Salinity severely hampers crop productivity worldwide and plant growth promoting bacteria could serve as a sustainable solution to improve plant growth under salt stress. However, the molecular mechanisms underlying salt stress tolerance promotion by beneficial bacteria remain unclear. In this work, six bacterial isolates from four different desert plant species were screened for their biochemical plant growth promoting traits and salinity stress tolerance promotion of the unknown host plant Arabidopsis thaliana. Five of the isolates induced variable root phenotypes but could all increase plant shoot and root weight under salinity stress. Inoculation of Arabidopsis with five isolates under salinity stress resulted in tissue-specific transcriptional changes of ion transporters and reduced Na+/K+ shoot ratios. The work provides first insights into the possible mechanisms and the commonality by which phylogenetically diverse bacteria from different desert plants induce salinity stress tolerance in Arabidopsis. The bacterial isolates provide new tools for studying abiotic stress tolerance mechanisms in plants and a promising agricultural solution for increasing crop yields in semi-arid regions.