Mycelial network-mediated rhizobial dispersal enhances legume nodulation

Abstract

The access of rhizobia to legume host is a prerequisite for nodulation. Rhizobia are poorly motile in soil, while filamentous fungi are known to grow extensively across soil pores. Since root exudates-driven bacterial chemotaxis cannot explain rhizobial long-distance dispersal, mycelia could constitute ideal dispersal networks to help rhizobial enrichment in the legume rhizosphere from bulk soil. Thus, we hypothesized that mycelia networks act as vectors that enable contact between rhizobia and legume and influence subsequent nodulation. By developing a soil microcosm system, we found that a facultatively biotrophic fungus, Phomopsis liquidambaris, helps rhizobial migration from bulk soil to the peanut (Arachis hypogaea) rhizosphere and, hence, triggers peanut–rhizobium nodulation but not seen in the absence of mycelia. Assays of dispersal modes suggested that cell proliferation and motility mediated rhizobial dispersal along mycelia, and fungal exudates might contribute to this process. Furthermore, transcriptomic analysis indicated that genes associated with the cell division, chemosensory system, flagellum biosynthesis, and motility were regulated by Ph. liquidambaris, thus accounting for the detected rhizobial dispersal along hyphae. Our results indicate that rhizobia use mycelia as dispersal networks that migrate to legume rhizosphere and trigger nodulation. This work highlights the importance of mycelial network-based bacterial dispersal in legume–rhizobium symbiosis.

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Fig. 1: Ph. liquidambaris transfers soil rhizobia to the rhizosphere of peanut.
Fig. 2: Ph. liquidambaris facilitates Bradyrhizobial dispersal in soil conditions.
Fig. 3: Ph. liquidambaris facilitates Bradyrhizobial dispersal, promotes Bradyrhizobial root infection, and triggers peanut–Bradyrhizobium interaction.
Fig. 4: Ph. liquidambaris networks help Bradyrhizobial dispersal.
Fig. 5: Analysis of Bradyrhizobial dispersal on mycelial networks of Ph. liquidambaris at 14 dai.
Fig. 6: Effects of Ph. liquidambaris exudates on Bradyrhizobial growth, biofilm formation, and chemotaxis.
Fig. 7: RNA-seq reveal the potential genetic mechanisms of rhizobial dispersal on Ph. liquidambaris networks.

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Acknowledgements

We thank Yin-Ping Zhang and Chao-Chao Hu of Analytical & Testing Center, Nanjing Normal University, for their help with the microscopic imaging. This work was financially supported by the National Natural Science Foundation of China (NSFC no. 31870478; 31370507); the Priority Academic Program Development of Jiangsu Higher Education Institutions; and Doctor Breeding Project of Nanjing Normal University (1812000006317).

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WZ, XGL, and CCD designed the experiments, analyzed the data, and wrote and revised the manuscript. WZ, KS, MJT, FJX, and MZ performed experiments. All of authors read and approved the final manuscript.

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Correspondence to Chuan-Chao Dai.

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Zhang, W., Li, XG., Sun, K. et al. Mycelial network-mediated rhizobial dispersal enhances legume nodulation. ISME J 14, 1015–1029 (2020). https://doi.org/10.1038/s41396-020-0587-5

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