Mechanical forces as information: an integrated approach to plant and animal development (original) (raw)

Developmental patterning by mechanical signals in Arabidopsis

Science (New York, N.Y.), 2008

A central question in developmental biology is whether and how mechanical forces serve as cues for cellular behavior and thereby regulate morphogenesis. We found that morphogenesis at the Arabidopsis shoot apex depends on the microtubule cytoskeleton, which in turn is regulated by mechanical stress. A combination of experiments and modeling shows that a feedback loop encompassing tissue morphology, stress patterns, and microtubule-mediated cellular properties is sufficient to account for the coordinated patterns of microtubule arrays observed in epidermal cells, as well as for patterns of apical morphogenesis.

A Comparative Mechanical Analysis of Plant and Animal Cells Reveals Convergence across Kingdoms

Biophysical Journal, 2014

Plant and animals have evolved different strategies for their development. Whether this is linked to major differences in their cell mechanics remains unclear, mainly because measurements on plant and animal cells relied on independent experiments and setups, thus hindering any direct comparison. In this study we used the same micro-rheometer to compare animal and plant single cell rheology. We found that wall-less plant cells exhibit the same weak power law rheology as animal cells, with comparable values of elastic and loss moduli. Remarkably, microtubules primarily contributed to the rheological behavior of wall-less plant cells whereas rheology of animal cells was mainly dependent on the actin network. Thus, plant and animal cells evolved different molecular strategies to reach a comparable cytoplasmic mechanical core, suggesting that evolutionary convergence could include the internal biophysical properties of cells.

Feedback from tissue mechanics self-organizes efficient outgrowth of plant organ

Biophysical Journal, 2019

Plant organ outgrowth superficially appears like the continuous mechanical deformation of a sheet of cells. Yet, how precisely cells as individual mechanical entities can act to morph a tissue reliably and efficiently into three dimensions during outgrowth is still puzzling especially when cells are tightly connected as in plant tissue. In plants, the mechanics of cells within a tissue is particularly well defined as individual cell growth is essentially the mechanical yielding of cell-wall in response to internal turgor pressure. Cell wall stiffness is controlled by biological signalling and, hence, cell growth is observed to respond to mechanical stresses building up within a tissue. What is the role of the mechanical feedback during morphing of tissue in three dimensions? Here, we develop a three dimensional vertex model to investigate tissue mechanics at the onset of organ outgrowth at the tip of a plant shoot. We find that organ height is primarily governed by the ratio of growth rates of faster growing cells initiating the organ to slower growing cells surrounding them. Remarkably, the outgrowth rate is higher when cells growth responds to the tissue-wide mechanical stresses. Our quantitative analysis of simulation data shows that tissue mechanical feedback on cell growth can act via twofold mechanism. First, the feedback guides patterns of cellular growth. Second, the feedback modifies the stress patterns on the cells, consequently amplifying and propagating growth anisotropies. This mechanism may allow plants to grow organs efficiently out of the meristem by reorganizing the cellular growth rather than inflating growth rates.

The Problem of Morphogenesis: unscripted biophysical control systems in plants

Abstract The relative simplicity of plant developmental sys- tems, having evolved within the universal constraints imposed by the plant cell wall, may allow us to outline a consistent developmental narrative that is not currently possible in the animal kingdom. In this article, I discuss three aspects of the development of the mature form in plants, approaching them in terms of the role played by the biophysics and mechanics of the cell wall during growth. First, I discuss axis extension in terms of a loss of stability-based model of cell wall stress relaxation and I introduce the possibility that cell wall stress relaxation can be modeled as a binary switch. Second, I consider meristem shape and surface conformation as a controlling element in the morphogenetic circuitry of plant organogenesis at the apex. Third, I approach the issue of reproductive differentiation and propose that the multicellular sporangium, a universal feature of land plants, acts as a stress–mechanical lens, focusing growth-induced stresses to create a geometrically precise mechanical singularity that can serve as an inducing developmental signal triggering the initiation of reproductive differentiation. Lastly, I offer these three examples of biophysically integrated control processes as entry points into a narrative that provides an independent, non-genetic context for understanding the evolution of the apoplast and the morphogenetic ontogeny of multicellular land plants.

Signals, Motors, Morphogenesis -the Cytoskeleton in Plant Development

Plant Biology, 1999

Plant shape can adapt to a changing environment. This requires a structure that (1) must be highly dynamic, (2) can respond to a range of signals, and (3) can control cellular morphogenesis. The cytoskeleton, microtubules, actin microfilaments, and cytoskeletal motors meets these requirements, and plants have evolved specific cytoskeletal arrays consisting of both microtubules and microfilaments that can link signal transduction to cellular morphogenesis: cortical microtubules, preprophase band, phragmoplast on the microtubular side, transvacuolar microfilament bundles, and phragmosome on the actin side. These cytoskeletal arrays are reviewed with special focus on the signal responses of higher plants. The signaltriggered dynamic response of the cytoskeleton must be based on spatial cues that organize assembly and disassembly of tubulin and actin. In this context the great morphogenetic potential of cytoskeletal motors is discussed. The review closes with an outlook on new methodological approaches to the problem of signal-triggered morphogenesis.

SPATIAL CONTROL OF CELL EXPANSION BY THE PLANT CYTOSKELETON

Annual Review of Cell and Developmental Biology, 2005

The cytoskeleton plays important roles in plant cell shape determination by influencing the patterns in which cell wall materials are deposited. Cortical microtubules are thought to orient the direction of cell expansion primarily via their influence on the deposition of cellulose into the wall, although the precise nature of the microtubule-cellulose relationship remains unclear. In both tipgrowing and diffusely growing cell types, F-actin promotes growth and also contributes to the spatial regulation of growth. F-actin has been proposed to play a variety of roles in the regulation of secretion in expanding cells, but its functions in cell growth control are not well understood. Recent work highlighted in this review on the morphogenesis of selected cell types has yielded substantial new insights into mechanisms governing the dynamics and organization of cytoskeletal filaments in expanding plant cells and how microtubules and F-actin interact to direct patterns of cell growth. Nevertheless, many important questions remain to be answered. 271 Annu. Rev. Cell. Dev. Biol. 2005.21:271-295. Downloaded from arjournals.annualreviews.org by University of California -San Diego on 10/18/05. For personal use only.

Emergent patterns of growth controlled by multicellular form and mechanics

Proceedings of The National Academy of Sciences, 2005

Spatial patterns of cellular growth generate mechanical stresses that help to push, fold, expand, and deform tissues into their specific forms. Genetic factors are thought to specify patterns of growth and other behaviors to drive morphogenesis. Here, we show that tissue form itself can feed back to regulate patterns of proliferation. Using microfabrication to control the organization of sheets of cells, we demonstrated the emergence of stable patterns of proliferative foci. Regions of concentrated growth corresponded to regions of high tractional stress generated within the sheet, as predicted by a finite-element model of multicellular mechanics and measured directly by using a micromechanical force sensor array. Inhibiting actomyosin-based tension or cadherin-mediated connections between cells disrupted the spatial pattern of proliferation. These findings demonstrate the existence of patterns of mechanical forces that originate from the contraction of cells, emerge from their multicellular organization, and result in patterns of growth. Thus, tissue form is not only a consequence but also an active regulator of tissue growth. morphogenesis ͉ pattern formation ͉ micropatterning ͉ cytoskeleton ͉ mechanotransduction Substrate Fabrication. Micropatterned substrata containing fibronectin-coated islands were fabricated as described in ref. 24. Briefly, glass coverslips were coated by electron beam evaporation with 2.0 nm of Ti, followed by 15 nm of Au. Elastomeric stamps containing a relief of the desired pattern were inked in an ethanolic solution of 2 mM hexadecanethiol (Sigma), dried under nitrogen, and placed in conformal contact for 2 s with the Au-coated coverslips. The unstamped regions of the coverslips were rendered nonadhesive by immersing them in an ethanolic solution of 2 mM tri(ethylene glycol)-terminated alkanethiol (Prochimia, Golansk, Poland) for 1 h. Substrata were rinsed, sterilized in ethanol, and incubated in 25 g͞ml fibronectin in PBS for 2 h.

Self-organized tissue mechanics underlie embryonic regulation

2021

Early amniote development is a highly regulative and self-organized process, capable to adapt to interference through cell-cell interactions, which are widely believed to be mediated by molecules. Analyzing intact and mechanically perturbed avian embryos, we show that the mechanical forces that drive embryogenesis self-organize in an analog of Turing’s molecular reaction-diffusion model, with contractility locally self-activating and the ensuing tension acting as a long-range inhibitor. This mechanical feedback governs the persistent pattern of tissue flows that shape the embryo and steers the concomitant emergence of embryonic territories by modulating gene expression, ensuring the formation of a single embryo under normal conditions, yet allowing the emergence of multiple, well-proportioned embryos upon perturbations. Thus, mechanical forces are a central signal in embryonic self-organization, feeding back onto gene expression to canalize both patterning and morphogenesis.