Dorsal mesoderm has a dual origin and forms by a novel mechanism in Hymenochirus, a relative of Xenopus

• Published in: Developmental biology 1996-02, Vol.174 (1), p.92-103
• Main Authors: Minsuk, S B, Keller, R E
• Format: Article
• Language: English
• Subjects: Animals; Embryonic Induction; Mesoderm - cytology; Microscopy, Electron, Scanning; Morphogenesis; Phylogeny; Pipidae - embryology
• ISSN: 0012-1606
• DOI: 10.1006/dbio.1996.0054

The dorsal mesoderm in the frog Hymenochirus forms by a mechanism not previously described in any other vertebrate. Unlike its close relative, Xenopus laevis, in which the mesoderm derives entirely from the deep mesenchymal cells of the marginal zone, Hymenochirus has "surface mesoderm" originating in the involuting marginal zone epithelium. Fluorescently labeled grafts show stage-specific invasion of deep axial tissue by cells originally located in the surface layer. These cells participate in normal mesoderm development. In video recordings, the labeled surface area shrinks as surface cells invade the deep layer. Furthermore, the mechanism of surface mesoderm morphogenesis differs from that described in other amphibians. Scanning electron microscopy at several neurula stages indicates that prospective somite cells do not individually detach from their epithelial neighbors to ingress into the deep layer, as seen in other amphibians; instead, their basal ends adhere to the somitic mesoderm as a coherent layer, taking on somitic morphology while still a part of the archenteron lining. This novel morphogenetic process we dub "relamination." Prospective notochord cells individually spread on the ventral surface of the notochord, gradually ingressing from their epithelial neighbors, but by a mechansism involving active pulling and spreading by their invasive basal ends rather than depending on apical constriction as do the corresponding "bottle cells" in other amphibians. Lateral endoderm migrates dorsally, replacing the relaminating surface mesoderm and fusing at the dorsal midline of the archenteron. These processes demonstrate the diversity of morphogenesis at the cellular, and presumably the molecular, level and shed light on the evolution of morphogenetic mechanisms.