在他们的进化过程中,植物核苷酸结合型富含亮氨酸的重复序列受体(NLR)已经获得了广泛不同的非常规整合结构域,这增强了它们检测病原体效应物的能力.然而,驱动具有整合域的NLR(NLR-ID)进化的功能动力学仍然知之甚少.这里,我们重建了一个易于非常规域整合的NLR基因座的进化史,并通过实验检验了有关NLR-ID进化的假设.我们表明,水稻(Oryzasativa)NLRPias可以识别稻瘟病真菌病原体稻瘟病的效应子AVR-Pias。Pias由功能专用的NLR对组成,辅助Pias-1和传感器Pias-2,其与先前表征的NLR的Pia对等位基因:辅助RGA4和传感器RGA5。值得注意的是,Pias-2在与RGA5的重金属相关(HMA)结构域相似的位置携带C末端DUF761结构域。系统学分析表明,Pias-2/RGA5传感器NLR在Oryza属中经历了反复的基因组重组,导致多达六个序列发散域整合。具有不同功能的等位基因NLR已在不同水稻谱系中保持跨种,以检测序列不同的病原体效应子。相比之下,Pias-1在整个进化过程中都保留了其NLR辅助活性,并且能够与发散的传感器-NLRRGA5一起运行以响应AVR-Pia。这些结果表明,相反的选择力驱动了成对NLR的进化:通过平衡传感器NLR的选择来维持高度动态的域集成事件,与辅助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 pathogen Magnaporthe 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 genus Oryza, resulting in up to six sequence-divergent domain integrations. Allelic NLRs with divergent functions have been maintained transspecies in different Oryza lineages 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.