Shanghai Center for Plant Stress Biology & National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences (CAS), Shanghai, China.
College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, China.
Nat Plants. 2019 Apr;5(4):424-435. doi: 10.1038/s41477-019-0402-3. Epub 2019 Apr 8.
Some overwintering plants acquire competence to flower, after experiencing prolonged cold in winter, through a process termed vernalization. In the crucifer plant Arabidopsis thaliana, prolonged cold induces chromatin-mediated silencing of the potent floral repressor FLOWERING LOCUS C (FLC) by Polycomb proteins. This vernalized state is epigenetically maintained or 'memorized' in warm rendering plants competent to flower in spring, but is reset in the next generation. Here, we show that in early embryogenesis, two homologous B3 domain transcription factors LEAFY COTYLEDON 2 (LEC2) and FUSCA3 (FUS3) compete against two repressive B3-containing epigenome readers and Polycomb partners known as VAL1 and VAL2 for the cis-regulatory cold memory element (CME) of FLC to disrupt Polycomb silencing. Consistently, crystal structures of B3-CME complexes show that B3, B3 and B3 employ a nearly identical binding interface for CME. We further found that LEC2 and FUS3 recruit the scaffold protein FRIGIDA in association with active chromatin modifiers to establish an active chromatin state at FLC, which results in resetting of the silenced FLC to active and erasing the epigenetic parental memory of winter cold in early embryos. Following embryo development, LEC2 and FUS3 are developmentally silenced throughout post-embryonic stages, enabling VALs to bind to the CME again at seedling stages at which plants experience winter cold. Our findings illustrate how overwintering crucifer annuals or biennials in temperate climates employ a subfamily of B3 domain proteins to switch on, off and on again the expression of a key flowering gene in the embryo-to-plant-to-embryo cycle, and thus to synchronize growth and development with seasonal temperature changes in their life cycles.
一些越冬植物在冬季经历长时间寒冷后，通过一个称为春化的过程获得开花能力。在十字花科植物拟南芥中，长时间的寒冷诱导多梳蛋白介导的花抑制因子 FLOWERING LOCUS C（FLC）的染色质沉默。这种春化状态在温暖的植物中被表观遗传维持或“记忆”，使其有能力在春天开花，但在下一代中被重置。在这里，我们表明在早期胚胎发生中，两个同源的 B3 结构域转录因子 LEAFY COTYLEDON 2（LEC2）和 FUSCA3（FUS3）与两个抑制性 B3 包含的表观基因组读取器和多梳蛋白伙伴 VAL1 和 VAL2 竞争，以获得 FLC 的顺式调控冷记忆元件（CME），从而破坏多梳蛋白沉默。一致地，B3-CME 复合物的晶体结构表明 B3、B3 和 B3 几乎使用相同的结合界面用于 CME。我们进一步发现 LEC2 和 FUS3 与活性染色质修饰物一起募集支架蛋白 FRIGIDA，在 FLC 处建立活性染色质状态，导致沉默的 FLC 被重置为活性，并在早期胚胎中擦除冬季寒冷的表观遗传亲本记忆。在胚胎发育之后，LEC2 和 FUS3 在整个胚胎后阶段被发育性沉默，使 VAL 能够在植物经历冬季寒冷的幼苗阶段再次结合到 CME。我们的发现说明了在温带气候中越冬的十字花科一年生或二年生植物如何利用 B3 结构域蛋白的一个亚家族来在胚胎到植物到胚胎的循环中打开、关闭和再次打开关键开花基因的表达，从而使其生长和发育与生命周期中的季节性温度变化同步。
