Biologia plantarum 59:131-138, 2015 | DOI: 10.1007/s10535-014-0470-1
Glucose application protects chloroplast ultrastructure in heat-stressed cucumber leaves through modifying antioxidant enzyme activity
- 1 State Key Laboratory of Crop Biology, College of Life Sciences, Shandong Agricultural University, Tai'an, Shandong, P.R. China
To elucidate a physiological mechanism of heat stress mitigation by exogenous glucose, seedlings of Cucumis sativus cv. Jinchun No. 4 were pretreated with glucose and then exposed to normal (25/18 °C) and elevated (42/38 °C) temperatures. We investigated whether glucose can protect cucumber plantlets and chloroplast ultrastructure from heat and whether this protection is associated with antioxidant enzymes, proline, and soluble sugars. Heat inhibited plant growth, disorganized membranes of 86.33 % of chloroplasts, and elevated the content of malondialdehyde (MDA), superoxide radical (O2 .-), and hydrogen peroxide (H2O2). An optimum concentration of glucose was 30 mM as it significantly alleviated plant growth inhibition and obviously reduced the content of MDA, O2 .-, and H2O2 under the heat stress. The pretreatment with 30 mM glucose mitigated heat-induced damage of chloroplast ultrastructure and changes in leaf morphology more than 30 mM mannitol suggesting that glucose did not act only as osmolyte. Moreover, the glucose pretreatment increased activities of some antioxidant enzymes and enhanced the content of proline and soluble sugars under the heat stress, as well as the transcriptions of Cu/Zn-superoxide dismutase, Mn-superoxide dismutase, catalase, and glutathione reductase genes. We conclude that the pretreatment with 30 mM glucose protected chloroplast ultrastructure and enhanced heat tolerance of the seedlings by the increased activites of antioxidants and the content of proline and soluble sugars, and repressed accumulation of reactive oxygen species.
Keywords: catalase; Cucumis sativus; glutathione reductase; H2O2; invertase; malondialdehyde; proline; soluble sugars; superoxide dismutase
Subjects: glucose; chloroplasts; heat stress; temperature - high; malondialdehyde; hydrogen peroxide; superoxide anion; catalase; superoxide dismutase; mannitol; ascorbate peroxidase; glutathione reductase; proline; soluble sugars; invertase; cucumber
Received: March 7, 2014; Revised: June 13, 2014; Accepted: June 16, 2014; Published: January 1, 2015 Show citation
| ACS | AIP | APA | ASA | Harvard | Chicago | IEEE | ISO690 | MLA | NLM | Turabian | Vancouver |
Huang, Y.-W., Zhou, Z.-Q., Yang, H.-X., Wei, C.-X., Wan, Y.-Y., Wang, X.-J., & Bai, J.-G. (2015). Glucose application protects chloroplast ultrastructure in heat-stressed cucumber leaves through modifying antioxidant enzyme activity. Biologia plantarum, 59(1), 131-138. doi: 10.1007/s10535-014-0470-1
References
- Almeselmani, M., Deshmukh, P.S., Sairam, R.K., Kushwaha, S.R., Singh, T.P.: Protective role of antioxidant enzymes under high temperature stress. - Plant Sci. 171: 382-388, 2006.
Go to original source...
- Baninasab, B., Ghobadi, C.: Influence of paclobutrazol and application methods on high-temperature stress injury in cucumber seedlings. - J. Plant Growth Regul. 30: 213-219, 2011.
- Bates, L.S., Waldren, R.P., Teare, I.D.: Rapid determination of free proline for water-stress studies. - Plant Soil 39: 205-207, 1973.
- Batta, S.K., Singh, R.: Sucrose metabolism in sugarcane grown under varying climatic conditions: synthesis and storage of sucrose in relation to the activities of sucrose synthase, sucrose phophate synthase and invertase. - Phytochemistry 25: 2431-2437, 1986.
- Bernt, E., Bergmeyer, H.U.: Inorganic peroxides. - In: Bergmeyer H.U. (ed.): Methods of Enzymatic Analysis. Pp. 2246-2248. Academic Press, New York 1974.
- 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. 72: 248-254, 1976.
- Dai, A.H., Nie, Y.X., Yu, B., Li, Q., Lu, L.Y., Bai, J.G.: Cinnamic acid pretreatment enhances heat tolerance of cucumber leaves through modulating antioxidant enzyme activity. - Environ. exp. Bot. 79: 1-10, 2012.
- Dhindsa, R.S., Plumb-Dhindsa, P., 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. 32: 93-101, 1981.
- Doulis, A.G., Debian, N., Kingston-Smith, A.H., Foyer, C.H.: Differential localization of antioxidants in maize leaves. - Plant Physiol. 114: 1031-1037, 1997.
- Elstner, E.F., Heupel, A.: Inhibition of nitrite formation from hydroxylammoniumchloride: a simple assay for superoxide dismutase. - Anal. Biochem. 70: 616-620, 1976.
- Foyer, C.H., Halliwell, B.: The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. - Planta 133: 21-25, 1976.
- Gao, Y., Guo, Y.K., Lin, S.H., Fang, Y.Y., Bai, J.G.: Hydrogen peroxide pretreatment alters the activity of antioxidant enzymes and protects chloroplast ultrastructure in heatstressed cucumber leaves. - Sci. Hort. 126: 20-26, 2010.
- Guri, A.: Variation in glutathione and ascorbic acid content among selected cultivars of Phaseolus vulgaris prior to and after exposure to ozone. - Can. J. Plant Sci. 63: 733-737, 1983.
- Helliot, B., Swennen, R., Poumay, Y., Frison, E., Lepoivre, P., Panis, B.: Ultrastructural changes associated with cryopreservation of banana (Musa spp.) highly proliferating meristems. - Plant Cell Rep. 21: 690-698, 2003.
- Hirabayashi, J.: On the origin of elementary hexoses. - Quart. Rev. Biol. 71: 365-380, 1996.
- Hoque, M.A., Banu, M.N., Okuma, E., Amako, K., Nakamura, Y., Shimoishi, Y., Murata, Y.: Exogenous proline and glycinebetaine increase NaCl-induced ascorbate-glutathione cycle enzyme activities, and proline improves salt tolerance more than glycinebetaine in tobacco Bright Yellow-2 suspension-cultured cells. - J. Plant Physiol. 164: 1457-1468, 2007.
- Hu, M., Shi, Z., Zhang, Z., Zhang, Y., Li, H.: Effects of exogenous glucose on seed germination and antioxidant capacity in wheat seedlings under salt stress. - Plant Growth Regul. 68: 177-188, 2012.
- Hu, M.Y., Li, H., Zhang, Y.J., Liu, Q.: Photosynthesis and related physiological characteristics affected by exogenous glucose in wheat seedlings under water stress. - Acta agron. sin. 35: 724-732, 2009.
- Huang, Y.W., Nie, Y.X., Wan, Y.Y., Chen, S.Y., Sun, Y., Wang, X.J., Bai, J.G.: Exogenous glucose regulates activities of antioxidant enzyme, soluble acid invertase and neutral invertase and alleviates dehydration stress of cucumber seedlings. - Sci. Hort. 162: 20-30, 2013.
- Hwang, S.Y., Lin, H.W., Chern, R.H., Lo, H.F., Li, L.: Reduced susceptibility to waterlogging together with high-light stress is related to increases in superoxide dismutase and catalase activities in sweet potato. - Plant Growth Regul. 27: 167-172, 1999.
- Jiang, W., Ding, M., Duan, Q., Zhou, Q., Huang, D.: Exogenous glucose preserves the quality of watermelon (Citrullus lanatus) plug seedlings for low-temperature storage. - Sci. Hort. 148: 23-29, 2012.
- Kumar, S., Singh, R., Nayyar, H.: α-Tocopherol application modulates the response of wheat (Triticum aestivum L.) seedlings to elevated temperatures by mitigation of stress injury and enhancement of antioxidants. - J. Plant Growth Regul. 32: 307-314, 2013.
- Lee, D.H., Lee, C.B.: Chilling stress-induced changes of antioxidant enzymes in the leaves of cucumber: in gel enzyme activity assays. - Plant Sci. 159: 75-85, 2000.
- Li, D.M., Guo, Y.K., Li, Q., Zhang, J., Wang, X.J., Bai, J.G.: The pretreatment of cucumber with methyl jasmonate regulates antioxidant enzyme activities and protects chloroplast and mitochondrial ultrastructure in chillingstressed leaves. - Sci. Hort. 143: 135-143, 2012.
- Li, Q., Yu, B., Gao, Y., Dai, A.H., Bai, J.G.: Cinnamic acid pretreatment mitigates chilling stress of cucumber leaves through altering antioxidant enzyme activity. - J. Plant Physiol. 168: 927-934, 2011.
- Liu, Z.J., Guo, Y.K., Bai, J.G.: Exogenous hydrogen peroxide changes antioxidant enzyme activity and protects ultrastructure in leaves of two cucumber ecotypes under osmotic stress. - J. Plant Growth Regual. 29: 171-183, 2010.
- Luo, Y., Gao, M., Wang, W., Zou, C.J.: Application of trehalose ameliorates heat stress and promotes recovery of winter wheat seedlings. - Biol Plant. 58: 395-398, 2014.
- Mishra, Y., Bhargava, P., Rai, L.C.: Differential induction of enzymes and antioxidants of the antioxidative defense system in Anabaena doliolum exposed to heat stress. - J. therm. Biol. 30: 524-531, 2005.
- Molassiotis, A., Sotiropoulos, T., Tanou, G., Diamantidis, G., Therios, I.: Boron-induced oxidative damage and antioxidant and nucleolytic responses in shoot tips culture of the apple rootstock EM9 (Malus domestica Borkh). - Environ. exp. Bot. 56: 54-62, 2006.
- Ozaki, K., Uchida, A., Takabe, T., Shinagawa, F., Tanaka, Y., Takabe, T., Hayashi, T., Hattori, T., Rai, A.K., Takabe, T.: Enrichment of sugar content in melon fruits by hydrogen peroxide treatment. - J. Plant Physiol. 166: 569-578, 2009.
- Pereira, G.J.G., Molina, S.M.G., Lea, P.J., Azevedo, R.A.: Activity of antioxidant enzymes in response to cadmium in Crotalaria juncea. - Plant Soil 239: 123-132, 2002.
- Santarius, K.A.: The protective effect of sugars on chloroplast membranes during temperature and water stress and its relationship to frost, desiccation and heat resistance. - Planta 113: 105-114, 1973.
- Seckin, B., Sekmen, A.H., Turkan, I.: An enhancing effect of exogenous mannitol on the antioxidant enzyme activities in roots of wheat under salt stress. - J. Plant Growth Regul. 28: 12-20, 2009.
- Shigeoka, S., Ishikawa, T., Tamoi, M., Miyagawa, Y., Takeda, T., Yabuta, Y., Yoshimura, K.: Regulation and function of ascorbate peroxidase isoenzymes. - J. exp. Bot. 53: 1305-1319, 2002.
- Stoyanova-Koleva, D., Stefanova, M., Čellárová, E., Kapchina-Toteva V.: Chloroplast ultrastructure of Hypericum perforatum plants regenerated in vitro after cryopreservation. - Biol. Plant. 57: 793-796, 2013.
- Sun, W.J., Nie, Y.X., Gao, Y., Dai, A.H., Bai, J.G.: Exogenous cinnamic acid regulates antioxidant enzyme activity and reduces lipid peroxidation in drought-stressed cucumber leaves. - Acta Physiol. Plant. 34: 641-655, 2012.
- Wahid, A., Gelani, S., Ashraf, M., Foolad, M.R.: Heat tolerance in plants: an overview. - Environ. exp. Bot. 61: 199-223, 2007.
- Xu, P.L., Guo, Y.K., Bai, J.G., Shang, L., Wang, X.J.: Effects of long-term chilling on ultrastructure and antioxidant activity in leaves of two cucumber cultivars under low light. - Physiol. Plant. 132: 467-478, 2008.
- Xu, S., Li, J.L., Zhang, X.Q., Wei, H., Cui, L.J.: Effects of heat acclimation pretreatment on changes of membrane lipid peroxidation, antioxidant metabolites, and ultrastructure of chloroplasts in two cool-season turfgrass species under heat stress. - Environ. exp. Bot. 56: 274-285, 2006.
- Yemm, E.W., Willis, A.J.: The estimation of carbohydrates in plant extracts by anthrone. - Biochem. J. 57: 508-514, 1954.
- Zhang, M., Duan, L., Tian, X., He, Z., Li, J., Wang, B., Li, Z.: Uniconazole-induced tolerance of soybean to water deficit stress in relation to changes in photosynthesis, hormones and antioxidant system. - J. Plant Physiol. 164: 709-717, 2007.
- Zhang, Y.P., He, J., Yang, S.J., Chen, Y.Y.: Exogenous 24-epibrassinolide ameliorates high temperature-induced inhibition of growth and photosynthesis in Cucumis melo. - Biol. Plant. 58: 311-318, 2014.
- Zhifang, G., Loescher, W.H.: Expression of a celery mannose 6-phosphate reductase in Arabidopsis thaliana enhances salt tolerance and induces biosynthesis of both mannitol and a glucosyl-mannitol dimer. - Plant Cell Environ. 26: 275-283, 2003.
- Zhu, Z., Wei, G., Li, J., Qian, Q., Yu, J.: Silicon alleviates salt stress and increases antioxidant enzymes activity in leaves of salt-stressed cucumber (Cucumis sativus L.). - Plant Sci. 167: 527-533, 2004.