Interacciones ecológicas de los hongos nematófagos y su potencial uso en cultivos tropicales

Adela  Quevedo; Freddy  Magdama; Jessenia  Castro; Marcos Vera-Morales

doi:10.17268/sci.agropecu.2022.009

Autores/as

Adela Quevedo Estudiante del Instituto de Posgrado. Maestría en Académica con Trayectoria de Investigación en Sanidad Vegetal. Universidad Técnica de Manabí, Código Postal 130105, Portoviejo, Manabí, Ecuador. https://orcid.org/0000-0001-5729-8643
Freddy Magdama Escuela Superior Politécnica del Litoral, Centro de Investigaciones Biotecnológicas del Ecuador. Campus Gustavo Galindo km 30.5 vía Perimetral, P.O. Box 09-01-5863, Guayaquil.
Jessenia Castro Universidad Técnica de Manabí, UTM, Código Postal 130105, Facultad de Ingeniería Agronómica, Km. 13.5 de la vía a Santa Ana. Portoviejo, Manabí, Ecuador
Marcos Vera-Morales Escuela Superior Politécnica del Litoral, ESPOL, Centro de Investigaciones Biotecnológicas del Ecuador, CIBE, Campus Gustavo Galindo Km. 30.5 vía Perimetral, P.O. Box 09-01-5863, Guayaquil, Ecuador https://orcid.org/0000-0003-2342-6269

DOI:

https://doi.org/10.17268/sci.agropecu.2022.009

Palabras clave:

control biológico, cultivos tropicales, ecología, hongos nematófagos, nematodos

Resumen

Los hongos nematófagos son capaces de alimentarse de nematodos en condiciones de escasez de nutrientes. Viven en el suelo y su estudio es importante dado el posible uso en el biocontrol de nematodos fitoparásitos. Estos hongos pueden ser cultivados en laboratorio usando diferentes medios y sustratos, convirtiéndose en potenciales agentes para uso de la agricultura en entornos tropicales. El objetivo fue revisar los avances científicos recientes en las interacciones ecológicas de los hongos nematófagos y sus presas, con énfasis en la utilización como controlador biológico. Dada la importancia de sus interacciones en el suelo, diversidad, abundancia, dispersión y colonización de diferentes tipos de hábitats, estos microorganismos fúngicos pueden ser especialistas o generalistas en la depredación de poblaciones de nematodos en sus diversos estadios (huevo, juvenil o adultos). También se describe brevemente los diferentes avances científicos y aplicaciones que han tenido los hongos depredadores en algunos cultivos tropicales de países de Latinoamérica. Después de estas exploraciones, es posible concluir que la aplicación integrada de microorganismos en el suelo podría mejorar la producción de algunos cultivares reduciendo eficientemente las poblaciones de nematodos. Además, podría mejorar la estructura de las interacciones tróficas del suelo, con tratamientos ambientalmente benignos que disminuyan la utilización de pesticidas químicos.

Citas

Abd-Elgawad, M. M. M., & Askary, T. H. (2018). Fungal and bacterial nematicides in integrated nematode management strategies. Egyptian Journal of Biological Pest Control, 28(1), 1–24.

Abd-Elgawad, M. M. M., & Askary, T. H. (2020). Factors affecting success of biological agents used in controlling the plant-parasitic nematodes. Egyptian Journal of Biological Pest Control, 30(1), 1–11.

Aboul-Eid, H. Z., Noweer, E. M. A., & Mona, E. M. A.-S. (2016). Efficacy of some biocontrol compounds on root-knot nematode, Meloidogyne incognita infesting potato under field conditions. Egyptian Journal of Biological Pest Control, 26(2), 217–222.

Ahmad, G., Khan, A., Khan, A. A., Ali, A., & Mohhamad, H. I. (2021). Biological control: a novel strategy for the control of the plant parasitic nematodes. Antonie van Leeuwenhoek 2021 114:7, 114(7), 885–912.

Åhman, J., Johansson, T., Olsson, M., Punt, P. J., van den Hondel, C. A. M. J. J., & Tunlid, A. (2002). Improving the pathogenicity of a nematode-trapping fungus by genetic engineering of a subtilisin with nematotoxic activity. Applied and Environmental Microbiology, 68(7), 3408–3415.

Akhtar, M., & Malik, A. (2000). Roles of organic soil amendments and soil organisms in the biological control of plant-parasitic nematodes: a review. Bioresource Technology, 74(1), 35–47.

Aminuzzaman, F. M., Xie, H. Y., Duan, W. J., Sun, B. D., & Liu, X. Z. (2013). Isolation of nematophagous fungi from eggs and females of Meloidogyne spp . and evaluation of their biological control potential. Biocontrol Science and Technology, 23(2), 170–182.

Andersson, K.-M., Kumar, D., Bentzer, J., Friman, E., Ahren, D., & Tunlid, A. (2014). Interspecific and host-related gene expression patterns in nematode-trapping fungi. Bmc Genomics, 15(968), 1–15.

Aranda-Martinez, A., Lenfant, N., Escudero, N., Zavala-Gonzalez, E. A., Henrissat, B., & Lopez-Llorca, L. V. (2016). CAZyme content of Pochonia chlamydosporia reflects that chitin and chitosan modification are involved in nematode parasitism. Environmental Microbiology, 18(11), 4200–4215.

Askary, T. H. (2015). Nematophagous fungi as biocontrol agents of phytonematodes. In T. Hassan & P. Pala (Eds.), Biocontrol agents of phytonematodes (pp. 81–125). CABI.

Baheti, B. L., Dodwadiya, M., & Bhati, S. S. (2017). Eco-friendly management of maize cyst nematode, Heterodera zeae on sweet corn ( Zea mays L. saccharata). Journal of Entomology and Zoology Studies, 5(6), 989–993.

Bajaj, H., & Walia, K. (2005). Studies on a Pasteuria isolate from an entomopathogenic nematode, Steinernema pakistanense (Nematoda: Steinernematidae). Nematology., 7(4), 637–640.

Balbino, H. M., Monteiro, T. S. A., Coutinho, R. R., Pacheco, P. V. M., & Freitas, L. G. de. (2021). Association of Duddingtonia flagrans with microorganisms for management of Meloidogyne javanica and acquisition of nutrients in soybean. Biological Control, 159, 104626.

Barman, A., Gohain, D., Bora, U., & Tamuli, R. (2018). Phospholipases play multiple cellular roles including growth, stress tolerance, sexual development, and virulence in fungi. Microbiological Research, 209, 55–69.

Bordallo, J. J., Lopez-Llorca, L. V, Jansson, H.-B., Salinas, J., Persmark, L., & Asensio, L. (2002). Colonization of plant roots by egg-parasitic and nematode-trapping fungi. New Phytologist, 154(2), 491–499.

Cabanillas, E., & Barker, K. R. (1989). Impact of Paecilomyces lilacinus inoculum level and application time on control of Meloidogyne incognita on tomato. Journal of Nematology, 21(1), 115.

Carneiro, R. M. D. G., Hidalgo-Díaz, L., Martins, I., Ayres de Souza, S. K. F., Guimarães de Sousa, M., & Tigano, M. S. (2011). Effect of nematophagous fungi on reproduction of Meloidogyne enterolobii on guava (Psidium guajava) plants. Nematology, 13(6), 721–728.

Chen, S. A., Lin, H. C., Schroeder, F. C., & Hsueh, Y. P. (2021). Prey sensing and response in a nematode-trapping fungus is governed by the MAPK pheromone response pathway. Genetics, 217(2). https://doi.org/10.1093/GENETICS/IYAA008

Chen, T.-H., Hsu, C.-S., Tsai, P.-J., Ho, Y.-F., & Lin, N.-S. (2001). Heterotrimeric G-protein and signal transduction in the nematode-trapping fungus Arthrobotrys dactyloides. Planta, 212(5), 858–863.

Chen, Y.-L., Gao, Y., Zhang, K.-Q., & Zou, C.-G. (2013). Autophagy is required for trap formation in the nematode-trapping fungus Arthrobotrys oligospora. Environmental Microbiology Reports, 5(4), 511–517.

Choe, A., von Reuss, S. H., Kogan, D., Gasser, R. B., Platzer, E. G., Schroeder, F. C., & Sternberg, P. W. (2012). Ascaroside signaling is widely conserved among nematodes. Current Biology, 22(9), 772–780.

Ciancio, A., Colagiero, M., Pentimone, I., & Rosso, L. (2016). Soil microbial communities and their potential for root-knot nematodes management: a review. Environmental Engineering and Management Journal, 15(8), 1833–1839.

Cooke, R. C. (1962). The ecology of nematode-trapping fungi in the soil. Annals of Applied Biology, 50(3), 507–513.

Cooke, R. C. (1963). The predaceous activity of nematode-trapping fungi added to soil. Annals of Applied Biology, 51(2), 295–299.

Dahlin, P., Eder, R., Consoli, E., Krauss, J., & Kiewnick, S. (2019). Integrated control of Meloidogyne incognita in tomatoes using fluopyram and Purpureocillium lilacinum strain 251. Crop Protection, 124, 104874.

Dallemole-Giaretta, R., Freitas, L. G., Lopes, E. A., Pereira, O. L., Zooca, R. J. F., & Ferraz, S. (2012). Screening of Pochonia chlamydosporia Brazilian isolates as biocontrol agents of Meloidogyne javanica. Crop Protection, 42, 102–107.

Dasgupta, M. K., & Khan, M. R. (2015). Nematophagous fungi: ecology, diversity and geographical distribution. In T. H. Askery & R. P. P. Martinelli (Eds.), Biocontrol agents of phytonematodes (pp. 126–162). CABI.

Dávila, L., & Hío, J. C. (2005). Evaluación de la actividad biocontroladora de Arthrobotrys sp. y Paecilomyces sp. sobre Meloidogyne javanica in vitro y bajo condiciones de invernadero en crisantemo (Drendranthema grandiflora Andernson). Agronomía Colombiana, 23(1), 91–101.

Dijksterhuis, J., Veenhuis, M., Harder, W., & Nordbring-Hertz, B. (1994). Nematophagous fungi: physiological aspects and structure–function relationships. In A. H. Rose & D. W. Tempest (Eds.), Advances in Microbial Physiology (Vol. 36, pp. 111–143). Academic Press.

Dowsett, J. A., Reid, J., & Hopkin, A. A. (1984). Microscopic observations on the trapping of nematodes by the predaceous fungus Dactylella cionopaga. Canadian Journal of Botany, 62(4), 674–679.

Duponnois, R., Kisa, M., & Plenchette, C. (2006). Phosphate-solubilizing potential of the nematophagous fungus Arthrobotrys oligospora. Journal of Plant Nutrition and Soil Science, 169(2), 280–282.

Ekmen, Z. I., Cakmak, I., Karagoz, M., Hazir, S., Ozer, N., & Kaya, H. K. (2010). Food preference of Sancassania polyphyllae (Acari: Acaridae): living entomopathogenic nematodes or insect tissues? Biocontrol Science and Technology, 20(6), 553–566.

Eo, J., Park, K.-C., Park, B.-B., Eo, J., Park, K.-C., & Park, B.-B. (2012). Short-term effects of organic waste amendments on soil biota: responses of soil food web under eggplant cultivation. Soil Research, 50(5), 436–441.

Erazo, N. S., Echeverría, M. M., Jave, J. L., León, H. A., Lindao, V. A., Manzano, J. C., & Inca, N. M. (2020). Effect of Pleurotus ostreatus (Jacq.) and Trichoderma harzianum (Rifai) on Meloidogyne incognita (Kofoid & White) in tomato ( Solanum lycopersicum Mill.). Acta Scientiarum. Biological Sciences, 42(1), e47522.

Farah, M. T., Nur, A. M., Mat, H., Hamdan, A., & Nik, N. a. I. I. (2019). Screening of nematophagous-fungi from fresh faeces of grazing animals and soils. Tropical Biomedicine, 36(3), 687–693.

Flores, B. G., Ponce, I. M., Plascencia, M. Á., Mendieta, A., & López, V. E. (2021). Advances in the biological control of phytoparasitic nematodes via the use of nematophagous fungi. World Journal of Microbiology and Biotechnology, 37(10), 1–14.

Forghani, F., & Hajihassani, A. (2020). Recent advances in the development of environmentally benign treatments to control root-knot nematodes. Frontiers in Plant Science, 11.

Fravel, D. R., Deahl, K. L., & Stommel, J. R. (2005). Compatibility of the biocontrol fungus Fusarium oxysporum strain CS-20 with selected fungicides. Biological Control, 34(2), 165–169.

Ghani, M. I., Ali, A., Atif, M. J., Ali, M., Amin, B., Anees, M., Khurshid, H., & Cheng, Z. (2019). Changes in the soil microbiome in eggplant monoculture revealed by high-throughput Illumina MiSeq sequencing as influenced by raw garlic stalk amendment. International Journal of Molecular Sciences, 20(9), E2125.

Giné, A., & Sorribas, F. J. (2017). Effect of plant resistance and BioAct WG (Purpureocillium lilacinum strain 251) on Meloidogyne incognita in a tomato–cucumber rotation in a greenhouse. Pest Management Science, 73(5), 880–887.

Grønvold, J., Nansen, P., Henriksen, S. A., Larsen, M., Wolstrup, J., Bresciani, J., Rawat, H., & Fribert, L. (1996). Induction of traps by Otertagia ostertagi larvae, chlamydospore production and growth rate in the nematode-trapping fungus Duddingtonia flagrans. Journal of Helminthology, 70(4), 291–297.

Hafeez, R., Sindhu, Z. ud D., Iqbal, Z., & Muhammad, G. (2020). Documentation of naturally occurring nematophagous fungi in faeces/soil in hilly areas of Pakistan and investigation of the effect of season on their frequency distribution. International Journal of Agriculture and Biology, 24, 517–522.

Hahn, M. H., May De Mio, L. L., Kuhn, O. J., & Duarte, H. da S. S. (2019). Nematophagous mushrooms can be an alternative to control Meloidogyne javanica. Biological Control, 138, 104024.

Hamza, M. A., Tazi, H., Fossati, O., Moukhli, A., Hicham, L., Ferji, Z., Roussos, S., El Mousadik, A., Boubaker, H., & Mateille, T. (2020). May passive dispersal of fungal enemies with native substrates in olive nurseries help to control phytonematodes? Biotechnologie Agronomie Societe Et Environnement, 24(1), 37–45.

Helmberger, M. S., Shields, E. J., & Wickings, K. G. (2017). Ecology of belowground biological control: Entomopathogenic nematode interactions with soil biota. Applied Soil Ecology, 121, 201–213.

Hidalgo-Diaz, L., Bourne, J. M., Kerry, B. R., & Rodriguez, M. G. (2010). Nematophagous Verticillium spp. in soils infested with Meloidogyne spp. in Cuba: Isolation and screening. International Journal of Pest Management, 46(4), 277–284.

Hodson, A. K., Siegel, J. P., & Lewis, E. E. (2012). Ecological influence of the entomopathogenic nematode, Steinernema carpocapsae , on pistachio orchard soil arthropods. Pedobiologia, 55(1), 51–58.

Hsueh, Y.-P., Mahanti, P., Schroeder, F. C., & Sternberg, P. W. (2013). Nematode-trapping fungi eavesdrop on nematode pheromones. Current Biology, 23(1), 83–86.

Hussain, M., Zouhar, M., & Rysanek, P. (2016). Potential of some nematophagous fungi against Meloidogyne hapla infection in Czech Republic. Pakistan Journal of Zoology, 49(1), 35–43.

Iqbal, M., Dubey, M., McEwan, K., Menzel, U., Franko, M. A., Viketoft, M., Jensen, D. F., & Karlsson, M. (2018). Evaluation of Clonostachys roseab for control of plant-Parasitic nematodes in soil and in roots of carrot and wheat. Phytopathology®, 108(1), 52–59.

Jaffee, B. A. (2004). Wood, nematodes, and the nematode-trapping fungus Arthrobotrys oligospora. Soil Biology and Biochemistry, 36(7), 1171–1178.

Jaffee, B., Phillips, R., Muldoon, A., & Mangel, M. (1992). Density-dependent host-pathogen dynamics in soil microcosms. Ecology, 73(2), 495–506.

Jang, J. Y., Choi, Y. H., Shin, T. S., Kim, T. H., Shin, K.-S., Park, H. W., Kim, Y. H., Kim, H., Choi, G. J., Jang, K. S., Cha, B., Kim, I. S., Myung, E. J., & Kim, J.-C. (2016). Biological control of Meloidogyne incognita by Aspergillus niger F22 producing oxalic acid. PLOS ONE, 11(6), e0156230.

Jatala, P., Kaltenbach, R., & Bocángel, M. (1979). Biological control of Meloidogyne incognita acrita and Globodera pallida on potatoes. Journal of Nematology, 11(303).

Ji, X., Yu, Z., Yang, J., Xu, J., Zhang, Y., Liu, S., Zou, C., Li, J., Liang, L., & Zhang, K.-Q. (2020). Expansion of adhesion genes drives pathogenic adaptation of nematode-trapping fungi. IScience, 23(5), 101057.

Jiang, X., Xiang, M., & Liu, X. (2017). Nematode-trapping fungi. Microbiology Spectrum, 5(1), 1–12.

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., & Perry, R. N. (2013). Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular Plant Pathology, 14(9), 946–961.

Kepenekci, I., Hazir, S., Oksal, E., & Lewis, E. E. (2018). Application methods of Steinernema feltiae, Xenorhabdus bovienii and Purpureocillium lilacinum to control root-knot nematodes in greenhouse tomato systems. Crop Protection, 108, 31–38.

Kerry, B. R. (2000). Rhizosphere interactions and the exploitation of microbial agents for the biological control of plant-parasitic nematodes. Annual Review of Phytopathology, 38, 423–441.

Khan, A., Williams, K. L., & Nevalainen, H. K. M. (2006). Infection of plant-parasitic nematodes by Paecilomyces lilacinus and Monacrosporium lysipagum. BioControl, 51(5), 659–678.

Klinter, S., Bulone, V., & Arvestad, L. (2019). Diversity and evolution of chitin synthases in oomycetes (Straminipila: Oomycota). Molecular Phylogenetics and Evolution, 139, 106558.

Koziak, A. T. E., Diaz, F. C., Diaz, J., Garcia, M., Janzen, D. H., & Thorn, R. G. (2007). Costa Rican species of Nematoctonus (anamorphic Pleurotaceae). Canadian Journal of Botany, 85(8), 749–761.

Kumar, D., Maurya, N., Kumar, P., Singh, H., & Addy, S. K. (2015). Assessment of germination and carnivorous activities of a nematode-trapping fungus Arthrobotrys dactyloides in fungistatic and fungicidal soil environment. Biological Control, 82, 76–85.

Kumar, D., & Singh, K. P. (2006). Assessment of predacity and efficacy of Arthrobotrys dactyloides for biological control of root knot disease of tomato. Journal of Phytopathology, 154(1), 1–5.

Kumar, N., Chindo, P. S., & Singh, K. P. (2011). The trapping fungus Dactylaria brochopaga: induction of trap formation, attraction, trapping and the development in some phytonematodes. Archives of Phytopathology and Plant Protection, 44(13), 1322–1334.

Leong, S. S., Leong, S. C. T., Pau, C. G., Andrew, G., & Beattie, C. (2021). In vitro bioassay of Purpureocillium lilacinum and Bacillus thuringiensis for control of Meloidogyne incognita on black pepper (Piper nigrum L.) in Sarawak, Malaysia, Northern Borneo. Journal of the Entomological Research Society, 23(1), 41–59.

Li, J., Zou, C., Xu, J., Ji, X., Niu, X., Yang, J., Huang, X., & Zhang, K.-Q. (2015). Molecular mechanisms of nematode-nematophagous microbe interactions: basis for ciological Control of plant-parasitic nematodes. Annual Review of Phytopathology, 53, 67–95.

Liang, L.-M., Zou, C.-G., Xu, J., & Zhang, K.-Q. (2019). Signal pathways involved in microbe–nematode interactions provide new insights into the biocontrol of plant-parasitic nematodes. Philosophical Transactions of the Royal Society B, 374(1767).

Liang, L., Liu, Z., Liu, L., Li, J., Gao, H., Yang, J., & Zhang, K. Q. (2016). The nitrate assimilation pathway is involved in the trap formation of Arthrobotrys oligospora, a nematode-trapping fungus. Fungal Genetics and Biology, 92, 33–39.

Liang, L., Shen, R., Mo, Y., Yang, J., Ji, X., & Zhang, K. Q. (2015). A proposed adhesin AoMad1 helps nematode-trapping fungus Arthrobotrys oligospora recognizing host signals for life-style switching. Fungal Genetics and Biology, 81, 172–181.

Liu, K., Tian, J., Xiang, M., & Liu, X. (2012). How carnivorous fungi use three-celled constricting rings to trap nematodes. Protein & Cell, 3(5), 325–328.

Liu, K., Zhang, W., Lai, Y., Xiang, M., Wang, X., Zhang, X., & Liu, X. (2014). Drechslerella stenobrocha genome illustrates the mechanism of constricting rings and the origin of nematode predation in fungi. BMC Genomics, 15, 114.

Lohde, G. (1874). Ueber einiger neue parasitische Pilze. Tageblatt Für Die Versammlung Deutscher Naturforscher Und Ärzte, 47, 203–206.

Meerupati, T., Andersson, K.-M., Friman, E., Kumar, D., Tunlid, A., & Ahrén, D. (2013). Genomic mechanisms accounting for the adaptation to parasitism in nematode-trapping fungi. PLOS Genetics, 9(11), e1003909.

Morgan, M., Behnke, J. M., Lucas, J. A., & Peberdy, J. F. (1997). In vitro assessment of the influence of nutrition, temperature and larval density on trapping of the infective larvae of Heligmosomoides polygyrus by Arthrobotrys oligospora, Duddingtonia flagrans and Monacrosporium megalosporum. Parasitology, 115(3), 303–310.

Murga-Gutierrez, S. N., Colagiero, M., Rosso, L. C., Sialer, M. M. F., & Ciancio, A. (2012). Root-knot nematodes from asparagus and associated biological antagonists in Peru. Nematropica, 42(1), 57–62.

Mwaheb, M. A. M. A., Hussain, M., Tian, J., Zhang, X., Hamid, M. I., El-Kassim, N. A., Hassan, G. M., Xiang, M., & Liu, X. (2017). Synergetic suppression of soybean cyst nematodes by chitosan and Hirsutella minnesotensis via the assembly of the soybean rhizosphere microbial communities. Biological Control, 115, 85–94.

Naranjo-Morán, J. A., Vera-Morales, M., Barcos-Arias, M. S., Oviedo-Anchundia, R. J., Sánchez-Rendón, V. E., & Pino-Acosta, A. Y. (2021). Dispersión y transporte de propágulos micorrícicos en el bosque seco tropical. Ecosistemas, 30(1), 2062–2062.

Naves, R. L., & Campos, V. P. (1991). Ocorrěncia de fungos predadores de nematóides no sul de Minas Gerais e estudo de capacidade predatória e crescimento in vitro de alguns de seus isolados. Nematologia Brasileira, XV(2), 152–162.

Nguyen, V. L., Bastow, J. L., Jaffee, B. A., & Strong, D. R. (2007). Response of nematode-trapping fungi to organic substrates in a coastal grassland soil. Mycological Research, 111(7), 856–862.

Nordbring-Hertz, B. (2004). Morphogenesis in the nematode-trapping fungus Arthrobotrys oligospora - an extensive plasticity of infection structures. Mycologist, 18(3), 125–133.

Nordbring-Hertz, B., Jansson, H.-B., & Tunlid, A. (2011). Nematophagous fungi. In eLS. American Cancer Society.

Olivares-Campos, B. O., López-Beltrán, M. A., & Lobo-Luján, D. (2019). Cambios de usos de suelo y vegetación en la comunidad agraria Kashaama, Anzoátegui, Venezuela: 2001-2013. Revista Geográfica de América Central, 2(63).

Olivares, Barlin O., Calero, J., Rey, J. C., Lobo, D., Landa, B. B., & Gómez, J. A. (2022). Correlation of banana productivity levels and soil morphological properties using regularized optimal scaling regression. Catena, 208, 105718.

Olivares, Barlin O., Rey, J. C., Lobo, D., Navas-Cortés, J. A., Gómez, J. A., & Landa, B. B. (2021a). Fusarium wilt of bananas: a review of agro-environmental factors in the Venezuelan production system affecting its development. Agronomy 2021, Vol. 11, Page 986, 11(5), 986.

Olivares, Barlin Orlando. (2016). Descripción del manejo de suelos en sistemas de producción agrícola del sector Hamaca de Anzoátegui, Venezuela. La Granja, 23(1), 14–24.

Olivares, Barlin Orlando, Araya-Alman, M., Acevedo-Opazo, C., Rey, J. C., Cañete-Salinas, P., Kurina, F. G., Balzarini, M., Lobo, D., Navas-Cortés, J. A., Landa, B. B., & Gómez, J. A. (2020). Relationship between soil properties and banana productivity in the two main cultivation areas in Venezuela. Journal of Soil Science and Plant Nutrition, 20(4), 2512–2524.

Olivares, Barlin Orlando, Paredes, F., Rey, J. C., Lobo, D., & Galvis-Causil, S. (2021b). The relationship between the normalized difference vegetation index, rainfall, and potential evapotranspiration in a banana plantation of Venezuela. SAINS TANAH - Journal of Soil Science and Agroclimatology, 18(1), 58–64.

Olthof, T. H. A., & Estey, R. H. (1963). A nematotoxin produced by the nematophagous fungus Arthrobotrys oligospora Fresenius. Nature, 197(4866), 514–515.

Osman, H. A., Ameen, H. H., Mohamed, M., & Elkelany, U. S. (2020). Efficacy of integrated microorganisms in controlling root-knot nematode Meloidogyne javanica infecting peanut plants under field conditions. Bulletin of the National Research Centre, 44(1), 134.

Pacheco, P. V. M., Monteiro, T. S. A., Coutinho, R. R., Balbino, H. M., & De Freitas, L. G. (2020). Fungal biocontrol reduces the populations of the lesion nematode, Pratylenchus brachyurus, in soybean and corn. Nematology, 23(6), 619–626.

Peiris, P. U. S., Li, Y., Brown, P., & Xu, C. (2020). Fungal biocontrol against Meloidogyne spp. in agricultural crops: A systematic review and meta-analysis. Biological Control, 144, 104235.

Peng, Y., Li, S. J., Yan, J., Tang, Y., Cheng, J. P., Gao, A. J., Yao, X., Ruan, J. J., & Xu, B. L. (2021). Research progress on phytopathogenic fungi and their role as biocontrol agents. Frontiers in Microbiology, 12, 1209.

Persmark, L., & Jansson, H.-B. (1997). Nematophagous fungi in the rhizosphere of agricultural crops. FEMS Microbiology Ecology, 22(4), 303–312.

Persson, Y., & Bååth, E. (1992). Quantification of mycoparasitism by the nematode-trapping fungus Arthrobotrys oligospora on Rhizoctonia solani and the influence of nutrient levels. FEMS Microbiology Letters, 101(1), 11–16.

Pramer, D. (1964). Nematode-trapping fungi. Science, 144(3617), 382–388.

Quevedo, A., Vera-Morales, M., Espinoza-Lozano, F., Castañeda-Ruiz, R. F., Sosa del Castillo, D., & Magdama, F. (2021). Assessing the predatory activity of Arthrobotrys oligosporus strain C-2197 as biocontrol of the root-knot nematode Meloidogyne spp. Bionatura, 6(1), 1586–1592.

Rosén, S., Sjollema, K., Veenhuis, M., & Tunlid, A. (1997). A cytoplasmic lectin produced by the fungus Arthrobotrys oligospora functions as a storage protein during saprophytic and parasitic growth. Microbiology, 143(8), 2593–2604.

Rubner, A. (1994). Predaceous fungi from Ecuador. Mycotaxon, 51, 143–151.

Salazar, C., Betancourth, C., & Castillo, A. (2012). Efecto de controladores biológicos sobre el nematodo Meloidogyne spp. en lulo (Solanum quitoense Lam). Revista de Ciencias Agrícolas, 29(2), 81–92.

Sánchez, J. Y., & Cardona, N. L. (2018). Evaluación del bioformulado y del filtrado crudo de Purpureocillium sp. cepa Udea0106 sobre nemátodos fitopatógenos en crisantemo (Dendranthema grandiflora). Biotecnología Aplicada, 35(2), 2221–2227.

Sasanelli, N., Konrat, A., Migunova, V., Toderas, I., Iurcu-Straistaru, E., Rusu, S., Bivol, A., Andoni, C., & Veronico, P. (2021). Review on control methods against plant parasitic nematodes applied in southern member states (C Zone) of the European Union. Agriculture 2021, Vol. 11, Page 602, 11(7), 602.

Saxena, G. (2018). Biological control of root-knot and cyst nematodes using nematophagous fungi. 221–237.

Silva, J. F., & Campos, V. P. (1991). Fungos endoparasitos de nematóides que ocurrem no sul de minas Gerais, Brasil 1. Aspectos morfológicos e do parastismo. Nematologia Brasileira, XV(2), 94–103.

Silva, S. D., Carneiro, R. M. D. G., Faria, M., Souza, D. A., Monnerat, R. G., & Lopes, R. B. (2017). Evaluation of Pochonia chlamydosporia and Purpureocillium lilacinum for suppression of Meloidogyne enterolobii on tomato and banana. Journal of Nematology, 49(1), 77–85.

Singh, K. P., Jaiswal, R. K., Kumar, N., & Kumar, D. (2007). Nematophagous fungi associated with root galls of rice caused by Meloidogyne graminicola and its control by Arthrobotrys dactyloides and Dactylaria brochopaga. Journal of Phytopathology, 155(4), 193–197.

Singh, S., & Mathur, N. (2010). Biological control of root-knot nematode, Meloidogyne incognita infesting tomato. Biocontrol Science and Technology, 20(8), 865–874.

Soares, F. E. de F., Gôlo, P. S., & Fernandes, É. K. K. (2020). Nematophagous and entomopathogenic fungi: new insights into the beneficial fungus-plant interaction. In V. Sharma, R. Salwan, & L. K. T. Al-Ani (Eds.), Molecular Aspects of Plant Beneficial Microbes in Agriculture (pp. 295–304). Academic Press.

Solano, T. F., Castillo, M. L. L., Medina, J., & del Pozo, E. M. (2015). Efectividad de hongos nematófagos sobre Meloidogyne incognita (Kofoid y White) Chitwood en tomate en condiciones de campo, Loja, Ecuador. Revista de Protección Vegetal, 29(3), 192.

Soliman, M. S., El-Deriny, M. M., Ibrahim, D. S. S., Zakaria, H., & Ahmed, Y. (2021). Suppression of root-knot nematode Meloidogyne incognita on tomato plants using the nematode trapping fungus Arthrobotrys oligospora Fresenius. Journal of Applied Microbiology. https://doi.org/10.1111/jam.15101

St. Leger, R. J., & Wang, J. B. (2020). Metarhizium : jack of all trades, master of many. Open Biology, 10(12), 200307.

Stelinski, L. L., Willett, D., Rivera, M. J., & Ali, J. G. (2019). “Tuning” communication among four trophic levels of the root biome to facilitate biological control. Biological Control, 131, 49–53.

Su, H. N., Xu, Y. Y., Wang, X., Zhang, K. Q., & Li, G. H. (2016). Induction of trap formation in nematode-trapping fungi by bacteria-released ammonia. Letters in Applied Microbiology, 62(4), 349–353.

Su, H., Zhao, Y., Zhou, J., Feng, H., Jiang, D., Zhang, K.-Q., & Yang, J. (2017). Trapping devices of nematode-trapping fungi: formation, evolution, and genomic perspectives. Biological Reviews of the Cambridge Philosophical Society, 92(1), 357–368.

Swe, A., Li, J., Zhang, K. Q., Pointing, S. B., Jeewon, R., & Hyde, K. D. (2011). Nematode-trapping fungi. Current Research in Environmental and Applied Mycology, 1(1), 1–26.

Thines, M. (2018). Oomycetes. Current Biology, 28(15), R812–R813.

Thongkaewyuan, A., & Chairin, T. (2018). Biocontrol of Meloidogyne incognita by Metarhizium guizhouense and its protease. Biological Control, 126, 142–146.

Topalović, O., & Heuer, H. (2019). Plant-nematode interactions assisted by microbes in the rhizosphere. Current Issues in Molecular Biology, 30(1), 75–88.

Tunlid, A., Jansson, H.-B., & Nordbring-Hertz, B. (1992). Fungal attachment to nematodes. Mycological Research, 96(6), 401–412.

van den Hoogen, J., Geisen, S., Routh, D., Ferris, H., Traunspurger, W., Wardle, D. A., de Goede, R. G. M., Adams, B. J., Ahmad, W., Andriuzzi, W. S., Bardgett, R. D., Bonkowski, M., Campos-Herrera, R., Cares, J. E., Caruso, T., de Brito Caixeta, L., Chen, X., Costa, S. R., Creamer, R., … Crowther, T. W. (2019). Soil nematode abundance and functional group composition at a global scale. Nature, 572(7768), 194–198.

Vidal-Diez de Ulzurrun, G., & Hsueh, Y.-P. (2018). Predator-prey interactions of nematode-trapping fungi and nematodes: both sides of the coin. Applied Microbiology and Biotechnology, 102(9), 3939–3949.

Wan, J., Dai, Z., Zhang, K., Li, G., & Zhao, P. (2021). Pathogenicity and metabolites of endoparasitic nematophagous fungus Drechmeria coniospora YMF1.01759 against nematodes. Microorganisms, 9(8).

Wang, B.-L., Chen, Y.-H., He, J.-N., Xue, H.-X., Yan, N., Zeng, Z.-J., Bennett, J. W., Zhang, K.-Q., & Niu, X.-M. (2018). Integrated metabolomics and morphogenesis reveal volatile signaling of the nematode-trapping fungus Arthrobotrys oligospora. Applied and Environmental Microbiology, 84(9), e02749-17.

Webster, J., & Weber, R. (2007). Anamorphic fungi (nematophagous and aquatic forms). In J. Webster & R. Weber (Eds.), Introduction to Fungi (3rd ed., pp. 673–701). Cambridge University Press.

Woodward, J. E., Walker, N. R., Dillwith, J. W., Zhang, H., & Martin, D. L. (2005). The influence of fungicides on Arthrobotrys oligospora in simulated putting green soil. Annals of Applied Biology, 146(1), 115–121.

Xiang, M., Xiang, P., Liu, X., & Zhang, L. (2010). Effect of environment on the abundance and activity of the nematophagous fungus Hirsutella minnesotensis in soil. FEMS Microbiology Ecology, 71(3), 413–417.

Xie, H., Aminuzzaman, F. M., Xu, L., Lai, Y., Li, F., & Liu, X. (2010). Trap induction and trapping in eight nematode-trapping fungi (Orbiliaceae) as affected by juvenile stage of Caenorhabditis elegans. Mycopathologia, 169(6), 467–473.

Xie, M., Bai, N., Yang, J., Jiang, K., Zhou, D., Zhao, Y., Li, D., Niu, X., Zhang, K. Q., & Yang, J. (2020). Protein kinase Ime2 is required for mycelial growth, conidiation, osmoregulation, and pathogenicity in nematode-trapping fungus Arthrobotrys oligospora. Frontiers in Microbiology, 10, 3065.

Xie, M., Ma, N., Bai, N., Zhu, M., Zhang, K. Q., & Yang, J. (2021). Phospholipase C (AoPLC2) regulates mycelial development, trap morphogenesis, and pathogenicity of the nematode-trapping fungus Arthrobotrys oligospora. Journal of Applied Microbiology.

Xie, M., Yang, J., Jiang, K., Bai, N., Zhu, M., Zhu, Y., Zhang, K. Q., & Yang, J. (2021). AoBck1 and AoMkk1 are necessary to maintain cell wall integrity, vegetative growth, conidiation, stress resistance, and pathogenicity in the nematode-trapping fungus Arthrobotrys oligospora. Frontiers in Microbiology, 12, 649582.

Yang, C.-T., Vidal-Diez de Ulzurrun, G., Gonçalves, A. P., Lin, H.-C., Chang, C.-W., Huang, T.-Y., Chen, S.-A., Lai, C.-K., Tsai, I. J., Schroeder, F. C., Stajich, J. E., & Hsueh, Y.-P. (2020). Natural diversity in the predatory behavior facilitates the establishment of a robust model strain for nematode-trapping fungi. Proceedings of the National Academy of Sciences of the United States of America, 117(12), 6762–6770.

Yang, Y., Yang, E., An, Z., & Liu, X. (2007). Evolution of nematode-trapping cells of predatory fungi of the Orbiliaceae based on evidence from rRNA-encoding DNA and multiprotein sequences. Proceedings of the National Academy of Sciences of the United States of America, 104(20), 8379–8384.

Yu, Y., Zhang, Y. K., Manohar, M., Artyukhin, A. B., Kumari, A., Tenjo-Castano, F. J., Nguyen, H., Routray, P., Choe, A., Klessig, D. F., & Schroeder, F. C. (2021). Nematode signaling molecules are extensively metabolized by animals, plants, and microorganisms. ACS Chemical Biology, 16(6), 1050–1058.

Zhang, Y., Li, S., Li, H., Wang, R., Zhang, K.-Q., & Xu, J. (2020). Fungi–nematode interactions: diversity, ecology, and biocontrol prospects in agriculture. Journal of Fungi, 6(4), 206.

Zhang, Y., Zhang, K.-Q., & Hyde, K. D. (2014). The ecology of nematophagous fungi in natural environments. In K.-Q. Zhang & K. D. Hyde (Eds.), Nematode-trapping fungi (pp. 211–229). Springer Netherlands.