Diversity-triggered 2-naphthoic acid exudation recruits keystone microbial taxa to promote soybean drought tolerance

 Highlights

• High rhizosphere microbial diversity improves soybean performance under drought

• Diversity-triggered 2-naphthoic acid accumulates under drought stress

• Sinorhizobium CS204 senses 2-naphthoic acid via chemoreceptors and ABC transporters

• S.CS204-metabolite synergy boosts nitrogen cycling and plant drought tolerance

Summary

Rhizosphere microbiomes are essential for plant growth and stress tolerance, yet how microbial diversity shapes drought resilience in soybean remains unclear. Here, we demonstrate that high rhizosphere microbial diversity, generated via dilution-to-extinction manipulation of soil microbiome diversity, improves soybean performance under drought. Integrated metabolomic and transcriptomic analyses identify 2-naphthoic acid as a diversity-induced root exudate that accumulates exclusively under drought. This metabolite selectively recruits Sinorhizobium CS204 via chemotaxis and ATP-binding cassette (ABC) transporter-mediated uptake, as confirmed by in vitro substrate utilization assays and targeted mutant construction. Molecular docking and microscale thermophoresis reveal direct interactions between this metabolite and nitrogen-cycling proteins, enhancing denitrification and nitrogen fixation of S.CS204. Co-application of 2-naphthoic acid and S.CS204 significantly improves plant nutrient acquisition and photosynthesis under drought. Collectively, our study underscores the pivotal role of rhizosphere microbial diversity in triggering the exudation of root metabolites to recruit keystone taxa, establishing microbe-plant synergies that bolster drought tolerance.

Read full article at:

https://www.sciencedirect.com/science/article/abs/pii/S1931312826000892