Epigenetic factors direct synergistic and antagonistic regulation of transposable elements in Arabidopsis.

IF 6.5 1区 生物学 Q1 PLANT SCIENCES Plant Physiology Pub Date : 2024-11-04 DOI:10.1093/plphys/kiae392
Jo-Wei Allison Hsieh, Ming-Ren Yen, Fu-Yu Hung, Keqiang Wu, Pao-Yang Chen
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Abstract

Arabidopsis (Arabidopsis thaliana) HISTONE DEACETYLASE 6 (HDA6) and HISTONE DEMETHYLASES LSD-LIKE 1 (LDL1) and LDL2 synergistically regulate the expression of long non-coding RNAs associated with H3Ac and H3K4me2. The underlying mechanisms of such highly coordinated interactions among genetic and epigenetic factors contributing to this collaborative regulation remain largely unclear. We analyzed all transposable elements (TEs) across the Arabidopsis genome and the individual and combined roles of HDA6 and LDL1/LDL2 by dissecting multilayered epigenomes and their association with transcription. Instead of an individual synergistic effect, we observed dual synergistic and antagonistic effects, which are positively associated with H3Ac and H3K4me2 while maintaining a negative but moderate association with DNA methylation. Specifically, 2 modes of synergistic regulation were discovered in TEs: 74% are primarily regulated by HDA6, with less dependence on LDL1/LDL2, and the remaining 26% are co-regulated by both. Between the 2 modes, we showed that HDA6 has a strong effect on TE silencing, whereas LDL1/LDL2 plays a weaker yet crucial role in co-regulation with HDA6. Our results led to a model of epigenomic regulation-the differential de-repression between the 2 modes of synergistic regulation of TEs was determined by H3Ac and H3K4me2 levels, where TEs are in accessible chromatins free of DNA methylation, and this open chromatin environment precedes transcriptional changes and epigenome patterning. Our results discovered unbalanced effects of genetic factors in synergistic regulation through delicately coordinated multilayered epigenomes and chromatin accessibility.

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表观遗传因子对拟南芥中转座元素的协同和拮抗调控起指导作用。
拟南芥(Arabidopsis thaliana)HISTONE DEACETYLASE 6(HDA6)和 HISTONE DEMETHYLASES LSD-LIKE 1(LDL1)和 LDL2 协同调控与 H3Ac 和 H3K4me2 相关的长非编码 RNA 的表达。遗传和表观遗传因子之间高度协调的相互作用促成了这种协同调控,但其潜在机制在很大程度上仍不清楚。我们通过剖析多层表观基因组及其与转录的关联,分析了拟南芥基因组中的所有转座元件(TE)以及 HDA6 和 LDL1/LDL2 的单独作用和联合作用。我们没有观察到单独的协同效应,而是观察到了协同和拮抗的双重效应,它们与 H3Ac 和 H3K4me2 呈正相关,同时与 DNA 甲基化保持负相关,但关系适中。具体来说,我们在 TEs 中发现了两种协同调控模式:74% 的 TEs 主要受 HDA6 调控,对 LDL1/LDL2 的依赖性较小;其余 26% 的 TEs 则受两者共同调控。在这两种模式之间,我们发现HDA6对TE的沉默有很强的作用,而LDL1/LDL2在与HDA6共同调控中的作用较弱,但却至关重要。我们的研究结果提出了一个表观基因组调控模型--两种协同调控模式对TE的不同去抑制作用由H3Ac和H3K4me2水平决定,TE处于无DNA甲基化的可访问染色质中,这种开放的染色质环境先于转录变化和表观基因组模式化。我们的研究结果发现了遗传因子在通过微妙协调的多层表观遗传组和染色质可及性进行协同调控方面的不平衡效应。
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来源期刊
Plant Physiology
Plant Physiology 生物-植物科学
CiteScore
12.20
自引率
5.40%
发文量
535
审稿时长
2.3 months
期刊介绍: Plant Physiology® is a distinguished and highly respected journal with a rich history dating back to its establishment in 1926. It stands as a leading international publication in the field of plant biology, covering a comprehensive range of topics from the molecular and structural aspects of plant life to systems biology and ecophysiology. Recognized as the most highly cited journal in plant sciences, Plant Physiology® is a testament to its commitment to excellence and the dissemination of groundbreaking research. As the official publication of the American Society of Plant Biologists, Plant Physiology® upholds rigorous peer-review standards, ensuring that the scientific community receives the highest quality research. The journal releases 12 issues annually, providing a steady stream of new findings and insights to its readership.
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