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. Overall design: Smart-Seq2 library from mature pollen and sperm cells Publicly-available RNA-seq datasets were processed in the same pipeline and are included for reference. Type SRA_ID Tissue RNA-seq SRR800753 Floral bud RNA-seq SRR800754 Floral bud RNA-seq SRR1207194 Carpel RNA-seq SRR1207195 Carpel RNA-seq SRR401413 Receptacle RNA-seq SRR401414 Receptacle RNA-seq SRR401415 Receptacle RNA-seq SRR401416 Receptacle RNA-seq SRR401417 Receptacle RNA-seq SRR401418 Receptacle RNA-seq SRR401419 Receptacle RNA-seq SRR401420 Receptacle RNA-seq SRR401421 Receptacle RNA-seq SRR1260032 Root apical meristem RNA-seq SRR1260033 Root apical meristem RNA-seq SRR949956 Shoot apical meristen RNA-seq SRR949965 Shoot apical meristen RNA-seq SRR949988 Shoot apical meristen RNA-seq SRR949989 Shoot apical meristen RNA-seq SRR515073 Seedling RNA-seq SRR515074 Seedling RNA-seq SRR527164 Seedling RNA-seq SRR527165 Seedling RNA-seq SRR493097 Leaf RNA-seq SRR493098 Leaf RNA-seq SRR493101 Leaf RNA-seq SRR1046909 Roots RNA-seq SRR1046910 Roots RNA-seq SRR5227391 Dry seeds RNA-seq SRR5227392 Dry seeds RNA-seq SRR5227393 Dry seeds RNA-seq SRR364465 1-cell/2-cell embryos RNA-seq SRR364466 1-cell/2-cell embryos RNA-seq SRR364467 8-cell embryos RNA-seq SRR364468 8-cell embryos RNA-seq SRR364469 ~32-cell embryos RNA-seq SRR364470 ~32-cell embryos