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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Main Authors: Boudon, Frédéric, Chopard, Jérôme, Ali, Olivier, Gilles, Benjamin, Hamant, Olivier, Boudaoud, Arezki, Traas, Jan, Godin, Christophe
Format: article biblioteca
Language:eng
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,
Online Access:http://agritrop.cirad.fr/574812/
http://agritrop.cirad.fr/574812/1/document_574812.pdf
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spelling 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.
institution CIRAD FR
collection DSpace
country Francia
countrycode FR
component Bibliográfico
access En linea
databasecode dig-cirad-fr
tag biblioteca
region Europa del Oeste
libraryname Biblioteca del CIRAD Francia
language eng
topic 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
spellingShingle 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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