Topological defects in the nematic order of actin fibres as organization centres of Hydra regeneration

Morphogenesis is a process in which a well-defined pattern of functional tissues emerges during the development. One of the great challenges in morphogenesis research is understanding the organizational principles responsible for the robust convergence of the process, across scales, to form viable organisms under variable conditions. Here we utilize the fresh water animal Hydra as a model system, focusing on the dynamics of the actin cytoskeleton during a regeneration process which is akin to development. We show that the nematic order of the supra-cellular actin fibres in regenerating Hydra defines a slowly-varying field, whose dynamics provide an effective description of the morphogenesis process. The nematic orientation field contains defects constrained by the topology of the regenerating tissue. These nematic topological defects are long-lived, yet display rich dynamics that can be related to the major morphological events during regeneration. In particular, we show that these defects act as organizing centres, with the main functional morphological features developing at defect sites. These results suggest a system of self-organization involving the actin cytoskeleton in the regenerating tissue that is based on mechanical feedback. We therefore view the nematic orientation field as a “mechanical morphogen”, whose interaction with other mechanical and biochemical morphogen fields leads to the robust development of the body plan of the regenerating Hydra.