NATIVE Trichoderma STRAINS FOR THE CONTROL OF GREY MOULD (Botrytis cinerea Pers.) IN FRUITS AND FLOWERS OF BLUEBERRY (Vaccinium corymbosum L.)

Yasmin Carmen Arestegui Cantoral, Eryka Gaslac Zumaeta, Betsabe Leon Ttacca

Abstract


Background. Gray mold disease caused by Botrytis cinerea Pers. is a phytosanitary problem in blueberry (Vaccinium corymbosum L.). It is characterized for affecting soft tissues (flowers and fruits) in the field and in the post-harvest stage, reducing crop yield. This has motivated to the search for native strains of Trichoderma that are effective in biological control. Objective. To determine the effect of 19 native Trichoderma strains on the control of gray mold on flowers and fruits of blueberry under laboratory conditions. Methodology. Under a complete randomized experimental design, mycoparasitism and antibiosis tests were carried out to evaluate colonization and mycelial inhibition of the pathogen, respectively, using the dual confrontation method and production of secondary metabolites. For the bioassays, a suspension of 1×106 conidia mL-1 per strain was sprayed on blueberry flowers and fruits. Disease incidence and severity were evaluated. Data were analyzed with the statistical program InfoStat. Results. All Trichoderma strains completely colonized the pathogen, being considered as aggressive mycoparasites and inhibited the mycelial growth of the pathogen up to 42.74%. Likewise, the application of Trichoderma spore suspension had inhibitory effects on gray mold, highlighting the strain HE- ArT161 that reduced the incidence (66.67% and 20%) and severity (34% and 12%), respectively in flowers and fruits. Implications. The use of these native strains of Trichoderma may contribute to future research in the field where they can be incorporated for an integrated management of the disease. Conclusion. These Trichoderma isolates against B. cinerea showed in vitro control, stimulating mycelial inhibition of the pathogen and reducing the development of disease lesions.

Keywords


Antibiosis; biocontrol; mycelial growth; mycoparasitism; pathogen.

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References


Agraria., 2022. Botrytis cinerea; la prevención es la clave del éxito. https://agraria.pe/noticias/botrytis-cinerea-la-prevencion-es-la-clave-del-exito-27734 (17 de diciembre 2023).

Asad, S.A., 2022. Mechanisms of action and biocontrol potential of Trichoderma against fungal plant diseases - A review. Ecological Complexity, 49, p.100978. https://doi.org/10.1016/J.ECOCOM.2021.100978

Bae, S.J., Mohanta, T.K., Chung, J.Y., Ryu, M., Park, G., Shim, S., Hong, S.B., Seo, H., Bae, D. W., Bae, I., Kim, J.J. and Bae, H., 2016. Trichoderma metabolites as biological control agents against Phytophthora pathogens. Biological Control, 92, pp. 128–138. https://doi.org/10.1016/j.biocontrol.2015.10.005

Bailey, B.A., Bae, H., Strem, M.D., Crozier, J., Thomas, S.E., Samuels, G.J., Vinyard, B.T. and Holmes, K.A., 2008. Antibiosis, mycoparasitism, and colonization success for endophytic Trichoderma isolates with biological control potential in Theobroma cacao. Biological Control, 46(1), pp. 24–35. https://doi.org/10.1016/j.biocontrol.2008.01.003

Baiyee, B., Pornsuriya, C., Ito, S. ichi and Sunpapao, A., 2019. Trichoderma spirale T76-1 displays biocontrol activity against leaf spot on lettuce (Lactuca sativa L.) caused by Corynespora cassiicola or Curvularia aeria. Biological Control, 129, pp. 195–200. https://doi.org/10.1016/j.biocontrol.2018.10.018

Barakat, R.M. and Al Masri, M.I., 2017. Effect of Trichoderma harzianum in combination with fungicides in controlling gray mould disease (Botrytis cinerea) of strawberry. American Journal of Plant Sciences, 8(4), pp. 651–665. https://doi.org/10.4236/ajps.2017.84045

Bello, F., Montironi, I.D., Medina, M.B., Munitz, M.S., Ferreira, F.V., Williman, C., Vázquez, D., Cariddi, L.N. and Musumeci, M.A., 2022. Mycofumigation of postharvest blueberries with volatile compounds from Trichoderma atroviride IC-11 is a promising tool to control rots caused by Botrytis cinerea. Food Microbiology, 106, pp. 1–14. https://doi.org/10.1016/j.fm.2022.104040

Contreras, H., Macías, L., Larsen, J. and Del Val, E., 2016. Ecological functions of Trichoderma spp. and their secondary metabolites in the rhizosphere: interactions with plants. FEMS Microbiology Ecology, 92(4), pp. 1–17. https://doi.org/10.1093/femsec/fiw036

Contreras-Cornejo, H.A., Orozco-Granados, O., Ramírez-Ordorica, A., García-Juárez, P., López-Bucio, J. and Macías-Rodríguez, L., 2022. Light and mycelial injury influences the volatile and non-volatile metabolites and the biocontrol properties of Trichoderma atroviride. Rhizosphere, 22, p.100511. https://doi.org/10.1016/j.rhisph.2022.100511

Contreras-Cornejo, H. A., Schmoll, M., Esquivel-Ayala, B. A., González-Esquivel, C. E., Rocha-Ramírez, V. and Larsen, J., 2024. Mechanisms for plant growth promotion activated by Trichoderma in natural and managed terrestrial ecosystem. Microbiological Research, 281, p.127621. https://doi.org/10.1016/j.micres.2024.127621

Cubilla Ríos, A.A., Ruíz Díaz, D.D., Romero Rodríguez, M.C., Flores Giubi, M.E. and Barúa Chamorro, J.E., 2019. Antibiosis of proteins and metabolites of three species of Trichoderma against paraguayan isolates of Macrophomina phaseolina. Agronomy Mesoamerican, 30(1), pp. 63–77. https://doi.org/https://doi.org/10.15517 /am.v30i1.34423

Chen, J., Zi, J., Gang, X., Guo, A., Tou, S. and Zhong, J., 2021. Botrytis cinerea causing gray mold of Polygonatum sibiricum (Huang Jing) in China. Crop Protection, 140, p.105424. https://doi.org/10.1016/j.cropro.2020.105424

Díaz García, E., Valenzuela Quintana, A., Troncoso Rojas, R., Gonzalez Mendoza, D. and Tiznado Hernández, M. 2022. Metabolitos bioactivos de Trichoderma para el control de hongos postcosecha en frutas y hortalizas. In: L.C. Montoya Ballesteros, M.E. Tiznado Hernandez, T.J. Madera Santana, J.F. Ayala Zavala, G.A. González Aguilar, eds. Tecnología, Ingeniería y Biotecnología de Alimentos de Origen Vegetal: Aprovecha­miento de sus Subproductos. CDMX:LIBERMEX-CIAD. Pp. 227–243.

Di Rienzo, J.A., Casanoves, F., Balzarini, M.G., Gonzalez, L., Tablada, M. and Robledo, C.W., 2008. InfoStat software estadistico, Manual del Usuario: Vol. Grupo Infostad (1.1). Universidad Nacional de Córdoba. https://www.infostat.com.ar/index.php?mod=page&id=34

Druzhinina, I.S., Seidl-Seiboth, V., Herrera-Estrella, A., Horwitz, B.A., Kenerley, C.M., Monte, E., Mukherjee, P.K., Zeilinger, S., Grigoriev, I.V. and Kubicek, C.P., 2011. Trichoderma: the genomics of opportunistic success. Nature Reviews Microbiology, 9, pp. 749-759.

Edgar, R.C., 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32(5), p.1792. https://doi.org/10.1093/NAR/GKH340

Edquen Q., M.N., 2019. Fungosis de Arándano (Vaccinium corymbosum L.) var. Biloxi en el Distrito de Jesús - Cajamarca. Tesis de Pregrado, Universidad Nacional de Cajamarca. http://hdl.handle.net/20.500.14074/3242

Geng, L., Fu, Y., Peng, X., Yang, Z., Zhang, M., Song, Z. and Ahammed, J., 2022. Biocontrol potential of Trichoderma harzianum against Botrytis cinerea in tomato plants. Biological Control, 174, pp. 1–12. https://doi.org/10.1016/j.biocontrol.2022.105019

Ferrada, E.E., Latorre, B.A., Zoffoli, J.P. and Castillo, A., 2016. Identification and characterization of botrytis blossom blight of Japanese plums caused by Botrytis cinerea and B. prunorum sp. nov. in Chile. Phytopathology, 106(2), 155–165. https://doi.org/10.1094/PHYTO-06-15-0143-R/ASSET/IMAGES/LARGE/PHYTO-06-15-0143-R_F6.JPEG

Gómez Ramírez, H., Soberanis Ramirez, W., Tenorio Cantoral, M. and Torres Del Aguila, E., 2013. Manual de producción y uso de hongos antagonistas. Ministerio de Agricultura, Servicio Nacional de Sanidad Agraria, Dirección de Sanidad Vegetal, Perú. https://www.senasa.gob.pe/senasa/wp-content/uploads/2017/09/Manual-de-Producci%C3%83%C2%B3n-y-Uso-de-Hongos-Antagonistas.pdf

Hammad, M., Guillemette, T., Alem, M., Bastide, F. and Louanchi, M. 2021. First report of three species of Trichoderma isolated from the rhizosphere in Algeria and the high antagonistic effect of Trichoderma brevicompactum to control grey mould disease of tomato. Biological Pest Control, 31(85), pp. 2–11. https://doi.org/https://doi.org/10.1186/s41938-021-00423-4

Harman, G.E., Howell, C.R., Viterbo, A. and Chet, I., 2004. Trichoderma spp.––opportunistic avirulent plant symbionts. Nature Reviews, 2, pp. 43–56. http://doi.org/10.1038/nrmicro797

Horst, L.E., Locke, J., Krause, C.R., McMahon, R.W., Madden, L.V. and Hoitink, H.A.J., 2005. Suppression of Botrytis blight of begonia by Trichoderma hamatum 382 in peat and compost-amended potting mixes. Plant Disease, 89, pp. 1195–1200. https://doi.org/10.1094/PD-89-1195

Huaman-Pilco, A.F., Torres-de la Cruz, M., Aime, M.C., Leiva-Espinoza, S.T., Oliva-Cruz, S.M. and Díaz-Valderrama, J.R., 2023. First report of thread blight caused by Marasmius tenuissimus on cacao (Theobroma cacao) in Peru. Plant Disease, 107(1), 219. https://doi.org/10.1094/PDIS-02-22-0420-PDN

Huang, L., Liu, M.D., Hu, Y.W., Chen, L.J., Deng, Y., Gu, Y.C., Bian, Q., Le Guo, D. and Wang, G.Z., 2024. Secondary metabolites isolated from Trichoderma hamatum b-3 and their fungicidal activity. Fitoterapia, 174, p.105880. https://doi.org/10.1016/j.fitote.2024.105880

INEI (Instituto Nacional de Estadística e Informática)., 2023. Producción de arándano alcanzó 42 mil 40 toneladas en noviembre del año 2022. Nota de prensa INEI, Perú. https://m.inei.gob.pe/prensa/noticias/produccion-de-arandano-alcanzo-42-mil-40-toneladas-en-noviembre-del-ano-2022-14170/#:~:text=Durante%20noviembre%20del%20a%C3%B1o%202022,conocer%20el%20Instituto%20Nacional%20de /

Jin, X., Guo, L., Jin, B., Zhu, S., Mei, X., Wu, J. and Liu, T., 2020. Inhibitory mechanism of 6-Pentyl-2H-pyran-2-one secreted by Trichoderma atroviride T2 against Cylindrocarpon destructans. Pesticide Biochemistry and Physiology, 170, p.104683. https://doi.org/10.1016/j.pestbp.2020.104683

Kaissoumi, H.E., Berbera, F., Mouden, N., Chahdi, A., Touhami, A.O., Selmaoui, K., Benkirane, R. and Douira, A., 2024. Tomato growth promotion by Trichoderma asperellum laboratory-made bioproduct. In: Sustainable and Green Technologies for Water and Environmental Management. Cham: Springer Nature Switzerland. pp.161-171.

Khan, R.A.A., Najeeb, S., Hussain, S., Xie, B. and Li, Y., 2020. Bioactive secondary metabolites from Trichoderma spp. against phytopathogenic fungi. Microorganisms, 8(6), pp.817. https://doi.org/10.3390/microorganisms8060817

Kottb, M., Gigolashvili, T., Großkinsky, D. K. and Piechulla, B., 2015. Trichoderma volatiles effecting arabidopsis : from inhibition to protection against pytopathogenic fungi. Frontiers in Microbiology, 6(995), pp.156172. https://doi.org/10.3389/fmicb.2015.00995

Kumar, S., Stecher, G., Li, M., Knyaz, C., and Tamura, K., 2018. MEGA X: Molecular Evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35(6), pp.1547. https://doi.org/10.1093/MOLBEV/MSY096

Limdolthamand, S., Songkumarn, P., Suwannarat, S., Jantasorn, A. and Dethoup, T., 2023. Biocontrol efficacy of endophytic Trichoderma spp. in fresh and dry powder formulations in controlling northern corn leaf blight in sweet corn. Biological Control, 181, p.105217. https://doi.org/10.1016/J.biocontrol.2023.105217

Martínez, M. and Moreno, Z., 2008. Estandarización de una metodología para la evaluación de eficacia de productos para la protección de cultivo (PPC) preventivos para el control de Botrytis sp., en condiciones semicontroladas. Tesis de Postgrado, Pontificia Universidad Javanica. http://hdl.handle.net/10554/8532

Martínez Padrón, H.Y., Torres Castillo, J.A., Rodríguez Herrera, R., López Santillán, J.A., Estrada Drouaillet, B. and Osorio Hernández, E., 2018. Identification and evaluation of secondary metabolites by gas chromatography-mass spectrometry (GC-MS) in native strains of Trichoderma species. African Journal of Biotechnology, 17(37), pp. 1162–1171. https://doi.org/10.5897/ajb2018.16546

Mazzei, P., Vinale, F., Woo, S.L., Pascale, A., Lorito, M. and Piccolo, A., 2016. Metabolomics by H-HRMAS-NMR of tomato plants treated with two secondary metabolites isolated from Trichoderma. Journal Agricultural Food Chemistry, 64, pp.3538-3545. http://doi.org/10.1021/acs.jafc.6b00801

Mesa Vanegas, A.M., Calle Osorno, J. and Marín Pavas, D.A., 2020. Metabolitos secundarios en Trichoderma spp. y sus aplicaciones biotecnológicas agrícolas. Actualidades Biológicas, 41(111), pp. 32–44. https://doi.org/10.17533/udea.acbi.v41n111a02

Miller, M.A., Pfeiffer, W. and Schwartz, T., 2011. The CIPRES science gateway: A community resource for phylogenetic analyses. TG’11: Proceedings of the TeraGrid 2011 Conference: Extreme Digital Discovery, Article No. 41. https://doi.org/10.1145/2016741.2016785

MINCETUR (Ministerio de Comercio Exterior y Turismo)., 2022. El arándano se posiciona como el principal producto de agroexportación nacional en los últimos doce meses - Noticias - Ministerio de Comercio Exterior y Turismo - Plataforma del Estado Peruano. https://n9.cl/8jw6z

Naeimi, S. and Zaré, R. 2013. Evaluation of indigenous Trichoderma spp. isolates in biological control of Botrytis cinerea, the causal agent of strawberry gray mold disease. BioControl in Plant Protection, 1(2), pp. 55–74. https://doi.org/10.22092/BCPP.2013.100609

Olowe, O.M., Nicola, L., Asemoloye, M.D., Akanmu, A.O. and Babalola, O.O., 2022. Trichoderma: Potential bio-resource for the management of tomato root rot diseases in Africa. Microbiological Research, 257, p.126978. https://doi.org/10.1016/J.MICRES.2022.126978

Ortiz, M., 2019. Enfermedades y plagas ponen a prueba a los arandaneros. Redagrícola Perú. https://www.redagricola.com/pe/enfermedades-y-plagas-ponen-a-prueba-a-los-arandaneros/

Pascale, A., Vinale, F., Manganiello, G., Nigro, M., Lanzuise, S., Ruocco, M., Marra, R., Lombardi, N., Woo, S.L. and Lorito, M., 2017. Trichoderma and its secondary metabolites improve yield and quality of grapes. Crop Protection, 92, pp. 176–181. https://doi.org/10.1016/j.cropro.2016.11.010

Pereira, F.T., Oliveira, J.B. D., Muniz, P.H.P., Peixoto, G.H.S., Guimarães, R.R. and Carvalho, D.D.C., 2019. Growth promotion and productivity of lettuce using Trichoderma spp. commercial strains. Horticultura Brasileira, 37(1), pp. 69–74. https://doi.org/10.1590/S0102-053620190111

Pincay, A., Viera, W., León, A., Noboa, M., Herrera, K. and Jackson, T., 2020. Evaluación in vitro del potencial antagonista de Trichoderma sp . y hongos endófitos de mora (Rubus glaucus Benth ) para el control de Botrytis cinerea. Science and Research, 6(1), pp. 109–124. https://doi.org/https://doi.org/10.5281/zenodo.4917695

Polat, ?., Baysal, Ö., Mercati, F., Gümrükcü, E., Sülü, G., Kitapc, A., Araniti, F. and Carimi, F., 2018. Infection, genetics and evolution characterization of Botrytis cinerea isolates collected on pepper in Southern Turkey by using molecular markers, fungicide resistance genes and virulence assay. Infection, Genetics and Evolution, 60, pp. 151–159. https://doi.org/10.1016/j.meegid.2018.02.019

Quijada, A., Méndez-Cárdenas, G., Hernández-Baños, B. and Álvarez-Buylla, E., 1997. La región de los ITS del ADN ribosomal del núcleo (nrADN), fuente de caracteres moleculares en la sistemática de las gimnospermas. Botanical Sciences, 60, pp.159–168. https://doi.org/10.17129/BOTSCI.1527

Rambaut, A., 2006. FigTree. Institute of Evolutionary Biology, Univ. of Edinburgh. http://tree.bio.ed.ac.uk/software/figtree/

Ramos, S. and Guillermo, L., 2021. Main diseases in postharvest blueberries, conventional and eco-friendly control methods. A review. LWT Food Science and Technology, 149, pp. 7–12. https://doi.org/10.1016/j.lwt.2021.112046

Rajani, P., Rajasekaran, C., Vasanthakumari, M.M., Olsson, S.B., Ravikanth, G. and Shaanker, R.U., 2021. Inhibition of plant pathogenic fungi by endophytic Trichoderma spp . through mycoparasitism and volatile organic compounds. Microbiological Research, 242, pp. 1–12. https://doi.org/10.1016/j.micres.2020.126595

Saito, S., Michailides, T.J. and Xiao, C.L. 2014. First report of Botrytis pseudocinerea causing gray mold on blueberry in North America. Plant Disease, 98(12), p.1743. https://doi.org/10.1094/PDIS-06-14-0573-PDN

Sridharan, A.P., Thankappan, S., Karthikeyan, G. and Uthandi, S., 2020. Comprehensive profiling of the VOCs of Trichoderma longibrachiatum EF5 while interacting with Sclerotium rolfsii and Macrophomina phaseolina. Microbiological Research, 236, pp. 1–13. https://doi.org/10.1016/j.micres.2020.126436

Stamatakis, A., 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30(9), p.1312. https://doi.org/10.1093/BIOINFORMATICS/BTU033

Stoppacher, N., Kluger, B., Zeilinger, S., Krska, R. and Schuhmacher, R., 2010. Identification and profiling of volatile metabolites of the biocontrol fungus Trichoderma atroviride by HS-SPME-GCMS. Journal of Microbiological Methods, 81(2), pp. 187-193. https://doi.org/10.1016/j.mimet.2010.03.011

Toome, M., Aime, C.M. and Roberson, R.W., 2013. Meredithblackwellia eburnea gen. et sp. nov., Kriegeriaceae fam. nov. and Kriegeriales ord. nov.—toward resolving higher-level classification in Microbotryomycetes. Mycologia, 105(2), p. 486–495. https://doi.org/10.3852/12-251

Vargas, A., Mukherjee, P.K., Laughlin, D., Wiest, A., Moran-Diez, M.E. and Kenerley, C.M., 2014. Role of gliotoxin in the symbiotic and pathogenic interactions of Trichoderma virens. Microbiology, 160, pp. 2319-2330. https://doi.org/10.1099/mic.0.079210-0

Xiao-Yan, Qing-Tao, S., Shu-Tao, X., Xiu-Lan, C., Cai-Yun, S. and Yu-Zhong, Z., 2006. Broad-spectrum antimicrobial activity and high stability of Trichokonins from Trichoderma koningii SMF2 against plant pathogens. FEMS Microbiology Letters, 260, pp. 119-125. https://doi.org/10.1111/j.1574-6968.2006.00316.x

Yedidia, I., Shoresh, M., Kerem, Z., Benhamou, N., Kapulnik, Y. and Chet, I., 2003. Concomitant induction of systemic resistance to Pseudomonas syringae pv. Lachrymans in cucumber by Trichoderma asperellum (T-203) and accumulation of phytoalexins. Applied and Environmental Microbiology, 69, pp. 7342–7353. https://doi.org/10.1128/AEM.69.12.7343-7353.2003

Zeilinger, S., Gruber, S., Bansal, R. and Mukherjee, P.K., 2016. Secondary metabolism in Trichoderma e Chemistry meets genomics. Fungal Biology Reviews, 30(2), pp. 74–90. https://doi.org/10.1016/j.fbr.2016.05.001

Zhang, S., Xu, B., Zhang, J. and Gan, Y., 2018. Identification of the antifungal activity of Trichoderma longibrachiatum T6 and assessment of bioactive substances in controlling phytopathgens. Pesticide Biochemistry and Physiology, 147, pp. 59–66. https://doi.org/10.1016/j.pestbp.2018.02.006

Zhang, J., Yang, H., Yu, Q.Y., Wu, M.D., Yang, L., Zhuang, W.Y., Chen, W.D. and Li, G.Q., 2016. Botrytis pyriformis sp. nov., a novel and likely saprophytic species of Botrytis. Mycologia, 108(4), 682–696. https://doi.org/10.3852/15-340




URN: http://www.revista.ccba.uady.mx/urn:ISSN:1870-0462-tsaes.v27i3.50724

DOI: http://dx.doi.org/10.56369/tsaes.5072



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