Abstract
A Turing mechanism implemented by BMP, SOX9 and WNT has been proposed to control mouse digit patterning. However, its generality and contribution to the morphological diversity of fins and limbs has not been explored. Here we provide evidence that the skeletal patterning of the catshark Scyliorhinus canicula pectoral fin is likely driven by a deeply conserved Bmp–Sox9–Wnt Turing network. In catshark fins, the distal nodular elements arise from a periodic spot pattern of Sox9 expression, in contrast to the stripe pattern in mouse digit patterning. However, our computer model shows that the Bmp–Sox9–Wnt network with altered spatial modulation can explain the Sox9 expression in catshark fins. Finally, experimental perturbation of Bmp or Wnt signalling in catshark embryos produces skeletal alterations which match in silico predictions. Together, our results suggest that the broad morphological diversity of the distal fin and limb elements arose from the spatial re-organization of a deeply conserved Turing mechanism.
Highlights
A Turing mechanism implemented by BMP, SOX9 and WNT has been proposed to control mouse digit patterning
We focus on the pectoral fin development of the catshark, Scyliorhinus canicula for two reasons: (a) its fin skeletal elements are formed by individual condensations[17], which are similar to the condensation process of tetrapod limbs; and (b) its genome is less derived than that of teleost genomes[18]
Our results suggest that the broad morphological diversity of the distal fin and limb elements arose from the spatial re-organization of a deeply conserved Turing mechanism
Summary
A Turing mechanism implemented by BMP, SOX9 and WNT has been proposed to control mouse digit patterning. We provide evidence that the skeletal patterning of the catshark Scyliorhinus canicula pectoral fin is likely driven by a deeply conserved Bmp–Sox9–Wnt Turing network. The distal nodular elements arise from a periodic spot pattern of Sox[9] expression, in contrast to the stripe pattern in mouse digit patterning. The digit-specific regulatory sequence of the murine Hoxa and d genes has recently been found in the genomes of the skate and the spotted gar, where they drive similar expression in the distal fin/limb bud[6,10]. It has been proposed that regulatory interactions between BMP, SOX9 and WNT form a Turing network that creates a periodic molecular pre-pattern specifying the positions of the digits (the BSW model)[12]. We focused our study on control of this spot pattern (rather than subsequent expression of Sox[9] proximally or distally) for two reasons: firstly, we are interested in the initial symmetry-breaking process responsible for the overall radial arrangement, and secondly because previous studies suggest that the mechanism of patterning the distal periodic elements shows molecular differences from those controlling more proximal elements[12,20]
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