In soil ecosystems, rhizobia occupy the rhizosphere of legume roots to form nodules, a process triggered by microbial recognition of specific root-derived signals (i.e., flavonoids). However, soil conditions can limit bacterial motility, restricting signal perception to the area directly influenced by roots. Legumes, like most plants of agricultural interest, associate with arbuscular mycorrhizal fungi, whose hyphae develop extensively in the soil, potentially providing an effective dispersal network for rhizobia. We hypothesized that mycelial networks of arbuscular mycorrhizal fungi play a role in signal transmission and act as a highway, enabling rhizobia to migrate from distant soil to the roots of leguminous plants. Using in vitro and greenhouse microcosm systems, we demonstrated that Rhizophagus irregularis helps Shinorhizobium meliloti to migrate towards the legume Medicago truncatula, triggering nodulation, a mechanism absent without the arbuscular mycorrhizal fungus. Metabolomics analysis revealed eight flavonoids unique to the compartment containing extraradical hyphae of the arbuscular mycorrhizal fungus linked to M. truncatula roots, associated with S. meliloti growth and nod gene expression. Rhizobia plated on the extraradical hyphae connecting two plants (the legume M. truncatula and non-legume Solanum tuberosum) by a common mycelium network, showed preference for the legume, suggesting the chemoattraction by specific signals transported by the fungus connected to the legume. Simultaneously, S. meliloti stimulated the cytoplasmic/protoplasmic flow in the hyphae, likely increasing the release of nutrients and signals. Our results highlight the importance of extraradical hyphae (i.e. the mycorrhizal pathway) of arbuscular mycorrhizal fungi for the migration of rhizobia over long distances to the roots, leading to nodulation.

中文翻译：

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丛枝菌根菌丝促进豆科植物的根瘤传播和结瘤


在土壤生态系统中，根瘤菌占据豆科植物根的根际形成根瘤，这一过程由微生物识别特定的根衍生信号（即类黄酮）触发。然而，土壤条件会限制细菌的运动，将信号感知限制在直接受根影响的区域。与大多数具有农业意义的植物一样，豆科植物与丛枝菌根真菌有关，其菌丝在土壤中广泛发育，可能为根瘤菌提供有效的传播网络。我们假设丛枝菌根真菌的菌丝网络在信号传输中发挥作用并充当高速公路，使根瘤菌能够从遥远的土壤迁移到豆科植物的根部。使用体外和温室微观系统，我们证明了 Rhizophagus irregularis 帮助 Shinorhizobium meliloti 迁移到豆科植物 Medicago truncatula，触发结瘤，这种机制在没有丛枝菌根真菌的情况下不存在。代谢组学分析显示，包含与 M. truncatula 根相连的丛枝菌根真菌的根外菌丝的隔室特有的 8 种黄酮类化合物，与 S. meliloti 的生长和 nod 基因表达有关。通过共同的菌丝体网络连接两种植物（豆科植物 M. truncatula 和非豆科植物 Solanum tuberosum）的根外菌丝涂板在根外菌丝上，显示出对豆科植物的偏好，表明与豆科植物相连的真菌运输的特定信号的趋化。同时，S. meliloti 刺激菌丝中的细胞质/原生质流动，可能增加营养物质和信号的释放。我们的结果强调了根外菌丝的重要性（即 菌根途径）用于根瘤菌长距离迁移到根部，导致结瘤。