The main body axis of all vertebrates has a repetitive, periodic structure, seen in the series of vertebrae, ribs, and segmental muscles of the neck, trunk, and tail. These segmental structures originate from the mesoderm that lies as a long slab on either side of the embryonic midline. This slab becomes broken up into a regular repetitive series of separate blocks, or somites—cohesive groups of cells, separated by clefts (Figure 21–38A). The somites form (as bilateral pairs) one after another, in a regular rhythm, starting in the region of the head and ending in the tail. Depending on the species, the final number of somites ranges from less than 40 (in a frog or a zebrafish) to more than 300 (in a snake).
The posterior, most immature part of the mesodermal slab, called the presomitic mesoderm, supplies the required cells: as the cells proliferate, this mesoderm of oscillation cycle of oscillation cycle tail moves back as new somites form
Figure 21–38 Somite formation in the chick embryo. (a) a chick embryo at 40 hours of incubation. (B) how the temporal oscillation of gene expression in the presomitic mesoderm becomes converted into a spatial alternating pattern of gene expression in the formed somites. In the posterior part of the presomitic mesoderm, each cell oscillates with a cycle time of 90 minutes. as cells mature and emerge from the presomitic region, their oscillation is gradually slowed down and finally brought to a halt, leaving them in a state that depends on the phase of the cycle they happen to be in at the critical moment. In this way, a temporal oscillation of gene expression traces out an alternating spatial pattern. (a, from Y.J. Jiang, L. Smithers and
J. Lewis, Curr. Biol. 8:r868–r871, 1998. With permission from elsevier.) retreats tailward, extending the embryo (Figure 21–38B). In the process, it deposits a trail of somites formed from cells that group together into blocks as they emerge from the anterior end of the presomitic region. The special character of the presomitic mesoderm is maintained by a combination of fibroblast growth factor (FGF) and Wnt signals, produced by a signaling center at the tail end of the embryo, and the range of these signals seems to define the length of the presomitic mesoderm. The somites emerge with clocklike timing, but what determines the rhythm of the process?
In the posterior part of the presomitic mesoderm, the expression of certain genes oscillates in time. Snapshots of gene expression taken by fixing embryos for analysis at different times in the oscillation cycle reveal what is happening, and the oscillations can now also be observed in time-lapse movies of embryos containing fluorescent reporters of individual oscillating genes. One new somite pair is formed in each oscillation cycle, and, in mutants where the oscillations fail to occur, somite segmentation is disrupted: the cells may still break up, belatedly, into separate clusters, but they do so in a haphazard, irregular way. The gene-expression oscillator controlling regular segmentation is called the segmentation clock. The length of one complete oscillation cycle depends on the species: it is 30 minutes in a zebrafish, 90 minutes in a chick, 120 minutes in a mouse.
As cells emerge from the presomitic mesoderm to form somites—in other words, as they escape from the influence of the FGF and Wnt signals—their oscillation stops. Some become arrested in one state, some in another, according to the phase of the oscillation cycle at the time they leave the presomitic region. In this way, the temporal oscillation of gene expression in the presomitic mesoderm leaves its trace in a spatially periodic pattern of gene expression in the maturing mesoderm; this in turn dictates how the tissue will break up into physically separate blocks, through effects on the pattern of cell–cell adhesion (see Figure 21–38B).