Dynamic Deposition of Histone Variant H3.3 Accompanies Developmental Remodeling of the <em>Arabidopsis</em> Transcriptome

In animals, replication-coupled histone H3.1 can be distinguished from replication-independent histone H3.3. H3.3 variants are enriched at active genes and their promoters. Furthermore, H3.3 is specifically incorporated upon gene activation. Histone H3 variants evolved independently in plants and animals, and it is unclear whether different replication-independent H3.3 variants developed similar properties in both phyla. We studied Arabidopsis H3 variants in order to find core properties of this class of histones. Here we present genome-wide maps of H3.3 and H3.1 enrichment and the dynamic changes of their profiles upon cell division arrest. We find H3.3 enrichment to positively correlate with gene expression and to be biased towards the transcription termination site. In contrast with H3.1, heterochromatic regions are mostly depleted of H3.3. We report that, in planta, dynamic changes in H3.3 profiles are associated with the extensive remodeling of the transcriptome that occurs during cell differentiation. We propose that H3.3 dynamics are linked to transcription and are involved in resetting covalent histone marks at a genomic scale during plant development. Our study suggests that H3 variants properties likely result from functionally convergent evolution.在动物体内，复制偶联型组蛋白H3.1（replication-coupled histone H3.1）与复制非依赖型组蛋白H3.3（replication-independent histone H3.3）可通过复制模式加以区分。H3.3变体富集于活跃基因及其启动子区域，且会在基因激活时被特异性整合至染色质。组蛋白H3变体在植物与动物中独立演化，目前尚不明确两类生物中不同的复制非依赖型H3.3变体是否具备相似的功能特性。为探究此类组蛋白的核心属性，我们以拟南芥（Arabidopsis）的H3变体为研究对象。本研究绘制了H3.3与H3.1的全基因组富集图谱（genome-wide maps），并分析了细胞分裂停滞（cell division arrest）时二者分布模式的动态变化。我们发现，H3.3的富集水平与基因表达量呈正相关，且偏向分布于转录终止位点（transcription termination site）。与H3.1不同的是，异染色质区域（heterochromatic regions）几乎不含H3.3。本研究表明，在植物体内，H3.3的分布模式动态变化与细胞分化（cell differentiation）过程中发生的转录组（transcriptome）大规模重塑密切相关。我们推测，H3.3的动态变化与转录过程相关联，并在植物发育的全基因组水平（genomic scale）上参与共价组蛋白修饰（covalent histone marks）的重置过程。本研究提示，H3变体的功能特性可能源自功能趋同演化（functionally convergent evolution）。