Understanding how plant antimicrobial "hot zones" can accelerate pathogen evolution

农业政策和作物生产导致大量粮食储备的粮食大山时代已经一去不复返了。相反，世界正面临着生产足够的粮食来养活不断增长的人口的重大挑战。粮食安全是一个主要的全球研究重点，我们知道，我们必须在未来20年内将粮食产量翻一番，才能跟上人口增长的步伐。要做到这一点，需要在粮食生产的许多方面进行改进。需要改进的主要领域之一是防止因植物病害造成的作物损失。大多数引起植物疾病的微生物都在与植物进行一场持续的军备竞赛，微生物正在迅速进化以感染抗病植物，而植物正在进化以抵抗病原体的攻击。在农业环境中，植物育种者面临着开发新的抗病品种以取代因微生物进化而失效的品种的日益困难的挑战。为了延长抗病植物品种的有用性，并降低微生物克服抗病性的速度，我们必须充分了解微生物是如何进化的以及这种进化的驱动因素。我们已经开发了一个模型系统来理解微生物进化以克服植物的抗病性。这个系统使用一种叫做丁香假单胞菌pv的细菌。phaseolicola （Pph）是引起豆科植物晕叶枯病的一种重要疾病，是研究微生物进化和增加或减少植物抗病持久性因素的一个很好的系统。在Pph和豆类的情况下，植物已经发展出识别特定Pph菌株的机制，从而抵抗入侵。在这个动态系统中，细菌有许多方法改变其基因组，从而改变其表达的蛋白质，以逃避植物的识别。细菌蛋白质的结构或生产的改变可能会阻止它们被潜在的寄主植物发现，并允许细菌在植物内生长。我们已经证明，Pph基因组的变化使这种细菌能够克服植物的抗病能力。Pph的某些菌株携带一种基因，该基因产生一种蛋白质，植物可以检测到属于Pph，提醒它触发防御系统，阻止Pph的生长。这种蛋白质的基因位于Pph基因组的一个被称为基因组岛的离散区域内。为了对抗植物的识别，Pph从染色体上移除基因组岛，这样子细胞就不再有这个岛了。有趣的是，我们观察到这种Pph的剧烈变化最常发生在抗性品种的感染位点“热区”。这些热区在细菌入侵后产生高度抗菌的条件。因此，抗性植物中发生的化学变化实际上加速了更具毒性的病原体的进化。最近，我们还证明了在植物组织中生长的细菌可以在一个称为转化的过程中获得吸收外来DNA的能力。这种新基因的获得可以使Pph在植物和细菌之间的斗争中获得优势。在本提案中，我们旨在研究“热区”的化学成分，以了解哪些因素负责诱导Pph基因丢失和基因获得。我们还旨在确定细菌中负责DNA摄取的基因，并了解“热区”中存在的信号如何导致Pph中DNA摄取增加。这项研究将有助于阐明支持细菌致病性进化和作物植物抗病能力崩溃的基本机制，为将来可能用于改进用于对抗致病微生物的疾病管理策略提供知识。

Gone are the days of food mountains whereby agricultural policies and crop production resulted in large stocks of food. Instead, the world is facing a major challenge to produce enough food to feed a growing population. Food security is a major global research priority and we know that we must double our food production within the next 20 years just to keep pace with population increases. To do this requires improvements in many aspects of food production. One of the major areas for improvement is preventing crop loss due to plant disease.Most of the microorganisms that cause plant disease are engaged in a constant arms race with plants such that microorganisms are rapidly evolving to infect disease resistant plants while plants are evolving to resist pathogen attack. In an agricultural setting, plant breeders face the increasingly difficult challenge of developing new disease-resistant varieties to replace those rendered ineffective due to microbial evolution. To prolong the usefulness of disease resistant plant varieties, and to reduce the rate at which microorganisms overcome disease resistance, it is imperative that we fully understand how microorganisms evolve and the drivers of this evolution. We have developed a model system for understanding microbial evolution to overcome plant disease resistance. This system uses a bacterium called Pseudomonas syringae pv. phaseolicola (Pph), which causes an important disease of bean plants known as halo blight, and represents an excellent system for studying both microbial evolution and the factors that increase or decrease the durability of plant disease resistance.In the case of Pph and bean, the plant has developed mechanisms to recognise specific strains of Pph, and so resist invasion. In this dynamic system the bacterium has a number of ways of changing its genome, and therefore the proteins it expresses, in order to evade plant recognition. Alterations in the structure or production of bacterial proteins may prevent their detection by potential host plants and allow the bacteria to grow within the plant. We have shown that changes in the genome of Pph allow this bacterium to overcome plant disease resistance. Certain strains of Pph carry a gene that produces a protein the plant can detect as belonging to Pph, alerting it to trigger its defence systems and prevent Pph growth. The gene for this protein lies within a discrete region of the Pph genome known as a genomic island. To counter plant recognition, Pph removes the genomic island from its chromosome such that daughter cells no longer have the island. Interestingly, we observed that this dramatic change in Pph occurs most frequently in infection site "hot zones" in resistant varieties of bean. These hot zones generate highly antimicrobial conditions following bacterial invasion. Therefore the chemical changes that occur in resistant plants actually accelerate the evolution of a more virulent form of the pathogen.More recently we have also shown that bacteria growing in plant tissue can become competent to take up foreign DNA in a process called transformation. This acquisition of new genes could allow Pph to gain an advantage in the fight between the plant and the bacterium. In this proposal we aim to study the chemical composition of the "hot zone" to understand which factors are responsible for inducing gene loss and gene gain in Pph. We also aim to identify the genes responsible for DNA uptake in the bacteria, and to understand how signals present in the "hot zone" cause increased DNA uptake in Pph. This research will help to elucidate the fundamental mechanisms underpinning the evolution of bacterial pathogenicity and the breakdown of disease resistance in crop plants, providing knowledge that, in the future, may be used to improve the disease management strategies used against disease-causing microorganisms.