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

Antonio Mulero-Aparicio,Tomislav Cernava,David Turrà,Angelika Schaefer,Antonio Di Pietro,Antonio Trapero,Gabriele Berg,Francisco Javier López-Escudero

doi:10.3389/fmicb.2019.01808

Antonio Mulero-Aparicio, Tomislav Cernava + Show 6 more

Open Access

https://doi.org/10.3389/fmicb.2019.01808

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Abstract

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.

Highlights

Verticillium species are generally widely distributed in soil, and are common plant endophytes (Pegg and Brady, 2002; Barbara and Clewes, 2003; Klosterman et al, 2009)
The effect of volatile organic compounds (VOCs) emitted by F. oxysporum FO12 and FO12sGFP on mycelial growth of different Verticillium isolates was assessed in co-incubation experiments
The effectiveness of VOCs emitted by F. oxysporum FO12 and FO12-super-folder green fluorescent protein (sGFP) against mycelial growth of Verticillium isolates was similar and no significant differences were found between the strains

Summary

Introduction

Verticillium species are generally widely distributed in soil, and are common plant endophytes (Pegg and Brady, 2002; Barbara and Clewes, 2003; Klosterman et al, 2009). Distinct Verticillium species represent a devastating group of plant pathogens that cause wilt disease in a large number of hosts worldwide. Increasing soil temperatures due to global warming further aggravate their capacity to infect host plants (Tjamos et al, 2000) Changes in their genomes resulting from interkingdom horizontal events have enhanced their adaptability and pathogenicity (Shi-Kunne et al, 2019). These pathogenic species cause losses in many herbaceous and woody crops with important economic impact (Hiemstra, 1998; Pegg and Brady, 2002). In Spain, a disease occurrence of 39% in affected orchards was reported in the last decades (BlancoLópez et al, 1984; Sánchez-Hernández et al, 1998)

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