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ZafA-mediated regulation of zinc homeostasis is required for virulence in the plant pathogen Fusarium oxysporum.

ABSTRACT: During infection, soilborne fungal pathogens face limiting conditions of different metal ions, including zinc. The role of zinc homeostasis in fungal pathogenicity on plants remains poorly understood. Here it is shown that the transcription factor ZafA, orthologous to Saccharomyces cerevisiae Zap1, functions as a key regulator of zinc homeostasis and virulence in Fusarium oxysporum, a cross-kingdom pathogen that causes vascular wilt on more than 100 plant species and opportunistic infections in humans. Expression of zafA is induced under zinc-limiting conditions and repressed by zinc. Interestingly, zafA is markedly up-regulated during early stages of plant infection, suggesting that F. oxysporum must cope with limited availability of zinc. Deletion of zafA results in deactivation of high-affinity zinc transporters, leading to impaired growth under zinc deficiency. Fusarium oxysporum strains lacking ZafA are reduced in their capability to invade and kill tomato plants and the non-vertebrate animal model Galleria mellonella. Collectively, the results indicate that ZafA-mediated adaptation to zinc deficiency is required for full virulence of F. oxysporum on plant and animal hosts.

SUBMITTER: Lopez-Berges MS

PROVIDER: S-EPMC6988419 | biostudies-literature | 2020 Feb

REPOSITORIES: biostudies-literature

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ZafA-mediated regulation of zinc homeostasis is required for virulence in the plant pathogen Fusarium oxysporum.

López-Berges Manuel S MS

Molecular plant pathology 20191121 2

During infection, soilborne fungal pathogens face limiting conditions of different metal ions, including zinc. The role of zinc homeostasis in fungal pathogenicity on plants remains poorly understood. Here it is shown that the transcription factor ZafA, orthologous to Saccharomyces cerevisiae Zap1, functions as a key regulator of zinc homeostasis and virulence in Fusarium oxysporum, a cross-kingdom pathogen that causes vascular wilt on more than 100 plant species and opportunistic infections in ...[more]

PMID: 31750619

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Project description:The regulation of intracellular levels of reactive oxygen species (ROS) is critical for developmental differentiation and virulence of many pathogenic fungi. In this report we demonstrate that a novel transmembrane protein, TmpL, is necessary for regulation of intracellular ROS levels and tolerance to external ROS, and is required for infection of plants by the necrotroph Alternaria brassicicola and for infection of mammals by the human pathogen Aspergillus fumigatus. In both fungi, tmpL encodes a predicted hybrid membrane protein containing an AMP-binding domain, six putative transmembrane domains, and an experimentally-validated FAD/NAD(P)-binding domain. Localization and gene expression analyses in A. brassicicola indicated that TmpL is associated with the Woronin body, a specialized peroxisome, and strongly expressed during conidiation and initial invasive growth in planta. A. brassicicola and A. fumigatus DeltatmpL strains exhibited abnormal conidiogenesis, accelerated aging, enhanced oxidative burst during conidiation, and hypersensitivity to oxidative stress when compared to wild-type or reconstituted strains. Moreover, A. brassicicola DeltatmpL strains, although capable of initial penetration, exhibited dramatically reduced invasive growth on Brassicas and Arabidopsis. Similarly, an A. fumigatus DeltatmpL mutant was dramatically less virulent than the wild-type and reconstituted strains in a murine model of invasive aspergillosis. Constitutive expression of the A. brassicicola yap1 ortholog in an A. brassicicola DeltatmpL strain resulted in high expression levels of genes associated with oxidative stress tolerance. Overexpression of yap1 in the DeltatmpL background complemented the majority of observed developmental phenotypic changes and partially restored virulence on plants. Yap1-GFP fusion strains utilizing the native yap1 promoter exhibited constitutive nuclear localization in the A. brassicicola DeltatmpL background. Collectively, we have discovered a novel protein involved in the virulence of both plant and animal fungal pathogens. Our results strongly suggest that dysregulation of oxidative stress homeostasis in the absence of TmpL is the underpinning cause of the developmental and virulence defects observed in these studies.

Dataset Information

ZafA-mediated regulation of zinc homeostasis is required for virulence in the plant pathogen Fusarium oxysporum.

Publications

ZafA-mediated regulation of zinc homeostasis is required for virulence in the plant pathogen Fusarium oxysporum.

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