Electric-Induced Reversal of Morphogenesis in Hydra

Morphogenesis involves the dynamic interplay of biochemical, mechanical, and electrical processes. Here, we ask to what extent can the course of morphogenesis be modulated and controlled by an external electric field? We show that at a critical amplitude, an external electric field can halt morphogenesis in Hydra regeneration. Moreover, above this critical amplitude, the electric field can lead to reversal dynamics: a fully developed Hydra folds back into its incipient spheroid morphology. The potential to renew morphogenesis is reexposed when the field is reduced back to amplitudes below criticality. These dynamics are accompanied by modulations of the Wnt3 activity, a central component of the head organizer in Hydra. The controlled backward-forward cycle of morphogenesis can be repeated several times, showing that the reversal trajectory maintains the integrity of the tissue and its regeneration capability. Each cycle of morphogenesis leads to a newly emerged body plan in the redeveloped folded tissue, which is not necessarily similar to the one before the reversal process. Reversal of morphogenesis is shown to be triggered by enhanced electrical excitations in the Hydra tissue, leading to intensified calcium activity. Folding back of the body-plan morphology together with the decay of a central biosignaling system, indicate that electrical processes are tightly integrated with biochemical and mechanical-structural processes in morphogenesis and play an instructive role to a level that can direct developmental trajectories. Reversal of morphogenesis by external fields calls for extending its framework beyond program-like, forward-driven, hierarchical processes based on reaction diffusion and positional information.