Abstract
The vertebrates are defined by their segmented vertebral column, and vertebral periodicity is thought to originate from embryonic segments, the somites. According to the widely accepted 'resegmentation' model, a single vertebra forms from the recombination of the anterior and posterior halves of two adjacent sclerotomes on both sides of the embryo. Although there is supporting evidence for this model in amniotes, it remains uncertain whether it applies to all vertebrates. To explore this, we have investigated vertebral patterning in the zebrafish. Surprisingly, we find that vertebral bodies (centra) arise by secretion of bone matrix from the notochord rather than somites; centra do not form via a cartilage intermediate stage, nor do they contain osteoblasts. Moreover, isolated, cultured notochords secrete bone matrix in vitro, and ablation of notochord cells at segmentally reiterated positions in vivo prevents the formation of centra. Analysis of fss mutant embryos, in which sclerotome segmentation is disrupted, shows that whereas neural arch segmentation is also disrupted, centrum development proceeds normally. These findings suggest that the notochord plays a key, perhaps ancient, role in the segmental patterning of vertebrae.
Highlights
The segmented vertebral column is the defining feature of the vertebrates, and is composed of an alternating pattern of bony vertebral bodies and intervertebral discs
We have undertaken a study of zebrafish vertebral patterning, and our results suggest that the notochord plays a central role in segmental patterning
Because a cartilage intermediate is not observed at any stage, bony centra in zebrafish do not develop by endochondral ossification, which is in marked contrast to amniotes (Dockter, 2000)
Summary
The segmented vertebral column is the defining feature of the vertebrates, and is composed of an alternating pattern of bony vertebral bodies (centra) and intervertebral discs. Sonic hedgehog (Shh) signalling (Fan et al, 1995; Fan and Tessier-Lavigne, 1994) and several transcription factors, including members of the Pax and Sox families (Akiyama et al, 2002; Balling et al, 1996; Smits and Lefebvre, 2003) and Bapx (Lettice et al, 1999; Tribioli and Lufkin, 1999), have been found to be required for sclerotome differentiation and proliferation (for a review, see Christ et al, 2000) Despite these insights at the molecular level, the relationship between somite patterning and vertebral segmentation remains to be firmly established. This has been termed ‘leaky’ resegmentation, and is consistent with a similar finding made in a previous study using the chick embryo (Stern and Keynes, 1987)
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