Diurnal regulation of SDG2 and JMJ14 by circadian clock oscillators orchestrates histone modification rhythms in Arabidopsis

First author: Qingxin Song; Affiliations: The University of Texas at Austin (德克萨斯大学奥斯汀分校): Austin, USA

Corresponding author: Z. Jeffrey Chen

Circadian rhythms modulate growth and development in all organisms through interlocking transcriptional-translational feedback loops. The transcriptional loop involves chromatin modifications of central circadian oscillators in mammals and plants. However, the molecular basis for rhythmic epigenetic modifications and circadian regulation is poorly understood. Here we report a feedback relationship between diurnal regulation of circadian clock genes and histone modifications in Arabidopsis. On one hand, the circadian oscillators CCA1 and LHY regulate diurnal expression of genes coding for the eraser (JMJ14) directly and writer (SDG2) indirectly for H3K4me3 modification, leading to rhythmic H3K4me3 changes in target genes. On the other hand, expression of circadian oscillator genes including CCA1 and LHY is associated with H3K4me3 levels and decreased in the sdg2 mutant but increased in the jmj14 mutant. At the genome-wide level, diurnal rhythms of H3K4me3 and another histone mark H3K9ac are associated with diurnal regulation of 20–30% of the expressed genes. While the majority (86%) of H3K4me3 and H3K9ac target genes overlap, only 13% of morning-phased and 22% of evening-phased genes had both H3K4me3 and H3K9ac peaks, suggesting specific roles of different histone modifications in diurnal gene expression. Circadian clock genes promote diurnal regulation of SDG2 and JMJ14 expression, which in turn regulate rhythmic histone modification dynamics for the clock and its output genes. This reciprocal regulatory module between chromatin modifiers and circadian clock oscillators orchestrates diurnal gene expression that governs plant growth and development.

在所有生物中，昼夜节律通过联系转录-翻译的反馈回路来调控生长和发育。在动植物中，转录回路涉及到核心生物钟振荡器的染色质修饰。然而，表观修饰的节律性与昼夜调控的分子基础还不是很清楚。本文中，作者报道了拟南芥中一个生物钟基因日调控与组蛋白修饰之间的反馈关系。一方面，生物钟振荡器CCA1和LHY直接调控H3K4me3修饰“eraser”基因JMJ14的日间表达，间接调控H3K4me3修饰“writer”基因SDG2的日间表达，从而影响靶基因上的H3K4me3节律性变化。另一方面，生物钟振荡器基因CCA1和LHY的表达与H3K4me3的水平相关，并且在sdg2突变体中降低，而在jmj14突变体中升高。在全基因组水平，H3K4me3和另外一个组蛋白标记H3K9ac的日间节律与20–30%表达基因的日间调控相关。大多数的H3K4me3和H3K9ac靶基因存在重叠，仅有13%的晨间基因和22%晚间基因均存在H3K4me3和H3K9ac峰值，说明不同的组蛋白修饰对于日间基因的表达存在各自的特定作用。生物钟基因促进SDG2和JMJ14基因表达的日间调控，反过来调控生物钟极其输出基因的组蛋白修饰节律性动态。这种染色质修饰基因与生物钟振荡器之间相互的调控模块控制日间基因表达，从而保证植物的生长和发育。

通讯：Z. Jeffrey Chen  (https://polyploidy.biosci.utexas.edu/polyploidy/principle-investigator)

个人简介：1984年，浙江农业大学，学士；1987年，南京农业大学，硕士；1993年，德克萨斯A&M大学，博士；1993-1995年，明尼苏达大学，博士后；1995-1999年，华盛顿大学，博士后 。

研究方向：植物多倍化和杂种优势的遗传和表观基础，及其对于作物驯化和改良的影响。

doi: https://doi.org/10.1186/s13059-019-1777-1

Journal: Genome Biology

Published date: August 20, 2019