Distinct function of SPL genes in age-related resistance in Arabidopsis.
Distinct function of SPL genes in age-related resistance in Arabidopsis.
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DOI：
10.1371/journal.ppat.1011218
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发表时间：
2023-03
期刊：
影响因子：
6.7
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中科院分区：
文献类型：
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在植物中，年龄相关抗性(ARR)指的是在新梢或器官成熟过程中获得的抗病能力。ARR是一种广泛存在的农艺性状，与营养生长期的变化有关，影响对多种病原菌的抗性。植物的先天免疫如何在芽成熟的连续阶段受到不同的调节尚不清楚。在这项工作中，我们发现拟南芥对其细菌病原菌丁香假单胞菌表现出ARR。番茄DC3000营养生长期变化。ARR激活的时间与miR156水平的暂时下降有关。MicroRNA miR156通过抑制SPL转录本的积累和翻译来维持幼年期。对11个SPL基因的功能缺失和功能获得突变的系统研究表明，SPL基因的一个子集，特别是SPL2、SPL10和SPL11，在成虫阶段激活了ARR。SPL10的免疫功能不依赖于其在形态发生中的作用。此外，SPL10部分通过直接激活PAD4介导了水杨酸(SA)途径的年龄依赖性增强。干扰SA的生物合成或信号转导取消了对PTO DC3000的ARR。我们的工作表明，拟南芥中的miR156-SPL10模块在发育过程中被部署来操作免疫输出。与年龄相关的免疫变化是动植物中普遍存在的现象。生物体如何将免疫成熟与发育时钟相结合是一个基本问题。异时microRNAs是发育时序的关键调节因子。我们发现，在拟南芥中，一个保守的异时微RNA(MiRNA)microRNA156调控着从幼体营养阶段到成体营养阶段的年龄相关抗性的发生时间。发育成熟和获得抗病之间的协调是通过miR156控制的具有不同功能的SPL转录因子实现的。SPL转录因子的一个子集通过直接激活防御信号中的关键基因来促进抗性。这项工作弥合了营养发育和年龄相关抗性之间的知识鸿沟。明确免疫发育调控机制，为解锁植物免疫的年龄限制，为精准农业的应用奠定基础。
In plants, age-related resistance (ARR) refers to a gain of disease resistance during shoot or organ maturation. ARR associated with vegetative phase change, a transition from juvenile to adult stage, is a widespread agronomic trait affecting resistance against multiple pathogens. How innate immunity in a plant is differentially regulated during successive stages of shoot maturation is unclear. In this work, we found that Arabidopsis thaliana showed ARR against its bacterial pathogen Pseudomonas syringae pv. tomato DC3000 during vegetative phase change. The timing of the ARR activation was associated with a temporal drop of miR156 level. The microRNA miR156 maintains juvenile phase by inhibiting the accumulation and translation of SPL transcripts. A systematic inspection of the loss- and gain-of-function mutants of 11 SPL genes revealed that a subset of SPL genes, notably SPL2, SPL10, and SPL11, activated ARR in adult stage. The immune function of SPL10 was independent of its role in morphogenesis. Furthermore, the SPL10 mediated an age-dependent augmentation of the salicylic acid (SA) pathway partially by direct activation of PAD4. Disrupting SA biosynthesis or signaling abolished the ARR against Pto DC3000. Our work demonstrated that the miR156-SPL10 module in Arabidopsis is deployed to operate immune outputs over developmental timing. Age-associated change of immunity is a widespread phenomenon in animals and plants. How organisms integrate immune maturation into a developmental clock is a fundamental question. Heterochronic microRNAs are key regulators of developmental timing. We found that a conserved heterochronic microRNA (miRNA) in Arabidopsis, microRNA156, regulates the timing of age-related resistance associated with a transition from the juvenile to the adult vegetative phase. The coordination between developmental maturation and gain of disease resistance is achieved through miR156-controlled SPL transcription factors with distinct functions. A subset of SPL transcription factors promoted resistance by directly activating key genes in defense signaling. This work bridges the knowledge gap between vegetative development and age-related resistance. Pinpointing mechanisms of the developmental regulation on immunity may pave a way for unlocking the age limit on plant immunity and lay a foundation to applications in the precision agriculture.
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