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A functional analysis of mitochondrial respiratory chain cytochrome bc₁ complex in Gaeumannomyces tritici by RNA silencing as a possible target of carabrone.

ABSTRACT: Gaeumannomyces tritici, an ascomycete soilborne fungus, causes a devastating root disease in wheat. Carabrone, a botanical bicyclic sesquiterpenic lactone, is a promising fungicidal agent that can effectively control G. tritici. However, the mechanism of action of carabrone against G. tritici remains largely unclear. Here, we used immunogold for subcellular localization of carabrone and the results showed that carabrone is subcellularly localized in the mitochondria of G. tritici. We then explored the functional analysis of genes GtCytc₁ , GtCytb, and GtIsp of the mitochondrial respiratory chain cytochrome bc₁ complex in G. tritici by RNA silencing as a possible target of carabrone. The results showed that the silenced mutant ?GtIsp is less sensitive to carabrone compared to ?GtCytc₁ and ?GtCytb. Compared with the control, the activities of complex III in all the strains, except ?GtIsp and carabrone-resistant isolate 24-HN-1, were significantly decreased following treatment with carabrone at EC₂₀ and EC₈₀ in vitro (40%-50% and 70%-80%, respectively). The activities of mitochondrial respiratory chain complex III and the mitochondrial respiration oxygen consumption rates in all the strains, except ?GtIsp and 24-HN-1, were higher with respect to the control when treated with carabrone at EC₂₀ in vivo. The rates of mitochondrial respiration of all strains, except ?GtIsp, were significantly inhibited following treatment with carabrone at EC₈₀ (ranging from 57% to 81%). This study reveals that the targeting of the iron-sulphur protein encoded by GtIsp is highly sensitive to carabrone and provides a direction for the research of carabrone's target.

SUBMITTER: Wang M

PROVIDER: S-EPMC7694678 | biostudies-literature | 2020 Dec

REPOSITORIES: biostudies-literature

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A functional analysis of mitochondrial respiratory chain cytochrome bc<sub>1</sub> complex in Gaeumannomyces tritici by RNA silencing as a possible target of carabrone.

Wang Mei M Ren Xingyu X Wang Lanying L Lu Xiang X Han Lirong L Zhang Xing X Feng Juntao J

Molecular plant pathology 20200930 12

Gaeumannomyces tritici, an ascomycete soilborne fungus, causes a devastating root disease in wheat. Carabrone, a botanical bicyclic sesquiterpenic lactone, is a promising fungicidal agent that can effectively control G. tritici. However, the mechanism of action of carabrone against G. tritici remains largely unclear. Here, we used immunogold for subcellular localization of carabrone and the results showed that carabrone is subcellularly localized in the mitochondria of G. tritici. We then explor ...[more]

PMID: 32997435

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Project description:Gaeumannomyces graminis var. tritici is a soilborne pathogen that causes "take-all" disease, affecting cereal roots. In wheat, G. graminis var. tritici is the most important biotic factor, causing around 30 to 50% losses of yield. Chemical control of this fungal disease is difficult because G. graminis var. tritici is able to reside for a long time in soils. Therefore, the development of environmentally friendly biotechnological strategies to diminish the incidence of soilborne diseases is highly desirable. Natural products are a promising strategy for biocontrol of plant pathogens. A special emphasis is on medicinal plants due to their reported fungitoxic effects. Drimys winteri (canelo) is a medicinal plant that is widely used by the Mapuche ethnic group from Chile due to its anti-inflammatory activity. In addition, inhibitory effects of canelo against phytopathogenic fungi and pest insects have been reported. In this study, we isolated, purified, and identified six drimane sesquiterpenoid compounds from canelo (drimenin, drimenol, polygodial, isodrimeninol, valdiviolide, and drimendiol). Then, we evaluated their antimicrobial effects against G. graminis var. tritici. Compounds were identified by comparing Fourier-transform infrared spectroscopy (FTIR) data and the retention time in thin-layer chromatography (TLC) with those of pure standards. The putative antagonistic effects were confirmed by assessing hyphal cell wall damage using confocal microscopy and lipid peroxidation. Here, we reported the high potential of drimane sesquiterpenoids as natural antifungals against G. graminis var. tritici. Polygodial and isodrimeninol were the most effective, with 50% lethal concentrations (LC50s) between 7 and 10 μg ml-1 and higher levels of fungal lipid peroxidation seen. Accordingly, natural sesquiterpenoids purified from canelo are biologically active against G. graminis var. tritici and could be used as natural biofungicides for sustainable agriculture.IMPORTANCE More than two billion tons of pesticides are used every year worldwide. An interesting sustainable alternative to control plant pathogens is the use of natural products obtained from plants, mainly medicinal plants that offer secondary metabolites important to human/animal health. In this study, we isolated and identified six pure drimane sesquiterpenoids obtained from the bark of Drimys winteri Additionally, we evaluated their antifungal activities against Gaeumannomyces graminis (the main biotic factor affecting cereal production, especially wheat) by assessing fungal cell wall damage and lipid peroxidation. The compounds obtained showed important antifungal properties against G. graminis var. tritici, mainly isodrimenol, which was the second-most-active compound after polygodial, with an LC50 against G. graminis var. tritici of around 9.5 μg ml-1 This information could be useful for the development of new natural or hemisynthetic antifungal agents against soilborne phytopathogens that could be used in green agriculture.

Dataset Information

A functional analysis of mitochondrial respiratory chain cytochrome bc1 complex in Gaeumannomyces tritici by RNA silencing as a possible target of carabrone.

Publications

A functional analysis of mitochondrial respiratory chain cytochrome bc<sub>1</sub> complex in Gaeumannomyces tritici by RNA silencing as a possible target of carabrone.

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A functional analysis of mitochondrial respiratory chain cytochrome bc₁ complex in Gaeumannomyces tritici by RNA silencing as a possible target of carabrone.