Phytosulfokine receptors mediate stomatal closure in response to abscisic acid by controlling reactive oxygen species levels in guard cells

Plants are exposed to multiple abiotic and biotic stresses. To coordinate and integrate stress signals at the tissue and organ level, plants require cell-to-cell communication. Phytohormones, including peptide hormones, are essential components in plant signaling processes. Phytosulfokine (PSK) is a peptide hormone that was recently shown to maintain growth and delay leaf senescence under drought conditions. This study shows that PSK signaling controls transpiration by mediating stomatal closure to prevent water loss. To elucidate the molecular mechanism by which PSKR signaling mediates stoma closure, ROS accumulation in response to the drought signal ABA was analyzed with an H2O2-sensitive dye. Guard cells of pskr1‑3 pskr2-1 plants accumulated less ROS when treated with ABA. Since ROS accumulation in guard cells depends on activation of NADPH oxidases RBOHD/F at the plasma membrane, we tested the hypothesis that RBOHD/F are activated by PSKRs. Förster Resonance Energy Transfer (FRET) analyses revealed proximity of PSKR1 and RBOHD/F in situ. In addition, the kinase domain of PSKR1 phosphorylated RBOHD and RBOHF in vitro, indicating that RBOHD/F may be substrates of PSKR1. Stoma closure requires rapid water movement out of guard cells and uptake of H2O2. The entry of H2O2 into guard cells is facilitated by the aquaporin PLASMA MEMBRANE INTRINSIC PROTEIN 2;1 (PIP2;1) that could also be a target of PSKRs. A kinase assay revealed phosphorylation of PIP2;1 by PSKR1 kinase in vitro providing first evidence that PSKR1 may control H2O2 uptake into guard cells. Taken together, PSKR signaling is required for ABA-mediated stomatal closure by controlling ABA-induced ROS accumulation in guard cells possibly through direct phosphorylation of RBOHD/F and/or PIP2;1 at the plasma membrane. 


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