Defects in the Ferroxidase That Participates in the Reductive Iron Assimilation System Results in Hypervirulence in <italic toggle="yes">Botrytis Cinerea</italic>

ABSTRACT The plant pathogen Botrytis cinerea is responsible for gray-mold disease, which infects a wide variety of species. The outcome of this host-pathogen interaction, a result of the interplay between plant defense and fungal virulence pathways, can be modulated by various environmental factors....

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Autores principales:	Esteban Vasquez-Montaño, Gustavo Hoppe, Andrea Vega, Consuelo Olivares-Yañez, Paulo Canessa
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Botrytis cinerea ferroxidase hypervirulence iron uptake multicopper oxidases reductive iron assimilation Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/80eae165186d4d7db9bc10aa4f497576
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spelling	oai:doaj.org-article:80eae165186d4d7db9bc10aa4f4975762021-11-15T15:56:44ZDefects in the Ferroxidase That Participates in the Reductive Iron Assimilation System Results in Hypervirulence in <italic toggle="yes">Botrytis Cinerea</italic>10.1128/mBio.01379-202150-7511https://doaj.org/article/80eae165186d4d7db9bc10aa4f4975762020-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01379-20https://doaj.org/toc/2150-7511ABSTRACT The plant pathogen Botrytis cinerea is responsible for gray-mold disease, which infects a wide variety of species. The outcome of this host-pathogen interaction, a result of the interplay between plant defense and fungal virulence pathways, can be modulated by various environmental factors. Among these, iron availability and acquisition play a crucial role in diverse biological functions. How B. cinerea obtains iron, an essential micronutrient, during infection is unknown. We set out to determine the role of the reductive iron assimilation (RIA) system during B. cinerea infection. This system comprises the BcFET1 ferroxidase, which belongs to the multicopper oxidase (MCO) family of proteins, and the BcFTR1 membrane-bound iron permease. Gene knockout and complementation studies revealed that, compared to the wild type, the bcfet1 mutant displays delayed conidiation, iron-dependent sclerotium production, and significantly reduced whole-cell iron content. Remarkably, this mutant exhibited a hypervirulence phenotype, whereas the bcftr1 mutant presents normal virulence and unaffected whole-cell iron levels and developmental programs. Interestingly, while in iron-starved plants wild-type B. cinerea produced slightly reduced necrotic lesions, the hypervirulence phenotype of the bcfet1 mutant is no longer observed in iron-deprived plants. This suggests that B. cinerea bcfet1 knockout mutants require plant-derived iron to achieve larger necrotic lesions, whereas in planta analyses of reactive oxygen species (ROS) revealed increased ROS levels only for infections caused by the bcfet1 mutant. These results suggest that increased ROS production, under an iron sufficiency environment, at least partly underlie the observed infection phenotype in this mutant. IMPORTANCE The plant-pathogenic fungus B. cinerea causes enormous economic losses, estimated at anywhere between $10 billion and $100 billion worldwide, under both pre- and postharvest conditions. Here, we present the characterization of a loss-of-function mutant in a component involved in iron acquisition that displays hypervirulence. While in different microbial systems iron uptake mechanisms appear to be critical to achieve full pathogenic potential, we found that the absence of the ferroxidase that is part of the reductive iron assimilation system leads to hypervirulence in this fungus. This is an unusual and rather underrepresented phenotype, which can be modulated by iron levels in the plant and provides an unexpected link between iron acquisition, reactive oxygen species (ROS) production, and pathogenesis in the Botrytis-plant interaction.Esteban Vasquez-MontañoGustavo HoppeAndrea VegaConsuelo Olivares-YañezPaulo CanessaAmerican Society for MicrobiologyarticleBotrytis cinereaferroxidasehypervirulenceiron uptakemulticopper oxidasesreductive iron assimilationMicrobiologyQR1-502ENmBio, Vol 11, Iss 4 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Botrytis cinerea ferroxidase hypervirulence iron uptake multicopper oxidases reductive iron assimilation Microbiology QR1-502
spellingShingle	Botrytis cinerea ferroxidase hypervirulence iron uptake multicopper oxidases reductive iron assimilation Microbiology QR1-502 Esteban Vasquez-Montaño Gustavo Hoppe Andrea Vega Consuelo Olivares-Yañez Paulo Canessa Defects in the Ferroxidase That Participates in the Reductive Iron Assimilation System Results in Hypervirulence in <italic toggle="yes">Botrytis Cinerea</italic>
description	ABSTRACT The plant pathogen Botrytis cinerea is responsible for gray-mold disease, which infects a wide variety of species. The outcome of this host-pathogen interaction, a result of the interplay between plant defense and fungal virulence pathways, can be modulated by various environmental factors. Among these, iron availability and acquisition play a crucial role in diverse biological functions. How B. cinerea obtains iron, an essential micronutrient, during infection is unknown. We set out to determine the role of the reductive iron assimilation (RIA) system during B. cinerea infection. This system comprises the BcFET1 ferroxidase, which belongs to the multicopper oxidase (MCO) family of proteins, and the BcFTR1 membrane-bound iron permease. Gene knockout and complementation studies revealed that, compared to the wild type, the bcfet1 mutant displays delayed conidiation, iron-dependent sclerotium production, and significantly reduced whole-cell iron content. Remarkably, this mutant exhibited a hypervirulence phenotype, whereas the bcftr1 mutant presents normal virulence and unaffected whole-cell iron levels and developmental programs. Interestingly, while in iron-starved plants wild-type B. cinerea produced slightly reduced necrotic lesions, the hypervirulence phenotype of the bcfet1 mutant is no longer observed in iron-deprived plants. This suggests that B. cinerea bcfet1 knockout mutants require plant-derived iron to achieve larger necrotic lesions, whereas in planta analyses of reactive oxygen species (ROS) revealed increased ROS levels only for infections caused by the bcfet1 mutant. These results suggest that increased ROS production, under an iron sufficiency environment, at least partly underlie the observed infection phenotype in this mutant. IMPORTANCE The plant-pathogenic fungus B. cinerea causes enormous economic losses, estimated at anywhere between $10 billion and $100 billion worldwide, under both pre- and postharvest conditions. Here, we present the characterization of a loss-of-function mutant in a component involved in iron acquisition that displays hypervirulence. While in different microbial systems iron uptake mechanisms appear to be critical to achieve full pathogenic potential, we found that the absence of the ferroxidase that is part of the reductive iron assimilation system leads to hypervirulence in this fungus. This is an unusual and rather underrepresented phenotype, which can be modulated by iron levels in the plant and provides an unexpected link between iron acquisition, reactive oxygen species (ROS) production, and pathogenesis in the Botrytis-plant interaction.
format	article
author	Esteban Vasquez-Montaño Gustavo Hoppe Andrea Vega Consuelo Olivares-Yañez Paulo Canessa
author_facet	Esteban Vasquez-Montaño Gustavo Hoppe Andrea Vega Consuelo Olivares-Yañez Paulo Canessa
author_sort	Esteban Vasquez-Montaño
title	Defects in the Ferroxidase That Participates in the Reductive Iron Assimilation System Results in Hypervirulence in <italic toggle="yes">Botrytis Cinerea</italic>
title_short	Defects in the Ferroxidase That Participates in the Reductive Iron Assimilation System Results in Hypervirulence in <italic toggle="yes">Botrytis Cinerea</italic>
title_full	Defects in the Ferroxidase That Participates in the Reductive Iron Assimilation System Results in Hypervirulence in <italic toggle="yes">Botrytis Cinerea</italic>
title_fullStr	Defects in the Ferroxidase That Participates in the Reductive Iron Assimilation System Results in Hypervirulence in <italic toggle="yes">Botrytis Cinerea</italic>
title_full_unstemmed	Defects in the Ferroxidase That Participates in the Reductive Iron Assimilation System Results in Hypervirulence in <italic toggle="yes">Botrytis Cinerea</italic>
title_sort	defects in the ferroxidase that participates in the reductive iron assimilation system results in hypervirulence in <italic toggle="yes">botrytis cinerea</italic>
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/80eae165186d4d7db9bc10aa4f497576
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Defects in the Ferroxidase That Participates in the Reductive Iron Assimilation System Results in Hypervirulence in <italic toggle="yes">Botrytis Cinerea</italic>

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