National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan, 430070, China.
Genome Biol. 2024 Oct 10;25(1):262. doi: 10.1186/s13059-024-03408-2.
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.
为了应对干旱胁迫（DS），植物经历了涉及到大量转录组重编程的复杂过程。然而，三维（3D）基因组的动态变化与基因共表达在干旱响应中的调节之间复杂的关系仍然是一个相对未被探索的领域。
在这项研究中，我们根据 H3K9ac 标记的基因组区域重建了高分辨率的 3D 基因组图谱，H3K9ac 是一种活跃的组蛋白修饰，它能对水稻土壤水分的变化做出动态响应。我们发现，在 DS 后，全基因组的 3D 基因组接触发生了断裂，超过 10000 个染色质环丢失，这些环在随后的再浇水过程中部分恢复。整合启动子-启动子相互作用（PPI）的环除了基础的 H3K9ac 修饰外，还对基因表达有贡献。此外，具有高亲和力介导 PPI 的 H3K9ac 标记启动子区域，被称为超级启动子区域（SPR），以类似于超级增强子的方式整合空间上聚集的 PPI。有趣的是，OsbZIP23 的敲除突变，一个明确的 DS 响应转录因子，导致超过 80%的 DS 特异性 PPI 发生分离，并且在 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 如何通过依赖于胁迫信号的方式靶向 RAB16C SPR，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时动态基因组折叠的原则和细节，并说明了 OsbZIP23 作为一个不可或缺的整合因子，它对水稻中 DS 下基因共表达所必需的独特的 3D 基因组组织起着至关重要的作用。
