Land plants thrive in soils showing vastly different properties and environmental stresses. Root systems can adapt to contrasting soil conditions and stresses, yet how their responses are programmed at the individual cell scale remains unclear. Using single-cell RNA sequencing and spatial transcriptomic approaches, we showed major expression changes in outer root cell types when comparing the single-cell transcriptomes of rice roots grown in gel versus soil conditions. These tissue-specific transcriptional responses are related to nutrient homeostasis, cell wall integrity and defence in response to heterogeneous soil versus homogeneous gel growth conditions. We also demonstrate how the model soil stress, termed compaction, triggers expression changes in cell wall remodelling and barrier formation in outer and inner root tissues, regulated by abscisic acid released from phloem cells. Our study reveals how root tissues communicate and adapt to contrasting soil conditions at single-cell resolution.