Integrative Analysis from the Epigenome to Translatome Uncovers Patterns of Dominant Nuclear Regulation during Transient Stress

Integrative Analysis from the Epigenome to Translatome Uncovers Patterns of Dominant Nuclear Regulation during Transient Stress
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DOI:
10.1105/tpc.19.00463
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发表时间:
2019-11-01
期刊:
影响因子:
11.6
通讯作者:
Bailey-Serres, Julia
Bailey-Serres, Julia
中科院分区:
生物学1区
文献类型:
--
作者:
Lee, Travis A.;Bailey-Serres, Julia

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基因调控是一个动态过程,涉及从染色质重塑到优先翻译等变化。为了了解整合的核和细胞质基因调控动态,我们进行了一项涵盖拟南芥幼苗对缺氧和复氧反应的表观基因组到翻译组的调查。这包括染色质测定(检查组蛋白、可及性、RNA 聚合酶 II [RNAPII] 和转录因子结合)和三种 RNA 测定(核、聚腺苷酸化和核糖体相关)。核调节的动态模式区分了应激诱导的 mRNA 和生长相关的 mRNA。缺氧反应基因转录本的快速上调及其优先翻译通常伴随着染色质可及性的增加、RNAPII 的参与以及组蛋白 2A.Z 关联的减少。缺氧促进了热应激转录物的逐渐上调,RNAPII 结合和核 RNA 增加证明了这一点,多腺苷酸化 RNA 水平仅在长时间应激或复氧后才会升高。快速上调基因的启动子与逐渐上调基因的启动子分别富集乙烯反应性和热休克因子转录因子的顺​​式元件。与生长相关的基因,包括许多编码胞浆核糖体蛋白的基因,经历了明显的组蛋白修饰,但在应激期间保留了 RNAPII 参与并积累了核转录本。重新通气后,逐渐上调且与生长相关的基因转录物迅速动员至核糖体。因此,核小体、转录本合成、积累和翻译的多级核调控可定制瞬时应激反应。
Gene regulation is a dynamic process involving changes ranging from the remodeling of chromatin to preferential translation. To understand integrated nuclear and cytoplasmic gene regulatory dynamics, we performed a survey spanning the epigenome to translatome of Arabidopsis (Arabidopsis thaliana) seedlings in response to hypoxia and reoxygenation. This included chromatin assays (examining histones, accessibility, RNA polymerase II [RNAPII], and transcription factor binding) and three RNA assays (nuclear, polyadenylated, and ribosome-associated). Dynamic patterns of nuclear regulation distinguished stress-induced and growth-associated mRNAs. The rapid upregulation of hypoxia-responsive gene transcripts and their preferential translation were generally accompanied by increased chromatin accessibility, RNAPII engagement, and reduced Histone 2A.Z association. Hypoxia promoted a progressive upregulation of heat stress transcripts, as evidenced by RNAPII binding and increased nuclear RNA, with polyadenylated RNA levels only elevated after prolonged stress or reoxygenation. Promoters of rapidly versus progressively upregulated genes were enriched for cis-elements of ethylene-responsive and heat shock factor transcription factors, respectively. Genes associated with growth, including many encoding cytosolic ribosomal proteins, underwent distinct histone modifications, yet retained RNAPII engagement and accumulated nuclear transcripts during the stress. Upon reaeration, progressively upregulated and growth-associated gene transcripts were rapidly mobilized to ribosomes. Thus, multilevel nuclear regulation of nucleosomes, transcript synthesis, accumulation, and translation tailor transient stress responses.