The plant hormone brassinosteroid (BR) plays essential roles in plant growth and development, while also controlling plant stress responses. This dual ability of BR is intriguing from a echanistic point of view and as a viable solution for stabilizing crop yields under the changing limatic conditions. Here we report a time course analysis of BR responses under both stress and no-stress conditions, the results of which establish that BR incorporates many stress-related features even under no-stress conditions, which are then accompanied by a dynamic stress response under unfavourable conditions. Found within the BR transcriptome were distinct molecular signatures of two stress hormones, abscisic acid and jasmonic acid, which were correlated with enhanced endogenous levels of the two hormones in BR-treated seedlings. The marked presence of genes related to protein metabolism and modification, defence responses and calcium signalling highlights the significance of their associated mechanisms and roles in BR processes. Functional analysis of loss-of-function mutants of a subset of genes selected from the BR transcriptome identified abiotic stress-related roles for 'ACID PHOSPHATASE5 (ACP5)', 'WRKY33', JACALIN-RELATED LECTIN1-3' ('JAC-LEC1-3') and a 'BR-RESPONSIVE-RECEPTOR-LIKE KINASE' ('BRRLK'). Overall, the results of this study provide a clear link between the molecular changes impacted by BR and its ability to confer broad-range stress tolerance, emphasize the importance of post-translational modification and protein turnover as BR regulatory mechanisms and demonstrate the BR transcriptome as a repertoire of new stress-related regulatory and structural genes.