Background <p>Trimethylation of histone H3 lysine 27 (H3K27me3) confers a repressive chromatin state and is dynamically deposited and removed to regulate gene expression throughout plant growth and development. Nevertheless, the three-dimensional epigenome architecture linked to H3K27me3 and its regulatory role in controlling rice development remain unclear.</p> Results <p>Here, we employ long-read ChIA-PET to map the genome topology associated with H3K27me3 in rice, identifying hundreds of repressive chromatin spatial clusters within chromosomes. The T-DNA insertional mutagenesis of <i>EMBRYONIC FLOWER 2b</i> (<i>OsEMF2b</i>) leads to disruption of H3K27me3-associated chromatin interaction networks. Notably, we discover that the three key flowering time loci, <i>Early heading date 1</i> (<i>Ehd1</i>) and <i>Heading date 3a</i> (<i>Hd3a</i>)/<i>Rice Flowering Locus T1</i> (<i>RFT1</i>) form an inter-chromosomal repressive chromatin spatial cluster as a <i>cis</i>-interaction hub. Further investigation reveals that Ghd7, Ghd8, and Hd1 undergo liquid-liquid phase separation and bind to <i>Ehd1</i>-<i>Hd3a</i>/<i>RFT1</i> repressive chromatin spatial cluster as <i>trans</i> flowering regulators.</p> Conclusion <p>Our findings elucidate a multi-dimensional topological framework of H3K27me3-associated loci in rice and identify a spatial flowering gene cluster regulated by the phase-separated repressor complex of Ghd7, Ghd8, and Hd1. These results expand our knowledge of the structural basis of the three-dimensional genome governing the transcriptional coordination of florigens in rice.</p>

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3D epigenome architecture orchestrates cis and trans regulation of flowering time in rice

  • Yue Li,
  • Zhanyi Zhang,
  • Leilei Qiu,
  • Ruiqin Zheng,
  • Hongmeijuan Li,
  • Zhilin Cao,
  • Minrong Guo,
  • Shuangqi Wang,
  • Liang Xie,
  • Pengpeng Guan,
  • Xingyu Huang,
  • Cuicui Shen,
  • Hong Wu,
  • Wenjun Li,
  • Weizhi Ouyang,
  • Ying Zhang,
  • Guoting Chen,
  • Mohamed Foda,
  • Jiapei Yan,
  • Changyin Wu,
  • Xinhao Ouyang,
  • Guoliang Li,
  • Yongzhong Xing,
  • Xingwang Li

摘要

Background

Trimethylation of histone H3 lysine 27 (H3K27me3) confers a repressive chromatin state and is dynamically deposited and removed to regulate gene expression throughout plant growth and development. Nevertheless, the three-dimensional epigenome architecture linked to H3K27me3 and its regulatory role in controlling rice development remain unclear.

Results

Here, we employ long-read ChIA-PET to map the genome topology associated with H3K27me3 in rice, identifying hundreds of repressive chromatin spatial clusters within chromosomes. The T-DNA insertional mutagenesis of EMBRYONIC FLOWER 2b (OsEMF2b) leads to disruption of H3K27me3-associated chromatin interaction networks. Notably, we discover that the three key flowering time loci, Early heading date 1 (Ehd1) and Heading date 3a (Hd3a)/Rice Flowering Locus T1 (RFT1) form an inter-chromosomal repressive chromatin spatial cluster as a cis-interaction hub. Further investigation reveals that Ghd7, Ghd8, and Hd1 undergo liquid-liquid phase separation and bind to Ehd1-Hd3a/RFT1 repressive chromatin spatial cluster as trans flowering regulators.

Conclusion

Our findings elucidate a multi-dimensional topological framework of H3K27me3-associated loci in rice and identify a spatial flowering gene cluster regulated by the phase-separated repressor complex of Ghd7, Ghd8, and Hd1. These results expand our knowledge of the structural basis of the three-dimensional genome governing the transcriptional coordination of florigens in rice.