Polycomb repressive complex 2 controls the embryo-to-seedling phase transition.
Polycomb repressive complex 2 controls the embryo-to-seedling phase transition.
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DOI：
10.1371/journal.pgen.1002014
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发表时间：
2011-03
期刊：
影响因子：
4.5
通讯作者：
Schnittger A
中科院分区：
文献类型：
--
作者：
Bouyer D;Roudier F;Heese M;Andersen ED;Gey D;Nowack MK;Goodrich J;Renou JP;Grini PE;Colot V;Schnittger A
多梳抑制复合体2 （Polycomb repression complex 2, PRC2）是表观遗传状态的关键调控因子，可催化组蛋白H3赖氨酸27三甲基化（H3K27me3），这是一种抑制染色质标记。PRC2的组成从人类到植物都是保守的，但PRC2在植物生命早期的功能尚不清楚，除了它是胚乳发育所必需的，胚乳是一种支持胚胎生长的营养组织。绕开了在胚乳中对PRC2的要求，我们获得了受精独立胚乳（FIE）的纯合零突变体，这是果蝇和哺乳动物PRC2不可或缺的组成部分Extra Sex Combs的单一拟南芥同源体。在这里，我们发现H3K27me3沉积在5个突变体中被全基因组消除，这证明了PRC2在植物和动物中放置该标记的基本功能。与动物相比，我们发现拟南芥的初始体形形成不需要PRC2功能。相反，我们的研究结果表明，五个突变种子表现出增强的休眠和萌发缺陷，表明在终止胚胎期方面存在缺陷。发芽后，5个突变苗转向不持续的生殖发育，产生肿瘤样的愈伤组织结构。进一步的全基因组研究表明，在五种幼苗中，只有一小部分PRC2靶点被转录激活，并且这种激活仅在少数情况下伴随着H3K4me3的沉积，H3K4me3是一种与基因活性相关的标记，被认为对H3K27me3起拮抗作用。研究发现，上调的PRC2靶基因在不同层次上起作用，从转录主调控因子到广泛的下游靶标。总的来说，我们的研究结果表明，prc2介导的调控代表了一个强大的系统，控制着发育阶段的转变，不仅从营养期到开花期，而且特别是从胚胎期到幼苗期。通过修饰组蛋白尾部对基因表达进行表观遗传调控是多细胞生物生长发育的基础。组蛋白3 （H3K27me3）赖氨酸27的三甲基化是多梳抑制复合物2 （PRC2）功能的标志，并与基因抑制有关。在这里，我们提出了一个遗传系统的发展，以产生拟南芥PRC2的纯合零突变体。第一个主要发现是H3K27me3在这些突变体中全局丢失。令人惊讶的是，我们发现最初的植物体组织和胚胎发育在很大程度上独立于PRC2的作用，这与动物PRC2突变体的胚胎致死性形成鲜明对比。然而，我们在这里表明，PRC2需要从胚胎阶段切换到幼苗阶段，突变种子表现出增强的休眠和萌发缺陷。事实上，许多控制种子成熟和休眠的基因都是由H3K27me3标记的，并且在PRC2缺失时被上调。陆地植物种子休眠的发明被认为是开花植物进化成功的主要原因之一，PRC2在胚胎到幼苗生长发育过程中的关键作用揭示了保守的分子机制对新功能的适应。
Polycomb repressive complex 2 (PRC2) is a key regulator of epigenetic states catalyzing histone H3 lysine 27 trimethylation (H3K27me3), a repressive chromatin mark. PRC2 composition is conserved from humans to plants, but the function of PRC2 during the early stage of plant life is unclear beyond the fact that it is required for the development of endosperm, a nutritive tissue that supports embryo growth. Circumventing the requirement of PRC2 in endosperm allowed us to generate viable homozygous null mutants for FERTILIZATION INDEPENDENT ENDOSPERM (FIE), which is the single Arabidopsis homolog of Extra Sex Combs, an indispensable component of Drosophila and mammalian PRC2. Here we show that H3K27me3 deposition is abolished genome-wide in fie mutants demonstrating the essential function of PRC2 in placing this mark in plants as in animals. In contrast to animals, we find that PRC2 function is not required for initial body plan formation in Arabidopsis. Rather, our results show that fie mutant seeds exhibit enhanced dormancy and germination defects, indicating a deficiency in terminating the embryonic phase. After germination, fie mutant seedlings switch to generative development that is not sustained, giving rise to neoplastic, callus-like structures. Further genome-wide studies showed that only a fraction of PRC2 targets are transcriptionally activated in fie seedlings and that this activation is accompanied in only a few cases with deposition of H3K4me3, a mark associated with gene activity and considered to act antagonistically to H3K27me3. Up-regulated PRC2 target genes were found to act at different hierarchical levels from transcriptional master regulators to a wide range of downstream targets. Collectively, our findings demonstrate that PRC2-mediated regulation represents a robust system controlling developmental phase transitions, not only from vegetative phase to flowering but also especially from embryonic phase to the seedling stage. Epigenetic regulation of gene expression through modifications of histone tails is fundamental for growth and development of multicellular organisms. The trimethylation of lysine 27 of histone 3 (H3K27me3) is the landmark of Polycomb Repressive Complex2 (PRC2) function and is associated with gene repression. Here we present the development of a genetic system to generate homozygous null mutants of Arabidopsis PRC2. A first major finding is that H3K27me3 is globally lost in these mutants. Surprisingly, we found that initial body plant organization and embryo development is largely independent of PRC2 action, which is in sharp contrast to embryonic lethality of PRC2 mutants in animals. However, we show here that PRC2 is required to switch from embryonic to seedling phase, and mutant seeds showed enhanced dormancy and germination defects. Indeed, many genes controlling seed maturation and dormancy are marked by H3K27me3 and are upregulated upon loss of PRC2. The invention of seed dormancy of land plants is regarded as one of the major reasons for the evolutionary success of flowering plants, and the here-discovered key role of PRC2 during the developmental phase transition from embryo to seedling growth reveals the adaptation of conserved molecular mechanisms to carry out new functions.
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