An environmentally regulated dichotomy in cell lineages of the root

Plant development is highly plastic, with growth and architecture continuously shaped by environmental conditions. Roots, for instance, adjust their development to local water, nutrient and soil conditions. Despite this plasticity, individual root cell types are generally viewed as largely homogeneous populations that progress along a single developmental trajectory1. Here we show that rather than progressing along a single developmental trajectory, most Arabidopsis root cell lineage trajectories exhibit a stereotyped bifid topology, as revealed by single-cell RNA sequencing and spatial transcript mapping. One branch is characterized by a transcriptional program that is shared across multiple cell types and enriched for genes associated with environmental responses, including abscisic acid (ABA) signalling. This state occurs reproducibly in a subset of cells across multiple cell types, independent of developmental lineage, thereby revealing an additional layer of root cell identity. It is conserved across Arabidopsis ecotypes and persists despite major perturbations in developmental identity. Moreover, it is reduced in ABA-deficient and ABA-insensitive mutants and becomes more prevalent under water-deficit conditions. Together, these findings reveal an additional layer of root cell identity that is superimposed on developmental lineage and its prevalence is modulated by environmental conditions. These results uncover a previously unrecognized source of environment-associated transcriptional heterogeneity shared across root cell types. An environment-regulated state is identified across multiple cell types at the root tip, revealing a shared dichotomy between cells with and without this state.