The allelic rice immune receptor Pikh confers extended resistance to strains of the blast fungus through a single polymorphism in the effector binding interface.

The allelic rice immune receptor Pikh confers extended resistance to strains of the blast fungus through a single polymorphism in the effector binding interface.
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等位基因水稻免疫受体Pikh通过效应器结合界面上的单一多态性赋予对稻瘟病菌菌株的延长抗性。

DOI:
10.1371/journal.ppat.1009368
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发表时间:
2021-03
期刊:
影响因子:
6.7
通讯作者:
Banfield MJ
Banfield MJ
中科院分区:
医学1区
文献类型:
--
作者:
De la Concepcion JC;Maidment JHR;Longya A;Xiao G;Franceschetti M;Banfield MJ

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军备竞赛共同进化推动病原体及其宿主免疫系统的快速适应性变化。植物细胞内NLR免疫受体检测由病原体递送的效应物以促进易感性,激活阻止定殖的免疫应答。因此,病原体效应物进化以逃避免疫识别并且高度可变。反过来,NLR受体是植物中最多样化的蛋白质家族之一,这种变异性支持效应子变体的差异识别。NLR识别效应子的自然变异的分子机制开始被阐明。水稻NLR对Pik-1/Pik-2识别来自稻瘟病菌的AVR-Pik效应子,触发限制稻瘟病感染的免疫反应。整合在受体Pik-1中的重金属相关(HMA)结构域中的等位基因变异赋予与AVR-Pik变体的差异结合,决定抗性特异性。先前的机制研究揭示了Pik等位基因Pikm如何通过专门的HMA/AVR-Pik结合界面将识别扩展到效应子变体。在这里,我们揭示了另一个Pik等位基因Pikh赋予的扩展识别特异性的机制基础。Pikh-HMA中的单个残基增加与AVR-Pik变体的结合,导致植物中的延长的效应器应答。与AVR-Pik变体复合的Pikh-HMA的晶体结构证实了Pikh和Pikm使用类似的分子机制来扩展其病原体识别谱。这项研究显示了不同的NLR受体等位基因如何在功能上会聚,以扩展对病原体效应物的识别特异性。植物病原体不断进化以克服免疫防御并成功地在宿主中定植,导致一些影响全球粮食生产的最具破坏性的疾病。为了保护自己,植物进化出了复杂的免疫系统,可以识别不同病原体的存在,并触发免疫反应来阻止它们的传播。植物免疫受体如何实现对特定病原体菌株的扩展识别,以及这种识别的分子细节才刚刚开始被理解。在这项研究中,我们的特点是如何一个水稻免疫受体的等位基因实现了广谱识别的效应从稻瘟病真菌。我们发现,这种受体已经进化出一个单一的变化,改变了它与不同效应变体结合的方式。这种变化增加了对这些变体的结合亲和力,并最终转化为免疫识别。有趣的是,不同的水稻免疫受体等位基因也以类似的方式实现了广谱效应识别。因此,不同的免疫受体等位基因可以会聚在类似的机制上,以实现对病原体效应物的扩展识别。这些知识有可能帮助合理设计植物免疫受体,使其对一些最具破坏性的病原体具有定制的抗性,这是植物生物技术的一个长期目标。
Arms race co-evolution drives rapid adaptive changes in pathogens and in the immune systems of their hosts. Plant intracellular NLR immune receptors detect effectors delivered by pathogens to promote susceptibility, activating an immune response that halts colonization. As a consequence, pathogen effectors evolve to escape immune recognition and are highly variable. In turn, NLR receptors are one of the most diverse protein families in plants, and this variability underpins differential recognition of effector variants. The molecular mechanisms underlying natural variation in effector recognition by NLRs are starting to be elucidated. The rice NLR pair Pik-1/Pik-2 recognizes AVR-Pik effectors from the blast fungus Magnaporthe oryzae, triggering immune responses that limit rice blast infection. Allelic variation in a heavy metal associated (HMA) domain integrated in the receptor Pik-1 confers differential binding to AVR-Pik variants, determining resistance specificity. Previous mechanistic studies uncovered how a Pik allele, Pikm, has extended recognition to effector variants through a specialized HMA/AVR-Pik binding interface. Here, we reveal the mechanistic basis of extended recognition specificity conferred by another Pik allele, Pikh. A single residue in Pikh-HMA increases binding to AVR-Pik variants, leading to an extended effector response in planta. The crystal structure of Pikh-HMA in complex with an AVR-Pik variant confirmed that Pikh and Pikm use a similar molecular mechanism to extend their pathogen recognition profile. This study shows how different NLR receptor alleles functionally converge to extend recognition specificity to pathogen effectors. Plant pathogens constantly evolve to overcome immune defences and successfully colonize hosts, resulting in some of the most devastating diseases that affect global food production. To defend themselves, plants have evolved a sophisticated immune system that recognizes the presence of different pathogens and triggers immune responses to stop their spread. How plant immune receptors achieve extended recognition to specific pathogen strains and the molecular details of this recognition is just starting to be understood. In this study, we characterize how an allele of a rice immune receptor achieves a broad-spectrum recognition of effectors from the rice blast fungus. We found that this receptor has evolved a single change that alters the way it binds to different effector variants. This change increases binding affinity to these variants and this is ultimately translated to immune recognition. Interestingly, a different rice immune receptor allele also achieves broad-spectrum effector recognition in a similar way. Therefore, different immune receptor alleles can converge on a similar mechanism to achieve extended recognition of pathogen effectors. This knowledge has the potential to help the rational design of plant immune receptors with bespoke resistance to some of the most destructive pathogens, which is a long-term goal in plant biotechnology.
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