Targeted reprogramming of H3K27me3 resets epigenetic memory in plant paternal chromatin [mature pollen]

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: Gene expression profiling of WT, htr10, elf6;ref6;jmj13 and elf6;ref6;jmj13;htr10 mutant pollen.

表观遗传标记（epigenetic marks）会在配子（gametes）中发生重编程，以重置下一代的基因组潜能（genomic potential）。在绝大多数动物物种中，父本染色质（paternal chromatin）会通过全基因组DNA甲基化（DNA methylation）清除以及组蛋白（histones）与鱼精蛋白（protamine）的替换被广泛重编程。然而，被子植物（flowering plants）的父本表观基因组究竟如何完成重编程仍不明确，因其精子染色质（sperm chromatin）既未发生去甲基化（demethylated），组蛋白也得以保留。本研究表明，精子特异性组蛋白H3.10（sperm-specific histone H3.10）对赖氨酸27甲基化（lysine 27 methylation）具有抗性，其在精子中的沉积可通过解偶联DNA复制（DNA replication）过程中的H3K27me3遗传，实现表观遗传标记H3K27me3的全局性特异性重设。H3K27me3的缺失会促进精子发生（spermatogenesis）必需基因的转录，并预先为精子构建染色质状态，该状态可预测下一代的基因表达模式，揭示了与植物早期发育协同的全局性表观遗传重编程浪潮。综上，与动物精子中表观遗传标记的无差别清除不同，植物演化出了一种特异性机制，可同时完成雄性配子分化与父本表观基因组重编程。实验设计概述：对野生型（WT）、htr10、elf6;ref6;jmj13以及elf6;ref6;jmj13;htr10突变体的花粉（pollen）进行基因表达谱分析（gene expression profiling）。