Extracellular ATP Acts on Jasmonate Signaling to Reinforce Plant Defense

Abstract

Damaged cells send various signals to stimulate defense responses. Recent identification and genetic studies of the plant purinoceptor, P2K1 (also known as DORN1), have demonstrated that extracellular ATP is a signal involved in plant stress responses, including wounding, perhaps to evoke plant defense. However, it remains largely unknown how extracellular ATP induces plant defense responses. Here, we demonstrate that extracellular ATP induces plant defense mediated through activation of the intracellular signaling of jasmonate (JA), a well-characterized defense hormone. In Arabidopsis (Arabidopsis thaliana) leaves, ATP pretreatment induced resistance against the necrotrophic fungus, Botrytis cinerea. The induced resistance was enhanced in the P2K1 receptor overexpression line, but reduced in the receptor mutant, dorn1-3. Mining the transcriptome data revealed that ATP induces a set of JA-induced genes. In addition, the P2K1-associated coexpression network contains defense-related genes, including those encoding jasmonate ZIM-domain (JAZ) proteins, which play key roles as repressors of JA signaling. We examined whether extracellular ATP impacts the stability of JAZ1 in Arabidopsis. The results showed that the JAZ1 stability decreased in response to ATP addition in a proteasome-dependent manner. This reduction required intracellular signaling via second messengers-cytosolic calcium, reactive oxygen species, and nitric oxide. Interestingly, the ATP-induced JAZ1 degradation was attenuated in the JA receptor mutant, coi1, but not in the JA biosynthesis mutant, aos, or upon addition of JA biosynthesis inhibitors. Immunoprecipitation analysis demonstrated that ATP increases the interaction between COI1 and JAZ1, suggesting direct cross talk between extracellular ATP and JA in intracellular signaling events. Taken together, these results suggest that extracellular ATP signaling directly impacts the JA signaling pathway to maximize plant defense responses.

Phosphate excess increases susceptibility to pathogen infection in rice

“…In this manner, extracellular ATP can be considered as a signalling molecule for the activation of Arabidopsis defence responses (Cao et al , ). More recently, extracellular ATP has been shown to play a role in the JA‐induced defence response of Arabidopsis through the direct activation of JA signalling (but not via JA biosynthesis) (Tripathi et al , ; Jewell et al , ). Evidence for a role of extracellular ATP as signalling molecule for the expression of defence responses in rice is, however, lacking.…”

Nucleotide Metabolism in Plants

“…Simultaneous genetic blockage of nucleoside uptake and hydrolysis leads to an accumulation of adenosine and uridine in the apoplast, a reduction of PSII efficiency, and a higher susceptibility to the necrotrophic fungus Botrytis cinerea, possibly caused by reduced expression of WRKY33 (Daumann et al, 2015), which is known to be essential for Botrytis resistance (Liu et al, 2015). Treatment with eATP increases the resistance to Botrytis (Tripathi et al, 2018), and the expression of WRKY33 and other defense-related genes is reduced in a DORN1 mutant and boosted in a DORN1 overexpression line upon challenge with eATP (Jewell et al, 2019). Taken together, these observations suggest that adenosine accumulation in the apoplast dampens the DORN1-mediated response, indicating that ENT3 and NSH3 are required to remove the breakdown products of eATP signaling.…”

Cereal Root Interactions with Soilborne Pathogens—From Trait to Gene and Back

“…Because DORN1 is highly expressed in roots [47], DORN1-mediated resistance is dependent upon the jasmonate signal pathway [45,46,119], and wheat roots appear to possess an active jasmonate signal pathway [120], we hypothesize that expression of the wheat orthologue of the DORN1 gene will confer resistance to the necrotroph R. solani AG-8, hemibiotroph F. culmorum, and possibly to nematodes that cause cellular damage while migrating through host root tissue.…”