Selection pressure on the rhizosphere microbiome can alter nitrogen use efficiency in seed yield in Brassica rapa

Authors: GARCIA, JOSHUA - Cornell University; GANNETT, MARIA - Cornell University; WEI, LIPING - Cornell University; CHENG, LIANG - Cornell University; HU, SHENGYUAN - Carnegie Mellon University; SPARKS, JED - Cornell University; Giovannoni, James; KAO-KNIFFIN, JENNY - Cornell University

Submitted to: Communications Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/6/2022
Publication Date: 12/6/2022
Citation: Garcia, J., Gannett, M., Wei, L., Cheng, L., Hu, S., Sparks, J., Giovannoni, J.J., Kao-Kniffin, J. 2022. Selection pressure on the rhizosphere microbiome can alter nitrogen use efficiency in seed yield in Brassica rapa. Communications Biology. https://doi.org/10.1038/s42003-022-03860-5.
DOI: https://doi.org/10.1038/s42003-022-03860-5

Interpretive Summary: In recent years, numerous plant microbiome studies have highlighted the intricate links between a plant host and its associated microbiomes. In the rhizosphere (the microbiological community surrounding the roots), microbiomes play a key role in processes that affect plant fitness, such as nutrient cycling and disease suppression. Given their influence on plant growth and health, microbial consortia in the rhizosphere have become targets for altering plant traits that may help improve agricultural productivity. Several studies have demonstrated the ability to alter host traits via selection (i.e. directed microbiome manipulation) for microbial consortia in the root zone. Here, we examined if plant productivity (i.e. aboveground biomass and seed yield) could be enhanced in the non-mycorrhizal host Brassica rapa through repeated selection for rhizosphere microbiota associated with increased aboveground biomass production over nine generations of plantings. Our results demonstrated that group-level bacterial interactions could be modified to collectively shift microbiome functions impacting the growth of the host plant under selection pressure and indicates microbiome manipulation can lead to increased yield.

Technical Abstract: Microbial experimental systems provide a platform to observe how networks of groups emerge to impact plant development. We applied selection pressure for microbiome enhancement of Brassica rapa biomass to examine adaptive bacterial group dynamics under soil nitrogen limitation. In the 9th and final generation of the experiment, selection pressure enhanced B. rapa seed yield and nitrogen use efficiency compared to our control treatment, with no effect between the random selection and control treatments. Aboveground biomass increased for both the high biomass selection and random selection plants. Soil bacterial diversity declined under high B. rapa biomass selection, suggesting a possible ecological filtering mechanism to remove bacterial taxa. Distinct sub-groups of interactions emerged among bacterial phyla such as Proteobacteria and Bacteroidetes in response to selection. Extended Local Similarity Analysis and NetShift indicated greater connectivity of the bacterial community, with more edges, shorter path lengths, and altered modularity through the course of selection for enhanced plant biomass. In contrast, bacterial communities under random selection and no selection showed less complex interaction profiles of bacterial taxa. These results suggest that group-level bacterial interactions could be modified to collectively shift microbiome functions impacting the growth of the host plant under soil nitrogen limitation.