Hex1, the Major Component of Woronin Bodies, Is Required for Normal Development, Pathogenicity, and Stress Response in the Plant Pathogenic Fungus <i>Verticillium dahliae</i>

Woronin bodies are membrane-bound organelles of filamentous ascomycetes that mediate hyphal compartmentalization by plugging septal pores upon hyphal damage. Their major component is the peroxisomal protein Hex1, which has also been implicated in additional cellular processes in fungi. Here, we anal...

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Main Authors: Vasileios Vangalis, Ioannis A. Papaioannou, Emmanouil A. Markakis, Michael Knop, Milton A. Typas
Format: Article
Language:English
Published: MDPI AG 2020-12-01
Series:Journal of Fungi
Subjects:
Online Access:https://www.mdpi.com/2309-608X/6/4/344
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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 Woronin bodies are membrane-bound organelles of filamentous ascomycetes that mediate hyphal compartmentalization by plugging septal pores upon hyphal damage. Their major component is the peroxisomal protein Hex1, which has also been implicated in additional cellular processes in fungi. Here, we analyzed the Hex1 homolog of <i>Verticillium dahliae</i>, an important asexual plant pathogen, and we report its pleiotropic involvement in fungal growth, physiology, stress response, and pathogenicity. Alternative splicing of the <i>Vdhex1</i> gene can lead to the production of two Hex1 isoforms, which are structurally similar to their <i>Neurospora crassa</i> homolog. We show that <i>Vd</i>Hex1 is targeted to the septum, consistently with its demonstrated function in sealing hyphal compartments to prevent excessive cytoplasmic bleeding upon injury. Furthermore, our investigation provides direct evidence for significant contributions of Hex1 in growth and morphogenesis, as well as in asexual reproduction capacity. We discovered that Hex1 is required both for normal responses to osmotic stress and factors that affect the cell wall and plasma-membrane integrity, and for normal resistance to oxidative stress and reactive oxygen species (ROS) homeostasis. The <i>Vdhex1</i> mutant exhibited diminished ability to colonize and cause disease on eggplant. Overall, we show that Hex1 has fundamentally important multifaceted roles in the biology of <i>V. dahliae</i>.
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spelling doaj.art-04f9b1a824a54e989d76e985330371db2023-11-20T23:47:45ZengMDPI AGJournal of Fungi2309-608X2020-12-016434410.3390/jof6040344Hex1, the Major Component of Woronin Bodies, Is Required for Normal Development, Pathogenicity, and Stress Response in the Plant Pathogenic Fungus <i>Verticillium dahliae</i>Vasileios 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, Heidelberg University (ZMBH), 69120 Heidelberg, GermanyLaboratory of Mycology, Department of Viticulture, Vegetable Crops, Floriculture and Plant Protection, Institute of Olive Tree, Subtropical Crops and Viticulture, N.A.G.R.E.F., Hellenic Agricultural Organization—DEMETER, 71307 Heraklion, Crete, GreeceCenter for Molecular Biology, Heidelberg University (ZMBH), 69120 Heidelberg, GermanyDepartment of Genetics & Biotechnology, Faculty of Biology, National and Kapodistrian University of Athens, 15784 Athens, GreeceWoronin bodies are membrane-bound organelles of filamentous ascomycetes that mediate hyphal compartmentalization by plugging septal pores upon hyphal damage. Their major component is the peroxisomal protein Hex1, which has also been implicated in additional cellular processes in fungi. Here, we analyzed the Hex1 homolog of <i>Verticillium dahliae</i>, an important asexual plant pathogen, and we report its pleiotropic involvement in fungal growth, physiology, stress response, and pathogenicity. Alternative splicing of the <i>Vdhex1</i> gene can lead to the production of two Hex1 isoforms, which are structurally similar to their <i>Neurospora crassa</i> homolog. We show that <i>Vd</i>Hex1 is targeted to the septum, consistently with its demonstrated function in sealing hyphal compartments to prevent excessive cytoplasmic bleeding upon injury. Furthermore, our investigation provides direct evidence for significant contributions of Hex1 in growth and morphogenesis, as well as in asexual reproduction capacity. We discovered that Hex1 is required both for normal responses to osmotic stress and factors that affect the cell wall and plasma-membrane integrity, and for normal resistance to oxidative stress and reactive oxygen species (ROS) homeostasis. The <i>Vdhex1</i> mutant exhibited diminished ability to colonize and cause disease on eggplant. Overall, we show that Hex1 has fundamentally important multifaceted roles in the biology of <i>V. dahliae</i>.https://www.mdpi.com/2309-608X/6/4/344septal porehyphal integrityvirulenceROSheterokaryon incompatibility
spellingShingle Vasileios Vangalis
Ioannis A. Papaioannou
Emmanouil A. Markakis
Michael Knop
Milton A. Typas
Hex1, the Major Component of Woronin Bodies, Is Required for Normal Development, Pathogenicity, and Stress Response in the Plant Pathogenic Fungus <i>Verticillium dahliae</i>
Journal of Fungi
septal pore
hyphal integrity
virulence
ROS
heterokaryon incompatibility
title Hex1, the Major Component of Woronin Bodies, Is Required for Normal Development, Pathogenicity, and Stress Response in the Plant Pathogenic Fungus <i>Verticillium dahliae</i>
title_full Hex1, the Major Component of Woronin Bodies, Is Required for Normal Development, Pathogenicity, and Stress Response in the Plant Pathogenic Fungus <i>Verticillium dahliae</i>
title_fullStr Hex1, the Major Component of Woronin Bodies, Is Required for Normal Development, Pathogenicity, and Stress Response in the Plant Pathogenic Fungus <i>Verticillium dahliae</i>
title_full_unstemmed Hex1, the Major Component of Woronin Bodies, Is Required for Normal Development, Pathogenicity, and Stress Response in the Plant Pathogenic Fungus <i>Verticillium dahliae</i>
title_short Hex1, the Major Component of Woronin Bodies, Is Required for Normal Development, Pathogenicity, and Stress Response in the Plant Pathogenic Fungus <i>Verticillium dahliae</i>
title_sort hex1 the major component of woronin bodies is required for normal development pathogenicity and stress response in the plant pathogenic fungus i verticillium dahliae i
topic septal pore
hyphal integrity
virulence
ROS
heterokaryon incompatibility
url https://www.mdpi.com/2309-608X/6/4/344
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