Sentinel Plants Enable Aboveground Detection of Belowground Soil Microbial Activity

Rhizosphere microbial processes play a central role in soil function and plant health yet remain difficult to monitor noninvasively and continuously. Engineered plants that detect microbially produced signals offer a scalable approach. However, existing systems have been limited to root-localized reporter readouts. Here, we optimize a synthetic p-coumaroyl-homoserine lactone (pC-HSL)-responsive circuit in Arabidopsis thaliana to enable aboveground reporting of belowground microbial activity. Sentinel plants detect root-applied pC-HSL at concentrations as low as 30 nM with a 25-fold increase in reporter expression in roots and a 270-fold increase in leaf fluorescence at 3 μM pC-HSL, demonstrating long-distance signal relay from roots to shoots. Moreover, sentinel plants report pC-HSL produced by engineered Escherichia coli and Pseudomonas putida at the root zone in both agar plate and agricultural soil assays. This work establishes a generalizable platform that enables plants to convert belowground microbial signals into visible aboveground readouts for noninvasive monitoring of rhizosphere microbial activity.