Rhizobium nitrogen-fixing nodule symbiosis occurs in two taxonomic lineages: legumes (Fabaceae) and the genus Parasponia (Cannabaceae). Both symbioses are initiated upon the perception of rhizobium-secreted lipochitooligosaccharides (LCOs), called Nod factors. Studies in the model legumes Lotus japonicus and Medicago truncatula showed that rhizobium LCOs are perceived by a heteromeric receptor complex of distinct Lys motif (LysM)-type transmembrane receptors named NOD FACTOR RECEPTOR1 (LjNFR1) and LjNFR5 (L. japonicus) and LYSM DOMAIN CONTAINING RECEPTOR KINASE3 (MtLYK3)-NOD FACTOR PERCEPTION (MtNFP; M. truncatula). Recent phylogenomic comparative analyses indicated that the nodulation traits of legumes, Parasponia spp., as well as so-called actinorhizal plants that establish a symbiosis with diazotrophic Frankia spp. bacteria share an evolutionary origin about 110 million years ago. However, the evolutionary trajectory of LysM-type LCO receptors remains elusive. By conducting phylogenetic analysis, transcomplementation studies, and CRISPR-Cas9 mutagenesis in Parasponia andersonii, we obtained insight into the origin of LCO receptors essential for nodulation. We identified four LysM-type receptors controlling nodulation in P. andersonii: PanLYK1, PanLYK3, PanNFP1, and PanNFP2. These genes evolved from ancient duplication events predating and coinciding with the origin of nodulation. Phylogenetic and functional analyses associated the occurrence of a functional NFP2-orthologous receptor to LCO-driven nodulation. Legumes and Parasponia spp. use orthologous LysM-type receptors to perceive rhizobium LCOs, suggesting a shared evolutionary origin of LCO-driven nodulation. Furthermore, we found that both PanLYK1 and PanLYK3 are essential for intracellular arbuscule formation of mutualistic endomycorrhizal fungi. PanLYK3 also acts as a chitin oligomer receptor essential for innate immune signaling, demonstrating functional analogy to CHITIN ELECITOR RECEPTOR KINASE-type receptors.

根瘤菌固氮根瘤共生发生在两个分类谱系中：豆科植物（豆科）和Parasponia属（大麻科）。两种共生都是在感知根瘤菌分泌的脂壳低聚糖（LCO）（称为 Nod 因子）时启动的。对模型豆科植物百脉根和蒺藜苜蓿的研究表明，根瘤菌 LCO 是由不同 Lys 基序 (LysM) 型跨膜受体的异聚受体复合物感知的，称为 NOD 因子受体 1 (LjNFR1) 和 LjNFR5 (苜蓿) 和 LYSM 结构域包含受体激酶3 (MtLYK3)-NOD 因子感知（MtNFP； M. truncatula ）。最近的系统发育比较分析表明，豆科植物、 Parasponia spp.以及与固氮营养性Frankia spp.建立共生的所谓放线菌植物的结瘤特征。细菌的进化起源大约在 1.1 亿年前。然而，LysM 型 LCO 受体的进化轨迹仍然难以捉摸。通过在Parasponia andersonii中进行系统发育分析、反式互补研究和 CRISPR-Cas9 诱变，我们深入了解了结瘤所必需的 LCO 受体的起源。我们鉴定了P. andersonii中控制结瘤的四种 LysM 型受体： PanLYK1 、 PanLYK3 、 PanNFP1和PanNFP2 。这些基因是从早于结瘤起源且与结瘤起源同时发生的古代复制事件进化而来的。系统发育和功能分析将功能性 NFP2 直系同源受体的出现与 LCO 驱动的结瘤相关联。豆类和Parasponia spp. 使用直系同源 LysM 型受体来感知根瘤菌 LCO，表明 LCO 驱动的结瘤具有共同的进化起源。此外，我们发现 PanLYK1 和 PanLYK3 对于共生内生菌根真菌的细胞内丛枝形成至关重要。 PanLYK3 还充当先天免疫信号传导所必需的几丁质寡聚物受体，证明其与几丁质发射器受体激酶型受体的功能相似。