Russian Journal of Plant Physiology

, Volume 65, Issue 6, pp 898–907 | Cite as

Piriformospora indica Alleviates Salinity by Boosting Redox Poise and Antioxidative Potential of Tomato

  • A. Ghorbani
  • S. M. RazaviEmail author
  • V. O. G. Omran
  • H. Pirdashti
Research Papers


More than 20% of irrigated land has been influenced by salt stress, decreasing crop production. In this research, we investigated the effect of different levels of salinity (0, 50, 100 and 150 mM NaCl) and the efficiency of Piriformospora indica on growth, biochemical traits, antioxidative defense system in tomato (Solanum lycopersicum L.). NaCl stress reduced chlorophyll content, height and biomass of plants. Higher level of salinity (150 mM) declined the plant height by 22.65%, total dry weight by 56.44% and total chlorophyll by 44.34%, however, P. indica inoculation raised plant height by 43.47%, dry weight by 69.23% and total chlorophyll content by 48.09%. Salinity stress increased H2O2, malondialdehyde (MDA), superoxide anion and 1,1-diphenyl-2-picrylhydrazyl (DPPH) level in leaves and roots tomato seedlings. However, P. indica inoculation reduced H2O2, MDA and superoxide anion and enhanced DPPH compared to non-inoculated plants at all NaCl levels. The total phenol and flavonoids increased with NaCl treatment. On the other hand, the total phenolic and flavonoid increased more in P. indica inoculated plants compared to non-inoculated ones. Moreover, inoculation of P. indica implicated noteworthy improvement of superoxide dismutase (SOD), ascorbate peroxidase (APX), catalase (CAT), dehydroascorbate reductase (DHAR), monodehydroascorbate reductase (MDHAR), and glutathione reductase (GR) activity in tomato upon salinity. Notably, colonization with P. indica significantly improved the content of reduced ascorbic acid (AsA), glutathione (GSH) and redox ratio in the tomato plants under salinity resulting in reduced redox state. Our findings confirmed that salinity had negative effect on tomato seedling; however, P. indica inoculation increased tolerance to salinity by improving the content of phenolic compounds, non-enzymatic antioxidants, and increasing the activity of antioxidant enzymes.


Solanum lycopersicum Piriformospora indica antioxidative enzymes endophyte fungi NaCl stress non-enzymatic antioxidants tomato plants 



ascorbate peroxidase


ascorbic acid






dehydroascorbate reductase




glutathione reductase


reduced glutathione


oxidized glutathione




monodehydroascorbate reductase


guaiacol peroxidase


reactive oxygen species


superoxide dismutase


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  1. 1.
    Porcel, R., Aroca, R., and Ruiz-Lozano, J.M., Salinity stress alleviation using arbuscular mycorrhizal fungi. A review, Agron. Sustain. Dev., 2012, vol. 32, pp. 181–200.CrossRefGoogle Scholar
  2. 2.
    Ahmad, P., Growth and antioxidant responses in mustard (Brassica juncea L.) plants subjected to combined effect of gibberellic acid and salinity, Arch. Agron. Soil Sci., 2010, vol. 56, pp. 575–588.CrossRefGoogle Scholar
  3. 3.
    Ahmad, P., Jaleel, C.A., Salem, M.A., Nabi, G., and Sharma, S., Roles of enzymatic and nonenzymatic antioxidants in plants during abiotic stress, Crit. Rev. Biotechnol., 2010, vol. 30, pp. 161–175.CrossRefPubMedGoogle Scholar
  4. 4.
    Rasool, S., Ahmad, A., Siddiqi, T.O., and Ahmad, P., Changes in growth, lipid peroxidation and some key antioxidant enzymes in chickpea genotypes under salt stress, Acta Physiol. Plant., 2013, vol. 35, pp. 1039–1050.CrossRefGoogle Scholar
  5. 5.
    Kumar, M., Yadav, V., Tuteja, N., and Johri, A.K., Antioxidant enzyme activities in maize plants colonized with Piriformospora indica, Microbiology, 2009, vol. 155, pp. 780–790.CrossRefPubMedGoogle Scholar
  6. 6.
    Jogawat, A., Saha, S., Bakshi, M., Dayaman, V., Kumar, M., Dua, M., Varma, A., Oelmüller, R., Tuteja, N., and Johri, A.K., Piriformospora indica rescues growth diminution of rice seedlings during high salt stress, Plant Signal. Behav., 2013, vol. 8. doi 10.4161/psb.26891Google Scholar
  7. 7.
    Waller, F., Achatz, B., Baltruschat, H., Fodor, J., Becker, K., Fischer, M., Heier, T., Hückelhoven, R., Neumann, C., von Wettstein, D., Franken, P., and Kogel, K.-H., The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield, Proc. Natl. Acad. Sci. USA, 2005, vol. 102, pp. 13 386–13 391.CrossRefGoogle Scholar
  8. 8.
    Bagheri, A.A., Saadatmand, S., Niknam, V., Nejadsatari, T., and Babaeizad, V., Effect of endophytic fungus, Piriformospora indica, on growth and activity of antioxidant enzymes of rice (Oryza sativa L.) under salinity stress, Int. J. Adv. Biol. Biomed. Res., 2013, vol. 1, pp. 1337–1350.Google Scholar
  9. 9.
    He, Z., He, C., Zhang, Z., Zou, Z., and Wang, H., Changes of antioxidative enzymes and cell membrane osmosis in tomato colonized by arbuscular mycorrhizae under NaCl stress, Colloids Surf. B. Biointerfaces, 2007, vol. 59, pp. 128–133.CrossRefPubMedGoogle Scholar
  10. 10.
    Hajiboland, R., Aliasgharzadeh, N., Laiegh, S.F., and Poschenrieder, C., Colonization with arbuscular mycorrhizal fungi improves salinity tolerance of tomato (Solanum lycopersicum L.) plants, Plant Soil, 2010, vol. 331, pp. 313–327.CrossRefGoogle Scholar
  11. 11.
    Ghorbanli, M., Ebrahimzadeh, H., and Sharifi, M., Effects of NaCl and mycorrhizal fungi on antioxidative enzymes in soybean, Biol. Plant., 2004, vol. 48, pp. 575–581.CrossRefGoogle Scholar
  12. 12.
    Abdel Latef, A.A. and He, C., Arbuscular mycorrhizal influence on growth, photosynthetic pigments, osmotic adjustment and oxidative stress in tomato plants subjected to low temperature stress, Acta Physiol. Plant., 2011, vol. 33, pp. 1217–1225.CrossRefGoogle Scholar
  13. 13.
    Arnon, D.I., Copper enzymes in isolated chloroplasts, polyphenoloxidase Beta vulgaris, Plant Physiol., 1949, vol. 24, pp. 1–15.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Phillips, J.M. and Hayman, D.S., Improved procedures for clearing roots and staining parasitic and vesicular- arbuscular mycorrhizal fungi for rapid assessment of infection, Trans. Br. Mycol. Soc., 1970, vol. 55, pp. 158–161.CrossRefGoogle Scholar
  15. 15.
    Velikova, V., Yordanov, I., and Edreva, A., Oxidative stress and some antioxidant systems in acid rain-treated bean plants, Plant Sci., 2000, vol. 151, pp. 59–66.CrossRefGoogle Scholar
  16. 16.
    Heath, R.L. and Packer, L., Photoperoxidation in isolated chloroplasts, Arch. Biochem. Biophys., 1968, vol. 125, pp. 189–198.CrossRefPubMedGoogle Scholar
  17. 17.
    Elstner, E.F. and Heupel, A., Inhibition of nitrite formation from hydroxylammoniumchloride: a simple assay for superoxide dismutase, Anal. Biochem., 1976, vol. 70, pp. 616–620.CrossRefPubMedGoogle Scholar
  18. 18.
    Brand-Williams, W., Cuvelier, M.E., and Berset, C., Use of a free radical method to evaluate antioxidant activity, LWT—Food Sci. Technol., 1995, vol. 28, pp. 25–30.Google Scholar
  19. 19.
    Chun, O.K., Kim, D.O., and Lee, C.Y., Superoxide radical scavenging activity of the major polyphenols in fresh plums, J. Agric. Food Chem., 2003, vol. 51, pp. 8067–8072.CrossRefPubMedGoogle Scholar
  20. 20.
    Jia, Z., Tang, M., and Wu, J., The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals, Food Chem., 1999, vol. 64, pp. 555–559.CrossRefGoogle Scholar
  21. 21.
    Gossett, D.R., Millhollon, E.P., and Lucas, M.C., Antioxidant response to NaCl stress in salt-tolerant and salt-sensitive cultivars of cotton, Crop Sci., 1994, vol. 34, pp. 706–714.CrossRefGoogle Scholar
  22. 22.
    Griffith, O.W., Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine, Anal. Biochem., 1980, vol. 106, pp. 207–212.CrossRefPubMedGoogle Scholar
  23. 23.
    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.Google Scholar
  24. 24.
    Luck, H., Catalase, in Methods of Enzymatic Analysis, Bergmeyer, H.U., Ed., New York: Academic, 1971, pp. 885–894.Google Scholar
  25. 25.
    Miyake, C. and Asada, K., Thylakoid-bound ascorbate peroxidase in spinach chloroplasts and photoreduction of its primary oxidation product monodehydroascorbate radicals in thylakoids, Plant Cell Physiol., 1992, vol. 33, pp. 541–553.Google Scholar
  26. 26.
    Carlberg, I. and Mannervik, B., Glutathione reductase, Methods Enzymol., 1985, vol. 113, pp. 484–490.CrossRefPubMedGoogle Scholar
  27. 27.
    Evelin, H., Kapoor, R., and Giri, B., Arbuscular mycorrhizal fungi in alleviation of salt stress: a review, Ann. Bot., 2009, vol. 104, pp. 1263–1280.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Kohler, J., Hernández, J.A., Caravaca, F., and Roldán, A., Induction of antioxidant enzymes is involved in the greater effectiveness of a PGPR versus AM fungi with respect to increasing the tolerance of lettuce to severe salt stress, Environ. Exp. Bot., 2009, vol. 65, pp. 245–252.CrossRefGoogle Scholar
  29. 29.
    Aroca, R., Ruiz-Lozano, J.M., Zamarreño, Á.M., Paz, J.A., García-Mina, J.M., Pozo, M.J., and López-Ráez, J.A., Arbuscular mycorrhizal symbiosis influences strigolactone production under salinity and alleviates salt stress in lettuce plants, J. Plant Physiol., 2013, vol. 170, pp. 47–55.CrossRefPubMedGoogle Scholar
  30. 30.
    Liu, T., Sheng, M., Wang, C.Y., Chen, H., Li, Z., and Tang, M., Impact of arbuscular mycorrhizal fungi on the growth, water status, and photosynthesis of hybrid poplar under drought stress and recovery, Photosynthetica, 2015, vol. 53, pp. 250–258.CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2018

Authors and Affiliations

  • A. Ghorbani
    • 1
  • S. M. Razavi
    • 1
    Email author
  • V. O. G. Omran
    • 2
  • H. Pirdashti
    • 2
  1. 1.Department of Biology, Faculty of SciencesUniversity of Mohaghegh ArdabiliArdabilIslamic Republic of Iran
  2. 2.Department of Agronomy, Genetics and Agricultural Biotechnology Institute of TabarestanSari Agricultural Science and Natural Resources UniversitySariIran

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