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Current Biology

Publication date: 2022-11-07
Volume: 32 Pages: 4707 -
Publisher: Elsevier (Cell Press)

Author:

Stokkermans, Anniek
Chakrabarti, Aditi ; Subramanian, Kaushikaram ; Wang, Ling ; Yin, Sifan ; Moghe, Prachiti ; Steenbergen, Petrus ; Moenke, Gregor ; Hiiragi, Takashi ; Prevedel, Robert ; Mahadevan, L ; Ikmi, Aissam

Keywords:

ANEMONE NEMATOSTELLA-VECTENSIS, AXIS, Biochemistry & Molecular Biology, Biology, Cell Biology, DIFFERENTIATION, GENERATION, Life Sciences & Biomedicine, Life Sciences & Biomedicine - Other Topics, MECHANOTRANSDUCTION, METAMORPHOSIS, Science & Technology, SEA, SEGMENTATION, SETTLEMENT, TISSUE MORPHOGENESIS, behavior, cnidaria, contractility, hydraulics, morphogenesis, motility, muscles, pressure, Animals, Larva, Morphogenesis, Sea Anemones, 06 Biological Sciences, 11 Medical and Health Sciences, 17 Psychology and Cognitive Sciences, Developmental Biology, 31 Biological sciences, 32 Biomedical and clinical sciences, 52 Psychology

Abstract:

Development is a highly dynamic process in which organisms often experience changes in both form and behavior, which are typically coupled to each other. However, little is known about how organismal-scale behaviors such as body contractility and motility impact morphogenesis. Here, we use the cnidarian Nematostella vectensis as a developmental model to uncover a mechanistic link between organismal size, shape, and behavior. Using quantitative live imaging in a large population of developing animals, combined with molecular and biophysical experiments, we demonstrate that the muscular-hydraulic machinery that controls body movement also drives larva-polyp morphogenesis. We show that organismal size largely depends on cavity inflation through fluid uptake, whereas body shape is constrained by the organization of the muscular system. The generation of ethograms identifies different trajectories of size and shape development in sessile and motile animals, which display distinct patterns of body contractions. With a simple theoretical model, we conceptualize how pressures generated by muscular hydraulics can act as a global mechanical regulator that coordinates tissue remodeling. Altogether, our findings illustrate how organismal contractility and motility behaviors can influence morphogenesis.