Limits...
A computational framework for 3D mechanical modeling of plant morphogenesis with cellular resolution.

Boudon F, Chopard J, Ali O, Gilles B, Hamant O, Boudaoud A, Traas J, Godin C - PLoS Comput. Biol. (2015)

Bottom Line: The model shows how forces generated by turgor-pressure can act both cell autonomously and non-cell autonomously to drive growth in different directions.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.

View Article: PubMed Central - PubMed

Affiliation: Virtual Plants Inria team, UMR AGAP, CIRAD, INRIA, INRA, Montpellier, France.

ABSTRACT
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.

Show MeSH

Related in: MedlinePlus

Schematic view of the regulation of growth in multicellular tissues.The different horizontal layers represent different levels of biological organization. The plain black arrows symbolize the downward stream of regulation between growth hormones and actual growth through transcription factors activation and physical quantities modulation. The red plain arrows depict the indirect, integrated relationships between transcription factor activation, physical quantities modulation and cell wall irreversible extension our computational framework attempts to grasp. Finally the black dashed upward arrows stand for possible feedback mechanisms from shape changes on the biochemical regulation of growth.
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4288716&req=5

pcbi-1003950-g001: Schematic view of the regulation of growth in multicellular tissues.The different horizontal layers represent different levels of biological organization. The plain black arrows symbolize the downward stream of regulation between growth hormones and actual growth through transcription factors activation and physical quantities modulation. The red plain arrows depict the indirect, integrated relationships between transcription factor activation, physical quantities modulation and cell wall irreversible extension our computational framework attempts to grasp. Finally the black dashed upward arrows stand for possible feedback mechanisms from shape changes on the biochemical regulation of growth.

Mentions: In a multicellular context, morphogenesis relies on differential growth across tissues. Each cell may feature specific values for the various parameters (turgor pressure, yielding threshold, extensibility…) used in Eq.(1). In principle, the regulation and coordination of these parameters is achieved through the action of the molecular regulatory networks that control the composition and mechanical properties of the cell wall, as described by the black arrows in Fig. 1. For example, cell wall modifying enzymes such as expansins, xyloglucan endo-tranglycosylases or pectin modifying enzymes are known to be triggered by transcription factors such as APETALA2 [9], MONOPTEROS [10] and AGAMOUS [11]. At the scale of the cell wall, actions of such enzymes have the potential to increase or decrease the viscosity and/or the rigidity of the wall. As a consequence, extensibility in Eq.(1) may be modified and affect growth.


A computational framework for 3D mechanical modeling of plant morphogenesis with cellular resolution.

Boudon F, Chopard J, Ali O, Gilles B, Hamant O, Boudaoud A, Traas J, Godin C - PLoS Comput. Biol. (2015)

Schematic view of the regulation of growth in multicellular tissues.The different horizontal layers represent different levels of biological organization. The plain black arrows symbolize the downward stream of regulation between growth hormones and actual growth through transcription factors activation and physical quantities modulation. The red plain arrows depict the indirect, integrated relationships between transcription factor activation, physical quantities modulation and cell wall irreversible extension our computational framework attempts to grasp. Finally the black dashed upward arrows stand for possible feedback mechanisms from shape changes on the biochemical regulation of growth.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4288716&req=5

pcbi-1003950-g001: Schematic view of the regulation of growth in multicellular tissues.The different horizontal layers represent different levels of biological organization. The plain black arrows symbolize the downward stream of regulation between growth hormones and actual growth through transcription factors activation and physical quantities modulation. The red plain arrows depict the indirect, integrated relationships between transcription factor activation, physical quantities modulation and cell wall irreversible extension our computational framework attempts to grasp. Finally the black dashed upward arrows stand for possible feedback mechanisms from shape changes on the biochemical regulation of growth.
Mentions: In a multicellular context, morphogenesis relies on differential growth across tissues. Each cell may feature specific values for the various parameters (turgor pressure, yielding threshold, extensibility…) used in Eq.(1). In principle, the regulation and coordination of these parameters is achieved through the action of the molecular regulatory networks that control the composition and mechanical properties of the cell wall, as described by the black arrows in Fig. 1. For example, cell wall modifying enzymes such as expansins, xyloglucan endo-tranglycosylases or pectin modifying enzymes are known to be triggered by transcription factors such as APETALA2 [9], MONOPTEROS [10] and AGAMOUS [11]. At the scale of the cell wall, actions of such enzymes have the potential to increase or decrease the viscosity and/or the rigidity of the wall. As a consequence, extensibility in Eq.(1) may be modified and affect growth.

Bottom Line: The model shows how forces generated by turgor-pressure can act both cell autonomously and non-cell autonomously to drive growth in different directions.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.

View Article: PubMed Central - PubMed

Affiliation: Virtual Plants Inria team, UMR AGAP, CIRAD, INRIA, INRA, Montpellier, France.

ABSTRACT
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.

Show MeSH
Related in: MedlinePlus