Roots and shoots thrive in distinct environments; nevertheless, roots possess the ability to sense adverse environmental conditions encountered by the shoots. The Shade Avoidance Response (SAR), induced by sub-optimal light conditions emanating from nearby vegetation, prompts the rapid growth of stems and petioles to optimize light absorption. However, this response also results in compromised root growth, thereby affecting the overall performance of plants negatively. Despite the pivotal role of roots in plant growth and productivity, there is limited knowledge regarding the mechanisms influencing root growth when shoots detect alterations in light conditions. Recognizing the significance of roots in the broader context of plant development, we aimed to unravel the mechanisms through which vegetative shading impacts root growth. To achieve this, we created a high-resolution spatiotemporal transcriptome map of shade-grown plant roots using single-cell RNA sequencing. This approach allowed us to unveil tissue-specific programs that impede root growth under shade. Our investigation revealed that the epidermal and pericycle cell types exhibited the most pronounced responses to shading. Furthermore, we identified several cell-type-specific transcriptional programs that collaboratively contribute to the inhibition of root growth under shaded conditions. This research enhances our understanding of how roots adapt to environmental cues and provides valuable insights for optimizing plant growth and productivity in varying light environments.