The NADPH Oxidase A of <i>Verticillium dahliae</i> Is Essential for Pathogenicity, Normal Development, and Stress Tolerance, and It Interacts with Yap1 to Regulate Redox Homeostasis
Maintenance of redox homeostasis is vital for aerobic organisms and particularly relevant to plant pathogens. A balance is required between their endogenous ROS production, which is important for their development and pathogenicity, and host-derived oxidative stress. Endogenous ROS in fungi are gene...
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| Format: | Article |
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MDPI AG
2021-09-01
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| Series: | Journal of Fungi |
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| Online Access: | https://www.mdpi.com/2309-608X/7/9/740 |
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| author | Vasileios Vangalis Ioannis A. Papaioannou Emmanouil A. Markakis Michael Knop Milton A. Typas |
| author_facet | Vasileios Vangalis Ioannis A. Papaioannou Emmanouil A. Markakis Michael Knop Milton A. Typas |
| author_sort | Vasileios Vangalis |
| collection | DOAJ |
| description | Maintenance of redox homeostasis is vital for aerobic organisms and particularly relevant to plant pathogens. A balance is required between their endogenous ROS production, which is important for their development and pathogenicity, and host-derived oxidative stress. Endogenous ROS in fungi are generated by membrane-bound NADPH oxidase (NOX) complexes and the mitochondrial respiratory chain, while transcription factor Yap1 is a major regulator of the antioxidant response. Here, we investigated the roles of NoxA and Yap1 in fundamental biological processes of the important plant pathogen <i>Verticillium dahliae</i>. Deletion of <i>noxA</i> impaired growth and morphogenesis, compromised formation of hyphopodia, diminished penetration ability and pathogenicity, increased sensitivity against antifungal agents, and dysregulated expression of antioxidant genes. On the other hand, deletion of <i>yap1</i> resulted in defects in conidial and microsclerotia formation, increased sensitivity against oxidative stress, and down-regulated antioxidant genes. Localized accumulation of ROS was observed before conidial fusion and during the heterokaryon incompatibility reaction upon nonself fusion. The frequency of inviable fusions was not affected by the deletion of Yap1. Analysis of a double knockout mutant revealed an epistatic relationship between <i>noxA</i> and <i>yap1</i>. Our results collectively reveal instrumental roles of NoxA and ROS homeostasis in the biology of <i>V. dahliae</i>. |
| first_indexed | 2024-03-10T07:31:56Z |
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| institution | Directory Open Access Journal |
| issn | 2309-608X |
| language | English |
| last_indexed | 2024-03-10T07:31:56Z |
| publishDate | 2021-09-01 |
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| series | Journal of Fungi |
| spelling | doaj.art-72e18e6f0f1a4c8c8d0669de94775d652023-11-22T13:48:15ZengMDPI AGJournal of Fungi2309-608X2021-09-017974010.3390/jof7090740The NADPH Oxidase A of <i>Verticillium dahliae</i> Is Essential for Pathogenicity, Normal Development, and Stress Tolerance, and It Interacts with Yap1 to Regulate Redox HomeostasisVasileios Vangalis0Ioannis A. Papaioannou1Emmanouil A. Markakis2Michael Knop3Milton A. Typas4Department of Genetics & Biotechnology, Faculty of Biology, National and Kapodistrian University of Athens, 15784 Athens, GreeceCenter for Molecular Biology of Heidelberg University (ZMBH), University of Heidelberg, 69120 Heidelberg, GermanyLaboratory of Mycology, Department of Viticulture, Vegetable Crops, Floriculture and Plant Protection, Institute of Olive Tree, Subtropical Crops and Viticulture, N.AG.RE.F., Hellenic Agricultural Organization-DIMITRA, 71307 Heraklion, Crete, GreeceCenter for Molecular Biology of Heidelberg University (ZMBH), University of Heidelberg, 69120 Heidelberg, GermanyDepartment of Genetics & Biotechnology, Faculty of Biology, National and Kapodistrian University of Athens, 15784 Athens, GreeceMaintenance of redox homeostasis is vital for aerobic organisms and particularly relevant to plant pathogens. A balance is required between their endogenous ROS production, which is important for their development and pathogenicity, and host-derived oxidative stress. Endogenous ROS in fungi are generated by membrane-bound NADPH oxidase (NOX) complexes and the mitochondrial respiratory chain, while transcription factor Yap1 is a major regulator of the antioxidant response. Here, we investigated the roles of NoxA and Yap1 in fundamental biological processes of the important plant pathogen <i>Verticillium dahliae</i>. Deletion of <i>noxA</i> impaired growth and morphogenesis, compromised formation of hyphopodia, diminished penetration ability and pathogenicity, increased sensitivity against antifungal agents, and dysregulated expression of antioxidant genes. On the other hand, deletion of <i>yap1</i> resulted in defects in conidial and microsclerotia formation, increased sensitivity against oxidative stress, and down-regulated antioxidant genes. Localized accumulation of ROS was observed before conidial fusion and during the heterokaryon incompatibility reaction upon nonself fusion. The frequency of inviable fusions was not affected by the deletion of Yap1. Analysis of a double knockout mutant revealed an epistatic relationship between <i>noxA</i> and <i>yap1</i>. Our results collectively reveal instrumental roles of NoxA and ROS homeostasis in the biology of <i>V. dahliae</i>.https://www.mdpi.com/2309-608X/7/9/740antioxidant responseconidial anastomosis tubes (CATs)heterokaryon incompatibilityoxidative stresspathogenicityreactive oxygen species (ROS) |
| spellingShingle | Vasileios Vangalis Ioannis A. Papaioannou Emmanouil A. Markakis Michael Knop Milton A. Typas The NADPH Oxidase A of <i>Verticillium dahliae</i> Is Essential for Pathogenicity, Normal Development, and Stress Tolerance, and It Interacts with Yap1 to Regulate Redox Homeostasis Journal of Fungi antioxidant response conidial anastomosis tubes (CATs) heterokaryon incompatibility oxidative stress pathogenicity reactive oxygen species (ROS) |
| title | The NADPH Oxidase A of <i>Verticillium dahliae</i> Is Essential for Pathogenicity, Normal Development, and Stress Tolerance, and It Interacts with Yap1 to Regulate Redox Homeostasis |
| title_full | The NADPH Oxidase A of <i>Verticillium dahliae</i> Is Essential for Pathogenicity, Normal Development, and Stress Tolerance, and It Interacts with Yap1 to Regulate Redox Homeostasis |
| title_fullStr | The NADPH Oxidase A of <i>Verticillium dahliae</i> Is Essential for Pathogenicity, Normal Development, and Stress Tolerance, and It Interacts with Yap1 to Regulate Redox Homeostasis |
| title_full_unstemmed | The NADPH Oxidase A of <i>Verticillium dahliae</i> Is Essential for Pathogenicity, Normal Development, and Stress Tolerance, and It Interacts with Yap1 to Regulate Redox Homeostasis |
| title_short | The NADPH Oxidase A of <i>Verticillium dahliae</i> Is Essential for Pathogenicity, Normal Development, and Stress Tolerance, and It Interacts with Yap1 to Regulate Redox Homeostasis |
| title_sort | nadph oxidase a of i verticillium dahliae i is essential for pathogenicity normal development and stress tolerance and it interacts with yap1 to regulate redox homeostasis |
| topic | antioxidant response conidial anastomosis tubes (CATs) heterokaryon incompatibility oxidative stress pathogenicity reactive oxygen species (ROS) |
| url | https://www.mdpi.com/2309-608X/7/9/740 |
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