Prosystemin-derived signals: bridging leaf microbiome dynamics and defense activation

AbstractThe use of plant-derived peptides as resistance inducers provides innovative and potentially environmentally friendly methods to safeguard crop health. Although their use is increasing rapidly, their broader impact, particularly on plant-associated microbiomes, remains underexplored. This study investigated the influence of a promising immunomodulatory peptide derived from the tomato defense protein prosystemin on the tomato phyllosphere microbiome. We applied the peptide via foliar spray biweekly to simulate common agricultural practices from the planting stage to two months post-germination. Using a shotgun metagenomics approach combined with qPCR, we identified bacterial communities of high abundance (up to 4.6 log10 bacterial 16S rRNA copies) and high diversity, mainly comprising Actino-, Alphaproteo- and Gammaproteobacteria, on all tomato leaves. The peptide treatment led to a significant and targeted shift in the bacterial community, characterized by reduced diversity and network complexity and species loss, i.e., Streptomyces. The enrichment was predominantly observed in bacterial genera such as Acinetobacter, Sphingobium, Sphingomonas, Brevundimonas, and Massilia, which are typically associated with improved plant growth and stress resilience. Intriguingly, shifts in both taxonomic and functional profile upon peptide application aligned with patterns typically observed during plant defense activation, involving jasmonic acid and related secondary metabolites. Members of the Sphingomonadaceae family, particularly Sphingobium yanoikuyae, have emerged as potential drivers of such microbial dynamics, likely adapting to plant upregulated defenses and potentially supporting its resilient phenotype. Overall, in addition to its well-established role in combating tomato pests and necrotrophic fungi, the prosystemin-derived peptide paves the way for disentangling peptide-induced resistance and its interplay with the plant microbiota.