Use of the Glomus etunicatum as biocontrol agent of the soybean cyst nematode




Biological control; Heterodera glycines; Glomus etunicatum; Mycorrhizal fungi.


This study investigated the effect of arbuscular mycorrhiza (Glomus etunicatum Becker & Gerd.), on the cyst nematode (Heterodera glycines Ichinohe), in a greenhouse. Mycorrhizal and non-mycorrhizal soybean plants were exposed to the pathogen at different initial population densities (0, 500, 1000, 2000, and 4000 nematodes eggs). Soybean growth, nematode reproduction, and the arbuscular mycorrhizal fungus’s capacity to decrease disease pressure were determined after 60 day-olds. The height of the plants was increased by 26% in the presence of arbuscular mycorrhizal fungus (AMF) despite of a higher initial population of cyst nematodes. The root length was, on average, 32.20% was greater in the presence of AMF. The number of nematodes females found in the root system of mycorrhizal plants was 28.21% lower than in non-mycorrhizal roots. These results suggest that AMF G. etunicatum acts indirectly, promoting an improvement in the nutritional plant status creating tolerance to the presence of the pathogen by soybean.


Abad, P., Gouzy, J., Aury, J. M., Castagnone-Sereno, P., Danchin, E. G. J., Deleury, E. & Wincker, P. (2008). Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nature Biotechnology, 26, 909-915.

Alban, R., Guerrero, R. & Toro, M. (2013). Interactions between a root-knot nematode (Meloidogyne exigua) and arbuscular mycorrhizae in coffee plant development (Coffea arabica). American Journal of Plant Sciences, 4(7), 19-23.

Alvarado-Herrejón, M., Larsen, J., Gavito, ME., Jaramillo-López, P. F., Vestberg, M., Martínez-Trujillo, M. & Carreón-Abud, Y. (2019). Relation between arbuscular mycorrhizal fungi, root-lesion nematodes and soil characteristics in maize agroecosystems. Applied Soil Ecology, 135, 1-8.

Bartlem, D. G., Jones, M. G. K. & Hammes, U. Z. (2014). Vascularization and nutriente delivery at root-knot nematode feeding sites in host roots. Journal of Experimental Botany, 65(7), 1789-1798.

Baum, C., El-Tohamy, W. & Gruda, N. (2015). Increasing the productivity and product quality of vegetable crops using arbuscular mycorrhizal fungi: a review. Scientia Horticulturae, 187, 131–141.

Cameron, D., Neal, A., Van Wees, .S & Ton, J. (2013). Mycorrhiza-induced resistence: more than the sum of its parts? Trends in Plant Science, 18, 539-545.

Ceustermans, A., Hemelrijck, V. W., Campenhout, J.V. & Bylemans, D. (2018). Effect of Arbuscular Mycorrhizal Fungi on Pratylenchus penetrans Infestation in Apple Seedlings under Greenhouse Conditions. Pathogens, 7(76), 1-10.

Chen, S., Zhao, H., Zoul, C., Li, Y., Chen, Y., Wang, Z., Jiang, Y., Liu, A., Zhao, P., Wang, Z. & Ahammed, G. J. (2017). Combined Inoculation with Multiple Arbuscular Mycorrhizal Fungi Improves Growth, Nutrient Uptake and Photosynthesis in Cucumber Seedlings. Frontiers Microbiology, 8.

Cofcewicz, E. T., Medeiros, C. A. B., Carneiro, R. M. D. G. & Pierobon, C. R. (2001). Interaction of arbusuclar mycorrhizal fungi Glomus etunicatum and Gigaspora margarita and root-knot nematode Meloidogyne incognita in tomato. Fitopatologia Brasileira, 26(1), 65–70.

Cotton, J. A., Lilley, C. J., Jones, L. M.,Kikuchi, T., Reid, A. J., Thorpe, P., Tsai, I. J., Beasley, H. Blok, V., Cock, P. J. A., Akker, S. E den, Holroyd, N., Hunt, M., Mantelin, S., Naghra, H., Pain, A., Palomares-Rius, J. E., Zarowiecki, M., Berriman, M.,Jones, J. T. & Urwin, P. E. (2014). The genome and life-stage specific transcriptomes of Globodera pallida elucidate Key aspects of plant parasitism by a cyst nematode. Genome Biology, 15, 1-17.

Curtis, R. H. C., Robinson, A. F. & Perry, R. N. (2009). Hatch and host location. In: Perry, R. N., Moens, M. & Starr, J. L. (eds) Root-knot nematodes. CAB International, Wallingford, 139–162.

De Coninck, B., Timmermans, P., Vos, C., Cammue, B. P. A. & Kazan, K. (2015). What lies beneath: belowground defense strategies in plants. Trends in Plant Science, 20, 91–101.

Dehne, H. W. (1982). Interaction between vesicular-arbuscular mycorrhizal fungi and plant pathogens. Phytopathology, 72, 1115-1119.

Ferraz, L. & Brown, D. (2002). An Introduction to Nematodes. Plant Nematology.

Gamalero, E., Pivato, B., Bona, E., Copetta, A., Avidano, L., Lingua, G. & Berta, G. (2010). Interactions between a fluorescent pseudomonad, an arbuscular mycorrhizal fungus and a hypovirulent isolate of Rhizoctonia solani affect plant growth and root architecture of tomato plants. Plant Biosystems, 144(3), 582-591.

Gheysen, G. & Mitchum, M. G. (2011). How nematodes manipulate plant development pathways for infection. Current Opinion in Plant Biology, 14(4), 415-421.

Gianinazzi, S., Gollote, A., Binet, M. Tuinen, Van, D., Redecker, D. & Wipf, D. (2010). Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza, 20(8), 519–530.

Grabau, Z. J. & Chen, S. (2020). Determining the role of plant-parasitic nematodes in the corn-soybean crop rotation yield effect using nematicide application: I. Corn. Agronomy Journal. 108, 782-793.

Guo, W., Chen, J. S., Zhang, F., Ze, Y. L. I., Chen, H. F., Zhang, C., Chen, L. I. M., Song, L. Y., Rong, L., Dong, C., Qing, N. H., Shui, L. C., Zhi, H. S., Zhong, L. Y., Xiao, J. Z., De Z. Q., Qing, B. Y., Wen, J. D., Xin, A. Z., Xin, J. S. & Yong, Q. J. (2020). Caracterization of Pingliang xiaoheidou (ZDD 11047), a soybean variety with resistance to soybean cyst nematode Heterodera glycines. Plant Molecular Biology.

Gutjahra, C. & Paszkowski, U. (2013). Multiple control levels of root system remodeling in arbuscular mycorrhizal symbiosis. Frontiers Plant Science, 4(204), 1-8.

Haarith, D., Bushley, K. E. & Chen, S. (2020). Fungal communities associated with Heterodera glycines and their potential in biological control: a current update. The Journal of Nematology, 52, 1-17.

Hammer, E. C., Pallon, J., Wallander, H. & Olsson, P. A. (2011). Tit for tat? A mycorrhizal fungus accumulates phosphorus under low plant carbon availability. FEMS Microbiology Ecology, 76(2), 236–244.

Harrier, L. A. & 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 Management Science 60(2), 149–57.

Hol, W. H. G. & Cook, R. (2005). Na overview of arbuscular mycorrhizal fungi-nematode interactions. Basic and Applied Ecology, 6(6), 489-503.

Jones, J. T., Haegeman, A., Danchin, E. G. J., Gaur, H. S., Helder, J., Jones, M. G. K., Kikuchi, T., Manzanilla-López, R., Palomares-Rius, J. E., Wesemael, W. M. L. e Perry, R. N. (2013). Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular Plant Pathology, 14, 946-961.

Junh, S. C., Martinez-Medina, A., Lopez-Raez, J. A. & Pozo, M. J. (2012). Mycorrhiza-induced resistance and priming of plant defenses. Journal of Chemical Ecology, 38, 651–664.

Kellam, M. K. & Schenck, N. C. (1980). Interaction between a vesicular-arbuscular mycorrhizal fungus and root-knot nematode on soybean. Phytopathology, 70, 293-296.

Khalil, S., Loynachan, T. E. & McNabb, H. S. J. (1992). Colonization of soybean by mycorrhizal fungi and spore populations in Iowa soils. Agronomy Journal, 84, 832-836.

Khalil, S. Loynachan, T. E. & Tabatabai, M. A. (1999). Plant determinants of mycorrhizal dependency in soybean. Agronomy Journal, 91, 135-141.

Koenning, S. R. & Wrather, J. A. (2018). Suppression of soybean yield potential in the continental United States from plant diseases estimated from 2006 to 2009. Plant Health Progress.

Ma, Y. Y., Li, Y. L., Isi, H. X., Guo, Q. & Xue, Q. H. (2017). Effects of two strains of Streptomyces on root-zone microbes and nematodes for biocontrol of root-knot nematode disease in tomato. Applied Soil Ecology. 112, 34–41.

Nicol, J. M., Turner, S. J., Coyne, D. L., Nijs, L. D., Hockland, S. & Maafi, Z. T. (2011). Current nematode threats to world agriculture. In: Jones, J., Gheysen G., Fenoll C. (Eds). Genomics and Molecular Genetics of Plant-Nematode Interactions. Springer, 21-43.

Nimnoia, P. & Ruanpanun, P. (2020). Suppression of root-knot nematode and plant growth promotion of chili (Capsicum flutescens L.) using co-inoculation of Streptomyces spp. Biological Control, 145, 104-244.

Parniske, M. (2008). Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nature Reviews Microbiology, 6, 763–775.

Perry, R. N & Moens, M. (2011). Introduction to plant -parasitic nematodes, modes of parasitismo. In: Jones, J., Gheysen G., Fenoll C. (Eds). Genomics and Molecular Genetics of Plant-Nematode Interactions. Springer,320.

Pozo, M. & Azcón-Aguilar, C. (2007). Unraveling mycorrhiza-induced resistence. Current Opinion in Plant Biology, 10(4), 393-398.

Rasmussen, P.U., Chareesri, A., Neilson, R., Bennett, A. E. & Tack, A. J. M. (2019). The impact of dispersal, plant genotype and nematodes on arbuscular mycorrhizal fungal colonization. Soil Biology and Biochemistry, 132, 28-35.

Ross, J. P. (1971). Effect of phosphate fertilization on yeld of mycorrhizal and nonmycorrhizal soybeans. Phytopathology, 61, 1400-1403.

Ruanpanun, P. & Chamswarng, C. (2016). Potential of actinomycetes isolated from earthworm castings in controlling root-knot nematode Meloidogyne incognita. Journal of General Plant Pathology, 82, 43–50.

Ruscitti, M., Arango, M. & Beltrano, J. (2017). Improvement of copper stress tolerance in pepper plants (Capsicum annuum L.) by inoculation with arbuscular mycorrhizal fungi. Theoretical and Experimental Plant Physiology, 29, 37–49.

Safir, G. R., Boyer, J. S. & Gerdemann, J. W. (1972). Nutrient status and mycorrhizal enhancement of water transport in soybean. Plant Physiology, 49, 700-703.

Schmutz, J., Cannon, S. B., Schlueter, J., Ma, J., Mitros, T., Nelson, W., Hyten, D. L., Song, Q., Thelen, J. J., Cheng, J., Xu, D., Hellsten, U., May, G. D., Yu, Y., Sakurai, T., Umezawa, T., Bhattacharyya, M. K., Sandhu, D., Valliyodan, B., Lindquist, E., Peto, M., Grant, D., Shu, S., Goodstein, D., Barry, K., Futrell-Griggs, M., Abernathy, B., Du, J.,Tian, Z., Zhu, L., Gill, N., Joshi, T., Libault, M., Sethuraman, A., Zhang, X., Shinozaki, K., Nguyen17, H. T., Wing, R. A., Cregan, P., Specht, J., Grimwood, J., Rokhsar, D.,Stacey, G., Shoemaker, R. C. & Scott, A. J. (2010). Genome sequence of the palaeopolyploid soybean. Nature, 463, 178–183.

Schouteden, N., Waele, D. D., Panis, B. & Vos, C. M. (2015). Arbuscular mycorrhhizal fungi for the biocontrol of plant-parasitic nematodes: A review of the mechanism involved. Frontiers in Microbiology, 6, 1-12.

Silveira, D. T. & Códova, F. P. (2009). A pesquisa científica. In: Gerhardt, T. A. & Silveira, D. T. (org). Métodos de pesquisa. SEAD/UFRGS.

Singh, L. P., Gill, S. S. & Tuteja, N. (2011). Unraveling the role of fungal symbionts in plan abiotic stress tolerance. Plant Signaling & Behavior, v. 6, 175-191.

Sohrabi, F., Sheikholeslami, M., Heydari, R., Rezaee, S. & Sharif, R. (2020). Investigating the efect of Glomus mosseae, Bacillus subtilis and Trichoderma harzianum on plant growth and controlling Meloidogyne javanica in tomato. Indian Phytopathology, 73 , Páginas293–300

Strom, N., Hu, W., Haarith, D., Chen, S. & Bushley, K. (2020). Interactions between soil properties, fungal communities, the soybean cyst nematode, and crop yield under continuous corn and soybean monoculture. Applied Soil Ecology, 147, 1-14.

Tihohod, D, & Santos, J. N. (1993). Heterodera glycines: Novo nematóide da soja no Brasil. Detecção e medidas preventivas. FUNEP, 23.

Todd, T. C., Winkler, H. E. & Wilson, G. W. T. (2001). Interaction of Heterodera glycines and Glomus mosseae on Soybean. Journal of Nematology, 33, 306-310.

Toumi, F., Waeyenberge, L., Viaene, N., Dababat, A., Nicol, J., Ogbonnava, F. & Moens, M. (2018). Cereal cyst nematodes: importance, distribution, identification, quantification, and control. European Journal of Plant Pathology. 150, 1–20.

Tylka, G. L., Hussey, R. S. & Roncadori, R. W. (1991). Interactions of vesicular-arbuscular mycorrhyzal fungi, phophoros, and Heterodera glycines on soybean. Journal of Nematology, 23(1), 122-133.

Vos, C. M., Yang, Y., Coninck, B. D. & Cammue, B. P. A. (2014). Fungal (-like) biocontrol organisms in tomato disease control. Biological Control, 74, 65–81.

Vos, C. M., Tesfahun, A. N., Panis, B., Waele, D. D. & Elsen, A. (2012). Arbuscular mycorrhizal fungi induce systemic resistence in tomato against the sedentary nematode Meloidogyne incógnita and the migratory nematode Pratylenchus penetrans. Applied Soil Ecology, 61, 1-6.

Wesemael, W. M. L., Viene, N. & Moens, M. (2011). Root-knot nematodes (Meloidogyne spp.) in Europe. Nematology, 13(1), 3-16.

Whipps, J. M. (2004). Prospects and limitations for mycorrhizas in biocontrol of root pathogens. Canadian Journal Botany, 82(8), 1198–1227.

Winkler, H. E., Hetrick, B. A. & Todd, T. C. (1994). Interactions of Heterodera glycines, Macrophomina phaseolina, and mycorrhizal fungi on soybean in Kansas. Journal of Nematology, 26, 675-682.

Wu, H. Y., He, Q., Liu, J. J. Luo, J. & Peng, D. L. (2014). Occurrence and development of the cereal cyst nematode (Heterodera avenae) in Shandong, China. Plant Disease Journal, 98, 1654-1660.




How to Cite

BENEDETTI , T. .; ANTONIOLLI, Z. I.; SORDI, E. .; CARVALHO, I. R. .; BORTOLUZZI, E. C. Use of the Glomus etunicatum as biocontrol agent of the soybean cyst nematode . Research, Society and Development, [S. l.], v. 10, n. 6, p. e7310615132, 2021. DOI: 10.33448/rsd-v10i6.15132. Disponível em: Acesso em: 20 jun. 2021.



Agrarian and Biological Sciences