Little is known about the way developmental cues affect how cells interpret their environment. We characterized the transcriptional response to high salinity of different cell layers and developmental stages of the Arabidopsis root and found that transcriptional responses are highly constrained by developmental parameters. These transcriptional changes lead to the differential regulation of specific biological functions in subsets of cell layers, several of which correspond to observable physiological changes. We showed that known stress pathways primarily control semiubiquitous responses and used mutants that disrupt epidermal patterning to reveal cell-layer-specific and inter-cell-layer effects. By performing a similar analysis using iron deprivation, we identified common cell-type-specific stress responses and revealed the crucial role the environment plays in defining the transcriptional outcome of cell-fate decisions.