Differentiation of the Metameric Pattern in the Embryonic Axis of the Mouse: II. Somitomeric Organization of the Presomitic Mesoderm

Abstract

The formation of the embryonic axis is brought about by the continuous recruitment of cells from the primitive streak, and at later stages from the tail bud. Presumptive somitic cells are first incorporated into presomitic mesoderm before they emerge as metamerically arranged somites. When the presomitic mesoderm was examined in stereo with the scanning electron microscope (SEM), mesenchymal cells were found to be already organized into segmental units. These segmental units are called somitomeres because of their striking similarity to structures in the embryonic axis of the chick embryo described by Meier [16]. Cells within the somitomere are arranged in concentric whorls about a core center, bisected by a medio-lateral seam which subdivides the cell population into anterior and posterior halves. The concentric configuration of the cells is most easily observed along the medial face of the presomitic mesoderm when it is generally wedge-shaped. Even tough the units are tandemly contiguous, somitomeric interfaces are distinguished by abrupt change in cellular orientation. Despite a nearly two-fold fluctuation in the overall size of the presomitic mesoderm during embryonic development, a relatively constant number of somitomeres (six) is found in tandem sequence. Somitomeric maturation culminating in somite formation involves compaction of the cell population, more orderly alignment of cells, reduction in extracellular space, and changes in the shape of the somitomere concomitant with neurulation. Though the more mature somitomere is about 70% the size of the most recently formed somitomere at the caudal end of the presomitic mesoderm, the average size of each somitomere is adjusted proportionally to the overall length of the presomitic mesoderm. In vitro culture of the presomitic mesoderm shows a direct developmental lineage between the somitomere and the somite, suggesting that somite formation is a morphologic manifestation of a somitomeric pattern laid down at an earlier stage in development. The somitomeric pattern in the paraxial mesoderm is the earliest recognizable morphologic evidence of metamerism in the embryonic axis. This pattern is later emulated by other tissues that are topographically associated with the paraxial mesoderm.