In response to drought stress (DS), plants undergo complex processes that entail significant transcriptome reprogramming. However, the intricate relationship between the dynamic alterations in the three-dimensional (3D) genome and the modulation of gene co-expression in drought responses remains a relatively unexplored area. In this study, we reconstruct high-resolution 3D genome maps based on genomic regions marked by H3K9ac, an active histone modification that dynamically responds to soil water variations in rice. We discover a genome-wide disconnection of 3D genome contact upon DS with over 10,000 chromatin loops lost, which are partially recovered in the subsequent re-watering. Loops integrating promoter–promoter interactions (PPI) contribute to gene expression in addition to basal H3K9ac modifications. Moreover, H3K9ac-marked promoter regions with high affinities in mediating PPIs, termed as super-promoter regions (SPRs), integrate spatially clustered PPIs in a super-enhancer-like manner. Interestingly, the knockout mutation of OsbZIP23, a well-defined DS-responsive transcription factor, leads to the disassociation of over 80% DS-specific PPIs and decreased expression of the corresponding genes under DS. As a case study, we show how OsbZIP23 integrates the PPI cluster formation and the co-expression of four dehydrin genes, RAB16A–D, through targeting the RAB16C SPR in a stress signaling-dependent manner. Our high-resolution 3D genome maps unveil the principles and details of dynamic genome folding in response to water supply variations and illustrate OsbZIP23 as an indispensable integrator of the yet unique 3D genome organization that is essential for gene co-expression under DS in rice.

中文翻译：

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水稻中 H3K9ac 标记的 3D 染色质相互作用的干旱响应动力学被 OsbZIP23 相关的超级增强子样启动子区域整合


为了响应干旱胁迫 （DS），植物经历了复杂的过程，需要显着的转录组重编程。然而，三维 （3D） 基因组的动态改变与干旱响应中基因共表达的调节之间的复杂关系仍然是一个相对未开发的领域。在这项研究中，我们基于 H3K9ac 标记的基因组区域重建了高分辨率 3D 基因组图谱，H3K9ac 是一种活性组蛋白修饰，可动态响应水稻土壤水分的变化。我们发现 DS 时 3D 基因组接触在全基因组范围内断开，丢失了超过 10,000 个染色质环，这些染色质环在随后的重新浇水中部分恢复。整合启动子-启动子相互作用 （PPI） 的环除了基础 H3K9ac 修饰外，还有助于基因表达。此外，在介导 PPI 方面具有高亲和力的 H3K9ac 标记的启动子区域，称为超级启动子区域 （SPR），以超级增强子样的方式整合空间聚集的 PPI。有趣的是，OsbZIP23 是一种定义明确的 DS 反应性转录因子，其敲除突变导致超过 80% 的 DS 特异性 PPI 解离，并在 DS 下相应基因的表达降低。作为一个案例研究，我们展示了 OsbZIP23 如何通过以应激信号依赖性方式靶向 RAB16C SPR 来整合 PPI 簇的形成和四个脱水素基因 RAB16A-D 的共表达。我们的高分辨率 3D 基因组图谱揭示了响应供水变化的动态基因组折叠的原理和细节，并说明了 OsbZIP23 是尚未独特的 3D 基因组组织不可或缺的集成者，这对于水稻 DS 下的基因共表达至关重要。