Arabidopsis COMPASS-like complexes mediate histone H3 lysine-4 trimethylation to control floral transition and plant development.
Arabidopsis COMPASS-like complexes mediate histone H3 lysine-4 trimethylation to control floral transition and plant development.
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DOI：
10.1371/journal.pgen.1001330
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发表时间：
2011-03
期刊：
影响因子：
4.5
通讯作者：
He Y
中科院分区：
文献类型：
--
作者：
Jiang D;Kong NC;Gu X;Li Z;He Y
在真核生物中，组蛋白H3赖氨酸-4 （H3K4）甲基化与转录基因相关。在果蝇和哺乳动物中，H3K4的二甲基化和三甲基化都与基因激活有关。与动物相比，拟南芥中H3K4的三甲基化，而不是H3K4的单甲基化或二甲基化，与转录激活有关。在酵母和哺乳动物中，H3K4甲基化是由被称为COMPASS或COMPASS样的H3K4甲基转移酶复合物催化的。在这里，我们报道了人类COMPASS和COMPASS样复合物核心成分Ash2、RbBP5和WDR5的拟南芥同源物在营养和生殖发育过程中形成一个核亚复合物，该亚复合物可能与多种推测的H3K4甲基转移酶相关。拟南芥Ash2 RELATIVE （ASH2R）功能缺失导致全基因组H3K4三甲基化显著降低，但二甲基化和单甲基化不显著。ASH2R或RbBP5同源基因的敲低会抑制拟南芥花的关键抑制因子开花位点C （FLC）和FLC同源基因的表达，从而加速花的转变。在体内，ASH2R与FLC和FLC同源物的染色质结合，是H3K4三甲基化所必需的，但不是这些位点的H3K4二甲基化所必需的；ASH2R的过表达导致其靶基因FLC和FLC同源基因中H3K4三甲基化升高，而非H3K4二甲基化，导致这些基因的表达被激活，从而导致开花晚。这些结果强烈提示FLC及其同系物中的H3K4三甲基化可以激活它们的表达，为H3K4三甲基化积累可以激活真核基因表达提供了具体证据。此外，我们的研究结果表明，拟南芥中存在多个compass样复合物，这些复合物在靶基因中沉积三甲基而不是二甲基或单甲基H3K4以促进其表达，这为在拟南芥中观察到的H3K4三甲基化（而不是H3K4二甲基化）与活性基因表达的偶联提供了分子解释。组蛋白可以共价修饰，组蛋白修饰调节染色质结构和基因转录。其中一种修饰是组蛋白H3赖氨酸-4 （H3K4）甲基化，可以是单甲基化、二甲基化或三甲基化。在果蝇和哺乳动物等动物中，H3K4的二甲基化和三甲基化都与活跃的基因表达有关。与动物相比，在开花植物拟南芥中，只有H3K4三甲基化与基因转录激活有关。在哺乳动物中，H3K4甲基化是由被称为compass样的H3K4甲基转移酶复合物催化的。在这里，我们报道了compass样H3K4甲基转移酶复合物在拟南芥中存在。核心复合蛋白的功能缺失导致拟南芥全基因组H3K4三甲基化显著降低，但二甲基化或单甲基化不会降低。我们对这些compass样复合物的几个直接靶基因的分析表明，它们介导三甲基的沉积，而不是二甲基H3K4在这些位点上激活它们的表达，为H3K4三甲基化积累可以激活真核基因表达的观点提供了具体的证据。此外，我们的研究结果为在拟南芥中观察到的H3K4三甲基化而非二甲基化与活性基因表达的偶联提供了分子解释。此外，我们发现H3K4三甲基化调节叶片生长发育、开花和胚胎发育。
Histone H3 lysine-4 (H3K4) methylation is associated with transcribed genes in eukaryotes. In Drosophila and mammals, both di- and tri-methylation of H3K4 are associated with gene activation. In contrast to animals, in Arabidopsis H3K4 trimethylation, but not mono- or di-methylation of H3K4, has been implicated in transcriptional activation. H3K4 methylation is catalyzed by the H3K4 methyltransferase complexes known as COMPASS or COMPASS-like in yeast and mammals. Here, we report that Arabidopsis homologs of the COMPASS and COMPASS-like complex core components known as Ash2, RbBP5, and WDR5 in humans form a nuclear subcomplex during vegetative and reproductive development, which can associate with multiple putative H3K4 methyltransferases. Loss of function of ARABIDOPSIS Ash2 RELATIVE (ASH2R) causes a great decrease in genome-wide H3K4 trimethylation, but not in di- or mono-methylation. Knockdown of ASH2R or the RbBP5 homolog suppresses the expression of a crucial Arabidopsis floral repressor, FLOWERING LOCUS C (FLC), and FLC homologs resulting in accelerated floral transition. ASH2R binds to the chromatin of FLC and FLC homologs in vivo and is required for H3K4 trimethylation, but not for H3K4 dimethylation in these loci; overexpression of ASH2R causes elevated H3K4 trimethylation, but not H3K4 dimethylation, in its target genes FLC and FLC homologs, resulting in activation of these gene expression and consequent late flowering. These results strongly suggest that H3K4 trimethylation in FLC and its homologs can activate their expression, providing concrete evidence that H3K4 trimethylation accumulation can activate eukaryotic gene expression. Furthermore, our findings suggest that there are multiple COMPASS-like complexes in Arabidopsis and that these complexes deposit trimethyl but not di- or mono-methyl H3K4 in target genes to promote their expression, providing a molecular explanation for the observed coupling of H3K4 trimethylation (but not H3K4 dimethylation) with active gene expression in Arabidopsis. Histones can be covalently modified and histone modifications regulate chromatin structure and gene transcription. One such modification is histone H3 lysine-4 (H3K4) methylation, which can be mono-, di-, or tri-methylated. In animals such as fruitfly and mammals, both di- and tri-methylation of H3K4 are associated with active gene expression. In contrast to animals, in the flowering plant Arabidopsis only H3K4 trimethylation has been implicated in gene transcriptional activation. H3K4 methylation is catalyzed by the H3K4 methyltransferase complexes known as COMPASS-like in mammals. Here, we report that COMPASS-like H3K4 methyltransferase complexes exist in Arabidopsis. Loss of function of a core complex protein causes a great decrease in Arabidopsis genome-wide H3K4 trimethylation, but not in di- or mono-methylation. Our analyses of several direct target genes of these COMPASS-like complexes show that they mediate deposition of trimethyl but not dimethyl H3K4 in these loci to activate their expression, providing concrete evidence for the notion that H3K4 trimethylation accumulation can activate eukaryotic gene expression. Furthermore, our findings provide a molecular explanation for the observed coupling of trimethylation but not dimethylation of H3K4 with active gene expression in Arabidopsis. In addition, we found that H3K4 trimethylation regulates leaf growth and development, flowering, and embryo development.
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