Deciphering plant stress memory: the exploration of how DNA methylation and the rhizosphere microbiome control stress memory in plants

植物病虫害和病原体对全球粮食供应构成重大威胁。农药目前是主要的控制策略，但有明确的证据表明，它们会对人类健康和更广泛的环境产生负面影响。为了确保我们的粮食供应有一个可持续的未来，农业必须放弃对有害化学农药的依赖。增强植物抵抗害虫（如毛毛虫）的自然能力将有助于实现这一目标。在这项研究中，我将破译植物免疫系统一个具有巨大开发潜力的方面的机制。在暴露于特定的环境刺激下，如轻微的虫害损害，植物对未来的攻击变得更有抵抗力。这种现象被称为获得性或诱导性抵抗，是应激记忆的一种。胁迫记忆的形成涉及植物表观基因组的变化，即调节植物基因组的化学修饰的集合。在最近发表的一篇文章中，我发现，在特定的基因组区域，DNA甲基化这一特定修饰的减少，对于持久的压力记忆和对咀嚼食草动物的抵抗力至关重要。DNA甲基化的去除，DNA去甲基化，也被证明通过控制根分泌物的产生和有益微生物的招募来影响植物根相关的微生物组。这些最近的发现提出了一个悬而未决的问题，植物的应激记忆是由DNA甲基化和微生物组的结合所支撑的吗？更具体地说，胁迫诱导的DNA甲基化缺失是否会调节植物根部有益微生物群的招募，这是否会促进胁迫记忆和持久的抗性？在这个奖学金中，我将研究这些及时的问题，并产生关于植物逆境适应机制的变革性新见解。该奖学金的研究计划将分为四个目标，利用重要作物物种番茄（目标1-3）和模式植物拟南芥（目标4）进行研究。目的1：研究植物在草食胁迫或使用诱导DNA去甲基化系统去除DNA甲基化后表达持久诱导抗性所需的功能性土壤微生物群。目的2：描述草食胁迫诱导的与胁迫记忆相关的根转录组变化的特征，并确定这是否会导致根分泌物和有益微生物群募集的长期变化。目的3：证明草食胁迫诱导DNA甲基化丢失，并确定这是否调节根分泌物代谢。目的4，扩大研究范围，以确定根相关微生物组中DNA甲基化依赖性变化对持久胁迫记忆的需求是否具有植物物种特异性。从这项研究中获得的知识将为培育新的作物品种提供信息，这些品种在不需要暴露于压力的情况下对害虫表现出更强的抵抗力。它还将指导新的土壤管理战略的发展，以促进诱导害虫抗性的微生物。这些新的害虫控制策略将有助于确保粮食的可持续生产，这将使农民、消费者和更广泛的环境受益。

Plant pests and pathogens pose a major threat to the global food supply. Pesticides are currently the primary control strategy however there is clear evidence that they can negatively impact the health of humans and the wider environment. To ensure a sustainable future for our food supply, agriculture must abandon its reliance on harmful chemical pesticides. Enhancing the plant's natural ability to resist pests such as caterpillars will help achieve this goal. In this fellowship I will decipher the mechanisms underpinning one aspect of the plants immune system which has great potential for exploitation. Following exposure to specific environmental stimuli such as mild pest damage, plants become more resistant to future attack. This phenomenon is known as acquired or induced resistance and is type of stress memory. The formation of stress memory involves changes in a plant's epigenome, the collection of chemical modifications which regulate the plants genome. In a recent publication I identified that a reduction in one specific modification, DNA methylation, at specific genomic regions is essential for long-lasting stress memory and resistance against chewing herbivores. The removal of DNA methylation, DNA demethylation, has also been shown to influence the plant root associated microbiome by controlling the production of root exudates and in turn the recruitment of beneficial microbes. These recent findings raise a major unanswered question, is stress memory in plants underpinned by the combination of DNA methylation and microbiomes? More specifically, does stress induced loss of DNA methylation regulate the recruitment of a beneficial microbiome to plant roots and does this facilitate stress memory and long-lasting resistance? In this fellowship I will investigate these timely questions and generate transformative new insights about the mechanisms of plant stress adaptation. The research programme for the fellowship will be split into four objectives addressed using the important crop species tomato (Solanum lycopersicum; Objectives 1-3) and the model plant Arabidopsis thaliana (Objective 4). Objective 1, investigate the requirement of a functional soil microbiome for plants to express long-lasting induced resistance after herbivory stress or removal of DNA methylation using an inducible DNA demethylation system. Objective 2, characterise the herbivory stress induced shift in the root transcriptome associated with stress memory and determine whether this results in a long-lasting change in root exudation and recruitment of a beneficial microbiome. Objective 3, demonstrate that herbivory stress induces a loss of DNA methylation and establish if this regulates root exudate metabolism. Objective 4, expand the research to ascertain whether the requirement of DNA methylation dependent changes in the root associated microbiome for long-lasting stress memory is plant species specific. The knowledge gained from this fellowship will inform the breeding of novel crop varieties which display enhanced resistance to pests without the requirement to be exposed to stress. It will also direct the development of new soil management strategies which promote pest-resistance inducing microbes. Together these novel pest control strategies will help ensure sustainable production of our food which will benefit farmers, consumers, and the wider environment.