Biocontrol and plant growth promoting traits of two avocado rhizobacteria are orchestrated by the emission of diffusible and volatile compounds

Avocado (Persea americana Mill.) is a tree crop of great social and economic importance. However, the crop productivity is hindered by fast-spreading diseases, which calls for the search of new biocontrol alternatives to mitigate the impact of avocado phytopathogens. Our objectives were to evaluate...

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Main Authors: Elvis M. Cortazar-Murillo, Alfonso Méndez-Bravo, Juan L. Monribot-Villanueva, Edith Garay-Serrano, Ana L. Kiel-Martínez, Mónica Ramírez-Vázquez, Edgar Guevara-Avendaño, Alejandro Méndez-Bravo, José A. Guerrero-Analco, Frédérique Reverchon
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-05-01
Series:Frontiers in Microbiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1152597/full
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author Elvis M. Cortazar-Murillo
Alfonso Méndez-Bravo
Juan L. Monribot-Villanueva
Edith Garay-Serrano
Ana L. Kiel-Martínez
Mónica Ramírez-Vázquez
Mónica Ramírez-Vázquez
Edgar Guevara-Avendaño
Alejandro Méndez-Bravo
José A. Guerrero-Analco
Frédérique Reverchon
author_facet Elvis M. Cortazar-Murillo
Alfonso Méndez-Bravo
Juan L. Monribot-Villanueva
Edith Garay-Serrano
Ana L. Kiel-Martínez
Mónica Ramírez-Vázquez
Mónica Ramírez-Vázquez
Edgar Guevara-Avendaño
Alejandro Méndez-Bravo
José A. Guerrero-Analco
Frédérique Reverchon
author_sort Elvis M. Cortazar-Murillo
collection DOAJ
description Avocado (Persea americana Mill.) is a tree crop of great social and economic importance. However, the crop productivity is hindered by fast-spreading diseases, which calls for the search of new biocontrol alternatives to mitigate the impact of avocado phytopathogens. Our objectives were to evaluate the antimicrobial activity of diffusible and volatile organic compounds (VOCs) produced by two avocado rhizobacteria (Bacillus A8a and HA) against phytopathogens Fusarium solani, Fusarium kuroshium, and Phytophthora cinnamomi, and assess their plant growth promoting effect in Arabidopsis thaliana. We found that, in vitro, VOCs emitted by both bacterial strains inhibited mycelial growth of the tested pathogens by at least 20%. Identification of bacterial VOCs by gas chromatography coupled to mass spectrometry (GC–MS) showed a predominance of ketones, alcohols and nitrogenous compounds, previously reported for their antimicrobial activity. Bacterial organic extracts obtained with ethyl acetate significantly reduced mycelial growth of F. solani, F. kuroshium, and P. cinnamomi, the highest inhibition being displayed by those from strain A8a (32, 77, and 100% inhibition, respectively). Tentative identifications carried out by liquid chromatography coupled to accurate mass spectrometry of diffusible metabolites in the bacterial extracts, evidenced the presence of some polyketides such as macrolactins and difficidin, hybrid peptides including bacillaene, and non-ribosomal peptides such as bacilysin, which have also been described in Bacillus spp. for antimicrobial activities. The plant growth regulator indole-3-acetic acid was also identified in the bacterial extracts. In vitro assays showed that VOCs from strain HA and diffusible compounds from strain A8a modified root development and increased fresh weight of A. thaliana. These compounds differentially activated several hormonal signaling pathways involved in development and defense responses in A. thaliana, such as auxin, jasmonic acid (JA) and salicylic acid (SA); genetic analyses suggested that developmental stimulation of the root system architecture by strain A8a was mediated by the auxin signaling pathway. Furthermore, both strains were able to enhance plant growth and decreased the symptoms of Fusarium wilt in A. thaliana when soil-inoculated. Collectively, our results evidence the potential of these two rhizobacterial strains and their metabolites as biocontrol agents of avocado pathogens and as biofertilizers.
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spelling doaj.art-7ece8ee4372d4e3c85ea02553fbe1e152023-05-03T05:23:20ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-05-011410.3389/fmicb.2023.11525971152597Biocontrol and plant growth promoting traits of two avocado rhizobacteria are orchestrated by the emission of diffusible and volatile compoundsElvis M. Cortazar-Murillo0Alfonso Méndez-Bravo1Juan L. Monribot-Villanueva2Edith Garay-Serrano3Ana L. Kiel-Martínez4Mónica Ramírez-Vázquez5Mónica Ramírez-Vázquez6Edgar Guevara-Avendaño7Alejandro Méndez-Bravo8José A. Guerrero-Analco9Frédérique Reverchon10Red de Estudios Moleculares Avanzados, Instituto de Ecología, A.C., Xalapa, Veracruz, MexicoCONACyT – Escuela Nacional de Estudios Superiores, Unidad Morelia, Laboratorio Nacional de Análisis y Síntesis Ecológica, Universidad Nacional Autónoma de México, Morelia, Michoacán, MexicoRed de Estudios Moleculares Avanzados, Instituto de Ecología, A.C., Xalapa, Veracruz, MexicoCONACyT – Red de Diversidad Biológica del Occidente Mexicano, Centro Regional del Bajío, Instituto de Ecología, A.C., Pátzcuaro, Michoacán, MexicoRed de Estudios Moleculares Avanzados, Instituto de Ecología, A.C., Xalapa, Veracruz, MexicoRed de Estudios Moleculares Avanzados, Instituto de Ecología, A.C., Xalapa, Veracruz, MexicoFacultad de Medicina, Universidad Nacional Autónoma de México, Ciudad de México, MexicoRed de Estudios Moleculares Avanzados, Instituto de Ecología, A.C., Xalapa, Veracruz, MexicoEscuela Nacional de Estudios Superiores Unidad Morelia, Laboratorio Nacional de Análisis y Síntesis Ecológica, Universidad Nacional Autónoma de México, Morelia, MexicoRed de Estudios Moleculares Avanzados, Instituto de Ecología, A.C., Xalapa, Veracruz, MexicoRed de Diversidad Biológica del Occidente Mexicano, Centro Regional del Bajío, Instituto de Ecología, A.C., Pátzcuaro, Michoacán, MexicoAvocado (Persea americana Mill.) is a tree crop of great social and economic importance. However, the crop productivity is hindered by fast-spreading diseases, which calls for the search of new biocontrol alternatives to mitigate the impact of avocado phytopathogens. Our objectives were to evaluate the antimicrobial activity of diffusible and volatile organic compounds (VOCs) produced by two avocado rhizobacteria (Bacillus A8a and HA) against phytopathogens Fusarium solani, Fusarium kuroshium, and Phytophthora cinnamomi, and assess their plant growth promoting effect in Arabidopsis thaliana. We found that, in vitro, VOCs emitted by both bacterial strains inhibited mycelial growth of the tested pathogens by at least 20%. Identification of bacterial VOCs by gas chromatography coupled to mass spectrometry (GC–MS) showed a predominance of ketones, alcohols and nitrogenous compounds, previously reported for their antimicrobial activity. Bacterial organic extracts obtained with ethyl acetate significantly reduced mycelial growth of F. solani, F. kuroshium, and P. cinnamomi, the highest inhibition being displayed by those from strain A8a (32, 77, and 100% inhibition, respectively). Tentative identifications carried out by liquid chromatography coupled to accurate mass spectrometry of diffusible metabolites in the bacterial extracts, evidenced the presence of some polyketides such as macrolactins and difficidin, hybrid peptides including bacillaene, and non-ribosomal peptides such as bacilysin, which have also been described in Bacillus spp. for antimicrobial activities. The plant growth regulator indole-3-acetic acid was also identified in the bacterial extracts. In vitro assays showed that VOCs from strain HA and diffusible compounds from strain A8a modified root development and increased fresh weight of A. thaliana. These compounds differentially activated several hormonal signaling pathways involved in development and defense responses in A. thaliana, such as auxin, jasmonic acid (JA) and salicylic acid (SA); genetic analyses suggested that developmental stimulation of the root system architecture by strain A8a was mediated by the auxin signaling pathway. Furthermore, both strains were able to enhance plant growth and decreased the symptoms of Fusarium wilt in A. thaliana when soil-inoculated. Collectively, our results evidence the potential of these two rhizobacterial strains and their metabolites as biocontrol agents of avocado pathogens and as biofertilizers.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1152597/fullantifungal polyketidesauxin signalingBacillusFusarium spp.Phytophthora cinnamomi
spellingShingle Elvis M. Cortazar-Murillo
Alfonso Méndez-Bravo
Juan L. Monribot-Villanueva
Edith Garay-Serrano
Ana L. Kiel-Martínez
Mónica Ramírez-Vázquez
Mónica Ramírez-Vázquez
Edgar Guevara-Avendaño
Alejandro Méndez-Bravo
José A. Guerrero-Analco
Frédérique Reverchon
Biocontrol and plant growth promoting traits of two avocado rhizobacteria are orchestrated by the emission of diffusible and volatile compounds
Frontiers in Microbiology
antifungal polyketides
auxin signaling
Bacillus
Fusarium spp.
Phytophthora cinnamomi
title Biocontrol and plant growth promoting traits of two avocado rhizobacteria are orchestrated by the emission of diffusible and volatile compounds
title_full Biocontrol and plant growth promoting traits of two avocado rhizobacteria are orchestrated by the emission of diffusible and volatile compounds
title_fullStr Biocontrol and plant growth promoting traits of two avocado rhizobacteria are orchestrated by the emission of diffusible and volatile compounds
title_full_unstemmed Biocontrol and plant growth promoting traits of two avocado rhizobacteria are orchestrated by the emission of diffusible and volatile compounds
title_short Biocontrol and plant growth promoting traits of two avocado rhizobacteria are orchestrated by the emission of diffusible and volatile compounds
title_sort biocontrol and plant growth promoting traits of two avocado rhizobacteria are orchestrated by the emission of diffusible and volatile compounds
topic antifungal polyketides
auxin signaling
Bacillus
Fusarium spp.
Phytophthora cinnamomi
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1152597/full
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