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The inability of a plant to run from danger or seek nutrients necessitates its capacity to change the environment of the surrounding soil for protection and sustenance. A unique plant process, the release of thousands of autonomous cells from the root cap, called root border cells, may play a role in the ability of the plant to regulate microbial populations and nutrient availability in the rhizosphere. In this study, evidence is presented showing that root border cells are a differentiated tissue, that the production of border cells is highly regulated and tied to cell turnover in the root cap and that products of border cells regulate cell division in the root cap meristem. In vivo labeling experiments demonstrate that 13% of the proteins that are abundant in preparations from border cells are undetectable in root tip cells. Differences between the two cell populations are apparent as soon as border cells separate from each other, even when they are still adhered to the root tip. Twenty-five percent of the proteins synthesized by border cells in a 1-hour period are rapidly excreted into the incubation medium. Border cells arise within the root cap meristem by cell division and their production is tightly regulated both developmentally and in response to border cell removal. Removal of border cells results in the induction of cell division in the transverse root cap meristem to 400% of the basal rate within 30 minutes. This elevated rate of mitosis is maintained for 1.5 h and falls to basal levels within 6 hours. During this time, mitosis in the root apical meristem remains constant. mRNA differential display analysis showed changes in gene expression in the root cap within 5 to 15 minutes of removal of border cells. Genes putatively involved in cell functions in three regions of the cap showed expected distribution patterns by in situ hybridization and RNA blot analysis revealed changes in their expression patterns were seen in response to border cell removal. The