Abstract
SPINDLY (SPY) gene encodes a putative O-linked N-acetyl-glucosamine transferase, and yeast two-hybrid assay identified GIGANTEA (GI) as a SPY-interacting partner in Arabidopsis. GIGANTEA gene was previously shown to be involved in the regulation of oxidative stress response; however, it is unclear whether SPY gene is also involved in oxidative stress response. Here we showed that SPY plays a role in the regulation of the oxidative stress response. The spy-1 mutant was more tolerant to paraquat (PQ)-or hydrogen peroxide (H2O2)-mediated oxidative stress than wild-type plants. Analyses of endogenous H2O2 and superoxide anion radicals as well as lipid peroxidation revealed that enhanced tolerance of the spy-1 mutant to PQ-stress was not due to defects in the PQ uptake or the PQ sequestration from its site of action but rather the spy-1 mutation alleviated oxidative damage of plant cells upon PQ stress. Higher constitutive activities of superoxide dismutase (SOD) and ascorbate peroxidase (APX) in spy-1 are more likely to be due to activation of both CSD2 gene encoding chloroplast Cu/Zn SOD and APX1 gene. Taken together, these results suggest that enhanced tolerance of the spy-1 mutant to oxidative stress is associated, at least in part, with constitutive activation of CSD2 and APX1.
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Abbreviations
- APX:
-
ascorbate peroxidase
- CAT:
-
catalase
- MDA:
-
malondialdehyde
- MS:
-
Murashige and Skoog nutrient medium
- PQ:
-
paraquat
- ROS:
-
reactive oxygen species
- RT-PCR:
-
reverse transcription PCR
- SOD:
-
superoxide dismutase
References
Dirk, I. and Marc, V.M., Oxidative Stress in Plants, Curr. Opin. Biotechnol., 1995, vol. 6, pp. 153–158.
Mittler, R., Oxidative Stress, Antioxidants and Stress Tolerance, Trends Plant Sci., 2002, vol. 7, pp. 405–410.
Eva, V., Dirk, I., and Frank, V.B., Signal Transduction during Oxidative Stress, J. Exp. Bot., 2002, vol. 53, pp. 1227–1236.
Scandalios, J.G., Oxidative Stress Responses — What Have Genome-Scale Studies Taught Us, Gen. Biol., 2002, vol. 3, pp. 10 191–10 196.
Desikan, R., AH-Mackerness, S., Hancock, J.T., and Neill, S.J., Regulation of the Arabidopsis Transcriptome by Oxidative Stress, Plant Physiol., 2001, vol. 127, pp. 159–172.
Alscher, R.G., Erturk, N., and Heath, L.S., Role of Superoxide Dismutases (SODs) in Controlling Oxidative Stress in Plants, J. Exp. Bot., 2002, vol. 53, pp. 1331–1341.
Shigeoka, S., Ishikawa, T., Tamoi, M., Miyagawa, Y., Takeda, T., Yabuta, Y., and Yoshimura, K., Regulation and Function of Ascorbate Peroxidase Isoenzymes, J. Exp. Bot., 2002, vol. 53, pp. 1305–1319.
Mittler, R., Vanderauwera, S., Gollery, M., and Breusegem, F.V., Reactive Oxygen Gene Network of Plants, Trends Plant Sci., 2004, vol. 9, pp. 490–498.
Thornton, T., Swain, S.M., and Olszewski, N., Gibberellin Signal Transduction Presents: The SPY Who O-GlcNAc’d Me, Trends Plant Sci., 1999, vol. 4, pp. 424–428.
Tseng, T.S., Salomé, P.A., McClung, C.R., and Olszewski, N.E., SPINDLY and GIGANTEA Interact and Act in Arabidopsis thaliana Pathways Involved in Light Responses, Flowering, and Rhythms in Cotyledon Movements, Plant Cell, 2004, vol. 16, pp. 1550–1563.
Huq, E., Tepperman, J.M., and Quail, P.H., GIGANTEA Is a Nuclear Protein Involved in Phytochrome Signaling in Arabidopsis, Proc. Natl. Acad. Sci. USA, 2000, vol. 97, pp. 9789–9794.
Koornneef, M., Hanhart, C.J., and van der Veen, J.H., A Genetic and Physiological Analysis of Late Flowering Mutants in Arabidopsis thaliana, Mol. Gen. Genet., 1991, vol. 229, pp. 57–66.
Eimert, K., Wang, S.M., Lue, W.L., and Chen, J., Monogenic Recessive Mutations Causing Both Late Floral Initiation and Excess Starch Accumulation in Arabidopsis, Plant Cell, 1995, vol. 7, pp. 1703–1712.
Fowler, S., Lee, K., Onouchi, H., Samach, A., Richardson, K., Morris, B., Coupland, G., and Putterill, J., GIGANTEA: A Circadian Clock-Controlled Gene That Regulates Photoperiodic Flowering in Arabidopsis and Encodes a Protein with Several Possible Membrane-Spanning Domains, EMBO J., 1999, vol. 18, pp. 4679–4688.
Park, D.H., Somers, D.E., Kim, Y.S., Choy, Y.H., Lim, H.K., Soh, M.S., Kim, H.J., Kay, S.A., and Nam, H.G., Control of Circadian Rhythms and Photoperiodic Flowering by the Arabidopsis GIGANTEA Gene, Science, 1999, vol. 285, pp. 1579–1582.
Kurepa, J., Smalle, J., van Montagu, M., and Inez, D., Oxidative Stress Tolerance and Longevity in Arabidopsis: The Late-Flowering Mutant gigantea Is Tolerant to Paraquat, Plant J., 1998, vol. 14, pp. 759–764.
Jacobsen, S.E. and Olszewski, N.E., Mutations at the SPINDLY Locus of Arabidopsis Alter Gibberellin Signal Transduction, Plant Cell, 1993, vol. 5, pp. 887–896.
Murashige, T. and Skoog, F., A Revised Medium for Rapid Growth and Bioassays with Tobacco Tissue Culture, Physiol. Plant., 1962, vol. 15, pp. 473–497.
Dhindsa, R.S., Dhindsa, P., and Thorpe, T.A., Leaf Senescence Correlated with Increased Levels of Membrane Permeability and Lipid Peroxidation and Decreased Levels of Superoxide Dismutase and Catalase, J. Exp. Bot., 1987, vol. 32, pp. 93–101.
Brennan, T. and Frenkel, C., Involvement of Hydrogen Peroxide in Regulation of Senescence in Pear, Plant Physiol., 1977, vol. 59, pp. 411–416.
Shah, K., Kumar, R.G., Verma, S., and Dubey, R.S., Effect of Cadmium on Lipid Peroxidation, Superoxide Anion Generation and Activities of Antioxidant Enzymes in Growing Rice Seedlings, Plant Sci., 2001, vol. 161, pp. 1135–1144.
Bradford, M.M., A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding, Anal. Biochem., 1976, vol. 72, pp. 248–254.
Beauchamp, C. and Fridovich, I., Superoxide Dismutase: Improved Assay and an Assay Applicable to PAGE, Anal. Biochem., 1971, vol. 44, pp. 276–287.
Cakmak, I. and Marschner, H., Magnesium Deficiency and High Light Intensity Enhance Activities of Superoxide Dismutase, Ascrobate Peroxidase, and Glutathione Reductase in Bean Leaves, Plant Physiol., 1992, vol. 98, pp. 1222–1227.
Nakano, Y. and Asada, K., Hydrogen Peroxide Is Scavenged by Ascorbate-Specific Peroxidase in Spinach Chloroplasts, Plant Cell Physiol., 1981, vol. 22, pp. 867–880.
Rao, M.V., Paliyath, G., Ormrod, D.P., Murr, D.P., and Watkins, C.B., Influence of Salicyclic Acid on H2O2 Production, Oxidative Stress, and H2O2-Metabolizing Enzymes (Salicyclic Acid-Mediated Oxidative Damage Requires H2O2), Plant Physiol., 1997, vol. 115, pp. 137–149.
Rao, M.V. and Davis, R.D., Ozone-Induced Cell Death Occurs via Two Distinct Mechanisms in Arabidopsis: The Role of Salicylic Acid, Plant J., 1999, vol. 17, pp. 603–614.
Van Camp, W., Bowler, C., Villarroel, R., Tsang, E.W., van Montagu, M., and Inze, D., Characterization of Iron Superoxide Dismutase cDNAs from Plants Obtained by Genetic Complementation in Escherichia coli, Proc. Natl. Acad. Sci. USA, 1990, vol. 87, pp. 9903–9907.
Davletova, S., Rizhsky, L., Liang, H., Shengqiang, Z., Oliver, D.J., Coutu, J., Shulaev, V., Schlauch, K., and Mittler, R., Cytosolic Ascorbate Peroxidase 1 Is a Central Component of the Reactive Oxygen Gene Network of Arabidopsis, Plant Cell, 2005, vol. 17, pp. 268–281.
Hart, J.J. and Ditomaso, J.M., Sequestration and Oxygen Radical Detoxification as Mechanisms of Paraquat Tolerance, Weed Sci., 1994, vol. 42, pp. 277–284.
Purba, E., Preston, C., and Powles, S.B., The Mechanism of Tolerance to Paraquat Is Strongly Temperature Dependent in Resistant Hordeum leporinum Link and H. glaucum Steud., Planta, 1995, vol. 196, pp. 464–468.
Kliebenstein, D.J., Monde, R., and Last, R.L., Superoxide Dismutase in Arabidopsis: An Eclectic Enzyme Family with Disparate Regulation and Protein Localization, Plant Physiol., 1998, vol. 118, pp. 637–650.
Mittler, R. and Zilinskas, B.A., Molecular Cloning and Characterization of a Gene Encoding Pea Cytosolic Ascorbate Peroxidase, J. Biol. Chem., 1992, vol. 267, pp. 21802–21807.
Mittler, R. and Zilinskas, B.A., Regulation of Pea Cytosolic Ascorbate Peroxidase and Other Antioxidant Enzymes during the Progression of Drought Stress and Following Recovery from Drought, Plant J., 1994, vol. 5, pp. 397–405.
Storozhenko, S., Pauw, P.D., Montagu, M.V., Inze, D., and Kushnir, S., The Heat-Shock Element Is a Functional Component of the Arabidopsis APX1 Gene Promoter, Plant Physiol., 1998, vol. 118, pp. 1005–1014.
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Published in Russian in Fiziologiya Rastenii, 2006, Vol. 53, No. 4, pp. 604–611.
The text was submitted by the authors in English.
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Cao, S.Q., Ye, M., Huang, Q. et al. A role for SPINDLY gene in the regulation of oxidative stress response in Arabidopsis . Russ J Plant Physiol 53, 541–547 (2006). https://doi.org/10.1134/S1021443706040170
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DOI: https://doi.org/10.1134/S1021443706040170