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Research Article

volume 38 issue 5 (october 2015) : 579-588,   Doi: 10.18805/lr.v38i5.5933

Induction of salt stress tolerance in cowpea [Vigna unguiculata (L.) Walp.] by arbuscular mycorrhizal fungi

H
Hashem Abeer
E
E.F. Abd Allah
A
A.A. Alqarawi
D
Dilfuza Egamberdieva
1Botany and Microbiology Department, Faculty of Science, King Saud University, P.O. Box. 2460 Riyadh 11451, Saudi Arabia.
Cite article:- Abeer Hashem, Allah Abd E.F., Alqarawi A.A., Egamberdieva Dilfuza (2025). Induction of salt stress tolerance in cowpea [Vigna unguiculata (L.) Walp.] by arbuscular mycorrhizal fungi. Legume Research. 38(5): 579-588. doi: 10.18805/lr.v38i5.5933.

ABSTRACT

The aim of present study was to examine the effect of arbuscular mycorrhizal fungi (AMF) on the growth, lipid peroxidation, antioxidant enzyme activity and some key physio-biochemical attributes in cowpea (Vigna unguiculata [L.] Walp.) subjected to salt stress. Salt stress (200 mM NaCl) reduced growth, biomass, relative water content and chlorophyll pigment content in cowpea leaves. AMF ameliorated the negative impact of salinity on the growth parameters studied. The activity of antioxidant enzymes such as superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX), peroxidase (POD) and glutathione reductase (GR) enhanced under salt stress and AMF inoculation further enhanced their activity, thus strengthening the plant’s defense system. Proline content increased in salt stressed plants as well as AMF-inoculated plants providing efficient protection against salt stress. Besides this AMF also increased uptake of mineral elements which have direct impact on the osmoregulation of the plants. The present study shows that AMF possesses the potential to enhance salt tolerance of cowpea.

REFERENCES


  1. Abdel Latef, A.A.H., Chaoxing, H. (2011). Effect of arbuscular mycorrhizal fungi on growth, mineral nutrition, antioxidant enzymes activity and fruit yield of tomato grown under salinity stress. Scientia Hort. 127: 228–233.

  2. Ahanger, M.A., Hashem, A., Abd Allah, E.F., Ahmad, P. (2014). Arbuscular mycorrhiza in crop improvement under environmental stress, In: Ahmad, P., Rasool, S. (Eds.), Emerging Technologies and Management of Crop Stress Tolerance, Volume 2. pp 69-95.

  3. Ahmad, P. (2010). Growth and antioxidant responses in mustard (Brassica juncea L.) plants subjected to combined effect of gibberellic acid and salinity. Arch. Agro. Soil Sci. 56: 575–588.

  4. Ahmad, P., Ashraf, M., Azooz, M.M., Rasool, S., Akram, N.A. (2014). Potassium starvation induced oxidative stress and antioxidant defense responses in Brassica juncea. J. Plant Int. 9: 1-9.

  5. Alexander, M. (1982). Most probable number method for microbial populations, In: Methods of Soil Analysis, Black, C.A., (Ed.), American Society of Agronomy, Madison, WI, USA. pp. 815-820.

  6. Alqarawi, A.A., Abd_Allah, E.F., Hashem, A. (2014a). Alleviation of salt-induced adverse impact via mycorrhizal fungi in Ephedra aphylla Forssk. J. Plant Interact. 9: 802–810.

  7. Alqarawi, A.A., Hashem A., Abd_Allah, E.F., Alshahrani, T.S., Al-Huqail, A.A. (2014b). Effect of salinity on moisture content, pigment system, and lipid composition in Ephedra alata Decne. Acta Biologica Hungarica 65: 61-71.

  8. Aroca, R., Ruiz-Lozano, J.M., Zamarreno, A., Paz, J.A., Garcia-Mina, J.M., Pozo, M,J., Lopez-Raez, J.A. (2013). Arbuscular mycorrhizal symbiosis influences strigolactone production under salinity and alleviates salt stress in lettuce plants. J. Plant Physiol. 170: 47–55.

  9. Arora, N., Bhardwaj, N., Sharma, P., Arora, H.K. (2008). 28-Homobrassinolide alleviates oxidative stress in salt treated maize (Zea mays L.) plants. Braz. J. Plant Physiol. 20: 153-157.

  10. Arulbalachandran, D., Ganesh, K.S., Subramani, A. (2009). Changes in metabolites and antioxidant enzyme activity of three Vigna Species induced by NaCl stress. Amer. Eur. J. Agron. 2: 109-116.

  11. Bayer, W.F., Fridovich, J.L. (1987). Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal. Biochem. 161: 559-566.

  12. Carlberg, I., Mannervik, B. (1985). Glutathione Reductase, Methods in Enzymology, vol. 113, Meister, A., Ed., New York, Academic, pp. 484-490. Cekic, F.O., Unyayar, S., Ortas, I. (2012). Effects of arbuscular mycorrhizal inoculation on biochemical parameters in Capsicum annuum grown under long term salt stress. Turk J. Bot. 36: 63-72.

  13. Chen, C., Tao, C., Peng, C., Ding, Y. (2007). Genetic analysis of salt stress responses in Asparagus Bean (Vigna unguiculata [L.] ssp. sesquipedalis Verdc.). J. Hered. 98: 655–665.

  14. Daniels, B.A., Skipper, H.D. (1982). Methods for the recovery and quantitative estimation of propagules from soil, In: Methods and Principles of Mycorrhizal Research, Schenck, N.C., (Eds.), The American Phytopathological Society. pp. 29-36,

  15. Egamberdieva, D., Shurigin, V., Gopalakrishnan, S., Sharma, R. (2015). Microbial strategy for the improvement of legume production under hostile environment. In: Mohamed Mahgoub Azooz and Parvaiz Ahmad (Eds.), Legumes under Environmental Stress: Yield, Improvement and Adaptations, Whiley and Sons, USA, 133-142 pp.

  16. Egamberdiyeva, D., Gafurova, L., Islam, K.R. (2007). Salinity effects on irrigated soil chemical and biological properties in the Syr-Darya basin of Uzbekistan. In: Lal R, Sulaimanov M, Stewart B, Hansen D, Doraiswamy P (Eds) Climate Change and Terrestrial C Sequestration in Central Asia, New York, Taylor-Francis,, pp 147-162.

  17. Freitas, V.S., Alencar, N.D.M., Lacerda, C.F., Prisco, J.Y., Gomes-Filho, E. (2011). Changes in physiological and biochemical indicators associated with salt tolerance in cotton, sorghum and cowpea. Afri. J. Bio. Res. 5: 264-271. Garg, N., Manchanda, G. (2009). Role of Arbuscular Mycorrhizae in the Alleviation of Ionic, Osmotic and oxidative stresses induced by salinity in Cajanus cajan (L.) Millsp. (pigeon pea) J. Agron. Crop Sci. 195: 110-123.

  18. Hadi, F., Hussain, F., Arif, M., 2012. Growth performance and comparison of cowpea varieties under different NaCl salinity stresses. Greener J. Physical Sci. 2: 44-49.

  19. Hajiboland, R., Aliasgharzadeh, A., Laiegh, S.F., Poschenrieder, C. (2010). Colonization with arbuscular mycorrhizal fungi improves salinity tolerance of tomato (Solanum lycopersicum L.) plants. Plant Soil 331: 313–327.

  20. Hameed, A., Egamberdieva, D., Abd_Allah, E.F., Hashem Abeer, Kumar, A., Ahmad, P. (2014). Salinity stress and arbuscular mycorrhizal symbiosis in plants. In: M. Miransari (Ed.), Use of Microbes for the Alleviation of Soil Stresses, Volume 1, DOI: 10.1007/978-1-4614-9466-9-7, © Springer Science+Business Media New York 2014. Pp 139-159.

  21. Harinasut, P., Srisunak, S., Pitukchaisopol, S., Charoensataporn, R. (2000). Mechanism of adaptation to increasing salinity of mulberry: Proline content and ascorbate peroxidase activity in leaves of multiple shoots. Sci. Asia. 26: 207–211.

  22. Hashem Abeer, Abd_Allah, E.F., Alqarawi, A.A., Alwhibi, Mona, S., Alenazi, M.M., Egamberdieva Dilfuza, Ahmad, P. (2015). Arbuscular mycorrhizal fungi mitigates NaCl induced adverse effects on Solanum lycopersicum L. Pak. J. Bot. 47: 327-340.

  23. Hashem, Abeer, Abd_Allah, E.F., El-Didamony G., Al Whibi Mona S., Asma A., Egamberdieva Dilfuza, Ahmad P. (2014a). Alleviation of adverse impact of salinity on faba bean (Vicia faba L.) by arbuscular mycorrhizal fungi. Pak. J. Bot. 46: 2003-2013.

  24. Hashem, Abeer, Abd_Allah, E.F., Alqarawi, A.A., Al Huqail, Asma A., Egamberdieva Dilfuza. (2014b). Alleviation of abiotic salt stress in Ochradenus baccatus (Del.) by Trichoderma hamatum (Bonord.) Bainier. J. Plant Interact. 9: 857-868.

  25. Heath, R.L., Packer, L. (1968). Photoperoxidation in isolated chlorplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch. Biochem. Biophys. 125: 189-198.

  26. Hiscox, J.D., Israelstam, G.F. (1979). A method for the extraction of chlorophyll from leaf tissue without maceration. Can. J. Bot. 57: 1332-1334.

  27. Hoagland, D.R., Arnon, D.I. (1950). The water-culture method for growing plants without soil, Calif. Agr. Expt. Sta. 347: 1-32. Kar, M., Mishra, D. (1976). Catalase, peroxidase, polyphenyl oxidase activities during rice leaf senescence. Plant Physiol. 57: 315–319.

  28. Lowry, O.H., Rosebrough, N.S., Farrand, A.L., Randall, R.J. (1951). Protein measurement with folin phenol reagent. J. Bio. Chem. 193: 263-275. Luck, H. (1974). Catalases, Methods of Enzymatic Analysis, vol. 2, Bregmeyer, H.U., (Ed.), New York, Academic.

  29. Mittal, S., Kumari, N., Sharma, V. (2012). Differential response of salt stress on Brassica juncea: photosynthetic performance, pigment, proline, D1 and antioxidant enzymes. Plant Physiol. Bioch. 54: 17–26.

  30. Nakano, Y., Asada, K. (1981). Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach-chloroplasts. Plant Cell Physiol. 22: 867-880.


  31. Phillips, J.M., Hayman, D.S. (1970). Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans. Brit. Mycol. Soc. 55: 158-161.

  32. Porcel, R., Aroca, R., Ruiz-Lozano, J.M. (2012). Salinity stress alleviation using arbuscular mycorrhizal fungi. A review. Agron. Sust. Dev. 32: 181–200.

  33. Rasool, S., Ahmad, A., Siddiqi, T.O., Ahmad, P. (2013). Changes in growth, lipid peroxidation and some key antioxidant enzymes in chickpea genotypes under salt stress. Acta. Physiol. Plant. 35: 1039-1050.

  34. Ruiz-Lozano, J.M., Porcel, R., Azcon, R., Aroca, R. (2012). Regulation by arbuscular mycorrhizae of the integrated physiological response to salinity in plants. New challenges in physiological and molecular studies. J. Exp. Bot. 63: 4033-4044.

  35. Sadasivam, S., Manickam, A. (1996). Biochemical methods. 2nd Edition, New Age International Publishers (P) Ltd., New Delhi, India. pp. 107-109.

  36. Sairam, R.K., Deshmukh, P.S., Shukla, D.S. (1997). Tolerance of drought and temperature stress in relation to increased antioxidant enzyme activity in wheat. J. Agron. Crop Sci. 178: 171-178.

  37. Shekoofeh, E., Sepideh, H., Roya, R. (2012). Role of mycorrhizal fungi and salicylic acid in salinity tolerance of Ocimum basilicum resistance to salinity. J. Biot. 11: 2223-2235.

  38. Sivritepe, N., Sivritepe, H.O., Eris, A. (2003). The effects of NaCl priming on salt tolerance in melon seedlings grown under saline conditions. Sci. Hortic. 97: 229-237.

  39. Smart, R.E., Bihgham, G.E. (1974). Rapid estimates of relative water content. Plant Physiol. 53: 258-260. Tang, M., Chen, H., Huang, J.C., Tian, Z.Q. (2009). AM fungi effects on the growth and physiology of Zea mays seedlings under diesel stress. Soil Bio. Bioch. 41: 936–940.

  40. Tuna, A.L., Kaya, C., Dikilitas, M., Higgs, D. (2008). The combined effects of gibberellic acid and salinity on some antioxidant enzyme activities, plant growth parameters and nutritional status in maize plants. Environ. Expt. Bot. 63: 1-9.

  41. Utobo, E.B., Ogbodo, E.N., Nwogbaga, A.C. (2011). Techniques for extraction and quantification of arbuscular rmycorrhizal fungi, Libyan Agric. Res. Center. Int. 2: 68-78.

  42. Wolf, B. (1982). A comprehensive system of leaf analysis and its use for diagnosing crop nutrient status. Comm. Soil Sci. Plant Anal. 13: 1035-1059.

  43. Wu, Q.S., Zou, Y.N., Abd_Allah, E.F. (2014). Mycorrhizal Association and ROS in Plants. In: P. Ahmad (Ed): Oxidative Damage to Plants. DOI: http://dx.doi.org/10.1016/B978-0-12-799963-0.00015-0 © 2014 Elsevier Inc. All rights reserved. Pp 453- 475.
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    Research Article

    volume 38 issue 5 (october 2015) : 579-588,   Doi: 10.18805/lr.v38i5.5933

    Induction of salt stress tolerance in cowpea [Vigna unguiculata (L.) Walp.] by arbuscular mycorrhizal fungi

    H
    Hashem Abeer
    E
    E.F. Abd Allah
    A
    A.A. Alqarawi
    D
    Dilfuza Egamberdieva
    1Botany and Microbiology Department, Faculty of Science, King Saud University, P.O. Box. 2460 Riyadh 11451, Saudi Arabia.
    Cite article:- Abeer Hashem, Allah Abd E.F., Alqarawi A.A., Egamberdieva Dilfuza (2025). Induction of salt stress tolerance in cowpea [Vigna unguiculata (L.) Walp.] by arbuscular mycorrhizal fungi. Legume Research. 38(5): 579-588. doi: 10.18805/lr.v38i5.5933.

    ABSTRACT

    The aim of present study was to examine the effect of arbuscular mycorrhizal fungi (AMF) on the growth, lipid peroxidation, antioxidant enzyme activity and some key physio-biochemical attributes in cowpea (Vigna unguiculata [L.] Walp.) subjected to salt stress. Salt stress (200 mM NaCl) reduced growth, biomass, relative water content and chlorophyll pigment content in cowpea leaves. AMF ameliorated the negative impact of salinity on the growth parameters studied. The activity of antioxidant enzymes such as superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX), peroxidase (POD) and glutathione reductase (GR) enhanced under salt stress and AMF inoculation further enhanced their activity, thus strengthening the plant’s defense system. Proline content increased in salt stressed plants as well as AMF-inoculated plants providing efficient protection against salt stress. Besides this AMF also increased uptake of mineral elements which have direct impact on the osmoregulation of the plants. The present study shows that AMF possesses the potential to enhance salt tolerance of cowpea.

    REFERENCES


    1. Abdel Latef, A.A.H., Chaoxing, H. (2011). Effect of arbuscular mycorrhizal fungi on growth, mineral nutrition, antioxidant enzymes activity and fruit yield of tomato grown under salinity stress. Scientia Hort. 127: 228–233.

    2. Ahanger, M.A., Hashem, A., Abd Allah, E.F., Ahmad, P. (2014). Arbuscular mycorrhiza in crop improvement under environmental stress, In: Ahmad, P., Rasool, S. (Eds.), Emerging Technologies and Management of Crop Stress Tolerance, Volume 2. pp 69-95.

    3. Ahmad, P. (2010). Growth and antioxidant responses in mustard (Brassica juncea L.) plants subjected to combined effect of gibberellic acid and salinity. Arch. Agro. Soil Sci. 56: 575–588.

    4. Ahmad, P., Ashraf, M., Azooz, M.M., Rasool, S., Akram, N.A. (2014). Potassium starvation induced oxidative stress and antioxidant defense responses in Brassica juncea. J. Plant Int. 9: 1-9.

    5. Alexander, M. (1982). Most probable number method for microbial populations, In: Methods of Soil Analysis, Black, C.A., (Ed.), American Society of Agronomy, Madison, WI, USA. pp. 815-820.

    6. Alqarawi, A.A., Abd_Allah, E.F., Hashem, A. (2014a). Alleviation of salt-induced adverse impact via mycorrhizal fungi in Ephedra aphylla Forssk. J. Plant Interact. 9: 802–810.

    7. Alqarawi, A.A., Hashem A., Abd_Allah, E.F., Alshahrani, T.S., Al-Huqail, A.A. (2014b). Effect of salinity on moisture content, pigment system, and lipid composition in Ephedra alata Decne. Acta Biologica Hungarica 65: 61-71.

    8. Aroca, R., Ruiz-Lozano, J.M., Zamarreno, A., Paz, J.A., Garcia-Mina, J.M., Pozo, M,J., Lopez-Raez, J.A. (2013). Arbuscular mycorrhizal symbiosis influences strigolactone production under salinity and alleviates salt stress in lettuce plants. J. Plant Physiol. 170: 47–55.

    9. Arora, N., Bhardwaj, N., Sharma, P., Arora, H.K. (2008). 28-Homobrassinolide alleviates oxidative stress in salt treated maize (Zea mays L.) plants. Braz. J. Plant Physiol. 20: 153-157.

    10. Arulbalachandran, D., Ganesh, K.S., Subramani, A. (2009). Changes in metabolites and antioxidant enzyme activity of three Vigna Species induced by NaCl stress. Amer. Eur. J. Agron. 2: 109-116.

    11. Bayer, W.F., Fridovich, J.L. (1987). Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal. Biochem. 161: 559-566.

    12. Carlberg, I., Mannervik, B. (1985). Glutathione Reductase, Methods in Enzymology, vol. 113, Meister, A., Ed., New York, Academic, pp. 484-490. Cekic, F.O., Unyayar, S., Ortas, I. (2012). Effects of arbuscular mycorrhizal inoculation on biochemical parameters in Capsicum annuum grown under long term salt stress. Turk J. Bot. 36: 63-72.

    13. Chen, C., Tao, C., Peng, C., Ding, Y. (2007). Genetic analysis of salt stress responses in Asparagus Bean (Vigna unguiculata [L.] ssp. sesquipedalis Verdc.). J. Hered. 98: 655–665.

    14. Daniels, B.A., Skipper, H.D. (1982). Methods for the recovery and quantitative estimation of propagules from soil, In: Methods and Principles of Mycorrhizal Research, Schenck, N.C., (Eds.), The American Phytopathological Society. pp. 29-36,

    15. Egamberdieva, D., Shurigin, V., Gopalakrishnan, S., Sharma, R. (2015). Microbial strategy for the improvement of legume production under hostile environment. In: Mohamed Mahgoub Azooz and Parvaiz Ahmad (Eds.), Legumes under Environmental Stress: Yield, Improvement and Adaptations, Whiley and Sons, USA, 133-142 pp.

    16. Egamberdiyeva, D., Gafurova, L., Islam, K.R. (2007). Salinity effects on irrigated soil chemical and biological properties in the Syr-Darya basin of Uzbekistan. In: Lal R, Sulaimanov M, Stewart B, Hansen D, Doraiswamy P (Eds) Climate Change and Terrestrial C Sequestration in Central Asia, New York, Taylor-Francis,, pp 147-162.

    17. Freitas, V.S., Alencar, N.D.M., Lacerda, C.F., Prisco, J.Y., Gomes-Filho, E. (2011). Changes in physiological and biochemical indicators associated with salt tolerance in cotton, sorghum and cowpea. Afri. J. Bio. Res. 5: 264-271. Garg, N., Manchanda, G. (2009). Role of Arbuscular Mycorrhizae in the Alleviation of Ionic, Osmotic and oxidative stresses induced by salinity in Cajanus cajan (L.) Millsp. (pigeon pea) J. Agron. Crop Sci. 195: 110-123.

    18. Hadi, F., Hussain, F., Arif, M., 2012. Growth performance and comparison of cowpea varieties under different NaCl salinity stresses. Greener J. Physical Sci. 2: 44-49.

    19. Hajiboland, R., Aliasgharzadeh, A., Laiegh, S.F., Poschenrieder, C. (2010). Colonization with arbuscular mycorrhizal fungi improves salinity tolerance of tomato (Solanum lycopersicum L.) plants. Plant Soil 331: 313–327.

    20. Hameed, A., Egamberdieva, D., Abd_Allah, E.F., Hashem Abeer, Kumar, A., Ahmad, P. (2014). Salinity stress and arbuscular mycorrhizal symbiosis in plants. In: M. Miransari (Ed.), Use of Microbes for the Alleviation of Soil Stresses, Volume 1, DOI: 10.1007/978-1-4614-9466-9-7, © Springer Science+Business Media New York 2014. Pp 139-159.

    21. Harinasut, P., Srisunak, S., Pitukchaisopol, S., Charoensataporn, R. (2000). Mechanism of adaptation to increasing salinity of mulberry: Proline content and ascorbate peroxidase activity in leaves of multiple shoots. Sci. Asia. 26: 207–211.

    22. Hashem Abeer, Abd_Allah, E.F., Alqarawi, A.A., Alwhibi, Mona, S., Alenazi, M.M., Egamberdieva Dilfuza, Ahmad, P. (2015). Arbuscular mycorrhizal fungi mitigates NaCl induced adverse effects on Solanum lycopersicum L. Pak. J. Bot. 47: 327-340.

    23. Hashem, Abeer, Abd_Allah, E.F., El-Didamony G., Al Whibi Mona S., Asma A., Egamberdieva Dilfuza, Ahmad P. (2014a). Alleviation of adverse impact of salinity on faba bean (Vicia faba L.) by arbuscular mycorrhizal fungi. Pak. J. Bot. 46: 2003-2013.

    24. Hashem, Abeer, Abd_Allah, E.F., Alqarawi, A.A., Al Huqail, Asma A., Egamberdieva Dilfuza. (2014b). Alleviation of abiotic salt stress in Ochradenus baccatus (Del.) by Trichoderma hamatum (Bonord.) Bainier. J. Plant Interact. 9: 857-868.

    25. Heath, R.L., Packer, L. (1968). Photoperoxidation in isolated chlorplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch. Biochem. Biophys. 125: 189-198.

    26. Hiscox, J.D., Israelstam, G.F. (1979). A method for the extraction of chlorophyll from leaf tissue without maceration. Can. J. Bot. 57: 1332-1334.

    27. Hoagland, D.R., Arnon, D.I. (1950). The water-culture method for growing plants without soil, Calif. Agr. Expt. Sta. 347: 1-32. Kar, M., Mishra, D. (1976). Catalase, peroxidase, polyphenyl oxidase activities during rice leaf senescence. Plant Physiol. 57: 315–319.

    28. Lowry, O.H., Rosebrough, N.S., Farrand, A.L., Randall, R.J. (1951). Protein measurement with folin phenol reagent. J. Bio. Chem. 193: 263-275. Luck, H. (1974). Catalases, Methods of Enzymatic Analysis, vol. 2, Bregmeyer, H.U., (Ed.), New York, Academic.

    29. Mittal, S., Kumari, N., Sharma, V. (2012). Differential response of salt stress on Brassica juncea: photosynthetic performance, pigment, proline, D1 and antioxidant enzymes. Plant Physiol. Bioch. 54: 17–26.

    30. Nakano, Y., Asada, K. (1981). Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach-chloroplasts. Plant Cell Physiol. 22: 867-880.


    31. Phillips, J.M., Hayman, D.S. (1970). Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans. Brit. Mycol. Soc. 55: 158-161.

    32. Porcel, R., Aroca, R., Ruiz-Lozano, J.M. (2012). Salinity stress alleviation using arbuscular mycorrhizal fungi. A review. Agron. Sust. Dev. 32: 181–200.

    33. Rasool, S., Ahmad, A., Siddiqi, T.O., Ahmad, P. (2013). Changes in growth, lipid peroxidation and some key antioxidant enzymes in chickpea genotypes under salt stress. Acta. Physiol. Plant. 35: 1039-1050.

    34. Ruiz-Lozano, J.M., Porcel, R., Azcon, R., Aroca, R. (2012). Regulation by arbuscular mycorrhizae of the integrated physiological response to salinity in plants. New challenges in physiological and molecular studies. J. Exp. Bot. 63: 4033-4044.

    35. Sadasivam, S., Manickam, A. (1996). Biochemical methods. 2nd Edition, New Age International Publishers (P) Ltd., New Delhi, India. pp. 107-109.

    36. Sairam, R.K., Deshmukh, P.S., Shukla, D.S. (1997). Tolerance of drought and temperature stress in relation to increased antioxidant enzyme activity in wheat. J. Agron. Crop Sci. 178: 171-178.

    37. Shekoofeh, E., Sepideh, H., Roya, R. (2012). Role of mycorrhizal fungi and salicylic acid in salinity tolerance of Ocimum basilicum resistance to salinity. J. Biot. 11: 2223-2235.

    38. Sivritepe, N., Sivritepe, H.O., Eris, A. (2003). The effects of NaCl priming on salt tolerance in melon seedlings grown under saline conditions. Sci. Hortic. 97: 229-237.

    39. Smart, R.E., Bihgham, G.E. (1974). Rapid estimates of relative water content. Plant Physiol. 53: 258-260. Tang, M., Chen, H., Huang, J.C., Tian, Z.Q. (2009). AM fungi effects on the growth and physiology of Zea mays seedlings under diesel stress. Soil Bio. Bioch. 41: 936–940.

    40. Tuna, A.L., Kaya, C., Dikilitas, M., Higgs, D. (2008). The combined effects of gibberellic acid and salinity on some antioxidant enzyme activities, plant growth parameters and nutritional status in maize plants. Environ. Expt. Bot. 63: 1-9.

    41. Utobo, E.B., Ogbodo, E.N., Nwogbaga, A.C. (2011). Techniques for extraction and quantification of arbuscular rmycorrhizal fungi, Libyan Agric. Res. Center. Int. 2: 68-78.

    42. Wolf, B. (1982). A comprehensive system of leaf analysis and its use for diagnosing crop nutrient status. Comm. Soil Sci. Plant Anal. 13: 1035-1059.

    43. Wu, Q.S., Zou, Y.N., Abd_Allah, E.F. (2014). Mycorrhizal Association and ROS in Plants. In: P. Ahmad (Ed): Oxidative Damage to Plants. DOI: http://dx.doi.org/10.1016/B978-0-12-799963-0.00015-0 © 2014 Elsevier Inc. All rights reserved. Pp 453- 475.
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