Skip to main content

Advertisement

SpringerLink
Log in

Arbuscular mycorrhizal symbiosis regulates the physiological responses, ion distribution and relevant gene expression to trigger salt stress tolerance in pistachio

  • Research Article
  • Published:
Physiology and Molecular Biology of Plants Aims and scope Submit manuscript

Abstract

Mycorrhizal symbiosis is generally considered effective in ameliorating plant tolerance to abiotic stress by altering gene expression, and evaluation of genes involved in ion homeostasis and nutrient uptake. This study aimed to use arbuscular mycorrhizal fungus (AMF) to alleviate salinity stress and analyse relevant gene expression in pistachio plants under No/NaCl stress in greenhouse conditions. Arbuscular mycorrhizal symbiosis was used to study the physiological responses, ion distribution and relevant gene expression in pistachio plants under salinity stress. After four months of symbiosis, mycorrhizal root colonization showed a significant reduction in all tested parameters under salt stress treatment compared to non-saline treatment. Salinity affected the morphological traits, and decreased the nutrient content including N, P, Mg and Fe as well as K/Na and Ca/Na ratios, relative water content (RWC), membrane stability index (MSI), and increased the concentration of K, Ca and Na nutrient, glycine betaine, ROS and MDA. Inoculation of seedlings with AMF mitigated the negative effects of salinity on plant growth as indicated by increasing the root colonization, morphological traits, glycine betaine, RWC and MSI. Specifically, under salinity stress, shoot and root dry weight, P and Fe nutrient content, K/Na and Ca/Na ratio of AMF plants were increased by 53.2, 48.6, 71.6, 60.2, 87.5, and 80.1% respectively, in contrast to those of the NMF plants. The contents of Na, O2•− and MDA in AMF plants were significantly decreased by 66.8, 36.8, and 23.1%, respectively at 250 mM NaCl. Moreover, salinity markedly increased SOS1, CCX2 and SKOR genes expression and the inoculation with AMF modulated these genes expression; however, NRT2.4, PHO1 and PIP2.4 gene expressions were increased by salinity and AMF. It could be concluded that inoculation of AMF with Rhizophagus irregularis conferred a larger endurance towards soil salinity in pistachio plants and stimulate the nutrient uptake and ionic homeostasis maintenance, superior RWC and osmoprotection, toxic ion partitioning, maintaining membrane integrity and the ion-relevant genes expression.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig.1
Fig. 2

Similar content being viewed by others

References

  • Abbaspour H (2010) Investigation of the effects of vesicular arbuscular mycorrhiza on mineral nutrition and growth of Carthamus tinctorius under salt stress conditions. Russian J Plant Physiol 57:526–531

    Article  CAS  Google Scholar 

  • Abbaspour H (2016) Contributions of arbuscular mycorrhizal fungi to growth, biomass and nutrient status of pistachio seedlings under saline conditions. J Nuts 7(1):67–74

    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 169:704–709

    Article  CAS  PubMed  Google Scholar 

  • Abd-Allah EF, Hashem A, Alqarawi AA, Bahkali AH, Alwhibi MS (2015) Enhancing growth performance and systemic acquired resistance of medicinal plant Sesbania sesban (L.) Merr using arbuscular mycorrhizal fungi under salt stress. Saudi J Biol Sci 22:274–283

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Abdel-Fattah GM, Asrar AWA (2012) Arbuscular mycorrhizal fungal application to improve growth and tolerance of wheat (Triticum aestivum L.) plants grown in saline soil. Acta Physiol Plant 34:267–277

    Article  CAS  Google Scholar 

  • Acosta-Motos JR, Ortuño MF, Bernal-Vicente A, Diaz-Vivancos P, Sanchez-Blanco MJ, Hernandez JA (2017) Plant responses to salt stress: adaptive mechanisms. Agronomy 7(1):18

    Article  CAS  Google Scholar 

  • Aliakbarkhani ST, Akbari M, Hassankhah A, Talaie A, Moghadam MF (2015) Phenotypic and genotypic variation in Iranian Pistachios. J Genet Eng Biotechno 13:235–241

    Article  Google Scholar 

  • Amin I, Rasool S, Mir MA, Wani W, Masoodi KZ, Ahmad P (2021) Ion homeostasis for salinity tolerance in plants: a molecular approach. Physiol Plant 171(4):578–594. https://doi.org/10.1111/ppl.13185

    Article  CAS  PubMed  Google Scholar 

  • Annunziata MG, Ciarmiello LF, Woodrow P, Dell’Aversana E, Carillo P (2019) Spatial and Temporal Profile of Glycine Betaine Accumulation in Plants Under Abiotic Stresses. Front Plant Sci 7(10):230. https://doi.org/10.3389/fpls.2019.00230

    Article  Google Scholar 

  • Ansari M, Shekari F, Mohammadi MH, Juhos K, Végvári G, Biró B (2019) Salt-tolerant plant growth-promoting bacteria enhanced salinity tolerance of salt-tolerant alfalfa (Medicago sativa L.) cultivars at high salinity. Acta Physiol Plant 41:195

    Article  CAS  Google Scholar 

  • 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(4):808–816

    Article  CAS  PubMed  Google Scholar 

  • Arzani A, Ashraf M (2016) Smart engineering of genetic resources for enhanced salinity tolerance in crop plants. Crit Rev Plant Sci 35:146–189

    Article  CAS  Google Scholar 

  • Ashraf M, Foolad MR (2013) Crop breeding for salt tolerance in the era of molecular markers and marker-assisted selection. Plant Breed 132:10–20

    Article  Google Scholar 

  • Ashraf M, Shahzad SM, Imtiaz M, Rizwan MS (2018) Salinity effects on nitrogen metabolism in plants–focusing on the activities of nitrogen metabolizing enzymes: a review. J Plant Nutrition 41(8):1065–81

    Article  CAS  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 

  • Biermann B, Linderman RG (1981) Quantifying vesicular-arbuscular mycorrhizae: a proposed method towards standardization. New Phytol 87(1):63–67

    Article  Google Scholar 

  • Cao K, Yu J, Xu D, Ai K, Bao E, Zou Z (2018) Exposure to lower red to far-red light ratios improve tomato tolerance to salt stress. BMC Plant Biol 18:92

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen S, Zhao H, Zou C, Li Y, ChenY Wang Z, Jiang Y, Liu A, Zhao P, Wang M, Ahammed GJ (2017) Combined inoculation with multiple arbuscular mycorrhizal fungi improves growth, nutrient uptake and photosynthesis in cucumber seedlings. Front Microbiol 8:2516

    Article  PubMed  PubMed Central  Google Scholar 

  • Dagar J, Minhas P (2016) Global Perspectives on agroforestry for the management of salt-affected soils. agroforestry for the management of waterlogged saline soils and poor-quality waters. Springer, pp 5–32.

  • Ebrahim MK, Saleem AR (2017) Alleviating salt stress in tomato inoculated with mycorrhizae: photosynthetic performance and enzymatic antioxidants. J Taibah Univ Sci 11:850–860

    Article  Google Scholar 

  • El-Beltagi HS, Mohamed HI (2013) Alleviation of cadmium toxicity in Pisum sativum L. seedlings by calcium chloride. Not Bot Horti Agrobo 41:157–168

    Article  CAS  Google Scholar 

  • 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 36:1771–1782

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  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 22:203–217

    Article  CAS  PubMed  Google Scholar 

  • Evelin H, Giri B, Kapoor R (2013) Ultrastructural evidence for AMF mediated salt stress mitigation in Trigonella foenum-graecum. Mycorrhiza 23:71–86

    Article  CAS  PubMed  Google Scholar 

  • Evelin H, Devi TS, Gupta S, Kapoor R (2019) Mitigation of salinity stress in plants by arbuscular mycorrhizal symbiosis: current understanding and new challenges. Front Plant Sci 12(10):470. https://doi.org/10.3389/fpls.2019.00470

    Article  Google Scholar 

  • FAOSTAT (2013) Food and agriculture organization of the united nations (FAO). FAOSTAT online statistical service. FAO, Rome. Available via http://faostat.fao.org/. Accessed 20 Oct 2014

  • Fattahi M, Mohammadkhani A, Shiran B, Baninasab B, Ravash R, Gogorcena Y (2021) Beneficial effect of mycorrhiza on nutritional uptake and oxidative balance in pistachio (Pistacia spp.) rootstocks submitted to drought and salinity stress. Sci Hortic 30(281):109937

    Article  CAS  Google Scholar 

  • Ferguson L, Kaur S, Epstein L (1997) Arbuscular mycorrhizal fungi on pistachio rootstocks in California. InII Int Symp Pistachios Almonds 470(24):211–218

    Google Scholar 

  • 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. https://doi.org/10.1371/journal.pone.0184158

    Article  CAS  PubMed  PubMed Central  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 165:1181–1192

    Article  PubMed  CAS  Google Scholar 

  • Gąstoł M, Domagała-Świątkiewicz I (2015) Mycorrhizal inoculation of apple in replant soils–enhanced tree growth and mineral nutrient status. Acta Sci Pol Hortorum Cultus 14:17–37

    Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  CAS  PubMed  Google Scholar 

  • Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 1:489–500

    Article  Google Scholar 

  • Giri B, Kapoor R, Mukerji K (2003) Influence of arbuscular mycorrhizal fungi and salinity on growth, biomass, and mineral nutrition of acacia auriculiformis. Biol Fert Soils 38:170–175

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Gururani MA, Ganesan M, Song IJ, Han Y, Kim JI, Lee HY, Song PS (2016) Transgenic turfgrasses expressing hyperactive Ser599Ala Phytochrome a mutant exhibit abiotic stress tolerance. J Plant Growth Regul 35(1):11–21

    Article  CAS  Google Scholar 

  • Gutjahr C, Parniske M (2013) Cell and developmental biology of arbuscular mycorrhiza symbiosis. Ann Rrev Cell Dev Bi 29:593–617

    Article  CAS  Google Scholar 

  • Hajiboland R, Norouzi F, Poschenrieder C (2014) Growth, physiological, biochemical and ionic responses of pistachio seedlings to mild and high salinity. Trees 28:1065–1078

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hashem A, Abd-Allah EF, Alqarawi AA, Al-Huqail AA, Wirth S, Egamberdieva D (2016) The interaction between arbuscular mycorrhizal fungi and endophytic bacteria enhances plant growth of Acacia gerrardii under salt stress. Front Microbiol 7:1089

    Article  PubMed  PubMed Central  Google Scholar 

  • Hashem A, Alqarawi AA, Radhakrishnan R, Al-Arjani ABF, Aldehaish HA, Egamberdieva D, Abd-Allah EF (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 25:1102–1114

    CAS  Google Scholar 

  • Hashem A, Abd-Allah EF, Alqarawi AA, Wirth S, Egamberdieva D (2019) Comparing symbiotic performance and physiological responses of two soybean cultivars to arbuscular mycorrhizal fungi under salt stress. Saudi J Biol Sci 26:38–48

    Article  CAS  PubMed  Google Scholar 

  • Hodge A, Fitter AH (2010) Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling. Proc Natl Acad Sci 107:13754–13759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang Z, He CX, He ZQ, Zou ZR, Zhang ZB (2010) The effects of arbuscular mycorrhizal fungi on reactive oxyradical scavenging system of tomato under salt tolerance. Agr Sci China 9:1150–1159

    Article  CAS  Google Scholar 

  • Huang CJ, Wei G, Jie YC, Xu JJ, Zhao SY, Wang LC, Anjum S (2015) Responses of gas exchange, chlorophyll synthesis and ROS-scavenging systems to salinity stress in two ramie (Boehmeria nivea L.) cultivars. Photosynthetica 53:455–463

    Article  CAS  Google Scholar 

  • Hussain S, Hussain S, Ali B, Ren X, Chen X, Li Q, Saqib M, Ahmad N (2021) Recent progress in understanding salinity tolerance in plants: Story of Na+/K+ balance and beyond. Plant Physiol Biochem 160:239–256. https://doi.org/10.1016/j.plaphy.2021.01.029

    Article  CAS  PubMed  Google Scholar 

  • Kapoor R, Evelin H, Devi TS, Gupta S (2019) Mitigation of salinity stress in plants by arbuscular mycorrhizal symbiosis: current understanding and new challenges. Front Plant Sci 10:470

    Article  PubMed  PubMed Central  Google Scholar 

  • Köhler B, Raschke K (2000) The delivery of salts to the xylem. Three types of anion conductance in the plasmalemma of the xylem parenchyma of roots of barley. Plant Physiol 122:243–254

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Li Z, Wang X, Chen J, Gao J, Zhou X, Kuai B (2016) CCX1, a putative Cation/Ca2+ exchanger, participates in regulation of reactive oxygen species homeostasis and leaf senescence. Plant Cell Physiol 57:2611–2619

    Article  CAS  PubMed  Google Scholar 

  • 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 398:195–206

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2- ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Long-Tang H, Li-Na Z, Li-Wei G, Anne-Aliénor V, Hervé S, Yi-Dong Z (2018) Constitutive expression of CmSKOR, an outward K+ channel gene from melon, in Arabidopsis thaliana involved in saline tolerance. Plant Sci 274:492–502

    Article  PubMed  CAS  Google Scholar 

  • Lueck C, Boltz D (1958) Indirect ultraviolet spectrophotometric determination of phosphorus. Anal Chem 30:183–185

    Article  CAS  Google Scholar 

  • Maathuis FJ, Amtmann A (1999) K+ nutrition and Na+ toxicity: the basis of cellular K+/Na+ ratios. Ann Bot 84:123–133

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Ann Rev Plant Biol 59:651–681

    Article  CAS  Google Scholar 

  • Ouziad F, Wilde P, Schmelzer E, Hildebrandt U, Bothe H (2006) Analysis of expression of aquaporins and Na+/H+ transporters in tomato colonized by arbuscular mycorrhizal fungi and affected by salt stress. Environ Exper Bot 57:177–186

    Article  CAS  Google Scholar 

  • Pedranzani H, Rodríguez-Rivera M, Gutiérrez M, Porcel R, Hause B, Ruiz-Lozano JM (2016) Arbuscular mycorrhizal symbiosis regulates physiology and performance of Digitaria eriantha plants subjected to abiotic stresses by modulating antioxidant and jasmonate levels. Mycorrhiza 26:141–152

    Article  CAS  PubMed  Google Scholar 

  • Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55(1):158-IN18

    Article  Google Scholar 

  • Rinaldelli E, Mancuso S (1996) Response of young mycorrhizal and non-mycorrhizal plants of olive tree (Olea europaea L.) to saline conditions. I. Short-term electrophysiological and long-term vegetative salt effects. Adv Hortic Sci 10(3):126–134

    Google Scholar 

  • Rodríguez-Rosales MP, Jiang X, Gálvez FJ, Aranda MN, Cubero B, Venema K (2008) Overexpression of the tomato K+/H+ antiporter LeNHX2 confers salt tolerance by improving potassium compartmentalization. New Phytol 179(2):366–377. https://doi.org/10.1111/j.1469-8137.2008.02461.x

    Article  CAS  PubMed  Google Scholar 

  • Rohani N, Daneshmand F, Vaziri A, Mahmoudi M, Saber-Mahani F (2019) Growth and some physiological characteristics of Pistacia vera L. cv Ahmad Aghaei in response to cadmium stress and Glomus mosseae symbiosis. S Afr J Bot 124:499–507. https://doi.org/10.1016/j.sajb.2019.06.001

    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 Exper Bot 63:4033–4044

    Article  CAS  Google Scholar 

  • Sairam RK, Deshmukh PS, Shukla DS (1997) Tolerance to droughtand temperaturestress in relation to increasedantioxidant enzymeactivity in wheat. J Agron Crop Sci 178:171–177

    Article  CAS  Google Scholar 

  • Shamshiri M, 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 63:101–110

    Article  CAS  Google Scholar 

  • Soleymanian S, Abbaspour H, Nafchi AM (2017) Alleviation of salt stress in pistachio (Pistacia vera L) seedlings inoculated with arbuscular mycorrhiza fungi. PCBMB 57–67.

  • Soltabayeva A, Ongaltay A, Omondi JO, Srivastava S (2021) Morphological, Physiological and Molecular Markers for Salt-Stressed Plants. Plants Basel 27 10(2):243. https://doi.org/10.3390/plants10020243

    Article  CAS  Google Scholar 

  • Talaat NB, Shawky BT (2014) Protective effects of arbuscular mycorrhizal fungi on wheat (Triticum aestivum L.) plants exposed to salinity. Environ Exper Bot 98:20–31

    Article  CAS  Google Scholar 

  • Talukdar D (2012) Exogenous calcium alleviates the impact of cadmium-induced oxidative stress in lens culinaris medic. seedlings through modulation of antioxidant enzyme activities. JCSB 15:325–334

    Google Scholar 

  • Tavanti TR, Melo AAR, Moreira LDK, Sanchez DEJ, Silva RDS, Silva RMD, Reis ARD (2021) Micronutrient fertilization enhances ROS scavenging system for alleviation of abiotic stresses in plants. Plant Physiol Biochem 160:386–396. https://doi.org/10.1016/j.plaphy.2021.01.040

    Article  CAS  PubMed  Google Scholar 

  • Trindade AV, Siqueira JO, Stürmer SL (2006) Arbuscular mycorrhizal fungi in papaya plantations of Espirito Santo and Bahia, Brazil. Braz J Microbiol 37:283–289

    Article  Google Scholar 

  • Vajpai M, Mukherjee M, Sankararamakrishnan R (2018) Cooperativity in Plant Plasma Membrane Intrinsic Proteins (PIPs): Mechanism of Increased Water Transport in Maize PIP1 Channels in Hetero-tetramers. Sci Rep 8:12055. https://doi.org/10.1038/s41598-018-30257-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Volkov V (2015) Salinity tolerance in plants. Quantitative approach to ion transport starting from halophytes and stepping to genetic and protein engineering for manipulating ion fluxes. Front Plant Sci 6:873

    PubMed  PubMed Central  Google Scholar 

  • Wang YY, Hsu PK, Tsay YF (2012) Uptake, allocation and signaling of nitrate. Trends Plant Sci 17:458–467

    Article  CAS  PubMed  Google Scholar 

  • Wang F, Sun Y, Shi Z (2019) Arbuscular mycorrhiza enhances biomass production and salt tolerance of sweet sorghum. Microorganisms 7:289

    Article  CAS  PubMed Central  Google Scholar 

  • Wolf B (1982) A comprehensive system of leaf analyses and its use for diagnosing crop nutrient status. Commun Soil Sci Plant Anal 13(12):1035–1059

    Article  CAS  Google Scholar 

  • Yasseen B, Jurjee J, Sofajy S (1987) Changes in some growth processes induced by NaCl in individual leaves of two barley cultivars. Indian J Plant Physiol 30:1–6

    CAS  Google Scholar 

  • Ye L, Zhao X, Bao E, Cao K, Zou Z (2019) Effects of arbuscular mycorrhizal fungi on watermelon growth, nutritional uptake, antioxidant and photosystem II Activities and stress-response gene expressions under salinity-alkalinity stresses. Front Plant Sci 10:863. https://doi.org/10.3389/fpls.2019.00863.eCollection

    Article  PubMed  PubMed Central  Google Scholar 

  • Yin X, Xia Y, Xie Q, Cao Y, Wang Z, Hao G, Song J, Zhou Y, Jiang X (2020) The protein kinase complex CBL10-CIPK8-SOS1 functions in Arabidopsis to regulate salt tolerance. J Exp Bot 25 71(6):1801–1814. https://doi.org/10.1093/jxb/erz549

    Article  CAS  Google Scholar 

  • Zhang N, Zhao B, Zhang HJ, Weeda S, Yang C, Yang ZC, Ren S, Guo YD (2013) Melatonin promotes water-stress tolerance, lateral root formation, and seed germination in cucumber (Cucumis sativus L.). J Pineal Res 54:15–23

    Article  CAS  PubMed  Google Scholar 

  • 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 423:125–140

    Article  CAS  Google Scholar 

  • Zhao H, Ye L, Wang ZX, Yang J, Wang J, Cao K, Zou Z (2016) Melatonin increases the chilling tolerance of chloroplast in cucumber seedlings by regulating photosynthetic electron flux and the ascorbate-glutathione cycle. Front Plant Sci 7:2016. https://doi.org/10.3389/fpls.2016.01814.eCollection

    Article  Google Scholar 

  • Zou YN, Wu QS, Huang YM, Ni QD, He XH (2013) Mycorrhizal-mediated lower proline accumulation in Poncirus trifoliata under water deficit derives from the integration of inhibition of proline synthesis with increase of proline degradation. PLoS ONE 8(11):e80568. https://doi.org/10.1371/journal.pone.008056

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Biology Department, North Tehran Branch, Islamic Azad University, Tehran, Iran

    Hossein Abbaspour

  2. Biology Department, Neyshabur Branch, Islamic Azad University, Neyshabur, Iran

    Fatemeh S. N. Pour

  3. Food Toxicology and Contaminants Department, National Research Center, Cairo, Egypt

    Mosaad A. Abdel-Wahhab

Authors
  1. Hossein Abbaspour
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fatemeh S. N. Pour
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mosaad A. Abdel-Wahhab
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

H. Abbaspour and Fatemeh S. Nematpour conceived the original idea, carried out the experiment, performed the computations and verified the analytical methods. M.A. Abdel-Wahhab edited the manuscript with support from Abbaspour and Pour. All authors discussed the results and contributed to the final manuscript.

Corresponding authors

Correspondence to Hossein Abbaspour or Mosaad A. Abdel-Wahhab.

Ethics declarations

Conflicts of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Abbaspour, H., Pour, F.S.N. & Abdel-Wahhab, M.A. Arbuscular mycorrhizal symbiosis regulates the physiological responses, ion distribution and relevant gene expression to trigger salt stress tolerance in pistachio. Physiol Mol Biol Plants 27, 1765–1778 (2021). https://doi.org/10.1007/s12298-021-01043-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12298-021-01043-w

Keywords

Search

Navigation