Uso e impacto de hongos entomopatógenos endofíticos: Su potencial en el contexto de la sostenibilidad agrícola
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https://doi.org/10.18633/biotecnia.v26.1986Palabras clave:
endófitos, enfermedades de plantas, manejo integrado de plagas, promotores del crecimientoResumen
El uso de hongos entomopatógenos (HE) como endófitos constituye una alternativa para la producción sustentable de alimentos, dado que el paradigma actual en la protección de cultivos se basa en el uso de plaguicidas organosintéticos, con más de dos millones de toneladas anuales. Por estas razones, los HE tienen la capacidad de vivir dentro de los tejidos vegetales como endófitos los cuales actúan como bioplaguicidas. Esta revision analiza y discute el estatus global de los hongos entomopatógenos endófitos (HEE), su potencial en la proteccion de plantas contra enfermedades y plagas de insectos y como promotores del crecimiento. Se examinan los éxitos, fracasos y perspectivas de aplicación en campo. Se han publicado más de 7000 estudios sobre HEE con importantes casos de éxito. Sin embargo, es necesario entender que la producción agrícola se basa en el uso de plaguicidas. Mientras ocurren cambios progresivos, es fundamental investigar el efecto de estas sustancias sobre la eficacia y presistencia de los HEE, considerando que el desconocimiento del efecto de los factores bióticos y abióticos sobre los HEE es una causa importante de freacasos. Estudios futuros deberán enfocarse en esclarecer aspectos como estrategias de aplicación, presistencia endófita y vias de transmisión para mejorar la sustentabilidad de la producción agrícola.
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Ahmad, I., Jiménez-Gasco, M., Luthe, D.S., Shakeel, S.N. and Barbercheck, M.E. 2020. Endophytic Me-tarhizium robertsii promotes maize growth, suppresses insect growth, and alters plant defense gene ex-pression. Biological Control. 144: 104167.
Ambele, C.F., Ekesi, S., Bisseleua, H.D., Babalola, O.O., Khamis, F.M., Djuideu, C.T. and Akutse, K.S. 2020. Entomopathogenic fungi as endophytes for biological control of subterranean termite pests at-tacking cocoa seedlings. Journal of Fungi. 6: 126.
Araus, J.L., Serret, M.D. and Lopes, M.S. 2019. Transgenic solutions to increase yield and stability in wheat: shining hope or flash in the pan?. Journal of Experimental Botany 70: 1419-1424.
Bamisile, B.S., Dash, C.K., Akutse, K.S., Keppanan, R. and Wang, L. 2018b. Fungal endophytes: beyond herbivore management. Frontiers in Microbiology. 9: 544.
Bamisile, B.S., Dash, C.K., Akutse, K.S., Keppanan, R., Afolabi, O.G., Hussain, M., Qasim, M. and Wang, L. 2018a. Prospects of endophytic fungal entomopathogens as biocontrol and plant growth promoting agents: An insight on how artificial inoculation methods affect endophytic colonization of host plants. Microbiological Research. 217: 34-50.
Barelli, L., Moonjely, S., Behie, S.W. and Bidochka, M.J. 2016. Fungi with multifunctional lifestyles: en-dophytic insect pathogenic fungi. Plant Molecular Biology. 90: 657-664.
Behie, S.W., Moreira, C.C., Sementchoukova, I., Barelli, L., Zelisko, P.M. and Bidochka, M.J. 2017. Car-bon translocation from a plant to an insect-pathogenic endophytic fungus. Nature Communications. 8: 1-5.
Bing, L.A. and Lewis, L.C. 1992. Endophytic Beauveria bassiana (Balsamo) Vuillemin in corn: the influ-ence of the plant growth stage and Ostrinia nubilalis (Hübner). Biocontrol Science and Technology. 2: 39-47.
Busby, P.E., Ridout, M. and Newcombe, G. 2016. Fungal endophytes: modifiers of plant disease. Plant Molecular Biology. 90: 645-655.
Canassa, F., Esteca, F.C., Moral, R.A., Meyling, N.V., Klingen, I. and Delalibera, I. 2020. Root inoculation of strawberry with the entomopathogenic fungi Metarhizium robertsii and Beauveria bassiana reduces incidence of the twospotted spider mite and selected insect pests and plant diseases in the field. Journal of Pest Science. 93: 261-274.
Carvalho, F.P. 2017. Pesticides, environment, and food safety. Food and Energy Security. 6: 48-60.
Clifton, E.H., Jaronski, S.T., Coates, B.S., Hodgson, E.W. and Gassmann, A.J. 2018. Effects of endophytic entomopathogenic fungi on soybean aphid and identification of Metarhizium isolates from agricultural fields. PLoS One. 13: e0194815.
da Costa Stuart, A.K., Stuart, R.M. and Pimentel, I.C. 2018. Effect of agrochemicals on endophytic fungi community associated with crops of organic and conventional soybean (Glycine max L. Mer-ril). Agriculture and Natural Resources. 52: 388-392.
Dara, S.K. 2019. Non-entomopathogenic roles of entomopathogenic fungi in promoting plant health and growth. Insects. 10: 277.
Dara, S.K., Dara, S.S. and Dara, S.S. 2017. Impact of entomopathogenic fungi on the growth, development, and health of cabbage growing under water stress. American Journal of Plant Sciences. 8: 76194.
Dara, S.K., Dara, S.S., Dara, S.S. and Anderson, T. 2016. First report of three entomopathogenic fungi of-fering protection against the plant pathogen, Fusarium oxysporum f. sp. vasinfectum. E-Journal of En-tomology and Biologicals.
Deutsch, C.A., Tewksbury, J.J., Tigchelaar, M., Battisti, D.S., Merrill, S.C., Huey, R.B. and Naylor, R.L. 2018. Increase in crop losses to insect pests in a warming climate. Science. 361: 916-919.
Devi, G. 2018. Nematophagous fungi: Metarhizium anisopliae. International Journal of Environmental Re-search. 3: 2110-2113.
Ganesan, M., Lee, H.Y., Kim, J.I. and Song, P.S. 2017. Development of transgenic crops based on photo‐biotechnology. Plant, Cell & Environment. 40: 2469-2486.
Garrido-Jurado, I., Resquín-Romero, G., Amarilla, S.P., Ríos-Moreno, A., Carrasco, L. and Quesada-Moraga, E. 2017. Transient endophytic colonization of melon plants by entomopathogenic fungi after foliar application for the control of Bemisia tabaci Gennadius (Hemiptera: Aleyrodi-dae). Journal of Pest Science. 90: 319-330.
Gathage, J.W., Lagat, Z.O., Fiaboe, K.K.M., Akutse, K.S., Ekesi, S. and Maniania, N.K. 2016. Prospects of fungal endophytes in the control of Liriomyza leafminer flies in common bean Phaseolus vulgaris under field conditions. BioControl. 61: 741-753.
Getahun, M.N., Biasazin, T.D., Wolde-Hawariat, Y., Bengtsson, J.M., Hillbur, Y. and Seyoum, E. 2016. Metarhizium sp. isolated from dead Pachnoda interrupta (Coleoptera: Scarabaeidae) as a potential en-tomopathogenic fungus for the pest insect: proof-of-concept for autodissemination. International Journal of Tropical Insect Science. 36: 1-9.
González-Mas, N., Cuenca-Medina, M., Gutiérrez-Sánchez, F. and Quesada-Moraga, E. 2019. Bottom-up effects of endophytic Beauveria bassiana on multitrophic interactions between the cotton aphid, Aphis gossypii, and its natural enemies in melon. Journal of Pest Science. 92: 1271-1281.
González‐Guzmán, A., Sacristán, D., Quesada‐Moraga, E., Torrent, J. del Campillo, M.C. and Sánchez‐Rodríguez, A.R. 2020. Effects of entomopathogenic fungi on growth and nutrition in wheat grown on two calcareous soils: Influence of the fungus application method. Annals of Applied Biology. 177: 26-40.
Greenfield, M., Gómez-Jiménez, M.I., Ortiz, V., Vega, F.E., Kramer, M. and Parsa, S. 2016. Beauveria bassiana and Metarhizium anisopliae endophytically colonize cassava roots following soil drench inoc-ulation. Biological Control. 95: 40-48.
Gutiérrez-Cárdenas, O.G., Cortez-Madrigal. H., Malo, E.A., Gómez-Ruíz, J. and Nord, R. 2019. Physio-logical and pathogenical characterization of Beauveria bassiana and Metarhizium anisopliae isolates for management of adult Spodoptera frugiperda. Southwestern Entomologist. 44: 409-421.
Jaber, L.R. 2018. Seed inoculation with endophytic fungal entomopathogens promotes plant growth and reduces crown and root rot (CRR) caused by Fusarium culmorum in wheat. Planta. 248: 1525-1535.
Jaber, L.R. and Enkerli, J. 2016. Effect of seed treatment duration on growth and colonization of Vicia faba by endophytic Beauveria bassiana and Metarhizium brunneum. Biological Control. 103: 187-195.
Jaber, L.R. and Enkerli, J. 2017. Fungal entomopathogens as endophytes: can they promote plant growth?. Biocontrol Science and Technology. 27: 28-41.
Jaber, L.R. and Ownley, B.H. 2017. Can we use entomopathogenic fungi as endophytes for dual biological control of insect pests and plant pathogens?. Biological Control. 116: 36-45.
Javed, K., Javed, H., Mukhtar, T. and Qiu, D. 2019. Pathogenicity of some entomopathogenic fungal strains to green peach aphid, Myzus persicae Sulzer (Homoptera: Aphididae). Egyptian Journal of Biological Pest Control. 29: 1-7.
Kabaluk, J.T., Lafontaine, J.P. and Borden, J.H. 2015. An attract and kill tactic for click beetles based on Metarhizium brunneum and a new formulation of sex pheromone. Journal of Pest Science. 88: 707-716.
Khare, E., Mishra, J. and Rora, N.K. 2018. Multifaceted interactions between endophytes and plant: devel-opments and prospects. Frontiers in Microbiology. 9: 2732.
Kumar, C.S., Jacob, T.K., Devasahayam, S., Thomas, S. and Geethu, C. 2018. Multifarious plant growth promotion by an entomopathogenic fungus Lecanicillium psalliotae. Microbiological Research. 207: 153-160.
Kumar, D. and Kalita, P. 2017. Reducing postharvest losses during storage of grain crops to strengthen food security in developing countries. Foods. 6: 8.
Kumar, M., Yusuf, M.A. and Nigam, M. 2018. An update on genetic modification of chickpea for increased yield and stress tolerance. Molecular Biotechnology. 60: 651-663.
Lechenet, M., Dessaint, F., Py, G., Makowski, D. and Munier-Jolain, N. 2017. Reducing pesticide use while preserving crop productivity and profitability on arable farms. Nature Plants. 3: 1-6.
Lee, Y.S. and Kim, Y.C. 2019. Tobacco growth promotion by the entomopathogenic fungus, Isaria javanica pf185. Mycobiology. 47: 126-133.
Lopez, D.C., Zhu-Salzman, K., Ek-Ramos, M.J. and Sword, G.A. 2014. The entomopathogenic fungal en-dophytes Purpureocillium lilacinum (formerly Paecilomyces lilacinus) and Beauveria bassiana nega-tively affect cotton aphid reproduction under both greenhouse and field conditions. PLoS One. 9: e103891.
Lu, B.R. and Yang, C. 2009. Gene flow from genetically modified rice to its wild relatives: Assessing po-tential ecological consequences. Biotechnology Advances. 27: 1083-1091.
Mantzoukas, S. and Eliopoulos, P.A. 2020. Endophytic entomopathogenic fungi: A valuable biological con-trol tool against plant pests. Applied Sciences. 10: 360.
Mantzoukas, S. and Grammatikopoulos, G. 2020. The effect of three entomopathogenic endophytes of the sweet sorghum on the growth and feeding performance of its pest, Sesamia nonagrioides larvae, and their efficacy under field conditions. Crop Protection. 127: 104952.
Martinez-Medina, A., Flors, V., Heil, M., Mauch-Mani, B., Pieterse, C.M., Pozo, M.J., Ton, J., van Dam, N.M. and Conrath, U. 2016. Recognizing plant defense priming. Trends in Plant Science. 21: 818-822.
Mayerhofer, J., Eckard, S., Hartmann, M., Grabenweger, G., Widmer, F., Leuchtmann, A. and Enkerli, J. 2017. Assessing effects of the entomopathogenic fungus Metarhizium brunneum on soil microbial communities in Agriotes spp. biological pest control. FEMS Microbiology Ecology. 93: fix117.
McKinnon, A.C., Saari, S., Moran-Diez, M.E., Meyling, N.V., Raad, M. and Glare, T.R. 2017. Beauveria bassiana as an endophyte: a critical review on associated methodology and biocontrol poten-tial. BioControl. 62: 1-17.
Mfuti, D.K., Subramanian, S., van Tol, R.W., Wiegers, G.L., de Kogel, W.J., Niassy, S., du Plessis, H., Ekesi, S. and Maniania, N.K. 2015. Spatial separation of semiochemical lurem‐TR and entomopatho-genic fungi to enhance their compatibility and infectivity in an autoinoculation system for thrips man-agement. Pest Management Science. 72: 131-139.
Mora-Aguilera, G., Cortez-Madrigal, H. and Acevedo-Sánchez, G. 2017. Epidemiology of entomopatho-gens: Basis for rational use of microbial control of insects. Southwestern Entomologist. 42: 153-169.
Morjan, W.E., Pedigo, L.P. and Lewis, L.C. 2002. Fungicidal effects of glyphosate and glyphosate formula-tions on four species of entomopathogenic fungi. Environmental Entomology. 31: 1206-1212.
Nord, R., Cortez-Madrigal, H., Rodríguez-Guzmán, E., Villar-Luna, E. and Gutiérrez-Cárdenas, O.G. 2020. Grafting wild tomato genotypes and Mexican landraces increases trichome density and resistance against pests. Southwestern Entomologist. 45: 649-662.
Pathan, E.K. and Deshpande, M.V. 2019. The puzzle of highly virulent Metarhizium anisopliae strains from Annona squamosa fields against Helicoverpa armigera. Journal of Basic Microbiology. 59: 392-401.
Pérez-González, O. and Sánchez-Peña, S.R. 2017. Compatibility in vitro and in vivo of the entomopathogenic fungi Beauveria bassiana and Hirsutella citriformis with selected insecticides. Southwestern Entomol-ogist. 42: 707-718.
Putnoky-Csicsó, B., Tonk, S., Szabó, A., Márton, Z., Bogdányi, F.T., Tóth, F., Abod, É., Bálint, J. and Ba-log, A. 2020. Effectiveness of the entomopathogenic fungal species Metarhizium anisopliae strain NCAIM 362 treatments against soil inhabiting Melolontha melolontha larvae in sweet potato (Ipomoea batatas L.). Journal of Fungi. 6: 116.
Quesada-Moraga, E. 2020. Entomopathogenic fungi as endophytes: their broader contribution to IPM and crop production. Biocontrol Science and Technology. 30: 864-867.
Ramakuwela, T., Hatting, J., Bock, C., Vega, F.E., Wells, L., Mbata, G.N. and Shapiro-Ilan, D. 2020. Es-tablishment of Beauveria bassiana as a fungal endophyte in pecan (Carya illinoinensis) seedlings and its virulence against pecan insect pests. Biological Control. 140: 104102.
Renuka, S., Ramanujam, B. and Poornesha, B. 2016. Endophytic ability of different isolates of ento-mopathogenic fungi Beauveria bassiana (Balsamo) Vuillemin in stem and leaf tissues of maize (Zea mays L.). Indian Journal of Microbiology. 56: 126-133.
Richter, D.L., Dixon, T.G. and Smith, J.K. 2016. Revival of saprotrophic and mycorrhizal basidiomycete cultures after 30 years in cold storage in sterile water. Canadian Journal of Microbiology. 54: 595-599.
Rivas-Franco, F., Hampton, J.G., Narciso, J., Rostás, M., Wessman, P., Saville, D.J., Jackson, T.A. and Glare, T.R. 2020. Effects of a maize root pest and fungal pathogen on entomopathogenic fungal rhizo-sphere colonization, endophytism and induction of plant hormones. Biological Control. 150: 104347.
Russo, M.L., Pelizza, S.A., Cabello, M.N., Stenglein, S.A. and Scorsetti, A.C. 2015. Endophytic coloniza-tion of tobacco, corn, wheat and soybeans by the fungal entomopathogen Beauveria bassi-ana (Ascomycota, Hypocreales). Biocontrol Science and Technology. 25: 475-480.
Russo, M.L., Pelizza, S.A., Vianna, M.F., Allegrucci, N., Cabello, M.N., Toledo, A.V., Mourelos, C. and Scorsetti, A.C. 2019. Effect of endophytic entomopathogenic fungi on soybean Glycine max (L.) Merr. growth and yield. Journal of King Saud University Science. 31: 728-736.
Sánchez-Rodríguez, A.R., Raya-Díaz, S., Zamarreño, Á.M., García-Mina, J.M., del Campillo M.C. and Quesada-Moraga, E. 2018. An endophytic Beauveria bassiana strain increases spike production in bread and durum wheat plants and effectively controls cotton leafworm (Spodoptera littoralis) lar-vae. Biological Control. 116: 90-102.
Stone, L.B. and Bidochka, M.J. 2020. The multifunctional lifestyles of Metarhizium: evolution and applica-tions. Applied Microbiology and Biotechnology. 104: 9935-9945.
Sun, T., Shen, Z., Shaukat, M., Du, C. and Ali, S. 2020. Endophytic isolates of Cordyceps fumosorosea to enhance the growth of Solanum melongena and reduce the survival of whitefly (Bemisia tabaci). Insects. 11: 78.
Tall, S. and Meyling, N.V. 2018. Probiotics for plants? Growth promotion by the entomopathogenic fungus Beauveria bassiana depends on nutrient availability. Microbial Ecology. 76: 1002-1008.
Tsatsakis, A.M., Nawaz, M.A., Kouretas, D., Balias, G., Savolainen, K., Tutelyan, V.A., Golokhvast, K.S., Lee, J.D., Yang, S.H. and Chung, G. 2017. Environmental impacts of genetically modified plants: a re-view. Environmental Research. 156: 818-833.
Ullah, M.I., Altaf, N., Afzal, M., Arshad, M., Mehmood, N., Riaz, M., Majeed, S., Ali, S., and Abdullah, A. 2019. Effects of entomopathogenic fungi on the biology of Spodoptera litura (Lepidoptera: Noctu-idae) and its reduviid predator, Rhynocoris marginatus (Heteroptera: Reduviidae). International Journal of Insect Science. 11: 1-7
Vega, F.E. 2018. The use of fungal entomopathogens as endophytes in biological control: a re-view. Mycologia. 110: 4-30.
Vega, F.E. and Blackwell, M. 2005. Insect-fungal associations: Ecology and evolution. Oxford University Press: Oxford, U.K.
Vega, F.E., Goettel, M.S,, Blackwell, M., Chandler, D., Jackson, M.A., Keller, S., Koike, M., Maniania, N.K., Monzón, A., Ownley, B.H., Pell, J.K., Rangel, D.E.N. and Roy, H.E. 2009. Fungal entomopath-ogens: new insights on their ecology. Fungal Ecology. 2: 149-159.
Veloz-Badillo, G.M., Riveros-Ramírez, J., Angel-Cuapio, A., Arce-Cervantes, O., Flores-Chávez, B., Espitia-López, J., Loera, O. and Garza-López, P.M. 2019. The endophytic capacity of the entomopath-ogenic fungus Beauveria bassiana caused inherent physiological response in two barley (Hordeum vulgare) varieties. 3 Biotech. 9: 1-6.
Wari, D., Okada, R., Takagi, M., Yaguchi, M., Kashima, T. and Ogawara, T. 2020. Augmentation and compatibility of Beauveria bassiana with pesticides against different growth stages of Bemisia tabaci (Gennadius); an in vitro and field approach. Pest Management Science. 76: 3236-3252.
Wei, Q.Y., Li, Y.Y., Xu, C., Wu, Y.X., Zhang, Y.R. and Liu, H. 2020. Endophytic colonization by Beau-veria bassiana increases the resistance of tomatoes against Bemisia tabaci. Arthropod-Plant Interactions. 14: 289-300.
Win, P.M., Matsumura, E. and Fukuda, K. 2021. Effects of pesticides on the diversity of endophytic fungi in Tea plants. Microbial Ecology. 82: 62-72.
Yun, H.G., Kim, D.J., Gwak, W.S., Shin, T.Y. and Woo, S.D. 2017. Entomopathogenic fungi as dual con-trol agents against both the pest Myzus persicae and phytopathogen Botrytis cinerea. Mycobiology. 45: 192-198.
Zhou, S., Qiu, H., Feng, C., Guo, Y., Wang, X. and Chen, C. 2016. Impact of deltamethrin on the endo-phytic fungal community of a Chinese cabbage, Brassica chinensis. Chemistry and Ecology. 32: 259-269.
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