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Mechanical forces as information: an integrated approach to plant and animal development

Mechanical forces such as tension and compression act throughout growth and development of multicellular organisms. These forces not only affect the size and shape of the cells and tissues but are capable of modifying the expression of genes and the localization of molecular components within the ce...

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Autores principales: Hernández-Hernández, Valeria, Rueda, Denisse, Caballero, Lorena, Alvarez-Buylla, Elena R., Benítez, Mariana
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4051191/
https://www.ncbi.nlm.nih.gov/pubmed/24959170
http://dx.doi.org/10.3389/fpls.2014.00265
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author Hernández-Hernández, Valeria
Rueda, Denisse
Caballero, Lorena
Alvarez-Buylla, Elena R.
Benítez, Mariana
author_facet Hernández-Hernández, Valeria
Rueda, Denisse
Caballero, Lorena
Alvarez-Buylla, Elena R.
Benítez, Mariana
author_sort Hernández-Hernández, Valeria
collection PubMed
description Mechanical forces such as tension and compression act throughout growth and development of multicellular organisms. These forces not only affect the size and shape of the cells and tissues but are capable of modifying the expression of genes and the localization of molecular components within the cell, in the plasma membrane, and in the plant cell wall. The magnitude and direction of these physical forces change with cellular and tissue properties such as elasticity. Thus, mechanical forces and the mesoscopic fields that emerge from their local action constitute important sources of positional information. Moreover, physical and biochemical processes interact in non-linear ways during tissue and organ growth in plants and animals. In this review we discuss how such mechanical forces are generated, transmitted, and sensed in these two lineages of multicellular organisms to yield long-range positional information. In order to do so we first outline a potentially common basis for studying patterning and mechanosensing that relies on the structural principle of tensegrity, and discuss how tensegral structures might arise in plants and animals. We then provide some examples of morphogenesis in which mechanical forces appear to act as positional information during development, offering a possible explanation for ubiquitous processes, such as the formation of periodic structures. Such examples, we argue, can be interpreted in terms of tensegral phenomena. Finally, we discuss the hypothesis of mechanically isotropic points as a potentially generic mechanism for the localization and maintenance of stem-cell niches in multicellular organisms. This comparative approach aims to help uncovering generic mechanisms of morphogenesis and thus reach a better understanding of the evolution and development of multicellular phenotypes, focusing on the role of physical forces in these processes.
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spelling pubmed-40511912014-06-23 Mechanical forces as information: an integrated approach to plant and animal development Hernández-Hernández, Valeria Rueda, Denisse Caballero, Lorena Alvarez-Buylla, Elena R. Benítez, Mariana Front Plant Sci Plant Science Mechanical forces such as tension and compression act throughout growth and development of multicellular organisms. These forces not only affect the size and shape of the cells and tissues but are capable of modifying the expression of genes and the localization of molecular components within the cell, in the plasma membrane, and in the plant cell wall. The magnitude and direction of these physical forces change with cellular and tissue properties such as elasticity. Thus, mechanical forces and the mesoscopic fields that emerge from their local action constitute important sources of positional information. Moreover, physical and biochemical processes interact in non-linear ways during tissue and organ growth in plants and animals. In this review we discuss how such mechanical forces are generated, transmitted, and sensed in these two lineages of multicellular organisms to yield long-range positional information. In order to do so we first outline a potentially common basis for studying patterning and mechanosensing that relies on the structural principle of tensegrity, and discuss how tensegral structures might arise in plants and animals. We then provide some examples of morphogenesis in which mechanical forces appear to act as positional information during development, offering a possible explanation for ubiquitous processes, such as the formation of periodic structures. Such examples, we argue, can be interpreted in terms of tensegral phenomena. Finally, we discuss the hypothesis of mechanically isotropic points as a potentially generic mechanism for the localization and maintenance of stem-cell niches in multicellular organisms. This comparative approach aims to help uncovering generic mechanisms of morphogenesis and thus reach a better understanding of the evolution and development of multicellular phenotypes, focusing on the role of physical forces in these processes. Frontiers Media S.A. 2014-06-10 /pmc/articles/PMC4051191/ /pubmed/24959170 http://dx.doi.org/10.3389/fpls.2014.00265 Text en Copyright © 2014 Hernández-Hernández, Rueda, Caballero, Alvarez-Buylla and Benítez. http://creativecommons.org/licenses/by/3.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Hernández-Hernández, Valeria
Rueda, Denisse
Caballero, Lorena
Alvarez-Buylla, Elena R.
Benítez, Mariana
Mechanical forces as information: an integrated approach to plant and animal development
title Mechanical forces as information: an integrated approach to plant and animal development
title_full Mechanical forces as information: an integrated approach to plant and animal development
title_fullStr Mechanical forces as information: an integrated approach to plant and animal development
title_full_unstemmed Mechanical forces as information: an integrated approach to plant and animal development
title_short Mechanical forces as information: an integrated approach to plant and animal development
title_sort mechanical forces as information: an integrated approach to plant and animal development
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4051191/
https://www.ncbi.nlm.nih.gov/pubmed/24959170
http://dx.doi.org/10.3389/fpls.2014.00265
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