Root-secreted bitter triterpene modulates the rhizosphere microbiota to improve plant fitness

Underground microbial ecosystems have profound impacts on plant health 1 – 5 . Recently, essential roles have been shown for plant specialized metabolites in shaping the rhizosphere microbiome 6 – 9 . However, the potential mechanisms underlying the root-to-soil delivery of these metabolites remain to be elucidated 10 . Cucurbitacins, the characteristic bitter triterpenoids in cucurbit plants (such as melon and watermelon), are synthesized by operon-like gene clusters 11 . Here we report two Multidrug and Toxic Compound Extrusion (MATE) proteins involved in the transport of their respective cucurbitacins, a process co-regulated with cucurbitacin biosynthesis. We further show that the transport of cucurbitacin B from the roots of melon into the soil modulates the rhizosphere microbiome by selectively enriching for two bacterial genera, Enterobacter and Bacillus , and we demonstrate that this, in turn, leads to robust resistance against the soil-borne wilt fungal pathogen, Fusarium oxysporum . Our study offers insights into how transporters for specialized metabolites manipulate the rhizosphere microbiota and thereby affect crop fitness.