Uncovering how plant pathogens take control of chloroplast protein import to limit chloroplast-mediated immunity

我们这个时代的一个关键全球挑战是提高农业产量，使其对压力和疾病具有弹性。人口的快速增长(到2050年将超过90亿)和人为气候变化共同给粮食安全和自然资源带来了越来越大的压力，因此出现了这一当务之急。为了迎接这一挑战，开发改良作物品种至关重要。通过对模式植物拟南芥的研究，我们以前在这方面取得了重要的突破：我们发现了一个名为SP1的基因，它通过一个名为“ChLORAD”的过程控制植物生长的各个方面；我们还展示了植物如何对干旱和盐碱(所谓的非生物胁迫)等不利环境条件做出有效反应。我们的最新结果(未发表，但在这里介绍)揭示了SP1在植物免疫中的另一个至关重要的功能，即植物抵御植物病原体威胁的方式。在这个项目中，我们将进行实验，以详细了解SP1的这一新功能；通过这样做，我们将为植物免疫的机制提供重要的新线索。SP1基因控制植物细胞内称为叶绿体的结构的形成和操作。叶绿体是正常的细胞成分(即细胞器)，它们定义了植物。它们含有绿色色素叶绿素，负责光合作用，光合作用利用阳光为细胞的活动提供动力。由于光合作用是向生物世界输入能量的唯一重要机制，叶绿体不仅对植物，而且对地球上的所有生命都具有巨大的重要性。叶绿体在植物免疫中也起着至关重要的作用，因此也是作物抗病工程的理想靶标。叶绿体由数千种不同的蛋白质组成，其中大部分由细胞核中的基因编码，因此在细胞基质中的叶绿体外合成，称为细胞质。由于每个叶绿体都被一个双膜层包围，因此需要复杂的设备来将这些蛋白质引入叶绿体。这包括两个分子机器，每个膜上一个，称为TOC(叶绿体外膜转运子)和TIC。每台机器由几种不同的蛋白质组成，它们协同工作。SP1基因编码一种被称为“泛素E3连接酶”的调节因子。这样的监管机构通过标记不需要的蛋白质来针对它们进行去除。SP1 E3连接酶介导某些TOC组分的去除，进而影响叶绿体输入的蛋白质。这种控制使植物能够在发育和适应逆境的过程中改变其叶绿体的功能。在非生物胁迫期间，SP1抑制光合作用机械部件的输入，从而限制光合作用。这看起来似乎适得其反，但实际上，在压力条件下，光合作用会过度产生被称为“ROS”的有毒化学物质。因此，在这些时候通过降低光合作用，植物更有可能存活下来。虽然ROS如果过度生产是有害的，但它们确实在免疫过程中作为信号发挥了有益的作用，通过协调抗病原体防御。我们的结果表明，病原体已经进化出机制，在感染过程中促进SP1的活性，限制光合作用，从而减少促进防御的ROS的合成。实际上，病原体颠覆了植物应对非生物胁迫的系统。我们将研究SP1在免疫中的作用，并阐明病原体如何影响SP1的活性。我们还将研究SP1对不同病原体的免疫相关功能，以及在作物中的功能。总体而言，我们将加强对植物免疫的了解，这是开发抗病能力提高的作物的关键。

A key global challenge of our era is to deliver increased agricultural yields that have resilience to stress and disease. This imperative arises because of rapid human population growth (set to exceed 9 billion by 2050) and anthropogenic climate change, which together place ever increasing pressures on food security and natural resources. To meet this challenge, it will be crucial to develop improved crop varieties. Through research on the model plant Arabidopsis, we previously made important breakthroughs that are pertinent in this regard: We discovered a gene called SP1 that controls diverse aspects of plant growth via a process named "CHLORAD"; and we showed how SP1 is needed for plants to mount effective responses to adverse environmental conditions like drought and salinity (so-called abiotic stresses).Our latest results (which are unpublished but presented here) uncover another, vitally important function of SP1, in plant immunity - i.e., in the way plants defend themselves against the threat of disease posed by plant pathogens. In this project, we will perform experiments to understand this new function of SP1 in detail; and, in doing so, we will shed significant new light on the mechanisms of plant immunity.The SP1 gene controls the formation and operation of structures inside plant cells called chloroplasts. Chloroplasts are normal cellular constituents (i.e., organelles), and they define plants. They contain the green pigment chlorophyll and are responsible for photosynthesis, which harnesses sunlight to power the activities of the cell. 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. Chloroplasts also have vital roles in plant immunity, and so are ideal targets for engineering disease resistance in crops.Chloroplasts are composed of thousands of different proteins, most of which are encoded by genes in the cell's nucleus and so are synthesized outside of the chloroplast in the cellular matrix known as the cytosol. As chloroplasts are each surrounded by a double-membrane envelope, sophisticated machinery is needed to bring about the import of these proteins into the chloroplast. This comprises two molecular machines, one in each membrane, called TOC (for "Translocon at the Outer membrane of Chloroplasts") and TIC. Each machine is composed of several different proteins that work cooperatively.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 mediates the removal of certain TOC components, and this in turn influences which proteins are imported by chloroplasts. Such control enables the plant to alter its chloroplasts' functions during development and in adaptation to stress. During abiotic stress, SP1 inhibits the import of photosynthetic machinery components, which limits photosynthesis. This may seem counterproductive, but actually under stress conditions photosynthesis can overproduce toxic chemicals called "ROS". Thus, by turning down photosynthesis at these times, the plants are more likely to survive.While ROS are harmful if overproduced, they do have a beneficial role to play as signals during immunity, by orchestrating anti-pathogen defences. Our results reveal that pathogens have evolved mechanisms to promote SP1 activity during infection, to limit photosynthesis and so reduce synthesis of defence-promoting ROS. In effect, the pathogens subvert the plant's system for dealing with abiotic stress. We will study the role of SP1 in immunity, and elucidate how pathogens affect SP1 activity. We will also examine the immunity-related functions of SP1 with regard to different pathogens, and in crop plants. Overall, we will enhance our understanding of plant immunity, which is key to the development of crops with improved disease resistance.