Extracellular ATP elicits DORN1-mediated RBOHD phosphorylation to regulate stomatal aperture

A multibillion dollar pharmaceutical industry targets purinergic signaling pathways in humans. However, in contrast, little is known about purinergic signaling in plants. Extracellular adenosine-5’-triphosphate (eATP) acts as a damage-associated molecular pattern (DAMP) in both animals and plants. The first plant eATP receptor, DORN1, was identified in Arabidopsis, defining a new kinase family (P2K) of purinoceptors. Stomates are leaf pores that control gas exchange and, therefore, impact critical functions such as photosynthesis and drought tolerance. Stomates are also the prefer entry point for leaf pathogens. The addition of ATP led to the rapid closure of Arabidopsis leaf stomates resulting in enhanced resistance to the bacterial pathogen Psuedomonas syringae. The data indicate that this response is mediated by eATP recognition by DORN1 followed by direct phosphorylation of the NADPH oxidase RBOHD, resulting in elevated production of reactive oxygen species and stomatal closure. Mutation of the DORN1 phosphorylation sites on RBOHD eliminated the ability of eATP to induce stomatal closure. To date, in contrast to work in animals, purinergic signaling in plants has been viewed as a curiosity without any direct, mechanistic connection to key plant processes. The data presented clearly demonstrates eATP as an important signal controlling stomatal aperture with important implications for the control of plant photosynthesis, water homeostasis, pathogen resistance and ultimately yield.