Mycelial network-mediated rhizobial dispersal enhances legume nodulation

• Published in: The ISME Journal 2020-04, Vol.14 (4), p.1015-1029
• Main Authors: Zhang, Wei, Li, Xiao-Gang, Sun, Kai, Tang, Meng-Jun, Xu, Fang-Ji, Zhang, Ming, Dai, Chuan-Chao
• Format: Article
• Language: English
• Subjects: 14/28; 14/63; 38/77; 38/91; 631/158/855; 631/326/171/1818; 631/326/2565/547; Arachis; Arachis hypogaea; Biomedical and Life Sciences; Biosynthesis; Cell division; Cell migration; Cell proliferation; Chemoreception; Chemotaxis; Dispersal; Dispersion; Ecology; Evolutionary Biology; Exudates; Exudation; Fabaceae - microbiology; Flagella; Fungi; Hyphae; Legumes; Leguminous plants; Life Sciences; Microbial Ecology; Microbial Genetics and Genomics; Microbiology; Motility; Mycelia; Networks; Nodulation; Peanuts; Phomopsis liquidambari; Rhizobium - genetics; Rhizobium - physiology; Rhizosphere; Soil; Soil Microbiology; Soil microorganisms; Soils; Symbiosis; Symbiosis - genetics; Vectors
• ISSN: 1751-7362; 1751-7370
• DOI: 10.1038/s41396-020-0587-5

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.