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Metabolomic Analysis of Extracellular Vesicles from the Cereal Fungal Pathogen Fusarium graminearum

Fusarium graminearum (F. graminearum) is a filamentous fungus that infects cereals such as corn, wheat, and barley, with serious impact on yield as well as quality when the grain is contaminated with mycotoxins. Despite the huge impact of F. graminearum on food security and mammalian health, the mec...

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Autores principales: Garcia-Ceron, Donovan, Truong, Thy T., Ratcliffe, Julian, McKenna, James A., Bleackley, Mark R., Anderson, Marilyn A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10219060/
https://www.ncbi.nlm.nih.gov/pubmed/37233218
http://dx.doi.org/10.3390/jof9050507
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author Garcia-Ceron, Donovan
Truong, Thy T.
Ratcliffe, Julian
McKenna, James A.
Bleackley, Mark R.
Anderson, Marilyn A.
author_facet Garcia-Ceron, Donovan
Truong, Thy T.
Ratcliffe, Julian
McKenna, James A.
Bleackley, Mark R.
Anderson, Marilyn A.
author_sort Garcia-Ceron, Donovan
collection PubMed
description Fusarium graminearum (F. graminearum) is a filamentous fungus that infects cereals such as corn, wheat, and barley, with serious impact on yield as well as quality when the grain is contaminated with mycotoxins. Despite the huge impact of F. graminearum on food security and mammalian health, the mechanisms used by F. graminearum to export virulence factors during infection are not fully understood and may involve non-classical secretory pathways. Extracellular vesicles (EVs) are lipid-bound compartments produced by cells of all kingdoms that transport several classes of macromolecules and are implicated in cell–cell communication. EVs produced by human fungal pathogens carry cargo that facilitate infection, leading us to ask whether plant fungal pathogens also deliver molecules that increase virulence via EVs. We examined the metabolome of the EVs produced by F. graminearum to determine whether they carry small molecules that could modulate plant–pathogen interactions. We discovered that EVs from F. graminearum were produced in liquid medium-containing inducers of trichothecene production, but in lower quantities compared to other media. Nanoparticle tracking analysis and cryo-electron microscopy revealed that the EVs were morphologically similar to EVs from other organisms; hence, the EVs were metabolically profiled using LC-ESI-MS/MS. This analysis revealed that EVs carry 2,4-dihydroxybenzophenone (BP-1) and metabolites that have been suggested by others to have a role in host–pathogen interactions. BP-1 reduced the growth of F. graminearum in an in vitro assay, suggesting that F. graminearum might use EVs to limit metabolite self-toxicity.
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spelling pubmed-102190602023-05-27 Metabolomic Analysis of Extracellular Vesicles from the Cereal Fungal Pathogen Fusarium graminearum Garcia-Ceron, Donovan Truong, Thy T. Ratcliffe, Julian McKenna, James A. Bleackley, Mark R. Anderson, Marilyn A. J Fungi (Basel) Article Fusarium graminearum (F. graminearum) is a filamentous fungus that infects cereals such as corn, wheat, and barley, with serious impact on yield as well as quality when the grain is contaminated with mycotoxins. Despite the huge impact of F. graminearum on food security and mammalian health, the mechanisms used by F. graminearum to export virulence factors during infection are not fully understood and may involve non-classical secretory pathways. Extracellular vesicles (EVs) are lipid-bound compartments produced by cells of all kingdoms that transport several classes of macromolecules and are implicated in cell–cell communication. EVs produced by human fungal pathogens carry cargo that facilitate infection, leading us to ask whether plant fungal pathogens also deliver molecules that increase virulence via EVs. We examined the metabolome of the EVs produced by F. graminearum to determine whether they carry small molecules that could modulate plant–pathogen interactions. We discovered that EVs from F. graminearum were produced in liquid medium-containing inducers of trichothecene production, but in lower quantities compared to other media. Nanoparticle tracking analysis and cryo-electron microscopy revealed that the EVs were morphologically similar to EVs from other organisms; hence, the EVs were metabolically profiled using LC-ESI-MS/MS. This analysis revealed that EVs carry 2,4-dihydroxybenzophenone (BP-1) and metabolites that have been suggested by others to have a role in host–pathogen interactions. BP-1 reduced the growth of F. graminearum in an in vitro assay, suggesting that F. graminearum might use EVs to limit metabolite self-toxicity. MDPI 2023-04-24 /pmc/articles/PMC10219060/ /pubmed/37233218 http://dx.doi.org/10.3390/jof9050507 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Garcia-Ceron, Donovan
Truong, Thy T.
Ratcliffe, Julian
McKenna, James A.
Bleackley, Mark R.
Anderson, Marilyn A.
Metabolomic Analysis of Extracellular Vesicles from the Cereal Fungal Pathogen Fusarium graminearum
title Metabolomic Analysis of Extracellular Vesicles from the Cereal Fungal Pathogen Fusarium graminearum
title_full Metabolomic Analysis of Extracellular Vesicles from the Cereal Fungal Pathogen Fusarium graminearum
title_fullStr Metabolomic Analysis of Extracellular Vesicles from the Cereal Fungal Pathogen Fusarium graminearum
title_full_unstemmed Metabolomic Analysis of Extracellular Vesicles from the Cereal Fungal Pathogen Fusarium graminearum
title_short Metabolomic Analysis of Extracellular Vesicles from the Cereal Fungal Pathogen Fusarium graminearum
title_sort metabolomic analysis of extracellular vesicles from the cereal fungal pathogen fusarium graminearum
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10219060/
https://www.ncbi.nlm.nih.gov/pubmed/37233218
http://dx.doi.org/10.3390/jof9050507
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