ABSTRACT Water deficit impairs growth and survival of plants. Many water stress responses are under control of abscisic acid (ABA) but little is known about growth control under osmotic stress. Based on the previously described growth-promoting activity of the peptide hormone phytosulfokine (PSK), we hypothesized that it may contribute to growth regulation under water stress conditions. To test this hypothesis, we analyzed the Arabidopsis thaliana PSK receptor (PSKR) null mutant pskr1-3 pskr2-1 under mannitol and drought stress. In particular under mild water stress, fresht weight and photosynthetic efficiency were more reduced in pskr1-3 pskr2-1 than in wild type. Hydroponic and grafting experiments showed that PSKR signaling was not required for long-distance signaling from mannitol-stressed roots to shoot but rather for cell growth promotion in the shoot. Unlike wild type, pskr1-3 pskr2-1 shoots did not accumulate ABA in response to mannitol, showed misregulation of ABA synthesis genes and elevated expression of ABI1 and ABI2 , repressors of ABA signaling whereas application of ABA partially reversed shoot growth inhibition by mannitol in pskr1-3 pskr2-1 . In turn, mannitol and ABA induced expression of PSK3 and PSKR1, and ABA promoted expression of PSK2 and PSK4 revealing feedback regulatory loops between PSKR and osmotic stress signaling. Highlight Phytosulfokine receptor signaling regulates ABA synthesis and signaling genes and promotes ABA accumulation in the shoot of water-stressed plants and maintains leaf growth and photosynthetic efficiency which ensures plant health.