Plants respond to environmental stimuli by altering gene transcription that is highly related with chromatin status, including histone modification, chromatin accessibility, and three-dimensional chromatin interaction. Vernalization is essential for the transition to reproductive growth for winter wheat. How wheat reshapes its chromatin features, especially chromatin interaction during vernalization, remains unknown. Combinatory analysis of gene transcription and histone modifications in winter wheat under different vernalization conditions identifies 17,669 differential expressed genes and thousands of differentially enriched peaks of H3K4me3, H3K27me3, and H3K9ac. We find dynamic gene expression across the vernalization process is highly associated with H3K4me3. More importantly, the dynamic H3K4me3- and H3K9ac-associated chromatin-chromatin interactions demonstrate that vernalization leads to increased chromatin interactions and gene activation. Remarkably, spatially distant targets of master regulators like VRN1 and VRT2 are gathered together by chromatin loops to achieve efficient transcription regulation, which is designated as a “shepherd” model. Furthermore, by integrating gene regulatory network for vernalization and natural variation of flowering time, TaZNF10 is identified as a negative regulator for vernalization-related flowering time in wheat. We reveal dynamic gene transcription network during vernalization and find that the spatially distant genes can be recruited together via chromatin loops associated with active histone mark thus to be more efficiently found and bound by upstream regulator. It provides new insights into understanding vernalization and response to environmental stimuli in wheat and other plants.

中文翻译：

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染色质环将上游调节因子的靶标聚集在一起，在小麦春化过程中进行有效的基因转录调控


植物通过改变与染色质状态高度相关的基因转录来响应环境刺激，包括组蛋白修饰、染色质可及性和三维染色质相互作用。春化对于冬小麦向生殖生长的过渡至关重要。小麦如何重塑其染色质特征，尤其是春化过程中的染色质相互作用，仍然未知。对不同春化条件下冬小麦基因转录和组蛋白修饰进行组合分析，鉴定出 H3K4me3、H3K27me3 和 H3K9ac 的 17,669 个差异表达基因和数千个差异富集峰。我们发现整个春化过程中的动态基因表达与 H3K4me3 高度相关。更重要的是，动态的 H3K4me3 和 H3K9ac 相关的染色质-染色质相互作用表明，春化导致染色质相互作用和基因激活增加。值得注意的是，VRN1 和 VRT2 等主调节因子的空间距离目标通过染色质环聚集在一起，以实现有效的转录调控，这被称为“牧羊人”模型。此外，通过整合春化和开花时间自然变化的基因调控网络，TaZNF10 被确定为小麦春化相关开花时间的负调节因子。我们揭示了春化过程中的动态基因转录网络，发现空间上距离远的基因可以通过与活性组蛋白标记相关的染色质环一起募集，从而更有效地被上游调节因子发现和结合。它为理解小麦和其他植物的春化和对环境刺激的反应提供了新的见解。