Mycelial network-mediated rhizobial dispersal enhances legume nodulation

First author: Wei Zhang; Affiliations:  Nanjing Normal University (南京师范大学): Nanjing, China

Corresponding author: Chuan-Chao Dai 

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 (趋化性) cannot explain rhizobial long-distance dispersal, mycelia (菌丝体) 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 (鞭毛) biosynthesis, and motility were regulated by Ph. liquidambaris, thus accounting for the detected rhizobial dispersal along hyphae (菌丝). 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.

根瘤菌接触到豆类植物宿主是结瘤的先决条件。根瘤菌在土壤中的运动能力很差，而丝状真菌能够在土壤孔隙间疯狂生长。由于根分泌物驱动的细菌化学趋向性并不能够解释根瘤菌的长距离扩散，而菌丝体正好构成了理想的网络体系，有助于将根瘤菌从大片土壤中富集到豆类植物的根际土壤。因此，作者假设菌丝体网络作为载体，将根瘤菌与豆类植物联系到一起，影响着后面豆类植物根组织的结瘤。通过开发一个土壤缩影系统，作者发现一个兼性活体营养真菌枫香拟茎点霉（Phomopsis liquidambaris）帮助根瘤菌从大片土壤聚集到花生（Arachis hypogaea）的根际周边，因此，诱导了花生-根瘤菌结瘤，而在缺失菌丝体的情况下则不会出现该现象。扩散模式的试验显示细胞增殖和移动介导了根瘤菌沿菌丝体的扩散，并且真菌分泌物可能作用于该进程。此外，转录组分析显示与细胞分裂、化学感应系统、鞭毛生物合成以及移动相关基因的表达在枫香拟茎点霉中受到的调控，因此解释了沿菌丝检测到的根瘤菌扩散。本文的研究结果揭示了根瘤菌利用菌丝体作为扩散网络，从而迁移到豆类植物的根际土壤中，最终诱导了结瘤过程。本文的工作揭示了菌丝体网络对于豆类植物-根瘤菌共生系统中细菌的扩散至关重要。

通讯：戴传超（http://sky.njnu.edu.cn/cn/szdw/jsmd）

个人简介：1992年，南京大学，学士；1998年，南京师范大学，硕士；2003年，中国药科大学，博士。

研究方向：（1）植物内生菌资源及其与宿主相互关系，（2）微生态制剂，（3）土壤生态与修复工程研究。

doi: https://doi.org/10.1038/s41396-020-0587-5

Journal: The ISME Journal

Published date: January 23, 2020