Cellular Heterogeneity in Pressure and Growth Emerges from Tissue Topology and Geometry

Long, Yuchen; Cheddadi, Ibrahim; Mosca, Gabriella; Mirabet, Vincent; Dumond, Mathilde; Kiss, Annamária; Traas, Jan; Godin, Christophe; Boudaoud, Arezki

doi:10.1016/j.cub.2020.02.027

Cited by 91 publications

(64 citation statements)

References 86 publications

(150 reference statements)

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“…Note also that for a given stress the turgor decreases with the number of edges n. Therefore, the yield turgor P Y depends both on n and R and is not a well defined parameter. It suggests also that cells with less neighbours should have a higher turgor, as experimentally observed in [21,22].…”

Section: First Extension: Multidimensional Growthsupporting

confidence: 59%

“…Cells then regulate the tissue deformations by locally modulating the material structure of their walls (stiffness and anisotropy) [6,[16][17][18][19][20]. However, the situation in real plants is more complex: turgor heterogeneity has been observed at cellular level [21,22], which challenges the assumption of very fast fluxes. As a matter of fact, the relative importance of fluxes or wall mechanics as limiting factors to growth has fuelled a long standing debate [3,23] and is still an open question.…”

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confidence: 99%

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Coupling water fluxes with cell wall mechanics in a multicellular model of plant development

Cheddadi

Génard

Bertin

et al. 2019

Preprint

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The growth of plant organs is a complex process powered by osmosis that attracts water inside the cells; this influx induces simultaneously an elastic extension of the walls and pressure in the cells, called turgor pressure; above a threshold, the walls yield and the cells grow. Based on Lockhart's seminal work, various models of plant morphogenesis have been proposed, either for single cells, or focusing on the wall mechanical properties. However, the synergistic coupling of fluxes and wall mechanics has not yet been fully addressed in a multicellular model. This work lays the foundations of such a model, by simplifying as much as possible each process and putting emphasis on the coupling itself. Its emergent properties are rich and can help to understand plant morphogenesis. In particular, we show that the model can display a new type of lateral inhibitory mechanism that could contribute to the amplification of growth heterogeneities, essential for shape differentiation.Plant growth and morphogenesis | Biophysics | Mathematical modelling | Emergence | Lateral inhibition P lants grow throughout their lifetime at the level of small regions containing undifferentiated cells, the meristems, located at the extremities of their axes. Growth is powered by osmosis that tends to attract water inside the cells. The corresponding increase in volume leads to simultaneous tension in the walls and hydrostatic pressure (so-called turgor pressure) in the cells. Continuous growth occurs thanks to the yielding of the walls to these stretching forces [1][2][3].This interplay between growth, water fluxes, wall stress and turgor was first modelled by Lockhart in 1965 [4], in the context of a single elongating cell. Recent models focused on how genes regulate growth at more integrated levels [5][6][7][8][9]. To accompany genetic, molecular, and biophysical analyses of growing tissues, various extensions of Lockhart's model to multicellular tissues have been developed. The resulting models are intrinsically complex as they represent collections from tens to thousands of cells in 2-or 3-dimensions interacting with each other. To cut down the complexity, several approaches abstract organ multicellular structures as polygonal networks of 1D visco-elastic springs either in 2D [7,[10][11][12] or in 3D [6,13] submitted to a steady turgor pressure. Other approaches try to represent more realistically the structure of the plant walls by 2D deformable wall elements able to respond locally to turgor pressure by anisotropic growth [8,14,15].Most of these approaches consider turgor as a constant driving force for growth, explicitely or implicitly assuming that fluxes occur much faster than wall synthesis. Cells then regulate the tissue deformations by locally modulating the material structure of their walls (stiffness and anisotropy) [6,[16][17][18][19][20]. However, the situation in real plants is more complex: turgor heterogeneity has been observed at cellular level [21,22], which challenges the assumption of very fast fluxes. As a matter of f...

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Section: First Extension: Multidimensional Growthsupporting

confidence: 59%

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confidence: 99%

Coupling water fluxes with cell wall mechanics in a multicellular model of plant development

Cheddadi

Génard

Bertin

et al. 2019

Preprint

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“…Growth of plant structures is complex and involves multiple tightly coordinated processes [29][30][31], including turgor driven growth of plant cells, wall softening (hydration), wall extension, wall deposition and cell division [29,[32][33][34]. Our model does not resolve these processes in detail.…”

Section: Figurementioning

confidence: 99%

Mathematical modeling of plant cell fate transitions controlled by hormonal signals

Klawe

Stiehl

Bastian

et al. 2019

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Coordination of fate transition and cell division is crucial to maintain the plant architecture and to achieve efficient production of plant organs. In this paper, we analysed the stem cell dynamics at the shoot apical meristem (SAM) that is one of the plant stem cells locations. We designed a mathematical model to elucidate the impact of hormonal signaling on the fate transition rates between different zones corresponding to slowly dividing stem cells and fast dividing transit amplifying cells. The model is based on a simplified two-dimensional disc geometry of the SAM and accounts for a continuous displacement towards the periphery of cells produced in the central zone. Coupling growth and hormonal signaling results in a nonlinear system of reaction-diffusion equations on a growing domain with the growth velocity depending on the model components. The model is tested by simulating perturbations in the level of key transcription factors that maintain SAM homeostasis. The model provides new insights on how the transcription factor HECATE is integrated in the regulatory network that governs stem cell differentiation. 1 SummaryPlants continuously generate new organs such as leaves, roots and flowers. This process is driven by stem cells which are located in specialized regions, so-called meristems. Dividing stem cells give rise to offspring that, during a process referred to as cell fate transition, become more specialized and give rise to organs. Plant architecture and crop yield crucially depend on the regulation of meristem dynamics. To better understand this regulation, we develop a computational model of the shoot meristem. The model describes the meristem as a two-dimensional disk that can grow and shrink over time, depending on the concentrations of the signalling factors in its interior. This allows studying how the non-linear interaction of multiple transcription factors is linked to cell division and fate-transition. We test the model by simulating perturbations of meristem signals and comparing them to experimental data. The model allows simulating different hypotheses about signal effects. Based on the model we study the specific role of the transcription factor HECATE and provide new insights in its action on cell dynamics and in its interrelation with other known transcription factors in the meristem. 4 ing molecules. Such models have been applied e.g., to investigate cytokinin signaling [11] and patterning of the shoot apical meristem [14,17]. To investigate the impact of HEC on fate transition and proliferation rates of cells in the CZ and PZ, we have recently proposed a model based on the population dynamics approach, in which dynamics of different cell subpopulations are described by ordinary differential equations [9]. Such approach allows tracking how changes in cell proliferation, fate transition, primordia formation and primordia separation affect the time evolution and steady-state size of the different SAM zones but does not take into account spatio-temporal dynamics of the underlying signal...

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“…The turgor pressure of growing cells, such as the cells of the shoot apical meristem (SAM), is in the range of 1 MPa (Beauzamy et al, 2015). In addition to developmental stage and environmental conditions, the size and local topology of the cells also contributes to heterogeneity in turgor pressure (Long et al, 2020).…”

Section: Mechanics In Plants Turgor Pressure and Epidermal Tensionmentioning

confidence: 99%

Mechanical feedback-loop regulation of morphogenesis in plants

Sampathkumar

2020

Development

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Morphogenesis is a highly controlled biological process that is crucial for organisms to develop cells and organs of a particular shape. Plants have the remarkable ability to adapt to changing environmental conditions, despite being sessile organisms with their cells affixed to each other by their cell wall. It is therefore evident that morphogenesis in plants requires the existence of robust sensing machineries at different scales. In this Review, I provide an overview on how mechanical forces are generated, sensed and transduced in plant cells. I then focus on how such forces regulate growth and form of plant cells and tissues.

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Cellular Heterogeneity in Pressure and Growth Emerges from Tissue Topology and Geometry

Cited by 91 publications

References 86 publications

Coupling water fluxes with cell wall mechanics in a multicellular model of plant development

Coupling water fluxes with cell wall mechanics in a multicellular model of plant development

Mathematical modeling of plant cell fate transitions controlled by hormonal signals

Mechanical feedback-loop regulation of morphogenesis in plants

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