Abstract
The vertebrate body is made by progressive addition of new tissue from progenitors at the posterior embryonic end. Axial extension involves different mechanisms that produce internal organs in the trunk but not in the tail. We show that Gdf11 signaling is a major coordinator of the trunk-to-tail transition. Without Gdf11 signaling, the switch from trunk to tail is significantly delayed, and its premature activation brings the hindlimbs and cloaca next to the forelimbs, leaving extremely short trunks. Gdf11 activity includes activation of Isl1 to promote formation of the hindlimbs and cloaca-associated mesoderm as the most posterior derivatives of lateral mesoderm progenitors. Gdf11 also coordinates reallocation of bipotent neuromesodermal progenitors from the anterior primitive streak to the tail bud, in part by reducing the retinoic acid available to the progenitors. Our findings provide a perspective to understand the evolution of the vertebrate body plan.
Highlights
Vertebrates display a large diversity of body shapes and sizes
Loss of Gdf11 Delays Trunk-to-Tail Transition in Mice Gdf11 mutant newborn animals present anterior homeotic transformations along the axial skeleton, with posterior displacement of the hindlimbs by six to eight vertebrae (McPherron et al, 1999). Analysis of these mutants at embryonic day (E)11.5 revealed that the hindlimb buds were more posteriorly located, producing an increased interlimb region by five or six somites when compared to wild-type embryos (Figures 1A and 1B)
Gdf11 mutant hindlimbs were visibly smaller than those of their wild-type littermates (Figures 1A and 1B), which contrasted with their normal morphology at E18.5 (Figures S1A and S1B available online)
Summary
Vertebrates display a large diversity of body shapes and sizes Despite such morphological variations, their primary body axis is always generated from head to tail through a similar principle, consisting of the progressive addition of new tissue at the posterior end of the embryo (reviewed in Stern et al, 2006; Wilson et al, 2009). Their primary body axis is always generated from head to tail through a similar principle, consisting of the progressive addition of new tissue at the posterior end of the embryo (reviewed in Stern et al, 2006; Wilson et al, 2009) This process requires a fine balance between the maintenance of progenitor pools and the continuous production of cells that form the different body structures. Elucidating the mechanisms that control this regional organization is essential to understand the evolution of the vertebrate body plan
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