Abstract
The morphologies of individual bones are crucial for their functions within the skeleton, and vary markedly during evolution. Recent studies have begun to reveal the detailed molecular genetic pathways that underlie skeletal morphogenesis. On the other hand, understanding of the process of morphogenesis itself has not kept pace with the molecular work. We examined, through an extended period of development in zebrafish, how a prominent craniofacial bone, the opercle (Op), attains its adult morphology. Using high-resolution confocal imaging of the vitally stained Op in live larvae, we show that the bone initially appears as a simple linear spicule, or spur, with a characteristic position and orientation, and lined by osteoblasts that we visualize by transgenic labeling. The Op then undergoes a stereotyped sequence of shape transitions, most notably during the larval period occurring through three weeks postfertilization. New shapes arise, and the bone grows in size, as a consequence of anisotropic addition of new mineralized bone matrix along specific regions of the pre-existing bone surfaces. We find that two modes of matrix addition, spurs and veils, are primarily associated with change in shape, whereas a third mode, incremental banding, largely accounts for growth in size. Furthermore, morphometric analyses show that shape development and growth follow different trajectories, suggesting separate control of bone shape and size. New osteoblast arrangements are associated with new patterns of matrix outgrowth, and we propose that fine developmental regulation of osteoblast position is a critical determinant of the spatiotemporal pattern of morphogenesis.
Highlights
Learning how different bones acquire unique morphologies has fascinated biologists for decades
In such early larvae the Op usually has the form of a small linear ‘spur’ (Figure 1A), and at this stage we can recognize it only by its early time of formation and by its location, for neighboring craniofacial dermal bones arise as linear spurs, each characterized by a specific time of appearance, location, and orientation
The bone continues to change in form, such that within about another week, it looks in silhouette roughly like a duck with its beak pointing upward (Figure 1E)
Summary
Learning how different bones acquire unique morphologies has fascinated biologists for decades. The mesenchymal condensations from which skeletal elements arise have been singled out as being important for the patterning especially of chondral bones (i.e. bones developing out of a cartilage template (reviews: [1,2]). Strong evidence for such condensation-intrinsic patterning comes from experiments where these condensations were placed into organ cultures, and observed to make cartilages with shapes reminiscent of those developing in vivo [3,4]. A suite of epithelial-mesenchymal signaling interactions, with signals going in both directions, likely underlies shape patterning of any dermal bone, as is currently under active investigation in many laboratories, including our own
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