Ricca’s factors as mobile proteinaceous effectors of electrical signaling

Highlights

• 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

Summary

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.