A Molecular Framework for Environment Responsive Chromatin Modification in Plants

为了在不断变化的环境中生存，植物必须能够感知周围环境并改变它们的生长和发育方式。此外，与动物相比，植物不能移动，因此它们必须进化出不同的方式来快速准确地做到这一点。动物和植物对环境做出反应的一种方式是通过修改支持其DNA的蛋白质支架（染色质）中的特定蛋白质（组蛋白）来改变其基因表达。例如，一种名为“多梳抑制复合物2”（PRC 2）的蛋白质复合物参与向组蛋白添加一种名为甲基化的化学标记，从而导致基因关闭。PRC 2存在于动物和植物中，但有趣的是，大多数植物都有多种不同的蛋白质组成复合物，这意味着它们有更广泛的潜在组合。这意味着植物有一个更大的“工具箱”来控制染色质甲基化的特异性和时间。植物中的PRC 2参与了各种不同的过程，包括调节种子发育和萌发，以及协调冬季后春季的开花。在一些情况下，甲基化的特定基因是已知的。然而，我们仍然对PRC 2如何直接感知外部世界并在需要时触发这些变化知之甚少。我们最近发现，一种名为VERNALIZATION 2（VRN 2）的植物PRC 2蛋白通常非常不稳定，但可以在某些环境条件下积累，包括在洪水和暴露于寒冷的温度下。这表明VRN 2可能在开花植物中充当PRC 2的“传感器”组件，确保某些基因的甲基化仅在正确的环境条件下触发。然而，目前我们仍然不太清楚一旦VRN 2稳定下来会发生什么。在拟南芥（一种植物模式生物）中使用一系列分子、生物化学、遗传和细胞生物学方法，我们试图通过回答几个及时的问题来解决我们知识中的这一空白：（1）VRN 2的增加和减少如何影响其他PRC 2变体并塑造PRC 2景观？(2)稳定VRN 2-PRC 2的全基因组靶点是什么？(3)环境引发的VRN 2增加如何转化为植物发育变化？通过在三个综合工作包中使用不同的实验方法来回答这些问题，我们将发现关于植物如何能够协调染色质甲基化以修改发育以响应其环境的有价值的新知识。这项工作将为我们理解植物如何直接翻译环境变化提供一个步骤这些变化可以通过将环境因素（例如季节或洪水等压力）转化为染色质修饰来重新编程基因表达，以使生长和发育与主要条件保持一致。至关重要的是，我们以前表明，控制VRN 2丰度的机制在开花植物中广泛保守-包括作物物种。因此，我们在这项工作中发现的基本新见解应该具有长期影响，因为它们将确定生物技术专家和植物育种家可以用来改善与生长和抗逆能力相关的农业重要性状的新分子靶标，这是确保全球粮食安全的关键目标。

To survive in changing environments, plants have to be able to sense their surroundings and modify how they grow and develop. Furthermore, in contrast to animals, plants cannot move and so they have had to evolve different ways in which to quickly and accurately do this. One way in which both animals and plants respond to the environment is through altering their gene expression by modifying specific proteins (histones) in the protein scaffold (chromatin) that supports their DNA. For example, a protein complex called the 'polycomb repressive complex 2' (PRC2) is involved in adding a chemical mark called methylation to histones, which causes genes to be switched off. The PRC2 is found in animals and plants, but interestingly most plants have a larger variety of the different proteins making up the complex, which means they have a broader range of potential combinations. This means that plants have a larger 'tool kit' for controlling the specificity and timing of chromatin methylation.The PRC2 in plants is involved in a variety of different processes, including the regulation of seed development and germination, and coordinating flowering in spring after winter. In several cases the specific genes that are methylated are known. However, we still know very little about how the PRC2 directly senses the outside world to trigger these changes only when they are needed. We recently showed that a plant PRC2 protein called VERNALIZATION2 (VRN2) is usually very unstable, but can accumulate under certain environmental conditions, including during flooding and exposure to cold temperatures. This suggests that VRN2 might act as a 'sensor' component of the PRC2 in flowering plants that ensures methylation of certain genes is only triggered under the right environmental conditions. However, at present we still do not know much about what happens once VRN2 is stabilised. Using a range of molecular, biochemistry, genetic and cell biology approaches in Arabidopsis (a plant model organism) we seek to address this gap in our knowledge by answering several timely questions: (1) How do increases and decreases in VRN2 affect the other PRC2 variants and shape the PRC2 landscape? (2) What are the genome-wide targets of stable VRN2-PRC2? (3) How do environment triggered increases in VRN2 translate into plant developmental changes? By answering these questions using diverse experimental approaches across three integrated work packages, we will uncover valuable new knowledge about how plants are able to coordinate chromatin methylation to modify development in response to their environment.This work will provide a step-change in our understanding of how plants directly translate environmental changes (e.g. the seasons, or stresses such as floods) into chromatin modifications that reprogram gene expression to align growth and development with the prevailing conditions. Crucially, we previously showed that the mechanism controlling VRN2 abundance is widely conserved in flowering plants - including crop species. As such, the fundamental new insights we uncover with this work should have longer term impact, as they will identify new molecular targets that biotechnologists and plant breeders can use to improve agriculturally important traits related to growth and stress-resilience, which is a key aim for ensuring global food security.