Histone modification dynamics at H3K27 are associated with altered transcription of in planta induced genes in Magnaporthe oryzae

Abstract

Transcriptional dynamic in response to environmental and developmental cues are fundamental to biology, yet many mechanistic aspects are poorly understood. One such example is fungal plant pathogens, which use secreted proteins and small molecules, termed effectors, to suppress host immunity and promote colonization. Effectors are highly expressed in planta but remain transcriptionally repressed ex planta, but our mechanistic understanding of these transcriptional dynamics remains limited. We tested the hypothesis that repressive histone modification at H3-Lys27 underlies transcriptional silencing ex planta, and that exchange for an active chemical modification contributes to transcription of in planta induced genes. Using genetics, chromatin immunoprecipitation and sequencing and RNA-sequencing, we determined that H3K27me3 provides significant local transcriptional repression. We detail how regions that lose H3K27me3 gain H3K27ac, and these changes are associated with increased transcription. Importantly, we observed that many in planta induced genes were marked by H3K27me3 during axenic growth, and detail how altered H3K27 modification influences transcription. ChIP-qPCR during in planta growth suggests that H3K27 modifications are generally stable, but can undergo dynamics at specific genomic locations. Our results support the hypothesis that dynamic histone modifications at H3K27 contributes to fungal genome regulation and specifically contributes to regulation of genes important during host infection.

Author summary

Fungal pathogens of crops and humans pose annual threats to our food and health. There are many steps to the host infection process, during which fungal pathogens display unique growth, and use specific genes to cause disease. Despite this knowledge, many aspects of how pathogens regulate their genome to enact this process remain unknown. Here, we demonstrate how chemical modification of lysine residues on the histone H3, which helps organize and control DNA usage, play an important regulatory role in the model fungal pathogen causing rice blast disease. Our analysis shows a significant association between genes important for host infection and H3 lysine 27 methylation. We show that by experimentally changing histone modifications, many fungal genes normally used during plant infection are turned on outside of the host. Furthermore, we detail how histone modifications can change naturally in the fungus during plant infection. These findings help broaden our knowledge of genome regulation for these pathogens, and advances the goal of a more comprehensive understanding of the infection process.