The Influence of Bioproducts on Mycorrhizal Occurrence and Diversity in the Rhizosphere of Strawberry Plants under Controlled Conditions


The new products obtained from natural resources are an alternative to methods based on traditional mineral fertilizers, which are destructive for soil mycorrhizal communities. Our experiment was carried out to evaluate the effect of organic fertilizers and amendments of very diverse composition on mycorrhizal abundance and diversity, as well as on root growth, in strawberry plants cv. “Honeoye”. The plants were grown in rhizoboxes filled with a podsolic soil. The plants were treated with granulated bovine manure, vermicompost extract, humates extract, plant extract, extract from seaweed species reinforced with humic and fulvic acids, a consortium of beneficial soil organisms, a stillage from yeast production and a solution of titanium. Plants treated with products and the microorganisms consortium also received half dose of manure. A standard mineral fertilization (NPK) and an unfertilized control were also included. The bioproducts based on humus-like substances and the yeast stillage had the greatest positive influence on the colonization of roots by arbuscular mycorrhizal fungi (AMF). The different treatments affected the diversity of AMF species present in the rhizospheric soil. All organic products, even though providing a significantly low amount of nutrients, enhanced root growth characteristics in comparison to the mineral fertilization.

Share and Cite:

Paszt, L. , Malusá, E. , Sumorok, B. , Canfora, L. , Derkowska, E. and Głuszek, S. (2015) The Influence of Bioproducts on Mycorrhizal Occurrence and Diversity in the Rhizosphere of Strawberry Plants under Controlled Conditions. Advances in Microbiology, 5, 40-53. doi: 10.4236/aim.2015.51005.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] Barak, P., Jobe, B., Krueger, A., Peterson, L. and Laird, D. (1997) Effects of Long-Term Soil Acidification Due to Nitrogen Fertilizer Inputs in Wisconsin. Plant and Soil, 197, 61-69.
[2] Marschner, P., Kandeler, E. and Marschner, B. (2003) Structure and Function of the Soil Microbial Community in a Long-Term Fertilizer Experiment. Soil Biology and Biochemistry, 35, 453-461.
[3] Malusá, E., Sas Paszt, L., Gluszek, S. and Ciesielska, J. (2014) Organic Fertilizers to Sustain Soil Fertility. In: Sinha, S. and Pant, K., Eds., “Fertilizers Technology Vol. 1: Synthesis”, Publishers Studium Press LLC, Houston, USA, 256-281.
[4] Kauffman, G.L., Kneivel, D.P. and Watschke, T.L. (2007) Effects of a Biostimulant on the Heat Tolerance Associated with Photosynthetic Capacity, Membrane Thermostability, and Polyphenol Production of Perennial Ryegrass. Crop Science, 47, 261-267.
[5] Corte, L., Dell’Abate, M.T., Magini, A., Migliore, M., Felici, B., Roscini, L., Sardella, R., Tancini, B., Emiliani, C., Cardinali, G. and Benedetti, A. (2013) Assessment of Safety and Efficiency of Nitrogen Organic Fertilizers from Animal-Based Protein Hydrolysates—A Laboratory Multidisciplinary Approach 2013. Journal of the Science Food Agriculture, 94, 235-245.
[6] Craigie, J. (2011) Seaweed Extract Stimuli in Plant Science and Agriculture. Journal of Applied Phycology, 23, 371-393.
[7] Wally, O.D., Critchley, A., Hiltz, D., Craigie, J., Han, X., Zaharia L.I., Abrams, S. and Prithiviraj, B. (2013) Regulation of Phytohormone Biosynthesis and Accumulation in Arabidopsis Following Treatment with Commercial Extract from the Marine Macroalga Ascophyllum nodosum. Journal of Plant Growth Regulation, 32, 324-339.
[8] Kuwada, K., Kuramoto, M., Utamura, M., Matsushita, I., Shibata, Y. and Ishii, T. (2005) Effect of Mannitol from Laminaria japonica, Other Sugar Alcohols, and Marine Alga Polysaccharides on in Vitro Hyphal Growth of Gigaspora margarita and Root Colonization of Trifoliate Orange. Plant and Soil, 276, 279-286.
[9] Kuwada, K., Wamocho, L.S., Utamur, M., Matsushita, I. and Ishii, T. (2006) Effect of Red and Green Algal Extracts on Hyphal Growth of Arbuscular Mycorrhizal Fungi, and on Mycorrhizal Development and Growth of Papaya and Passionfruit. Agronomy Journal, 98, 1340-1344.
[10] Chen, J. (2006) The Combined Use of Chemical and Organic Fertilizers and/or Biofertilizer for Crop Growth and Soil Fertility. International Workshop on Sustained Management of the Soil-Rhizosphere System for Efficient Crop Production and Fertilizer Use, Bangkok, 1-11.
[11] Smith, S.E. and Read, D.J. (2008) Mycorrhizal Symbiosis. 3rd Edition, Elsevier and Academic, New York, London, Burlington, San Diego.
[12] Bardi, L. and Malusá, E. (2012) Drought and Nutritional Stresses in Plant: Alleviating Role of Rhizospheric Microorganisms. In: Haryana, N. and Punj, S., Eds., Abiotic Stress: New Research, Nova Science Publishers, Inc., Hauppauge, 1-57.
[13] Dunne, M.J. and Fitter, A.H. (1989) The Phosphorus Budget of Field-Grown Strawberry (Fragaria x ananassa cv. Hapil) Crop: Evidence for a Mycorrhizal Contribution. Annals of Applied Biology, 114, 185-193.
[14] Sas Paszt, L. and Zurawicz, E. (2005) Studies of the Rhizosphere of Strawberry Plants at the Research Institute of Pomology and Floriculture in Skierniewice, Poland. International Journal of Plant Science, 5, 115-126.
[15] Derkowska, E., Sas Paszt, L., Sumorok, B., Szwonek, E. and Gluszek, S. (2008) The Influence of Mycorrhization and Organic Mulches on Mycorrhizal Frequency in Apple and Strawberry Roots. Journal Fruit Ornamental Plant Research, 16, 227-242.
[16] Didier, M.F., Hamel, C., Dalpé, Y. and Khanizadeh, S. (2003) Diversity of Native Endomycorrhizal Fungi in Selected Strawberry Field Soils of Southern Quebec. Small Fruits Review, 2, 61-71.
[17] Botham, R., Collin, C. and Ashman, T. (2009) Plant-Mycorrhizal Fungus Interactions Affect the Expression of Inbreeding Depression in Wild Strawberry. International Journal of Plant Science, 170, 143-150.
[18] Sas Paszt, L., Sumorok, B., Malusá, E., Gluszek, S. and Derkowska, E. (2011) The Influence of Bioproducts on Root Growth and Mycorrhizal Occurrence in the Rhizosphere of Strawberry Plants cv. “Elsanta”. Journal of Fruit and Ornamental Plant Research, 19, 13-34.
[19] Azcón-Aquilar, C. and Barea, J.M. (1992) Interactions between Mycorrhizal Fungi and Other Rhizosphere Microorganisms. In: Allen, M.J., Ed., Mycorrhizal Functioning. An Integrative Plant-Fungal Process, CH Publishing, Ottawa, Canada, 163-198.
[20] Oehl, F., Sieverding, E., Mader, P., Dubois, D., Ineichen, K., Boller, T. and Wiemken, A. (2004) Impact of Long-Term Conventional and Organic Farming on the Diversity of Arbuscular Mycorrhizal Fungi. Oecologia, 138, 574-583.
[21] Borowicz, V.A. (2010) The Impact of Arbuscular Mycorrhizal Fungi on Strawberry Tolerance to Root Damage and Drought Stress. Pedobiologia, 53, 265-270.
[22] Li, H., Smith, F.A., Dickson, S., Holloway, R.E. and Smith, S.E. (2008) Plant Growth Depressions in Arbuscular Mycorrhizal Symbioses: Not Just Caused by Carbon Drain? New Phytologist, 178, 852-862.
[23] Schroeder, M.S. and Janos, D.P. (2004) Phosphorus and Intraspecific Density Alter Plant Responses to Arbuscular Mycorrhizas. Plant and Soil, 264, 335-348.
[24] Gosling, P., Hodge, A., Goodlass, G. and Bending, G.D. (2006) Arbuscular Mycorrhizal Fungi and Organic Farming. Agriculture, Ecosystems & Environment, 113, 17-35.
[25] Philips, J.M. and Hayman, D.A. (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] Turnau, K., Ryszka, P., Gianinazzi-Pearson, V. and van Tuinen, D. (2001) Identification of Arbuscular Mycorrhizal Fungi in Soils and Roots of Plants Colonizing Zinc Wastes in Southern Poland. Mycorrhiza, 10, 169-174.
[27] Sumorok, B., Michalska-Hejduk, D. and Sas Paszt, L. (2008) Badania mikoryz u roslin zbiorowisk okresowo zalewanych. In: Mulenko, W., Ed., Mikologiczne badania terenowe. Przewodnik metodyczny, Wydawnictwo UMCS, Lublin, Poland, 132-141.
[28] Trouvelot, A., Kough, J.L. and Gianinazzi-Pearson, V. (1986) Mesure du taux de mycorhization VA d’un systeme radiculaire. Recherche de methods d’estimation ayant une signification fonctionnelle. In: Gianinazzi-Pearson, V., Gianinazzi, S., Eds., Physiological and Genetical Aspects of Mycorrhizae, INRA, Paris, 217-221.
[29] Blaszkowski, J. (2003) Arbuscular Mycorrhizal Fungi (Glomeromycota). Endogone and Complexipes Species Deposited in the Department of Plant Pathology, University of Agriculture in Szczecin, Poland.
[30] Brundrett, M.C., Bougher, N., Dell, B., Grove, T. and Malajczuk, N. (1996) Working with Mycorrhizas in Forestry and Agriculture. ACIAR Monograph Series, Pirie Printers, Canberra, 374.
[31] Blaszkowski, J. (2008) Metody izolowania, hodowania i identyfikowania arbuskularnych grzybów mikoryzowych z gromady Glomeromycota. In: Mulenko, W., Ed., Mikologiczne badania terenowe. Przewodnik metodyczny, Wydawnictwo UMCS, Lublin, Poland, 142-163.
[32] Schüßler, A. and Walker, C. (2010) The Glomeromycota: A Species List with New Families and New Genera. Schüßler, A., Walker, C., Gloucester, published in libraries at Royal Botanic Garden Edinburgh, Kew, Botanische Staatssammlung Munich, and Oregon State University.
[33] Ostrowska, A., Gawliński, S. and Szczubialka, Z. (1991) Metody analizy i ocen wlasciwosci gleb i roslin. Instytut Ochrony Srodowiska, Warszawa, Poland.
[34] Berta, G., Trotta, A., Fusconi, A., Hooker, J., Munro, M., Atkinson, D., Giovannetti, M., Marini, S., Fortuna, P., Tisserant, B., Gianinazzi-Pearson, V. and Gianinazzi, S. (1995) Arbuscular Mycorrhizal Induced Changes to Plant Growth and Root System Morphology in Prunus cerasifera. Tree Physiology, 15, 281-293.
[35] Gryndler, M., Hrselová, H., Sudová, R., Gryndlerová, H., Rezácová, V. and Merhautová, V. (2005) Hyphal Growth and Mycorrhiza Formation by the Arbuscular Mycorrhizal Fungus Glomus claroideum BEG 23 Is Stimulated by Humic Substances. Mycorrhiza, 15, 483-488.
[36] Nardi, S., Pizzeghello, D., Muscolo, A. and Vianello, A. (2002) Physiological Effects of Humic Substances on Higher Plants. Soil Biology & Biochemistry, 34, 1527-1536.
[37] Ayuso, M., Hernandez, T., Garcia, C. and Pascual, J.A. (1996) Stimulation of Barley Growth and Nutrient Absorption by Humic Substances Originating from Various Organic Materials. Bioresource Technology, 57, 251-257.
[38] Tahir, M.M., Khurshid, M., Khan, M.Z., Abbasi, M.K. and Kazmi, M.H. (2011) Lignite-Derived Humic Acid Effect on Growth of Wheat Plants in Different Soils. Pedosphere, 21, 124-131.
[39] Kuwada, K., Kuramoto, M., Utamura, M., Matsushita, I. and Ishii, T. (2006) Isolation and Structural Elucidation of a Growth Stimulant for Arbuscular Mycorrhizal Fungus from Laminaria japonica Areschoug. Journal of Applied Phycology, 18, 795-800.
[40] Kuwada, K., Ishii, T., Matsushita, I., Matsumoto, I. and Kadoya, K. (1999) Effect of Seaweed Extracts on Hyphal Growth of Vesicular-Arbuscular Mycorrhizal Fungi and Their Infectivity on Trifoliate Orange Roots. Journal of the Japanese Society for Horticultural Science, 68, 321-326.
[41] Luthje, S. and Bottger, M. (1995) On the Function of a K-Type Vitamin in Plasma Membranes of Maize (Zea mays L.) Roots. Mitteilungen Aus Dem Institut für Allgemeine Botanik der Universitat Hamburg, 25, 5-13.
[42] Bansal, M. and Mukerji, K.G. (1994) Positive Correlation between AM-Induced Changes in Root Exudation and Mycorrhizosphere Mycoflora. Mycorrhiza, 5, 39-44.
[43] Bücking, H., Abubaker, J., Govindarajulu, M., Tala, M., Pfeffer, P.E., Nagahashi, G., Lammers, P. and Shachar-Hill, Y. (2008) Root Exudates Stimulate the Uptake and Metabolism of Organic Carbon in Germinating Spores of Glomus intraradices. New Phytologist, 180, 684-695.
[44] Singh, G.S., Kapoor, A. and Wange, S.S. (1991) The Enhancement of Root Colonisation of Legumes by Vesicular-Arbuscular Mycorrhizal (VAM) Fungi Through the Inoculation of the Legume Seed with Commercial Yeast (Saccharomyces cerevisiae). Plant and Soil, 131, 129-133.
[45] Sampedro, I., Aranda, E., Scervino, J.M., Fracchia, S., Garcia-Romera, I., Ocampo, J.A. and Godeas, A. (2004) Improvement by Soil Yeasts of Arbuscular Mycorrhizal Symbiosis of Soybean (Glycine max) Colonized by Glomus mosseae. Mycorrhiza, 14, 229-234.
[46] Hamel, C., Dalpé, Y., Lapierre, C., Simard, R.R. and Smith, D.L. (1994) Composition of the Vesicular-Arbuscular Mycorrhizal Fungi Population in an Old Meadow as Affected by pH, Phosphorus and Soil Disturbance. Agriculture, Ecosystems & Environment, 49, 223-231.
[47] Nurlaeny, N., Marschner, H. and George, E. (1996) Effects of Liming and Mycorrhizal Colonization on Soil Phosphate Depletion and Phosphate Uptake by Maize (Zea mays L.) and Soybean (Glycine max L.) Grown in Two Tropical Acid Soils. Plant and Soil, 181, 275-285.
[48] Wang, G.M., Stribley, D.P., Tinker, P.B. and Walker, C. (1993) Effects of pH on Arbuscular Mycorrhiza. I. Field Observations on the Long-Term Liming Experiments at Rothamsted and Wobum. New Phytologist, 124, 465-472.
[49] Bermudez, M. and Azcón, R. (1996) Calcium Uptake by Alfalfa as Modified by a Mycorrhizal Fungus and Liming. Symbiosis, 20, 175-184.
[50] Miller, R.L. and Jackson, L.E. (1998) Survey of Vesicular-Arbuscular Mycorrhizae in Lettuce Production in Relation to Management and Soil Factors. The Journal of Agricultural Science, 130, 173-182.
[51] Liu, A., Hamel, C., Hamilton, R.I., Ma, B.L. and Smith, D.L. (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.
[52] Kahiluoto, H., Ketoja, E., Vestberg, M. and Saarela, I. (2001) Promotion of AM Utilization through Reduced P Fertilization 2. Field Studies. Plant and Soil, 231, 65-71.
[53] Burrows, R.L. and Pfleger, F.L. (2002) Arbuscular Mycorrhizal Fungi Respond to Increasing Plant Diversity. Canadian Journal of Botany, 80, 120-130.
[54] Treseder, K.K. and Allen, M.F. (2002) Direct Nitrogen and Phosphorus Limitation of Arbuscular Mycorrhizal Fungi: A Model and Field Test. New Phytologist, 155, 507-515.
[55] Harinikumar, K.M. and Bagyaraj, D.J. (1989) Effect of Cropping Sequence, Fertilizers and Farmyard Manure on Vesicular-Arbuscular Mycorrhizal Fungi in Different Crops over Three Consecutive Seasons. Biology & Fertility of Soils, 7, 173-175.
[56] Ryan, M.H., Chilvers, G.A. and Dumaresq, D.C. (1994) Colonisation of Wheat by VA-Mycorrhizal Fungi Was Found to Be Higher on a Farm Managed in an Organic Manner than on a Conventional Neighbor. Plant and Soil, 160, 33-40.
[57] Douds Jr., D.D., Galvez, L., Franke-Snyder, M., Reider, C. and Drinkwater, L.E. (1997) Effect of Compost Addition and Crop Rotation Point upon VAM Fungi. Agriculture, Ecosystems & Environment, 65, 257-266.
[58] Pasolon, Y.B., Hirata, H. and Barrow, N.J. (1993) Effect of White Clover (Trifolium repens L.) Intercropping on Growth and Nutrient Uptake of Upland Rice (Oryza sativa L.) in Relation to VA-Mycorrhizae and Soil Fertility. Developments in Plant and Soil Sciences, 54, 331-334.
[59] Jordan, N.R., Zhang, J. and Huerd, S. (2000) Arbuscular-Mycorrhizal Fungi, Potential Roles in Weed Management. Weed Research, 40, 397-410.
[60] Johnson, N.C. (1993) Can Fertilisation of Soil Select Less Mutualistic Mycorrhizae? Ecological Applications, 3, 749-757.
[61] Grzyb, Z.S., Piotrowski, W., Sas Paszt, L. and Bielicki, P. (2013) Influence of the Granular Formulation of Florovit on the Quality of Apple and Sour Cherry Maidens in the Organic Nursery—Preliminary Results. Journal of Research and Application in Agricultural Engineering, 58, 193-197.
[62] Sivasankari, S., Venkatesalu, V., Anatharaj, M. and Chandrasekaran, M. (2006) Effect of Seaweed Extract on the Growth and Biochemical Constitutes of Vigna sinensis. Bioresource Technology, 97, 1745-1751.
[63] Malusà, E., Sas Paszt, L., Popińska, W. and Zurawicz, E. (2007) The Effect of a Substrate Containing Arbuscular Mycorrhizal Fungi and Rhizosphere Microorganisms (Trichoderma, Bacillus, Pseudomonas and Streptomyces) and Foliar Fertilization on Growth Response and Rhizosphere pH of Three Strawberry Cultivars. International Journal of Fruit Science, 6, 25-41.
[64] Cerdán, M., Sánchez-Sánchez, A., Jordá, J.D., Juárez, M. and Sánchez-Andreu, J. (2013) Effect of Commercial Amino Acids on Iron Nutrition of Tomato Plants Grown under Lime-Induced Iron Deficiency. Journal of Plant Nutrition and Soil Science, 176, 859-866.
[65] Norman, J.R., Atkinson, D. and Hooker, J.E. (1996) Arbuscular Mycorrhizal Fungal-Induced Alteration to Root Architecture in Strawberry and Induced Resistance to the Root Pathogen Phytophthora fragariae. Plant and Soil, 185, 191-198.
[66] Malusá, E., Sas-Paszt, L., Jadczuk-Tobjasz, E., Juszczuk, I., Rychter, A., Ciesielska, J. and Popinska, W. (2010) The Effect of Organic Fertilizers and Amendments on Photosynthesis and N Metabolism in Strawberry. 28th International Horticultural Congress, Lisbon, 22-27 August 2010, 637.
[67] Douds, D.D., Janke, R.R. and Peters, S.E. (1993) VAM Fungus Spore Populations and Colonization of Roots of Maize and Soybean under Conventional and Low-Input Sustainable Agriculture. Agriculture, Ecosystems & Environment, 43, 325-335.
[68] Franke-Snyder, M., Douds Jr., D.D., Galvez, L., Phillips, J.G., Wagoner, P., Drinkwater, L. and Morton, J.B. (2001) Diversity of Communities of Arbuscular Mycorrhizal (AM) Fungi Present in Conventional versus Low-Input Agricultural Sites in Eastern Pennsylvania, USA. Applied Soil Ecology, 16, 35-48.
[69] Kurle, J.E. and Pfleger, F.L. (1994) Arbuscular Mycorrhizal Fungus Spore Populations Respond to Conversions between Low-Input and Conventional Management Practices in a Corn-Soybean Rotation. Agronomy Journal, 86, 467-475.
[70] Sjoberg, J., Persson, P., Martensson, A., Mattsson, L., Adholeya, A. and Alstrom, S. (2004) Occurrence of Glomeromycota Spores and some Arbuscular Mycorrhiza Fungal Species in Arable Fields in Sweden. Acta Agriculturae Scandinavica, Section B-Soil & Plant Science, 54, 202-212.
[71] Sumorok, B., Sas Paszt, L., Gluszek, S., Derkowska, E. and Zurawicz, E. (2011) The Effect of Mycorrhization and Mulching of Apple Trees “Gold Milenium” and Blackcurrant Bushes “Tiben” on the Occurrence of Arbuscular Mycorrhizal Fungi. Journal of Fruit and Ornamental Plant Research, 19, 35-49.
[72] Purin, S., Filho, K.O. and Stürmer, S.L. (2006) Mycorrhizae Activity and Diversity in Conventional and Organic Apple Orchards from Brazil. Soil Biology & Biochemistry, 38, 1831-1839.
[73] Ellis, J.R., Roder, W. and Mason, S.C. (1992) Grain Sorghum-Soybean Rotation and Fertilization Influence on Vesicular-Arbuscular Mycorrhizal Fungi. Soil Science Society of America Journal, 56, 783-794.
[74] Blaszkowski, J. (1993) Comparative Studies of the Occurrence of Arbuscular Fungi and Mycorrhizae (Glomales) in Cultivated and Uncultivated Soils of Poland. Acta Mycologica, 28, 93-140.

Copyright © 2023 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.