The endophytic fungi and their potential uses in agriculture

Main Article Content

Belkis Peteira Delgado
Jersys Arévalo Ortega
Danay Ynfante Martínez
Benedicto Martínez Coca

Abstract

The objective of this work was to review different issues related to endophytes of fungal origin, with emphasis on their functions (especially those related to plant protection). In this paper, the general concept of endophyte, its classification, general procedures for its isolation, characterization and conservation are detailed. Some of its most important functions are mentioned and explained, and examples of its functions in plant protection including the risk of their application, are described, and so are the cases of mixed application with other endophytes or with other biological controls with predator or parasitoid function.

Article Details

How to Cite
Peteira Delgado, B., Arévalo Ortega, J., Ynfante Martínez, D., & Martínez Coca, B. (2021). The endophytic fungi and their potential uses in agriculture. Revista De Protección Vegetal, 36(3). Retrieved from https://revistas.censa.edu.cu/index.php/RPV/article/view/1167
Section
REVIEW ARTICLES

References

Peteira B. La resistencia inducida como alternativa para el manejo de plagas en las plantas de cultivo. Rev. Protección Veg. 2020; 35 (1): 1-12.

Wafaa MH. Role of entophytic microorganisms in biocontrol of plant diseases. Life Science Journal. 2010; 7 (2): 57-62.

Stępniewska Z, Kuźniar A. Endophytic microorganisms—promising applications in bioremediation of greenhouse gases. Appl Microbiol Biotechnol 2013; 97:9589-9596.

Sánchez-Rodríguez AR, Raya-Díaz S, Zamarreño AM, García-Mina JM, del Campillo MC, Quesada-Moraga E. An endophytic Beauveria bassiana strain increases spike production in bread and durum wheat plants and effectively controls cotton leafworm (Spodoptera littoralis) larvae. Biological Control. 2017: 1049-9644. doi:10.1016/j.biocontrol.2017.01.012.

Morales García D. Bioprospección de hongos endófitos para el control biológico del nematodo barrenador Radopholus similis (Cobb) Thorn en el cultivo del banano. Trabajo Final de Graduación sometido al Tribunal del Área Académica Agroforestal del Instituto Tecnológico de Costa Rica para optar por el grado de Magister en Gestión de Recursos Naturales y Tecnologías de Producción. Campus Cartago, Costa Rica. 2014, págs.

Mishra Y, Singh A, Batra A, Sharma MM. Understanding the biodiversity and biological applications of endophytic fungi: A Review. J Microb Biochem Technol. 2014, S8:004. doi:10.4172/1948-5948.S8-004.

Yan-Ling Li, Xiao-Ming Xin, Zheng-Yao Chang, Ren-Jiu Shi1, Zeng-Min Miao, Jing Ding, et al. The endophytic fungi of Salvia miltiorrhiza Bge.f. alba are a potential source of natural antioxidants. Botanical Studies. 2015; 56 (5): 1-7.

Xiang Sun, Liang-Dong Guo. Endophytic fungal diversity: review of traditional and molecular techniques. Mycology: An International Journal on Fungal Biology. 2012; 3 (1): 65-76

Azevedo JL, Araujo WL. Diversity and applications of endophytic fungi isolated from tropical plants. In: Ganguli BN, Deshmukh SK (eds) Fungi multifaceted microbes. Anamaya, New Delh. 2007

Dina Pezo Santillan. Bioprotección de Plukenetia volubilis L. con el hongo Trichoderma sp. para reducir los daños de Meloidogyne incognita bajo condiciones de vivero. Tesis para optar el título profesional de ingeniero agrónomo. Universidad nacional de San Martín-Tarapoto, Facultad de Ciencias Agrarias Escuela Profesional de Agronomía. Tarapoto – Perú. 2016, 49 págs.

Bandara W, Seneviratne G, Kulasooriya A. Interactions among endophytic bacteria and fungi: effect and potentials. J Biosci. 2006; 31: 645-650.

Saucedo-García A, Anaya AL, Espinosa-García FJ, González MC. Diversity and communities of foliar endophytic fungi from different agroecosystems of Coffea arabica L. in two regions of Veracruz, Mexico. PLoS ONE. 2014; 9 (6): e98454. doi:10.1371/journal.pone.0098454.

Kumar DSS, Hyde KD. Biodiversity and tissue-recurrence of endophytic fungi in Tripterygium wilfordii. Fungal Diversity. 2004; 17: 69-90.

Macaya-Sanz D, Eugenio M.E, Martín-Sampedro R, Fillat U, Ibarra D, Del Barrio A, et al. Diversidad de hongos endófitos en especies forestales y su posible papel en la defensa de su hospedante y la degradación de la madera. 7mo Congreso Forestal Español. Gestión del Monte: Servicios ambientales y bioeconomía. 26-30 de Junio del 2017, Plasencia Cáceres, Extremadura. Ed. Soc. española de Ciencias Forestales. ISBN 978-84-941695-2-6.

Wilberforce EM, Boddy L, Griffiths R, Griffith GW. Agricultural management affects communities of culturable root-endophytic fungi in temperate grasslands. Soil Biology & Biochemistry. 2003; 35: 1143-1154.

Gómez Krupko M. Aislamiento y evaluación antifúngica de hongos endófitos de Acalypha gaumeri Pax y K. Hoffm. Tesis en opción al título de•Maestro en Ciencias Biológicas (Ciencias Biológicas: Opción Biotecnología). Centro de Investigación Científica de Yucatán, A.C. 2014. Págs. 99.

Rodríguez RJ, White Jr JF, Arnold AE, Redman RS. Fungal endophytes: diversity and functional roles. New Phytologist. 2009; 182: 314-330. doi: 10.1111/j.1469-8137.2009.02773.

Jalgaonwala RE, Vishwas MB, Totaram MR. A review: Natural products from plant associated endophytic fungi. J Microbiol. Biotech. Res. 2011; 1 (2): 21-32.

Sánchez-Fernández RE, Sánchez-Ortiz BL, Monserrat Sandoval-Espinosa YK, Ulloa-Benítez Á, Armendáriz-Guillén B, García-Méndez MC, et al. Hongos endófitos: fuente potencial de metabolitos secundarios bioactivos con utilidad en agricultura y medicina. Revista Especializada en Ciencias Químico-Biológicas. 2013; 16 (2):132-146.

Saikkonen K, Faeth SH, Helander M, Sullivan TJ. Fungal endophytes: A continuum of interactions with host plants. Annual Review of Ecology and Systematics. 1998; 29: 319-343.

Sánchez MMS. Estudio de la micobiota endofítica asociada a las gramíneas Dactylis glomerata, Holcus lanatus, Ammophila arenaría y Elymus farctus. Tesis en opción al Grado Científico de Doctor en Ciencias. Universidad de Salamanca. España. 2009; 272 pág.

Gamboa-Gaitán MA. Hongos endófitos tropicales: Conocimiento actual y perspectivas. Acta Biológica Colombiana. 2006; 11: 3-20.

Lodge DJ. Diversidad mundial y regional de hongos. En: M. Hernández, A García, F. Álvarez y M. Ulloa (Eds.). Enfoques contemporáneos para el estudio de la biodiversidad. Ediciones Científicas Universitarias UNAM, México. 2001; 291-304 pág.

Suryanarayanan TS, Thirunavukkarasu N, Govindarajulu MB, Sasse F, Jansen R, Murali TS. Fungal endophytes and bioprospecting. Fungal Biology Reviews. 2009; 23 (1-2): 9-19.

Anteneh Ademe Mengistu. Endophytes: colonization, behaviour, and their role in defense mechanism. Hindawi International Journal of Microbiology. 2020; 1-8. Article ID 6927219, https://doi.org/10.1155/2020/6927219.

Bamisope SB, Akutse KS, Dash CK, Qasim M, Aguila LCR, Ashraf HJ, et al. Effects of seedling age on colonization patterns of Citrus limon plants by endophytic Beauveria bassiana and Metarhizium anisopliae and their influence on seedlings growth. J. Fungi. 2020; 6 (29): 2-15. doi:10.3390/jof6010029.

González Mas N. Respuesta de Aphis gossypii Glover (Homoptera: Aphididae) y sus enemigos naturales entomófagos a la colonización de plantas de melón por hongos entomopatógenos endófitos. Tesis presentada en opción al grado científico de Doctor en Ciencias. Universidad de Córdoba, Argentina. 2019. 187 págs.

Wheatley WM, Kemp HW, Simpson WR, Hume DE, Nicol HI, Kemp DR, et al. Viability of endemic endophyte (Neotyphodium lolii) and perennial ryegrass (Lolium perenne) seed at retail and wholesale outlets in south-eastern Australia. Seed Science and Technology. 2007; 35: 360-370. https://doi.org/10.15258/sst.2007.35.2.11.

Eaton CJ, Cox MP, Scott B. What triggers grass endophytes to switch from mutualism to pathogenism? Plant Science. 2011; 180: 190-195.

Hamilton CE, Bauerle TL. A new currency for mutualism? Fungal endophytes alter antioxidant activity in hosts responding to drought. Fungal Diversity. 2012; 54: 39-49.

Ueno AC. Cambios mediados por el ozono sobre la simbiosis entre pastos y hongos endófitos de transmisión vertical. Tesis presentada en opción del Grado Científico de Doctor en Ciencias. Universidad de Buenos Aires, Área Ciencias Agropecuarias. Facultad de Agronomía, Universidad de Buenos Aires. 2012;195 págs.

Spiridon M, Eliopoulos PA. Endophytic entomopathogenic fungi: A valuable biological control tool against plant pests. Appl. Sci. 2020; 10 (360): 1-13. doi:10.3390/app10010360.

Ramesh Maheshwari. What is an endophytic fungus? Current Science. 2006; 90 (10): 1309.

Syed Baker, Satish S. Endophytes: Natural Warehouse of Bioactive Compounds. Drug Invention Today. 2012; 4 (11): 548-553.

Tayung K, Jha DK. Endophytic fungi as potential sources of bioactive natural products: prospects and challenges. Rev. Plant Pathol. 2014; 6: 299-334. r

Shashank AT, Rakesh Kumar KL, Ramakrishna D, Kiran S, Kosturkova G, Gokare RA. Current Understanding of Endophytes: Their Relevance, Importance, and Industrial Potentials. IOSR Journal of Biotechnology and Biochemistry (IOSR-JBB). 2017; 3: 43-59. ISSN: 2455-264X

VanderMolen KM, Raja HA, El-Elimat T, Oberlies NH. Evaluation of culture media for the production of secondary metabolites in a natural products screening program. AMB Express. 2013; 3: 71.Disponible en: http://www.amb-express.com/content/3/1/71. Consultado: 1/8/2021

Infante D, Martínez B, González N, Reyes Y. Mecanismos de acción de Trichoderma frente a hongos fitopatógenos. Rev Protección Veg. 2009; 24 (1): 14-21.

Kaul S, Sharma T, Dhar MK. “Omics” tools for better understanding the plant–endophyte interactions. Front. Plant Sci. 2016; 7: 955. doi: 10.3389/fpls.2016.00955.

Ayomide Emmanuel Fadiji, Oluranti OB. Metagenomics methods for the study of plant-associated microbial communities: A review. Journal of Microbiological Methods. 2020; 170: 105860.

Souvik Kusari, Hertweck C, Spiteller M. Chemical Ecology of Endophytic Fungi: Origins of Secondary Metabolites. Chemistry & Biology. 2012; 19 (7): 792-798.

Hardoim PR, van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A, et al. The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev. 2015. doi:10.1128/MMBR.00050-14.

Muhammad Waqas, Khan AL, Kamran M, Hamayun M, Kang S-M, Kim Y-H, et al. Endophytic fungi produce gibberellins and indoleacetic acid and promotes host-plant growth during stress. Molecules. 2012; 17: 10754-10773. doi:10.3390/molecules170910754.

Chiang YM, Lee KH, Sanchez JF, Keller NP, Wang CC. Unlocking fungal cryptic natural products. Natural Product Communications. 2009; 4 (11): 1505-1510.

Bertrand S, Schumpp O, Bohni N, Monod M, Gindro K, Wolfender JL. De novo production of metabolites by fungal co-culture of Trichophyton rubrum and Bionectria ochro/euca. Journal of Natural Products. 2013; 76 (6): 1157-65.

Raya-Díaz S, Quesada-Moraga E, Barrón V, del Campillo MC, Sánchez-Rodríguez AR. Redefining the dose of the entomopathogenic fungus Metarhizium brunneum (Ascomycota: Hypocreales) to increase Fe bioavailability and promote plant growth in calcareous and sandy soils. Plant and Soil. 2017a; 418: 387-404, doi:10.1007/s11104-017-3303-0.

Raya-Díaz S, Sánchez-Rodríguez AR, Segura-Fernández JM, del Campillo M C, Quesada-Moraga E. Entomopathogenic fungi-based mechanisms for improved Fe nutrition in sorghum plants grown on calcareous substrates. PLoS ONE. 2017b 12: (e0185903). doi: 10.1371/journal.pone.0185903.

Barra-Bucarei L, González MG, Iglesias AF, Aguayo GS, Peñalosa MG, Vera PV. Beauveria bassiana multifunction as an endophyte: growth promotion and biologic control of Trialeurodes vaporariorum, (Westwood) (Hemiptera: Aleyrodidae) in Tomato. Insects. 2020; 11: 591; doi:10.3390/insects11090591.

Hamilton CE, Gundel PE, Helander M, Saikkonen K. Endophytic mediation of reactive oxygen species and antioxidant activity in plants: A review. Fungal Diversity. 2012; 54, 1-10.

Santos Cruz J, da Silva CA, Hamerski L. Natural products from endophytic fungi associated with Rubiaceae species. J. Fungi. 2020; 6, 128. doi:10.3390/jof6030128.

Gaurav Kumar, Chandra P, Choudhary M. Endophytic fungi: a potential source of bioactive compounds. Chem Sci Rev Lett. 2017; 6 (24): 2373-2381.

Shukla ST, Habbu PV, Kulkarni VH, Jagadish KS, Pandey AR, Sutariya VN. Endophytic microbes: A novel source for biologically/pharmacologically active secondary metabolites. Asian Journal of Pharmacology and Toxicology. 2014; 2 (3): 01-16.

Mahendra Rai, Rathod D, Agarkar G, Dar M, Brestic M, Pastore GM, et al. Fungal growth promotor endophytes: a pragmatic approach towards sustainable food and agriculture. Symbiosis. 2014. DOI 10.1007/s13199-014-0273-3.

HEmmanuel Ortiz-Espinoza, Villegas-Rodríguez F, Ramírez-Tobías HM, Hernández-Arteaga LE, Marín-Sánchez J. La inoculación con hongos endófitos entomopatógenos en semilla genera una respuesta fisiológica y promueve el crecimiento vegetal en plantas de chile poblano en invernadero. Nova Scientia. 2020; 12 (2): 1-27. doi.org/10.21640/ns.v12i25.2586.

González-Marquetti I, Infante-Martínez D, Arias-Vargas Y, Gorrita-Ramírez S, Hernández-García T, de la Noval-Pons BM, et al. Efecto de Trichoderma asperellum Samuels, Lieckfeldt & Nirenberg sobre indicadores de crecimiento y desarrollo de Phaseolus vulgaris L. cultivar BAT-304. Rev. Protección Veg. 2019;34(2) Epub 27-Ago- versión impresa ISSN 1010-2752versión On-line ISSN 2224-4697

Arévalo-Ortega J, Hernández Socorro MA, Lamz Piedra A, Montes de Oca N, Hidalgo-Díaz L. Efecto de Pochonia chlamydosporia var. catenulata (Goddard) Zare y Gams como endófito facultativo en frijol (Phaseolus vulgaris L.). Rev. Protección Veg. 2019; 34(2), mayo-agosto, ISSN: 2224-4697

Hernández Socorro MA, Arévalo Ortega J, Marrero Roque D, Hidalgo Díaz L. Efecto de Klamic® en la estimulación del crecimiento de vitroplantas de plátanos y bananos Cultivos Tropicales. 2016; 37(4): 168-172.

Arévalo Ortega J, Hernández Socorro MA, Alfonso de la Cruz R, Montes de Oca Martínez N, Hidalgo-Díaz L. Validación de Pochonia chlamydosporia (Goddard) y Gams en el manejo agronómico de vitroplantas Musa paradisiaca L. en fase de adaptación ex vitro. Rev. Protección Veg. 2020; 35(2).

Bamisile BS, Dash CK, Akutse KS, Keppanan R and Wang L. Fungal Endophytes: Beyond Herbivore Management. Front. Microbiol. 2018; 9: 544. doi: 10.3389/fmicb.2018.00544.

Hidalgo-Díaz L, CeiroW. Interacción entre Pochonia chlamydosporia var. catenulata (Kamyschko ex Barron y Onions) Zare y Gams y Meloidogyne incognita (Kofoid y White) Chitwood en tomate en presencia de NaCl. Rev. Protección Veg. 2017; 32(1):76-81.

Saikkonen K, Gundel P, Helander M. Chemical ecology mediated by fungal endophytes in grasses. Journal of Chemical Ecology. 2013; 39: 962–968.

Spiering MJ, Moon CD, Wilkinson HH, Schardl CL. Gene clusters for insecticidal loline alkaloids in the grass-endophytic fungus Neotyphodium uncinatum. Genetics. 2005; 169: 1403-1414.

Rasmussen S, Parsons AJ, Bassett S, Christensen MJ, Hume DE, Johnson LJ, et al. High nitrogen supply and carbohydrate content reduce fungal endophyte and alkaloid concentration in Lolium perenne. New Phytologist. 2007; 173: 787-797.

Zhang D-X, Nagabhyru P, Schardl CL. Regulation of a chemical defense against herbivory produced by symbiotic fungi in grass plants. Plant Physiology. 2009; 150: 1072–1082.

Poveda J, Abril-Urias P, Escobar C. Biological control of plant-parasitic nematodes by filamentous fungi inducers of resistance: Trichoderma, mycorrhizal and endophytic fungi. Front. Microbiol. 2020; 11: 992. doi: 10.3389/fmicb.2020.00992.

Bastías Campos DA. Mecanismos de resistencia a insectos en pastos que forman simbiosis con hongos endófitos. Tesis presentada en opción al Grado Científico de Doctor en Ciencias. Universidad de Buenos Aires, Área Ciencias Agropecuarias. 2018. 96 págs.

González-Mas N, Sánchez-Ortiz A, Valverde-García P, Quesada-Moraga E. Effects of endophytic entomopathogenic ascomycetes on the life-history traits of Aphis gossypii Glover and its interactions with melon Plants. Insects. 2019; 10: 165; doi:10.3390/insects10060165.

Pocurull M, Fullana AM, Ferro M, Valero P, Escudero N, Saus E, et al. Commercial formulates of Trichoderma induce systemic plant resistance to Meloidogyne incognita in tomato and the effect is additive to that of the Mi-1.2 resistance gene. Front. Microbiol. 2020; 10: 3042. doi: 10.3389/fmicb.2019.03042.

Hernández-Ochandía D, Rodríguez MG, Peteira P, Miranda I, Arias Y, Martínez B. Efecto de cepas de Trichoderma asperellum Samuels, Lieckfeldt y Nirenberg sobre el desarrollo del tomate y Meloidogyne incognita (Kofoid Y White) Chitwood. Rev. Protección Veg. 2015; 30(2):139-147.

Miranda Cabrera I, Hernández-Ochandía D, Hernández del Amo Y, Martínez Coca B, Rodríguez Hernández MG. Modelación de la interacción Meloidogyne incognita (Kofoid y White) Chitwood- Trichoderma asperellum Samuels, Lieckfeldt & Nirenberg en garbanzo (Cicer arietinum L.). Rev. Protección Veg. 2016; 31(3):194-200.

Simon Kiarie, Johnson ON, Gohole LS., Maniania NK, Subramanian S. Impact of fungal endophyte colonization of maize (Zea mays L.) on induced resistance to thrips- and aphid-transmitted viruses. Plants. 2020; 9: 416. doi:10.3390/plants9040416.

González‑Mas N, Cuenca‑Medina M, Gutierrez‑Sanchez F, Quesada‑Moraga E. 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. 2019. https://doi.org/10.1007/s10340-019-01098-5.

Muvea AM, Subramanian S, Maniania NK, Poehling H-M, Ekesi S, Meyhöfer R Endophytic colonization of onions induces resistance against viruliferous thrips and virus replication. Front. Plant Sci. 2018; 9: 1785. doi: 10.3389/fpls.2018.01785.

Sikora RA. Management of the antagonistic potential in agricultural ecosystems for biological control of plant parasitic nematodes. Phytopathology. 1992; 30: 245-270.

Zum Felde A. Studies on characteristics of the antogonistic relationship between Radopholus similis (Cobb) Thorne and the mutualistic endophytic fungi in Nematode Supressive Banana Plants (Musa AAA). Tesis en opción al Grado Científico de Doctro en Ciencias. Alemania Universidad de Bonn. 2008. 93p.

Chaves N. Utilización de bacterias y hongos endofíticos para el control biológico del Nematodo Barrenador Radopholus similis (Cobb) Thorn. Tesis en Opción al Grado Científico de Master en Ciencias. Turrialba, CR. CATIE. 2007. 85p.

Pocasangre LE, zum Felde A, Cañizares C, Riveros AS, Rosales FE, Sikora R. Manejo alternativo de fitonematodos en banano y plátano. In Memorias, XVI reunión internacional de ACORBAT, Oaxaca, MX. 2004. 106-112 págs.

Waqas Wakil, Tahir M, Al-Sadi AM, Shapiro-Ilan D. Interactions between two invertebrate pathogens: an endophytic fungus and an externally applied bacterium. Microbiol. 2020. doi.org/10.3389/fmicb.2020.522368.

Bamisope SB, Dash CK, Akutse KS, Qasim M, Aguila LCR, Wang F, et al. Endophytic Beauveria bassiana in foliar-treated citrus limon plants acting as a growth suppressor to three successive generations of Diaphorina citri Kuwayama (Hemiptera: Liviidae). Insects. 2019; 10 (176): 1-15. doi:10.3390/insects10060176.

Arévalo J, Martínez B, Hernández MA, Alfonso R, Ynfante D, Hidalgo-Díaz L. Efecto de la aplicación conjunta de P. chlamydosporia (Goddard) Zare y Gams y T. asperellum Samuels, Lieckfeldt y Nirenberg en vitroplantas de banano (Musa sp.). Rev. Protección Veg. 2021; 36(1). E-ISSN: 2224-4697

Pell JK, Vandenberg JD. Interactions among the aphid Diuraphis noxia, the entomopathogenic fungus Paecilomyces fumosoroseus and the coccinellid Hippodamia convergens. Biocontrol Sci Techn. 2002; 12: 217-224.

Roy HE, Brown P, Rothery P, Ware RL, Majerus MEN. Interactions between the fungal pathogen Beauveria bassiana and three species of coccinellid: Harmonia axyridis, Coccinella septempunctata and Adalia bipunctata. Biocontrol. 2008; 53:265-276.

Portilla M, Snodgrass G, Luttrell R. Lethal and sub-lethal effects of Beauveria bassiana (Cordycipitaceae) strain NI8 on Chrysoperla rufilabris (Neuroptera: Chrysopidae). Florida Entomologist. 2017;100 (3):627-633.

Oreste M, Bubici G, Poliseno M, Tarasco E. Effect of Beauveria bassiana and Metarhizium anisopliae on the Trialeurodes vaporariorum - Encarsia formosa system. J Pest Sci. 2016; 89:153-160. doi:10.1007/s10340-015-0660-4.

Shrestha G, Enkegaard A, Reddy GVP, Skovgard H, Steenberg T. Susceptibility of larvae and pupae of the aphid parasitoid Aphelinus ribisnigri ribisnigri (Hymenoptera: Aphelinidae) to the entomopathogenic fungus Beauveria bassiana. Annals of the Entomological Society of America. 2017; 110 (1):121-127. doi: 10.1093/aesa/saw066.

Ríos-Moreno A, Quesada-Moraga E, Garrido-Jurado I. Treatments with Metarhizium brunneum BIPESCO5 and EAMa 01/58-Su strains (Ascomycota: Hypocreales) are low risk for the generalist predator Chrysoperla carnea. J Pest Sci 2018; 91:385-394.

González-Mas N, Cuenca-Medina M, Gutiérrez-Sánchez F, Quesada- Moraga E. 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. 2019. doi.org/10.1007/s10340-019-01098-5.

Zum Felde A, Pocasangre LE, Carñizares Monteros CA, Sikora RA, Rosales FE, Riveros AS. Effect of combined inoculations of endophytic fungi on the biocontrol of Radopholus similis. Info Musa. 2006; 15 (1-2).

Castro López MA, Martínez Osorio JW. Compatibility of Beauveria bassiana and Metarhizium anisopliae with Chrysoperla externa depredator of Trialeurodes vaporariorum. Chilean J. Agric. Anim. Sci., ex Agro-Ciencia. 2019; 35 (1): 38-48.

Canassa F, Tall S, Moral RA, de Lara IAR, Delalibera Jr.I, Meyling NV. Effects of bean seed treatment by the entomopathogenic fungi Metarhizium robertsii and Beauveria bassiana on plant growth, spider mite populations and behavior of predatory mites. Biological Control. 2019; 132: 199-208.

Scorsetti AC, Pelizza S, Fogel MN, Vianna F, Schneider MI. Interactions between the entomopathogenic fungus Beauveria bassiana and the Neotropical predator Eriopis connexa (Coleoptera: Coccinellidae): Implications in biological control of pest. Journal of Plant Protection Research. 2017; 57 (4): 389-395. doi: 10.1515/jppr-2017-0053.

Martin Heil. The Microbe-Free Plant: Fact or Artifact. Cap. 114. En: Biological Nitrogen Fixation, Volume 2, First Edition. Edited by Frans J. de Bruijn. Published 2015 by John Wiley & Sons, Inc. 2015: 1163-1174.

Sinno M, Ranesi M, Gioia L, d’Errico G, Woo SL. Endophytic fungi of tomato and their potential applications for crop improvement. Agriculture. 2020; 10(587): 1-. 20. doi:10.3390/agriculture10120587.

Abello JF, Kelemu S. Hongos endófitos: ventajas adaptativas que habitan en el interior de las plantas. Revista Corpoica – Ciencia y Tecnología Agropecuaria. 2006; 7 (2):55-57.

Most read articles by the same author(s)

> >>