The Role of Volatile Organic Compounds and Rhizosphere Competence in Mode of Action of the Non-pathogenic Fusarium oxysporum FO12 Toward Verticillium Wilt

Verticillium wilts caused by Verticillium spp. are among the most challenging plant diseases to control and affect numerous hosts worldwide. Due to the lack of effective, conventional control methods, integrated control strategies provide a promising approach to manage these diseases. The non-pathog...

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Main Authors: Antonio Mulero-Aparicio, Tomislav Cernava, David Turrà, Angelika Schaefer, Antonio Di Pietro, Francisco Javier López-Escudero, Antonio Trapero, Gabriele Berg
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-08-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2019.01808/full
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author Antonio Mulero-Aparicio
Antonio Mulero-Aparicio
Tomislav Cernava
David Turrà
Angelika Schaefer
Antonio Di Pietro
Francisco Javier López-Escudero
Antonio Trapero
Gabriele Berg
author_facet Antonio Mulero-Aparicio
Antonio Mulero-Aparicio
Tomislav Cernava
David Turrà
Angelika Schaefer
Antonio Di Pietro
Francisco Javier López-Escudero
Antonio Trapero
Gabriele Berg
author_sort Antonio Mulero-Aparicio
collection DOAJ
description Verticillium wilts caused by Verticillium spp. are among the most challenging plant diseases to control and affect numerous hosts worldwide. Due to the lack of effective, conventional control methods, integrated control strategies provide a promising approach to manage these diseases. The non-pathogenic Fusarium oxysporum strain FO12 was reported in previous studies to be an effective biocontrol agent against Verticillium dahliae, however, its mode of action remains to be elucidated. In this study, complementary in vitro and in vivo experiments were conducted in order to explore the implications of inhibitory substances and rhizosphere competence in antagonistic effects of FO12 against V. dahliae and V. longisporum. Volatile organic compounds and soluble substances produced by FO12, which caused significant inhibition of mycelial growth and microsclerotia viability in the two tested Verticillium species, were identified by means of gas and liquid chromatography-mass spectrometry. We showed that the antagonistic effect of F. oxysporum FO12 is partially due to the production of bioactive compounds such as 3-methyl-1-butanol and 2-methyl-1-butanol, among others. Several metabolic pathways of FO12 were altered upon contact with V. dahliae ELV22 volatiles. The reduced production of alpha, alpha-trehalose, a metabolite used in starch and sucrose metabolism, suggests that the biocontrol agent activates its stress response in the presence of the phytopathogen. Microscopic analysis using sGFP-tagged FO12 on oil seed rape as a model plant suggests that the biocontrol strain is an efficient root colonizer, which could compete with V. dahliae in the same ecological niche. The findings obtained in this study provide new insights into the mode of action of this potential biocontrol agent, which are relevant for controlling Verticillium wilt through an ecologically friendly approach.
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spelling doaj.art-148aafd9ef18496fb7a333519e27faac2022-12-21T23:15:51ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-08-011010.3389/fmicb.2019.01808468375The Role of Volatile Organic Compounds and Rhizosphere Competence in Mode of Action of the Non-pathogenic Fusarium oxysporum FO12 Toward Verticillium WiltAntonio Mulero-Aparicio0Antonio Mulero-Aparicio1Tomislav Cernava2David Turrà3Angelika Schaefer4Antonio Di Pietro5Francisco Javier López-Escudero6Antonio Trapero7Gabriele Berg8Grupo de Patología Agroforestal, Escuela Técnica Superior de Ingenieros Agrónomos y de Montes, Departamento de Agronomía, Universidad de Córdoba, Córdoba, SpainInstitute of Environmental Biotechnology, Graz University of Technology, Graz, AustriaInstitute of Environmental Biotechnology, Graz University of Technology, Graz, AustriaDepartamento de Genética, Campus de Excelencia Internacional Agroalimentario (ceiA3), Universidad de Córdoba, Córdoba, SpainInstitute of Environmental Biotechnology, Graz University of Technology, Graz, AustriaDepartamento de Genética, Campus de Excelencia Internacional Agroalimentario (ceiA3), Universidad de Córdoba, Córdoba, SpainGrupo de Patología Agroforestal, Escuela Técnica Superior de Ingenieros Agrónomos y de Montes, Departamento de Agronomía, Universidad de Córdoba, Córdoba, SpainGrupo de Patología Agroforestal, Escuela Técnica Superior de Ingenieros Agrónomos y de Montes, Departamento de Agronomía, Universidad de Córdoba, Córdoba, SpainInstitute of Environmental Biotechnology, Graz University of Technology, Graz, AustriaVerticillium wilts caused by Verticillium spp. are among the most challenging plant diseases to control and affect numerous hosts worldwide. Due to the lack of effective, conventional control methods, integrated control strategies provide a promising approach to manage these diseases. The non-pathogenic Fusarium oxysporum strain FO12 was reported in previous studies to be an effective biocontrol agent against Verticillium dahliae, however, its mode of action remains to be elucidated. In this study, complementary in vitro and in vivo experiments were conducted in order to explore the implications of inhibitory substances and rhizosphere competence in antagonistic effects of FO12 against V. dahliae and V. longisporum. Volatile organic compounds and soluble substances produced by FO12, which caused significant inhibition of mycelial growth and microsclerotia viability in the two tested Verticillium species, were identified by means of gas and liquid chromatography-mass spectrometry. We showed that the antagonistic effect of F. oxysporum FO12 is partially due to the production of bioactive compounds such as 3-methyl-1-butanol and 2-methyl-1-butanol, among others. Several metabolic pathways of FO12 were altered upon contact with V. dahliae ELV22 volatiles. The reduced production of alpha, alpha-trehalose, a metabolite used in starch and sucrose metabolism, suggests that the biocontrol agent activates its stress response in the presence of the phytopathogen. Microscopic analysis using sGFP-tagged FO12 on oil seed rape as a model plant suggests that the biocontrol strain is an efficient root colonizer, which could compete with V. dahliae in the same ecological niche. The findings obtained in this study provide new insights into the mode of action of this potential biocontrol agent, which are relevant for controlling Verticillium wilt through an ecologically friendly approach.https://www.frontiersin.org/article/10.3389/fmicb.2019.01808/fullanti-fungal volatilesbiological controlmode of actionVerticillium wiltmVOCs
spellingShingle Antonio Mulero-Aparicio
Antonio Mulero-Aparicio
Tomislav Cernava
David Turrà
Angelika Schaefer
Antonio Di Pietro
Francisco Javier López-Escudero
Antonio Trapero
Gabriele Berg
The Role of Volatile Organic Compounds and Rhizosphere Competence in Mode of Action of the Non-pathogenic Fusarium oxysporum FO12 Toward Verticillium Wilt
Frontiers in Microbiology
anti-fungal volatiles
biological control
mode of action
Verticillium wilt
mVOCs
title The Role of Volatile Organic Compounds and Rhizosphere Competence in Mode of Action of the Non-pathogenic Fusarium oxysporum FO12 Toward Verticillium Wilt
title_full The Role of Volatile Organic Compounds and Rhizosphere Competence in Mode of Action of the Non-pathogenic Fusarium oxysporum FO12 Toward Verticillium Wilt
title_fullStr The Role of Volatile Organic Compounds and Rhizosphere Competence in Mode of Action of the Non-pathogenic Fusarium oxysporum FO12 Toward Verticillium Wilt
title_full_unstemmed The Role of Volatile Organic Compounds and Rhizosphere Competence in Mode of Action of the Non-pathogenic Fusarium oxysporum FO12 Toward Verticillium Wilt
title_short The Role of Volatile Organic Compounds and Rhizosphere Competence in Mode of Action of the Non-pathogenic Fusarium oxysporum FO12 Toward Verticillium Wilt
title_sort role of volatile organic compounds and rhizosphere competence in mode of action of the non pathogenic fusarium oxysporum fo12 toward verticillium wilt
topic anti-fungal volatiles
biological control
mode of action
Verticillium wilt
mVOCs
url https://www.frontiersin.org/article/10.3389/fmicb.2019.01808/full
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