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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...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Frontiers Media S.A.
2014
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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. |
format | Online Article Text |
id | pubmed-4051191 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2014 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
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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