Targeted reprogramming of H3K27me3 resets epigenetic memory in plant paternal chromatin

Targeted reprogramming of H3K27me3 resets epigenetic memory in plant paternal chromatin
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DOI:
10.1038/s41556-020-0515-y
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发表时间:
2020-05-11
影响因子:
21.3
通讯作者:
Berger, Frederic
Berger, Frederic
中科院分区:
生物学1区
文献类型:
--
作者:
Borg, Michael;Jacob, Yannick;Berger, Frederic

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博格等人报道,精子特异性组蛋白变体H3.10的掺入(其抵抗K27甲基化)导致H3K27 me3从植物精子染色质中去除,从而促进精子特异性基因的表达。在哺乳动物中,通过DNA甲基化的全局擦除和组蛋白与鱼精蛋白的交换,父体染色质被广泛地重新编程(1,2)。由于DNA没有去甲基化,组蛋白保留在精子中,因此在开花植物中父系表观基因组是如何被重新编程的仍然不清楚(3,4)。在这里,我们描述了一个多层次的机制,H3K27me3是全球性的损失,从组蛋白为基础的精子染色质在拟南芥。该机制涉及H3K27me3写入器的沉默、H3K27me3擦除器的活性和精子特异性组蛋白H3.10的沉积(参考文献(5)),我们表明该组蛋白对赖氨酸27甲基化免疫。H3K27me3的缺失促进了精子发生所必需的基因的转录,并使精子预先具有预测下一代基因表达的染色质状态。因此,植物已经进化出一种特殊的机制,可以同时分化雄配子和重编程父本表观基因组。
Borg et al. report that incorporation of the sperm-specific histone variant H3.10, which resists K27 methylation, causes H3K27me3 removal from sperm chromatin in plants, thus facilitating the expression of sperm-specific genes.Epigenetic marks are reprogrammed in the gametes to reset genomic potential in the next generation. In mammals, paternal chromatin is extensively reprogrammed through the global erasure of DNA methylation and the exchange of histones with protamines(1,2). Precisely how the paternal epigenome is reprogrammed in flowering plants has remained unclear since DNA is not demethylated and histones are retained in sperm(3,4). Here, we describe a multi-layered mechanism by which H3K27me3 is globally lost from histone-based sperm chromatin in Arabidopsis. This mechanism involves the silencing of H3K27me3 writers, activity of H3K27me3 erasers and deposition of a sperm-specific histone, H3.10 (ref. (5)), which we show is immune to lysine 27 methylation. The loss of H3K27me3 facilitates the transcription of genes essential for spermatogenesis and pre-configures sperm with a chromatin state that forecasts gene expression in the next generation. Thus, plants have evolved a specific mechanism to simultaneously differentiate male gametes and reprogram the paternal epigenome.