Beyond Systemin: the multifaced role of ProSys_(1-178) in tomato defense

Plants constantly face multiple biotic and abiotic stresses, which they counteract through sophisticated immune mechanisms based on the recognition of endogenous and exogenous elicitors. Tomato Systemin (Sys), released from the C-terminal region of Prosystemin (ProSys), is a well-known peptide that activates jasmonic acid (JA)-dependent defense responses. In contrast, the N-terminal fragment ProSys_(1-178), lacking the Sys peptide, has recently emerged as an independent defense inducer, likely involving an OG-mediated pathway distinct from the JA signalling triggered by Sys. In this study, we investigated the molecular and biological responses elicited by ProSys_(1-178) in comparison with Sys by combining comparative transcriptomic analyses of ProSys_(1-178) and full-length ProSys (ProSys_FL) transgenic tomato plants with bioassays of peptide treated plants. Transcriptomic analysis revealed that ProSys_(1-178) induced a substantially broader transcriptional reprogramming than ProSys_FL, with only 46 differentially expressed genes in common, that displayed opposite expression patterns. Both transgenic lines conferred resistance against Spodoptera littoralis and Botrytis cinerea. Moreover, exogenous application of ProSys_(1-178) and Sys differentially modulated local and systemic defense-related gene expression and significantly reduced B. cinerea disease severity. Although Sys provided stronger protection against the fungal pathogen, ProSys_(1-178) modulated a broader set of defense-related genes, suggesting the activation of a distinct immune pathway. The induction of a polygalacturonase gene, together with the previous detection of short OGs in ProSys_(1-178)-expressing plants, is consistent with, but does not establish, an OG-associated component of this response. Overall, our findings support a multifaceted role for ProSys(1-178) in tomato immunity.