The Arabidopsis <i>e</i>ATP receptor DORN1 and CNGC19 calcium channel act in tandem to regulate plant defense upon <i>Spodoptera litura</i> herbivory

Abstract

Plants deploy cellular calcium (Ca2+) elevation in environmental stress signaling. Extracellular ATP (eATP) is released into the extracellular matrix when cells are wounded. DOES NOT RESPOND TO NUCLEOTIDES 1 (DORN1), a key legume-type lectin receptor, senses and binds eATP and activates Ca2+ signaling. No evidence directly links calcium-mediated eATP signaling to resistance against insect herbivores. Here, we report up-regulation of DORN1 transcripts in response to wounding and Spodoptera litura feeding in Arabidopsis. Loss of function of DORN1 resulted in increased S. litura feeding compared with the wild type. Plant immunity was compromised in dorn1 mutants as they showed reduced S. litura oral secretion-mediated Ca2+ elevation, jasmonic acid accumulation, and expression of jasmonate responsive genes. The herbivory-induced calcium channel, CYCLIC NUCLEOTIDE GATED CHANNEL 19 (CNGC19), co-expresses with DORN1. We found that eATP-induced Ca2+ elevation requires functional CNGC19. Loss of function of DORN1 and CNGC19 substantially increased the susceptibility to S. litura, mediated by reduced accumulation of jasmonates. We also demonstrated a plausible interaction of CNGC19 with DORN1. Our results indicate damage-released eATP and its receptor DORN1 in herbivory-induced defense signaling. DORN1 together with the Ca2+ channel CNGC19 generate the eATP-induced Ca2+ elevation, leading to the activation of immune signaling.