Trichoderma asperellum as a preventive and curative agent to control Fusarium wilt in Stevia rebaudiana
Stevia has been introduced in many countries for the production of sugar-free sweeteners. Concurrently, several emerging pathogens have been described in this plant host. One of the latest has been Fusarium oxysporum, a well-known soil-borne pathogen causing vascular wilt in many plants. Classical m...
- Autores:
- Tipo de recurso:
- Fecha de publicación:
- 2021
- Institución:
- Universidad de Medellín
- Repositorio:
- Repositorio UDEM
- Idioma:
- eng
- OAI Identifier:
- oai:repository.udem.edu.co:11407/5900
- Acceso en línea:
- http://hdl.handle.net/11407/5900
- Palabra clave:
- Antagonism
Biological control
Fusarium oxysporum
Mycoparasitism
Trichoderma asperellum
- Rights
- License
- http://purl.org/coar/access_right/c_16ec
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dc.title.none.fl_str_mv |
Trichoderma asperellum as a preventive and curative agent to control Fusarium wilt in Stevia rebaudiana |
title |
Trichoderma asperellum as a preventive and curative agent to control Fusarium wilt in Stevia rebaudiana |
spellingShingle |
Trichoderma asperellum as a preventive and curative agent to control Fusarium wilt in Stevia rebaudiana Antagonism Biological control Fusarium oxysporum Mycoparasitism Trichoderma asperellum |
title_short |
Trichoderma asperellum as a preventive and curative agent to control Fusarium wilt in Stevia rebaudiana |
title_full |
Trichoderma asperellum as a preventive and curative agent to control Fusarium wilt in Stevia rebaudiana |
title_fullStr |
Trichoderma asperellum as a preventive and curative agent to control Fusarium wilt in Stevia rebaudiana |
title_full_unstemmed |
Trichoderma asperellum as a preventive and curative agent to control Fusarium wilt in Stevia rebaudiana |
title_sort |
Trichoderma asperellum as a preventive and curative agent to control Fusarium wilt in Stevia rebaudiana |
dc.subject.spa.fl_str_mv |
Antagonism Biological control Fusarium oxysporum Mycoparasitism Trichoderma asperellum |
topic |
Antagonism Biological control Fusarium oxysporum Mycoparasitism Trichoderma asperellum |
description |
Stevia has been introduced in many countries for the production of sugar-free sweeteners. Concurrently, several emerging pathogens have been described in this plant host. One of the latest has been Fusarium oxysporum, a well-known soil-borne pathogen causing vascular wilt in many plants. Classical methods to control Fusarium wilt are being questioned, and biocontrol agents are gaining importance as part of integrated approaches to manage the disease. Different species of Trichoderma have been described as optimal candidates to control F. oxysporum. However, their effectiveness is generally reported in annual plants and efficacy depends on the application protocol. We conducted an experiment to assess the preventive or curative potential of the rhizospheric T. asperellum UDEAGIEM-H01 strain against F. oxysporum on rooted cuttings of S. rebaudiana. After 33 days, F. oxysporum-infected stevia seedlings were severely affected (90% of disease incidence). Contrastingly, only 10% of the T. asperellum pre-treated plants and 70% of the post-treated showed Fusarium wilt symptoms. Dual confrontation assays proved the potential antagonistic effect of T. asperellum against F. oxysporum and five additional soil-borne pathogens affecting S. rebaudiana. Further in vitro tests revealed that this new strain of T. asperellum produces phytohormones (salicylic and jasmonic acid), and the secretion of cell-wall degrading enzymes (chitinases and cellulases); this ability could be related to its antagonistic and mycoparasitic activity. The present work concluded that T. asperellum UDEAGIEM-H01 has a high ability, mainly as a preventive agent, to control F. oxysporum in stevia plants showing further antagonistic effects and mycoparasitism on other fungal pathogens. © 2021 Elsevier Inc. |
publishDate |
2021 |
dc.date.accessioned.none.fl_str_mv |
2021-02-05T14:57:40Z |
dc.date.available.none.fl_str_mv |
2021-02-05T14:57:40Z |
dc.date.none.fl_str_mv |
2021 |
dc.type.eng.fl_str_mv |
Article |
dc.type.coarversion.fl_str_mv |
http://purl.org/coar/version/c_970fb48d4fbd8a85 |
dc.type.coar.fl_str_mv |
http://purl.org/coar/resource_type/c_6501 http://purl.org/coar/resource_type/c_2df8fbb1 |
dc.type.driver.none.fl_str_mv |
info:eu-repo/semantics/article |
dc.identifier.issn.none.fl_str_mv |
10499644 |
dc.identifier.uri.none.fl_str_mv |
http://hdl.handle.net/11407/5900 |
dc.identifier.doi.none.fl_str_mv |
10.1016/j.biocontrol.2021.104537 |
identifier_str_mv |
10499644 10.1016/j.biocontrol.2021.104537 |
url |
http://hdl.handle.net/11407/5900 |
dc.language.iso.none.fl_str_mv |
eng |
language |
eng |
dc.relation.isversionof.none.fl_str_mv |
https://www.scopus.com/inward/record.uri?eid=2-s2.0-85099623312&doi=10.1016%2fj.biocontrol.2021.104537&partnerID=40&md5=7dcccc5ba150cce83b28690787f25a6a |
dc.relation.citationvolume.none.fl_str_mv |
155 |
dc.relation.references.none.fl_str_mv |
Abawi, G.S., Widmer, T.L., Impact of soil health management practices on soilborne pathogens, nematodes and root diseases of vegetable crops (2000) Appl. Soil Ecol., 15, pp. 37-47 Abbas, A., Jiang, D., Fu, Y., Trichoderma spp. as antagonist of Rhizoctonia solani (2017) J. Plant Pathol. Microbiol., 8 (402) Agrawal, T., Kotasthane, A., Chitinolytic assay of indigenous Trichoderma isolates collected from different geographical locations of Chhattisgarh in Central India (2012) Springer Plus, 73 (1), pp. 2-3 Akila, R., Rajendran, L., Harish, S., Saveetha, K., Raguchander, T., Samiyappan, R., Combined application of botanical formulations and biocontrol agents for the management of Fusarium oxysporum f. sp. cubense (Foc) causing Fusarium wilt in banana (2011) Biol. Control, 57, pp. 175-183 Al-Ahmadi, A., Subedi, A., Wang, G., Choudhary, R., Fakhoury, A., Watson, D.G., Detection of charcoal rot (Macrophomina phaseolina) toxin effects in soybean (Glycine max) seedlings using hyperspectral spectroscopy (2018) Comput. Electron. Agric., 150 (188), p. 195 Al-Ani, L.K.T., Trichoderma: Beneficial Role in Sustainable Agriculture by Plant Disease Management (2018), Springer Nature Singapore Pte Ltd Bambharolia, R.P., Patel, S.V., Khatrani, T.J., Goalkiya, B.A., Antagonism of Trichoderma spp. against Macrophomina phaseolina: evaluation of coiling and cell wall degrading enzymatic activities (2012) J. Plant Pathol. Microbiol. Bell, D.K., Well, H.D., Markham, C.R., “In vitro” antagonism of Trichoderma species against six fungal plant pathogens (1982) Ecol. Epidemiol., 72, pp. 379-382 Ben-Amira, M., Lopez, D., Triki-Mohamed, A., Khouaja, A., Chaar, H., Fumanal, B., Gousset-Dupont, A., Venisse, J.S., Beneficial effect of Trichoderma harzianum strain Ths97 in biocontrolling Fusarium solani causal agent of root rot disease in olive trees (2017) Biol. Control., 110, pp. 70-78 Benitez, T., Rincon, A.M., Limon, M.C., Codon, A.C., Biocontrol mechanisms of Trichoderma strains (2004) Int. Microbiol., 7, pp. 249-260 Bolognesi, C., Genotoxicity of pesticides: a review of human biomonitoring studies (2003) Mutat. Res. Rev. Mutat. Res., 543, pp. 251-272 Brandle, J.E., Starratt, A.N., Gijzen, M., Stevia rebaudiana: its agricultural, biological, and chemical properties (1998) Can. J. Plant Sci., 78 (4), pp. 527-536 Brimner, T.A., Boland, G.J., A review of the non-target effects of fungi used to biologically control plant diseases (2003) Agric. Ecosyst. Environ., 100, pp. 3-16 Brotman, Y., Kapuganti, J.G., Viterbo, A., Trichoderma (2010) Curr. Biol., 20 (9), pp. R390-R391 Bubici, G., Kaushal, M., Prigigallo, M.I., Gómez-Lama Cabanás, C., Mercado-Blanco, J., Biological control agents against Fusarium wilt of banana (2019) Front. Microbiol. Camprubí, A., Calvet, C., Estaún, V., Growth enhancement of Citrus reshni after inoculation with Glomus intraradices and Trichoderma aureoviride and associated effects on microbial populations and enzyme activity in potting mixes (1995) Plant Soil, 173 (2), pp. 233-238 Carisse, O., Philion, V., Rolland, D., Bernier, J., Effect of fall application of fungal antagonists on spring ascospore production of the apple scab pathogen, Venturia inaequalis (2000) Phytopathology, 90, pp. 31-37 Contreras-Cornejo, H.A., Macías-Rodríguez, L., López-Bucio, J.S., López-Bucio, J., Enhanced Plant Immunity using Trichoderma (2014), Elsevier Cordier, C., Alabouvette, C., Effects of the introduction of a biocontrol strain of Trichoderma atroviride on non target soil micro-organisms (2009) Eur. J. Soil Biol., 4, pp. 267-274 de Souza, R.M., Seibert, D., Quesada, H.B., Bassetti, F.D., Fagundes-Klen, M.R., Bergamasco, R., Occurrence, impacts and general aspects of pesticides in surface water: a review (2020) Process Saf. Environ. Protect., 135, pp. 22-37 Dean, R., Van Kan, J.A.L., Pretorius, Z.A., Hammond-Kosack, K.E., Di Pietro, A., Spanu, P.D., Rudd, J.J., Foster, G.D., The top 10 fungal pathogens in molecular plant pathology (2012) Mol. Plant Pathol., 13 (4), pp. 414-430 Díaz-Gutiérrez, C., Poschenrieder, C., Arroyave, C., Martos, S., Peláez, C., First report of Fusarium oxysporum causing vascular wilt of Stevia rebaudiana in Colombia (2019) Plant Dis., 103 (7), p. 1779 Dissanayake, A.J., Liu, M., Zhang, W., Chen, Z., Udayanga, D., Chukeatirote, E., Li, X., Hyde, K.D., Morphological and molecular characterization of Diaporthe species associated with grapevine trunk disease in China (2015) Fungal Biol., 119, pp. 283-294 Druzhinina, I.S., Seidil-Seiboth, V., Herrera-Estrella, A., Horwitz, B.A., Kenerly, C.M., Monte, E., Mukherjee, P.K., Kubicek, C.P., Trichoderma: the genomics of opportunistic success (2011) Nat. Rev. Microbiol., 9, pp. 749-759 Estrada, G., Sandoval, I., Patogenicidad de especies de Curvularia en arroz (2004) Fitosanidad, 8 (4), pp. 23-26. , http://www.redalyc.org/articulo.oa?id=209117865004, Available in Farrar, J.J., Davis, R.M., Canevari, W.M., Fouche, C.F., First report of Verticillium dahliae on Stevia (Stevia rebaudiana) in North America (2007) Plant Dis., 84 (8), p. 922 Fravel, D.R., Commercialization and implementation of biocontrol (2005) Annu. Rev. Phytopathol., 43, pp. 337-359 Goswami, R.S., Punja, Z.K., Molecular and biochemical characterization of defense responses in ginseng (Panax quinquefolius) roots challenged with Fusarium equiseti (2008) Physiol. Mol. Plant Pathol., 72 (1-3), pp. 10-20. , https://doi.org/10-20.10.1016/j.pmpp.2008.04.006 Harman, G.E., Overview of mechanisms and uses of Trichoderma spp (2006) Phytopathology, 96, pp. 190-194 Harman, G.E., Hayes, C.K., Lorito, M., Broadway, R.M., Di Pietro, A., Peterbauer, C., Chitinolytic enzymes of Trichoderma harzianum: purification of chitobiosidase and endochitinase (1993) Phytopathology, 83, pp. 313-318 Harman, G.E., Howell, C.R., Viterbo, A., Chet, I., Lorito, M., Trichoderma species opportunistic, avirulent plant symbionts (2004) Nat. Rev. Microbiol., 2, pp. 43-56 Hermosa, R., Viterbo, A., Chet, I., Monte, E., Plant-beneficial effects of Trichoderma and of its genes (2012) Microbiology, 158, pp. 17-25 Herrera-Téllez, V.I., Cruz-Olmedo, A.K., Plasencia, J., Gavilanes-Ruiz, M., Arce-Cervantes, O., Hernández-León, S., Saucedo-García, M., The Protective effect of Trichoderma asperellum on tomato plants against Fusarium oxysporum and Botrytis cinerea diseases involves inhibition of reactive oxygen species production (2019) Int. J. Mol. Sci., 20, pp. 1-13 Howell, C.R., Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts (2003) Plant Dis., 87, pp. 4-10 Juliatti, F.C., Rezende, A.A., Marinho-Juliatti, B.C., Morais, T.P., Trichoderma as a biocontrol agent against Sclerotinia stem rot or white mold on soybeans in Brazil: usage and technology (2019) Trichoderma – The Most Widely Used Fungicide, pp. 1-24. , M.M. Shad IntechOpen Kang, S., Demers, J., Jimenez-Gasco, M.M., Rep, M., Fusarium oxysporum (2014) Genomics of Plant-Associated Fungi and Oomycetes: Dicot Pathogens©Springer-Verlag Berlin Heidelberg, , R.A. Dean A. Lichens-Park C. Kole Koehler, A.M., Shew, H., First report of stem rot of Stevia caused by Sclerotinia sclerotiorum in North Carolina (2014) Plant Dis., 98 (10), p. 1433 Koehler, A.M., Shew, H.D., First report of charcoal rot of Stevia caused by Macrophomina phaseolina in North Carolina (2017) Plant Dis., 102 (1), p. 241 Koehler, A.M., Shew, H., First report of stem and root rot of stevia caused by Sclerotium rolfsii in North Carolina (2014) Plant Dis., 98 (7), p. 1005 Koehler, A.M., Lookabaugh, E.C., Shew, B.B., Shew, H.D., First report of pythium root rot of Stevia caused by Pythium myriotylum, P. irregulare, and P. aphanidermatum in North Carolina (2017) Plant Dis., 101 (7), p. 1331 Lemus-Mondaca, R., Vega-Gálvez, A., Zura-Bravo, L., Ah-Hen, K., Stevia rebaudiana Bertoni, source of a high-potency natural sweetener: a comprehensive review on the biochemical, nutritional and functional aspects (2012) Food Chem., 132, pp. 1121-1132 Llugany, M., Martin, S.R., Barceló, J., Poschenrieder, C., Endogenous jasmonic and salicylic acids levels in the Cd-hyperaccumulator Noccaea (Thlaspi) praecox exposed to fungal infection and/or mechanical stress (2013) Plant Cell Rep., 32, pp. 1243-1249 López-López, N., Segarra, G., Vergara, O., López-Fabal, A., Trillas, M.I., Compost from forest cleaning green waste and Trichoderma asperellum strain T34 reduced incidence of Fusarium circinatum in Pinus radiata seedlings (2015) Biol. Control, 95, pp. 31-39 López-Zapata, S.P., Castaño-Zapata, J., (2019), Manejo integrado del mal de Panamá [Fusarium oxysporum Schlechtend.: Fr. sp. cubense (E.F. SM.) W.C. Snyder & H.N. Hansen]: una revisión. Rev. U.D.C.A Act. & Div. Cient. 22(2):e1240 Mazrou, Y.S.S., Makhlouf, A.H., Elseehy, M.M., Awad, M.F., Hassan, M.M., Antagonistic activity and molecular characterization of biological control agent Trichoderma harzianum from Saudi Arabia (2020) Egypt. J. Pest control., 30 (4), pp. 1-8 McGovern, R.J., Management of tomato diseases caused by Fusarium oxysporum (2015) Crop Prot., 73, pp. 78-92 Meftaul, I.M., Venkateswarlu, K., Dharmarajan, R., Annamalai, P., Megharaj, M., Pesticides in the urban environment: a potential threat that knocks at the door (2020) Sci. Total Environ., 711 Mohiddin, F.A., Khan, M.R., Khan, S.M., Why Trichoderma is considered super hero (super fungus) against the evil parasites? (2010) Plant Pathol. J., 9 (3), pp. 92-102 Molina, A.B., Fabregar, E.G., Ramillete, E.G., Sinohin, V.O., Viljoen, A., Field resistance of selected banana cultivars against tropical race 4 of Fusarium oxysporum f. sp. cubense in the Philippines (2011) Phytopathology, 101, p. S122 Monfil, V.O., Casas-Flores, S., Molecular mechanisms of biocontrol in Trichoderma spp. and their applications in agriculture (2014) Biotechnology and Biology of Trichoderma, pp. 29-453. , V. Gupta M. Schmoll A. Herrera-Estrella R. Upadhyay I. Druzhinina M. Tuohy Elsevier Mukherjee, P.K., Horwitz, B.A., Kenerley, C.M., Secondary metabolism in Trichoderma—a genomic perspective (2012) Microbiol. SGM, 158, pp. 35-45 Murashige, T., Skoog, F.A., Revised medium for rapid growth and bio-assays with tobacco tissue culture (1962) Physiol. Plant., 15, pp. 473-497 Nel, B., Steinberg, C., Labuschagne, N., Viljoen, A., The potential of nonpathogenic Fusarium oxysporum and other biological control organisms for suppressing fusarium wilt of banana (2006) Plant. Pathol., 55 (2), pp. 217-223 Ploetz, R.C., Diseases of tropical perennial crops: challenging problems in diverse environments (2007) Plant Dis., 91 (6), pp. 644-663 Promwee, A., Yenjit, P., Issarakraisila, M., Intana, W., Chamswarng, C., Efficacy of indigenous Trichoderma harzianum in controlling Phytophthora leaf fall (Phytophthora palmivora) in Thai rubber trees (2017) J. Plant Dis. Prot., 124, pp. 41-50 Raguchander, T., Jayashree, K., Samiyappan, S., Management of Fusarium wilt of banana using antagonistic microorganisms (1997) J. Biol. Control., 11, pp. 101-105 Raza, W., Ling, N., Zhang, R., Huang, Q., Xu, Y., Shen, Q., Success evaluation of the biological control of Fusarium wilts of cucumber, banana, and tomato since 2000 and future research strategies (2017) Crit. Rev. Biotechnol., 37 (2), pp. 202-212 Rojas-Avelizapa, L.I., Cruz-Camarillo, R., Guerrero, M.I., Rodríguez-Vázquez, R., Ibarra, J.E., Selection and characterization of a proteo-chitinolytic strain of Bacillus thuringiensis, able to grow in shrimp waste media (1999) World J. Microbiol. Biotechnol., 15 (2), pp. 299-308 Royse, D.J., Ries, S.M., The influence of fungi isolated from peach twigs on the pathogenicity of Cytospora cincta (1978) Ecol. Epidemiol., 68, pp. 603-607 Salas-Marina, M.A., Silva-Flores, M.A., Uresti-Rivera, E.E., Castro-Longoria, E., Herrera-Estrella, A., Casa-Flores, S., Colonization of Arabidopsis roots by Trichoderma atroviride promotes growth and enhances systemic disease resistance through jasmonic acid/ethylene and salicylic acid pathways (2011) Eur. J. Plant Pathol., 131, pp. 15-26 Sanchez, A.D., Ousset, M.J., Sosa, M.C., Biological control of Phytophthora collar rot of pear using regional Trichoderma strains with multiple mechanisms (2019) Biol. Control. Sanchez-Hernandez, M.E., Ruiz-Davila, A., Perez De Algaba, A., Blanco-Lopez, M.A., Trapero-Casas, A., Occurrence and etiology of death of young olive trees in southern Spain (1998) Eur. J. Plant Pathol., 104, pp. 347-357 Saravanakumar, K., Yu, C., Dou, K., Wang, M., Li, Y., Chen, J., Synergistic effect of Trichoderma-derived antifungal metabolites and cell wall degrading enzymes on enhanced biocontrol of Fusarium oxysporum f. sp. Cucumerinum (2016) Biol. Control., 94, pp. 37-46 Segarra, G., Jauregui, O., Casanova, E., Trillas, I., Simultaneous quantitative LC-ESI–MS/MS analyses of salicylic acid and jasmonic acid in crude extracts of Cucumis sativus under biotic stress (2006) Phytochemistry, 67, pp. 395-401 Shang, J., Liu, B., Xu, Z., Efficacy of Trichoderma asperellum TC01 against anthracnose and growth promotion of Camellia sinensis seedlings (2020) Biol. Control, 143 Sharavanan, P.T., Muthusamy, M., Marimuthu, T., Development of integrated approach to manage the fusarial wilt of banana (2003) Crop Prot., 22, pp. 1117-1123 Sharma, R., Magotra, A., Manhas, R., Chaubey, A., Antagonistic potential of a psychrotrophic fungus: Trichoderma velutinum ACR-P1 (2017) Biol. Control, 115, pp. 12-17 Shoresh, M., Harman, G.E., Mastouri, F., Induced systemic resistance and plant responses to fungal biocontrol agents (2010) Annu. Rev. Phytopathol., 48, pp. 21-43 Singh, D.P., Kumari, M., Prakash, H.G., Rao, G.P., Solomon, S., Phytochemical and Pharmacological Importance of Stevia: a calorie-free natural sweetener (2019) Sugar Tech., 21, pp. 227-234 Stewart, J.E., Turner, A.N., Brewer, M.T., Evolutionary history and variation in host range of three Stagonosporopsis species causing gummy stem blight of cucurbits (2015) Fungal Biol., 119, pp. 370-382 Thangavelu, R., Gopi, M., Combined application of native Trichoderma isolates possessing multiple functions for the control of Fusarium wilt disease in banana cv. Grand Naine (2015) Biolcontrol Sci. Technol., 25 (10), pp. 1147-1164 Thangavelu, R., Palaniswami, A., Velazhahan, R., Mass production of Trichoderma harzianum for managing fusarium wilt of banana (2004) Agric. Ecosyst. Environ., 103 (1), pp. 259-263 Toghueo, R.M.K., Eke, P., Zabalgogeazcoa, I., Rodríguez-Vásquez de Aldana, B., Nana, L.W., Boyom, F.F., Biocontrol and growth enhancement potential of two endophytic Trichoderma spp. from Terminalia catappa against the causative agent of Common Bean Root Rot (Fusarium solani) (2016) Biol. Control, 96, pp. 8-20 Tondje, P.R., Roberts, D.P., Bon, M.C., Widmer, T., Samuels, G.J., Ismaiel, A., Begoude, A.D., Hebbar, K.P., Isolation and identification of mycoparasitic isolates of Trichoderma asperellum with potential for suppression of black pod disease of cacao in Cameroon (2007) Biol. Control, 43, pp. 202-212 Viterbo, A., Horwitz, B.A., Mycoparasitism (2010) Cellular and Molecular Biology of Filamentous Fungi, pp. 676-693. , K.A. Borkovich D.J. Ebbole American Society for Microbiology Washington Viterbo, A., Haran, S., Friesem, D., Ramot, O., Chet, I., Antifungal activity of a novel endochitinase gene (chit36) from Trichoderma harzianum Rifai TM (2001) FEMS Microbiol. Lett., 200 (2), pp. 169-174 Vos, C.M., De Cremer, K., Cammue, B.P., De Coninck, B., The toolbox of Trichoderma spp. in the biocontrol of Botrytis cinerea disease (2015) Mol. Plant Pathol., 16 (4), pp. 400-412 Wibowo, A., Santosa, A.T., Subandiyah, S., Hermanto, C., Taylor, M.F.P., Control of Fusarium wilt of banana by using Trichoderma harzianum and resistant banana cultivars (2013) Acta Hortic., 975, pp. 173-177 Woo, S.L., Scala, F., Ruocco, M., Lorito, M., The molecular biology of the interactions between Trichoderma spp., phytopathogenic fungi, and plants (2006) Phytopathology, 96, pp. 181-185 Zeilinger, S., Gruber, S.G., Bansal, R., Mukherjee, P.K., Secondary metabolism in Trichoderma – chemistry meets genomics (2016) Fungal Biol. Rev., 30 (2), pp. 1-17 Zhang, N., He, X., Zhang, J., Raza, W., Ling, N., Ruan, Y.-Z., Shen, Q.R., Huang, Q.W., Suppression of Fusarium wilt of banana with application of bio-organic fertilizers (2014) Pedosphere, 24 (5), pp. 613-624 Zhang, X.Y., Hu, J., Zhou, H.Y., Hao, J.J., Xue, Y.F., Chen, H., Wang, B.G., First report of Fusarium oxysporum and F. solani causing Fusarium dry rot of carrot in China (2014) Plant Dis., 98 (9). , 1273–1273 Zhu, Y., Lujan, P.A., Wedegaertner, T., Nichols, R., Abdelraheem, A., Zhang, J.F., Sanogo, S., First report of Fusarium oxysporum f. sp. vasinfectum Race 4 causing Fusarium wilt of cotton in New Mexico, U.S.A (2019) Plant Dis., 104 (2). , 588–588 |
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http://purl.org/coar/access_right/c_16ec |
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http://purl.org/coar/access_right/c_16ec |
dc.publisher.none.fl_str_mv |
Academic Press Inc. |
dc.publisher.program.spa.fl_str_mv |
Ingeniería Ambiental |
dc.publisher.faculty.spa.fl_str_mv |
Facultad de Ingenierías |
publisher.none.fl_str_mv |
Academic Press Inc. |
dc.source.none.fl_str_mv |
Biological Control |
institution |
Universidad de Medellín |
repository.name.fl_str_mv |
Repositorio Institucional Universidad de Medellin |
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repositorio@udem.edu.co |
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1814159230049976320 |
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20212021-02-05T14:57:40Z2021-02-05T14:57:40Z10499644http://hdl.handle.net/11407/590010.1016/j.biocontrol.2021.104537Stevia has been introduced in many countries for the production of sugar-free sweeteners. Concurrently, several emerging pathogens have been described in this plant host. One of the latest has been Fusarium oxysporum, a well-known soil-borne pathogen causing vascular wilt in many plants. Classical methods to control Fusarium wilt are being questioned, and biocontrol agents are gaining importance as part of integrated approaches to manage the disease. Different species of Trichoderma have been described as optimal candidates to control F. oxysporum. However, their effectiveness is generally reported in annual plants and efficacy depends on the application protocol. We conducted an experiment to assess the preventive or curative potential of the rhizospheric T. asperellum UDEAGIEM-H01 strain against F. oxysporum on rooted cuttings of S. rebaudiana. After 33 days, F. oxysporum-infected stevia seedlings were severely affected (90% of disease incidence). Contrastingly, only 10% of the T. asperellum pre-treated plants and 70% of the post-treated showed Fusarium wilt symptoms. Dual confrontation assays proved the potential antagonistic effect of T. asperellum against F. oxysporum and five additional soil-borne pathogens affecting S. rebaudiana. Further in vitro tests revealed that this new strain of T. asperellum produces phytohormones (salicylic and jasmonic acid), and the secretion of cell-wall degrading enzymes (chitinases and cellulases); this ability could be related to its antagonistic and mycoparasitic activity. The present work concluded that T. asperellum UDEAGIEM-H01 has a high ability, mainly as a preventive agent, to control F. oxysporum in stevia plants showing further antagonistic effects and mycoparasitism on other fungal pathogens. © 2021 Elsevier Inc.engAcademic Press Inc.Ingeniería AmbientalFacultad de Ingenieríashttps://www.scopus.com/inward/record.uri?eid=2-s2.0-85099623312&doi=10.1016%2fj.biocontrol.2021.104537&partnerID=40&md5=7dcccc5ba150cce83b28690787f25a6a155Abawi, G.S., Widmer, T.L., Impact of soil health management practices on soilborne pathogens, nematodes and root diseases of vegetable crops (2000) Appl. Soil Ecol., 15, pp. 37-47Abbas, A., Jiang, D., Fu, Y., Trichoderma spp. as antagonist of Rhizoctonia solani (2017) J. Plant Pathol. Microbiol., 8 (402)Agrawal, T., Kotasthane, A., Chitinolytic assay of indigenous Trichoderma isolates collected from different geographical locations of Chhattisgarh in Central India (2012) Springer Plus, 73 (1), pp. 2-3Akila, R., Rajendran, L., Harish, S., Saveetha, K., Raguchander, T., Samiyappan, R., Combined application of botanical formulations and biocontrol agents for the management of Fusarium oxysporum f. sp. cubense (Foc) causing Fusarium wilt in banana (2011) Biol. Control, 57, pp. 175-183Al-Ahmadi, A., Subedi, A., Wang, G., Choudhary, R., Fakhoury, A., Watson, D.G., Detection of charcoal rot (Macrophomina phaseolina) toxin effects in soybean (Glycine max) seedlings using hyperspectral spectroscopy (2018) Comput. Electron. Agric., 150 (188), p. 195Al-Ani, L.K.T., Trichoderma: Beneficial Role in Sustainable Agriculture by Plant Disease Management (2018), Springer Nature Singapore Pte LtdBambharolia, R.P., Patel, S.V., Khatrani, T.J., Goalkiya, B.A., Antagonism of Trichoderma spp. against Macrophomina phaseolina: evaluation of coiling and cell wall degrading enzymatic activities (2012) J. Plant Pathol. Microbiol.Bell, D.K., Well, H.D., Markham, C.R., “In vitro” antagonism of Trichoderma species against six fungal plant pathogens (1982) Ecol. Epidemiol., 72, pp. 379-382Ben-Amira, M., Lopez, D., Triki-Mohamed, A., Khouaja, A., Chaar, H., Fumanal, B., Gousset-Dupont, A., Venisse, J.S., Beneficial effect of Trichoderma harzianum strain Ths97 in biocontrolling Fusarium solani causal agent of root rot disease in olive trees (2017) Biol. Control., 110, pp. 70-78Benitez, T., Rincon, A.M., Limon, M.C., Codon, A.C., Biocontrol mechanisms of Trichoderma strains (2004) Int. Microbiol., 7, pp. 249-260Bolognesi, C., Genotoxicity of pesticides: a review of human biomonitoring studies (2003) Mutat. Res. Rev. Mutat. Res., 543, pp. 251-272Brandle, J.E., Starratt, A.N., Gijzen, M., Stevia rebaudiana: its agricultural, biological, and chemical properties (1998) Can. J. Plant Sci., 78 (4), pp. 527-536Brimner, T.A., Boland, G.J., A review of the non-target effects of fungi used to biologically control plant diseases (2003) Agric. Ecosyst. Environ., 100, pp. 3-16Brotman, Y., Kapuganti, J.G., Viterbo, A., Trichoderma (2010) Curr. Biol., 20 (9), pp. R390-R391Bubici, G., Kaushal, M., Prigigallo, M.I., Gómez-Lama Cabanás, C., Mercado-Blanco, J., Biological control agents against Fusarium wilt of banana (2019) Front. Microbiol.Camprubí, A., Calvet, C., Estaún, V., Growth enhancement of Citrus reshni after inoculation with Glomus intraradices and Trichoderma aureoviride and associated effects on microbial populations and enzyme activity in potting mixes (1995) Plant Soil, 173 (2), pp. 233-238Carisse, O., Philion, V., Rolland, D., Bernier, J., Effect of fall application of fungal antagonists on spring ascospore production of the apple scab pathogen, Venturia inaequalis (2000) Phytopathology, 90, pp. 31-37Contreras-Cornejo, H.A., Macías-Rodríguez, L., López-Bucio, J.S., López-Bucio, J., Enhanced Plant Immunity using Trichoderma (2014), ElsevierCordier, C., Alabouvette, C., Effects of the introduction of a biocontrol strain of Trichoderma atroviride on non target soil micro-organisms (2009) Eur. J. Soil Biol., 4, pp. 267-274de Souza, R.M., Seibert, D., Quesada, H.B., Bassetti, F.D., Fagundes-Klen, M.R., Bergamasco, R., Occurrence, impacts and general aspects of pesticides in surface water: a review (2020) Process Saf. Environ. Protect., 135, pp. 22-37Dean, R., Van Kan, J.A.L., Pretorius, Z.A., Hammond-Kosack, K.E., Di Pietro, A., Spanu, P.D., Rudd, J.J., Foster, G.D., The top 10 fungal pathogens in molecular plant pathology (2012) Mol. Plant Pathol., 13 (4), pp. 414-430Díaz-Gutiérrez, C., Poschenrieder, C., Arroyave, C., Martos, S., Peláez, C., First report of Fusarium oxysporum causing vascular wilt of Stevia rebaudiana in Colombia (2019) Plant Dis., 103 (7), p. 1779Dissanayake, A.J., Liu, M., Zhang, W., Chen, Z., Udayanga, D., Chukeatirote, E., Li, X., Hyde, K.D., Morphological and molecular characterization of Diaporthe species associated with grapevine trunk disease in China (2015) Fungal Biol., 119, pp. 283-294Druzhinina, I.S., Seidil-Seiboth, V., Herrera-Estrella, A., Horwitz, B.A., Kenerly, C.M., Monte, E., Mukherjee, P.K., Kubicek, C.P., Trichoderma: the genomics of opportunistic success (2011) Nat. Rev. Microbiol., 9, pp. 749-759Estrada, G., Sandoval, I., Patogenicidad de especies de Curvularia en arroz (2004) Fitosanidad, 8 (4), pp. 23-26. , http://www.redalyc.org/articulo.oa?id=209117865004, Available inFarrar, J.J., Davis, R.M., Canevari, W.M., Fouche, C.F., First report of Verticillium dahliae on Stevia (Stevia rebaudiana) in North America (2007) Plant Dis., 84 (8), p. 922Fravel, D.R., Commercialization and implementation of biocontrol (2005) Annu. Rev. Phytopathol., 43, pp. 337-359Goswami, R.S., Punja, Z.K., Molecular and biochemical characterization of defense responses in ginseng (Panax quinquefolius) roots challenged with Fusarium equiseti (2008) Physiol. Mol. Plant Pathol., 72 (1-3), pp. 10-20. , https://doi.org/10-20.10.1016/j.pmpp.2008.04.006Harman, G.E., Overview of mechanisms and uses of Trichoderma spp (2006) Phytopathology, 96, pp. 190-194Harman, G.E., Hayes, C.K., Lorito, M., Broadway, R.M., Di Pietro, A., Peterbauer, C., Chitinolytic enzymes of Trichoderma harzianum: purification of chitobiosidase and endochitinase (1993) Phytopathology, 83, pp. 313-318Harman, G.E., Howell, C.R., Viterbo, A., Chet, I., Lorito, M., Trichoderma species opportunistic, avirulent plant symbionts (2004) Nat. Rev. Microbiol., 2, pp. 43-56Hermosa, R., Viterbo, A., Chet, I., Monte, E., Plant-beneficial effects of Trichoderma and of its genes (2012) Microbiology, 158, pp. 17-25Herrera-Téllez, V.I., Cruz-Olmedo, A.K., Plasencia, J., Gavilanes-Ruiz, M., Arce-Cervantes, O., Hernández-León, S., Saucedo-García, M., The Protective effect of Trichoderma asperellum on tomato plants against Fusarium oxysporum and Botrytis cinerea diseases involves inhibition of reactive oxygen species production (2019) Int. J. Mol. Sci., 20, pp. 1-13Howell, C.R., Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts (2003) Plant Dis., 87, pp. 4-10Juliatti, F.C., Rezende, A.A., Marinho-Juliatti, B.C., Morais, T.P., Trichoderma as a biocontrol agent against Sclerotinia stem rot or white mold on soybeans in Brazil: usage and technology (2019) Trichoderma – The Most Widely Used Fungicide, pp. 1-24. , M.M. Shad IntechOpenKang, S., Demers, J., Jimenez-Gasco, M.M., Rep, M., Fusarium oxysporum (2014) Genomics of Plant-Associated Fungi and Oomycetes: Dicot Pathogens©Springer-Verlag Berlin Heidelberg, , R.A. Dean A. Lichens-Park C. KoleKoehler, A.M., Shew, H., First report of stem rot of Stevia caused by Sclerotinia sclerotiorum in North Carolina (2014) Plant Dis., 98 (10), p. 1433Koehler, A.M., Shew, H.D., First report of charcoal rot of Stevia caused by Macrophomina phaseolina in North Carolina (2017) Plant Dis., 102 (1), p. 241Koehler, A.M., Shew, H., First report of stem and root rot of stevia caused by Sclerotium rolfsii in North Carolina (2014) Plant Dis., 98 (7), p. 1005Koehler, A.M., Lookabaugh, E.C., Shew, B.B., Shew, H.D., First report of pythium root rot of Stevia caused by Pythium myriotylum, P. irregulare, and P. aphanidermatum in North Carolina (2017) Plant Dis., 101 (7), p. 1331Lemus-Mondaca, R., Vega-Gálvez, A., Zura-Bravo, L., Ah-Hen, K., Stevia rebaudiana Bertoni, source of a high-potency natural sweetener: a comprehensive review on the biochemical, nutritional and functional aspects (2012) Food Chem., 132, pp. 1121-1132Llugany, M., Martin, S.R., Barceló, J., Poschenrieder, C., Endogenous jasmonic and salicylic acids levels in the Cd-hyperaccumulator Noccaea (Thlaspi) praecox exposed to fungal infection and/or mechanical stress (2013) Plant Cell Rep., 32, pp. 1243-1249López-López, N., Segarra, G., Vergara, O., López-Fabal, A., Trillas, M.I., Compost from forest cleaning green waste and Trichoderma asperellum strain T34 reduced incidence of Fusarium circinatum in Pinus radiata seedlings (2015) Biol. Control, 95, pp. 31-39López-Zapata, S.P., Castaño-Zapata, J., (2019), Manejo integrado del mal de Panamá [Fusarium oxysporum Schlechtend.: Fr. sp. cubense (E.F. SM.) W.C. Snyder & H.N. Hansen]: una revisión. Rev. U.D.C.A Act. & Div. Cient. 22(2):e1240Mazrou, Y.S.S., Makhlouf, A.H., Elseehy, M.M., Awad, M.F., Hassan, M.M., Antagonistic activity and molecular characterization of biological control agent Trichoderma harzianum from Saudi Arabia (2020) Egypt. J. Pest control., 30 (4), pp. 1-8McGovern, R.J., Management of tomato diseases caused by Fusarium oxysporum (2015) Crop Prot., 73, pp. 78-92Meftaul, I.M., Venkateswarlu, K., Dharmarajan, R., Annamalai, P., Megharaj, M., Pesticides in the urban environment: a potential threat that knocks at the door (2020) Sci. Total Environ., 711Mohiddin, F.A., Khan, M.R., Khan, S.M., Why Trichoderma is considered super hero (super fungus) against the evil parasites? (2010) Plant Pathol. J., 9 (3), pp. 92-102Molina, A.B., Fabregar, E.G., Ramillete, E.G., Sinohin, V.O., Viljoen, A., Field resistance of selected banana cultivars against tropical race 4 of Fusarium oxysporum f. sp. cubense in the Philippines (2011) Phytopathology, 101, p. S122Monfil, V.O., Casas-Flores, S., Molecular mechanisms of biocontrol in Trichoderma spp. and their applications in agriculture (2014) Biotechnology and Biology of Trichoderma, pp. 29-453. , V. Gupta M. Schmoll A. Herrera-Estrella R. Upadhyay I. Druzhinina M. Tuohy ElsevierMukherjee, P.K., Horwitz, B.A., Kenerley, C.M., Secondary metabolism in Trichoderma—a genomic perspective (2012) Microbiol. SGM, 158, pp. 35-45Murashige, T., Skoog, F.A., Revised medium for rapid growth and bio-assays with tobacco tissue culture (1962) Physiol. Plant., 15, pp. 473-497Nel, B., Steinberg, C., Labuschagne, N., Viljoen, A., The potential of nonpathogenic Fusarium oxysporum and other biological control organisms for suppressing fusarium wilt of banana (2006) Plant. Pathol., 55 (2), pp. 217-223Ploetz, R.C., Diseases of tropical perennial crops: challenging problems in diverse environments (2007) Plant Dis., 91 (6), pp. 644-663Promwee, A., Yenjit, P., Issarakraisila, M., Intana, W., Chamswarng, C., Efficacy of indigenous Trichoderma harzianum in controlling Phytophthora leaf fall (Phytophthora palmivora) in Thai rubber trees (2017) J. Plant Dis. Prot., 124, pp. 41-50Raguchander, T., Jayashree, K., Samiyappan, S., Management of Fusarium wilt of banana using antagonistic microorganisms (1997) J. Biol. Control., 11, pp. 101-105Raza, W., Ling, N., Zhang, R., Huang, Q., Xu, Y., Shen, Q., Success evaluation of the biological control of Fusarium wilts of cucumber, banana, and tomato since 2000 and future research strategies (2017) Crit. Rev. Biotechnol., 37 (2), pp. 202-212Rojas-Avelizapa, L.I., Cruz-Camarillo, R., Guerrero, M.I., Rodríguez-Vázquez, R., Ibarra, J.E., Selection and characterization of a proteo-chitinolytic strain of Bacillus thuringiensis, able to grow in shrimp waste media (1999) World J. Microbiol. Biotechnol., 15 (2), pp. 299-308Royse, D.J., Ries, S.M., The influence of fungi isolated from peach twigs on the pathogenicity of Cytospora cincta (1978) Ecol. Epidemiol., 68, pp. 603-607Salas-Marina, M.A., Silva-Flores, M.A., Uresti-Rivera, E.E., Castro-Longoria, E., Herrera-Estrella, A., Casa-Flores, S., Colonization of Arabidopsis roots by Trichoderma atroviride promotes growth and enhances systemic disease resistance through jasmonic acid/ethylene and salicylic acid pathways (2011) Eur. J. Plant Pathol., 131, pp. 15-26Sanchez, A.D., Ousset, M.J., Sosa, M.C., Biological control of Phytophthora collar rot of pear using regional Trichoderma strains with multiple mechanisms (2019) Biol. Control.Sanchez-Hernandez, M.E., Ruiz-Davila, A., Perez De Algaba, A., Blanco-Lopez, M.A., Trapero-Casas, A., Occurrence and etiology of death of young olive trees in southern Spain (1998) Eur. J. Plant Pathol., 104, pp. 347-357Saravanakumar, K., Yu, C., Dou, K., Wang, M., Li, Y., Chen, J., Synergistic effect of Trichoderma-derived antifungal metabolites and cell wall degrading enzymes on enhanced biocontrol of Fusarium oxysporum f. sp. Cucumerinum (2016) Biol. Control., 94, pp. 37-46Segarra, G., Jauregui, O., Casanova, E., Trillas, I., Simultaneous quantitative LC-ESI–MS/MS analyses of salicylic acid and jasmonic acid in crude extracts of Cucumis sativus under biotic stress (2006) Phytochemistry, 67, pp. 395-401Shang, J., Liu, B., Xu, Z., Efficacy of Trichoderma asperellum TC01 against anthracnose and growth promotion of Camellia sinensis seedlings (2020) Biol. Control, 143Sharavanan, P.T., Muthusamy, M., Marimuthu, T., Development of integrated approach to manage the fusarial wilt of banana (2003) Crop Prot., 22, pp. 1117-1123Sharma, R., Magotra, A., Manhas, R., Chaubey, A., Antagonistic potential of a psychrotrophic fungus: Trichoderma velutinum ACR-P1 (2017) Biol. Control, 115, pp. 12-17Shoresh, M., Harman, G.E., Mastouri, F., Induced systemic resistance and plant responses to fungal biocontrol agents (2010) Annu. Rev. Phytopathol., 48, pp. 21-43Singh, D.P., Kumari, M., Prakash, H.G., Rao, G.P., Solomon, S., Phytochemical and Pharmacological Importance of Stevia: a calorie-free natural sweetener (2019) Sugar Tech., 21, pp. 227-234Stewart, J.E., Turner, A.N., Brewer, M.T., Evolutionary history and variation in host range of three Stagonosporopsis species causing gummy stem blight of cucurbits (2015) Fungal Biol., 119, pp. 370-382Thangavelu, R., Gopi, M., Combined application of native Trichoderma isolates possessing multiple functions for the control of Fusarium wilt disease in banana cv. Grand Naine (2015) Biolcontrol Sci. Technol., 25 (10), pp. 1147-1164Thangavelu, R., Palaniswami, A., Velazhahan, R., Mass production of Trichoderma harzianum for managing fusarium wilt of banana (2004) Agric. Ecosyst. Environ., 103 (1), pp. 259-263Toghueo, R.M.K., Eke, P., Zabalgogeazcoa, I., Rodríguez-Vásquez de Aldana, B., Nana, L.W., Boyom, F.F., Biocontrol and growth enhancement potential of two endophytic Trichoderma spp. from Terminalia catappa against the causative agent of Common Bean Root Rot (Fusarium solani) (2016) Biol. Control, 96, pp. 8-20Tondje, P.R., Roberts, D.P., Bon, M.C., Widmer, T., Samuels, G.J., Ismaiel, A., Begoude, A.D., Hebbar, K.P., Isolation and identification of mycoparasitic isolates of Trichoderma asperellum with potential for suppression of black pod disease of cacao in Cameroon (2007) Biol. Control, 43, pp. 202-212Viterbo, A., Horwitz, B.A., Mycoparasitism (2010) Cellular and Molecular Biology of Filamentous Fungi, pp. 676-693. , K.A. Borkovich D.J. Ebbole American Society for Microbiology WashingtonViterbo, A., Haran, S., Friesem, D., Ramot, O., Chet, I., Antifungal activity of a novel endochitinase gene (chit36) from Trichoderma harzianum Rifai TM (2001) FEMS Microbiol. Lett., 200 (2), pp. 169-174Vos, C.M., De Cremer, K., Cammue, B.P., De Coninck, B., The toolbox of Trichoderma spp. in the biocontrol of Botrytis cinerea disease (2015) Mol. Plant Pathol., 16 (4), pp. 400-412Wibowo, A., Santosa, A.T., Subandiyah, S., Hermanto, C., Taylor, M.F.P., Control of Fusarium wilt of banana by using Trichoderma harzianum and resistant banana cultivars (2013) Acta Hortic., 975, pp. 173-177Woo, S.L., Scala, F., Ruocco, M., Lorito, M., The molecular biology of the interactions between Trichoderma spp., phytopathogenic fungi, and plants (2006) Phytopathology, 96, pp. 181-185Zeilinger, S., Gruber, S.G., Bansal, R., Mukherjee, P.K., Secondary metabolism in Trichoderma – chemistry meets genomics (2016) Fungal Biol. Rev., 30 (2), pp. 1-17Zhang, N., He, X., Zhang, J., Raza, W., Ling, N., Ruan, Y.-Z., Shen, Q.R., Huang, Q.W., Suppression of Fusarium wilt of banana with application of bio-organic fertilizers (2014) Pedosphere, 24 (5), pp. 613-624Zhang, X.Y., Hu, J., Zhou, H.Y., Hao, J.J., Xue, Y.F., Chen, H., Wang, B.G., First report of Fusarium oxysporum and F. solani causing Fusarium dry rot of carrot in China (2014) Plant Dis., 98 (9). , 1273–1273Zhu, Y., Lujan, P.A., Wedegaertner, T., Nichols, R., Abdelraheem, A., Zhang, J.F., Sanogo, S., First report of Fusarium oxysporum f. sp. vasinfectum Race 4 causing Fusarium wilt of cotton in New Mexico, U.S.A (2019) Plant Dis., 104 (2). , 588–588Biological ControlAntagonismBiological controlFusarium oxysporumMycoparasitismTrichoderma asperellumTrichoderma asperellum as a preventive and curative agent to control Fusarium wilt in Stevia rebaudianaArticleinfo:eu-repo/semantics/articlehttp://purl.org/coar/version/c_970fb48d4fbd8a85http://purl.org/coar/resource_type/c_6501http://purl.org/coar/resource_type/c_2df8fbb1Díaz-Gutiérrez, C., Interdisciplinary Group of Molecular Studies, Chemical Institute, Faculty of Exact and Natural Sciences, University of Antioquia, Medellin, 1226, ColombiaArroyave, C., Interdisciplinary Group of Molecular Studies, Chemical Institute, Faculty of Exact and Natural Sciences, University of Antioquia, Medellin, 1226, Colombia, Faculty of Engineer, University of Medellin, Medellin, 1983, ColombiaLlugany, M., Plant Physiology Laboratory, Biosciences Faculty, 08193, Autonomous University of Barcelona, Bellaterra (Cerdanyola del Vallès), Barcelona, SpainPoschenrieder, C., Plant Physiology Laboratory, Biosciences Faculty, 08193, Autonomous University of Barcelona, Bellaterra (Cerdanyola del Vallès), Barcelona, SpainMartos, S., Plant Physiology Laboratory, Biosciences Faculty, 08193, Autonomous University of Barcelona, Bellaterra (Cerdanyola del Vallès), Barcelona, SpainPeláez, C., Interdisciplinary Group of Molecular Studies, Chemical Institute, Faculty of Exact and Natural Sciences, University of Antioquia, Medellin, 1226, Colombiahttp://purl.org/coar/access_right/c_16ecDíaz-Gutiérrez C.Arroyave C.Llugany M.Poschenrieder C.Martos S.Peláez C.11407/5900oai:repository.udem.edu.co:11407/59002021-02-05 09:57:40.17Repositorio Institucional Universidad de Medellinrepositorio@udem.edu.co |