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Do Mycorrhizal Fungi Enable Plants to Cope with Abiotic Stresses by Overcoming the Detrimental Effects of Salinity and Improving Drought Tolerance?

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Symbiotic Soil Microorganisms

Part of the book series: Soil Biology ((SOILBIOL,volume 60))

Abstract

Soil salinization and drought are major and growing ecological problems. They limit the productivity of crop plants cultivated on more than 20% of total agricultural lands worldwide. Global climate changes and sequences of agriculture-related management practices would induce salinity to more than 50% of the arable land by 2050. Excess salt in soil impedes plant photosynthetic processes, seed germination, and root uptake of water and nutrients such as K+. Under the same soil and climate conditions, water deficiency is also one of the serious limiting factors for plant growth and food security. Application of biological processes such as mycorrhizal fungi as inoculants provide a cost-effective long-term solution for coping with saline and drought conditions. Inoculation of mycorrhizal fungi along with certain microbial strains in salt and drought-affected soils increase root infection. Arbuscular mycorrhizal fungi (AMF) are renowned for effective scavengers of free radicals in soil thereby increasing soil parameters optimal for plant growth. The mechanism to cope with drought stress involves in AMF-enhance drought and salt tolerance through direct water and nutrient uptake via extraradical hyphae, better root system architecture, enhancement of antioxidant defense systems, and greater osmotic adjustment. Mycorrhizal colonization upregulates the expression of chloroplast genes in leaves, and genes encoding membrane transport proteins involved in K+/Na+ homeostasis in roots. Mycorrhizal inoculated seedlings exhibit high root salicylic acid concentrations and lower leaf and root jasmonic acid concentrations under salt stress. The AMF improve root hydraulic conductivity as well as the plant water status and tolerance under drought stress. Essential nutrients are also taken up through mycorrhizal hyphae and differences in P and K acquisition, transpiration, and stomatal conductance are related to mycorrhizal efficiencies of different fungi. Indigenous microorganisms may be a promising biological technology to improve plant performance and development and to alleviate salt stress damage.

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References

  • Abbas T, Rizwan M, Ali S, Adrees M, Zia-ur-Rehman M, Qayyum MF et al (2018) Effect of biochar on alleviation of cadmium toxicity in wheat (Triticum aestivum L.) grown on Cd-contaminated saline soil. Environ Sci Pollut Res 25(26):25668–25680

    Article  CAS  Google Scholar 

  • Abbaspour H, Saeidi-Sar S, Afshari H, Abdel-Wahhab MA (2012) Tolerance of mycorrhiza infected Pistachio (Pistacia vera L.) seedling to drought stress under glasshouse conditions. J Plant Physiol 169(7):704–709

    Article  CAS  Google Scholar 

  • Abdel-Salam E, Alatar A, El-Sheikh MA (2018) Inoculation with arbuscular mycorrhizal fungi alleviates harmful effects of drought stress on damask rose. Saudi J Biol Sci 25(8):1772–1780

    Article  Google Scholar 

  • Abu-Elsaoud AM, Nafady NA, Abdel-Azeem AM (2017) Arbuscular mycorrhizal strategy for zinc mycoremediation and diminished translocation to shoots and grains in wheat. PLoS One 12(11):e0188220

    Article  CAS  Google Scholar 

  • Adiku S, Renger M, Wessolek G, Facklam M, Hecht-Bucholtz C (2001) Simulation of the dry matter production and seed yield of common beans under varying soil water and salinity conditions. Agric Water Manag 47(1):55–68

    Article  Google Scholar 

  • Al-Karaki GN (1998) Benefit, cost and water-use efficiency of arbuscular mycorrhizal durum wheat grown under drought stress. Mycorrhiza 8(1):41–45

    Article  Google Scholar 

  • Al-Karaki GN (2000) Growth of mycorrhizal tomato and mineral acquisition under salt stress. Mycorrhiza 10(2):51–54

    Article  CAS  Google Scholar 

  • Al-Karaki GN, Clark RB (1999) Mycorrhizal influence on protein and lipid of durum wheat grown at different soil phosphorus levels. Mycorrhiza 9(2):97–101

    Article  CAS  Google Scholar 

  • Al-Karaki GN, Al-Raddad A, Clark RB (1998) Water stress and mycorrhizal isolate effects on growth and nutrient acquisition of wheat. J Plant Nutr 21(5):891–902

    Article  CAS  Google Scholar 

  • Al-Karaki GN, Hammad R, Rusan M (2001) Response of two tomato cultivars differing in salt tolerance to inoculation with mycorrhizal fungi under salt stress. Mycorrhiza 11(1):43–47

    Article  CAS  Google Scholar 

  • Al-Karaki G, McMichael B, Zak J (2004) Field response of wheat to arbuscular mycorrhizal fungi and drought stress. Mycorrhiza 14(4):263–269

    Article  Google Scholar 

  • Al-Khaliel AS (2010) Effect of salinity stress on mycorrhizal association and growth response of peanut infected by Glomus mosseae. Plant Soil Envir 56(7):318–324

    Article  CAS  Google Scholar 

  • Ali S, Rizwan M, Qayyum MF, Ok YS, Ibrahim M, Riaz M, Arif MS, Hafeez F, Al-Wabel MI, Shahzad AN (2017) Biochar soil amendment on alleviation of drought and salt stress in plants: a critical review. Environ Sci Pollut Res 24(14):12700–12712

    Google Scholar 

  • Allen MF (2007) Mycorrhizal fungi: highways for water and nutrients in arid soils. Vadose Zone J 6(2):291–297

    Article  Google Scholar 

  • Amanifar S, Khodabandeloo M, Fard EM, Askari MS, Ashrafi M (2019) Alleviation of salt stress and changes in glycyrrhizin accumulation by arbuscular mycorrhiza in liquorice (Glycyrrhiza glabra) grown under salinity stress. Environ Exp Bot 160:25–34

    Article  CAS  Google Scholar 

  • Amiri R, Nikbakht A, Etemadi N, Sabzalian MR (2017) Nutritional status, essential oil changes and water-use efficiency of rose geranium in response to arbuscular mycorrhizal fungi and water deficiency stress. Symbiosis 73(1):15–25

    Article  CAS  Google Scholar 

  • Aroca R, Ruiz-Lozano JM, Zamarreño ÁM, Paz JA, García-Mina JM, Pozo MJ et al (2013) Arbuscular mycorrhizal symbiosis influences strigolactone production under salinity and alleviates salt stress in lettuce plants. J Plant Physiol 170(1):47–55

    Article  CAS  Google Scholar 

  • Aroca R, Abu-Elsaoud AM, Nafady NA, Abdel-Azeem AM (2017) Arbuscular mycorrhizal strategy for zinc mycoremediation and diminished translocation to shoots and grains in wheat. PLoS One 12(11):e0188220

    Article  CAS  Google Scholar 

  • Ashok Aggarwal NK, Karishma, Neetu, Tanwar A, Gupta KK (2012) Arbuscular mycorrhizal symbiosis and alleviation of salinity stress. J Appl Natl Sci 4(1):144–155

    Article  Google Scholar 

  • Askari A, Ardakani M, Vazan S, Paknejad F, Hosseini Y (2018) The effect of mycorrhizal symbiosis and seed priming on the amount of chlorophyll index and absorption of nutrients under drought stress in sesame plant under field conditions. Appl Ecol Environ Res 16(1):335–357

    Article  Google Scholar 

  • Asrar A, Abdel-Fattah G, Elhindi K (2012) Improving growth, flower yield, and water relations of snapdragon (Antirrhinum majus L.) plants grown under well-watered and water-stress conditions using arbuscular mycorrhizal fungi. Photosynthetica 50(2):305–316

    Article  CAS  Google Scholar 

  • Atul-Nayyar A, Hamel C, Hanson K, Germida J (2009) The arbuscular mycorrhizal symbiosis links N mineralization to plant demand. Mycorrhiza 19(4):239–246

    Article  CAS  Google Scholar 

  • Auge RM (2004) Arbuscular mycorrhizae and soil/plant water relations. Can J Soil Sci 84(4):373–381

    Article  Google Scholar 

  • Bagheri V, Shamshiri MH, Shirani H, Roosta HR (2011) Effect of mycorrhizal inoculation on ecophysiological responses of pistachio plants grown under different water regimes. Photosynthetica 49(4):531–538

    Article  Google Scholar 

  • Bagheri V, Shamshiri M, Shirani H, Roosta H (2012) Nutrient uptake and distribution in mycorrhizal pistachio seedlings under drought stress. J Agric Sci Technol 14:1591–1604

    Google Scholar 

  • Bago B, Vierheilig H, Piché Y, Azcón-Aguilar C (1996) Nitrate depletion and pH changes induced by the extraradical mycelium of the arbuscular mycorrhizal fungus Glomus intraradices grown in monoxenic culture. New Phytol 133(2):273–280

    Article  CAS  Google Scholar 

  • Barea JM, Calvet C, Estaun V, Camprubi A (1996) Biological control as a key component in sustainable agriculture. Plant Soil 185(2):171–172

    Article  CAS  Google Scholar 

  • Barun Kumar Manjhi SP, Meena SK, Yadav RS, Alvina F, Singh HB, Rakshit A (2016) Mycorrhizoremediation of nickel and cadmium: a promising technology. Nat Environ Pollut Technol 15:647–652

    Google Scholar 

  • Baum C, El-Tohamy W, Gruda N (2015) Increasing the productivity and product quality of vegetable crops using arbuscular mycorrhizal fungi: a review. Sci Hortic 187:131–141

    Article  Google Scholar 

  • Bedini S, Ramasamy C, Giovannetti M (2009) Glomalin-related soil protein as an indicator of the impact of different agronomical practices on soil quality. Asp Appl Biol 98:75–80

    Google Scholar 

  • Belmondo S, Fiorilli V, Pérez-Tienda J, Ferrol N, Marmeisse R, Lanfranco L (2014) A dipeptide transporter from the arbuscular mycorrhizal fungus Rhizophagus irregularis is upregulated in the intraradical phase. Front Plant Sci 5:436

    Article  Google Scholar 

  • Bencherif K, Boutekrabt A, Fontaine J, Laruelle F, Dalpè Y, Lounès-Hadj SA (2015) Impact of soil salinity on arbuscular mycorrhizal fungi biodiversity and microflora biomass associated with Tamarix articulata Vahll rhizosphere in arid and semi-arid Algerian areas. Sci Total Environ 533:488–494

    Article  CAS  Google Scholar 

  • Benlloch-González M, Fournier JM, Benlloch M (2009) K+ deprivation induces xylem water and K+ transport in sunflower: evidence for a co-ordinated control. J Exp Bot 61(1):157–164

    Article  CAS  Google Scholar 

  • Bernardo L, Carletti P, Badeck FW, Rizza F, Morcia C, Ghizzoni R et al (2019) Metabolomic responses triggered by arbuscular mycorrhiza enhance tolerance to water stress in wheat cultivars. Plant Physiol Biochem 137:203–212

    Article  CAS  Google Scholar 

  • Berruti A, Borriello R, Orgiazzi A, Barbera AC, Lumini E, Bianciotto V (2014) Arbuscular mycorrhizal fungi and their value for ecosystem management. In: Biodiversity: the dynamic balance of the planet. InTech, Rijeta, Croacia, pp 159–191

    Google Scholar 

  • Biswas A, Biswas A (2014) Comprehensive approaches in rehabilitating salt affected soils: a review on Indian perspective. Open Trans Geosci 1(1):13–24

    Article  Google Scholar 

  • Bitterlich M, Rouphael Y, Graefe J, Franken P (2018) Arbuscular mycorrhizas: a promising component of plant production systems provided favorable conditions for their growth. Front Plant Sci 9:1329

    Article  Google Scholar 

  • Boldt-Burisch K, Naeth MA, Schneider U, Schneider B, Huttl RF (2018) Plant growth and arbuscular mycorrhizae development in oil sands processing by-products. Sci Total Environ 621:30–39

    Article  CAS  Google Scholar 

  • Borde M, Dudhane M, Jite P (2012) Growth, water use efficiency and antioxidant defense responses of mycorrhizal and non mycorrhizal Allium sativum L. under drought stress condition. Ann Plant Sci 1(1):6–11

    Google Scholar 

  • Bothe H (2012) Arbuscular mycorrhiza and salt tolerance of plants. Symbiosis 58(1–3):7–16

    Article  CAS  Google Scholar 

  • Brundrett M (1991) Mycorrhizas in natural ecosystems. Adv Ecol Res 21:171–313

    Article  Google Scholar 

  • Bucher M (2007) Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytol 173(1):11–26

    Article  CAS  Google Scholar 

  • Bücking H, Kafle A (2015) Role of arbuscular mycorrhizal fungi in the nitrogen uptake of plants: current knowledge and research gaps. Agronomy 5(4):587

    Article  CAS  Google Scholar 

  • Budi SW, Setyaningsih L (2013) Arbuscular mycorrhizal fungi and biochar improved early growth of Neem (Melia azedarach Linn.) seedling under greenhouse conditions. Jurnal Manajemen Hutan Tropika 19(2):103–110

    Google Scholar 

  • Calabrese S, Pérez-Tienda J, Ellerbeck M, Arnould C, Chatagnier O, Boller T et al (2016) GintAMT3–a low-affinity ammonium transporter of the arbuscular mycorrhizal Rhizophagus irregularis. Front Plant Sci 7:679

    Article  Google Scholar 

  • Cappellazzo G, Lanfranco L, Fitz M, Wipf D, Bonfante P (2008) Characterization of an amino acid permease from the endomycorrhizal fungus Glomus mosseae. Plant Physiol 147(1):429–437

    Article  CAS  Google Scholar 

  • Carvalho LM, Correia PM, Martins-Loucao MA (2004) Arbuscular mycorrhizal fungal propagules in a salt marsh. Mycorrhiza 14(3):165–170

    Article  Google Scholar 

  • Carvalho LM, Caçador I, Martins-Loução MA (2006) Arbuscular mycorrhizal fungi enhance root cadmium and copper accumulation in the roots of the salt marsh plant Aster tripolium L. Plant Soil 285(1–2):161–169

    Article  CAS  Google Scholar 

  • Cekic FO, 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(1):63–72

    CAS  Google Scholar 

  • Chang W, Sui X, Fan X-X, Jia T-T, Song F-Q (2018) Arbuscular mycorrhizal symbiosis modulates antioxidant response and ion distribution in salt-stressed Elaeagnus angustifolia seedlings. Front Microbiol 9:652

    Article  Google Scholar 

  • Chen BD, Zhu YG, Duan J, Xiao XY, Smith SE (2007) Effects of the arbuscular mycorrhizal fungus Glomus mosseae on growth and metal uptake by four plant species in copper mine tailings. Environ Pollut 147(2):374–380

    Article  CAS  Google Scholar 

  • Chen M, Arato M, Borghi L, Nouri E, Reinhardt D (2018) Beneficial services of arbuscular mycorrhizal fungi – from ecology to application. Front Plant Sci 9:1270

    Article  Google Scholar 

  • Chi G-G, Srivastava AK, Wu Q-S (2018) Exogenous easily extractable glomalin-related soil protein improves drought tolerance of trifoliate orange. Arch Agron Soil Sci 64(10):1341–1350

    Article  CAS  Google Scholar 

  • Chitarra W, Pagliarani C, Maserti B, Lumini E, Siciliano I, Cascone P et al (2016) Insights on the impact of arbuscular mycorrhizal symbiosis on tomato tolerance to water stress. Plant Physiol 2016:00307

    Google Scholar 

  • Cimen B, Yesiloglu T (2016) Rootstock breeding for abiotic stress tolerance in citrus. In: Abiotic and biotic stress in plants-recent advances and future perspectives. InTech, London

    Google Scholar 

  • Cliquet JB, Murray PJ, Boucaud J (1997) Effect of the arbuscular mycorrhizal fungus Glomus fasciculatum on the uptake of amino nitrogen by Lolium perenne. New Phytol 137(2):345–349

    Article  CAS  Google Scholar 

  • Courty PE, Smith P, Koegel S, Redecker D, Wipf D (2015) Inorganic nitrogen uptake and transport in beneficial plant root-microbe interactions. Crit Rev Plant Sci 34(1–3):4–16

    Article  CAS  Google Scholar 

  • Coutinho ES, Barbosa M, Beiroz W, Mescolotti DLC, Bonfim JA, Louro Berbara RL et al (2019) Soil constraints for arbuscular mycorrhizal fungi spore community in degraded sites of rupestrian grassland: implications for restoration. Eur J Soil Biol 90:51–57

    Article  Google Scholar 

  • Daei G, Ardekani M, Rejali F, Teimuri S, Miransari M (2009) Alleviation of salinity stress on wheat yield, yield components, and nutrient uptake using arbuscular mycorrhizal fungi under field conditions. J Plant Physiol 166(6):617–625

    Article  CAS  Google Scholar 

  • Dahlawi S, Naeem A, Rengel Z, Naidu R (2018) Biochar application for the remediation of salt-affected soils: challenges and opportunities. Sci Total Environ 625:320–335

    Article  CAS  Google Scholar 

  • Dickinson D, Balduccio L, Buysse J, Ronsse F, Huylenbroeck G, Prins W (2015) Cost-benefit analysis of using biochar to improve cereals agriculture. GCB Bioenergy 7(4):850–864

    Article  Google Scholar 

  • Duc NH, Csintalan Z, Posta K (2018) Arbuscular mycorrhizal fungi mitigate negative effects of combined drought and heat stress on tomato plants. Plant Physiol Biochem 132:297–307

    Article  CAS  Google Scholar 

  • Durán P, Acuña J, Armada E, López-Castillo O, Cornejo P, Mora M et al (2016) Inoculation with selenobacteria and arbuscular mycorrhizal fungi to enhance selenium content in lettuce plants and improve tolerance against drought stress. J Soil Sci Plant Nutr 16(1):211–225

    Google Scholar 

  • Egamberdieva D, Kucharova Z (2009) Selection for root colonising bacteria stimulating wheat growth in saline soils. Biol Fertil Soils 45(6):563–571

    Article  Google Scholar 

  • Egamberdieva D, Wirth S, Behrendt U, Ahmad P, Berg G (2017) Antimicrobial activity of medicinal plants correlates with the proportion of antagonistic endophytes. Front Microbiol 8:199

    Article  Google Scholar 

  • Elhindi KM, El-Din AS, 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(1):170–179

    Article  CAS  Google Scholar 

  • Estrada B, Aroca R, Maathuis FJM, 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(10):1771–1782

    Article  CAS  Google Scholar 

  • Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104(7):1263–1280

    Article  CAS  Google Scholar 

  • 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(3):203–217

    Article  CAS  Google Scholar 

  • 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 Physiol Plant 33(4):1533

    Article  Google Scholar 

  • Farhangi-Abriz S, Torabian S (2017) Antioxidant enzyme and osmotic adjustment changes in bean seedlings as affected by biochar under salt stress. Ecotox Environ Safe 137:64–70

    Article  CAS  Google Scholar 

  • 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(4):185–190

    Article  CAS  Google Scholar 

  • Ferguson L, Kaur S, Epstein L (1998) Arbuscular mycorrhizal fungi on pistachio rootstocks in California. In: Ferguson L, Kester D (eds) Second international symposium on pistachios and almonds. Acta Horticulturae. International Society Horticultural Science, Leuven 1, pp 211–218

    Google Scholar 

  • Frey B, Schüepp H (1993) Acquisition of nitrogen by external hyphae of arbuscular mycorrhizal fungi associated with Zea mays L. New Phytol 124(2):221–230

    Article  Google Scholar 

  • Füzy A, Biró B, Tóth T, Hildebrandt U, Bothe H (2008) Drought, but not salinity, determines the apparent effectiveness of halophytes colonized by arbuscular mycorrhizal fungi. J Plant Physiol 165(11):1181–1192

    Article  CAS  Google Scholar 

  • Gadkar V, David-Schwartz R, Kunik T, Kapulnik Y (2001) Arbuscular mycorrhizal fungal colonization. Factors involved in host recognition. Plant Physiol 127(4):1493–1499

    Article  CAS  Google Scholar 

  • Gai JP, Fan JQ, Zhang SB, Mi NN, Christie P, Li XL et al (2018) Direct effects of soil cadmium on the growth and activity of arbuscular mycorrhizal fungi. Rhizosphere 7:43–48

    Article  Google Scholar 

  • García I, Mendoza R, Pomar MC (2008) Deficit and excess of soil water impact on plant growth of Lotus tenuis by affecting nutrient uptake and arbuscular mycorrhizal symbiosis. Plant Soil 304(1–2):117–131

    Article  CAS  Google Scholar 

  • 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(3):371–387

    Article  CAS  Google Scholar 

  • Garg N, Bharti A (2018) Salicylic acid improves arbuscular mycorrhizal symbiosis, and chickpea growth and yield by modulating carbohydrate metabolism under salt stress. Mycorrhiza 28(8):727–746

    Article  CAS  Google Scholar 

  • 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.(pigeonpea). J Agron Crop Sci 195(2):110–123

    Article  CAS  Google Scholar 

  • Gholamhoseini M, Ghalavand A, Dolatabadian A, Jamshidi E, Khodaei-Joghan A (2013) Effects of arbuscular mycorrhizal inoculation on growth, yield, nutrient uptake and irrigation water productivity of sunflowers grown under drought stress. Agric Water Manag 117:106–114

    Article  Google Scholar 

  • Giasson P, Jaouich A, Cayer P, Gagné S, Moutoglis P, Massicotte L (2006) Enhanced phytoremediation: a study of mycorrhizoremediation of heavy metal–contaminated soil. Remediat J 17(1):97–110

    Article  Google Scholar 

  • Giri B, Kapoor R, Mukerji K (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(4):753–760

    Article  CAS  Google Scholar 

  • Gong M, Tang M, Chen H, Zhang Q, Feng X (2013) Effects of two Glomus species on the growth and physiological performance of Sophora davidii seedlings under water stress. New For 44(3):399–408

    Article  Google Scholar 

  • Grattan S, Grieve C (1998) Salinity–mineral nutrient relations in horticultural crops. Sci Hortic 78(1–4):127–157

    Article  Google Scholar 

  • Grimaldo-Pantoja GL, Niu GH, Sun YP, Castro-Rocha A, Alvarez-Parrilla E, Flores-Margez JR et al (2017) Negative effect of saline irrigation on yield components and phytochemicals of pepper (Capsicum annuum) inoculated with arbuscular mycorrhizal fungi. Rev Fitotec Mex 40(2):141–149

    Google Scholar 

  • Haghighi M, Mohammadnia S, Attai Z, Pessarakli M (2017) Effects of mycorrhiza inoculation on cucumber growth irrigated with saline water. J Plant Nutr 40(1):128–137

    Article  CAS  Google Scholar 

  • Hamilton EW III, Frank DA (2001) Can plants stimulate soil microbes and their own nutrient supply? Evidence from a grazing tolerant grass. Ecology 82(9):2397–2402

    Article  Google Scholar 

  • Hammer EC, Nasr H, Pallon J, Olsson PA, Wallander H (2011) Elemental composition of arbuscular mycorrhizal fungi at high salinity. Mycorrhiza 21(2):117–129

    Article  CAS  Google Scholar 

  • Hammer EC, Forstreuter M, Rillig MC, Kohler J (2015) Biochar increases arbuscular mycorrhizal plant growth enhancement and ameliorates salinity stress. Appl Soil Ecol 96:114–121

    Article  Google Scholar 

  • Hasegawa PM, Bressan RA, Zhu J-K, Bohnert HJ (2000a) Plant cellular and molecular responses to high salinity. Annu Rev Plant Biol 51(1):463–499

    Article  CAS  Google Scholar 

  • Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000b) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499

    Article  CAS  Google Scholar 

  • Hashem A, Alqarawi AA, Radhakrishnan R, Al-Arjani A-BF, Aldehaish HA, Egamberdieva D et al (2018) Arbuscular mycorrhizal fungi regulate the oxidative system, hormones and ionic equilibrium to trigger salt stress tolerance in Cucumis sativus L. Saudi J Biol Sci 25(6):1102–1114

    Article  CAS  Google Scholar 

  • Hashem A, Kumar A, Al-Dbass AM, Alqarawi AA, Al-Arjani A-BF, Singh G et al (2019) Arbuscular mycorrhizal fungi and biochar improves drought tolerance in chickpea. Saudi J Biol Sci 26(3):614–624

    Article  CAS  Google Scholar 

  • Heidari M, Karami V (2014) Effects of different mycorrhiza species on grain yield, nutrient uptake and oil content of sunflower under water stress. J Saudi Soc Agric Sci 13(1):9–13

    Google Scholar 

  • Helander M, Saloniemi I, Omacini M, Druille M, Salminen J-P, Saikkonen K (2018) Glyphosate decreases mycorrhizal colonization and affects plant-soil feedback. Sci Total Environ 642:285–291

    Article  CAS  Google Scholar 

  • Hodge A (2001) Arbuscular mycorrhizal fungi influence decomposition of, but not plant nutrient capture from, glycine patches in soil. New Phytol 151(3):725–734

    Article  CAS  Google Scholar 

  • Hodge A, Campbell CD, Fitter AH (2001) An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413(6853):297

    Article  CAS  Google Scholar 

  • Hokmabadi H, Arzani K, Grierson P (2005) Growth, chemical composition, and carbon isotope discrimination of pistachio (Pistacia vera L.) rootstock seedlings in response to salinity. Aust J Agric Res 56(2):135–144

    Article  CAS  Google Scholar 

  • Horneck DA, Ellsworth JW, Hopkins BG, Sullivan DM, Stevens RG (2007) Managing salt-affected soils for crop production.

    Google Scholar 

  • Hu YC, Schmidhalter U (2005) Drought and salinity: a comparison of their effects on mineral nutrition of plants. J Plant Nutr Soil Sci 168(4):541–549

    Article  CAS  Google Scholar 

  • Jeffery S, Bezemer TM, Cornelissen G, Kuyper TW, Lehmann J, Mommer L et al (2015) The way forward in biochar research: targeting trade-offs between the potential wins. GCB Bioenergy 7(1):1–13

    Article  CAS  Google Scholar 

  • Ji L, Tan W, Chen X (2019) Arbuscular mycorrhizal mycelial networks and glomalin-related soil protein increase soil aggregation in Calcaric Regosol under well-watered and drought stress conditions. Soil Tillage Res 185:1–8

    Article  Google Scholar 

  • Jiang X, Huang Y (2003) Mechanism of contribution of mycorrhizal fungi to plant saline-alkali tolerance. Ecol Environ 12(3):353–356

    Google Scholar 

  • Jones CG, Lawton JH, Shachak M (1997) Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78(7):1946

    Article  Google Scholar 

  • Juniper S, Abbott LK (2006) Soil salinity delays germination and limits growth of hyphae from propagules of arbuscular mycorrhizal fungi. Mycorrhiza 16(5):371–379

    Article  CAS  Google Scholar 

  • Kaya C, Ashraf M, Sonmez O, Aydemir S, Tuna AL, Cullu MA (2009) The influence of arbuscular mycorrhizal colonisation on key growth parameters and fruit yield of pepper plants grown at high salinity. Sci Hortic 121(1):1–6

    Article  CAS  Google Scholar 

  • Khan AG (2005) Role of soil microbes in the rhizospheres of plants growing on trace metal contaminated soils in phytoremediation. J Trace Elem Med Biol 18(4):355–364

    Article  CAS  Google Scholar 

  • Khan AG (2006) Mycorrhizoremediation—an enhanced form of phytoremediation. J Zhejiang Univ Sci B 7(7):503–514

    Article  Google Scholar 

  • Khan A, Sharif M, Ali A, Shah SNM, Mian IA, Wahid F et al (2014) Potential of AM fungi in phytoremediation of heavy metals and effect on yield of wheat crop. Am J Plant Sci 05(11):1578–1586

    Article  CAS  Google Scholar 

  • Kim H-S, Kim K-R, Yang JE, Ok YS, Owens G, Nehls T et al (2016) Effect of biochar on reclaimed tidal land soil properties and maize (Zea mays L.) response. Chemosphere 142:153–159

    Article  CAS  Google Scholar 

  • Koegel S, Brulé D, Wiemken A, Boller T, Courty P-E (2015) The effect of different nitrogen sources on the symbiotic interaction between Sorghum bicolor and Glomus intraradices: expression of plant and fungal genes involved in nitrogen assimilation. Soil Biol Biochem 86:159–163

    Article  CAS  Google Scholar 

  • Kumar A, Verma JP (2018) Does plant—microbe interaction confer stress tolerance in plants: a review? Microbiol Res 207:41–52

    Article  CAS  Google Scholar 

  • Kumar A, Dames JF, Gupta A, Sharma S, Gilbert JA, Ahmad P (2015) Current developments in arbuscular mycorrhizal fungi research and its role in salinity stress alleviation: a biotechnological perspective. Crit Rev Biotechnol 35(4):461–474

    Article  CAS  Google Scholar 

  • Lal R (2002) Carbon sequestration in dryland ecosystems of West Asia and North Africa. Land Degrad Dev 13(1):45–59

    Article  Google Scholar 

  • Lashari MS, Liu Y, Li L, Pan W, Fu J, Pan G et al (2013) Effects of amendment of biochar-manure compost in conjunction with pyroligneous solution on soil quality and wheat yield of a salt-stressed cropland from Central China great plain. Field Crop Res 144:113–118

    Article  Google Scholar 

  • Latef AAHA, Chaoxing H (2011) Effect of arbuscular mycorrhizal fungi on growth, mineral nutrition, antioxidant enzymes activity and fruit yield of tomato grown under salinity stress. Sci Hortic 127(3):228–233

    Article  CAS  Google Scholar 

  • Latef A, He CX (2011) Effect of arbuscular mycorrhizal fungi on growth, mineral nutrition, antioxidant enzymes activity and fruit yield of tomato grown under salinity stress. Sci Hortic 127(3):228–233

    Article  CAS  Google Scholar 

  • Läuchli A, Epstein E (1990) Plant responses to saline and sodic conditions. Agric Salinity Assess Manag 71:113–137

    Google Scholar 

  • Le Pioufle O, Declerck S (2018) Reducing water availability impacts the development of the arbuscular mycorrhizal fungus Rhizophagus irregularis MUCL 41833 and its ability to take up and transport phosphorus under in vitro conditions. Front Microbiol 9:1254

    Article  Google Scholar 

  • Lehnert H, Serfling A, Friedt W, Ordon F (2018) Genome wide association studies reveal genomic regions associated with the response of wheat (Triticum aestivum L.) to mycorrhizae under drought stress conditions. Front Plant Sci 9:1728

    Article  Google Scholar 

  • Lenoir I, Fontaine J, Sahraoui ALH (2016) Arbuscular mycorrhizal fungal responses to abiotic stresses: a review. Phytochemistry 123:4–15

    Article  CAS  Google Scholar 

  • Li T, Hu YJ, Hao ZP, Li H, Wang YS, Chen BD (2013) First cloning and characterization of two functional aquaporin genes from an arbuscular mycorrhizal fungus Glomus intraradices. New Phytol 197(2):617–630

    Article  CAS  Google Scholar 

  • Li J-T, Yang Y, He C, Huang L, Ban Y, Tang M (2017) The effects of arbuscular mycorrhizal fungi on glomalin-related soil protein distribution, aggregate stability and their relationships with soil properties at different soil depths in lead-zinc contaminated area. PLoS One 12(8):e0182264

    Article  CAS  Google Scholar 

  • Liang C-C, Li T, Xiao Y-P, Liu M-J, Zhang H-B, Zhao Z-W (2009) Effects of inoculation with arbuscular mycorrhizal fungi on maize grown in multi-metal contaminated soils. Int J Phytoremediation 11(8):692–703

    Article  CAS  Google Scholar 

  • Liu T, Sheng M, Wang C, Chen H, Li Z, Tang M (2015) Impact of arbuscular mycorrhizal fungi on the growth, water status, and photosynthesis of hybrid poplar under drought stress and recovery. Photosynthetica 53(2):250–258

    Article  CAS  Google Scholar 

  • Liu C, Dai Z, Cui M, Lu W, Sun H (2018a) Arbuscular mycorrhizal fungi alleviate boron toxicity in Puccinellia tenuiflora under the combined stresses of salt and drought. Environ Pollut 240:557–565

    Article  CAS  Google Scholar 

  • Liu C-Y, Zhang F, Zhang D-J, Srivastava AK, Wu Q-S, Zou Y-N (2018b) Mycorrhiza stimulates root-hair growth and IAA synthesis and transport in trifoliate orange under drought stress. Sci Rep 8(1):1978

    Article  CAS  Google Scholar 

  • Liu CY, Zhang F, Zhang DJ, Srivastava AK, Wu QS, Zou YN (2018c) Mycorrhiza stimulates root-hair growth and IAA synthesis and transport in trifoliate orange under drought stress. Sci Rep 8:9

    CAS  Google Scholar 

  • Loha A, Kashyap AK, Sharma P (2018) A putative cyclin, SiPHO80 from root endophytic fungus Serendipita indica regulates phosphate homeostasis, salinity and heavy metal toxicity tolerance. Biochem Biophys Res Commun 507(1–4):414–419

    Article  CAS  Google Scholar 

  • López-Pedrosa A, González-Guerrero M, Valderas A, Azcón-Aguilar C, Ferrol N (2006) GintAMT1 encodes a functional high-affinity ammonium transporter that is expressed in the extraradical mycelium of Glomus intraradices. Fungal Genet Biol 43(2):102–110

    Article  CAS  Google Scholar 

  • Lopez-Raez JA (2016) How drought and salinity affect arbuscular mycorrhizal symbiosis and strigolactone biosynthesis? Planta 243(6):1375–1385

    Article  CAS  Google Scholar 

  • Lovelock CE, Wright SF, Clark DA, Ruess RW (2004) Soil stocks of glomalin produced by arbuscular mycorrhizal fungi across a tropical rain forest landscape. J Ecol 92(2):278–287

    Article  CAS  Google Scholar 

  • Maggio A, Reddy MP, Joly RJ (2000) Leaf gas exchange and solute accumulation in the halophyte Salvadora persica grown at moderate salinity. Environ Exp Bot 44(1):31–38

    Article  CAS  Google Scholar 

  • Mardukhi B, Rejali F, Daei G, Ardakani MR, Malakouti MJ, Miransari M (2011) Arbuscular mycorrhizas enhance nutrient uptake in different wheat genotypes at high salinity levels under field and greenhouse conditions. C R Biol 334(7):564–571

    Article  CAS  Google Scholar 

  • Marschner H, Dell B (1994) Nutrient uptake in mycorrhizal symbiosis. Plant Soil 159(1):89–102

    Article  CAS  Google Scholar 

  • Miransari M (2014) Use of microbes for the alleviation of soil stresses. Springer, Dordrecht

    Book  Google Scholar 

  • Miransari M (2016) Stress and mycorrhizal plant. In: Recent Advances on Mycorrhizal Fungi. Springer, Cham, pp 63–79

    Chapter  Google Scholar 

  • Mirzaei J, Moradi M (2017) Relationships between flora biodiversity, soil physiochemical properties, and arbuscular mycorrhizal fungi (AMF) diversity in a semi-arid forest. Plant Ecol Evol 150(2):151–159

    Article  Google Scholar 

  • Mohammad MJ, Malkawi HI, Shibli R (2003) Effects of arbuscular mycorrhizal fungi and phosphorus fertilization on growth and nutrient uptake of barley grown on soils with different levels of salts. J Plant Nutr 26(1):125–137

    Article  CAS  Google Scholar 

  • Mollinedo J, Schumacher TE, Chintala R (2016) Biochar effects on phenotypic characteristics of “wild” and “sickle” Medicago truncatula genotypes. Plant Soil 400(1–2):1–14

    Article  CAS  Google Scholar 

  • Mosse B, Stribley D, Le Tacon F (1981) Ecology of mycorrhizae and mycorrhizal fungi. Adv Microbial Ecol 5:137–210

    Article  Google Scholar 

  • Mukherjee A, Zimmerman AR (2013) Organic carbon and nutrient release from a range of laboratory-produced biochars and biochar–soil mixtures. Geoderma 193:122–130

    Article  CAS  Google Scholar 

  • Naher UA, Othman R, Panhwar QA (2013) Beneficial effects of Mycorrhizal Association for Crop Production in the tropics—a review. Int J Agric Biol 15(5):1021–1028

    Google Scholar 

  • Nakano A, Takahashi K, Koide RT, Kimura M (2001) Determination of the nitrogen source for arbuscular mycorrhizal fungi by 15 N application to soil and plants. Mycorrhiza 10(6):267–273

    Article  CAS  Google Scholar 

  • Nasim G (2010) The role of arbuscular mycorrhizae in inducing resistance to drought and salinity stress in crops. In: Plant adaptation and phytoremediation. Springer, Berlin, pp 119–141

    Chapter  Google Scholar 

  • Navarro JM, Pérez-Tornero O, Morte A (2014) Alleviation of salt stress in citrus seedlings inoculated with arbuscular mycorrhizal fungi depends on the rootstock salt tolerance. J Plant Physiol 171(1):76–85

    Article  CAS  Google Scholar 

  • Neumann E, George E (2004) Colonisation with the arbuscular mycorrhizal fungus Glomus mosseae (Nicol. & Gerd.) enhanced phosphorus uptake from dry soil in Sorghum bicolor (L.). Plant Soil 261:245–255

    Article  CAS  Google Scholar 

  • Oliveira RS, Carvalho P, Marques G, Ferreira L, Nunes M, Rocha I et al (2017) Increased protein content of chickpea (Cicer arietinum L.) inoculated with arbuscular mycorrhizal fungi and nitrogen-fixing bacteria under water deficit conditions. J Sci Food Agric 97(13):4379–4385

    Article  CAS  Google Scholar 

  • Olmo M, Villar R, Salazar P, Alburquerque JA (2016) Changes in soil nutrient availability explain biochar’s impact on wheat root development. Plant Soil 399(1–2):333–343

    Article  CAS  Google Scholar 

  • Ortas I (2016) Role of mycorrhizae and biochar on plant growth and soil quality. In: Bruckman VJ, Varol EA, Uzun BB, Liu JF (eds) Biochar, a Regıonal supply chain approach in view of climate change mitigation. Cambridge Universitey Press, Cambridge, UK, p 398

    Google Scholar 

  • Ortaş I, Rafique M (2017) The mechanisms of nutrient uptake by arbuscular mycorrhizae. In: Varma A, Prasad R, Tuteja N (eds) Mycorrhiza—nutrient uptake, biocontrol, ecorestoration. Springer, Cham, pp 1–19

    Google Scholar 

  • Ortuno MF, Lorente B, Hernandez JA, Sanchez-Blanco MJ (2018) Mycorrhizal inoculation on compost substrate affects nutritional balance, water uptake and photosynthetic efficiency in Cistus albidus plants submitted to water stress. Braz J Bot 41(2):299–310

    Article  Google Scholar 

  • Osakabe Y, Osakabe K, Shinozaki K, Tran L-SP (2014) Response of plants to water stress. Front Plant Sci 5:86

    Article  Google Scholar 

  • Ouledali S, Ennajeh M, Ferrandino A, Khemira H, Schubert A, Secchi F (2019) Influence of arbuscular mycorrhizal fungi inoculation on the control of stomata functioning by abscisic acid (ABA) in drought-stressed olive plants. S Afr J Bot 121:152–158

    Article  CAS  Google Scholar 

  • Oyewole BO, Olawuyi OJ, Odebode AC, Abiala MA (2017) Influence of Arbuscular mycorrhiza fungi (AMF) on drought tolerance and charcoal rot disease of cowpea. Biotechnol Rep 14:8–15

    Article  CAS  Google Scholar 

  • Pavithra D, Yapa N (2018) Arbuscular mycorrhizal fungi inoculation enhances drought stress tolerance of plants. Groundw Sustain Dev 7:490–494

    Article  Google Scholar 

  • Paymaneh Z, Sarcheshmehpour M, Bukovská P, Jansa J (2019) Could indigenous arbuscular mycorrhizal communities be used to improve tolerance of pistachio to salinity and/or drought? Symbiosis:1–15

    Google Scholar 

  • Pérez-Tienda J, Testillano PS, Balestrini R, Fiorilli V, Azcón-Aguilar C, Ferrol N (2011) GintAMT2, a new member of the ammonium transporter family in the arbuscular mycorrhizal fungus Glomus intraradices. Fungal Genet Biol 48(11):1044–1055

    Article  CAS  Google Scholar 

  • Peterson RL, Massicotte HB (2004) Exploring structural definitions of mycorrhizas, with emphasis on nutrient-exchange interfaces. Can J Bot 82(8):1074–1088

    Article  Google Scholar 

  • Porcel R, Aroca R, Ruiz-Lozano JM (2012) Salinity stress alleviation using arbuscular mycorrhizal fungi. A review. Agron Sustain Dev 32(1):181–200

    Article  CAS  Google Scholar 

  • 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(7):673–684

    Article  CAS  Google Scholar 

  • Porras-Soriano A, Luisa Soriano-Martin M, Porras-Piedra A, Azcon R (2009a) Arbuscular mycorrhizal fungi increased growth, nutrient uptake and tolerance to salinity in olive trees under nursery conditions. J Plant Physiol 166(13):1350–1359

    Article  CAS  Google Scholar 

  • Porras-Soriano A, Soriano-Martín ML, Porras-Piedra A, Azcón R (2009b) Arbuscular mycorrhizal fungi increased growth, nutrient uptake and tolerance to salinity in olive trees under nursery conditions. J Plant Physiol 166(13):1350–1359

    Article  CAS  Google Scholar 

  • Puga A, Abreu C, Melo L, Beesley L (2015) Biochar application to a contaminated soil reduces the availability and plant uptake of zinc, lead and cadmium. J Environ Manag 159:86–93

    Article  CAS  Google Scholar 

  • Quiroga G, Erice G, Aroca R, Zamarreño ÁM, García-Mina JM, Ruiz-Lozano JM (2018) Arbuscular mycorrhizal symbiosis and salicylic acid regulate aquaporins and root hydraulic properties in maize plants subjected to drought. Agric Water Manag 202:271–284

    Article  Google Scholar 

  • Rafique M, Sultan T, Ortas I, Chaudhary HJ (2017) Enhancement of maize plant growth with inoculation of phosphate-solubilizing bacteria and biochar amendment in soil. Soil Sci Plant Nutr 63:460–469

    Article  CAS  Google Scholar 

  • Redon P-O, Béguiristain T, Leyval C (2008) Influence of Glomus intraradices on Cd partitioning in a pot experiment with Medicago truncatula in four contaminated soils. Soil Biol Biochem 40(10):2710–2712

    Article  CAS  Google Scholar 

  • Rillig MC, Mummey DL (2006) Mycorrhizas and soil structure. New Phytol 171(1):41–53

    Article  CAS  Google Scholar 

  • Rivero J, Alvarez D, Flors V, Azcon-Aguilar C, Pozo MJ (2018) Root metabolic plasticity underlies functional diversity in mycorrhiza-enhanced stress tolerance in tomato. New Phytol 220(4):1322–1336

    Article  CAS  Google Scholar 

  • Rouphael Y, Franken P, Schneider C, Schwarz D, Giovannetti M, Agnolucci M et al (2015) Arbuscular mycorrhizal fungi act as biostimulants in horticultural crops. Sci Hortic 196:91–108

    Article  Google Scholar 

  • Roy M, Roychowdhury R, Mukherjee P (2018) Remediation of fly ash dumpsites through bioenergy crop plantation and generation: a review. Pedosphere 28(4):561–580

    Article  Google Scholar 

  • Ruiz-Lozano JM, Collados C, Barea JM, Azcón R (2001) Arbuscular mycorrhizal symbiosis can alleviate drought-induced nodule senescence in soybean plants. New Phytol 151(2):493–502

    Article  CAS  Google Scholar 

  • Ruiz-Lozano JM, Porcel R, Aroca R (2006) Does the enhanced tolerance of arbuscular mycorrhizal plants to water deficit involve modulation of drought-induced plant genes? New Phytol 171(4):693–698

    Article  CAS  Google Scholar 

  • Ruiz-Lozano JM, Porcel R, Azcón C, 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(11):4033–4044

    Article  CAS  Google Scholar 

  • Ruiz-Lozano JM, Porcel R, Calvo-Polanco M, Aroca R (2018) Improvement of salt tolerance in rice plants by arbuscular mycorrhizal symbiosis. In: Root biology. Springer, Cham, pp 259–279

    Chapter  Google Scholar 

  • Ruíz-Sánchez M, Armada E, Muñoz Y, de Salamone IEG, Aroca R, Ruíz-Lozano JM et al (2011) Azospirillum and arbuscular mycorrhizal colonization enhance rice growth and physiological traits under well-watered and drought conditions. J Plant Physiol 168(10):1031–1037

    Article  CAS  Google Scholar 

  • Santander C, Aroca R, Ruiz-Lozano JM, Olave J, Cartes P, Borie F et al (2017) Arbuscular mycorrhiza effects on plant performance under osmotic stress. Mycorrhiza 27(7):639–657

    Article  CAS  Google Scholar 

  • 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 Agric Sci 53(2):399–406

    Google Scholar 

  • Shabani L, Sabzalian MR (2016) Mostafavi pour S. Arbuscular mycorrhiza affects nickel translocation and expression of ABC transporter and metallothionein genes in Festuca arundinacea. Mycorrhiza 26(1):67–76

    Article  CAS  Google Scholar 

  • Shamshiri MH, Fattahi M (2016) Effects of arbuscular mycorrhizal fungi on photosystem II activity of three pistachio rootstocks under salt stress as probed by the OJIP-test. Russ J Plant Physiol 63(1):101–110

    Article  CAS  Google Scholar 

  • Shen Q, Hedley M, Arbestain MC, Kirschbaum MUF (2016) Can biochar increase the bioavailability of phosphorus? J Soil Sci Plant Nut 16(2):268–286

    CAS  Google Scholar 

  • Sheng M, Tang M, Chen 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(6–7):287–296

    Article  CAS  Google Scholar 

  • Shirani H, Shamshiri M, Bagheri V, Roosta H (2018) Nutrient uptake and distribution in mycorrhizal pistachio seedlings under drought stress. J Agric Sci Technol 14:1591–1604

    Google Scholar 

  • Smith P (2016) Soil carbon sequestration and biochar as negative emission technologies. Glob Chang Biol 22(3):1315–1324

    Article  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, Third edn. Academic, San Diego, CA

    Google Scholar 

  • Soka GE, Ritchie ME (2018) Arbuscular mycorrhizal spore composition and diversity associated with different land uses in a tropical savanna landscape. Tanzania Appl Soil Ecol 125:222–232

    Article  Google Scholar 

  • Stevens KJ, Wall CB, Janssen JA (2011) Effects of arbuscular mycorrhizal fungi on seedling growth and development of two wetland plants, Bidens frondosa L., and Eclipta prostrata (L.) L., grown under three levels of water availability. Mycorrhiza 21(4):279–288

    Article  Google Scholar 

  • Subramanian K, Santhanakrishnan P, Balasubramanian P (2006) Responses of field grown tomato plants to arbuscular mycorrhizal fungal colonization under varying intensities of drought stress. Sci Hortic 107(3):245–253

    Article  Google Scholar 

  • Sudhir P, Murthy S (2004) Effects of salt stress on basic processes of photosynthesis. Photosynthetica 42(2):481–486

    Article  CAS  Google Scholar 

  • Sun X, Shi J, Ding G (2017) Combined effects of arbuscular mycorrhiza and drought stress on plant growth and mortality of forage sorghum. Appl Soil Ecol 119:384–391

    Article  Google Scholar 

  • Swaty RL, Deckert RJ, Whitham TG, Gehring CA (2004) Ectomycorrhizal abundance and community composition shifts with drought: predictions from tree rings. Ecology 85(4):1072–1084

    Article  Google Scholar 

  • Thomas H, Morgan W, Humphreys M (2003) Designing grasses with a future–combining the attributes of Lolium and Festuca. Euphytica 133(1):19–26

    Article  Google Scholar 

  • Thomas SC, Frye S, Gale N, Garmon M, Launchbury R, Machado N et al (2013) Biochar mitigates negative effects of salt additions on two herbaceous plant species. J Environ Manag 129:62–68

    Article  CAS  Google Scholar 

  • Tobar R, Azcón R, Barea J (1994a) Improved nitrogen uptake and transport from 15N-labelled nitrate by external hyphae of arbuscular mycorrhiza under water-stressed conditions. New Phytol 126(1):119–122

    Article  Google Scholar 

  • Tobar R, Azcón R, Barea J (1994b) The improvement of plant N acquisition from an ammonium-treated, drought-stressed soil by the fungal symbiont in arbuscular mycorrhizae. Mycorrhiza 4(3):105–108

    Article  Google Scholar 

  • Treu R, Falandysz J (2017) Mycoremediation of hydrocarbons with basidiomycetes-a review. J Environ Sci Health B 52(3):148–155

    Article  CAS  Google Scholar 

  • Trouvelot S, Heloir MC, Poinssot B, Gauthier A, Paris F, Guillier C et al (2014) Carbohydrates in plant immunity and plant protection: roles and potential application as foliar sprays. Front Plant Sci 5:592

    Article  Google Scholar 

  • Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218(1):1–14

    Article  CAS  Google Scholar 

  • Wang F, Lin X, Yin R (2005) Heavy metal uptake by arbuscular mycorrhizas of Elsholtzia splendens and the potential for phytoremediation of contaminated soil. Plant Soil 269(1–2):225–232

    Article  CAS  Google Scholar 

  • Wang P, Srivastava AK, Zhang YC, Wu QS (2016) Inoculation response of mycorrhizas on morphology and physiological behaviour of trifoliate orange (Poncirus trifoliata) roots under salt stress. Indian J Agric Sci 86(11):1438–1442

    CAS  Google Scholar 

  • Wu QS, Xia RX (2006) Arbuscular mycorrhizal fungi influence growth, osmotic adjustment and photosynthesis of citrus under well-watered and water stress conditions. J Plant Physiol 163(4):417–425

    Article  CAS  Google Scholar 

  • Wu QS, Zou YN, Xia RX (2006) Effects of water stress and arbuscular mycorrhizal fungi on reactive oxygen metabolism and antioxidant production by citrus (citrus tangerine) roots. Eur J Soil Biol 42(3):166–172

    Article  CAS  Google Scholar 

  • Wu QS, Zou YN, Liu W, Ye X, Zai H, Zhao L (2010) Alleviation of salt stress in citrus seedlings inoculated with mycorrhiza: changes in leaf antioxidant defense systems. Plant Soil Environ 56(10):470–475

    Article  CAS  Google Scholar 

  • Wu Q-S, Zou Y-N, He X-H (2011) Differences of hyphal and soil phosphatase activities in drought-stressed mycorrhizal trifoliate orange (Poncirus trifoliata) seedlings. Sci Hortic 129(2):294–298

    Article  CAS  Google Scholar 

  • Wu QS, Srivastava AK, Zou YN (2013) AMF-induced tolerance to drought stress in citrus: a review. Sci Hortic 164:77–87

    Article  CAS  Google Scholar 

  • Xu L, Li T, Wu Z, Feng H, Yu M, Zhang X et al (2018) Arbuscular mycorrhiza enhances drought tolerance of tomato plants by regulating the 14-3-3 genes in the ABA signaling pathway. Appl Soil Ecol 125:213–221

    Article  Google Scholar 

  • Yamato M, Ikeda S, Iwase K (2008) Community of arbuscular mycorrhizal fungi in a coastal vegetation on Okinawa island and effect of the isolated fungi on growth of sorghum under salt-treated conditions. Mycorrhiza 18(5):241–249

    Article  Google Scholar 

  • Yang SJ, Zhang ZL, Xue YX, Zhang ZF, Shi SY (2014) Arbuscular mycorrhizal fungi increase salt tolerance of apple seedlings. Bot Stud 55:7

    Article  CAS  Google Scholar 

  • Yang YR, He CJ, Huang L, Ban YH, Tang M (2017) The effects of arbuscular mycorrhizal fungi on glomalin-related soil protein distribution, aggregate stability and their relationships with soil properties at different soil depths in lead-zinc contaminated area. PLoS One 12(8):e0182264

    Article  CAS  Google Scholar 

  • Yu H, Zou W, Chen J, Chen H, Yu Z, Huang J et al (2019) Biochar amendment improves crop production in problem soils: a review. J Environ Manag 232:8–21

    Article  CAS  Google Scholar 

  • Zaefarian F, Rezvani M, Ardakani MR, Rejali F, Miransari M (2013) Impact of mycorrhizae formation on the phosphorus and heavy-metal uptake of alfalfa. Commun Soil Sci Plant Anal 44(8):1340–1352

    Article  CAS  Google Scholar 

  • Zarik L, Meddich A, Hijri M, Hafidi M, Ouhammou A, Ouahmane L et al (2016) Use of arbuscular mycorrhizal fungi to improve the drought tolerance of Cupressus atlantica G. C R Biol 339(5–6):185–196

    Article  Google Scholar 

  • Zhang XH, Zhu YG, Chen BD, Lin AJ, Smith SE, Smith FA (2005) Arbuscular mycorrhizal fungi contribute to resistance of upland rice to combined metal contamination of soil. J Plant Nutr 28(12):2065–2077

    Article  CAS  Google Scholar 

  • Zhang Q, Xu L, Tang J, Bai M, Chen X (2011) Arbuscular mycorrhizal mediation of biomass–density relationship of Medicago sativa L. under two water conditions in a field experiment. Mycorrhiza 21(4):269–277

    Article  Google Scholar 

  • Zhang Z, Wang Q, Wang H, Nie S, Liang Z (2017) Effects of soil salinity on the content, composition, and ion binding capacity of glomalin-related soil protein (GRSP). Sci Total Environ 581–582:657–665

    Article  CAS  Google Scholar 

  • Zhang T, Hu Y, Zhang K, Tian C, Guo J (2018) Arbuscular mycorrhizal fungi improve plant growth of Ricinus communis by altering photosynthetic properties and increasing pigments under drought and salt stress. Ind Crop Prod 117:13–19

    Article  CAS  Google Scholar 

  • Zhang W, Wang C, Liu M, Yu Y (2019a) Integrated reclamation of saline soil nitrogen transformation in the hyphosphere by earthworms and arbuscular mycorrhizal fungus. Appl Soil Ecol 135:137–146

    Article  Google Scholar 

  • Zhang F, Liu M, Li Y, Che Y, Xiao Y (2019b) Effects of arbuscular mycorrhizal fungi, biochar and cadmium on the yield and element uptake of Medicago sativa. Sci Total Environ 655:1150–1158

    Article  CAS  Google Scholar 

  • Zhu X, Song F, Liu S, Liu T, Zhou X (2012) Arbuscular mycorrhizae improves photosynthesis and water status of Zea mays L. under drought stress. Plant Soil Environ 58(4):186–191

    Article  CAS  Google Scholar 

  • Zrnic M, Siric I (2017) The application of mycorrhiza in horticulture Primjena mikorize u hortikulturi. J Cent Eur Agric 18(3):706–732

    Article  Google Scholar 

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Ortas, I., Rafique, M., Çekiç, F.Ö. (2021). Do Mycorrhizal Fungi Enable Plants to Cope with Abiotic Stresses by Overcoming the Detrimental Effects of Salinity and Improving Drought Tolerance?. In: Shrivastava, N., Mahajan, S., Varma, A. (eds) Symbiotic Soil Microorganisms. Soil Biology, vol 60. Springer, Cham. https://doi.org/10.1007/978-3-030-51916-2_23

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