Avances recientes y perspectivas científicas y tecnológicas del biocontrol ejercido por Trichoderma spp.
Palabras clave:
Hongos, Mecanismos, Control, Fermentación, EnzimasResumen
En la actualidad, la agricultura depende en gran medida del uso de productos químicos sintéticos para controlar los microorganismos fitopatógenos que provocan grandes pérdidas en los cultivos. Una alternativa promisoria para remplazar el uso de estos productos es la implementación de agentes de control biológico, tal es el caso de los hongos filamentosos pertenecientes al género Trichoderma. Estos microorganismos poseen diversos mecanismos para su supervivencia y proliferación incluyendo el micoparasitismo de hongos fitopatógenos, así como también la utilización de sustratos complejos y diversos. Estos atributos son de gran importancia económica puesto que conducen a la oportunidad de ser usados en la producción de metabolitos de interés para control biológico de fitopatógenos bajo el esquema de procesos inductivos, además de ser características susceptibles al mejoramiento genético para potencializar sus mecanismos de control como lo es la producción de enzimas.
Referencias
Agrios, GN. (2006). Enfermedades de las plantas causadas por hongos. Pp:273-530. In: Grupo Noriega (eds.). Fitopatología. Editorial Limusa S.A. De C.V., 1995. México. 838 p.
Anees, M., Tronsmo, A., Edel-Hermann, V. y col. (2010). Characterization of field isolates of Trichoderma antagonistic against Rhizoctonia solani. Fungal Biology, 114:691-701. https://doi.org/10.1016/j.funbio.2010.05.007
Arauz, L.F. (1998). Hongos fitopatógenos. Pp:105-136. In: Carazo G, Murillo M, Fernández G, Brenes S, Ramírez L, Araya C (eds.). Fitopatología Un Enfoque Agroecológico. Editorial de la Universidad de Costa Rica. Costa Rica. 471p.
Babbal, A., Khasa, Y.P. (2017). Microbes as biocontrol agents. Pp:507-552. In: Kumar V, Kumar M, Sharma S, Prasad R (eds.). Probiotics and Plant Health. Springer Singapore. Singapore. 600p. https://doi.org/10.1007/978-981-10-3473-2_24
Bai, Z., Jin, B., Li, Y. y col. (2008). Utilization of winery wastes for Trichoderma viride biocontrol agent production by solid state fermentation. Journal of Environmental Sciences, 20:353-358. https://doi.org/10.1016/S1001-0742(08)60055-8
Ben Taher, I., Bennour, H., Fickers, P. y col. (2017). Valorization of potato peels residues on cellulase production using a mixed culture of Aspergillus niger ATCC 16404 and Trichoderma reesei DSMZ 970. Waste and Biomass Valorization, 8:183-192. https://doi.org/10.1007/s12649-016-9558-5
Buenrostro-Figueroa, J., de la Garza-Toledo, H., Ibarra-Junquera, V. y col. (2010). Juice extraction from mango pulp using an enzymatic complex of Trichoderma sp. produced by solid-state fermentation. Food Science and Biotechnology, 19:1387-1390. https://doi.org/10.1007/s10068-010-0197-5
Burmeister, L., Hau, B. (2009). Control of the bean rust fungus Uromyces appendiculatus by means of Trichoderma harzianum: leaf disc assays on the antibiotic effect of spore suspensions and culture filtrates. BioControl, 54:575–585. https://doi.org/10.1007/s10526-008-9202-9
Capucho, A.S., Zambolim, E.M., Freitas, R.L. y col. (2012). Identification of race XXXIII of Hemileia vastatrix on Coffea arabica catimor derivatives in Brazil. Australasian Plant Disease Notes, 7:189-191. https://doi.org/10.1007/s13314-012-0081-7
Contreras-Cornejo, H.A., Macías-Rodríguez, L., Herrera-Estrella, A. y col. (2014). The 4-phosphopantetheinyl transferase of Trichoderma virens plays a role in plant protection against Botrytis cinerea through volatile organic compound emission. Plant and Soil, 379:261-274. https://doi.org/10. 1007/s11104-014-2069-x
Coradi, G.V., da Visitação, V.L., de Lima, E.A. y col. (2013). Comparing submerged and solid-state fermentation of agro-industrial residues for the production and characterization of lipase by Trichoderma harzianum. Annals of Microbiology, 63:533-540. https://doi.org/10.1007/s13213-012-0500-1
De la Cruz-Quiroz, R., Robledo-Padilla, F., Aguilar, C.N. y col. (2017). Forced aeration influence on the production of spores by Trichoderma strains. Waste and Biomass Valorization, 8:2263-2270. https://doi.org/10.1007/ s12649-017-0045-4
De la Cruz-Quiroz, R., Roussos, S., Hernández-Castillo, D. y col. (2015). Challenges and opportunities of the bio-pesticides production by solid-state fermentation: filamentous fungi as a model. Critical Reviews in Biotechnology, 35:326-333. http://dx.doi.org/10.3109/07388551.2013.857292
De la Cruz-Quiroz, R., Roussos, S., Hernandez-Castillo, D. y col. 2017. Solid-state fermentation in a bag bioreactor: effect of corn cob mixed with phytopathogen biomass on spore and cellulase production by Trichoderma asperellum. Pp:43-56. In: Jozala AF (ed.). Fermentation Processes. InTech. 310 p. http://dx.doi.org/10.5772/64643
De los Santos-Villalobos, S., Guzmán-Ortiz, D.A., Gómez-Lim. M.A., y col. (2013). Potential use of Trichoderma asperellum (Samuels, Liechfeldt et Nirenberg) T8a as a biological control agent against anthracnose in mango (Mangifera indica L.). Biological Control, 64:37-44. https://doi.org/10.1016/j.biocontrol .2012.10.006
De Souza, J.T., Trocoli, R.O., Monteiro, F.P. (2016). Plants from the Caatinga biome harbor endophytic Trichoderma species active in the biocontrol of pineapple fusariosis. Biological Control, 94:25-32. https://doi.org/10.1016/j.biocontro l.2015.12.005
Deng, S., Lorito, M., Penttilä, M. y col. (2007). Overexpression of an endochitinase gene (ThEn-42) in Trichoderma atroviride for increased production of antifungal enzymes and enhanced antagonist action against pathogenic fungi. Applied Biochemistry and Biotechnology, 142:81-94. https://doi .org/10.1007/s12010-007-0012-9
Dik, A., Elad, Y. (1999). Comparison of antagonists of Botrytis cinerea in greenhouse-grown cucumber and tomato under different climatic conditions. European Journal of Plant Pathology, 105:123-137 https://doi.org/10.1023/A:1008778213278
Feofilova, E.P. (2010). The fungal cell wall: modern concepts of its composition and biological function. Microbiology, 79:711-720. https://doi.org/10. 1134/S0026261710060019
Ferrigo, D., Raiola, A., Rasera, R., and Causin, R. (2014). Trichoderma harzianum seed treatment controls Fusarium verticillioides colonization and fumonisin contamination in maize under field conditions. Crop Protection, 65:51-56. https://doi.org/10.1016/j.cropro.2014.06.018
Freeman, S., Minz, D., Kolesnik, I., y col. (2004). Trichoderma biocontrol of Colletotrichum acutatum and Botrytis cinerea and survival in strawberry. European Journal of Plant Pathology, 110:361-370. https://doi.org/ 10.1023/B:EJPP.0000021057.93305.d9
Freeman, S., Sztejnberg, A., Chet, I. (1986). Evaluation of Trichoderma as a biocontrol agent for Rosellinia necatrix. Plant and Soil, 94:163-170. https://doi.org/10.1007/BF02374340
Galletti, S., Burzi, P.L., Cerato, C. y col. (2008). Trichoderma as a potential biocontrol agent for Cercospora leaf spot of sugar beet. BioControl, 53:917-930. https://doi.org/10.1007/s10526-007-9113-1
Geraldine, A.M., Lopes, F.A.C., Carvalho, D.D.C. y col. (2013). Cell wall-degrading enzymes and parasitism of sclerotia are key factors on field biocontrol of white mold by Trichoderma spp. Biological Control, 67:308-316. https://doi.org/ 10.1016/j.biocontrol.2013.09.013
Grujić, M., Dojnov, B., Potočnik, I. y col. (2015). Spent mushroom compost as substrate for the production of industrially important hydrolytic enzymes by fungi Trichoderma spp. and Aspergillus niger in solid state fermentation. International Biodeterioration & Biodegradation, 104:290-298. https:// doi.org/10.1016/j.ibiod.2015.04.029
Horst, R.K. (2013). Downy mildews. Pp:181-186. In: Department of Plant Pathology and Plant-Microbe Biology, Cornell University (eds.). Westcott's Plant Disease Handbook. Springer Science+Business Media Dordrecht. 826 p. https://do i.org/10.1007/978-94-007-2141-8_27
Jeleń, H., Błaszczyk, L., Chełkowski, J. y col. (2014). Formation of 6-n-pentyl-2H-pyran-2-one (6-PAP) and other volatiles by different Trichoderma species. Mycological Progress, 13:589-600. https://doi.org/10.1007/s11557-013-0942-2
Jiang, H., Zhang, L., Zhang, J. y col. (2016). Antagonistic interaction between Trichoderma asperellum and Phytophthora capsici in vitro. Journal of Zhejiang University-SCIENCE B, 17:271-281. https://doi.org/10.1631/ jzus.B1500243
John, N.S., Anjanadevi, I.P., Nath, V.S. y col. (2015). Characterization of Trichoderma isolates against Sclerotium rolfsii, the collar rot pathogen of Amorphophallus – a polyphasic approach. Biological Control, 90:164-172. https://doi.org/10.1016/j.biocontrol.2015.07.001
Judelson, H.S. (2014). Phytophthora infestans. Pp:175-208. In: Dean R, Lichens-Park A and Kole C (eds.). Genomics of Plant-Associated Fungi and Oomycetes:Dicot Pathogens. Springer, Berlin, Heidelberg. Alemania. 239 p. https://doi.org/10.1007/978-3-662-44056-8_9
Kamala, T., Indira, S. (2011). Evaluation of indigenous Trichoderma isolates from Manipur as biocontrol agent against Pythium aphanidermatum on common beans. 3 Biotech., 1:217–225. https://doi.org/10.1007/s13205-011-0027-3
Kamle, M., Kumar, P. (2016). Colletotrichum gloeosporioides: pathogen of anthracnose disease in mango (Mangifera indica L.). Pp:207-219. In: Kumar P, Gupta V, Tiwari A, Kamle M (eds.). Current Trends in Plant Disease Diagnostics and Management Practices. Fungal Biology. Springer, Cham. 469 p. https://doi.org/10.1007/978-3-319-27312-9_9
Keswani, C., Mishra, S., Sarma, B.K. y col. (2014). Unraveling the efficient applications of secondary metabolites of various Trichoderma spp. Applied Microbiology and Biotechnology, 98:533-544. https://doi.org/10.10 07/s00253-013-5344-5
Kotasthane, A., Agrawal, T., Kushwah, R. y col. (2015). In-vitro antagonism of Trichoderma spp. against Sclerotium rolfsii and Rhizoctonia solani and their response towards growth of cucumber, bottle gourd and bitter gourd. European Journal of Plant Pathology, 141:523-543. https://doi. org/10.1007/s10658-014-0560-0
Lah, T.N.T., Norulaini, N.A.N., Shahadat, M. y col. (2016). Utilization of industrial waste for the production of cellulase by the cultivation of Trichoderma via solid state fermentation. Environmental Processes, 3:803-814. https://doi.org/10.1007/s40710-016-0185-8
Landero, V.N., Nieto, A.D., Téliz, O.D. y col. (2015). Biological control of anthracnose by postharvest application of Trichoderma spp. on maradol papaya fruit. Biological Control, 91:88-93. https://doi.org/10.1016/j.biocontrol.2015. 08.002
Li, C., Lin, F., Li, Y. y col. (2016). A β-glucosidase hyper-production Trichoderma reeseimutant reveals a potential role of cel3D in cellulase production. Microbial Cell Factories, 15:151. https://doi.org/10.1186/s12934-016-0550-3
Ma’tat’a, M., Cibulová, A., Varečka, L. y col. (2016). Plant waste residues as inducers of extracellular proteases for a deuteromycete fungus Trichoderma atroviride. Chemical Papers, 70:1039-1048. https://doi.org/10.1515/ chempap-2016-0040
Martínez-Medina, A., Del Mar, Alguacil, M., Pascual, J.A. y col. (2014). Phytohormone profiles induced by Trichoderma isolates correspond with their biocontrol and plant growth-promoting activity on melon plants. Journal of Chemical Ecology, 40:804-815. https://doi.org/10.1007/s 10886-014-0478-1
Marzano, M., Gallo, A., Altomare, C. (2013). Improvement of biocontrol efficacy of Trichoderma harzianum vs. Fusarium oxysporum f. sp. lycopersicithrough UV-induced tolerance to fusaric acid. Biological Control, 67:397-408. https://doi.org/10.1016/j.biocontrol.2013.09.008
Mbarga, J.B., Begoude, B.A.D., Ambang, Z. y col. (2014). A new oil-based formulation of Trichoderma asperellum for the biological control of cacao black pod disease caused by Phytophthora megakarya. Biological Control, 77:15-22. https://doi.org/10.1016/j.biocontrol.2014.06.004
Oberoi, H.S., Babbar, N., Dhaliwal, S.S. y col. (2012). Enhanced oil recovery by pre-treatment of mustard seeds using crude enzyme extract obtained from mixed-culture solid-state fermentation of kinnow (Citrus reticulata) waste and wheat bran. Food and Bioprocess Technology, 5:759-767. https://doi.org/10.1007/s11947-010-0380-y
Pandey, V., Shukla, A., Kumar, J. (2016). Physiological and molecular signaling involved in disease management through Trichoderma: an effective biocontrol paradigm. Pp:317-346. In: Kumar P, Gupta V, Tiwari A, Kamle M. (eds). Current Trends in Plant Disease Diagnostics and Management Practices. Fungal Biology. Springer, Cham. 469 p. https://doi.org/10. 07/978-3-319-27312-9_14
Patil, A.S., Patil, S.R., Paikrao, H.M. (2016). Trichoderma secondary metabolites: their biochemistry and possible role in disease management. Pp:69-102. In: Choudhary D, Varma A (eds.). Microbial-mediated Induced Systemic Resistance in Plants. Springer Science+Business Media Singapore. Singapore. 226 p. https://doi.org/10.1007/978-981-10-0388-2_6
Perelló, A.E., Moreno, M.V., Mónaco, C. y col. (2009). Biological control of Septoria tritici blotch on wheat by Trichoderma spp. under field conditions in Argentina. BioControl, 54:113-122. https://doi.org/10.1 007/s10526-008-9159-8
Pitt, J.I., and Hocking, A.D. (2009). Fresh and perishable foods. Pp:383-400. In: Fungi and Food Spoilage. Springer, Boston, MA. USA. 519 p. https://doi.org/10.1007/978-0-387-92207-2_11
Qualhato, T.F., Lopes, F.A.C., Steindorff, A.S. y col. (2013). Mycoparasitism studies of Trichoderma species against three phytopathogenic fungi: evaluation of antagonism and hydrolytic enzyme production. Biotechnology Letters, 35:1461-1468. https://doi.org/10.1007/s10529-013-1225-3
Rey, M., Delgado-Jarana, J., Benítez, T. (2001). Improved antifungal activity of a mutant of Trichoderma harzianum CECT 2413 which produces more extracellular proteins. Applied Microbiology and Biotechnology, 55:604-608. https://doi.org/10.1007/s002530000551
Safari, Sinegani, A.A., Ghanbari, M., Janjan, A. (2009). Improvement of digestibility of sunflower and corn residues by some saprophytic fungi. Journal of Material Cycles and Waste Management, 11:293-298. https://doi.org/10.1007/s10163-009-0245-5
Sain, S.K., and Pandey, A.K. (2016). Evaluation of Some Trichoderma harzianum isolates for the management of soilborne diseases of brinjal and okra. Proceedings of the National Academy of Sciences, India Section B: Biological Sciences, 1:1-10. https://doi.org/10.1007/s40011-016-0824-x
Sandhya, C., Binod, P., Nampoothiri, K.M. y col. (2005). Microbial synthesis of chitinase in solid cultures and its potential as a biocontrol agent against phytopathogenic fungus Colletotrichum gloeosporioides. Applied Biochemistry and Biotechnology, 127:1-15. https://doi.org/10.1385/A BAB:127:1:001
Sanzani, S.M., Reverberi, M., Geisen, R. (2016). Mycotoxins in harvested fruits and vegetables: insights in producing fungi, biological role, conducive conditions, and tools to manage postharvest contamination. Postharvest Biology and Technology, 122:95-105. https://doi.org/10.1016/j.postharvbio.2016.07. 003
Sempere, F., Santamarina, M.P. (2007). In vitro biocontrol analysis of Alternaria alternata (Fr.) Keissler under different environmental conditions. Mycopathologia, 163:183-190. https://doi.org/10.1007/s11046-007-0101-x
Sriwati, R., Melnick, R.L., Muarif, R. y col. (2015). Trichoderma from Aceh Sumatra reduce Phytophthora lesions on pods and cacao seedlings. Biological Control, 89:33-41. https://doi.org/10.1016/j.biocontrol.2015.04.018
Szabo, L.J., Cuomo, C.A., Park, R.F. (2014). Puccinia graminis. Pp:177-196. In: Dean R, Lichens-Park A, Kole C (eds.). Genomics of Plant-Associated Fungi: Monocot Pathogens. Springer-Verlag Berlin Heidelberg. Alemania. 201 p. https://doi.org/10.1007/978-3-662-44053-7_8
Toghueo, R.K., Eke, P., Zabalgogeazcoa, I. y col. (2016). Biocontrol and growth enhancement potential of two endophytic Trichoderma spp. from Terminalia catappa against the causative agent of common bean root rot (Fusarium solani). Biological Control, 96:8-20. https://doi.org/10.1016/j.biocontro l.2016.01.008
Tosa, Y., Chuma, I. (2014). Classification and parasitic specialization of blast fungi. Journal of General Plant Pathology, 80:202-209. https://doi.org/10.100 7/s10327-014-0513-7
Troian, R.F., Steindorff, A.S., Ramada, M.H.S. y col. (2014). Mycoparasitism studies of Trichoderma harzianum against Sclerotinia sclerotiorum: evaluation of antagonism and expression of cell wall-degrading enzymes genes. Biotechnology Letters, 36:2095-2101. https://doi.org/10.1007/s10529-014-1583-5
Tronsmo, A., Dennis, C. (1977). The use of Trichoderma species to control strawberry fruit rots. Netherlands Journal of Plant Pathology, 83:449-455. https://doi.org/10.1007/BF03041462
Van Dam, N.M., Weinhold, A., Garbeva, P. (2016). Calling in the dark: the role of volatiles for communication in the rhizosphere. Pp:175-210. In: Blande J, Glinwood R (eds.). Deciphering Chemical Language of Plant Communication. Signaling and Communication in Plants. Springer International Publishing Switzerland. 326 p. https://doi.org/10.1007/978-3-319-33498-1_8
Viterbo, A., Ramot, O., Chernin, L. y col. (2002). Significance of lytic enzymes from Trichoderma spp. in the biocontrol of fungal plant pathogens. Antonie van Leeuwenhoek, 81:549-556. https://doi.org/10.1023/A:1020553 421740
Widmer, T.L. (2014). Screening Trichoderma species for biological control activity against Phytophthora ramorum in soil. Biological Control, 79:43-48. https://doi.org/10.1016/j.biocontrol.2014.08.003
Xie, L., Zhao, J., Wu, J. y col. (2015). Efficient hydrolysis of corncob residue through cellulolytic enzymes from Trichoderma strain G26 and L-lactic acid preparation with the hydrolysate. Bioresource Technology 193:331-336. https://doi.org/10.1016/j.biortech.2015.06.101
Yang, H.H., Yang, S.L., Peng, K.C. y col. (2009). Induced proteome of Trichoderma harzianum by Botrytis cinerea. Mycological Research 113:924-932. https://doi.org/10.1016/j.mycres.2009.04.004
Yang, L., Yang, Q., Sun, K. y col. (2010). Agrobacteriumtumefaciens-mediated transformation of SOD gene to Trichoderma harzianum. World Journal of Microbiology and Biotechnology, 26:353-358. https://doi.org/10.1 007/s11274-009-0182-4
Yang, L., Yang, Q., Sun, K. y col. (2011). Agrobacterium tumefaciens mediated transformation of ChiV gene to Trichoderma harzianum. Applied Biochemistry and Biotechnology, 163:937-945. https://doi.org/10.10 07/s12010-010-9097-7
Zhang, X., Li, X., Xia, L. (2015). Heterologous expression of an alkali and thermotolerant lipase from Talaromyces thermophilus in Trichoderma reesei. Applied Biochemistry and Biotechnology, 176:1722-1735. https://doi.org/10.1007/s12010-015-1673-4
