Septation of Infectious Hyphae Is Critical for Appressoria Formation and Virulence in the Smut Fungus Ustilago Maydis

Johannes Freitag,Daniel Lanver,Christian Böhmer,Kay Oliver Schink,Björn Sandrock,Michael Bölker,Brett Tyler

doi:10.1371/journal.ppat.1002044

Abstract

Differentiation of hyphae into specialized infection structures, known as appressoria, is a common feature of plant pathogenic fungi that penetrate the plant cuticle. Appressorium formation in U. maydis is triggered by environmental signals but the molecular mechanism of this hyphal differentiation is largely unknown. Infectious hyphae grow on the leaf surface by inserting regularly spaced retraction septa at the distal end of the tip cell leaving empty sections of collapsed hyphae behind. Here we show that formation of retraction septa is critical for appressorium formation and virulence in U. maydis. We demonstrate that the diaphanous-related formin Drf1 is necessary for actomyosin ring formation during septation of infectious hyphae. Drf1 acts as an effector of a Cdc42 GTPase signaling module, which also consists of the Cdc42-specific guanine nucleotide exchange factor Don1 and the Ste20-like kinase Don3. Deletion of drf1, don1 or don3 abolished formation of retraction septa resulting in reduced virulence. Appressorium formation in these mutants was not completely blocked but infection structures were found only at the tip of short filaments indicating that retraction septa are necessary for appressorium formation in extended infectious hyphae. In addition, appressoria of drf1 mutants penetrated the plant tissue less frequently.

Highlights

Penetration of the plant cuticle is a prerequisite for the establishment of many plant-fungal interactions and involves the formation of specialized infection structures, called appressoria
In this study we identified for the first time a signaling module regulating formation of retraction septa in fungal hyphae
After penetration of the plant, cell cycle arrest is released and hyphal septation is resumed in planta but was found to be independent of Cdc42 and Drf1

Summary

Introduction

Penetration of the plant cuticle is a prerequisite for the establishment of many plant-fungal interactions and involves the formation of specialized infection structures, called appressoria. Appressoria are often melanized and contain thickened cell walls, which are necessary to generate the mechanical force to break through the cuticle of the plant epidermis. This process is driven by turgor-derived osmotic pressure and often involves targeted secretion of lytic enzymes [2,3,4]. Induction of appressorium formation is intricately regulated and triggered by chemical signals, hydrophobicity and surface texture [2,5]. The massive reorganisation of the fungal cell observed during differentiation of infection structures is coupled to cell cycle regulation [2]

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Discussion

Conclusion