Mineral deficiency is a major problem in agriculture. Plant adaption to low mineral environments involves signaling between shoots and roots, via the food transport cells, the sieve elements. However, due to the sequestered position of the sieve elements in the vascular bundles, identifying shoot-to-root mobile signals is challenging. In herbaceous species, sieve elements and companion cells (CCs) are isolated from other leaf tissues. We hypothesize that phloem CCs play an essential role by synthesizing shoot-to-root signals in response to mineral deficiency. To test this hypothesis, we analyzed gene expression responses in Arabidopsis CCs under phosphorus deficiency using TRAP-Seq. Phosphorus was chosen for its importance in plant growth and the known role of shoot-to-root signaling in regulating root phosphate transporters during deficiency. Our findings revealed that CCs exhibit more dramatic molecular responses than other leaf cells. We also found that many genes altered in CCs have potential functions in regulating root growth. This is unexpected because it has been widely believed that shoot-to-root signaling is not involved in root growth regulation under P deficiency. The importance of CCs in regulating mineral deficiency may extend beyond phosphorus because shoot-to-root signaling is a common response to the deficiency of various minerals.