SlS5H silencing reveals specific pathogen-triggered salicylic acid metabolism in tomato

• DOI: 10.1186/s12870-022-03939-5
• Publication Date: 2022-11-29T07:30:23Z
• Authors: C. Payá; S. Minguillón; M. Hernández; S. M. Miguel; L. Campos; I. Rodrigo; J. M. Bellés; M. P. López-Gresa; P. Lisón
• Keywords: Plant stress; 0303 health sciences; Pathogen; Research; Gentisates; Botany; Defence; Pseudomonas syringae; Salicylic acid; Tomato; 03 medical and health sciences; Solanum lycopersicum; QK1-989; BIOQUIMICA Y BIOLOGIA MOLECULAR; Metabolomics; Phenolics; Salicylic Acid

AbstractBackgroundSalicylic acid (SA) is a major plant hormone that mediates the defence pathway against pathogens. SA accumulates in highly variable amounts depending on the plant-pathogen system, and several enzyme activities participate in the restoration of its levels. Gentisic acid (GA) is the product of the 5-hydroxylation of SA, which is catalysed by S5H, an enzyme activity regarded as a major player in SA homeostasis. GA accumulates at high levels in tomato plants infected by Citrus Exocortis Viroid (CEVd), and to a lesser extend uponPseudomonas syringaeDC3000 pv.tomato(Pst) infection.ResultsWe have studied the induction of tomatoSlS5Hgene by different pathogens, and its expression correlates with the accumulation of GA. Transient over-expression ofSlS5HinNicotiana benthamianaconfirmed that SA is processed by SlS5H in vivo.SlS5H-silenced tomato plants were generated, displaying a smaller size and early senescence, together with hypersusceptibility to the necrotrophic fungusBotrytis cinerea. In contrast, these transgenic lines exhibited an increased defence response and resistance to both CEVd andPstinfections. Alternative SA processing appears to occur for each specific pathogenic interaction to cope with SA levels. InSlS5H-silenced plants infected with CEVd, glycosylated SA was the most discriminant metabolite found. Instead, inPst-infected transgenic plants, SA appeared to be rerouted to other phenolics such as feruloyldopamine, feruloylquinic acid, feruloylgalactarate and 2-hydroxyglutarate.ConclusionUsingSlS5H-silenced plants as a tool to unbalance SA levels, we have studied the re-routing of SA upon CEVd andPstinfections and found that, despite the common origin and role for SA in plant pathogenesis, there appear to be different pathogen-specific, alternate homeostasis pathways.