Biology subjects

Boudaoud, A.

Publications and source records attributed to Boudaoud, A..

6 recordsLinked to original sources

bioRxiv2018

A gradient in inner pressure of germline cells controls overlaying epithelial cell morphogenesis

It is unknown how growth in one tissue impacts morphogenesis in a neighboring tissue. To address this, we used the Drosophila ovarian follicle, where a cluster of 15 nurse cells and a posteriorly located oocyte are surrounded by a layer of epithelial cells. It is known that as the nurse cells grow, the overlying epithelial cells flatten in a wave that begins in the anterior. Here, we demonstrate that an anterior to posterior gradient of decreasing cytoplasmic pressure is present across the nurse cells and that this gradient acts through TGF{beta} to control both the triggering and the progression of the wave of epithelial cell flattening. Our data indicate that intrinsic nurse cell growth is important to control proper nurse cell pressure. Finally, we reveal that nurse cell pressure and subsequent TGF{beta} activity in the StC combine to increase follicle elongation in the anterior, which is crucial for allowing nurse cell growth and pressure control. More generally, our results reveal that during development, inner cytoplasmic pressure in individual cells has an important role in shaping their neighbors. Impact StatementCell shape change depends on extrinsic forces exerted by cytoplasmic pressure in neighbouring cells.

developmental biology↗

bioRxiv2018

Modulation of tissue growth heterogeneity by responses to mechanical stress

Morphogenesis often yields organs with robust size and shapes, whereas cell growth and deformation feature significant spatio-temporal variability. Here, we investigate whether tissue responses to mechanical signals contribute to resolve this apparent paradox. We built a model of growing tissues made of fiber-like material, which may account for the cytoskeleton, polar cell-cell adhesion, or the extracellular matrix in animals, and for the cell wall in plants. We considered the synthesis and remodeling of this material, as well as the modulation of synthesis by isotropic and anisotropic response to mechanical stress. Formally, our model describes an expanding, mechanoresponsive, nematic, and active fluid. We show that mechanical responses buffer localized perturbations, with two possible regimes - hypo-responsive and hyper-responsive, and the transition between the two corresponds to a minimum value of the relaxation time. Whereas robustness of shapes suggests that growth fluctuations are confined to small scales, our model yields growth fluctuations that have long-range correlations. This indicates that growth fluctuations are a significant source of heterogeneity in development. Nevertheless, we find that mechanical responses may dampen such fluctuations, with a specific magnitude of anisotropic response that minimizes heterogeneity of tissue contours. We finally discuss how our predictions might apply to the development of plants and animals. Altogether, our results call for the systematic quantification of fluctuations in growing tissues.

biophysics↗

bioRxiv2018

Cellular heterogeneity in pressure and growth emerges from tissue topology and geometry

Cell-to-cell heterogeneity prevails in many biological systems, although its origin and function are often unclear. Cell hydrostatic pressure, alias turgor pressure, is essential in physiology and morphogenesis, and its spatial variations are often overlooked. Here, based on a mathematical model describing cell mechanics and water movement in a plant tissue, we predict that cell pressure anticorrelates with cell neighbour number. Using atomic force microscopy, we confirm this prediction in the Arabidopsis shoot apical meristem, a population of stem cells that generate all plant aerial organs. Pressure is predicted to correlate either positively or negatively with cellular growth rate depending on osmotic drive, cell wall extensibility, and hydraulic conductivity. The meristem exhibits one of these two regimes depending on conditions, suggesting that, in this tissue, water conductivity is non-negligible in growth control. Our results illustrate links between local topology, cell mechanical state and cell growth, with potential roles in tissue homeostasis.

biophysics↗

bioRxiv2018

MECHANOSENSATION DYNAMICALLY COORDINATES POLAR GROWTH AND CELL WALL ASSEMBLY TO PROMOTE CELL SURVIVAL

How growing cells cope with size expansion while ensuring mechanical integrity is not known. In walled cells, such as those of microbes and plants, growth and viability are both supported by a thin and rigid encasing cell wall (CW). We deciphered the dynamic mechanisms controlling wall surface assembly during cell growth, using a novel sub-resolution microscopy approach to monitor CW thickness in live rod-shaped fission yeast cells. We found that polar cell growth yielded wall thinning, and that thickness negatively influenced growth. Thickness at growing tips exhibited oscillating behavior with thickening phases followed by thinning phases, indicative of a delayed feedback promoting thickness homeostasis. This feedback was mediated by mechanosensing through the cell wall integrity pathway, which probes strain in the wall to adjust synthase localization and activity to surface growth. Mutants defective in thickness homeostasis lysed by rupturing the wall demonstrating its essential role for walled cell survival.

cell biology↗

bioRxiv2017

The self-organization of plant microtubules in three dimensions enables stable cortical localization and sensitivity to external cues

Many cell functions rely on the ability of microtubules to self-organize as complex networks. In plants, cortical microtubules are essential to determine cell shape as they guide the deposition of cellulose microfibrils, and thus control mechanical anisotropy in the cell wall. Here we analyze how, in turn, cell shape may influence microtubule behavior. Using a computational model of microtubules enclosed in a three-dimensional space, We show that the microtubule network has spontaneous configurations that could explain many experimental observations without resorting to specific regulation. In particular, we find that the preferred localization of microtubules at the cortex emerges from directional persistence of the microtubules, combined with their growth mode. We identified microtubule parameters that seem relatively insensitive to cell shape, such as length or number. In contrast, microtubule array anisotropy depends strongly on local curvature of the cell surface and global orientation follows robustly the longest axis of the cell. Lastly, we found that the network is capable of reorienting toward weak external directional cues. Altogether our simulations show that the microtubule network is a good transducer of weak external polarity, while at the same time, it easily reaches stable global configurations.\n\nAuthor summaryPlants exhibit an astonishing diversity in architecture and shape. A key to such diversity is the ability of their cells to coordinate and grow to reach a broad spectrum of sizes and shapes. Cell growth in plants is guided by the microtubule cytoskeleton. Here, we seek to understand how microtubules self-organize close to the cell surface. We build upon previous two-dimensional models and we consider microtubules as lines growing in three dimensions, accounting for interactions between microtubules or between microtubules and the cell surface. We show that microtubule arrays are able to adapt to various cell shapes and to reorient in response to factors such as signals or environment. Altogether, our results help to understand how the microtubule cytoskeleton contributes to the diversity of plant shapes and to how these shapes adapt to environment.

cell biology↗

bioRxiv2017

Cells From The Same Lineage Switch From Reduction To Enhancement Of Size Variability In Arabidopsis Sepals

Organs form with remarkably consistent sizes and shapes during development, whereas a high variability in size and growth is observed at cell level. Given this contrast, it is unclear how such consistency at organ scale can emerge from cellular behavior. We examine the growth of cell lineages, or groups of cells that are the progeny of a single mother cell. At early stages of the lineage, we find that initially smaller lineages grow faster than the larger ones reducing variability in lineage size, a phenomenon we refer to as size uniformization. In contrast at later stages of the lineage, size variability is enhanced when initially larger cell lineages grow faster than the smaller ones. Our results imply that the cell lineage changes its growth pattern at a tipping point. Finally, we found that the growth heterogeneity of individual cells within a lineage is correlated with fast growth of the lineage. Consequently, fast growing lineages show greater cell growth heterogeneity, leading to uniformization in lineage size. Thus, cellular variability in growth contributes toward decreasing variability of cell lineages throughout the sepal.

developmental biology↗