Cargando…

Patterning of morphogenetic anisotropy fields

Orientational order, encoded in anisotropic fields, plays an important role during the development of an organism. A striking example of this is the freshwater polyp Hydra, where topological defects in the muscle fiber orientation have been shown to localize to key features of the body plan. This bo...

Descripción completa

Detalles Bibliográficos
Autores principales: Wang, Zihang, Marchetti, M. Cristina, Brauns, Fridtjof
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10068776/
https://www.ncbi.nlm.nih.gov/pubmed/36947516
http://dx.doi.org/10.1073/pnas.2220167120
_version_ 1785018732970508288
author Wang, Zihang
Marchetti, M. Cristina
Brauns, Fridtjof
author_facet Wang, Zihang
Marchetti, M. Cristina
Brauns, Fridtjof
author_sort Wang, Zihang
collection PubMed
description Orientational order, encoded in anisotropic fields, plays an important role during the development of an organism. A striking example of this is the freshwater polyp Hydra, where topological defects in the muscle fiber orientation have been shown to localize to key features of the body plan. This body plan is organized by morphogen concentration gradients, raising the question how muscle fiber orientation, morphogen gradients and body shape interact. Here, we introduce a minimal model that couples nematic orientational order to the gradient of a morphogen field. We show that on a planar surface, alignment to a radial concentration gradient can induce unbinding of topological defects, as observed during budding and tentacle formation in Hydra, and stabilize aster/vortex-like defects, as observed at a Hydra’s mouth. On curved surfaces mimicking the morphologies of Hydra in various stages of development—from spheroid to adult—our model reproduces the experimentally observed reorganization of orientational order. Our results suggest how gradient alignment and curvature effects may work together to control orientational order during development and lay the foundations for future modeling efforts that will include the tissue mechanics that drive shape deformations.
format Online
Article
Text
id pubmed-10068776
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher National Academy of Sciences
record_format MEDLINE/PubMed
spelling pubmed-100687762023-09-22 Patterning of morphogenetic anisotropy fields Wang, Zihang Marchetti, M. Cristina Brauns, Fridtjof Proc Natl Acad Sci U S A Physical Sciences Orientational order, encoded in anisotropic fields, plays an important role during the development of an organism. A striking example of this is the freshwater polyp Hydra, where topological defects in the muscle fiber orientation have been shown to localize to key features of the body plan. This body plan is organized by morphogen concentration gradients, raising the question how muscle fiber orientation, morphogen gradients and body shape interact. Here, we introduce a minimal model that couples nematic orientational order to the gradient of a morphogen field. We show that on a planar surface, alignment to a radial concentration gradient can induce unbinding of topological defects, as observed during budding and tentacle formation in Hydra, and stabilize aster/vortex-like defects, as observed at a Hydra’s mouth. On curved surfaces mimicking the morphologies of Hydra in various stages of development—from spheroid to adult—our model reproduces the experimentally observed reorganization of orientational order. Our results suggest how gradient alignment and curvature effects may work together to control orientational order during development and lay the foundations for future modeling efforts that will include the tissue mechanics that drive shape deformations. National Academy of Sciences 2023-03-22 2023-03-28 /pmc/articles/PMC10068776/ /pubmed/36947516 http://dx.doi.org/10.1073/pnas.2220167120 Text en Copyright © 2023 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Physical Sciences
Wang, Zihang
Marchetti, M. Cristina
Brauns, Fridtjof
Patterning of morphogenetic anisotropy fields
title Patterning of morphogenetic anisotropy fields
title_full Patterning of morphogenetic anisotropy fields
title_fullStr Patterning of morphogenetic anisotropy fields
title_full_unstemmed Patterning of morphogenetic anisotropy fields
title_short Patterning of morphogenetic anisotropy fields
title_sort patterning of morphogenetic anisotropy fields
topic Physical Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10068776/
https://www.ncbi.nlm.nih.gov/pubmed/36947516
http://dx.doi.org/10.1073/pnas.2220167120
work_keys_str_mv AT wangzihang patterningofmorphogeneticanisotropyfields
AT marchettimcristina patterningofmorphogeneticanisotropyfields
AT braunsfridtjof patterningofmorphogeneticanisotropyfields