Anterior-posterior differences in vertebrate segments: specification of trunk and tail somites in the zebrafish blastula.

During vertebrate embryogenesis, the primary body axis grows posteriorly and is concomitantly segmented into somites, the precursors of the vertebral column, skeletal muscle, and dermis. The somites arise sequentially, with the anterior somites that give rise to the cervical vertebrae created early. The more posterior somites that become the thoracic, lumbar, and sacral vertebrae form at progressively later times. During the axis elongation period, the embryo must parse the somite precursors appropriately so that there are enough cells remaining to make the most posterior somites at the end of somitogenesis. How the embryo allocates these cells is not well understood. However, in this issue, Szeto and Kimelman (2006) address this question by showing that cells are specified to give rise to anterior trunk, posterior trunk, and tail somites. They find that this cell fate decision occurs surprisingly early in zebrafish development, prior to gastrulation, in response to nodal, fgf, and bmp signaling (Fig. 1; Szeto and Kimelman 2006). Their data link the processes of mesoderm induction and patterning with vertebrate segmentation and elucidate a mechanism by which the embryo reserves a somite precursor population for the formation of the more posterior body segments. While the number of vertebrae varies greatly among different species (Richardson et al. 1998), somite number within a given species is remarkably consistent. The question arises, how does the embryo determine the appropriate somite number and size while the field of cells to be segmented continues to grow posteriorly? Experimentally manipulated Xenopus embryos, with large portions of the blastula physically removed, develop into embryos two-thirds smaller than normal, yet form the same number of segments and at the same rate as unmanipulated sibling embryos. Thus, the embryo “knows” the species-specific number of somites that it needs to generate and divides the available cell population accordingly; that is, there does not appear to be a physical constraint defining the number of cells in a given segment. In these smaller embryos, each segment consists of fewer cells than the somites of their normal-sized siblings (Cooke 1975). Furthermore, knypek; trilobite double mutants, which are much shorter than a wild-type zebrafish embryo due to a severe convergence extension defect, form somites only two cells in length, while zebrafish somites are normally five cells in length (Henry et al. 2000). Consideration of the regulative capacity of vertebrate segmentation led to the proposal that somitogenesis is controlled by a “clock and wavefront” whereby the clock represents a mechanism that causes the somite precursors to oscillate. Cells would only be able to form a segment during a brief period within each cycle of the somite clock. The wavefront represents the progression of tissue maturation and cell differentiation that sweeps head-to-tail along the primary axis of the embryo (Cooke and Zeeman 1975; Cooke 1998). In this model, a somite forms when the wavefront encounters a group of cells in the correct, permissive phase of the clock. Thus, somite length and rate of formation are dependent on the frequency of the clock/oscillator and the velocity of the wavefront. The regulative capacity of this mechanism allows the embryo to parse cells into segments at a rate that would retain enough cells to populate the most posterior somites. During the past 10 years, molecular evidence for both a clock and a wavefront has emerged (Pourquié 2003; Rida et al. 2004). However, Szeto and Kimelman (2006) find an additional mechanism by which the zebrafish embryo parses its supply of somite progenitors. They find that the anlagen of the anterior trunk, posterior trunk, and tail somites are specified before gastrulation, 5, 13.5, and 16.5 h before the onset of segmentation of each anlagen, respectively.