Regulatory Roles of Histone Modifications in Filamentous Fungal Pathogens

Abstract

Filamentous fungal pathogens have evolved diverse strategies to infect a variety of hosts including plants and insects. The dynamic infection process requires rapid and fine-tuning regulation of fungal gene expression programs in response to the changing host environment and defenses. Therefore, transcriptional reprogramming of fungal pathogens is critical for fungal development and pathogenicity. Histone post-translational modification, one of the main mechanisms of epigenetic regulation, has been shown to play an important role in the regulation of gene expressions, and is involved in, e.g., fungal development, infection-related morphogenesis, environmental stress responses, biosynthesis of secondary metabolites, and pathogenicity. This review highlights recent findings and insights into regulatory mechanisms of histone methylation and acetylation in fungal development and pathogenicity, as well as their roles in modulating pathogenic fungi-host interactions.

Keywords: filamentous fungal pathogens; fungal pathogenicity; histone acetylation; histone methylation; pathogenic fungi–host interactions.

Figure 1

A schematic model of histone lysine methylation and acetylation and their regulatory roles in filamentous fungal pathogens. Histone lysine methyltransferases (HKMTs), histone lysine demethyltransferases (HKDMs), histone acetylases (HATs), and histone deacetylases (HDACs) for each lysine residue reported in filamentous fungal pathogens are depicted. Detailed information about these enzymes for respective lysine residues in specific fungal species is included in the text. These histone modifications affect chromatin structures to regulate gene transcription. In general, modifications with methylation of H3K4, H3K36, and H3K79, as well as histone acetylation, result in a relaxed and open chromatin (euchromatin) that provides accessibility to the transcription machinery and thus enables gene activation. In contrast, modifications with methylation of H3K9, H3K27, and H4K20, as well as histone deacetylation, lead to a condensed and less accessible chromatin (heterochromatin) that restricts DNA accessibility to the transcription machinery and represses gene transcription. Gene regulation mediated by histone modifications finally controls multiple phenotypic plasticity, including conidiation, biosynthesis of secondary metabolite toxins, infection structure differentiation, effector production, stress responses, and virulence in filamentous fungal pathogens. SM, secondary metabolite; DON, deoxynivalenol; ROS, reactive oxygen species.