A novel bivalent chromatin associates with rapid induction of camalexin biosynthesis genes in response to a pathogen signal in Arabidopsis

Abstract

Temporal dynamics of gene expression underpin responses to internal and environmental stimuli. In eukaryotes, regulation of gene induction includes changing chromatin states at target genes and recruiting the transcriptional machinery that includes transcription factors. As one of the most potent defense compounds in Arabidopsis thaliana, camalexin can be rapidly induced by bacterial and fungal infections. Though several transcription factors controlling camalexin biosynthesis genes have been characterized, how the rapid activation of genes in this pathway upon a pathogen signal is enabled remains unknown. By combining publicly available epigenomic data with in vivo chromatin modification mapping, we found that camalexin biosynthesis genes are marked with two epigenetic modifications with opposite effects on gene expression, H3K27me3 (repression) and H3K18ac (activation), to form a previously uncharacterized type of bivalent chromatin. Mutants with reduced H3K27m3 or H3K18ac suggested that both modifications were required to determine the timing of gene expression and metabolite accumulation at an early stage of the stress response. Our study indicates that the H3K27me3-H3K18ac bivalent chromatin, which we name a kairostat, plays an important role controlling the timely induction of gene expression upon stimuli in plants.

Plant biosynthetic gene clusters in the context of metabolic evolution

“… 127 H3K27me3, along with H3K18ac, is involved in induction of biosynthetic genes to pathogen responses in Arabidopsis. 140 …”

“…127 H3K27me3, along with H3K18ac, is involved in induction of biosynthetic genes to pathogen responses in Arabidopsis. 140 It appears that H3K27me3 may be involved not just in intracluster regulation but in the co-regulation and spatial connection of genetically distant loci involved in the same pathway. Perhaps through H3K27me3, loci that are unclustered on the linear genome can cluster in three dimensions.…”

Polycomb Repressive Complex 2 in Eukaryotes—An Evolutionary Perspective

“…An exception to this is regions of bivalent chromatin where activating and repressive modifications co-localize to potentiate rapid change of gene transcription. In both plant and animals, the best well-described bivalent chromatin is marked by H3K27me3 and H3K4me3 ([ 155 ], reviewed in the work of [ 203 ]), but other active modifications may co-localize with H3K27me3 including H3K4me1 in Brassica napus [ 204 ], or H3K18ac in the camalexin biosynthesis genes in A. thaliana [ 205 ]. In mammals, H3K27me3 is promoted in a self-reinforcement loop.…”

Multi-Omics-Based Discovery of Plant Signaling Molecules

“…Via ChIP-seq analysis, plant triterpenes thalianol and marneral biosynthetic gene clusters were found to be regulated by histone modification with histone 3 lysine trimethylation (H3K27me3) and the histone2 variant H2A.Z reported to repress and activate the thalianol and marneral gene clusters, respectively [29]. Besides triterpenes, camalexin biosynthesis genes were also found to contain epigenetic marks with H3K18ac and H3K27me3 found to activate and repress gene expression, respectively [30]. Similarly, the diterpene gene cluster responsible for the biosynthesis of the antifungal diterpene, ent-5,10-diketo-casbene, was recently found to also be under the regulation of epigenetic modifications with H3K27me3 acting as a repression mark [31].…”