While many phenylpropanoid pathway-derived molecules act as physical and
chemical barriers to pests and pathogens, comparatively little is known
about their role in regulating plant immunity. To explore this research
field, we transiently perturbed the phenylpropanoid pathway through
application of the CINNAMIC ACID-4-HYDROXYLASE (C4H) inhibitor
piperonylic acid (PA). Using bioassays involving diverse pests and
pathogens, we show that transient C4H inhibition triggers systemic,
broad-spectrum resistance in higher plant without affecting growth. PA
treatment enhances tomato (Solanum lycopersicum) resistance in field and
laboratory conditions, thereby illustrating the potential of
phenylpropanoid pathway perturbation in crop protection. At the
molecular level, transcriptome and metabolome analyses reveal that
transient C4H inhibition in tomato reprograms phenylpropanoid and
flavonoid metabolism, systemically induces immune signaling and
pathogenesis-related genes, and locally affects reactive oxygen species
metabolism. Furthermore, C4H inhibition primes cell wall modification
and phenolic compound accumulation in response to root-knot nematode
infection. Although PA treatment induces local accumulation of the
phytohormone salicylic acid, the PA resistance phenotype is preserved in
tomato plants expressing the salicylic acid-degrading NahG construct.
Together, our results demonstrate that transient phenylpropanoid pathway
perturbation is a conserved inducer of plant resistance and thus
highlight the crucial regulatory role of this pathway in plant immunity.