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By providing adaptive advantages to plants, desert microorganisms are emerging as promising solutions to mitigate the negative and abrupt effects of climate change in agriculture. Among these, pseudomonads, commonly found in soil and in association with plants' root system, have been shown to enhance plant tolerance to salinity and drought, primarily affecting root system architecture in various hosts. However, a comprehensive understanding of how these bacteria affect plant responses at the cellular, physiological and molecular levels is still lacking. In this study, we investigated the effects of two Pseudomonas spp. strains, E102 and E141, which were previously isolated from date palm roots and have demonstrated efficacy in promoting drought tolerance in their hosts. These strains colonize plant roots, influencing root architecture by inhibiting primary root growth while promoting root hair elongation and lateral root formation. Strains E102 and E141 increased auxin levels in Arabidopsis, whereas this effect was diminished in IAA-defective mutant strains, which exhibited reduced IAA production. In all cases, the effectiveness of the bacteria relies on the functioning of the plant auxin response and transport machinery. Notably, such physiological and morphological changes provide an adaptive advantage to the plant, specifically under stress conditions such as salinity. Collectively, this study demonstrates that by leveraging the host's auxin signalling machinery, strains E102 and E141 significantly improve plant resilience to abiotic stresses, positioning them as potential biopromoters/bioprotectors for crop production and ecosystem restoration in alignment with Nature-based Solution approaches., (© 2024 The Author(s). Microbial Biotechnology published by John Wiley & Sons Ltd.)