Ricca’s factors as mobile proteinaceous effectors of electrical signaling

Leaf-feeding insects trigger high-amplitude, defense-inducing electrical signals called slow wave potentials (SWPs). These signals are thought to be triggered by the long-distance transport of low molecular mass elicitors termed Ricca’s factors. We sought mediators of leaf-to-leaf electrical signaling in Arabidopsis thaliana and identified them as β-THIOGLUCOSIDE GLUCOHYDROLASE 1 and 2 (TGG1 and TGG2). SWP propagation from insect feeding sites was strongly attenuated in tgg1 tgg2 mutants and wound-response cytosolic Ca2+ increases were reduced in these plants. Recombinant TGG1 fed into the xylem elicited wild-type-like membrane depolarization and Ca2+ transients. Moreover, TGGs catalyze the deglucosidation of glucosinolates. Metabolite profiling revealed rapid wound-induced breakdown of aliphatic glucosinolates in primary veins. Using in vivo chemical trapping, we found evidence for roles of short-lived aglycone intermediates generated by glucosinolate hydrolysis in SWP membrane depolarization. Our findings reveal a mechanism whereby organ-to-organ protein transport plays a major role in electrical signaling. [Display omitted] •Leaf wounding triggers electrical signals that reach distal undamaged leaves•Leaf-to-leaf electrical signal propagation depends on mobile glucohydrolase enzymes•Glucohydrolase enzymes generate short-lived aglucone elicitors of membrane depolarization•Inter-organ protein mobility underlies electrical signaling in a wounded plant β-THIOGLUCOSIDE GLUCOHYDROLASE 1 and 2 as xylem-mobile factors to generate membrane depolarizing elicitors in the veins of wounded Arabidopsis, highlighting a mechanism for inter-organ electrical signaling in wounded plants.