A genetically linked pair of NLR immune receptors show contrasting patterns of evolution
A genetically linked pair of NLR immune receptors show contrasting patterns of evolution
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一对基因连锁的 NLR 免疫受体表现出截然不同的进化模式
DOI：
10.1101/2021.09.01.458560
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发表时间：
2021
期刊：
影响因子：
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通讯作者：
Terauchi Ryohei
中科院分区：
文献类型：
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作者：
Shimizu Motoki;Hirabuchi Akiko;Sugihara Yu;Abe Akira;Takeda Takumi;Kobayashi Michie;Hiraka Yukie;Kanzaki Eiko;Oikawa Kaori;Saitoh Hiromasa;Langner Thorsten;Banfield Mark J.;Kamoun Sophien;Terauchi Ryohei
在整个进化过程中，植物核苷酸结合的富亮氨酸重复受体(NLR)已经获得了广泛差异的非传统整合结构域，从而增强了它们检测病原体效应物的能力。然而，推动具有整合域的NLR(NLR-ID)进化的功能动力学仍然知之甚少。在这里，我们重建了一个倾向于非传统区域整合的NLR基因座的进化历史，并通过实验测试了关于NLR-ID进化的假设。我们发现水稻NLR PIAS识别稻瘟病菌的效应因子AVR-PIAS。PIAS由一对功能专门化的NLR组成，即辅助子PIAS-1和传感器PIAS-2，这与先前描述的PIA NLRs对等位：辅助子RGA4和传感器RGA5。值得注意的是，PIAS-2携带一个C-末端的DUF761结构域，位置与RGA5的重金属相关(HMA)结构域相似。系统基因组学分析表明，PIAS-2/RGA5传感器NLRs在水稻基因组内经历了反复的基因组重组，导致了多达6个序列分歧区域的整合。具有不同功能的等位基因NLR一直被保持在不同的水稻品种中，以检测序列差异的病原体效应器。相比之下，PIAS-1在整个进化过程中保持了其NLR辅助活性，并能够与发散传感器-NLR RGA5一起对AVR-Pia做出反应。这些结果表明，相反的选择性力量推动了成对NLR的进化：通过平衡传感器NLR的选择来维持高度动态的结构域整合事件，与针对辅助NLR的免疫信号的纯化选择和功能保守形成鲜明对比。
Throughout their evolution, plant nucleotide-binding leucine-rich-repeat receptors (NLRs) have acquired widely divergent unconventional integrated domains that enhance their ability to detect pathogen effectors. However, the functional dynamics that drive the evolution of NLRs with integrated domains (NLR-IDs) remain poorly understood. Here, we reconstructed the evolutionary history of an NLR locus prone to unconventional domain integration and experimentally tested hypotheses about the evolution of NLR-IDs. We show that the rice (Oryza sativa) NLR Pias recognizes the effector AVR-Pias of the blast fungal pathogenMagnaporthe oryzae. Pias consists of a functionally specialized NLR pair, the helper Pias-1 and the sensor Pias-2, that is allelic to the previously characterized Pia pair of NLRs: the helper RGA4 and the sensor RGA5. Remarkably, Pias-2 carries a C-terminal DUF761 domain at a similar position to the heavy metal–associated (HMA) domain of RGA5. Phylogenomic analysis showed that Pias-2/RGA5 sensor NLRs have undergone recurrent genomic recombination within the genusOryza, resulting in up to six sequence-divergent domain integrations. Allelic NLRs with divergent functions have been maintained transspecies in differentOryzalineages to detect sequence-divergent pathogen effectors. By contrast, Pias-1 has retained its NLR helper activity throughout evolution and is capable of functioning together with the divergent sensor-NLR RGA5 to respond to AVR-Pia. These results suggest that opposite selective forces have driven the evolution of paired NLRs: highly dynamic domain integration events maintained by balancing selection for sensor NLRs, in sharp contrast to purifying selection and functional conservation of immune signaling for helper NLRs.