Nitrogen fertilization modulates beneficial rhizosphere interactions through signaling effect of nitric oxide
An Kang, Nan Zhang, Weibing Xun, Xiaoyan Dong, Ming Xiao, Zihao Liu, Zhihui Xu, Haichao Feng, Jianwen Zou, Qirong Shen, Zhang Rui-fu
Abstract
Chemical nitrogen (N) fertilization is customary for increasing N inputs in agroecosystems. The nutritional effects of N fertilization on plants and soil microbes have been well studied. However, the signaling effects of N fertilization on rhizosphere plant-microbe interactions and the following feedback to plant performance remain unknown. Here, we investigated the effect of different N fertilizations on the behavior of the plant growth-promoting rhizobacteria (PGPR) Bacillus velezensis SQR9 in the cucumber (Cucumis sativus L.) rhizosphere. Moderate N fertilization promoted higher rhizosphere colonization of strain SQR9 than insufficient or excessive N input. Nitric oxide (NO) produced through the denitrification process under N fertilization was identified as the signaling molecule that dominates the root colonization of PGPR, and this effect could be neutralized by the NO-specific scavenger 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxy-3-oxide. Gene expression analysis demonstrated that NO regulated the biofilm formation of strain SQR9 by affecting the synthesis of extracellular matrix γ-polyglutamic acid, consequently impacting its root colonization. Finally, we demonstrated that moderate N fertilization-modulated enhanced PGPR root colonization can significantly promote plant growth and nitrogen use efficiency. This study provides insights into our understanding of the beneficial rhizosphere plant-microbe interactions under N fertilization and suggests that rational fertilization is critical to promote beneficial rhizosphere interactions for sustainable agricultural production.