Plasticity of body axis polarity in Hydra regeneration under constraints

One of the major events in animal morphogenesis is the emergence of a polar body axis. Here, we combine classic grafting techniques with live imaging to study the emergence of body axis polarity during whole body regeneration in Hydra. Composite tissues are made by fusing two rings, excised from separate animals, in different configurations that vary in the relative polarity and original position of the rings along the body axis of the parent animals. We find that under frustrating initial configurations, body axis polarity that is otherwise stably inherited from the parent animal, can become labile and even be reversed. The site of head regeneration exhibits a bias for the edges of the fused doublets, even when this involves polarity reversal in the tissue, emphasizing the importance of structural factors in head formation. The doublets edges invariably contain defects in the organization of the supra-cellular actin fibers, which form as the tissue ring seals on each side. We suggest that the presence of a defect can act as an "attractor" for head formation at the edge, even though a defect is neither required nor sufficient for head formation. The observation of head formation at an originally distal edge of the tissue upon polarity reversal, is not compatible with models of Hydra regeneration based solely on preexisting morphogen gradients. Rather, our results suggest that body axis determination is a dynamic process that involves mechanical feedback and signaling processes that are sensitive to the original polarity and position of the excised tissues. Significance statementThe formation of a polar body axis is one of the most basic steps in defining the body plan of a developing animal. Here we study the emergence of polarity in Hydra regenerating from composite tissue segments under constraints. We show that these frustrating conditions expose non-trivial dynamics, reflecting the integration of the memory of the tissues original polarity and position in the parent animal with dynamic biochemical and mechanical processes. In particular, we demonstrate that the organization of the cytoskeleton participates together with biochemical signaling processes in feedback loops that eventually result in the formation and stabilization of the animals body axis. We conclude that preexisting biochemical gradients in the tissue cannot by themselves explain axis determination.