Mycorrhizal inoculation as an alternative for the ecological production of tomato (Lycopersicon esculentum Mill.)
More details
Hide details
Department of Plant Protection, University of Life Sciences in Lublin, Leszczyńskiego 7, 20-069 Lublin, Poland
Department of Plant Protection, College of Agriculture and Forestry, University of Mosul, 41002 Mosul, Iraq
Barbara Skwarylo   

Department of Plant Protection, University of Life Sciences in Lublin, Leszczyńskiego 7, 20-069, Lublin, Poland
Publication date: 2020-04-03
Final revision date: 2019-12-19
Acceptance date: 2020-02-14
Int. Agrophys. 2020, 34(2): 253–264
The aim of study was to investigate the effect of two mycorrhizal fungus species Claroideoglomus etunicatum and Rhizophagus intraradices on the uptake of macronutrients and on the growth and yield of tomato hybrid plants cultivated in an ecological system. The experiment was carried out at an ecological farm in Grądy in the Lublin province of Poland, for three years (2015-2017). The experimental treatments included plants inoculated with Claroideoglomus etunicatum, Rhizophagus intraradices and plants without mycorrhizal inoculation used as a control. The mycorrhization of tomato roots with Claroideoglomus etunicatum and Rhizophagus intraradices resulted in an improved uptake of Ca and K through the plants. The length of the tomato roots, especially for the cultivars treated with Claroideoglomus etunicatum, were statistically longer than those of the control. Tomato roots inoculation with both of the studied mycorrhizal fungus strains significantly influenced the number of tomato leaves and improved the health status of the plant. The yield of tomato was not significantly affected by mycorrhization but Claroideoglomus etunicatum, to a greater extent than Rhizophagus intraradices reduced the yield of diseased fruit compared to the control. Among the studied mycorrhizal fungus species, better results were obtained with the application of Claroideoglomus etunicatum as compared with Rhizophagus intraradices for all examined features. Mycorrhizal inoculation contributed to the better growth of the plants, it improved their health and may be beneficially applied in the ecological production of tomatoes.
Abdel-Fattah G.M. and Asrar A.W.A., 2012. Arbuscular mycorrhizal fungal application to improve growth and tolerance of wheat (Triticum aestivum L.) plants grown in saline soil. Acta Physiol. Plant, 34 (1), 267-277.
Afzal I., Hussain B., Basra S.M.A., Ullah S.H., Shakeel Q., and Kamran M., 2015. Foliar application of potassium improves fruit quality and yield of tomato plants. Acta Sci. Pol-Hortoru., 14 (1), 3-13.
Akköprü A. and Demir S., 2005. Biological control of Fusarium wilt in tomato caused by Fusarium oxysporum f. sp. lycopersici by AMF Glomus intraradices and some rhizobacteria. J. Phytopathol., 153(9), 544-550.
Al-Askar A.A. and Rashad Y.M., 2010. Arbuscular Mycorrhizal Fungi: A biocontrol agent against Common Bean Fusarium Root Rot Disease. Plant Pathology J., 9, 31-38.
Berta G., Sampo S., Gamalero E., Massa N., and Lemanceau P., 2005. Suppression of Rhizoctonia root-rot of tomato by Glomus mossae BEG12 and Pseudomonas fluorescens A6RI is associated with their effect on the pathogen growth and on the root morphogenesis. Eur. J. Plant Pathol., 111 (3), 279-288.
Bi H.H., Song Y., and Zeng R.S., 2007. Biochemical and molecular responses of host plants to mycorrhizal infection and their roles in plant defence. Allelopathy J., 20(1), 15.
Błaszkowski J., 2012. Glomeromycota. In: Szafer Institute of Botany Polish Academy of Sciences, Kraków, 1-303.
Bosco M., Giovannetti G., Picard C., Baruffa E., Brondolo A., and Sabbioni F., 2007. Commercial plant-probiotic microorganisms for sustainable organic tomato production systems. In: Improving sustainability in organic and low-input food production systems (Eds U. Niggli, C. Leifert, T. Alföldi, L. Lück, H. Willer) . Proc. 3rd QLIF Congress, Stuttgart, FiBL, Frick, 268-271.
Candido V., Campanelli G., D’Addabbo T., Castronuovo D., Perniola M., and Camele I., 2015. Growth and yield promoting effect of artificial mycorrhization on field tomato at different irrigation regimes. Sci. Hortic., 187, 35-43.
Castillo C., Morales A., Rubio R., and Bare J.M., 2013. Interactions between native arbuscular mycorrhizal fungi and phosphate solubilizing fungi and their effect to improve plant development and fruit production by Capsicum annuum L. Afr. J. Microbiol. Res., 7 (26), 3331-3340.
Cimen I., Pirinc V.E.D.A.., Doran I., and Turgay B., 2010. Effect of soil solarization and arbuscular mycorrhizal fungus (Glomus intraradices) on yield and blossom-end rot of tomato. Int. J. Agric. Biol., 12, 551-555.
Colella T., Candido V., Campanelli G., Camele I., and Battaglia D., 2014. Effect of irrigation regimes and artificial mycorrhization on insect pest infestations and yield in tomato crop. Phytoparasitica, 42(2), 235-246.
Conversa G., Elia A., and La Rotonda P., 2007. Mycorrhizal inoculation and phosphorus fertilization effect on growth and yield of processing tomato. Acta Hortic., 758, 333-338.
Conversa G., Lazzizera C., Bonasia A., and Elia A., 2013. Yield and phosphorus uptake of a processing tomato crop grown at different phosphorus levels in a calcareous soil as affected by mycorrhizal inoculation under field conditions. Biol. Fert. Soils, 49(6), 691-703.
Donkó Á., Zanathy G., Èros-Honti Z., Villangó S., and Bisztray G.D., 2014. Changes of mycorrhizal colonization along moist gradient in a vineyard of Eger (Hungary). Acta Universitatis Sapientiae Agric. Environ., 6 (1), 13-23.
Ezzo M.I., Glala A.A., Habib H.A.M., and Helaly A.A., 2010. Response of sweet pepper grown in sandy and clay soil lysimeters to water regimes. American-Eurasian J. Agric. Environ. Sci., 8(1), 18-26.
FAOSTAT, 2014. Production crops: Tomatoes. FAOSTAT Agricultural production database.
Feng G., Zhang F. S., Li X.L., Tian C.Y., Tang C., and 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, 185-190.
Fritz M., Jakobsen I., Lyngkjaer M.F., Thordal-Christensen H., and Pons-Kühnemann J., 2006. Arbuscular mycorrhiza reduces susceptibility of tomato to Alternaria solani. Mycorrhiza, 16, 413-419.
Garmendia I., Goicechea N., and Aguirreolea J., 2004. Plant phenology influences the effect of mycorrhizal fungi on the development of verticillium-induced wilt in pepper. Eur. J. Plant Pathol., 110, 227-238.
George E., Häussler K., Vetterlein D., Gorgus E., and Marschner H., 1992. Water and nutrient translocation by hyphae of Glomus mosseae. Can. J. Botany, 70, 2130-2137.
Guru V., Tholkappian P., and Viswanathan K., 2011. Influence of arbuscular mycorrhizal fungi and Azospirillum co-inoculation on the growth characteristics. Nutritional content, and yield of tomato crops grown in south India. Indian. J. Fund. Appl. Life Sci., 1(4), 84-92.
Hao Z., Christie P., Qin L., Wang C., and Li X., 2005. Control of Fusarium wilt of cucumber seedlings by inoculation with an arbuscular mycorrhizal fungus. J. Plant Nutr., 28(11), 1961-1974.
Harrier L.A. and Watson C.A., 2004. The potential role of arbuscular mycorrhizal (AM) fungi in the bioprotection of plants against soil-borne pathogens in organic and/or other sustainable farming systems. Pest. Manag. Sci., 60(2), 149-157.
Hart M., Ehret D.L., Krumbein A., Leung C., Murchm S., Turim C., and Franken P., 2015. Inoculation with arbuscular mycorrhizal fungi improves the nutritional value of tomatoes. Mycorrhiza, 25, 359-376.
Jamiołkowska A., Księżniak A., Gałązka A., Hetman B., Kopacki M., and Skwaryło-Bednarz B., 2018. Impact of abiotic factors on development of the community of arbuscular mycorrhizal fungi in the soil. Int. Agrophys., 32, 133-140.
Jamiołkowska A., Księżniak A., Hetman B., Kopacki M., Skwaryło-Bednarz B., Gałązka A., and Thanoon A.H., 2017. Interactions of arbuscular mycorrhizal fungi with plants and soil microflora. Acta Sci. Pol-Hortoru., 16(5), 89-95.
Joseph P.J. and Sivaprasad P., 2012. The potential of arbuscular mycorrhizal associations for biocontrol of soilborne diseases. In: Biocontrol potential and its exploitation in sustainable agriculture: crop diseases, weeds and nematodes (Eds R.K. Upadhyay, K.G. Mukerij, B. Chamola). Springer Science Business Media, New York, 139-153.
Jung S.C., Martinez-Medina A., Lopez-Raez J.A., and Pozo M.J., 2012. Mycorrhiza-induced resistance and priming of plant defenses. J. Chem. Ecol., 38 (6), 651-664.
Kabała C., Charzyński P., Chodorowski J., Drewnik M., Glina B., Greinert A., Hulisz P., Jankowski M., Jonczak J., Łabaz B., Łachacz A., Marzec M., Mendyk Ł., Musiał P., Musielok Ł., Smreczak B., Sowiński P., Świtoniak M., Uzarowicz Ł., and Waroszewski J., 2019. Polish Soil Classification, 6th edition – principles, classification scheme and correlations. Soil Sci. Annual, 70(2), 71-97.
Kapoor R., 2008. Induced resistance in mycorrhizal tomato is correlated to concentration of jasmonic acid. OnLine J. Biol. Sci., 8(3), 49-56.
Kasiamdari R.S., Smith S.E., Smith F.A., and Scott E.S., 2002. Influence of the mycorrhizal fungus, Glomus coronatum, and soil phosphorus on infection and disease caused by binucleate Rhizoctonia and Rhizoctonia solani on mung bean (Vigna radiata). Plant Soil, 238(2), 235-244.
Kobra N., Jalil K., and Youbert G., 2009. Effects of three Glomus species as biocontrol agents against Verticillium-induced wilt in cotton. J. Plant Prot. Res., 49(2), 185-189.
Kothari S.K., Marschner H., and George E., 1990. Effect of VA mycorrhizal fungi and rhizosphere microorganisms on root and shoot morphology, growth and water relations in maize. New Phytologist., 116, 303-311.
Liu J., Maldonado-Mendoza I., Lopez-Meyer M., Cheung F., Town C.D., and Harrison M.J., 2007. Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. Plant J., 50(3), 529-544.
Lopez-Ráez J.A., Verhage A., Fernandez I., Garcia J.M., Azcon-Aguilar C., Flors V., and Pozo M.J., 2010. Hormonal and transcriptional profiles highlight common and differential host responses to arbuscular mycorrhizal fungi and the regulation of the oxylipin pathway. J. Exp. Bot., 61, 2589-2601.
Maboko M.M., Bertling I., and Du Plooy C.P., 2013. Arbuscular mycorrhiza has limited effects on yield and quality of tomatoes grown under soilless cultivation. Acta Agr. Scand. B-S. P., 63(3), 261-270.
Manila S. and Nelson R., 2014. Biochemical changes induced in tomato as a result of arbuscular mycorrhizal fungal colonization and tomato wilt pathogen infection. Asian J. Plant Sci. Res., 4(1), 62-68.
Michałojć Z., Jarosz Z., Pitura K., and Dzida K., 2015. Effect of mycorrhizal colonization and nutrient solutions concentration on the yielding and chemical composition of tomato grown in rockwool and straw medium. Acta Sci. Pol-Hortoru., 14, 15-27.
Nicola S., Tibaldi G., and Fontana E., 2009. Tomato production systems and their application to the tropics. Acta Hortic., 821, 27-34.
Nzanza B., Marais D., and Soundy P., 2012. Effect of arbuscular mycorrhizal fungal inoculation and biochar amendment on growth and yield of tomato. Int. J. Agric. Biol., 14, 965-969.
Oehl F., Sieverding E., Palenzuela J., Ineichen K., and da Silva G.A., 2011. Advances in Glomeromycota taxonomy and classification. IMA Fungus, 2, 191-199.
Ordookhani K., Khavazi K., Moezzi A., and Rejali, F., 2010. Influence of PGPR and AMF on antioxidant activity, lycopene and potassium content in tomato. Afr. J. Agric. Res., 5(10), 1108-1116.
Oseni T.O., Shongwe N.S., and Masarirambi M.T., 2010. Effect of arbuscular mycorrhiza (AM) inoculation on the performance of tomato nursery seedlings in vermiculite. Int. J. Agric. Biol., 12, 789-792.
Palenzuela J., Ferrol N., Boller T., Azcón-Aguilar C., and Oehl F., 2008. Otospora bareai, a new fungal species in the Glomeromycetes from a dolomitic shrubland in the Natural Park of Sierra de Baza (Granada, Spain). Mycologia, 100 (2), 296-305.
Panthee D.R. and Chen F., 2010. Genomics of fungal disease resistance in tomato. Curr. Genomics, 11(1), 30-39.
Paszkowski U., 2006. Mutualism and parasitism: The yin and yang of plant symbioses. Curr. Opin. Plant Biol., 9(4), 364-370.
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. T. Brit. Mycol. Soc., 55 (1), 158-161.
Pozo M.J. and Azcón-Aguilar C., 2007. Unraveling mycorrhiza-induced resistance. Curr. Opin. Plant Biol., 10(4), 393-398.
Pozo M.J., Cordier C., Dumas-Gaudot E., Gianinazzi S., Barea J.M., and Azcón-Aguilar C., 2002. Localized versus systemic effect of arbuscular mycorrhizal fungi on defence responses to Phytophthora infection in tomato plants. J. Exp. Bot., 53, 525-534.
Pozo M.J., Van Loon L.C., and Pieterse C.M.J., 2005. Jasmonates-signals in plant-microbe interactions. J. Plant Growth Regul., 23(3), 211-222.
Ruiz-Lozano J.M., Azcon R, and Gomez M., 1996. Alleviation of salt stress by arbuscular-mycorrhizal Glomus species in Lactuca sativa plants. Physiol. Plantarum, 98(4), 767-772.
Sadasivam S. and Manickam A., 2005. Biochemical methods. 2nd edn New Age International, New Delhi.
Smith S.E. and Smith F.A., 2011. Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystems scales. Annu. Rev. Plant Biol., 62, 227-250.
Song Y., Chen D., Lu K., Sun Z., and Zeng R., 2015. Enhanced tomato disease resistance primed by arbuscular mycorrhizal fungus. Front Plant Sci., 6, 786.
Song Y.Y., Zeng R.S., Xu J.F., Li J., Shen X., and Yihdego W.G. 2010. Interplant communication of tomato plants through underground common mycorrhizal networks. PLoS ONE 5(10):e13324.
Subramanian K.S., Santhanakrishnan P., and 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.
Tahat M.M., and Kamaruzaman Sijam Othman R., 2010. Mycorrhizal fungi as a biocontrol. Agent Plant Pathol. J., 9, 198-207.
Tanwar A., Aggarwal A., Kadian N., and Gupta A., 2013. Arbuscular mycorrhizal inoculation and super phosphate application influence plant growth and yield of Capsicum annuum. J. Soil Sci. Plant Nut., 13(1), 55-66.‏
Treseder K.K., 2013. The extent of mycorrhizal colonization of roots and its influence on plant growth and phosphorus content. Plant Soil, 371, 1-13.
Walker C., Vestberg M., and Schüßler A., 2007. Nomenclatural clarifications in Glomeromycota. Mycol. Res., 111, 253-255.
Walling S.Z. and Zabinski C.A., 2006. Defoliation effects on arbuscular mycorrhizae and plant growth of two native bunchgrasses and an invasive forb. Appl. Soil Ecol., 32(1), 111-117.
Wang C., Li X., Zhou J., Wang G., and Dong Y., 2008. Effects of arbuscular mycorrhizal fungi on growth and yield of cucumber plants. Commun. Soil Sci. Plan., 39(3-4), 499-509.
Welbaum G.E., 2015. Vegetable Production and Practices. CAB International. Wallingforth. Oxfordshire, UK, 1-486.
Wenzel H., 1948. Zur erfassung des schadenausmasses in pflanzenschutzversuchen. Pflanzenschutz-Ber., 15, 81-84.
Wu Q.S., Zou Y.N., Liu W., Ye X.F., Zai H.F., and Zhao L.J., 2010. Alleviation of salt stress in citrus seedlings inoculated with mycorrhiza: changes in leaf antioxidant defense systems. Plant Soil Environ., 56(10), 470-475.
Zeng R.S., 2006. Disease resistance in plants through mycorrhizal fungi induced allelochemicals. In: Allelochemical. Biological Control of Plant Pathogens and Diseases (Eds Inderjit, Mukerji K.) Disease Management of Fruits and Vegetables, Springer, Dordrecht, 2, 181-192.