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. Engineered sentinel plants that use bacterial-to-plant communication channels are promising. However, no such efforts have thus far enabled a detectable aboveground response in the sentinel plant. Here, we optimize a previously described synthetic bacteria-to-plant communication channel based on the p-coumaroyl-homoserine lactone (pC-HSL) signaling molecule in plants to function as aboveground sentinels of belowground microbial activities. Arabidopsis thaliana sentinel plants harboring this optimized circuit detect root-applied pC-HSL at concentrations as low as 30 nM in roots and 3 M in leaves, demonstrating long-distance signal transmission from below ground to aboveground tissues. Moreover, sentinel plants report pC-HSL production by engineered Escherichia coli and Pseudomonas putida colonizing plant roots in both plate and soil assays. These results establish an engineered plant platform that converts rhizosphere microbial activity into a visible aboveground signal, enabling a minimally invasive platform for monitoring rhizosphere microbial gene expression and for precision agriculture and soil management.