Generality of vertebrate developmental patterns: evidence for a dermomyotome in fish

Abstract

SummaryThe somitic compartment that gives rise to trunk muscle and dermis in amniotes is an epithelial sheet on the external surface of the somite, and is known as the dermomyotome. However, despite its central role in the development of the trunk and limbs, the evolutionary history of the dermomyotome and its role in non-amniotes is poorly understood. We have tested whether a tissue with the morphological and molecular characteristics of a dermomyotome exists in non-amniotes. We show that representatives of the agnathans and of all major clades of gnathostomes each have a layer of cells on the surface of the somite, external to the embryonic myotome. These external cells do not show any signs of terminal myogenic or dermogenic differentiation. Moreover, in the embryos of bony fishes as diverse as sturgeons (Chondrostei) and zebrafish (Teleostei) this layer of cells expresses the pax 3 and 7 genes that mark myogenic precursors. Some of the pax7-expressing cells also express the differentiation-promoting myogenic regulatory factor Myogenin and appear to enter into the myotome. We therefore suggest that the dermomyotome is an ancient and conserved structure that evolved prior to the last common ancestor of all vertebrates. The identification of a dermomyotome in fish makes it possible to apply the powerful cellular and genetic approaches available in zebrafish to the understanding of this key developmental structure.

Muscle stem cells and model systems for their investigation

“…However, the recent identification of the external Pax7-expressing somitic layer in zebrafish (Hollway et al, 2007;Stellabotte et al, 2007;Hammond et al, 2007) and its role in muscle growth strongly suggests that this cell population may correspond to a dermomyotome. Importantly, a similar layer of cells external to the embryonic myotome has been previously detected in several other lower vertebrates such as the lamprey (Nakao, 1977), sturgeon (Devoto et al, 2006), and lungfish (Maurer, 1906). They have been found in diverse teleosts, including the sea bass (Veggetti et al, 1990), herring (Johnston, 1993), and gilthead sea bream (Ramirez-Zarzoza et al, 1995), as well as in the amphibians Xenopus laevis (Hamilton, 1969) and European common frog (Maurer, 1906).…”

“…Some of these cells were also found to be myogenin-positive. The external Pax7-positive cells as well as those located deeper in the myotome, on the surface of differentiating fibers were also detected in the sturgeon (Devoto et al, 2006). Of interest, in amphibians, external cells also are the source of myogenic precursors (Grimaldi et al, 2004).…”

“…Because of the expression of a similar set of genes, Devoto et al (2006) suggest that the external layer of cells includes multipotent myogenic precursors and is an ancient and conserved structure, homologous to the amniote dermomyotome. Other authors (Hollway et al, 2007) argue that the external Pax7-positive somitic cells arise by means of the whole somite rotation and, thus, are not equivalent of the amniote dermomyotome.…”

A hedgehog homolog is involved in muscle formation and organization of Sepia officinalis (mollusca) mantle

“…These muscle precursor cells subsequently migrate into the "myoblast mass" and contribute to mantle muscle growth and spatial organization. For this reason, we speculate that such an embryonic structure could play a similar role of the layer of cells that Devoto et al (2006) have described in fish. This cell layer located underneath the epithelium and lining the surface of the somite is formed by myogenic precursors that migrate into the myotome, where they differentiate in muscle fibres.…”

Muscle differentiation in blackspot seabream (Pagellus bogaraveo, Brunnich): Histochemical and immunohistochemical study of the fibre types

“…The primary phase has been well studied in a very few species, most notably Danio rerio (Hamilton) (Devoto et al, 1996(Devoto et al, , 2006Stickney et al, 2000), but the post-embryonic myogenic phases (stratified hyperplasia during larval life, and the later mosaic hyperplasia) have received much less attention. Larval growth is important, however, for survival in the first few weeks post-hatching, and the last phase, mosaic hyperplasia, is by far the greatest contributor to the muscle growth that brings fish to commercial size for aquaculture; so, these phases are of considerable practical as well as biological interest.…”