Abstract
Despite the considerable contribution of xylem development (xylogenesis) to plant biomass accumulation, its epigenetic regulation is poorly understood. Furthermore, the relative contributions of histone modifications to transcriptional regulation is not well studied in plants. We investigated the biological relevance of H3K4me3 and H3K27me3 in secondary xylem development using ChIP-seq and their association with transcript levels among other histone modifications in woody and herbaceous models. In developing secondary xylem of the woody model Eucalyptus grandis, H3K4me3 and H3K27me3 genomic spans were distinctly associated with xylogenesis-related processes, with (late) lignification pathways enriched for putative bivalent domains, but not early secondary cell wall polysaccharide deposition. H3K27me3-occupied genes, of which 753 (~31%) are novel targets, were enriched for transcriptional regulation and flower development and had significant preferential expression in roots. Linear regression models of the ChIP-seq profiles predicted ~50% of transcript abundance measured with strand-specific RNA-seq, confirmed in a parallel analysis in Arabidopsis where integration of seven additional histone modifications each contributed smaller proportions of unique information to the predictive models. This study uncovers the biological importance of histone modification antagonism and genomic span in xylogenesis and quantifies for the first time the relative correlations of histone modifications with transcript abundance in plants.
Highlights
Eukaryotic genomes are compartmentalised into distinct chromatin states that profoundly influence transcriptional activity in a cell-specific manner
After confirming the specificity of commercial ChIP-seq antibodies against H3K4me[3] and H3K27me[3] peptides (Supplementary Fig. S2), ChIP-seq was performed based on Encyclopedia of DNA Element (ENCODE) guidelines[22], yielding highly immuno-enriched ChIP-seq libraries (Supplementary Fig. S3) with a low percentage of reads mapping to plastids (Supplementary Table S1)
We determined the deposition preferences of H3K4me[3] and H3K27me[3] relative to transcriptional start sites (TSS) by plotting relative per-base library coverage across all annotated genes anchored at the TSS
Summary
Eukaryotic genomes are compartmentalised into distinct chromatin states that profoundly influence transcriptional activity in a cell-specific manner. Xylogenesis (wood formation, or secondary growth) represents a strong and permanent carbon sink in plants and a commitment to a cell fate ending in cell death During this developmental process, xylem initial cells produced by the meristematic vascular cambium undergo elongation, secondary cell wall (SCW) deposition, lignification and programmed cell death (in the case of fibres and vessels) in a narrow tissue layer within the stem[3, 4]. The majority of plant epigenomic studies, have been based on whole organs or complex mixtures of tissues that provide limited resolution of cell- or tissue-specific epigenetic regulation during development. H3K4 trimethylation is generally established at the 5′ region of transcribed genes by homologs of the yeast SET1 histone methyltransferase[9, 10], reinforcing transcription by recruiting pre-initiation complex machinery[11]. Optimal modelling approaches and the relative importance of different HMs remain to be explored in plants
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