Effect of Endophytic Fungus, Piriformospora Indica, on Growth and Activity of Antioxidant Enzymes of Rice (Oryza Sativa L.) Under Salinity Stress

Document Type: Original Article

Authors

1 Department of Biology, Science and Research branch, Islamic Azad University, Tehran, Iran

2 School of Biology and Center of Excellence in Phylogeny of Living Organisms, College of Sciences, University of Tehran, Tehran, Iran

3 Department of Plant protection,University of Agricultural and Natural Resources, Sari, Iran

Abstract

Abiotic stresses including salinity are the major limiting factors of growth and crop production worldwide. Microbial endophytes as the most important soil microorganisms, by modifying plants at genetical, physiological and ecological levels increase their yield per area unit and provide the possibility of crop production in saline and arid soils or climates with biotic and abiotic stresses. The endophytic fungus, Piriformospora indica has a pronounced growth-promoting activity and also increases plant resistance to environmental stresses including salinity, drought and plant pathogens. We compared some growth parameters, physiological and biochemical responses such as total soluble proteins, Relative Water Content(RWC), lipid peroxidation, free proline content, and enzyme antioxidants(catalase, glutathione reductase, superoxide dismutase, ascorbate peroxidase) activity of p.indica–inoculated and non-p.indica-inoculated(controls) rice(Oryza sativa) under salt stress. The obtained results show that P. indica increase the biomass of aerial parts and root, total soluble proteins, Relative Water Content (RWC), free proline content and enzyme antioxidants activity of inoculated rice in compared to the controls. In contrast, Lipid peroxidation decreased in inoculated rice in compared to the controls. The obtained results of this research indicated that the effective role of this fungus to improve growth of rice under salt stress conditions

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Abtahi, A. (1992). The tolorance limitation of plant against to salinity. Technical journal, 16, Pedology group, Agricultural faculty, Shiraz University.
Aebi, H. (1974). Catalases, in: H.U. Bergmeyer (Ed.), Methods of enzymatic analysis. Academic Press, NY, 2: 673-684.
Alguacil, M. M., Hernandez, J. A., Caravaca, F., Portillo, B. &Roldan, A. (2003). Antioxidant enzyme activities in shoots from three mycorrhizal shrub species afforested in a degraded semi-arid soil. Physiol Plant, 118: 562–570.
Badawi, GH., Kawano, N., Yamauchi, Y., Shimada, E., Sasaki, R., Kubo, A. and Tanaka, K. (2004).
Over-expression of ascorbate peroxidase in tobacco chloroplasts enhances the tolerance to salt stress and water deficit. Physiologia Plantarum, 121: 231–238.
Bates, LS., Waldern, RP. And Teare, ID. (1973). Rapid determination of free proline for water stress studies. Plant Soil, 39: 205-207.
Blilou, I., Bueno, P., Ocampo, J. A. and Garcia-Garrido, J. (2000).Induction of catalase and ascorbate peroxidase activities in tobacco roots inoculated with the arbuscular mycorrhizal Glomus mosseae. Mycol Res, 104: 722–725.
Bor, M., Ozdemir, F. and Turkan, I. (2003). The effect of salt stress on lipid peroxidation and antioxidants in leaves of sugar beet Beta vulgaris L. and wild beet Beta maritima L. Plant Science, 164: 77–84.
Borsani, O., Valpuesta,V and M.A.(2001). Botella, Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant Physiol, 126: 1024–1030
Bradford, M. M. (1976). A rapid and sensitive method for the quantification of microgram quantities of protein utilization the principle of protein-dye binding. Anals of Biochemistry, 72: 348-354.
Dat, J., Vandenabeele, S., Vranova, E., Van Montagu, M., Inze, D and Van Breusegem, F. (2000). Dual action of the active oxygen species during plant stress responses. Cell. Mol Life Sci, 57: 779–795.
De Gara, L., De Pinto, M. C. & Tommasi, F. (2003). The antioxidant systems vis-a`-vis reactive oxygen species during plant–pathogen interaction. Plant Physiol Biochem, 41: 863–870.
Druege U, Baltruschat H, Franken P. (2007). Piriformospora indica promotes adventitious root formation in cuttings. Scientia Horticulturae,112: 422–426.
Heath, RL. and Packer, L. (1968). Photoperoxidarion in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Archive of Biochemistry and Biophysics, 125: 189-198.
Hernandez, JA., Olmos, E., Corpas, FJ., Sevilla, F. and Del Rio, LA. (1995). Salt-induced oxidative stress in chloroplasts of pea-plants. Plant Science, 105: 151–167.
Hernandez, JA., Jimenez, A., Mullineaux, PM. and Sevilla, F. (2000). Tolerance of pea (Pisum sativum L.) to long-term salt stress is associated with induction of antioxidant defenses. Plant, Cell & Environment, 23: 853–862.
Hua, X. J., Van De Cotte, B., Montagu, M. V., and Verbruggen, N. (1997). Developmental regulation of pyroline-5-carboxylate reductase gene expression in Arabidopsis. Plant Physiology, 114: 1215-1224.
Imlay, JA. (2003). Pathways of oxidative damage. Annu Rev Microbiol, 57: 395–418.
Shannon, MC. (1997). Adaptation of plants to salinity. Advances in Agronomy, 60: 75–120.
Jebara, C., Jebara, M., Limam, F. and Elarbi Aouani, M. (2005). Changes in ascorbate peroxidase, catalase, guaiacol peroxidase and superoxide dismutase activities in common bean (Phaseolus vulgaris) nodules under salt stress. Journal of Plant Physiology, 162: 929-936.
Lee D. H., Kim Y. S. and Lee C. B. (2001). The inductive responses of the antioxidant enzymes by salt stress in rice (Oryza sativa L.). J. Plant Physiol, 158: 737–745.
Lutts, S., Majerus, V. and Kinet, J.M. (1999). NaCl effects on prolin metabolism in rice seedlings. PHysiol. Plant, 105: 450-458.
Maslenkova, L. T., Miteva, T. S. and Popoval, P. (1999). Changes in the polypeptide patterns of barley seedling exposed to jasmonic acid and salinity. Plant Physiology, 98: 700-707.
Mittler, R. (2002). Oxidative stress, antioxidants and stress tolerance.Trends Plant Sci, 7: 405–410.
Nagamiya, K., Motohashi, T., Nakao, K., Prodhan, SH., Hattori, E., Hirose, S.,Ozawa, K., Ohkawa, Y., Takabe, Tand Takabe, T et al. (2007). Enhancement of salt tolerance in transgenic rice expressing an Escherichia coli catalase gene, kat E. Plant Biotechnology Reports, 1: 49–55.
Ozkur, O., Ozdemir, F., Bor, M. and Turkan I. (2009). Physiochemical and antioxidant responses of the perennial xerophyte Capparis ovata Desf to drought. Environmental and Experimental Botany, 66: 487-492.
Peškan-Berghöfer T., Shahollari B., Giong P.H., Hehl S., Markert C., Blanke V., Kost G., Varma, A and Oelmüller, R. (2004). Association of Piriformospora indica with Arabidopsis thaliana roots represents a novel system to study beneficial plant– microbe interactions and involves early plant protein modifications in the endoplasmic reticulum and at the plasma membrane. Physiologia Plantarum, 122: 465–477.
Porcel, R., Barea, J. M. & Ruiz-Lozano, J. M. (2003). Antioxidant activities in mycorrhizal soybean plants under drought stress and their possible relationship to the process of nodule senescence. New Phytol, 157: 135–143.
Rao, MV., Paliyath, G. and Ormrod, DP. (1996). Ultraviolet-B- and ozone-induced biochemical changes in antioxidant enzymes of Arabidopsis thaliana. Plant Physiology, 110: 25-136.
Requena, N., Perez-Solis, E., Azcon-Aguilar, C., Jeffries, P. & Barea,J. M. (2001). Management of indigenous plant–microbe symbioses aids restoration of decertified ecosystems. Appl Environ Microbiol,
67: 495–498.
Sekmen, AH., Turkan, I. and Takio, S. (2007). Differential responses of antioxidative enzymes and lipid peroxidation to salt stress in salt-tolerant Plantago maritima and salt-sensitive Plantago media. Physiologia Plantarum, 131: 399–411.
Serfling, A., Wirsel, S. G. R., Lind, V. & Deising, H. B. (2007). Performance of the biocontrol fungus Piriformospora indica on wheat under greenhouse and field conditions. Phytopathology, 97: 523–531.
Sherameti, I., Shahollari, B., Venus, Y., Altschmied, L., Varma, A. & Oelmuller, R. (2005). The endophytic fungus Piriformospora indica stimulates the expression of nitrate reductase and the
Sudhakar, P. R., Reddy, M. P. and Veeranjaneyulu, K. (1993). Effect of salt stress on the enzymes of proline synthesis and oxidation in green seedling. Journal of Plant Physiology, 141: 621-623.
Toro, M., Azcon, R. & Barea, J. M. (1998). The use of isotopic dilution techniques to evaluate the interactive effects of Rhizobium genotype, mycorrhizal fungi, phosphate-solubilizing rhizobacterias and rock phosphate on nitrogen and phosphorus acquisition by Medicago sativa. New Phytol, 138: 265–273.
Ushimaru, T., Nakagawa. T., Fujioka. Y., Daicho, K., Naito, M., Yamauchi, Y.,Nonaka, H., Amako, K., Yamawaki, K and Murata, N. (2006). Transgenic Arabidopsis plants expressing the rice dehydroascorbate reductase gene are resistant to salt stress. Journal of Plant Physiology, 163: 1179–1184.
Vanacker, H., Harbinson, J., Ruisch, J., Carver, T. L. W. & Foyer, C. H.(1998). Antioxidant defenses of the apoplast. Protoplasma, 205: 129–140.
Verma, S., Varma, A., Rexer, K. H., Kost, G., Sarbhoy, A., Bisen, P., Butehorn, B. and Franken, ph. (1998). Piriformospora indica gen.E sp. Nov., A new root-colonizing Fungus. Mycologia, 95: 896-903.
Verma, S., Varma, A., Rexer, K. H., Kost,G., Sarbhoy, A., Bisen, P., Butehorn, B.(1990). Interactions between water-stress and different mycorrhizal inoculate on plant growth and mycorrhizal development in maize and sorghum. Plant Soil, 121:179-186
Vierheilig, H., Coughlan, A. P., Wyss, U. and Piche, Y. (1998). Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Applied and Environmental Microbiology, 64: 5004–5007.
Waller, F., Achatz, B. and Baltruschat, H. (2005). The endophytic fungus Piriformospora indica reprograms barley to salt- stress tolerance, disease resistance and higher yield. PNAS, 102: 13386-13391
Wu, G. S., Shortt, B. J., Lawrence, E. B., Leon, J., Fitzsimmons, K. C.,Levine, E. B., Raskin, I. & Shah, D. M. (1997). Activation of host defense mechanisms by elevated production of H2O2 in transgenic plants. Plant Physiol, 115: 427–435.
Yang, YL., Guo, JK., Zhang, F., Zhaob, LQ. and Zhang, LX. (2004). NaCl induced changes of the H+-ATPase in root plasma membrane of two wheat cultivars. Plant Science, 166: 913–918.