Shanghai Collaborative Innovation Center of Agri-Seeds / School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, China.
National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Hubei Key Laboratory of Agricultural Bioinformatics, College of Informatics, Huazhong Agricultural University, Wuhan, 430070, China.
J Adv Res. 2022 Dec;42:41-53. doi: 10.1016/j.jare.2022.07.007. Epub 2022 Aug 4.
Polyploidy is a major force in plant evolution and the domestication of cultivated crops.
The study aimed to explore the relationship and underlying mechanism between three-dimensional (3D) chromatin organization and gene transcription upon rice genome duplication.
The 3D chromatin structures between diploid (2C) and autotetraploid (4C) rice were compared using high-throughput chromosome conformation capture (Hi-C) analysis. The study combined genetics, transcriptomics, whole-genome bisulfite sequencing (WGBS-seq) and 3D genomics approaches to uncover the mechanism for DNA methylation in modulating gene transcription through 3D chromatin architectures upon rice genome duplication.
We found that 4C rice presents weakened intra-chromosomal interactions compared to its 2C progenitor in some chromosomes. In addition, we found that changes of 3D chromatin organizations including chromatin compartments, topologically associating domains (TADs), and loops, are uncorrelated with gene transcription. Moreover, DNA methylations in the regulatory sequences of genes in compartment A/B switched regions and TAD boundaries are unrelated to their expression. Importantly, although there was no significant difference in the methylation levels in transposable elements (TEs) in differentially expressed gene (DEG) and non-DEG promoters between 2C and 4C rice, we found that the hypermethylated TEs across genes in compartment A/B switched regions and TAD boundaries may suppress the expression of these genes.
The study proposed that the rice genome doubling might modulate TE methylation to buffer the effects of chromatin architecture on gene transcription in compartment A/B switched regions and TAD boundaries, resulting in the disconnection between 3D chromatin structure alteration and gene transcription upon rice genome duplication.
多倍体是植物进化和栽培作物驯化的主要力量。
本研究旨在探索水稻基因组加倍过程中三维（3D）染色质构象与基因转录之间的关系及其潜在机制。
利用高通量染色体构象捕获（Hi-C）分析比较了二倍体（2C）和同源四倍体（4C）水稻之间的 3D 染色质结构。该研究结合遗传学、转录组学、全基因组亚硫酸氢盐测序（WGBS-seq）和 3D 基因组学方法，揭示了水稻基因组加倍过程中 DNA 甲基化通过 3D 染色质构象调节基因转录的机制。
我们发现，与 2C 亲本品系相比，4C 水稻在一些染色体上表现出较弱的染色体内相互作用。此外，我们发现 3D 染色质构象的变化，包括染色质区室、拓扑关联域（TADs）和环，与基因转录无关。此外，位于区室 A/B 转换区和 TAD 边界的基因调控序列中的 DNA 甲基化与其表达无关。重要的是，尽管在 2C 和 4C 水稻中差异表达基因（DEG）和非 DEG 启动子中转座元件（TEs）的甲基化水平没有显著差异，但我们发现区室 A/B 转换区和 TAD 边界处基因中高度甲基化的 TEs 可能抑制这些基因的表达。
本研究提出，水稻基因组加倍可能通过调节 TEs 甲基化来缓冲染色质构象对区室 A/B 转换区和 TAD 边界基因转录的影响，导致水稻基因组加倍过程中 3D 染色质结构改变与基因转录之间的脱节。
