Nitrogen fixation and crop productivity enhancements codriven by intercrop root exudates and key rhizosphere bacteria

1. Crop diversity management is widely used to increase agricultural productivity and sustainability. Recent studies have demonstrated that maize root exudates can drive interspecific facilitation to enhance N2 fixation of bean in intercropping systems. However, the mechanisms of N2 fixation enhancement stimulated by root exudates in the intercropping systems remain unclear. 2. Four experiments were designed to provide a progressively deeper understanding of how root exudates stimulate microbial-mediated N2 fixation. First, the effects of faba bean/maize intercropping on yields and soil microbial communities were determined in a field experiment. Second, root-derived interspecific facilitation was evaluated using a root partitioning approach. Third, the key microbial taxa in the faba bean rhizosphere were traced using 13C-labeled maize root exudates. Fourth, the codriven mechanism of maize root exudates and microorganisms in the faba bean rhizosphere were explored. 3. Faba bean/maize intercropping with maize residue return increased the yields of faba bean (26%), maize (27%), and broccoli (9.1%) compared to that under monocropping. Nodulin-like 4 (NODL4), chalcone-flavanone isomerase (CFI), and early nodulin-like (ENODL2) gene expression in faba bean roots intercropped with maize increased by 1.5-2.3-fold compared to that observed under monoculture. More than half of the N2 fixation of faba bean increase under intercropping was due to interactions with microorganisms. Nine key bacterial genera in the faba bean rhizosphere were identified by 13C-DNA based stable isotope probing analysis. Among them Agromyces, Arthrobacter, Bacillus, Lysobacter, and Paenibacillus directly fix N2, while Gemmatimonas, Heliobacillus, Natronocella, and Sorangium increase the N2 fixation capacity of Azotobacter by providing additional carbon sources. These key bacteria triggered by maize root exudates played an important role in the rhizosphere facilitation of intercropping. 4. Synthesis and applications. We demonstrated a novel root-root facilitation of N2 fixation and increased crop yields codriven by root exudates and rhizosphere bacteria under faba bean/maize intercropping, and nine key bacteria associated with this process were identified by 13C-DNA based stable isotope probing. We recommend the adoption and optimization of intercropping systems with residue return to reduce the shortcomings of continuous cropping and to increase the sustainability of crop production.Funding provided by: Special Research Funding for Public Benefit Industries (Agriculture) of China*Crossref Funder Registry ID: Award Number: 201503121-05Funding provided by: Shandong "Double Tops" Program, the Funds of Science and Technology of Shandong*Crossref Funder Registry ID: Award Number: 2019YQ014Funding provided by: State Key Laboratory of Crop Biology Priority Open Fund*Crossref Funder Registry ID: Award Number: 2018 kf04Funding provided by: NSFC project*Crossref Funder Registry ID: Award Number: 41671253Funding provided by: Program of Competitive Growth of Kazan Federal University*Crossref Funder Registry ID: Award Number: Funding provided by: RUDN University program 5-100*Crossref Funder Registry ID: Award Number: Funding provided by: Special Research Funding for Public Benefit Industries (Agriculture) of ChinaCrossref Funder Registry ID: Award Number: 201503121-05Funding provided by: State Key Laboratory of Crop Biology Priority Open FundCrossref Funder Registry ID: Award Number: 2018 kf04Funding provided by: NSFC projectCrossref Funder Registry ID: Award Number: 41671253Funding provided by: Program of Competitive Growth of Kazan Federal UniversityCrossref Funder Registry ID: Funding provided by: RUDN University program 5-100Crossref Funder Registry ID