Drought-responsive dynamics of H3K9ac-marked 3D chromatin interactions are integrated by OsbZIP23-associated super-enhancer-like promoter regions in rice

IF 10.1 1区 生物学 Q1 BIOTECHNOLOGY & APPLIED MICROBIOLOGY
Yu Chang, Jiahan Liu, Minrong Guo, Weizhi Ouyang, Jiapei Yan, Lizhong Xiong, Xingwang Li
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Abstract

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.
水稻中与 OsbZIP23 相关的超级增强子样启动子区整合了 H3K9ac 标记的三维染色质相互作用的干旱响应动态变化
在应对干旱胁迫(DS)时,植物会经历复杂的过程,其中包括显著的转录组重构。然而,三维(3D)基因组的动态变化与干旱响应中基因共表达调控之间错综复杂的关系仍是一个相对尚未探索的领域。在本研究中,我们根据H3K9ac标记的基因组区域重建了高分辨率的三维基因组图谱,H3K9ac是一种活性组蛋白修饰,可动态响应水稻的土壤水分变化。我们发现,在水稻缺水时,全基因组的三维基因组接触断开,有超过 10,000 个染色质环丢失,但在随后的再浇水中又部分恢复。除了基本的 H3K9ac 修饰外,整合启动子-启动子相互作用(PPI)的环路也有助于基因表达。此外,H3K9ac标记的启动子区域在介导PPI方面具有很高的亲和力,被称为超级启动子区域(SPRs),它们以类似超级增强子的方式整合了空间集群的PPI。有趣的是,OsbZIP23(一种定义明确的DS反应性转录因子)的基因敲除突变会导致80%以上的DS特异性PPIs分离,并导致相应基因在DS条件下的表达量减少。作为一个案例研究,我们展示了OsbZIP23是如何通过靶向RAB16C SPR以胁迫信号依赖的方式整合PPI簇的形成和四个脱水素基因RAB16A-D的共表达的。我们的高分辨率三维基因组图谱揭示了响应水分供应变化的动态基因组折叠的原理和细节,并说明了OsbZIP23是水稻独特的三维基因组组织不可或缺的整合者,它对DS条件下的基因共表达至关重要。
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来源期刊
Genome Biology
Genome Biology Biochemistry, Genetics and Molecular Biology-Genetics
CiteScore
21.00
自引率
3.30%
发文量
241
审稿时长
2 months
期刊介绍: Genome Biology stands as a premier platform for exceptional research across all domains of biology and biomedicine, explored through a genomic and post-genomic lens. With an impressive impact factor of 12.3 (2022),* the journal secures its position as the 3rd-ranked research journal in the Genetics and Heredity category and the 2nd-ranked research journal in the Biotechnology and Applied Microbiology category by Thomson Reuters. Notably, Genome Biology holds the distinction of being the highest-ranked open-access journal in this category. Our dedicated team of highly trained in-house Editors collaborates closely with our esteemed Editorial Board of international experts, ensuring the journal remains on the forefront of scientific advances and community standards. Regular engagement with researchers at conferences and institute visits underscores our commitment to staying abreast of the latest developments in the field.
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