Role of the chloroplast ubiquitin E3 ligase SP1 in abiotic stress tolerance in plants

随着人口迅速增长，到2050年将达到90亿，而且由于自然资源面临的压力不断增加，提高作物产量和抵御气候变化和次优生长条件的驱动力比以往任何时候都更强大。为了满足这些需求，必须开发改良的作物品种。通过对模式植物塔勒水芹（Arabidopsis thaliana）的研究，我们最近取得了一项可能对粮食安全具有重要意义的重大突破：我们发现了一个名为SP1的基因，它控制着植物生长的重要方面，并发现它在植物应对水分胁迫和高盐度等不利环境条件（统称为非生物胁迫）方面很重要。通过修饰SP1的表达，可以使塔勒水芹植物对这种胁迫更耐受。本课题研究SP1基因，通过对小麦的研究，阐明SP1基因与逆境反应的关系，并探讨其在作物改良中的潜在用途。SP1基因调节植物细胞内称为叶绿体的结构的发育。叶绿体是正常的细胞成分（即，它们是细胞器），在许多方面它们定义了植物。它们含有绿色色素叶绿素，负责光合作用--这是一个捕捉阳光能量并利用它为细胞活动提供动力的重要过程，例如通过将空气中的二氧化碳转化为糖。由于光合作用是能量输入到生命世界的唯一重要机制，叶绿体不仅对植物而且对地球上的所有生命都非常重要。但光合作用也有可能产生有毒的"活性氧"（ROS），特别是在条件具有挑战性的情况下，因此叶绿体在应激反应中也起着关键作用。（这是它们作为自由生活的光合细菌进化起源的遗迹），因此可以制造一些自己的蛋白质，形成叶绿体所需的数千种不同蛋白质中的大多数由细胞核中的基因编码。这些核编码的蛋白质是在叶绿体外的细胞基质（称为细胞质）中产生的。由于每个叶绿体都被双层膜包围，它们已经进化出复杂的蛋白质输入机制，驱动从细胞质中摄取蛋白质。这种机器包括两个分子机器：一个在被称为TOC（“叶绿体外膜处的易位子”的缩写）的外膜中，另一个在被称为TIC的内膜中。每个机器都由几种不同的蛋白质组成，在输入过程中相互配合。SP1基因编码一种称为“泛素E3连接酶”的调节因子。这些调节器通过标记不需要的蛋白质来清除它们。SP1 E3连接酶特异性地作用于TOC机制的组分，从而控制TOC组成和功能，使得仅输入所需的蛋白质。当叶绿体必须经历重大的功能变化时，例如在适应胁迫期间，这种控制是重要的。我们认为，SP1的行为在胁迫期间，以限制进口的光合机构的新组件，以减弱光合活性，从而减轻压力的负面影响。通过限制胁迫期间的光合作用，SP1降低了ROS过量产生的可能性，使植物不太可能遭受严重或致命的胁迫相关损害。在这个项目中获得的知识将提高我们对植物对不利环境的反应的理解，并可能提高作物对这种条件的适应性。干旱和盐碱化是影响作物产量的最重要因素之一，每年仅干旱造成的全球作物损失估计就达100亿美元。我们认为，我们与SP1的合作可能有助于减轻此类损失。

With the human population growing rapidly and set to reach 9 billion by 2050, and because of ever increasing pressure on natural resources, the drivers for increased crop yields and for resilience to climate change and sub-optimal growing conditions are stronger than ever. To meet these demands it will be essential to develop improved crop varieties. Through research on the model plant thale cress (Arabidopsis thaliana), we recently made a significant breakthrough that may have important implications for food security: We discovered a gene called SP1 that controls important aspects of plant growth, and found it to be important in plant responses to adverse environmental conditions such as water stress and high salinity (collectively, abiotic stresses). By modifying SP1 expression, thale cress plants can be made more tolerant of such stresses. In this project, we will study the SP1 gene to elucidate how it is involved in stress responses, and investigate its potential use for crop improvement by conducting studies in wheat.The SP1 gene regulates the development of structures inside plant cells called chloroplasts. Chloroplasts are normal cellular constituents (i.e., they are organelles), and in many ways they define plants. They contain the green pigment chlorophyll and are responsible for photosynthesis - the vital process that captures sunlight energy and uses it to power the activities of the cell, for example by converting carbon dioxide from the air into sugars. As photosynthesis is the only significant mechanism of energy-input into the living world, chloroplasts are of huge importance, not just to plants but to all life on Earth. But photosynthesis also has the potential to generate toxic "reactive oxygen species" (ROS), particularly when conditions are challenging, and so chloroplasts have a critical role in stress responses too.Although chloroplasts do contain DNA (a relic of their evolutionary origins as free-living photosynthetic bacteria) and so can make some of their own proteins, most of the thousands of different proteins needed to form a chloroplast are encoded by genes in the cell nucleus. These nucleus-encoded proteins are made outside of the chloroplast in the cellular matrix known as the cytosol. As chloroplasts are each surrounded by a double membrane envelope, they have evolved sophisticated protein import machinery that drives the uptake of proteins from the cytosol. This machinery comprises two molecular machines: one in the outer envelope membrane called TOC (an abbreviation of "Translocon at the outer membrane of chloroplasts") and another in the inner membrane called TIC. Each machine is composed of several different proteins that cooperate during import.The SP1 gene encodes a type of regulatory factor called a "ubiquitin E3 ligase". Such regulators work by labelling-up unwanted proteins to target them for removal. The SP1 E3 ligase specifically acts on components of the TOC machinery, thereby controlling TOC composition and function so that only the desired proteins are imported. Such control is important when chloroplasts must undergo major functional changes, for example during adaptation to stress. We believe that SP1 acts during stress to limit the import of new components of the photosynthetic apparatus, in order to attenuate photosynthetic activity and so mitigate the negative effects of stress. By limiting photosynthesis during stress, SP1 reduces the potential for ROS overproduction such that plants are less likely to suffer serious or fatal stress-related damage.Knowledge gained during this project will improve our understanding of plant responses to adverse environments, and may enable improved resilience of crops to such conditions. Drought and salinity are among the most significant factors affecting crop yields, with annual global crop losses due to drought alone estimated at $10bn. We believe that our work with SP1 may help to alleviate such losses.