This study elucidates the mechanisms by which coumaric acid—a persistent allelochemical in continuous cropping soils—drives cropping obstacles through an integrated multi-omics and ecological approach. While prior work identified coumaric acid as a key autotoxin, how it migrates in soil, reshapes the microbiome, and reprograms plant metabolism has remained unresolved. We show that as cropping duration increases, coumaric acid retention in soil is prolonged, amplifying its phytotoxicity. The compound directly suppresses tobacco growth by disrupting antioxidant systems and hormonal balance. Concurrently, it reshapes the rhizosphere microbiome, favoring saprophytic and potentially pathogenic fungi over beneficial bacteria. Multi-omics analyses revealed that coumaric acid redirects carbon flux toward stress defense while impairing starch/sucrose metabolism and the biosynthesis of protective phenylpropanoids/flavonoids, culminating in energy depletion, oxidative damage, and stunted root development. By linking soil chemical dynamics, microbial ecology, and plant molecular networks, this work provides an integrative framework that informs sustainable mitigation strategies. • Coumaric acid soil retention prolongs with continuous cropping, amplifying rhizosphere persistence and phytotoxicity. • Coumaric acid redirects carbon flux to defense while impairing starch/sucrose and phenylpropanoid/flavonoid metabolism. • It reshapes the rhizosphere microbiome, favoring saprophytic/pathogenic fungi over beneficial bacteria. • Multi-omics integration reveals disrupted antioxidant systems, hormonal imbalance, and energy depletion in tobacco. • An integrative framework links soil chemistry, microbial ecology, and plant molecular networks to inform mitigation.
Shi et al. (Fri,) studied this question.