Canalized Morphogenesis Driven by Inherited Tissue Asymmetries in Hydra Regeneration

Abstract

The emergence and stabilization of a body axis is a major step in animal morphogenesis, determining the symmetry of the body plan as well as its polarity. To advance our understanding of the emergence of body axis polarity, we study regenerating Hydra. Axis polarity is strongly memorized in Hydra regeneration even in small tissue segments. What type of processes confer this memory? To gain insight into the emerging polarity, we utilize frustrating initial conditions by studying regenerating tissue strips which fold into hollow spheroids by adhering their distal ends of opposite original polarities. Despite the convoluted folding process and the tissue rearrangements during regeneration, these tissue strips develop in a reproducible manner, preserving the original polarity and yielding an ordered body plan. These observations suggest that the integration of mechanical and biochemical processes supported by their mutual feedback attracts the tissue dynamics towards a well-defined developmental trajectory biased by weak inherited cues from the parent animal. Hydra thus provide an example of dynamic canalization in which the dynamic rules are instilled, but, in contrast to the classical picture, the detailed developmental trajectory does not unfold in a programmatic manner.

Plasticity of body axis polarity in Hydra regeneration under constraints

“…S5 , Movie 8 ) or in regenerating tissue fragments 38 . This is also compatible with our recent experiments on tissue strips 39 , showing the emergence of an aster-like defect following the folding of the tissue segment into a hollow spheroid and the emergence of an organizer at the same site without the existence of an explicit preexisting local signaling source.…”

“…The observed bias favoring organizer formation at aster-like defect sites in regenerating ring doublets, is well-aligned with recent results by us and others, that identified the aster-like defects (i.e. + 1 nematic topological defects) as organization centers for head formation in regenerating Hydra tissue pieces 38 , 39 and mouth formation in regenerating jellyfish 40 . The inherent structure of these defects as focal points of multiple contractile actin fibers implies that these sites are mechanically unique 38 .…”

“…Rather than seeking a specific molecular precursor or a well-defined causal trajectory for head regeneration, we claim that the formation of a new head organizer arises from a multi-faceted integration of diverse contributions that can proceed along different developmental paths. Furthermore, while the current views of polarity emphasize diffusible biochemical signals as the main carriers of polarity information, we suggest that additional factors such as mechanical processes can contribute to the establishment of a polar body axis 38 , 39 , 41 . More broadly, we believe that such an integrated framework that takes into account the symbiotic interactions between the different mechanical and biochemical factors will be essential for deciphering the mechanisms responsible for polarity determination in animal morphogenesis.…”

“…This defect is shown to emerge via different routes, either appearing at the onset of the regeneration process as the tissue heals at the edge of the ring doublet, or developing later (accompanied by a protrusion) at the fusion site. The role of the defect in head formation remains unclear, yet recent results by us 38 , 39 and others 40 suggest that the presence of a defect may provide local mechanical cues that can reinforce the formation of the head organizer at the defect site.…”

Hydramorphogenesis as phase-transition dynamics

“…It remains for future work to understand the detailed mechanisms leading to the feedback between curvature and the Ca 2+ activity as well as the details of how this activity is reflected in the distribution of the internal active actomyosin forces. Finally, the body-axis alignment, dictated by the longitudinal supracellular actin fibers, and the axis polarity which determines the position of the head in the regenerating tissue segment, are both strongly inherited from the parent Hydra 7,20,[49][50][51][52][53] . An important open issue is the effects of these symmetry-breaking fields on morphogenesis.…”