A computational framework for 3D mechanical modeling of plant morphogenesis with cellular resolution
The link between genetic regulation and the definition of form and size during morphogenesis remains largely an open question in both plant and animal biology. This is partially due to the complexity of the process, involving extensive molecular networks, multiple feedbacks between different scales of organization and physical forces operating at multiple levels. Here we present a conceptual and modeling framework aimed at generating an integrated understanding of morphogenesis in plants. This framework is based on the biophysical properties of plant cells, which are under high internal turgor pressure, and are prevented from bursting because of the presence of a rigid cell wall. To control cell growth, the underlying molecular networks must interfere locally with the elastic and/or plastic extensibility of this cell wall. We present a model in the form of a three dimensional (3D) virtual tissue, where growth depends on the local modulation of wall mechanical properties and turgor pressure. The model shows how forces generated by turgor-pressure can act both cell autonomously and non-cell autonomously to drive growth in different directions. We use simulations to explore lateral organ formation at the shoot apical meristem. Although different scenarios lead to similar shape changes, they are not equivalent and lead to different, testable predictions regarding the mechanical and geometrical properties of the growing lateral organs. Using flower development as an example, we further show how a limited number of gene activities can explain the complex shape changes that accompany organ outgrowth.
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Subjects: | U10 - Informatique, mathématiques et statistiques, F62 - Physiologie végétale - Croissance et développement, F50 - Anatomie et morphologie des plantes, morphogénèse, propriété mécanique, modèle de simulation, paroi cellulaire, http://aims.fao.org/aos/agrovoc/c_4943, http://aims.fao.org/aos/agrovoc/c_4683, http://aims.fao.org/aos/agrovoc/c_24242, http://aims.fao.org/aos/agrovoc/c_1415, |
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dig-cirad-fr-5748122024-04-24T11:31:18Z http://agritrop.cirad.fr/574812/ http://agritrop.cirad.fr/574812/ A computational framework for 3D mechanical modeling of plant morphogenesis with cellular resolution. Boudon Frédéric, Chopard Jérôme, Ali Olivier, Gilles Benjamin, Hamant Olivier, Boudaoud Arezki, Traas Jan, Godin Christophe. 2015. PLoS Computational Biology, 11 (1):e1003950, 16 p.https://doi.org/10.1371/journal.pcbi.1003950 <https://doi.org/10.1371/journal.pcbi.1003950> A computational framework for 3D mechanical modeling of plant morphogenesis with cellular resolution Boudon, Frédéric Chopard, Jérôme Ali, Olivier Gilles, Benjamin Hamant, Olivier Boudaoud, Arezki Traas, Jan Godin, Christophe eng 2015 PLoS Computational Biology U10 - Informatique, mathématiques et statistiques F62 - Physiologie végétale - Croissance et développement F50 - Anatomie et morphologie des plantes morphogénèse propriété mécanique modèle de simulation paroi cellulaire http://aims.fao.org/aos/agrovoc/c_4943 http://aims.fao.org/aos/agrovoc/c_4683 http://aims.fao.org/aos/agrovoc/c_24242 http://aims.fao.org/aos/agrovoc/c_1415 The link between genetic regulation and the definition of form and size during morphogenesis remains largely an open question in both plant and animal biology. This is partially due to the complexity of the process, involving extensive molecular networks, multiple feedbacks between different scales of organization and physical forces operating at multiple levels. Here we present a conceptual and modeling framework aimed at generating an integrated understanding of morphogenesis in plants. This framework is based on the biophysical properties of plant cells, which are under high internal turgor pressure, and are prevented from bursting because of the presence of a rigid cell wall. To control cell growth, the underlying molecular networks must interfere locally with the elastic and/or plastic extensibility of this cell wall. We present a model in the form of a three dimensional (3D) virtual tissue, where growth depends on the local modulation of wall mechanical properties and turgor pressure. The model shows how forces generated by turgor-pressure can act both cell autonomously and non-cell autonomously to drive growth in different directions. We use simulations to explore lateral organ formation at the shoot apical meristem. Although different scenarios lead to similar shape changes, they are not equivalent and lead to different, testable predictions regarding the mechanical and geometrical properties of the growing lateral organs. Using flower development as an example, we further show how a limited number of gene activities can explain the complex shape changes that accompany organ outgrowth. article info:eu-repo/semantics/article Journal Article info:eu-repo/semantics/publishedVersion http://agritrop.cirad.fr/574812/1/document_574812.pdf application/pdf Cirad license info:eu-repo/semantics/openAccess https://agritrop.cirad.fr/mention_legale.html https://doi.org/10.1371/journal.pcbi.1003950 10.1371/journal.pcbi.1003950 info:eu-repo/semantics/altIdentifier/doi/10.1371/journal.pcbi.1003950 info:eu-repo/semantics/altIdentifier/purl/https://doi.org/10.1371/journal.pcbi.1003950 info:eu-repo/semantics/reference/purl/https://gforge.inria.fr/frs/download.php/file/33843/sofatissue.tgz. |
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U10 - Informatique, mathématiques et statistiques F62 - Physiologie végétale - Croissance et développement F50 - Anatomie et morphologie des plantes morphogénèse propriété mécanique modèle de simulation paroi cellulaire http://aims.fao.org/aos/agrovoc/c_4943 http://aims.fao.org/aos/agrovoc/c_4683 http://aims.fao.org/aos/agrovoc/c_24242 http://aims.fao.org/aos/agrovoc/c_1415 U10 - Informatique, mathématiques et statistiques F62 - Physiologie végétale - Croissance et développement F50 - Anatomie et morphologie des plantes morphogénèse propriété mécanique modèle de simulation paroi cellulaire http://aims.fao.org/aos/agrovoc/c_4943 http://aims.fao.org/aos/agrovoc/c_4683 http://aims.fao.org/aos/agrovoc/c_24242 http://aims.fao.org/aos/agrovoc/c_1415 |
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U10 - Informatique, mathématiques et statistiques F62 - Physiologie végétale - Croissance et développement F50 - Anatomie et morphologie des plantes morphogénèse propriété mécanique modèle de simulation paroi cellulaire http://aims.fao.org/aos/agrovoc/c_4943 http://aims.fao.org/aos/agrovoc/c_4683 http://aims.fao.org/aos/agrovoc/c_24242 http://aims.fao.org/aos/agrovoc/c_1415 U10 - Informatique, mathématiques et statistiques F62 - Physiologie végétale - Croissance et développement F50 - Anatomie et morphologie des plantes morphogénèse propriété mécanique modèle de simulation paroi cellulaire http://aims.fao.org/aos/agrovoc/c_4943 http://aims.fao.org/aos/agrovoc/c_4683 http://aims.fao.org/aos/agrovoc/c_24242 http://aims.fao.org/aos/agrovoc/c_1415 Boudon, Frédéric Chopard, Jérôme Ali, Olivier Gilles, Benjamin Hamant, Olivier Boudaoud, Arezki Traas, Jan Godin, Christophe A computational framework for 3D mechanical modeling of plant morphogenesis with cellular resolution |
description |
The link between genetic regulation and the definition of form and size during morphogenesis remains largely an open question in both plant and animal biology. This is partially due to the complexity of the process, involving extensive molecular networks, multiple feedbacks between different scales of organization and physical forces operating at multiple levels. Here we present a conceptual and modeling framework aimed at generating an integrated understanding of morphogenesis in plants. This framework is based on the biophysical properties of plant cells, which are under high internal turgor pressure, and are prevented from bursting because of the presence of a rigid cell wall. To control cell growth, the underlying molecular networks must interfere locally with the elastic and/or plastic extensibility of this cell wall. We present a model in the form of a three dimensional (3D) virtual tissue, where growth depends on the local modulation of wall mechanical properties and turgor pressure. The model shows how forces generated by turgor-pressure can act both cell autonomously and non-cell autonomously to drive growth in different directions. We use simulations to explore lateral organ formation at the shoot apical meristem. Although different scenarios lead to similar shape changes, they are not equivalent and lead to different, testable predictions regarding the mechanical and geometrical properties of the growing lateral organs. Using flower development as an example, we further show how a limited number of gene activities can explain the complex shape changes that accompany organ outgrowth. |
format |
article |
topic_facet |
U10 - Informatique, mathématiques et statistiques F62 - Physiologie végétale - Croissance et développement F50 - Anatomie et morphologie des plantes morphogénèse propriété mécanique modèle de simulation paroi cellulaire http://aims.fao.org/aos/agrovoc/c_4943 http://aims.fao.org/aos/agrovoc/c_4683 http://aims.fao.org/aos/agrovoc/c_24242 http://aims.fao.org/aos/agrovoc/c_1415 |
author |
Boudon, Frédéric Chopard, Jérôme Ali, Olivier Gilles, Benjamin Hamant, Olivier Boudaoud, Arezki Traas, Jan Godin, Christophe |
author_facet |
Boudon, Frédéric Chopard, Jérôme Ali, Olivier Gilles, Benjamin Hamant, Olivier Boudaoud, Arezki Traas, Jan Godin, Christophe |
author_sort |
Boudon, Frédéric |
title |
A computational framework for 3D mechanical modeling of plant morphogenesis with cellular resolution |
title_short |
A computational framework for 3D mechanical modeling of plant morphogenesis with cellular resolution |
title_full |
A computational framework for 3D mechanical modeling of plant morphogenesis with cellular resolution |
title_fullStr |
A computational framework for 3D mechanical modeling of plant morphogenesis with cellular resolution |
title_full_unstemmed |
A computational framework for 3D mechanical modeling of plant morphogenesis with cellular resolution |
title_sort |
computational framework for 3d mechanical modeling of plant morphogenesis with cellular resolution |
url |
http://agritrop.cirad.fr/574812/ http://agritrop.cirad.fr/574812/1/document_574812.pdf |
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