Hydroxycinnamic Acid Amides Emerge as Multifunctional Molecules Involved in Regeneration and Volatile Signalling...

Hydroxycinnamic acid amides (HCAAs) are phenylpropanoid-derived metabolites traditionally associated with antimicrobial defence and cell wall reinforcement during plant-pathogen interactions. However, their contribution to plant responses to mechanical injury, particularly in wound healing and damage-induced signalling, remains poorly understood. In this study, we investigated the wound-induced responses in tomato (Solanum lycopersicum) using a 35S::THT system in which tyramine hydroxycinnamoyl transferase (THT), a key enzyme controlling HCAAs biosynthesis, is overexpressed. By integrating metabolite profiling, gene expression analyses, confocal microscopy, antioxidant capacity assays, and volatile organic compound (VOCs) analysis, we characterised local and systemic responses to mechanical damage. The 35S::THT line displayed a stronger wound-induced accumulation of HCAAs compared to WT, with consistently higher levels of free amides and increased accumulation of tyramine-derived amides in the cell wall-bound fraction following wounding, which was associated with pronounced structural reinforcement at injury sites. Enhanced vascular lignification, increased suberization, and callose deposition were observed, collectively contributing to improved tissue regeneration capacity or associated with enhanced tissue regeneration capacity. These structural changes were accompanied by alterations in redox-related responses, supporting a role for HCAAs in modulating oxidative balance during wound repair. In addition to local effects, the 35S::THT line emitted a specific wound-responsive VOC blend, capable of inducing defence-related gene expression in neighbouring wild-type even in the absence of direct injury, suggesting a role for HCAAs in airborne signalling and defence priming. Together, these results show that a metabolic background characterised by elevated HCAAs levels is associated with coordinated changes in structural reinforcement, redox responses, regeneration, and volatile-mediated communication during the tomato wound response. These observations support the idea that HCAAs may act as important integrative components linking local and systemic responses to mechanical stress.