State Key Laboratory of Genetic Engineering, Collaborative Innovation Center for Genetics and Development, International Associated Laboratory of CNRS-Fudan-HUNAU on Plant Epigenome Research, Department of Biochemistry, Institute of Plant Biology, School of Life Sciences, Fudan University, Shanghai, 200438, China.
Universitè de Strasbourg, CNRS, IBMP UPR 2357, Strasbourg, F-67000, France.
Plant J. 2020 Aug;103(3):1010-1024. doi: 10.1111/tpj.14780. Epub 2020 May 12.
Histones are highly basic proteins involved in packaging DNA into chromatin, and histone modifications are fundamental in epigenetic regulation in eukaryotes. Among the numerous chromatin modifiers identified in Arabidopsis (Arabidopsis thaliana), MORF-RELATED GENE (MRG)1 and MRG2 have redundant functions in reading histone H3 lysine 36 trimethylation (H3K36me3). Here, we show that MRG2 binds histone chaperones belonging to the NUCLEOSOME ASSEMBLY PROTEIN 1 (NAP1) family, including NAP1-RELATED PROTEIN (NRP)1 and NRP2. Characterization of the loss-of-function mutants mrg1 mrg2, nrp1 nrp2 and mrg1 mrg2 nrp1 nrp2 revealed that MRG1/MRG2 and NRP1/NRP2 regulate flowering time through fine-tuning transcription of floral genes by distinct molecular mechanisms. In particular, the physical interaction between NRP1/NRP2 and MRG1/MRG2 inhibited the binding of MRG1/MRG2 to the transcription factor CONSTANS (CO), leading to a transcriptional repression of FLOWERING LOCUS T (FT) through impeded H4K5 acetylation (H4K5ac) within the FT chromatin. By contrast, NRP1/NRP2 and MRG1/MRG2 act together, likely in a multiprotein complex manner, in promoting the transcription of FLOWERING LOCUS C (FLC) via an increase of both H4K5ac and H3K9ac in the FLC chromatin. Because the expression pattern of FLC represents the major category of differentially expressed genes identified by genome-wide RNA-sequencing analysis in the mrg1 mrg2, nrp1 nrp2 and mrg1 mrg2 nrp1 nrp2 mutants, it is reasonable to speculate that the NRP1/NRP2-MRG1/MRG2 complex may be involved in transcriptional activation of genes beyond FLC and flowering time control.
组蛋白是高度碱性的蛋白质，参与将 DNA 包装成染色质，组蛋白修饰是真核生物中表观遗传调控的基础。在拟南芥（Arabidopsis thaliana）中鉴定的众多染色质修饰因子中，MORF-RELATED GENE（MRG）1 和 MRG2 在读取组蛋白 H3 赖氨酸 36 三甲基化（H3K36me3）方面具有冗余功能。在这里，我们表明 MRG2 与属于核小体组装蛋白 1（NAP1）家族的组蛋白伴侣结合，包括 NAP1-RELATED PROTEIN（NRP）1 和 NRP2。mrg1 mrg2、nrp1 nrp2 和 mrg1 mrg2 nrp1 nrp2 功能丧失突变体的特征表明，MRG1/MRG2 和 NRP1/NRP2 通过不同的分子机制精细调节花基因的转录来调节开花时间。特别是，NRP1/NRP2 与 MRG1/MRG2 之间的物理相互作用抑制了 MRG1/MRG2 与转录因子 CONSTANS（CO）的结合，导致通过阻碍 FT 染色质内的 FT 转录因子 CONSTANS（CO）的结合，FT 的转录受到抑制。相反，NRP1/NRP2 和 MRG1/MRG2 共同作用，可能以多蛋白复合物的方式，通过增加 FLC 染色质中的 H4K5ac 和 H3K9ac 来促进 FLOWERING LOCUS C（FLC）的转录。由于 FLC 的表达模式代表了在 mrg1 mrg2、nrp1 nrp2 和 mrg1 mrg2 nrp1 nrp2 突变体中通过全基因组 RNA-seq 分析鉴定的差异表达基因的主要类别，因此可以合理地推测 NRP1/NRP2-MRG1/MRG2 复合物可能参与 FLC 以外的基因的转录激活和开花时间控制。
