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

Vasileios Vangalis,Milton A. Typas,Michael Knop,Ioannis A. Papaioannou,Emmanouil A. Markakis

doi:10.3390/jof6040344

Abstract

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 Verticillium dahliae, an important asexual plant pathogen, and we report its pleiotropic involvement in fungal growth, physiology, stress response, and pathogenicity. Alternative splicing of the Vdhex1 gene can lead to the production of two Hex1 isoforms, which are structurally similar to their Neurospora crassa homolog. We show that VdHex1 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 Vdhex1 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 V. dahliae.

Highlights

The undifferentiated body of a typical filamentous fungus is the mycelium, a complex network of branched tubular cells called hyphae
These transitions led to the evolution of the syncytial mycelium, which is characterized by cytoplasmic continuity [52]
Uncontrolled intercompartmental traffic would lead to increased exposure to biotic and abiotic risks that could rapidly propagate throughout the mycelium [3,4,5,6,7], which underlines the necessity for a trade-off between continuity and conditional control of exchanges

Summary

Introduction

The undifferentiated body (or thallus) of a typical filamentous fungus is the mycelium, a complex network of branched tubular cells called hyphae In most fungi, these are partitioned into distinct cellular compartments by internal cross-walls, the septae [1,2]. Hyphal compartments are continuous with one another due to the occurrence of septal pores, which allow the intercellular flow of cytoplasm, including organelles, ensuring the rapid translocation of nutrients during colony establishment and facilitating the maintenance of cellular homeostasis during mycelial growth [3] This ability of the mycelium to function as an integrated syncytium-like organism exposes it to a number of risks, J. The intercompartmental traffic in hyphae must be highly regulated in order to protect the mycelium from such hazards, as well as to permit cellular heterogeneity and differentiation during developmental processes [3,4,5,6,7]

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Conclusion