Eggs and embryos of the purple sea urchin (Strongylocentrotus purpuratus) contain profilin that is partly supplied from maternal sources and partly produced by the gastrula. The maternal profilin protein content is about 13 microM and it persists in the embryo at least through gastrulation. Transcript quantitation from probe excess titrations show that very few profilin gene transcripts are present in the embryo during cleavage, but that they increase at the onset of gastrulation. By in situ hybridization, the newly synthesized profilin transcripts are localized in mesenchyme cells. Profilin gene expression increases when mesenchyme cells initiate migration and filopodial extension and retraction. We show that there are three isoforms of maternal profilin protein produced from the single copy gene during oogenesis. However, the blastula stage embryo only produces the major isoform, whereas the acidic isoform is produced in the early stages of gastrulation and the basic isoform appears by the end of gastrulation. Based on transcript prevalence and protein production rates, our calculations indicate that the amount of new protein produced in the mesenchyme cells in 12 hr is at maximum < 2% of that supplied from maternal sources. Because of the large amount of maternally supplied profilin present in the egg and embryo, we suggest that it may be used in the cytokinetic processes of cleavage. Alternatively, because of the small amount of embryonically produced profilin, we suggest that it may function in the cytoskeletal shape changes required for filopodial extension and motility in the mesenchyme cells during gastrulation.