Stochasticity and the limits of molecular signaling in plant development.

Understanding plant development is in part a theoretical endeavor that can only succeed if it is based upon a correctly contrived axiomatic framework. Here I revisit some of the basic assumptions that frame our understanding of plant development and suggest that we consider an alternative informational ecosystem that more faithfully reflects the physical and architectural realities of plant tissue and organ growth. I discuss molecular signaling as a stochastic process and propose that the iterative and architectural nature of plant growth is more usefully represented by deterministic models based upon structural, surficial, and stress-mechanical information networks that come into play at the trans-cellular level.

Microbead encapsulation of living plant protoplasts: A new tool for the handling of single plant cells.

PREMISE OF THE STUDY: Understanding plant cell biomechanics has been hampered by a lack of appropriate experimental tools. Here we introduce a protocol for the incorporation of individual plant protoplasts into precisely sized agarose microbeads. This technology may lead to new ways to manipulate the physical and chemical microenvironment of individual plant cells. METHODS AND RESULTS: Living protoplasts obtained from BY-2 tobacco suspension cultures were continuously incorporated into a stream of agarose microdroplets, collected in cooled mineral oil as gelled microbeads, and then transferred into liquid MS medium for culture. In this first report, we show that spherical microbeads containing living protoplasts can be easily generated in quantity and that these encapsulated cells continue to grow and divide. CONCLUSIONS: Microbead encapsulation of protoplasts affords the opportunity to precisely control the physical microenvironment of individual plant cells. Ultimately, this method may help facilitate novel studies in plant biomechanics.

The problem of morphogenesis: unscripted biophysical control systems in plants.

The relative simplicity of plant developmental systems, 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, nongenetic context for understanding the evolution of the apoplast and the morphogenetic ontogeny of multicellular land plants.

Loss of stability: a new look at the physics of cell wall behavior during plant cell growth.

In this article we investigate aspects of turgor-driven plant cell growth within the framework of a model derived from the Eulerian concept of instability. In particular we explore the relationship between cell geometry and cell turgor pressure by extending loss of stability theory to encompass cylindrical cells. Beginning with an analysis of the three-dimensional stress and strain of a cylindrical pressure vessel, we demonstrate that loss of stability is the inevitable result of gradually increasing internal pressure in a cylindrical cell. The turgor pressure predictions based on this model differ from the more traditional viscoelastic or creep-based models in that they incorporate both cell geometry and wall mechanical properties in a single term. To confirm our predicted working turgor pressures, we obtained wall dimensions, elastic moduli, and turgor pressures of sequential internodal cells of intact Chara corallina plants by direct measurement. The results show that turgor pressure predictions based on loss of stability theory fall within the expected physiological range of turgor pressures for this plant. We also studied the effect of varying wall Poisson's ratio nu on extension growth in living cells, showing that while increasing elastic modulus has an understandably negative effect on wall expansion, increasing Poisson's ratio would be expected to accelerate wall expansion.

Loss of stability, pH, and the anisotropic extensibility of Chara cell walls.

We investigated the effects of acid conditions on the extensibility of isolated wall segments from growing Chara corallina cells, providing the first detailed multi-azimuthal description of the anisotropic elastic modulus of the walls. The values of anisotropic modulus were obtained by loading a tensile force on wall ribbons excised from the cell walls along twelve different azimuths, and measuring the resulting elongation of the ribbons. Our study differs from previous studies in which mechanical loading of the wall materials was performed under creep conditions. We used ramp-loading conditions which meet the requirements for Loss of Stability. The results show that whereas a linear relationship between wall extension and log time is typical for creep-based experiments, it is not seen under ramp-loading conditions. To clarify the relative values of the wall moduli, the complete all-around anisotropic modulus is presented in polar coordinates, with the value of longitudinal modulus normalized to one unit. Acid pH enhances the extensibility of the wall materials, especially when medium pH

Loss of stability-a new model for stress relaxation in plant cell walls.

This study addresses the mechanism of wall stress relaxation in growing plant cells. The current viscoelastic model of cell wall relaxation, which dates from the work of Preston, Cleland, Lockhart, and others in the 1960s, has serious shortcomings. It has been shown however that the theory of loss of stability (LOS) can be applied to materials in tension, leading to the conclusion that the relaxation of stresses in the walls of any pressure vessel is rigorously modeled using LOS. We propose that LOS also provides a more appropriate and versatile model of stress relaxation in growing plant cells. We argue that when treated as a manifestation of LOS, the regulation of cell turgor has a rigorous and demonstrable basis in the geometrical and physical properties of the cell wall and the cell's ability to import water. Thus plant cell growth can be regarded as an inherently self-limiting process, tunable by biochemical or structural means. Lastly, despite the current limitations of our model, we apply direct measurement of elastic modulus, wall thickness and cell radius obtained from cylindrical Chara corallina cells to generate an initial calculation of critical pressures in a hypothetical spherical cell with the same material properties.