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.