Muscular hydraulics drive larva-polyp morphogenesis

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

doi:10.1016/j.cub.2022.08.065

Muscular hydraulics drive larva-polyp morphogenesis

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

Hubrecht Institute

Onderzoeksoutput: Bijdrage aan wetenschappelijk tijdschrift/periodieke uitgave › Artikel › Wetenschappelijk › peer review

3 Citaten (Scopus)

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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.

Originele taal-2	Engels
Pagina's (van-tot)	4707-4718.e8
Tijdschrift	Current Biology
Volume	32
Nummer van het tijdschrift	21
DOI's	https://doi.org/10.1016/j.cub.2022.08.065
Status	Gepubliceerd - 07 nov. 2022

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10.1016/j.cub.2022.08.065

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title = "Muscular hydraulics drive larva-polyp morphogenesis",

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.",

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author = "Anniek Stokkermans and Aditi Chakrabarti and Kaushikaram Subramanian and Ling Wang and Sifan Yin and Prachiti Moghe and Petrus Steenbergen and Gregor M{\"o}nke and Takashi Hiiragi and Robert Prevedel and L Mahadevan and Aissam Ikmi",

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doi = "10.1016/j.cub.2022.08.065",

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AU - Stokkermans, Anniek

AU - Chakrabarti, Aditi

AU - Subramanian, Kaushikaram

AU - Wang, Ling

AU - Yin, Sifan

AU - Moghe, Prachiti

AU - Steenbergen, Petrus

AU - Mönke, Gregor

AU - Hiiragi, Takashi

AU - Prevedel, Robert

AU - Mahadevan, L

AU - Ikmi, Aissam

PY - 2022/11/7

Y1 - 2022/11/7

N2 - 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.

AB - 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.

KW - Animals

KW - Larva

KW - Morphogenesis

KW - Sea Anemones

U2 - 10.1016/j.cub.2022.08.065

DO - 10.1016/j.cub.2022.08.065

M3 - Article

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VL - 32

SP - 4707-4718.e8

JO - Current Biology

JF - Current Biology

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Muscular hydraulics drive larva-polyp morphogenesis

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