Institute of Genetics, Heinrich-Heine-University Duesseldorf, Duesseldorf, Germany.
PLoS Genet. 2011 Apr;7(4):e1002040. doi: 10.1371/journal.pgen.1002040. Epub 2011 Apr 7.
During growth of multicellular organisms, identities of stem cells and differentiated cells need to be maintained. Cell fate is epigenetically controlled by the conserved Polycomb-group (Pc-G) proteins that repress their target genes by catalyzing histone H3 lysine 27 trimethylation (H3K27me3). Although H3K27me3 is associated with mitotically stable gene repression, a large fraction of H3K27me3 target genes are tissue-specifically activated during differentiation processes. However, in plants it is currently unclear whether H3K27me3 is already present in undifferentiated cells and dynamically regulated to permit tissue-specific gene repression or activation. We used whole-genome tiling arrays to identify the H3K27me3 target genes in undifferentiated cells of the shoot apical meristem and in differentiated leaf cells. Hundreds of genes gain or lose H3K27me3 upon differentiation, demonstrating dynamic regulation of an epigenetic modification in plants. H3K27me3 is correlated with gene repression, and its release preferentially results in tissue-specific gene activation, both during differentiation and in Pc-G mutants. We further reveal meristem- and leaf-specific targeting of individual gene families including known but also likely novel regulators of differentiation and stem cell regulation. Interestingly, H3K27me3 directly represses only specific transcription factor families, but indirectly activates others through H3K27me3-mediated silencing of microRNA genes. Furthermore, H3K27me3 targeting of genes involved in biosynthesis, transport, perception, and signal transduction of the phytohormone auxin demonstrates control of an entire signaling pathway. Based on these and previous analyses, we propose that H3K27me3 is one of the major determinants of tissue-specific expression patterns in plants, which restricts expression of its direct targets and promotes gene expression indirectly by repressing miRNA genes.
在多细胞生物的生长过程中，需要维持干细胞和分化细胞的身份。细胞命运由保守的多梳组（Pc-G）蛋白通过催化组蛋白 H3 赖氨酸 27 三甲基化（H3K27me3）来表观遗传控制。尽管 H3K27me3 与有丝分裂稳定的基因抑制有关，但在分化过程中，很大一部分 H3K27me3 靶基因是组织特异性激活的。然而，目前在植物中尚不清楚 H3K27me3 是否已经存在于未分化细胞中，并通过动态调节来允许组织特异性基因抑制或激活。我们使用全基因组平铺阵列来鉴定茎尖分生组织未分化细胞和分化叶片细胞中 H3K27me3 的靶基因。数百个基因在分化时获得或失去 H3K27me3，这表明植物中一种表观遗传修饰的动态调节。H3K27me3 与基因抑制相关，其释放优先导致组织特异性基因激活，这既发生在分化过程中，也发生在 Pc-G 突变体中。我们进一步揭示了单个基因家族在分生组织和叶片中的特异性靶向，包括已知的但也可能是新的分化和干细胞调控的调控因子。有趣的是，H3K27me3 仅直接抑制特定的转录因子家族，但通过 H3K27me3 介导的 microRNA 基因沉默间接激活其他家族。此外，H3K27me3 靶向参与植物激素生长素生物合成、运输、感知和信号转导的基因，证明了对整个信号通路的控制。基于这些和以前的分析，我们提出 H3K27me3 是植物组织特异性表达模式的主要决定因素之一，它限制了其直接靶基因的表达，并通过抑制 microRNA 基因间接促进基因表达。
