Targeted reprogramming of H3K27me3 resets epigenetic memory in plant paternal chromatin

Epigenetic marks are reprogrammed in the gametes to reset genomic potential in the next generation. In most animal species, paternal chromatin is extensively reprogrammed through the global erasure of DNA methylation and the exchange of histones with protamine. Precisely how the paternal epigenome is reprogrammed in flowering plants remains unclear since sperm chromatin is not demethylated and histones are retained. Here, we show that the sperm-specific histone, H3.10, is immune to lysine 27 methylation and that its deposition in sperm contributes to the global and specific resetting of the epigenetic mark H3K27me3 by uncoupling its inheritance during DNA replication. The loss of H3K27me3 facilitates transcription of genes essential for spermatogenesis and pre-configures sperm with a chromatin state that forecasts gene expression in the next generation, revealing a global wave of epigenetic resetting that coordinates with early plant life. Thus, in contrast to the indiscriminate removal of epigenetic marks in animal sperm, plants have evolved a specific mechanism to simultaneously differentiate male gametes and reprogram the paternal epigenome. Genome-wide maps of H3K4me3, H3K27ac, H3K27me1, H3K27me3 and H3.10 deposition in Arabidopsis sperm chromatin