Transgenerational immune priming in plants

植物的跨代免疫启动

• 批准号: BB/L008939/1
• 负责人: Michael Roberts
• 金额: $ 71.13万
• 依托单位: Lancaster University
• 依托单位国家: 英国
• 项目类别: Research Grant
• 财政年份: 2014
• 资助国家: 英国
• 起止时间: 2014 至 无数据
• 项目状态: 已结题
• 来源: https://gtr.ukri.org/projects?ref=BB%2FL008939%2F1
• 关键词: Transgenerational; immune; priming; plants

In response to stress, plants and animals can exhibit rapid changes in their biology, enabling them to maximise their fitness. Exposure to stress can also generate long-term immunological 'memory', which enables the individual to develop faster and stronger defence responses to future exposures. Over recent years, evidence has accumulated that exposure of an individual to stress can also influence future stress responses in its offspring. Such effects are referred to as 'transgenerational', and are assumed to have evolved to maximise survival of an individual's gene pool in future generations, which are likely to encounter similar stresses.We recently made the important discovery that progeny from diseased plants are more resistant than genetically identical offspring from healthy plants. This increased resistance persisted over at least two stress-free generations, suggesting epigenetic inheritance. Resistant progeny did not show increased defence activity in the absence of pathogens, but instead exhibited an increased responsiveness of defence genes to infection. We therefore refer to this phenomenon as 'transgenerational immune priming' (TGIP), since progeny plants are 'primed' to respond more rapidly to infection. Importantly, we have begun to uncover the mechanisms underpinning this immunological plant memory, and discovered that TGIP is based on DNA methylation, a reversible DNA modification that can have a profound impact on gene activity without changes in DNA sequence.Transgenerational immune responses have important implications for natural plant populations, and present an opportunity for exploitation in sustainable agriculture. The ability to improve resistance to pests and diseases through epigenetic manipulation provides a new mechanism by which reliance on chemicals can be reduced without having to change the genetic make-up of our elite crop varieties.In this project, we will investigate the biological significance of TGIP and the molecular mechanisms behind it. Firstly, we will examine whether TGIP can be established when disease stress is experienced only by the maternal plant, or whether paternal tissues can also transmit priming information. This will provide clues as to how TGIP evolved and the mechanism by which it is established. As well as measuring the benefits of TGIP in terms of increased stress resistance in offspring, we will also identify where there are trade-offs: when priming against one form of stress has a negative impact on tolerance to another. Thus, we will employ different forms of stress (disease, herbivory, salinity) to induce TGIP in different parental lines, and then measure the degree of resistance to each of these different stresses in their progeny. These costs and benefits will be measured initially in terms of stress resistance phenotypes, but to add depth of understanding, we will follow up with assays to measure expression of a defined set of stress-responsive marker genes and use mass spectrometry to generate metabolite profiles. Finally, we will grow progeny lines from primed populations in competition to test for overall reproductive fitness benefits for TGIP.In parallel with these phenomenological studies, we will exploit next-generation sequencing technologies to identify the mechanisms involved in the establishment and maintenance of TGIP. Since long-term epigenetic changes in gene responsiveness are associated with DNA methylation, we will profile genome-wide DNA methylation patterns in control and primed plants. Thus, we will identify differentially-methylated regions linked to enhanced stress resistance. We have evidence that certain forms of small RNA molecule (siRNAs) known to regulate DNA methylation are important in establishing TGIP. Therefore, we will also profile siRNAs in control and primed plants to identify correlations between differentially expressed siRNAs and DNA methylation patterns.

作为对压力的反应，植物和动物的生物学可以表现出快速的变化，使它们能够最大限度地保持自己的健康。暴露在压力下也会产生长期的免疫‘记忆’，这使个体能够对未来的暴露产生更快、更强的防御反应。近年来，越来越多的证据表明，一个人暴露在压力之下也会影响其后代未来的压力反应。这种效应被称为跨代效应，被认为是为了最大限度地提高一个人的基因库在后代中的存活率，而后代可能会遇到类似的压力。我们最近有了一个重要发现，即来自患病植物的后代比来自健康植物的基因相同的后代更具抵抗力。这种增强的抗性持续了至少两代无压力的世代，这表明是表观遗传。在没有病原体的情况下，抗性后代并没有表现出更强的防御活性，而是表现出防御基因对感染的更强的反应性。因此，我们将这种现象称为“跨代免疫启动”(TGIP)，因为后代植物被“启动”以对感染做出更快的反应。重要的是，我们已经开始揭示这种免疫植物记忆的机制，并发现TGIP是基于DNA甲基化的，这是一种可逆的DNA修饰，可以在不改变DNA序列的情况下对基因活性产生深远影响。跨代免疫反应对自然植物种群具有重要意义，并为可持续农业提供了开发机会。通过表观遗传操作提高对病虫害的抗性的能力提供了一种新的机制，通过这种机制可以减少对化学物质的依赖，而不必改变我们优良作物品种的遗传构成。在这个项目中，我们将研究TGIP的生物学意义及其背后的分子机制。首先，我们将研究当只有母本植物经历疾病胁迫时，是否可以建立TGIP，或者父本组织是否也可以传递启动信息。这将为TGIP是如何演变的以及建立它的机制提供线索。除了通过提高后代的抗应激能力来衡量TGIP的好处之外，我们还将确定哪些方面存在权衡：当针对一种形式的应激进行准备时，会对另一种形式的应激耐力产生负面影响。因此，我们将利用不同形式的逆境(疾病、草食、盐度)在不同的亲本中诱导TGIP，然后测量它们的后代对这些不同逆境的抗性程度。这些成本和收益最初将根据抗逆性表型进行衡量，但为了增加理解的深度，我们将随后进行分析，以测量一组已定义的应激反应标记基因的表达，并使用质谱学来生成代谢物图谱。在这些现象学研究的同时，我们将利用下一代测序技术来确定建立和维持TGIP的机制。由于基因反应的长期表观遗传变化与DNA甲基化有关，我们将描述对照和启动植物的全基因组DNA甲基化模式。因此，我们将确定与增强的抗逆性相关的差异甲基化区域。我们有证据表明，某些形式的已知调节DNA甲基化的小RNA分子(SiRNAs)在建立TGIP中是重要的。因此，我们还将分析对照和启动植物中的siRNAs，以确定差异表达的siRNAs和DNA甲基化模式之间的相关性。

项目成果

Glutamate receptor-like channels in plants: a role as amino acid sensors in plant defence?

• DOI: 10.12703/p6-37
• 发表时间: 2014
• 期刊: F1000prime reports
• 作者: Forde BG;Roberts MR
• 通讯作者: Roberts MR

Keeping it in the family: transgenerational memories of plant defence.

将其保留在家庭中：植物防御的跨代记忆。

• DOI: 10.1079/pavsnnr201510026
• 发表时间: 2015
• 期刊: CABI Reviews
• 作者: Prashant Singh P

Costs and Benefits of Transgenerational Induced Resistance in Arabidopsis.

• DOI: 10.3389/fpls.2021.644999
• 发表时间: 2021
• 期刊: Frontiers in plant science
• 影响因子: 5.6
• 作者: López Sánchez A;Pascual-Pardo D;Furci L;Roberts MR;Ton J
• 通讯作者: Ton J

The role of DNA (de)methylation in immune responsiveness of Arabidopsis.

• DOI: 10.1111/tpj.13252
• 发表时间: 2016-11
• 期刊: The Plant journal : for cell and molecular biology
• 作者: López Sánchez A;Stassen JH;Furci L;Smith LM;Ton J
• 通讯作者: Ton J

The relationship between transgenerational acquired resistance and global DNA methylation in Arabidopsis.

• DOI: 10.1038/s41598-018-32448-5
• 发表时间: 2018-10-03
• 期刊: Scientific reports
• 影响因子: 4.6
• 作者: Stassen JHM;López A;Jain R;Pascual-Pardo D;Luna E;Smith LM;Ton J
• 通讯作者: Ton J