The Mechanisms Involved in Improving the Tolerance of Plants to Salt Stress Using Arbuscular Mycorrhizal Fungi

  • Magdi T. Abdelhamid
  • Raafat R. El-Masry
  • Darwish S. Darwish
  • Mazhar M. F. Abdalla
  • Shinya Oba
  • Ragab Ragab
Part of the Soil Biology book series (SOILBIOL, volume 56)


Salinity is considered as one of the most harming stresses faced by the plant in regard to its survival and productivity. A new biological approach “plant-microbe interaction” such as arbuscular mycorrhizal (AM) fungi to address salinity problem has recently gained momentum. Therefore, this chapter aims to provide a general overview about salinity and its effects on plant and soil, and the use of AM fungal inoculant applied to plants to alleviate salinity effects, and the mechanism of AM fungi to increase the tolerance of plants to salt stress with a crucial discussion of major accomplishments reported in this area. The results show that some mechanism of how AM fungi can increase the plant salt tolerance might work well in this regard. AM fungi maintain a superior K+:Na+ ratio that is considered as one of AM fungi’s strategies to improve tolerance to salt stress and boost absorption of P, K+, and Ca2+ over harmful Na+, thus sustaining lesser Na+:K+ ratio under salt stress. The improvement in chlorophyll as a result of AM fungi is owing in particular to the increased uptake of magnesium. AM fungi inoculation increases the activity of antioxidant enzymes in plants such as peroxidase (POD), superoxide dismutase (SOD), and catalase (CAT), which scavenge reactive oxygen species (ROS) and relieve salt stress. An additional salt tolerance mechanism by AM fungi increases the non-antioxidant of plants by accumulating osmolytes such as proline, which maintain the osmotic adjustment of plants under salinity stress. Thus, application of AM fungi inoculant is more probably due to its economic benefits under salt stress.


Antioxidants Arbuscular mycorrhizal (AM) fungi Ionic balance Oxidative stress Salinity Salt stress 



The first author Dr. Magdi Abdelhamid would like to express his gratitude to his colleagues at the Department of Botany, National Research Center, Egypt, for their valuable contribution in some phases of this study.


  1. Abd-Alla MH, Omar SA, Karanxha S (2000) The impact of pesticides on arbuscular mycorrhizal and nitrogen-fixing symbioses in legumes. Appl Soil Ecol 14:191–200CrossRefGoogle Scholar
  2. Abdel Latef AA (2010) Changes of antioxidative enzymes in salinity tolerance among different wheat cultivars. Cereal Res Commun 38:43–55CrossRefGoogle Scholar
  3. Abdelhamid MT, Shokr M, Bekheta MA (2010) Growth, root characteristics, and leaf nutrients accumulation of four faba bean (Vicia faba L.) cultivars differing in their broomrape tolerance and the soil properties in relation to salinity. Commun Soil Sci Plant Anal 41:2713–2728CrossRefGoogle Scholar
  4. Abdelhamid MT, Rady M, Osman A, Abdalla M (2013a) Exogenous application of proline alleviates salt-induced oxidative stress in Phaseolus vulgaris L. plants. J Hortic Sci Biotech 88:439–446CrossRefGoogle Scholar
  5. Abdelhamid MT, Sadak MSH, Schmidhalter U, El-Saady A (2013b) Interactive effects of salinity stress and nicotinamide on physiological and biochemical parameters of faba bean plant. Acta Biol Colomb 18:499–510Google Scholar
  6. Abouelsaad I, Renault S (2018) Enhanced oxidative stress in the jasmonic acid-deficient tomato mutant def-1 exposed to NaCl stress. J Plant Physiol 226:136–144PubMedCrossRefGoogle Scholar
  7. Adiku G, Renger M, Wessolek G, Facklam M, Hech-Bischoltz C (2001) Simulation of dry matter production and seed yield of common beans under varying soil water and salinity conditions. Agric Water Manag 47:55–68CrossRefGoogle Scholar
  8. Ahanger MA, Tyagi SR, Wani MR, Ahmad P (2014) Drought tolerance: role of organic osmolytes, growth regulators, and mineral nutrients. In: Ahmad P, Wani MR (eds) Physiological mechanisms and adaptation strategies in plants under changing environment, vol 1. Springer, New York, pp 25–55CrossRefGoogle Scholar
  9. Ahmad P, Gadgil K, Sharma S (2008) Effect of cadmium and lead on growth, biochemical parameters and uptake in Lemna polyrrhiza L. Plant Soil Environ 54:262–270CrossRefGoogle Scholar
  10. Ahmad P, Jaleel CA, Sharma S (2010) Antioxidative defense system, lipid peroxidation, proline metabolizing enzymes and biochemical activity in two Morus alba genotypes subjected to NaCl stress. Russ J Plant Physiol 57:509–517CrossRefGoogle Scholar
  11. Ahmad P, Ozturk M, Sharma S, Gucel S (2014) Effect of sodium carbonate-induced salinityalkalinity on some key osmoprotectants, protein profile, antioxidant enzymes, and lipid peroxidation in two mulberry (Morus alba L.) cultivars. J Plant Interact 9:460–467CrossRefGoogle Scholar
  12. Ahmad H, Hayat S, Ali M, Liu T, Cheng Z (2018) The combination of arbuscular mycorrhizal fungi inoculation (Glomus versiforme) and 28-homobrassinolide spraying intervals improves growth by enhancing photosynthesis, nutrient absorption, and antioxidant system in cucumber (Cucumis sativus L.) under salinity. Ecol Evol 8:5724–5740PubMedPubMedCentralCrossRefGoogle Scholar
  13. Al-Garni SMS (2006) Increasing NaCl-salt tolerance of a halophytic plant Phragmites australis by mycorrhizal symbiosis. Am Eurasian J Agric Environ Sci 1:119–126Google Scholar
  14. Alguacil MM, Hernández JA, Caravaca F, Portillo B, Roldán A (2003) Antioxidant enzyme activities in shoots from three mycorrhizal shrub species afforested in a degraded semi-arid soil. Plant Physiol 118:562–570CrossRefGoogle Scholar
  15. Alia, Prasad KVSK, Saradhi PP (1995) Effect of zinc on free radicals and proline in Brassica and Cajanus. Phytochemistry 39:45–47CrossRefGoogle Scholar
  16. Al-Karaki G, Hammad R (2001) Mycorrhizal influence on fruit yield and mineral content of tomato grown under salt stress. J Plant Nutr 24:1311–1323CrossRefGoogle Scholar
  17. Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53:1331–1341PubMedCrossRefGoogle Scholar
  18. Aroca R, Porcel R, Ruiz-Lozano JM (2007) How does Arbuscular mycorrhizal symbiosis regulate root hydraulic properties and plasma membrane aquaporins in Phaseolus vulgaris under drought, cold or salinity stresses? New Phytol 173:808–816PubMedPubMedCentralCrossRefGoogle Scholar
  19. Aroca R, Ruiz-Lozano JM, Zamarreno AM, Paz JA, García-Mina JM, Pozo MJ, López-Ráez JA (2013) Arbuscular mycorrhizal symbiosis influences strigolactone production under salinity and alleviates salt stress in lettuce plants. J Plant Physiol 170:47–55PubMedPubMedCentralCrossRefGoogle Scholar
  20. Asghari HR, Marschner P, Smith SE, Smith FA (2005) Growth response of Atriplex nummularia to inoculation with arbuscular mycorrhizal fungi at different salinity levels. Plant Soil 273:245–256CrossRefGoogle Scholar
  21. Ashraf M (1994) Breeding for salinity tolerance in plants. Crit Rev Plant Sci 13:17–42CrossRefGoogle Scholar
  22. Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:207–216CrossRefGoogle Scholar
  23. Awad N, Turky A, Abdelhamid M, Attia M (2012) Ameliorate of environmental salt stress on the growth of Zea mays L plants by exopolysaccharides producing bacteria. J Appl Sci Res 8:2033–2044Google Scholar
  24. Bach E, dos Santos Seger GD, de Carvalho Fernandes G, Lisboa BB, Passaglia LMP (2016) Evaluation of biological control and rhizosphere competence of plant growth promoting bacteria. Appl Soil Ecol 99:141–149CrossRefGoogle Scholar
  25. Bago B, Pfeffer PE, Shachar-Hill Y (2000) Carbon metabolism and transport in arbuscular mycorrhiza. Plant Physiol 124:949–958PubMedPubMedCentralCrossRefGoogle Scholar
  26. Bargaz A, Nassar RMA, Rady MM, Gaballah MS, Thompson SM, Brestic M, Schmidhalter U, Abdelhamid MT (2016) Improved salinity tolerance by phosphorus fertilizer in two Phaseolus vulgaris recombinant inbred lines contrasting in their phosphorus deficiency sensitivity. J Agron Crop Sci 202:497–507CrossRefGoogle Scholar
  27. Basu S, Rabara RC, Negi S (2018) AMF: the future prospect for sustainable agriculture. Physiol Mol Plant Path 102:36–45CrossRefGoogle Scholar
  28. Bekheta MA, Abdelhamid MT, El-Morsi AA (2009) Physiological response of Vicia faba to prohexadione–calcium under saline conditions. Planta Daninha 27:769–779CrossRefGoogle Scholar
  29. Bharti N, Barnawal D, Awasthi A, Yadav A, Kalra A (2014) Plant growth promoting rhizobacteria alleviate salinity induced negative effects on growth, oil content and physiological status in Mentha arvensis. Acta Physiol Plant 36:45–60CrossRefGoogle Scholar
  30. Bockheim JG, Gennadiyev AN (2000) The role of soil-forming processes in the definition of taxa in soil taxonomy and the world soil reference base. Geoderma 95:53–72CrossRefGoogle Scholar
  31. Borde MY, Dudhane MP, Jite PK (2010) AM fungi influences the photosynthetic activity, growth and antioxidant enzymes in Allium sativum L. under salinity condition. Not Sci Biol 2:64–71CrossRefGoogle Scholar
  32. Borde MY, Dudhane MP, Jite PK (2011) Growth photosynthetic activity and antioxidant responses of mycorrhizal and non-mycorrhizal bajra (Pennisetum glaucum) crop under salinity stress condition. Crop Prot 30:265–271CrossRefGoogle Scholar
  33. Bothe H (2012) Arbuscular mycorrhiza and salt tolerance of plants. Symbiosis 58:7–16CrossRefGoogle Scholar
  34. Cantrell IC, Linderman RG (2001) Preinoculation of lettuce and onion with VA mycorrhizal fungi reduces deleterious effects of soil salinity. Plant Soil 233:269–281CrossRefGoogle Scholar
  35. Chen J, Zhang H, Zhang X, Tang M (2017) Arbuscular mycorrhizal symbiosis alleviates salt stress in black locust through improved photosynthesis, water status, and KC/NaC homeostasis. Front Plant Sci 8:1739. CrossRefPubMedPubMedCentralGoogle Scholar
  36. Colla G, Rouphael Y, Cardarelli M, Tullio M, Rivera CM, Rea E (2008) Alleviation of salt stress by arbuscular mycorrhizal in zucchini plants grown at low and high phosphorus concentration. Biol Fertil Soils 44:501–509CrossRefGoogle Scholar
  37. Das P, Nutan KK, Singla-Pareek SL, Pareek A (2015) Understanding salinity responses and adopting “omics-based” approaches to generate salinity tolerant cultivars of rice. Front Plant Sci 6:712. CrossRefPubMedPubMedCentralGoogle Scholar
  38. Datta P, Kulkarni M (2014) Arbuscular mycorrhizal colonization enhances biochemical status in and mitigates adverse salt effect on two legumes. Not Sci Biol 6:381–393CrossRefGoogle Scholar
  39. Dawood MG, Taie HAA, Nassar RMA, Abdelhamid MT, Schmidhalter U (2014a) The changes induced in the physiological, biochemical and anatomical structure of Vicia faba by the exogenous application of proline under seawater stress. S Afr J Bot 93:54–63CrossRefGoogle Scholar
  40. Dawood MG, Abdelhamid MT, Schmidhalter U (2014b) Potassium fertiliser enhances the salt-tolerance of common bean (Phaseolus vulgaris L.). J Hortic Sci Biotech 89:185–192CrossRefGoogle Scholar
  41. Dawood MG, El-Metwally IM, Abdelhamid MT (2016) Physiological response of lupine and associated weeds grown at salt-affected soil to α-tocopherol and hoeing treatments. Gesunde Pflanzen 68:117–127CrossRefGoogle Scholar
  42. De Oliveira DFB, Endres L, Silva JV, Clemente PRA (2017) Pre-colonized seedlings with arbuscular mycorrhizal fungi: an alternative for the cultivation of Jatropha curcas L. in salinized soils. Theor Exp Plant Physiol 29:129–142CrossRefGoogle Scholar
  43. Elhindi K, Sharaf El Din A, Abdel-Salam E, Elgorban A (2016) Amelioration of salinity stress in different basil (Ocimum basilicum L.) varieties by vesicular arbuscular mycorrhizal fungi. Acta Agric Scand B Soil Plant Sci 66:583–592Google Scholar
  44. Elhindi KM, Sharaf El-Din A, Elgorban AM (2017) The impact of arbuscular mycorrhizal fungi in mitigating salt-induced adverse effects in sweet basil (Ocimum basilicum L.). Saudi J Biol Sci 24:170–179PubMedCrossRefGoogle Scholar
  45. El-Lethy SR, Abdelhamid MT, Reda F (2013) Effect of potassium application on wheat (Triticum aestivum L.) cultivars grown under salinity stress. World Appl Sci J 26:840–850Google Scholar
  46. Ellis J (2017) Can plant microbiome studies lead to effective biocontrol of plant diseases? Mol Plant Microbe. PubMedCrossRefGoogle Scholar
  47. El-Mashad AAA, Mohamed HI (2012) Brassinolide alleviates salt stress and increases antioxidant activity of cowpea plants (Vigna sinensis). Protoplasma 249:625–635CrossRefGoogle Scholar
  48. El-Metwally IM, Ali OAM, Abdelhamid MT (2015) Response of wheat (Triticum aestivum L.) and associated grassy weeds grown in salt-affected soil to effects of graminicides and indole acetic acid. Agriculture 61:1–11Google Scholar
  49. Epstein E (1977) Genetic potentials for solving problems of soil mineral stress: adaptation of crops to salinity. In: Wright MJ (ed) Plant adaptation to mineral stress in problem soils. Cornell University, Ithaca, pp 73–123Google Scholar
  50. Errakhi R, Bouteau F, Barakate M, Lebrihi A (2016) Isolation and characterization of antibiotics produced by Streptomyces J-2 and their role in biocontrol of plant diseases, especially grey mould. In: Compant S, Mathieu F (eds) Biocontrol of major grapevine diseases: leading research. CAB International, Wallingford, pp 76–83CrossRefGoogle Scholar
  51. Estrada B, Aroca R, Maathuis FJ, Barea JM, Ruiz-Lozano JM (2013) Arbuscular mycorrhizal fungi native from a Mediterranean saline area enhance maize tolerance to salinity through improved ion homeostasis. Plant Cell Environ 36:1771–1782PubMedCrossRefGoogle Scholar
  52. Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1280PubMedPubMedCentralCrossRefGoogle Scholar
  53. Evelin H, Giri B, Kapoor R (2012) Contribution of Glomus intraradices inoculation to nutrient acquisition and mitigation of ionic imbalance in NaCl-stressed Trigonella foenum-graecum. Mycorrhiza 22:203–217PubMedPubMedCentralCrossRefGoogle Scholar
  54. Fan X, Chang W, Fenga F, Song F (2018) Responses of photosynthesis-related parameters and chloroplast ultrastructure to atrazine in alfalfa (Medicago sativa L.) inoculated with arbuscular mycorrhizal fungi. Ecotoxicol Environ Saf 166:102–108PubMedCrossRefGoogle Scholar
  55. Feng G, Zhang FS, Li XL, Tian CY, Tang C, Rengel Z (2002) Improved tolerance of maize plants to salt stress by arbuscular mycorrhiza is related to higher accumulation of soluble sugars in roots. Mycorrhiza 12:185–190CrossRefPubMedPubMedCentralGoogle Scholar
  56. Fileccia V, Ruisi P, Ingraffia R, Giambalvo D, Frenda AS, Martinelli F (2017) Arbuscular mycorrhizal symbiosis mitigates the negative effects of salinity on durum wheat. PLoS One 12(9):e0184158. CrossRefPubMedPubMedCentralGoogle Scholar
  57. Flowers TJ, Colmer TD (2015) Plant salt tolerance: adaptations in halophytes. Ann Bot 115:327–331PubMedPubMedCentralCrossRefGoogle Scholar
  58. Garg N, Bhandari P (2016) Silicon nutrition and mycorrhizal inoculations improve growth, nutrient status, K+/Na+ ratio and yield of Cicer arietinum L. genotypes under salinity stress. Plant Growth Regul 78:371–387CrossRefGoogle Scholar
  59. Garg N, Manchanda G (2009) Role of arbuscular mycorrhizae in the alleviation of ionic, osmotic and oxidative stresses induced by Mycorrhiza salinity in Cajanus cajan (L.) Millsp. (pigeonpea). J Agron Crop Sci 195:110–123CrossRefGoogle Scholar
  60. Garg N, Singla P (2016) Stimulation of nitrogen fixation and trehalose biosynthesis by naringenin (Nar) and arbuscular mycorrhiza (AM) in chickpea under salinity stress. Plant Growth Regul 80:5–22CrossRefGoogle Scholar
  61. Gharsallah C, Fakhfakh H, Grubb D, Gorsane F (2016) Effect of salt stress on ion concentration, proline content, antioxidant enzyme activities and gene expression in tomato cultivars. AoB Plants. PubMedPubMedCentralCrossRefGoogle Scholar
  62. Ghorbanli H, Ebrahimzadeh M, Sharifi M (2004) Effects of NaCl and mycorrhizal fungi on antioxidative enzymes in soybean. Biol Plant 48:575–581CrossRefGoogle Scholar
  63. Gianinazzi S, Gollotte A, Binet M, van Tuinen D, Redecker D, Wipf D (2010) Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20:519–530PubMedCrossRefGoogle Scholar
  64. Giri B, Mukerji KG (2004) Mycorrhizal inoculants alleviate salt stress in Sesbania aegyptiaca and Sesbania grandiflora under field conditions: evidence for reduced sodium and improved magnesium uptake. Mycorrhiza 14:307–312PubMedPubMedCentralCrossRefGoogle Scholar
  65. Giri B, Kapoor R, Mukerji KG (2007) Improved tolerance of Acacia nilotica to salt stress by arbuscular mycorrhiza, Glomus fasciculatum may be partly related to elevated K/Na ratios in root and shoot tissues. Microb Ecol 54:753–760CrossRefPubMedPubMedCentralGoogle Scholar
  66. Gopal S, Chandrasekaran M, Shagol C, Kim K, Sa T (2012) Spore associated bacteria (SAB) of arbuscular mycorrhizal fungi (AMF) and plant growth promoting rhizobacteria (PGPR) increase nutrient uptake and plant growth under stress conditions. Korean J Soil Sci Fertil 45:582–592CrossRefGoogle Scholar
  67. Grieve CM, Grattan SR, Maas EV (2008) Plant salt tolerance. In: Wallender WW, Tanj KK (eds) Agricultural salinity assessment and management. American Society of Civil Engineers, Reston, pp 405–459Google Scholar
  68. Gupta ML, Khaliq A, Pandey R, Shukla RS, Singh HK, Kumar S (2000) Vesicular–arbuscular mycorrhizal fungi associated with Ocimum spp. J Herbs Spices Med Plants 7:57–63CrossRefGoogle Scholar
  69. Haas D, Défago G (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat Rev Microbiol 3:307–319PubMedCrossRefGoogle Scholar
  70. Haghighi M, Mohammadnia S, Attai Z, Pessarakli M (2017) Effects of mycorrhiza inoculation on cucumber growth irrigated with saline water. J Plant Nutr 40:128–137CrossRefGoogle Scholar
  71. Hajiboland R, Joudmand A, Fotouhi K (2009) The K/Na replacement and function of antioxidant defense system in sugar beet (Beta vulgaris L.) cultivars. Acta Agric Scand B Soil Plant Sci 59:246–259Google Scholar
  72. Hajiboland R, Aliasgharzadeh S, Laiegh F, Poschenrieder C (2010) Colonization with arbuscular mycorrhizal fungi improves salinity tolerance of tomato (Solanum lycopersicum L.) plants. Plant Soil 331:313–327CrossRefGoogle Scholar
  73. Hameed A, Egamberdieva D, Abd Allah EF, Hashem A, Kumar A, Ahmad P (2014) Salinity stress and arbuscular mycorrhizal symbiosis in plants. In: Miransari M (ed) Use of microbes for the alleviation of soil stresses, vol 1. Springer, New York, pp 139–159CrossRefGoogle Scholar
  74. Hammer EC, Nasr H, Pallon J, Olsson PA, Wallander H (2011) Elemental composition of arbuscular mycorrhizal fungi at high salinity. Mycorrhiza 21:117–129CrossRefGoogle Scholar
  75. Hanin M, Ebel C, Ngom M, Laplaze L, Masmoudi K (2016) New insights on plant salt tolerance mechanisms and their potential use for breeding. Front Plant Sci 7:1787. CrossRefPubMedPubMedCentralGoogle Scholar
  76. Hashem A, Abd_Allah EF, Alqarawi AA, Wirth S, Egamberdieva D (2016a) Arbuscular mycorrhizal fungi alleviate salt stress in lupine (Lupinus termis Forsik) through modulation of antioxidant defense systems and physiological traits. Legume Res 39:198–207Google Scholar
  77. Hashem AEF, Abd_Allah EF, Alqarawi AA, Al-Huqail AA, Shah MA (2016b) Induction of osmoregulation and modulation of salt stress in Acacia gerrardii Benth. by arbuscular mycorrhizal fungi and Bacillus subtilis (BERA 71). BioMed Res Int 2016, 6294098, 11 p. CrossRefGoogle Scholar
  78. Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments: a review. Plant Signal Behav 7:1456–1466PubMedPubMedCentralCrossRefGoogle Scholar
  79. He Z, He C, Zhang Z, Zou Z, Wang H (2007) Changes of antioxidative enzymes and cell membrane osmosis in tomato colonized by arbuscular mycorrhizae under NaCl stress. Colloids Surf B Biointerfaces 59:128–133PubMedCrossRefGoogle Scholar
  80. Hegazi AM, El-Shraiy AM, Ghoname AA (2017) Mitigation of salt stress negative effects on sweet pepper using arbuscular mycorrhizal fungi (AMF), Bacillus megaterium and Brassinosteroids (BRs). Gesunde Pflanzen 69:91–102CrossRefGoogle Scholar
  81. Hellal FA, Abdelhameid MT, Abo-Basha DM, Zewainy RM (2012) Alleviation of the adverse effects of soil salinity stress by foliar application of silicon on faba bean (Vicia faba L.). J Appl Sci Res 8:4428–4433Google Scholar
  82. Hernandez JA, Olmos E, Corpas FJ, Sevilla F, Delrio LA (1995) Salt induced oxidative stress in chloroplast of pea plants. Plant Sci 105:151–167CrossRefGoogle Scholar
  83. Ismail AM, Horie T (2017) Genomics, physiology, and molecular breeding approaches for improving salt tolerance. Annu Rev Plant Biol 68:405–434. CrossRefPubMedGoogle Scholar
  84. Jahromi F, Aroca R, Porcel R, Ruiz-Lozano JM (2008) Influence of salinity on the in vitro development of Glomus intraradices and on the in vivo physiological and molecular responses of mycorrhizal lettuce plants. Microb Ecol 55:45–53CrossRefPubMedPubMedCentralGoogle Scholar
  85. Jiang M, Zhang J (2002) Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize-leaves. J Exp Bot 53:2401–2410PubMedCrossRefGoogle Scholar
  86. Kaya C, Ashraf M, Sonmez O, Aydemir S, Tuna AL, Cullu MA (2009) The influence of arbuscular mycorrhizal colonization on key growth parameters and fruit yield of pepper plants grown at high salinity. Sci Hortic 121:1–6CrossRefGoogle Scholar
  87. Khalloufia M, Martínez-Andújara C, Lachaâlb M, Karray-Bouraouib N, Pérez-Alfoceaa F, Albacete A (2017) The interaction between foliar GA3 application and arbuscular mycorrhizal fungi inoculation improves growth in salinized tomato (Solanum lycopersicum L.) plants by modifying the hormonal balance. J Plant Physiol 214:134–144CrossRefGoogle Scholar
  88. Khan S, Hanjra MA (2008) Sustainable land and water management policies and practices: a pathway to environmental sustainability in large irrigation systems. Land Degrad Dev 19:469–487CrossRefGoogle Scholar
  89. Kingsbury RW, Epstein E (1984) Selection for salt resistant spring wheat. Crop Sci 24:310–315CrossRefGoogle Scholar
  90. Kishor PBK, Hong Z, Miao GH, Hu CAA, Verma DPS (1995) Over expression of Δ1-pyrroline-5-carboxylate synthetase increase proline production and confers osmotolerance in transgenic plants. Plant Physiol 108:1387–1394PubMedPubMedCentralCrossRefGoogle Scholar
  91. Kohler J, Hernández JA, Caravaca F, Roldan A (2009) 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 65:245–252CrossRefGoogle Scholar
  92. Kour D, Rana KL, Verma P, Yadav AN, Kumar V, Dhaliwal HS (2017) Biofertilizers: eco-friendly technologies and bioresources for sustainable agriculture. In: Proceeding of international conference on innovative research in engineering science and technology, IREST/PP/014Google Scholar
  93. Landi S, Hausman J-F, Guerriero G, Esposito S (2017) Poaceae vs. abiotic stress: focus on drought and salt stress, recent insights and perspectives. Front Plant Sci 8:1214. CrossRefPubMedPubMedCentralGoogle Scholar
  94. Lin J, Wang Y, Sun S, Mu C, Yan X (2017) Effects of arbuscular mycorrhizal fungi on the growth, photosynthesis and photosynthetic pigments of Leymus chinensis seedlings under salt-alkali stress and nitrogen deposition. Sci Total Environ 576:234–241PubMedCrossRefGoogle Scholar
  95. Liu S, Guo X, Feng G, Maimaitiaili B, Fan J, He X (2016) Indigenous arbuscular mycorrhizal fungi can alleviate salt stress and promote growth of cotton and maize in saline fields. Plant Soil 398:195–206CrossRefGoogle Scholar
  96. Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158CrossRefGoogle Scholar
  97. Manchanda G, Garg N (2007) Endomycorrhizal and rhizobial symbiosis: how much do they share? J Plant Interact 2:79–88CrossRefGoogle Scholar
  98. Mardukhi B, Rejali F, Daei G, Ardakani M, Malakouti MJ, Miransari M (2015) Mineral uptake of mycorrhizal wheat (Triticum aestivum L.) under salinity stress. Commun Soil Sci Plant Anal 46:343–357CrossRefGoogle Scholar
  99. Mehdy MC (1994) Active oxygen species in plant defense against pathogens. Plant Physiol 105:467–472PubMedPubMedCentralCrossRefGoogle Scholar
  100. Metternicht GI, Zinck JA (2003) Remote sensing of soil salinity: potentials and constraints. Remote Sens Environ 85:1–20CrossRefGoogle Scholar
  101. Metwally RA, Abdelhameed RE (2018) Synergistic effect of arbuscular mycorrhizal fungi on growth and physiology of salt-stressed Trigonella foenum-graecum plants. Biocatal Agric Biotechnol 16:538–544CrossRefGoogle Scholar
  102. Miransari M (2010) Contribution of arbuscular mycorrhizal symbiosis to plant growth under different types of soil stress. Plant Biol 12:563–569PubMedPubMedCentralGoogle Scholar
  103. Miransari M, Bahrami H, Rejali F, Malakouti M (2008) Using arbuscular mycorrhiza to alleviate the stress of soil compaction on wheat (Triticum aestivum L.) growth. Soil Biol Biochem 40:1197–1206CrossRefGoogle Scholar
  104. Munns R (2005) Genes and salt tolerance: bringing them together. New Phytol 167:645–663PubMedPubMedCentralCrossRefGoogle Scholar
  105. Munns R, Gilliham M (2015) Salinity tolerance of crops—what is the cost? New Phytol 208:668–673PubMedPubMedCentralCrossRefGoogle Scholar
  106. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681PubMedPubMedCentralCrossRefGoogle Scholar
  107. Munns R, James RA, Läuchli A (2006) Approaches to increasing the salt tolerance of wheat and other cereals. J Exp Bot 57:1025–1043PubMedCrossRefGoogle Scholar
  108. Namdari A, Arani AB, Moradi A (2018) Arbuscular mycorrhizal (Funneliformis mosseae) improves alfalfa (Medicago sativa L.) re-growth ability in saline soil through enhanced nitrogen remobilization and improved nutritional balance. J Cent Eur Agri 19:166–183CrossRefGoogle Scholar
  109. Negrão S, Schmöckel SM, Tester M (2017) Evaluating physiological responses of plants to salinity stress. Ann Bot 119:1–11PubMedCrossRefPubMedCentralGoogle Scholar
  110. Nongpiur RC, Singla-Pareek SL, Pareek A (2016) Genomics approaches for improving salinity stress tolerance in crop plants. Curr Genomics 17:343–357PubMedPubMedCentralCrossRefGoogle Scholar
  111. Nunez M, Mazzafera P, Mazorra LM, Siqueira WJ, Zullo MAT (2003) Influence of brassinosteroid analogue on antioxidant enzymes in rice grown in culture medium with NaCl. Biol Plant 47:67–70CrossRefGoogle Scholar
  112. Orabi SA, Abdelhamid MT (2016) Protective role of α-tocopherol on two Vicia faba cultivars against seawater-induced lipid peroxidation by enhancing capacity of anti-oxidative system. J Saudi Soc Agric Sci 15:145–154Google Scholar
  113. Ouda S, Noreldin T, Mounzer O, Abdelhamid MT (2015) CropSyst model for wheat irrigation water management with fresh and poor quality water. J Water Land Devel 27:41–50CrossRefGoogle Scholar
  114. Pal KK, Gardener BM (2006) Biological control of plant pathogens. Plant Health Instructor 2:1117–1142Google Scholar
  115. Pandey R, Garg N (2017) High effectiveness of Rhizophagus irregularis is linked to superior modulation of antioxidant defence mechanisms in Cajanus cajan (L.) Millsp. genotypes grown under salinity stress. Mycorrhiza 27:669–682PubMedCrossRefGoogle Scholar
  116. Pankievicz V, Amaral FP, Santos KF, Agtuca B, Xu Y, Schueller MJ, Arisi ACM, Steffens M, Souza EM, Pedrosa FO (2015) Robust biological nitrogen fixation in a model grass–bacterial association. Plant J 81:907–919PubMedCrossRefGoogle Scholar
  117. Parida SK, Das AB (2005) Salt tolerance and salinity effects on plants. Ecotoxicol Environ Saf 60:324–349CrossRefGoogle Scholar
  118. Patel D, Saraf M (2013) Influence of soil ameliorants and microflora on induction of antioxidant enzymes and growth promotion of Jatropha curcas L. under saline condition. Eur J Soil Biol 55:47–54CrossRefGoogle Scholar
  119. Pollastri S, Savvides A, Pesando M, Lumini E, Volpe MG, Ozudogru EA, Faccio A, De Cunzo F, Michelozzi M, Lambardi M, Fotopoulos V, Loreto F, Centritto M, Balestrini R (2018) Impact of two arbuscular mycorrhizal fungi on Arundo donax L. response to salt stress. Planta 247:573–585PubMedCrossRefGoogle Scholar
  120. Porcel R, Aroca R, Ruiz-Lozano JM (2012) Salinity stress alleviation using arbuscular mycorrhizal fungi. A review. Agron Sustain Dev 32:181–200CrossRefGoogle Scholar
  121. Porcel R, Aroca R, Azcon R, Ruiz-Lozano JM (2016) Regulation of cation transporter genes by the arbuscular mycorrhizal symbiosis in rice plants subjected to salinity suggests improved salt tolerance due to reduced Na+ root-to-shoot distribution. Mycorrhiza 26:673–684CrossRefPubMedPubMedCentralGoogle Scholar
  122. Prasad R, Bhola D, Akdi K, Cruz C, Sairam KVSS, Tuteja N, Varma A (2017) Introduction to mycorrhiza: historical development. In: Varma A, Prasad R, Tuteja N (eds) Mycorrhiza. Springer, Cham, pp 1–7Google Scholar
  123. Qadir M, Quillérou E, Nangia V, Murtaza G, Singh M, Thomas RJ, Drechsel P, Noble AD (2014) Economics of salt-induced land degradation and restoration. Nat Resour Forum 38:282–295CrossRefGoogle Scholar
  124. Rabie GH (2005) Influence of arbuscular mycorrhizal fungi and kinetin on the response of mungbean plants to irrigation with seawater. Mycorrhiza 15:225–230PubMedCrossRefGoogle Scholar
  125. Rabie GH, Almadini AM (2005) Role of bioinoculants in development of salt-tolerance of Vicia faba plants under salinity stress. Afr J Biotechnol 4:210–220Google Scholar
  126. Rady MM, Sadak MS, El-Lethy SR, Abdelhamid EM, Abdelhamid MT (2015) Exogenous α-tocopherol has a beneficial effect on Glycine max (L.) plants irrigated with diluted sea water. J Hortic Sci Biotech 90:195–202CrossRefGoogle Scholar
  127. Rady MM, Semida WM, Hemida KA, Abdelhamid MT (2016a) The effect of compost on growth and yield of Phaseolus vulgaris plants grown under saline soil. Int J Recycl Org Waste Agr 5:311–321CrossRefGoogle Scholar
  128. Rady MM, Mounzer OH, Alarcón JJ, Abdelhamid MT, Howladar SM (2016b) Growth, heavy metal status and yield of salt-stressed wheat (Triticum aestivum L.) plants as affected by the integrated application of bio-, organic and inorganic nitrogen-fertilizers. J Appl Bot Food Qual 89:21–28Google Scholar
  129. Rai MK, Kalia RK, Singh R, Gangola MP, Dhawan AK (2011) Developing stress tolerant plants through in vitro selection – an overview of the recent progress. Environ Exp Bot 71:89–98CrossRefGoogle Scholar
  130. Ramos AC, Facanha AR, Palma LM, Okorokov LA, Cruz ZMA, Silva AG (2011) An outlook on ion signaling and ionome of mycorrhizal symbiosis. Braz J Plant Physiol 23:79–89CrossRefGoogle Scholar
  131. Renault S (2012) Salinity tolerance of Cornus sericea seedlings from three provenances. Acta Physiol Plant 34:1735–1746CrossRefGoogle Scholar
  132. Rivero J, Alvarez D, Flors V, Azcón-Aguilar C, Pozo MJ (2018) Root metabolic plasticity underlies functional diversity in mycorrhiza-enhanced stress tolerance in tomato. New Phytol 220:1322–1336. CrossRefPubMedGoogle Scholar
  133. Roberts JKM, Linker CS, Benoit AG, Jardetzky O, Nieman RH (1984) Salt Stimulation of Phosphate Uptake in Maize Root Tips Studied by 31P Nuclear Magnetic Resonance. Plant Physiol 75:947–950PubMedPubMedCentralCrossRefGoogle Scholar
  134. Roy SJ, Negrão S, Tester M et al (2014) Salt resistant crop plants. Curr Opin Biotechnol 26:115–124. CrossRefPubMedPubMedCentralGoogle Scholar
  135. Ruiz-Lozano JM, Azcon R (1995) Hyphal contribution to water uptake in mycorrhizal plants as affected by the fungal species and water status. Physiol Plant 95:472–478CrossRefGoogle Scholar
  136. Sadak MS, Abdelhamid MT (2015) Influence of amino acids mixture application on some biochemical aspects, antioxidant enzymes and endogenous polyamines of Vicia faba plant grown under seawater salinity stress. Gesunde Pflanzen 67:119–129CrossRefGoogle Scholar
  137. Sadak MSH, Abdelhamid MT, Schmidhalter U (2015) Effect of foliar application of amino acids on plant yield and physiological parameters in bean plants irrigated with seawater. Acta Biolo Colomb 20:141–152CrossRefGoogle Scholar
  138. Sallakua G, Sandén H, Babaj I, Kaciu S, Balliu A, Rewald B (2019) Specific nutrient absorption rates of transplanted cucumber seedlings are highly related to RGR and influenced by grafting method, AMF inoculation and salinity. Sci Hortic 243:177–188CrossRefGoogle Scholar
  139. Sanchez FJ, Manzanares M, De Andres EF, Tenorio JL, Ayerbe L (1998) Turgor maintenance, osmotic adjustment and soluble sugar and proline accumulation in 49 pea cultivars in response to water stress. Field Crop Res 59:225–235CrossRefGoogle Scholar
  140. Sannazzaro AI, Echeverria M, Alberto EO, Ruiz OA, Menendez AB (2007) Modulation of polyamine balance in Lotus glaber by salinity and arbuscular mycorrhiza. Plant Physiol Biochem 45:39–46PubMedPubMedCentralCrossRefGoogle Scholar
  141. Satir NY, Ortas I, Satir O (2016) The influence of mycorrhizal species on sour orange (Citrus aurantium L.) growth under saline soil conditions. Pak J Agri Sci 53:399–406Google Scholar
  142. Saxena B, Shukla K, Giri B (2017) Arbuscular mycorrhizal fungi and tolerance of salt stress in plants. In: Wu Q-S (ed) Arbuscular mycorrhizas and stress tolerance of plants. Springer Nature, Singapore, pp 67–97CrossRefGoogle Scholar
  143. Schubler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421CrossRefGoogle Scholar
  144. Semida WM, Taha RS, Abdelhamid MT, Rady MM (2014) Foliar-applied α-tocopherol enhances salt-tolerance in Vicia faba L. plants grown under saline conditions. S Afr J Bot 95:24–31CrossRefGoogle Scholar
  145. Serrano R, Rodriguez-Navarro A (2001) Ion homeostasis during salt stress in plants. Curr Opin Cell Biol 13:399–404PubMedCrossRefGoogle Scholar
  146. Sharifi M, Ghorbanli M, Ebrahimzadeh H (2007) Improved growth of salinity-stressed soybean after inoculation with pre-treated mycorrhizal fungi. J Plant Physiol 164:1144–1151PubMedPubMedCentralCrossRefGoogle Scholar
  147. Shekoofeh E, Sepideh H, Roya R (2012) Role of mycorrhizal fungi and salicylic acid in salinity tolerance of Ocimum basilicum resistance to salinity. Afr J Biotechnol 11:2223–2235Google Scholar
  148. Sheng M, Tang M, Chan H, Yang B, Zhang F, Huang Y (2008) Influence of arbuscular mycorrhizae on photosynthesis and water status of maize plants under salt stress. Mycorrhiza 18:287–296PubMedPubMedCentralCrossRefGoogle Scholar
  149. Sheng M, Tang M, Zhang F, Huang Y (2011) Influence of arbuscular mycorrhiza on organic solutes in maize leaves under salt stress. Mycorrhiza 21:423–430PubMedPubMedCentralCrossRefGoogle Scholar
  150. Shokri S, Maadi B (2009) Effects of arbuscular mycorrhizal fungus on the mineral nutrition and yield of Trifolium alexandrinum plants under salinity stress. J Agron 8:79–83CrossRefGoogle Scholar
  151. Singh RP, Choudhary A, Gulati A, Dahiya HC, Jaiwal PK, Sengar RS (1997) Response of plants to salinity in interaction with other abiotic and biotic factors. In: Jaiwal PK, Singh RP, Gulati A (eds) Strategies for improving salt tolerance in higher plants. Science, Enfield, pp 25–39Google Scholar
  152. Talaat NB, Shawky BT (2012) 24-Epibrassinolide ameliorates the saline stress and improves the productivity of wheat (Triticum aestivum L.). Environ Exp Bot 82:80–88CrossRefGoogle Scholar
  153. Talaat NB, Ghoniem AE, Abdelhamid MT, Shawky BT (2015) Effective microorganisms improve growth performance, alter nutrients acquisition and induce compatible solutes accumulation in common bean (Phaseolus vulgaris L.) plants subjected to salinity stress. Plant Growth Regul 75:281–295CrossRefGoogle Scholar
  154. Tofighi C, Khavari-Nejad RA, Najafi F, Razavi K, Rejali F (2017) Brassinosteroid (BR) and arbuscular mycorrhizal (AM) fungi alleviate salinity in wheat. J Plant Nutr 40:1091–1098CrossRefGoogle Scholar
  155. Tomar NS, Agarwal RM (2013) Influence of treatment of Jatropha curcas L. leachates and potassium on growth and phytochemical constituents of wheat (Triticum aestivum L.). Am J Plant Sci 4:1134–1150CrossRefGoogle Scholar
  156. Upreti KK, Bhatt RM, Panneerselvam P, Varalakshmi LR (2016) Morpho-physiological responses of grape rootstock ‘Dogridge’ to arbuscular mycorrhizal fungi inoculation under salinity stress. Int J Fruit Sci 16:191–209CrossRefGoogle Scholar
  157. Van Breusegem F, Vranova E, Dat JF, Inze (2001) The role of active oxygen species in plant signal transduction. Plant Sci 161:405–414CrossRefGoogle Scholar
  158. Verma P, Yadav A, Khannam K, Panjiar N, Kumar S, Saxena A, Suman A (2015) Assessment of genetic diversity and plant growth promoting attributes of psychrotolerant bacteria allied with wheat (Triticum aestivum) from the northern hills zone of India. Ann Microbiol 65:1885–1899CrossRefGoogle Scholar
  159. Wang Y, Wang M, Li Y, Wu A, Huang J (2018) Effects of arbuscular mycorrhizal fungi on growth and nitrogen uptake of Chrysanthemum morifolium under salt stress. PLoS One 13(4):e0196408. CrossRefPubMedPubMedCentralGoogle Scholar
  160. Wu QS, Zou YN, He XH (2010) Contributions of arbuscular mycorrhizal fungi to growth, photosynthesis, root morphology and ionic balance of citrus seedlings under salt stress. Acta Physiol Plant 32:297–304CrossRefGoogle Scholar
  161. Yadav AN, Kumar R, Kumar S, Kumar V, Sugitha TCK, Singh B, Chauhan VS, Dhaliwal HS, Saxena AK (2017a) Beneficial microbiomes: biodiversity and potential biotechnological applications for sustainable agriculture and human health. J Appl Biol Biotechnol 5:45–57Google Scholar
  162. Yadav AN, Verma P, Kumar S, Kumar V, Kumar M, Singh BP, Saxena AK, Dhaliwal HS (2017b) Actinobacteria from rhizosphere: molecular diversity, distributions and potential biotechnological applications. In: Singh BP, Gupta VK, Passari AK (eds) New and future developments in microbial biotechnology and bioengineering actinobacteria: diversity and biotechnological applications. Elsevier, Atlanta, pp 13–41Google Scholar
  163. Yadav AN, Verma P, Kour D, Rana KL, Kumar V, Singh B, Chauhan VS, Sugitha TCK, Saxena AK, Dhaliwal HS (2017c) Plant microbiomes and its beneficial multifunctional plant growth promoting attributes. Int J Environ Sci Nat Resour 3:1–8Google Scholar
  164. Yamato M, Ikeda S, Iwase K (2008) Community of arbuscular mycorrhizal fungi in coastal vegetation on Okinawa Island and effect of the isolated fungi on growth of sorghum under salt-treated conditions. Mycorrhiza 18:241–249PubMedPubMedCentralCrossRefGoogle Scholar
  165. Yano-Melo AM, Saggin OJ, Maia LC (2003) Tolerance of mycorrhized banana (Musa sp. cv. Pacovan) plantlets to saline stress. Agric Ecosyst Environ 95:343–348CrossRefGoogle Scholar
  166. Yoshiba Y, Kiyosue T, Katagiri T, Ueda H, Mizoguchi T, Yamaguchishinozaki K, Wada K, Harada Y, Shinozaki K (1995) Correlation between the induction of a gene for delta (1)- pyrroline-5-carboxylate synthetase and the accumulation of proline in Arabidopsis thaliana under osmotic stress. Plant J 7:751–760PubMedPubMedCentralCrossRefGoogle Scholar
  167. Zhang Y, Wang P, Wu Q-H, Zou Y-N, Bao Q, Wu Q-S (2017) Arbuscular mycorrhizas improve plant growth and soil structure in trifoliate orange under salt stress. Arch Agron Soil Sci 63:491–500CrossRefGoogle Scholar
  168. Zhang W, Wang C, Lu T, Zheng Y (2018) Cooperation between arbuscular mycorrhizal fungi and earthworms promotes the physiological adaptation of maize under a high salt stress. Plant Soil 423:125–140CrossRefGoogle Scholar
  169. ZhongQun H, ChaoXing H, Zhang ZB, Zou ZR, Wang HS (2007) Changes of antioxidative enzymes and cell membrane osmosis in tomato colonized by arbuscular mycorrhizae under NaCl stress. Colloids Surf B Biointerfaces 59(2):128–133CrossRefGoogle Scholar
  170. Zhu X, Song F, Liu S, Liu F (2016) Role of arbuscular mycorrhiza in alleviating salinity stress in wheat (Triticum aestivum L.) grown under ambient and elevated CO2. J Agro Crop Sci 202:486–496CrossRefGoogle Scholar
  171. Zhu XQ, Tang M, Zhang HQ (2017) Arbuscular mycorrhizal fungi enhanced the growth, photosynthesis, and calorific value of black locust under salt stress. Photosynthetica 55:378–385CrossRefGoogle Scholar
  172. Zhu X, Cao Q, Sun L, Yang X, Yang W, Zhang H (2018) Stomatal conductance and morphology of arbuscular mycorrhizal wheat plants response to elevated CO 2and NaCl stress. Front Plant Sci 9:1363. CrossRefPubMedPubMedCentralGoogle Scholar
  173. Zuccarini P, Okurowska P (2008) Effects of mycorrhizal colonization and fertilization on growth and photosynthesis of sweet basil under salt stress. J Plant Nutr 31:497–513CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Magdi T. Abdelhamid
    • 1
  • Raafat R. El-Masry
    • 1
  • Darwish S. Darwish
    • 2
  • Mazhar M. F. Abdalla
    • 2
  • Shinya Oba
    • 3
  • Ragab Ragab
    • 4
  1. 1.Botany DepartmentNational Research CentreGizaEgypt
  2. 2.Faculty of Agriculture, Agronomy DepartmentCairo UniversityGizaEgypt
  3. 3.Faculty of Applied Biological Sciences, Plant Production Control LabGifu UniversityGifuJapan
  4. 4.Centre for Ecology and Hydrology (CEH)WallingfordUK

Personalised recommendations