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

植物害虫和病原体对全球粮食供应构成重大威胁。农药是目前的主要控制策略，但有明确的证据表明，它们可能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。增强植物抵抗毛虫等害虫的天然能力将有助于实现这一目标。在这个奖学金中，我将破译植物免疫系统的一个方面的机制，这具有很大的开发潜力。在暴露于特定的环境刺激，如轻微的虫害后，植物对未来的攻击更具抵抗力。这种现象被称为获得性或诱导性抗性，是一种压力记忆。胁迫记忆的形成涉及植物表观基因组的变化，表观基因组是调节植物基因组的化学修饰的集合。在最近的一篇文章中，我发现在特定的基因组区域减少一种特定的修饰，DNA甲基化，对于持久的压力记忆和抵抗咀嚼食草动物是必不可少的。DNA甲基化的去除，DNA去甲基化，也已被证明通过控制根分泌物的产生和有益微生物的募集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主要的未回答的问题，植物中的压力记忆是由DNA甲基化和微生物组的组合支撑的吗？更具体地说，胁迫诱导的DNA甲基化丧失是否会调节有益微生物组向植物根部的募集，这是否有助于胁迫记忆和持久抗性？在这个奖学金，我将调查这些及时的问题，并产生有关植物胁迫适应机制的变革性的新见解。该研究金的研究计划将分为四个目标，使用重要的作物品种番茄（Solanum lycopersicum;目标1-3）和模式植物拟南芥（目标4）。目的1、利用诱导型DNA去甲基化系统研究植物在植食性胁迫或去除DNA甲基化后表达持久诱导抗性对功能性土壤微生物组的需求。目的2，研究与胁迫记忆相关的植物胁迫诱导的根转录组的变化，并确定这是否会导致根分泌和有益微生物组的招募的长期变化。目的3，证明草食胁迫诱导DNA甲基化的丧失，并确定这是否调节根系分泌物代谢。目的4，扩大研究范围，以确定长期胁迫记忆对根相关微生物组DNA甲基化依赖性变化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，这些品种对害虫表现出更强的抗性，而不需要暴露在压力下。它还将指导新的土壤管理策略的发展，促进抗虫害诱导微生物。这些新的害虫控制策略将有助于确保我们的食物可持续生产，这将有利于农民，消费者和更广泛的环境。

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.