Field Application of the Mycorrhizal Fungus Rhizophagus irregularis Increases the Yield of Wheat Crop and Affects Soil Microbial Functionalities


The aim of this study was to test the impact of Rhizophagus irregularis, an arbuscular mycorrhizal fungus (AMF), on durum wheat growth and soil microbial functionalities in a field inoculation trial conducted in Morocco. The results showed that i) the R. irregularis inoculum effectively improved wheat growth, ii) wheat growth promotion depended on the soil mycorrhizal infectivity and iii) functional abilities of soil microflora depended on AMF inoculation. This study confirms that field AMF inoculation can be proposed as an effective agronomic practice in wheat production and as a sustainable cultural practice to manage soil biofunctioning. To fully promote inoculation practices, a better knowledge of AMF ecology has to be acquired to better adapt AMF inoculation to environmental conditions, and thus warrant better yields and agricultural sustainability.

Share and Cite:

Wahbi, S. , Prin, Y. , Maghraoui, T. , Sanguin, H. , Thioulouse, J. , Oufdou, K. , Hafidi, M. and Duponnois, R. (2015) Field Application of the Mycorrhizal Fungus Rhizophagus irregularis Increases the Yield of Wheat Crop and Affects Soil Microbial Functionalities. American Journal of Plant Sciences, 6, 3205-3215. doi: 10.4236/ajps.2015.619312.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] Smith, S.E. and Read, D.J. (2008) Mycorrhizal Symbiosis. 3rd Edition, Academic Press, Amsterdam.
[2] van der Heijden, M.G.A., Klironomos, J.N., Ursic, M., Moutoglis, P., Streitwolf-Engel, R., Boller, T., Wiemken, A. and Sanders, I.R. (1998) Mycorrhizal Fungal Diversity Determines Plant Biodiversity, Ecosystem Variability and Productivity. Nature, 396, 72-75.
[3] Klironomos, J.N., McCune, J., Hart, M. and Neville, J. (2000) The Influence of Arbuscular Mycorrhizae on the Relationship between Plant Diversity and Productivity. Ecology Letters, 3, 137-141.
[4] O’Connor, P.J., Smith, S.E. and Smith, F.A. (2002) Arbuscular Mycorrhizas Influence Plant Diversity and Community Structure in a Semiarid Herbland. New Phytologist, 154, 209-218.
[5] West, H.M. (1996) Influence of Arbuscular Mycorrhizal Infection on Competition between Holcus lanatus and Dactylis glomerata. Journal of Ecology, 84, 429-438.
[6] Marler, M.J., Zabinski, C.A. and Callaway, R.M. (1999) Mycorrhizae Indirectly Enhance Competitive Effects of an Invasive Forb on a Native Bunchgrass. Ecology, 80, 1180-1186.[1180:MIECEO]2.0.CO;2
[7] van der Heijden, M.G.A., Wiemken, A. and Sanders, I.R. (2003) Different Arbuscular Mycorrhizal Fungi Alter Coexistence and Resource Distribution between Co-Occurring Plant. New Phytologist, 157, 569-578.
[8] Rambelli, A. (1973) The Rhizosphere of Mycorrhizae. In: Marks, G.C. and Kozlowski, T.T., Eds., Ectomycorrhizae: Their Ecology and Physiology, Academic Press, New York, 299-343.
[9] Leyval, C. and Berthelin, J. (1993) Rhizodeposition and Net Release of Soluble Compounds by Pine and Beech Seedlings Inoculated with Rhizobacteria and Ectomycorrhizal Fungi. Biology and Fertility of Soils, 15, 259-267.
[10] Linderman, R.G. (1988) Mycorrhizal Interactions with the Rhizosphere Microflora: The Mycorrhizosphere Effect. Phytopathology, 78, 366-371.
[11] Linderman, R.G. (2008) The Mycorrhizosphere Phenomenon. In: Feldman, F., Kapulnik, Y. and Barr, J., Eds., Mycorrhiza Works, Deutsche Phytomedizinische Gesellschaft, Braunschweig, 341-355.
[12] Johansson, J.F., Paul, L.R. and Finlay, P.R. (2004) Microbial Interactions in the Mycorrhizosphere and Their Significance for Sustainable Agriculture. FEMS Microbiology and Ecology, 48, 1-13.
[13] Duponnois, R., Colombet, A., Hien, V. and Thioulouse, J. (2005) The Mycorrhizal Fungus Glomus intraradices and Rock Phosphate Amendment Influence Plant Growth and Microbial Activity in the Rhizosphere of Acacia holosericea. Soil Biology and Biochemistry, 37, 1460-1468.
[14] Artursson, V., Finlay, R.D. and Jansson, J.K. (2006) Interactions between Arbuscular Mycorrhizal Fungi and Bacteria and Their Potential for Stimulating Plant Growth. Environmental Microbiology, 8, 1-10.
[15] Klironomos, J.N. (2000) Host-Specificity and Functional Diversity among Arbuscular Mycorrhizal Fungi. In: Bell, C.R., Brylinski, M. and Johnson-Green, P., Eds., Proceedings of the 8th International Symposium on Microbial Ecology, Atlantic Canada Society from Microbial Ecology, Halifax, 845-851.
[16] Munkvold, L., Kjoller, R., Vestberg, M., Rosendahl, S. and Jakobsen, I. (2004) High Functional Diversity within Species of Arbuscular Mycorrhizal Fungi. New Phytologist, 164, 357-364.
[17] Lekberg, Y. and Koide, T. (2005) Is Plant Performance Limited by Abundance of Arbuscular Mycorrhizal Fungi? A Meta-Analysis of Studies Published between 1988 and 2003. New Phytologist, 168, 189-204.
[18] Avio, L., Pellegrino, E., Bonari, E. and Giovannetti, M. (2006) Functional Diversity of Arbuscular Mycorrhizal Fungal Isolates in Relation to Extraradical Mycelial Network. New Phytologist, 172, 347-357.
[19] Wilcox, J. and Makowski, D. (2014) A Meta-Analysis of the Predicted Effects of Climate Change on Wheat Yields Using Simulation Studies. Field Crops Research, 156, 180-190.
[20] Campiglia, E., Mancinelli, R., De Stefanis, E., Pucciarmati, S. and Radicetti, E. (2015) The long-Term Effects of Conventional and Organic Cropping Systems, Tillage Managements and Weather Conditions on Yield and Grain Quality of Durum Wheat (Triticum durum Desf.) in the Mediterranean Environment of Central Italy. Field Crops Research, 176, 34-44.
[21] Simane, B., Peacock, J.M. and Struik, P.C. (1993) Differences in Developmental Plasticity and Growth Rate among Drought-Resistant and Susceptible Cultivars of Durum Ehat (Triticum turgidum L. var. durum). Plant & Soil, 157, 155-166.
[22] Hetrick, B.A.D., Wilson, G.W.T. and Cox, T.S. (1993) Mycorrhizal Dependence of Modern Wheat Cultivars and Ancestors: A Synthesis. Canadian Journal of Botany, 71, 512-518.
[23] Pellegrino, E., Opik, M., Bonari, E. and Ercoli, L. (2015) Responses of Wheat to Arbuscular Fungi: A Meta-Analysis of Field Studies from 1975 to 2013. Soil Biology & Biochemistry, 84, 210-217.
[24] John, M.K. (1970) Colorimetric Determination in Soil and Plant Material with Ascorbic Acid. Soil Science, 68, 171-177.
[25] Phillips, J.M. and Hayman, D.S. (1970) Improved Procedures for Clearing Roots and Staining Parasitic and Vesicular-Arbuscular Mycorrhizal Fungi for Rapid Assessment of Infection. Transactions of the British Mycological Society, 55, 158-161.
[26] Giovanetti, M. and Mosse, B. (1980) An Evaluation of Techniques for Measuring Vesicular Arbuscular Mycorrhizal Infection in Roots. New Phytologist, 84, 489-500.
[27] Rubio, R., Borie, F., Schalchli, C., Castillo, C. and Azcon, R. (2003) Occurrence and Effect of Arbuscular Mycorrhizal Propagules in Wheat as Affected by the Source and Amount of Phosphorus Fertilizer and Fungal Inoculation. Applied Soil Ecology, 23, 245-255.
[28] Degens, B.P. and Harris, J.A. (1997) Development of a Physiological Approach to Measuring the Metabolic Diversity of Soil Microbial Communities. Soil Biology & Biochemistry, 29, 1309-1320.
[29] Boudiaf, I., Baudoin, E., Sanguin, H., Beddiar, A., Thioulouse, J., Galiana, A., Prin Y., Le Roux, C., Lebrun, M. and Duponnois R. (2013) The Exotic Legume Tree Species, Acacia mearnsii, Alters Microbial Soil Functionalities and the Early Development of a Native Tree Species, Quercus suber, in North Africa. Soil Biology and Biochemistry, 65, 172-179.
[30] Magurran, A.E. (1988) Ecological Diversity and Its Measurement. Croom Helm, London.
[31] Kisa, M., Sanon, A., Thioulouse, J., Assigbetse, K., Sylla, S., Spichiger, R., Dieng, L., Berthelin, J., Prin, Y., Galiana, A., Lepage, M. and Duponnopis, R. (2007) Arbuscular Mycorrhizal Symbiosis Can Counterbalance the Negative Influence of the Exotic Tree Species Eucalyptus camaldulensis on the Structure and Functioning of Soil Microbial Communities in a Sahelian Soil. FEMS Microbiology Ecology, 62, 32-44.
[32] Venables, W.N. and Ripley, B.D. (2002) Modern Applied Statistics. Springer, New York.
[33] R Development Core Team (2010) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
[34] Pinheiro, J.C. and Bates, D.M. (2000) Mixed-Effects Models in S and S-PLUS. Springer, New York.
[35] Ryan, M.H., Chilvers, G.A. and Dumarsq, D.C. (1994) Colonization of Wheat by VA Mycorrhizal Fungi Was Found to Higher on a Farm Managed in an Organic Manner than on a Conventional Neighbour. Plant & Soil, 160, 33-40.
[36] Graham, J.H. and Abbott, L.K. (2000) Wheat Responses to Aggressive and Non-Aggressive Arbuscular Mycorrhizal Fungi. Plant & Soil, 220, 207-218.
[37] Duponnois, R. and Plenchette, C. (2003) A Mycorrhiza Helper Bacterium (MHB) Enhances Ectomycorrhizal and Endomycorrhizal Symbiosis of Australian Acacia Species. Mycorrhiza, 13, 85-91.
[38] Dabire, A.P., Hien, V., Kisa, M., Bilgo, A., Sangare, K.S., Plenchette, C., Galiana, A., Prin, Y. and Duponnois, R. (2007) Responses of Soil Microbial Catabolic Diversity to Arbuscular Mycorrhizal Inoculation and Soil Disinfection. Mycorrhiza, 17, 537-545.
[39] Xavier, L.J. and Germida, J.J. (1997) Growth Response of Lentil and Wheat to Glomus clarum NT4 over a Range of P Levels in a Saskatchewan Soil Containing Indigenous AM Fungi. Mycorrhiza, 7, 3-8.
[40] Al-Karaki, G.N. and Clark, R.B. (1999) Mycorrhizal Influence on Protein and Lipid of Durum Wheat Grown at Different Soil Phosphorus Levels. Mycorrhiza, 9, 97-101.
[41] Lehmann, A., Barto, K., Powell, J.R. and Rillig, M.C. (2012) Mycorrhizal Responsiveness Trends in Annual Crop Plants and Their Wild Relatives: A Meta-Analysis on Studies from 1981 to 2010. Plant & Soil, 355, 231-250.
[42] Verbruggen, E., van der Heijden, M.G.A., Rillig, M.C. and Kiers, E.T. (2012) Mycorrhizal Fungal Establishment in Agricultural Soils: Factors Determining Inoculation Success. New Phytologist, 197, 1025-1026.
[43] Romina Romaniuk, R., Giuffré, L., Costantini, A. and Nannipieri, P. (2011) Assessment of Soil Microbial Diversity Measurements as Indicators of Soil Functioning in Organic and Conventional Horticulture Systems. Ecological Indicators, 11, 1345-1353.
[44] Bilgo, A., Sangare, K.S., Thioulouse, J., Prin, Y., Hien, V., Galiana, A., Baudoin, E., Hafidi, M., Ba, A.M. and Duponnois, R. (2011) Response of Native Soil Microbial Functions to the Controlled Mycorrhization of an Exotic Tree Legume, Acacia holosericea in a Sahelian Ecosystem. Mycorrhiza, 22, 175-187.
[45] Giller, K.E., Beare, M.H., Lavelle, P., Izac, A.M.N. and Swift, M.J. (1997) Agricultural Intensification, Soil Biodiversity and Agrosystem Function. Applied Soil Ecology, 6, 3-16.
[46] Degens, B.P. (1998) Decreases in Microbial Functional Diversity Do Not Result in Corresponding Changes in Decomposition under Different Moisture Conditions. Soil Biology & Biochemistry, 30, 1989-2000.
[47] Degens, B.P., Schipper, L.A., Sparling, G.P. and Duncan, L.C. (2001) Is the Microbial Community in a Soil with Reduced Catabolic Diversity Less Resistant to Stress or Disturbance? Soil Biology & Biochemistry, 33, 1143-1153.
[48] Ryan, P.R., Delhaise, E. and Jones, D.L. (2001) Function and Mechanism of Organic Anion Exudation from Plant Roots. Annual Review of Plant Physiology, 52, 527-560.
[49] Illmer, P. and Schinner, F. (1992) Solubilization of Inorganic Phosphate by Microorganisms Isolated from Forest Soil. Soil Biology & Biochemistry, 24, 389-395.

Copyright © 2022 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.