Plant development is extremely flexible as compared to animals. Roots, for instance, can adapt their development to their substrate, water and nutrient availability, or the local biome. This plasticity of root development suggests that, at a cellular level, environmental inputs should have a substantial impact on cell fates. However, the diversity of root cell identities at the root tip is currently viewed as ontogenetically driven, with discrete cell types arising from stem cells along a linear differentiation trajectory, very similarly to animal lineages, with no impact from environmental conditions. We used scRNA-seq and spatial mapping to deeply explore the trajectories of cell states at the tip of Arabidopsis roots, known to contain multiple developing lineages. We found that, contrary to the current model of cell identity acquisition in the root, most lineage trajectories exhibit a stereotyped bifid topology with two developmental trajectories rather than one. The formation of one of the trajectories is driven by a strong and specific activation of genes involved in the responses to various environmental stimuli, which affects only a subset of the cells in multiple cell types simultaneously. This reveals another layer of patterning of cell identities in the root that is independent of cell ontogeny. We demonstrate the robustness of this environmentally responsive transcriptional state by showing that it is present in a mutant where cell type identities are greatly perturbed, as well as in different Arabidopsis ecotypes. We show that ecotype-specific differentially expressed genes known to be involved in environmental responses are part of this state. Finally, we demonstrate that the root can adapt the proportion of cells that acquire this state in response to environmental signals such as nutrient availability. The discovery of this alternate fate trajectory reveals new layers of cell identity that may underpin the adaptive potential of plant development.