Abstract: Drought is the primary cause of global agricultural losses and represents a major threat to worldwide food security. Currently, plant biotechnology stands out as the most promising strategy to increase crop growth in rain-fed conditions. The main mechanisms underlying drought resistance have been uncovered by studies of plant physiology and by engineering crops with drought-resistant genes. However, plants with enhanced drought resistance usually display lower levels of growth, highlighting the need to search for novel strategies capable of uncoupling drought resistance from growth. Here, we show that the brassinosteroid family of receptors, in addition to promoting growth, guides phenotypic adaptation to a great variety of drought stress traits analyzed herein. Whilst mutations in the ubiquitously localized BRI1 receptor pathway show an enhanced drought resistance at the expense of plant growth, we found that vascular-enriched BRL3 receptors confer drought tolerance without penalizing overall growth. Systematic analyses reveal that upon drought stress the BRL3 receptor pathway triggers the synthesis and mobilization of osmoprotectant metabolites, mainly proline and sugars. This preferentially occurs in the vascular tissues of the roots and favors overall plant growth. Altogether, our results uncover a new role for the spatial control of BR signaling in drought tolerance, and offer a novel strategy to address food security issues in an increasingly water-limited climate. Overall design: 28 days old root system were collected from soil, quickly washed in water and flash-frozen. Experiment with a bifactorial design. Factor one is the genotype, which include WT (Col-0) and 35S:BRL3. Factor two is the condition, which include control (Properly watered) and 5 days of drought (water-hold) conditions. 3 Biological replicates were collected per each genotype and condition.