Gallic Acid-Responsive microRNAs Reprogram Lignification During Drought Acclimation Process in Spearmint

Mentha spicata L. (spearmint) is a high-value aromatic and medicinal species, whose productivity is strongly affected by water deficit. Nevertheless, the molecular mechanisms underlying drought acclimation in this mint remain largely unexplored. Thus, here, we investigated the microRNA-mediated regulatory processes triggered in M. spicata under drought stress (DS) and following treatment with gallic acid (GA), a natural phenolic compound that our research group has already documented to be a potential biostimulant for spearmint. A small-RNA sequencing approach revealed that both DS and GA induced substantial changes of the expressed miRNome, modulating 35 microRNAs (e.g., miR397a, miR159a, miR172b) whose predicted targets (e.g., Laccase-2, MYB transcription factors) are known to be involved also in lignin production. In detail, DS induced upregulation of lignin biosynthetic genes, enhancement of Laccase activity, and shifting in lignin monomer composition, promoting the putative reinforcement of the cell wall as expected during water deficiency. Conversely, GA treatment attenuated DS-induced stress, regulating microRNA-mRNA modules which balanced phytochemical and hormonal response while maintaining controlled lignification and optimising xylem function. These results highlight the pivotal role of microRNAs in orchestrating drought acclimation in M. spicata and identify GA as a compensatory agent under water-limiting conditions, capable of fine-tuning growth, cell wall remodelling, and redox homeostasis. Collectively, our findings provide molecular insights into biostimulant-mediated stress resilience and identify GA treatment as a promising biotechnological strategy to improve drought tolerance in Lamiaceae crops.