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.
Highlights
Epigenetic regulation of gene expression is common across many organisms including animals, plants and fungi, regulating diverse processes such as development, disease, and environmental response [1,2,3,4]
Using a combination of fungal molecular genetics, epigenomics, and transcriptomics analysis, we demonstrate that histone modification dynamics at H3K27 can regulate specific genomic loci, often important during host infection, supporting the hypothesis
The genome-wide domains for H3K27me3 and H3K27ac occupied discrete genomic regions in M. oryzae, with H3K27me3 forming longer discreate blocks, and H3K27ac having a more continuous distribution but shorter domains (Fig 1B and 1C)
Summary
Epigenetic regulation of gene expression is common across many organisms including animals, plants and fungi, regulating diverse processes such as development, disease, and environmental response [1,2,3,4]. Nuclear DNA is packaged around histone proteins to form nucleosomes [5]. Post-translational chemical modifications to histone tails provide epigenetic information contributing to genome regulation [6]. These modifications contribute to active, poised, or silenced transcription by affecting DNA-protein interactions, referred to as chromatin, which contributes to DNA accessibility and positioning in the nucleus [7,8]. Histone modifications may function alone but they can influence other histone modifications, termed cross-talk, to produce different chromatin states giving rise to a histone code regulating DNA functions [6,12]. In Drosophila and mouse H3K27me and H3K27ac are mutually exclusive, and H3K27ac can antagonize H3K27me mediated gene silencing [13,14]
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