Effects of Arbuscular Mycorrhizal Fungi on Growth and Nutrient Uptake of Apple Rootstocks in Calcareous Soil

Document Type: Research paper


Department of Horticultural Science, College of Agriculture, Shiraz University


The effects of three Arbuscular Mycorrhizal Fungi (AMF) species (Glomus versiforme, Claroideoglomus etunicatum and Rhizophagus intraradices) were studied on the growth parameters and nutrient uptake of three apple rootstocks (M.9, M.7 and MM.106). The soil medium contained a high level of calcium carbonate (38.65%). The results showed that AMF inoculation could increase almost all growth parameters. Plants inoculated with G. versiforme had the highest shoot height, stem diameter, leaf size, and biomass compared to other AMF species. Rootstocks also varied substantially in their growth. MM.106 exhibited the highest growth in general, whereas the M.9 had the lowest. Plants inoculated with mycorrhizal fungi contained more N, P, Ca, Mg, Zn, and Fe compared to those of Non Mycorhizal (NM) control plants. However, AMF inoculation did not influence concentrations of K, Cu, and Mn in the leaf. Rootstocks exhibited various nutrient concentrations in their leaves and the highest concentrations of K, Ca, Mg, and Zn were measured in MM.106. The highest leaf concentration of N, Fe, Mn, and Cu occurred in M.9, while the M.7 accumulated the highest amount of P in its leaves. Here we demonstrate the beneficial effects of symbiosis between apple rootstocks and AMF species in calcareous soil with a very high level of lime concentration.


Aguirre, P.B., Y.K. Al-Hinai, T.R. Roper, and A.R. Krueger. 2001. Apple Tree Rootstock and Fertilizer Application Timing Affect Nitrogen Uptake. HortScience 36 (7):1202-1205.
Aliasgharzadeh, N., N.S. Rastin, H. Towfighi, and A. Alizadeh. 2001. Occurrence of Arbuscular Mycorrhizal Fungi in Saline Soils of the Tabriz Plain of Iran in Relation to Some Physical and Chemical Properties of Soil. Mycorrhiza 11:119–122.
Amiri, M.E., and E. Fallahi. 2009. Potential of Mineral Uptake Efficiency by Some Apple Rootstocks. The proceedings of the International Plant Nutrition Colloquium XVI, Dep. Plant Sci., UC Davis.
Ardestani, M. 2015. Analysis of Apple Market in Iran and the World. Ministry of Agriculture, Research Institute for Planning, Agricultural Economy and Rural Development. (in Farsi) 22 p.
Arines, J., A. Vilarijo, and M. Sainz. 1989. Effect of Different Inoculums of VAM Fungi on Manganese Content and Content and Concentration in Red Clover Plants. New Phytol. 112:215-219.
Aroca, R., R. Porcel, and J.M. Ruiz-Lozano. 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. 173:808-816.
Bremner, J.M. 1996. Nitrogen Total. PP.1085-1122. In: Klute, A., et al. (Eds.), Methods of Soil Analysis, Part III, 3rdEd. ASA, Madison, WI.
Bolan, N.S. 1991. A Critical Review on the Role of Mycorrhizal Fungi in the Uptake of Phosphorus by Plants. Plant Soil 134:189–207.
Caris, C., W. Hördt, H.J. Hawkins, V. Römheld, and E. George. 1998. Studies of Iron Transport by Arbuscular Mycorrhizal Hyphae from Soil to Peanut and Sorghum Plants. Mycorrhiza 8:35–39.
Cavallazzi, J.R.P., O.K. Filho, S.L. Stürmer, P.T. Rygiewicz, M.M. de Mendonça. 2007. Screening and Selecting Arbuscular Mycorrhizal Fungi Forinoculating Micropropagated Apple Rootstocks in Acid Soils. Plant Cell Tiss. Organ Cult. 90:117–129.
Chapman, H.D., and D.F. Pratt. 1961. Methods of Analysis for Soil, Plant, and Water. Univ. of Calif., Div. of Agr. Sci., 60 p.
Dong, S., L. Cheng, and L.H. Fuchigami. 1998. Nutrient Uptake by New Roots of Six Clonal Apple Rootstocks. HortScience 34:492.
Fallahi, E., B.R. Simons, J.K. Fellman, M.A. Longstroth, and W.M. Colt. 1994. Tree Growth and Productivity and Postharvest Fruit Quality in Various Strains of ‘Delicious’ Apple. J. Amer. Soc. Hort. Sci. 119:389-395.
Fallahi, E., W.M. Colt, B. Fallahi, and Ik-Jo Chun. 2002. The Importance of Apple Rootstocks on Tree Growth, Yield, Fruit Quality, Leaf Nutrition, and Photosynthesis with an Emphasis on ‘Fuji’. HortTechnology 12 (1):38-44.
FAOSTAT. 2013. Food and Agriculture Organization of the United Nations. Available at: http://faostat. Fao.Org/336.default.Asp.
Gange, A.C. 2001. Species-Specific Responses of a Root- And Shoot-Feeding Insect to Arbuscular Mycorrhizal Colonization of Its Host Plant. New Phytol. 150:611-618.
Geddeda, Y.I., J.M. Trappe, and R.L. Stebbins. 1984. Effects of Vesicular–Arbuscular Mycorrhizae and Phosphorus on Apple Seedlings. J. Aemr. Soc. Hort. Sci. 109:24–27.
Gnekow, M.A., and H. Marschner. 1989. Role of VA-mycorrhiza in Growth and Mineral Nutrition of Apple (Malus pulmila var. domestica) Rootstock Cuttings. Plant Soil 119:285–293.
Graham, J.H. 2000. Assessing Costs of Arbuscular Mycorrhizal Symbiosis in 

Agroecosystems. In G.K. Podila, and J.R. Douds, Eds, Current Advances in Mycorrhizae Research. American Phytopathological Society Press, St. Paul, MN, pp. 127–140
Harrison, M.J., and M.L. Van Buuren. 1995. A Phosphate Transporter from the Mycorrhizal Fungus Glomus versiforme. Nature 378:626-629.
Hildebrandt, U., F. Ouziad, F.J. Marner, and H. Bothe. 2006. The Bacterium Paenibacillus validus Stimulates Growth of the Arbuscular Mycorrhizal Fungus Glomus intraradices up to the Formation of Fertile Spores. FEMS Microbiol. Lett. 254:258–267.
Hoda, A.K., M.E. Ahmed, M.E.S. Samy, and M.A.N. Amal. 2011. Improved Growth of Salinity- Stressed Citrus after Inoculation with Mycorrhizal Fungi. Scientia Hort. 130:624-632.
Hodge, A., T. Helgason, and A.H. Fitter. 2010. Nutritional ecology of arbuscular mycorrhizal fungi. Fungal Ecol. 3: 267-273.
Hodge, A, C.D. Campbell, and A.H. Fitter. 2001. An Arbuscular Mycorrhizal Fungus Accelerates Decomposition and Acquires Nitrogen Directly from Organic Material. Nature 413:297–299.
Kariman, K.H., E.M. Goltapeh, and V. Minassian. 2005. Arbuscular Mycorrhizal Fungi from Iran. J. Agr. Technol. 1(2):301-313.
Kayan, N. 2008. Variation for Yield Components in Two Winter Sown Lentil Cultivars (Lens culinaris Medic.). Bulg. J. Agr. Sci. 14:460-465.
Koltai, H., V. Gadkar, and Y. Kapulnik. 2010. Biochemical and Practical Views of Arbuscular Mycorrhizal Fungus-Host Association in Horticultural Crops. Hort. Rev. 36:257–287.
Kormanik, P.P., and A.C. McGraw. 1982. Quantification of Vesicular-Arbuscular Mycorrhizae in Plant Roots. In: N.C. Schenck (Eds.) Methods and Principles of Mycorrhizal Research. The American Phytopathological Society. pp. 37-36.
Kucukyumuk, Z., and I. Erdal. 2011. Rootstocks and Cultivar Effect on Mineral Nutrition, Seasonal Nutrient Variation and Correlations Among Leaf, Flower and Fruit Nutrient Concentration in Apple Trees. Bulg. J. Agr. Sci. 17 (No 5):633-641.
Liu, A., C. Hamel, R.I. Hamilton, B.L. Ma, and D.L. Smith. 2000. Acquisition of Cu, Zn, Mn and Fe by Mycorrhizal Maize (Zea mays L.)
Grown in Soil at Different P and Micronutrient Levels. Mycorrhiza 9:331–336. Liu, R. and F. Wang. 2003. Selection of Appropriate Host Plants Used in Trap Culture of Arbuscular Mycorrhizal Fungi. Mycorrhiza 13:123–127
Malakouti, M. J. 2006. Nutritional Disorders in Fruit Trees on the Calcareous Soils of Iran. Proceedings of the 18th World Congress of Soil Science: Frontiers of Soil science Technology and the Information Age. Philadelphia, Pennsylvania, USA. Miller, D.D., P.A. Domoto, and C. Walker 1985 Colonization and Efficacy of Different Endomycorrhizal Fungi with Apple Seedlings at Two Phosphorus Levels. New Phytol. 100:393–402.
Morin, F., J.A. Fortin, C. Hamel, and D.L. Smith. 1994. Apple Rootstock Response to Vesicular-Arbuscular Mycorrhizal Fungi in a High Phosphorus Soil. J. Amer. Soc. Hort. Sci. 119 (3):578-583.
Neilsen, G.H., P. Parchomchuk, R. Berard, and D. Neilsen. 1997. Irrigation Frequency and Quantity Affect Root and Top Growth of Fertigated ‘Mcintosh’ Apple on M.9, M.26 and M.7 Rootstock. Can. J. Plant Sci. 77:133–139.
Schnepf, A., D. Jones, and T. Roose. 2011. Modelling Nutrient Uptake by Individual Hyphae of Arbuscular Mycorrhizal Fungi: Temporal and Spatial Scales for an Experimental Design. Bull. Math. Biol. 73:2175-2200.
Schubert, A., and G. Lubraco. 2000. Mycorrhizal Inoculation Enhances Growth and Nutrient Uptake of Micropropagated Apple Rootstocks During Weaning in Commercial Substrates of High Nutrient Availability. Appl. Soil Ecol. 15:113–118. Sharma, S.D., N.C. Sharma, C.L. Sharma, P. Kumar, A. Chandel. 2012. Glomus–Azotobacter Symbiosis in Apple under Reduced Inorganic Nutrient Fertilization for Sustainable and Economic Orcharding Enterprise. Scientia Hort. 146:175–181.
Smith, F.A., E.J. Grace, and S.E. Smith. 2009. More than a Carbon Economy: Nutrient Trade and Ecological Sustainability in Facultative Arbuscular Mycorrhizal Symbioses. New Phytol. 182: 347-358.
Vigo, C., J.R. Norman, and J.E. Hooker. 2000. Biocontrol of the Pathogen Phytophthora parasitica by Arbuscular Mycorrhizal Fungi is a 

Consequence of Effects on Infection Loci. Plant Pathol. 49:509–514.
Webster, A.D. and S.J. Wertheim. 2003. Apple rootstocks. In; Ferree, D.C., and I.J. Warrington (Eds.). Apples, Botany, Production and Uses. CABI Publishing. pp. 91-125.
Wu, Q.S., G.H. Li, and Y.N. Zou. 2011. Roles of Arbuscular Mycorrhizal Fungi on Growth and Nutrient Acquistion of Peach (Prunus persica L. Batsch) Seedling. J. Animal plant Sci. 21 (4):746-750.
Yano-Melo, A.M., L.C. Maia, O.J. Sagginjr, J.M. Lima Filaho, and N.F. Melo. 1999. Effect of Arbuscular Mycorrhizal Fungi on the Acclimatization of Micro Propagated Banana Plantlets. Mycorrhiza 9:119-123.
Zarei, M., S. König, S. Hempel, M.K. Nekouei, G.H. Savaghebi, and F. Buscot. 2008a. Community Structure of Arbuscular
Mycorrhizal Fungi Associated to Veronica rechingeri at the Anguran Zinc and Lead Mining Region. Environmental Pollution. 156:1277–1283.
Zarei, M., N. Saleh-Rastin, G.H. Salehi Jouzani, G.H. Savaghebi, and F. Buscot. 2008b. Arbuscular Mycorrhizal Abundance in Contaminated Soils Around a Zinc and Lead Deposit. European J. Soil. Biol. 44:381-391.
Zarei, M., N. Saleh-Rastin, H.A. Alikhani, and N. Aliasgharzadeh. 2006. Responses of Lentil to Co-inoculation with Phosphate-Solubilisingrhizobial Strains and Arbuscular Mycorrhizal Fungi. J. Plant Nut. 29:1509-1522.