Laboratory of Mycology, Earth and Life Institute, Université catholique de Louvain-UCLouvain, Croix du Sud 2, L7.05.06B-1348, Louvain-la-Neuve, Belgium.
College of Resources and Environmental Sciences, China Agricultural University, No. 2 Yuanmingyuan West Road, Haidian District, Beijing 100193, China.
ISME J. 2024 Jan 8;18(1). doi: 10.1093/ismejo/wrae185.
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 Sinorhizobium 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.
在土壤生态系统中，根瘤菌占据豆科植物根部的根际，形成根瘤，这一过程是由微生物识别特定的根衍生信号（即类黄酮）触发的。然而，土壤条件会限制细菌的运动性，从而将信号感知限制在受根直接影响的区域。豆科植物与丛枝菌根真菌（arbuscular mycorrhizal fungi）共生，后者的菌丝在土壤中广泛发育，这可能为根瘤菌提供了有效的扩散网络。我们假设，丛枝菌根真菌的菌丝网络在信号传递中发挥作用，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。我们使用体外和温室微宇宙系统证明，粗糙球腔菌（Rhizophagus irregularis）帮助苜蓿中华根瘤菌（Shinorhizobium meliloti）向豆科植物紫花苜蓿（Medicago truncatula）迁移，引发结瘤，而没有丛枝菌根真菌则不会触发这一机制。代谢组学分析揭示了与紫花苜蓿根相关的丛枝菌根真菌外生菌丝隔室中特有的八种类黄酮，这些类黄酮与苜蓿中华根瘤菌的生长和结瘤基因表达相关。在由共同菌丝网络连接的两株植物（豆科植物紫花苜蓿和非豆科植物马铃薯）的外生菌丝上接种根瘤菌，表现出对豆科植物的偏好，这表明真菌连接到豆科植物的特定信号具有化感吸引力。同时，苜蓿中华根瘤菌刺激了菌丝的细胞质/原生质流，可能增加了养分和信号的释放。我们的研究结果强调了丛枝菌根真菌外生菌丝（即菌根途径）在根瘤菌长距离迁移到根部并导致结瘤中的重要性。
