Turning a plant tissue into a living cell froth through isotropic growth

Corson, Francis; Hamant, Olivier; Bohn, Steffen; Traas, Jan; Boudaoud, Arezki; Couder, Y.

doi:10.1073/pnas.0812493106

Cited by 112 publications

(105 citation statements)

References 24 publications

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“…That biomechanically induced mechanical stresses may be involved in cell wall orientation is consistent with many observations (e.g., Corson et al, 2009, although see Mirabet et al, 2011. The simplest plant cells are parenchyma cells, which have thin primary walls and are therefore hydrostatic.…”

Section: Future Cell Wall (Fcw)supporting

confidence: 75%

Dynamical patterning modules in plant development and evolution

Hernández-Hernández

Niklas²,

Newman³

et al. 2012

Int. J. Dev. Biol.

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Broad comparative studies at the level of developmental processes are necessary to fully understand the evolution of development and phenotypes. The concept of dynamical patterning modules (DPMs) provides a framework for studying developmental processes in the context of wide comparative analyses. DPMs are defined as sets of ancient, conserved gene products and molecular networks, in conjunction with the physical morphogenetic and patterning processes they mobilize in the context of multicellularity. The theoretical framework based on DPMs originally postulated that each module generates a key morphological motif of the basic animal body plans and organ forms. Here, we use a previous definition of the plant multicellular body plan and describe the basic DPMs underlying the main features of plant development. For each DPM, we identify characteristic molecules and molecular networks, and when possible, the physical processes they mobilize. We then briefly review the phyletic distribution of these molecules across the various plant lineages. Although many of the basic plant DPMs are significantly different from those of animals, the framework established by a DPM perspective on plant development is essential for comparative analyses aiming to provide a truly mechanistic explanation for organic development across all plant and animal lineages.

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Section: Future Cell Wall (Fcw)supporting

confidence: 75%

Dynamical patterning modules in plant development and evolution

Hernández-Hernández

Niklas²,

Newman³

et al. 2012

Int. J. Dev. Biol.

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“…S20) is that the difference in per unit size growth rates between sisters is driven primarily by the asymmetrical division of the mother cell rather than by other size-related metrics with which asymmetrical division is correlated. This phenomenon is not straightforwardly accounted for by a cell wall growth rate that depends on elastic stress or strain of the wall, a mechanism that partially controls growth rate and is modulated by turgor (45)(46)(47)(48). How this sistercell growth heterogeneity can be integrated with the report that growth heterogeneity is induced by neighbor interactions (30) is a future challenge.…”

Section: Discussionmentioning

confidence: 99%

Cell size and growth regulation in the Arabidopsis thaliana apical stem cell niche

Willis

Refahi

Wightman

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

180

217

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Cell size and growth kinetics are fundamental cellular properties with important physiological implications. Classical studies on yeast, and recently on bacteria, have identified rules for cell size regulation in single cells, but in the more complex environment of multicellular tissues, data have been lacking. In this study, to characterize cell size and growth regulation in a multicellular context, we developed a 4D imaging pipeline and applied it to track and quantify epidermal cells over 3-4 d in Arabidopsis thaliana shoot apical meristems. We found that a cell size checkpoint is not the trigger for G2/M or cytokinesis, refuting the unexamined assumption that meristematic cells trigger cell cycle phases upon reaching a critical size. Our data also rule out models in which cells undergo G2/M at a fixed time after birth, or by adding a critical size increment between G2/M transitions. Rather, cell size regulation was intermediate between the critical size and critical increment paradigms, meaning that cell size fluctuations decay by ∼75% in one generation compared with 100% (critical size) and 50% (critical increment). Notably, this behavior was independent of local cell-cell contact topologies and of position within the tissue. Cells grew exponentially throughout the first >80% of the cell cycle, but following an asymmetrical division, the small daughter grew at a faster exponential rate than the large daughter, an observation that potentially challenges present models of growth regulation. These growth and division behaviors place strong constraints on quantitative mechanistic descriptions of the cell cycle and growth control.cell size | cell growth | cell cycle | homeostasis | plant stem cells H ow cells coordinate growth and division to achieve a particular cell size remains a fundamental question in biology. Our understanding of this basic property of cells is limited, in part, by the lack of quantitative data on cellular growth and size kinetics over multiple generations, especially in higher eukaryotes (1). Classical studies of cell size homeostasis focused on whether division occurred upon reaching a critical size or after a fixed time period has elapsed (2, 3). However, time-lapse studies of single-celled organisms spanning a range of bacteria (4-7) and the yeast Saccharomyces cerevisiae (8) have recently indicated that cell size is regulated by the addition of a fixed volume increment between divisions. Identification of the size regulation behavior constrains the set of feasible molecular scenarios for how growth and division are coordinated with the cell cycle (8-10). In multicellular tissues, the loss of growth and division/cell cycle coordination could have an impact on the organism's development, yet, to the best of our knowledge, cell growth and size kinetics have never before been measured over generations in a tissue context. The experimental challenges are particularly acute because interdivision times are often on the order of tens of hours, cells have a diversity of shapes necessitating di...

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“…Modeling has greatly contributed to our understanding of the genetic and physical processes underlying development (32). Numerous modeling studies of animal and plant systems have been key to emphasize the role of these processes in the regulation of cell proliferation (33,34), but few have considered the biphasic nature of plant tissues. In early work in the laboratory (17), such models were based on cell wall segments represented as a set of two parallel springs, where the elastic properties of each spring were controlled by the corresponding adjacent cell.…”

Section: A Simple Experimental System For Quantitative Analysis Of Plantmentioning

confidence: 99%

Coordination of plant cell division and expansion in a simple morphogenetic system

Dupuy

Mackenzie

Haseloff

2010

Proc. Natl. Acad. Sci. U.S.A.

126

107

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Morphogenesis in plants arises from the interplay of genetic and physical interactions within a growing network of cells. The physical aspects of cell proliferation and differentiation are genetically regulated, but constrained by mechanical interactions between the cells. Higher plant tissues consist of an elaborate three-dimensional matrix of active cytoplasm and extracellular matrix, where it is difficult to obtain direct measurements of geometry or cell interactions. To properly understand the workings of plant morphogenesis, it is necessary to have biological systems that allow simple and direct observation of these processes. We have adopted a highly simplified plant system to investigate how cell proliferation and expansion is coordinated during morphogenesis. Coleocheate scutata is a microscopic fresh-water green alga with simple anatomical features that allow for accurate quantification of morphogenetic processes. Image analysis techniques were used to extract precise models for cell geometry and physical parameters for growth. This allowed construction of a deformable finite element model for growth of the whole organism, which incorporated cell biophysical properties, viscous expansion of cell walls, and rules for regulation of cell behavior. The study showed that a simple set of autonomous, cell-based rules are sufficient to account for the morphological and dynamic properties of Coleochaete growth. A variety of morphogenetic behavior emerged from the application of these local rules. Cell shape sensing is sufficient to explain the patterns of cell division during growth. This simplifying principle is likely to have application in modeling and design for engineering of higher plant tissues.biophysics | Coleochaete | dynamics | morphogenesis microscopy

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Turning a plant tissue into a living cell froth through isotropic growth

Cited by 112 publications

References 24 publications

Dynamical patterning modules in plant development and evolution

Dynamical patterning modules in plant development and evolution

Cell size and growth regulation in the Arabidopsis thaliana apical stem cell niche

Coordination of plant cell division and expansion in a simple morphogenetic system

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