The Hos2 Histone Deacetylase Controls Ustilago maydis Virulence through Direct Regulation of Mating-Type Genes.

Alberto Elías-Villalobos,Alfonso Fernández-Álvarez,Dominique Helmlinger,José I Ibeas,Ismael Moreno-Sánchez,Jörg Kämper

doi:10.1371/journal.ppat.1005134

Abstract

Morphological changes are critical for host colonisation in plant pathogenic fungi. These changes occur at specific stages of their pathogenic cycle in response to environmental signals and are mediated by transcription factors, which act as master regulators. Histone deacetylases (HDACs) play crucial roles in regulating gene expression, for example by locally modulating the accessibility of chromatin to transcriptional regulators. It has been reported that HDACs play important roles in the virulence of plant fungi. However, the specific environment-sensing pathways that control fungal virulence via HDACs remain poorly characterised. Here we address this question using the maize pathogen Ustilago maydis. We find that the HDAC Hos2 is required for the dimorphic switch and pathogenic development in U. maydis. The deletion of hos2 abolishes the cAMP-dependent expression of mating type genes. Moreover, ChIP experiments detect Hos2 binding to the gene bodies of mating-type genes, which increases in proportion to their expression level following cAMP addition. These observations suggest that Hos2 acts as a downstream component of the cAMP-PKA pathway to control the expression of mating-type genes. Interestingly, we found that Clr3, another HDAC present in U. maydis, also contributes to the cAMP-dependent regulation of mating-type gene expression, demonstrating that Hos2 is not the only HDAC involved in this control system. Overall, our results provide new insights into the role of HDACs in fungal phytopathogenesis.

Highlights

The switch between yeast and hypha stages, or dimorphism, is a key morphological conversion required for the virulence of several animal and plant pathogenic fungi [1,2,3,4]
We found that Clr3, another Histone deacetylases (HDACs) present in U. maydis, contributes to the cAMP-dependent regulation of mating-type gene expression, demonstrating that Hos2 is not the only HDAC involved in this control system
A BLAST search and phylogenetic analysis revealed that Ustilago maydis genome harbours six putative class I and II HDACs, a putative orthologue of each HDAC found in Saccharomyces cerevisiae, Candida albicans, and Schizosaccharomyces pombe, except for the Rpd3/Clr6 HDAC, for which we found two distinct homologues in U. maydis (Fig 1A)

Summary

Introduction

The switch between yeast and hypha stages, or dimorphism, is a key morphological conversion required for the virulence of several animal and plant pathogenic fungi [1,2,3,4]. This process occurs at specific stages of fungal infection and is tightly controlled. The two best studied signalling pathways regulating gene expression during dimorphism are the mitogen activated protein (MAP) kinase cascade and the cyclic-AMP protein kinase A (cAMP-PKA) pathway Their activation is typically controlled by specific environmental stimuli and results in the induction of master regulatory genes [5,6,7,8]. The transition from the yeast form to the infective filamentous one is crucial for U. maydis pathogenicity

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Conclusion