Calcium fluctuations drive morphological patterning at the onset of Hydra morphogenesis

TL;DR

This study reveals that calcium fluctuations act as a key integrator in Hydra morphogenesis, with external electric fields modulating these fluctuations and influencing the developmental transition from spheroid to elongated body shape.

Contribution

It demonstrates that calcium spatial fluctuations are crucial in morphogenesis and introduces a method to control development using external electric fields, revealing a phase transition-like behavior.

Findings

Calcium fluctuations increase during halted morphogenesis under electric fields.

Normalized calcium fluctuation distributions are universal across samples.

Morphogenesis resembles a dynamical phase transition.

Abstract

Morphogenesis in animal development involves significant morphological transitions leading to the emerging body plan of a mature animal. Understanding how the collective physical processes drive robust morphological patterning requires a coarse-grained description of the dynamics and the characterization of the underlying fields. Here I show that calcium spatial fluctuations serve as an integrator field of the electrical-mechanical processes of morphogenesis in whole-body Hydra regeneration and drive the morphological dynamics. We utilize external electric fields to control the developmental process and study a critical transition in morphogenesis, from the initial spheroidal shape of the tissue to an elongated cylindrical shape defining the body plan of a mature animal. Morphogenesis paused under external voltage is associated with a significant increase of the calcium activity compared with the activity supporting normal development. The enhanced calcium activity is characterized by intensified spatial fluctuations, extended spatial correlations across the tissue and faster temporal fluctuations. In contrast, the normal morphogenesis process is characterized by relatively moderate calcium fluctuation activity and restrained spatial correlations. Our methodology of controlling morphogenesis by a physical electric field allows us to gain a global statistical view of the dynamics. It shows that the normalized calcium spatial fluctuations exhibit a universal shape distribution, across tissue samples and conditions, suggesting the existence of a global constrain over these fluctuations. Studying the correlations in space and time of the calcium fluctuation field at the onset of morphogenesis opens a new vista on this process and paints a picture of development analogous to a dynamical phase transition.