgements
We are grateful to Dr. Nigel M. Crawford for providing the Atnoa1 seeds. This work was supported by the National Key Basic Research Special Funds of China (Grant no. 2006CB100101) and the Key Natural Science Foundation of Hebei Normal University (Grant no. L2007Z08).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Zhang, L., Zhou, S., Xuan, Y. et al. Protective Effect of Nitric Oxide against Oxidative Damage in Arabidopsis Leaves under Ultraviolet-B Irradiation. J. Plant Biol. 52, 135–140 (2009). https://doi.org/10.1007/s12374-009-9013-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12374-009-9013-2