Developmental role of dpp in the gastropod shell plate and co-option of the dpp signaling pathway in the evolution of the operculum

• Published in: Developmental biology 2012-06, Vol.366 (2), p.367-373
• Main Authors: Hashimoto, Naoki, Kurita, Yoshihisa, Wada, Hiroshi
• Format: Article
• Language: English
• Subjects: abnormal development; Animal Shells - embryology; Animal Shells - physiology; Animals; Biological Evolution; cell proliferation; chitin synthase; double-stranded RNA; dpp; edge effects; evolution; ferritin; Gastropod; Gastropoda; Gastropoda - embryology; Gene Expression Regulation, Developmental; genes; grainyhead; Homeodomain Proteins - physiology; Mollusc; Mollusca; molluscs; Operculum; secretion; Shell plate; Signal Transduction
• ISSN: 0012-1606; 1095-564X
• DOI: 10.1016/j.ydbio.2012.04.010

The operculum is a novel structure in gastropod molluscs. Because the operculum shows notable similarities to the shell plate, we asked whether there were an evolutionary link between these two secretory organs. We found that some of the genes involved in shell-field development are expressed in the operculum, such as dpp and grainyhead, whereas engrailed and Hox1 are not. Specific knockdown of dpp by injection of double-stranded RNA (dsRNA) resulted in malformation of the shell plate. The shell plate was smaller due to failure of activation of cell proliferation in the shell-field margin. The expressions of grainyhead and chitin synthase 1 in the shell field margin were suppressed by dpp-dsRNA. However, matrix secretion was not completely abolished, and the expressions of ferritin, engrailed or Hox1 were not affected by dpp-dsRNA, indicating that dpp is partly involved in the developmental pathway for shell matrix secretion. We also present evidence that dpp performs a key role in operculum development. Indeed, dpp-dsRNA impaired matrix secretion in the operculum as well as expression of grainyhead. Based on these observations that dpp is important for development of both the shell plate and operculum, we conclude that co-option of dpp to the posterior part of the foot contributed to the innovation of the operculum in gastropods. ► Dpp is required for expressions of chitin synthase 1 and grainyhead in shell field margin. ► Knockdown of dpp led to suppression of cell proliferation in the mantle edge. ► Dpp is essential for operculum development and grainyhead expression. ► Co-option of dpp-grainyhead pathway may have contributed evolution of the operculum.