Deciphering molecular events behind Systemin-induced resistance against Botrytis cinerea in tomato plants

J Exp Bot. 2024 Apr 6:erae146. doi: 10.1093/jxb/erae146. Online ahead of print.

Abstract

Plant defense peptides are paramount endogenous danger signals secreted after a challenge intensifying the plant immune response. The peptidic hormone Systemin (Sys) was shown to participate in resistance in several plant-pathosystems, although the mechanisms behind Sys-IR when exogenously applied remain elusive. We performed proteomic, metabolomic and enzymatic studies to decipher the Sys-induced changes in tomato plants either in the absence or the presence of Botrytis cinerea infection. Sys-treatments triggered direct proteomic rearrangement mostly involved in carbon metabolism and photosynthesis. However, the final induction of defense proteins required concurrent challenge, triggering priming of pathogen-targeted proteins. Conversely, at the metabolomic level, Sys-treated plants showed an alternative behaviour following a general priming profile. Out of the primed metabolites, the flavonoids rutin and isorhamnetin and two alkaloids correlated with the proteins 4-coumarate-CoA-ligase and chalcone-flavanone-isomerase triggered by Sys treatment. In addition, the proteomic and enzymatic analyses revealed that Sys conditioned the primary metabolism towards the production of available sugars that could be fuelling the priming of callose deposition in Sys-treated plants, furthermore PR1 appeared as as key element in Sys-induced resistance. Collectively, the direct induction of proteins and priming of specific secondary metabolites in Sys-treated plants indicated that posttranslational protein regulation is an additional component of priming against necrotrophic fungi.