Effect of root inoculation of mycorrhiza fungi (Glomus mosseae) on growth and ‎resistance to drought stress in Gleditsia caspica seedlings

Document Type : Full Paper


1 M. Sc.‎‏ ‏Graduate, Faculty of Agriculture and Natural Resources, Arak University, Arak, Iran

2 Associate Professor, Faculty of Agriculture and Natural Resources, Arak University, Arak, Iran


Drought is one of the most important environmental factors which limit the growth of woody plant. In order to evaluvate the resistance of Caspian locust seedlings to drought stress through inoculation with arbuscular mycorrhiza fungi a factorial experiment was performed in completely randomized design in 2016-2018. The factors were included mycorrhiza at two levels (inoculation and uninoculated with Glomus moseae) and drought stress at two levels (Well-watered and withholding water). Drought stress significantly reduced growth traits such as relative water content, percentage of aerial and root dry biomass, content of total chlorophyll, total carotenoid content and cell membrane stability index and significantly increased proline content. Root inoculation of seedlings with mycorrhizal fungi improved relative water content (14%), total carotenoid content (25%), aerial dry biomass percentage (4.5%), root dry biomass percentage (6.2%), and total antioxidant capacity (54.8%) than to uninoculated seedlings. Also, cell membrane stability index, total chlorophyll content, total phenol content and total flavonoid content in inoculated seedlings were higher than non-inoculated seedlings under both drought and normal irrigation conditions. Overall, the results showed that mycorrhizal fungi improved growth characteristics and reduced adverse effects of drought stress by increasing antioxidant compounds in Caspian locust seedlings.


  1. Abbaspour, H., Saeid-Sar, S. & Afshari, H. (2011). Improving drought tolerance of Pistacia vera seedlings by arbuscular mycorrhiza under greenhouse condition. Journal of Medicinal Plants Research, 5(32), 7065-7072.
  2. Akowuah, G.A., Ismail, Z., Norhayati, I. & Sadikun, A. (2005). The effects of different extraction solvents of varying polarities on polyphenols of Orthosiphon stamineus and evaluation of the free radical-scavenging activity. Food Chemistry, 93, 311-317.
  3. Andre, C.M., Schafleitner, R., Legay, S., Lefevre, I., Aliaga, C.A.A., Nomberto, G., Hoffmann, L., Hausman, J.F., Larondelle, Y. & Evers, D. (2009). Gene expression changes related to the production of phenolic compounds in potato tubers grown under drought stress. Phytochemistry, 70(9), 1107-1116.
  4. Arndt, S.K., Cliford, S.C., Wanek, W., Joness, H.G. & Popp, M. (2001). Physiological and morphological adaptations of the fruit tree Ziziphus rotundifolia in response to progressive drought stress. Tree Physiology, 21, 705-715.
  5. Ashraf, M. & Foolad, M.R. (2007). Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environmental and Experimental Botany, 59, 206-216.
  6. Asrar, A.A., Abdel-Fattah, G.M. & Elhindi, K.M. (2012). Improving growth, flower yield and water relations of snapdragon (Antirhinum majus) plants grown under well-watered and water-stress conditions using arbuscular mycorrhizal fungi. Photosynthetica, 50, 305-316.
  7. Bainard, L.D., Klironomos, J.N. & Gordon, A.M. (2011). The mycorrhizal status and colonization of 26 tree species growing in urban and rural environments. Mycorrhiza, 21 (2), 91-96.
  8. Baslam, M., Esteban, R., Garcia-Plazaola, J.I. & Goicoechea, N. (2013). Effectiveness of arbuscular mycorrhizal fungi (AMF) for inducing the accumulation of major carotenoids, chlorophylls and tocopherol in green and red leaf lettuces. Applied Microbiology and Biotechnology, 97, 3119-3128.
  9. Bates, L.S., Waldren, R.P. & Teare, L.D. (1973). Rapid determination of free proline for water-stress studies. Plant Soil. 39, 205-207.
  10. Beltrano, J. & Ronco, M.G. (2008). Improved tolerance of wheat plants (Triticum aestivum) to drought stress and rewatering by the arbuscular mycorrhizal fungus Glomus claroideum: effect on growth and cell membrane stability. Brazilian Journal of Plant Physiology, 20 (1), 29-37.
  11. Beltrano, J., Ruscitti, M., Arango, M.C. & Ronco, M. (2013). Effects of arbuscular mycorrhiza inoculation on plant growth, biological and physiological parameters and mineral nutrition in pepper grown under different salinity and p levels. Soil Science and Plant Nutrition, 13, 123-141.
  12. Ceccarelli, N., Curadi, M., Martelloni, L., Sbrana, C., Picciarelli, P. & Giovannetti, M. (2010). Mycorrhizal colonization impacts on phenolic content and antioxidant properties of artichoke leaves and flower heads two years after field Plant and Soil. 335, 311 -323.
  13. Chang, W.C., Kim, S.C., Hwang, S.S., Choi, B.K. & Kim, S.K. (2002). Antioxidant activity and free radical scavenging capacity between Korean medicinal plants and flavonoids by assay-guided comparison. Plant Science, 163, 1161-1168.
  14. Chu, Y.H., Chang, C.L. & Hsu, H.F. (2000). Flavonoid content of several vegetable and their antioxidant activity. Journal of the Science of Food and Agriculture, 80(5), 561-566.
  15. Fan, Q.J. & Liu, J.H. (2011). Colonization with arbuscular mycorrhizal fungus affects growth, drought tolerance and expression of stress-responsive genes in Poncirus trifoliata. Acta Physiologiae Plantarum, 33, 1533-1542.
  16. Farrokhvand, I., Reezi, S., Barzegar, R. & Fattahi, M. (2020). Effect of symbiosis of several mycorrhiza arbuscular fungi species on some quality ‎and physiological indices of potted lisianthus flower ‎(Eustoma grandiflorum ‘Matador Blue’)‎. Iranian Journal of Horticultural Science, 50 (4), 815-824. (In Farsi).
  17. Ferrat, I.L. & Lova, C.J. (1999). Relation between relative water content, nitrogen pools and growth of Phaseolus vulgaris and P. acutifolius A. Gray during water deficit. Crop Science, 39: 467-474.
  18. Fouad, M.O., Essahibi, A., Benhiba, L. & Qaddoury, A. (2014). Effectiveness of arbuscular mycorrhizal fungi in the protection of olive plants against oxidative stress induced by drought. Spanish Journal of Agricultural Research, 12(3), 763-771.
  19. Frosi, G., Barros, V.A., Oliveira, M.T. Santos, M., Ramos, D.G. Maia, L.C. & Santos M.G. (2016). Symbiosis with AMF and leaf Pi supply increases water deficit tolerance of woody species from seasonal dry tropical forest. Plant Physiology, 207, 84-93.
  20. Gill, S.S. & Tuteja, N. (2010). Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry, 48, 909-930.
  21. Giovannetti, H.W. & Mosse, B. (1980). An evaluation techniques for measuring vesicular arbescular mycorrhiza infection in roots. New Phytologist, 84, 489-500.
  22. Goss, M.J., Carvalho, M. & Brito, I. (2017). Functional diversity of mycorrhiza and sustainable agriculture, management to overcome biotic and abiotic stresses. Academic Press.
  23. Huxley, A., Griffiths, M. & Levy, M. (1999). The new royal horticultural society dictionary of gardening. Macmillan Press.
  24. Inze, D. (2008). Oxidative stress in plant. Environmental and Experimental Botany, 48(5), 351-358.
  25. Jeyaramraja, P.R., Meenakshi, S.N., Kumar, R.S., Joshi, S.D. and Ramasubramanian, (2005). Water deficit induced oxidative damage in tea (Camelia sinensis) plants. Journal of Plant Physiology, 162, 413-419
  26. Joshi, P. & Swami, A. (2007). Physiological responses of some tree species under roadside automobile pollution stress around city of Haridwar, India. The Environmentalist, 27 (3), 365-374.
  27. Karlidag, H., Yildirim, E. & Turan, M. (2009). Salicylic acid ameliorates the adverse effect of salt stress on strawberry. Science Agriculture, 66 (2), 180- 187.
  28. Khaleghi, A. (2014). Study of resistance to freezing temperatures and response to drought in Maclura pomifera for urban greenspace application. Ph.D. Thesis. College of Agriculture and Natural Resources, University of Tehran, Iran. (in Farsi).
  29. Khaleghi, A., Naderi, R., Brunetti, , Maserti, B.E., Salami, S.A. & Babalar M. (2019). Morphological, physiochemical and antioxidant responses of Maclura pomifera to drought stress. Scientific Reports, 9:19250.
  30. Khaleghi, A., Naderi, R., Salami, A., Babalar, M., Roohollahi, I. & Khaleghi, G. (2016). Evaluation of salicylic acid and spermidine on reduce drought stress injuries of one-year-old Maclura pomifera Journal of Crops Improvement, 18 (1), 231-244. (in Farsi).
  31. Kranner, I., Beckett, R.P., Wornik, S., Zorn, M. & Pfeifhofer H.W. (2002) Revival of a resurrection plant correlates with its antioxidant status. The Plant Journal, 31, 13–24.
  32. Krasensky, J. & Jonak, C. (2012). Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. Experimental Botany, 63, 1593-1608.
  33. Djeridane, A., Yousfi, M. & Nadjemi, B. (2006). Antioxidant activity of some Algerian medicinal plants extracts containing phenolic compounds. Food Chemistry, 97, 654-660.
  34. Lichtenthaler, H.K. & Wellburnt, A.R. (1983). Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochemical Society Transactions, 11: 591–592.
  35. Maiquetía, M., Cáceres, A. & Herrera, A. (2009). Mycorrhization and phosphorus nutrition affect water relations and CAM induction by drought in seedlings of Clusia minor. Annals of Botany, 103, 525-532.
  36. Martinova, V., van Geel, M., Lievens, B. & Honnay, O. (2016). Strong differences in Quercus robur-associated ectomycorrhizal fungal communities along a forest-city soil sealing gradient. Fungal Ecology, 20, 88-96.
  37. Morello, J.R., Romero, M.P., Ramo, & Motilva, M.J. )2005(. Evaluation of L-phenylalanine ammonia-lyase activity and phenolic profile in olive drupe (Olea europaea L.) from fruit setting period to harvesting time. Plant Science, 168, 65-72.
  38. Morte, A., Dıaz, G., Rodrıguez, P., Alarcon, J.J. & Sanchez-Blanco, M.J. (2001). Growth and water relations in mycorrhizal and nonmycorrhizal Pinus halepensis plants in response to drought. Biologia Plantarum, 44, 263-267.
  39. Noroozi-Raeis-Danaie, M. Mirzaie-Nodoushan, H. Maddah-Arefi H. & Jafari A.A. (2009). Spiny trunk in Caspian locust (Gleditsia caspica) and its variation in half-sib progenies. Iranian Journal of Rangelands and Forests Plant Breeding and Genetic Research, 17 (2), 222-233. (in Farsi).
  40. Ortega, U., Dunabeitia, M., Menendez, S., Gonzalez-Murua, C. & Majada, J. (2004). Effectiveness of mycorrhizal inoculation in the nursery on growth and water relations of Pinus radiata in different water regimes. Tree Physiology, 24, 65-73.
  41. Otgonsuren, B., Rewald, B., Godbold, D.L. & Göransson, H. (2016). Ectomycorrhizal inoculation of Populus nigra modifies the response of absorptive root respiration and root surface enzyme activity tosalinity stress. Flora, 224, 123-129.
  42. 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. Transactions of the British Mycological Society, 55(1), 158-168.
  43. Ruiz-Lozano, J.M. (2003). Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress. New perspectives for molecular studies. Mycorrhiza, 13, 309-317.
  44. Sangtarash, M.H., Qaderi, M.M., Chinnappa, C.C. & Reid, D.M. (2009). Carotenoid differential sensitivity of canola (Brassica napus) seedlings to ultraviolet-B radiation, water stress and abscisic acid. Environmental and Experimental Botany, 66(2), 212-219.
  45. Seki, M. Umezawa, T., Urano, K. & Shinozaki, K. (2007). Regulatory metabolic networks in drought stress responses. Plant Biology, 10, 296–302.
  46. Shi, L., Guttenberger, M., Kottke, I. & Hampp, R. (2002). The effect of drought on mycorrhizas of beech (Fagus sylvatica): changes in community structure, and the content of carbohydrates and nitrogen storage bodies of the fungi. Mycorrhiza, 12, 303-311.
  47. Silva, E.N., Ribeiro, R.V., Ferreira-Silva, S.L., Viegas, R.A. & Silveira J.A.G. (2010). Comparative effects of salinity and water stress on photosynthesis, water relations and growth of Jatropha curcas Journal of Arid Environments, 74, 1130-1137.
  48. Simard, S.W., Beiler, K.J., Bingham, M.A., Deslippe, J.R., Philip, L.J. & Teste, F.P., (2012). Mycorrhizal networks: mechanisms, ecology and modelling. Fungal Biology Reviews, 26, 39-60.
  49. Singleton, V.L. & Rossi, J.A. (1965). Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. American Journal of Enology and Viticulture, 16, 144-158.
  50. Smith, S.E. & Smith, F.A., (2011). Roles of arbuscular mycorrhizas in plant nutrient and growth: new paradigms from cellular to ecosystem scales. Annual Review of Plant Biology, 62, 227-250.
  51. Tattini, M., Galardi, C., Pinelli, P., Massari, R., Remorini, D. & Agati, G. (2004). Differential accumulation of flavonoids and hydroxycinnamates in leaves of Ligustrum vulgare under excess light and drought stress. New Phytologist, 163, 547-561.
  52. Timonen, S. & Kauppinen, P. (2008). Mycorrhizal colonisation patterns of Tilia trees in street, nursery and forest habitats in southern Finland. Urban Forestry & Urban Greening, 7 (4), 265-276.
  53. Tyagi, J., Varma, A. & Pudake, R.N. (2017). Evaluation of comparative effects of arbuscular mycorrhiza (Rhizophagus intraradices) and endophyte (Piriformospora indica) association with finger millet (Eleusine coracana) under drought stress. European Journal of Soil Biology, 81, 1-10.
  54. Wu, Q.S. & Xia, R.X. (2006). Arbuscular mycorrhizal fungi influence growth, osmotic adjustment and photosynthesis of citrus under well-watered and water stress conditions. Journal of Plant Physiology, 163, 417-425.
  55. Wu, Q.S., Srivastava, A.K. & Zou, Y.N. (2013). AMF-induced tolerance to drought stress in citrus: A review. Scientia Horticulturae, 164, 77-87.
  56. Wu, Q.S., Zou, Y.N. & He, X.H. (2011). Difference of hyphal and soil phosphatase activities in drought-stressed mycorrhizal trifoliate orange (Poncirus trifoliate) seedlings. Scientia Horticulturae, 129, 294-298.
  57. Wu, Q.S., Zou, Y.N. & Xia, R.X. (2006). Effects of water stress and arbuscular mycorrhizal fungi on reactive oxygen metabolism and antioxidant production by citrus (Citrus tangerine) roots. European Journal of Soil Biology, 42, 166-177.
  58. Yang, F. & Miao, L.F. (2010). Adaptive responses to progressive drought stress in two poplar species originating from different altitudes. Silva Fennica, 44(1), 23-37.
  59. Yooyongwech, S., Phaukinsang, N., Cha-um, S. & Supaibulwatana, K. (2013). Arbuscular mycorrhiza improved growth performance in Macadamia tetraphylla grown under water deficit stress involves soluble sugar and proline accumulation. Plant Growth Regulation, 69, 285-293.
  60. Zakerian, F., Sefidkon, F., Abbaszadeh, B. & Kalate-Jari, S. (2020). Effect of drought stress and mycorrhizal fungi on physiological traits and essential ‎oil percentage of Satureja sahandicaIranian Journal of Horticultural Science, 51 (1), 189-201. (In Farsi).