Mechanical forces as information: an integrated approach to plant and animal development

Abstract

Mechanical forces such as tension and compression act throughout growth and development of multicellular organisms. These forces not only affect the size and shape of the cells and tissues but are capable of modifying the expression of genes and the localization of molecular components within the cell, in the plasma membrane, and in the plant cell wall. The magnitude and direction of these physical forces change with cellular and tissue properties such as elasticity. Thus, mechanical forces and the mesoscopic fields that emerge from their local action constitute important sources of positional information. Moreover, physical and biochemical processes interact in non-linear ways during tissue and organ growth in plants and animals. In this review we discuss how such mechanical forces are generated, transmitted, and sensed in these two lineages of multicellular organisms to yield long-range positional information. In order to do so we first outline a potentially common basis for studying patterning and mechanosensing that relies on the structural principle of tensegrity, and discuss how tensegral structures might arise in plants and animals. We then provide some examples of morphogenesis in which mechanical forces appear to act as positional information during development, offering a possible explanation for ubiquitous processes, such as the formation of periodic structures. Such examples, we argue, can be interpreted in terms of tensegral phenomena. Finally, we discuss the hypothesis of mechanically isotropic points as a potentially generic mechanism for the localization and maintenance of stem-cell niches in multicellular organisms. This comparative approach aims to help uncovering generic mechanisms of morphogenesis and thus reach a better understanding of the evolution and development of multicellular phenotypes, focusing on the role of physical forces in these processes.

Keywords: mechanical forces; multicellular development; positional information; stem-cell niches; tensegrity.

Figure B1.1

The stress tensor of a cubic body in Cartesian coordinates. For each coordinate x, y, or z, there are three stress components. In this case the normal stresses coincide with the cartesian axes. There always exists a coordinate system in which all tangential stresses are zero, and the nonzero normal stresses are called principal stresses.

Figure B1.2

Principal stresses in a curvilinear coordinate system. A schematic cylinder subjected to internal pressure P is shown. The surface of the cylinder exerts forces due to the pressure P, which distributes as stresses in the directions r, θ, z. The radial stress, σ_r, is normal to the surface, the stress σ_θ is tangential to the surface and the axial stress σ_z is in the direction of the z axis.

Figure 1

Schematic representation of tensegrity construction in animals and plants. (A) In animals, the architecture results from the interplay between compressive microtubules and tensile actin filaments; this structure allows to both perceive mechanical signals and to maintain cell shape. (B) In plants turgor pressure exerted by the cytoplasma and vacuole (blue) pulls out against cellulose microfibrils, which are tensed; the rigid cell wall gives shape to cells and the cytoskeleton is released from the architectural function.

Figure 2

Mechanical forces as positional dependent information in the formation of periodic structures in plants and animals. (A) In vertebrates, the formation of pigment patterns is determined by attraction/repulsion of chromatocytes and the deformation of the mesenchyme that generate tension tracks through which cells migrate. (B) In plants, the enhancement of cell wall and tissue elasticity by auxin creates undulations at the SAM surface. Furthermore, auxin regulates genetic programs that promote cell proliferation and differentiation into the different organ primordia. The modification of the mechanical field serves as positional information for the polarization of the PIN auxin efflux transporters. In both examples, long-range forces caused by changes in the mechanical field have a delimited range of action which is indicated by the periodicity of patterns.

Figure 3

Schematic representation of the structural similarities in the organization of stem cell niches (SCMs) in plants and animals. (A) Drosophila melanogaster ovary, and (B) root apical meristem (RAM) of Arabidopsis thaliana. In both cases, organizer cells (orange) are surrounded by pluripotent stem cells (blue) that divide rapidly and that, after a determined number of divisions, elongate, and acquire a particular cell fate.

Figure B2.1

Principal planes. (A) A solid body subjected to uniaxial tension and the principal plane, which is parallel to the direction of applied force. All tangential or shear stresses are zero along this plane. (B) The plane that is perpendicular to the principal plane undergoes the maximal shear stresses generated by uniaxial stress σ_x.

Figure B2.2

Confocal coordinate system modeling an apical dome. Periclines are the red curves corresponding to the v coordinate and anticlines correspond to the u coordinate. The curved boundary of the surface is represented by the curve v = 6, which is under tension produced by internal pressure. The singularity of the system is marked by an asterisk. The curves (u, v) coincide with stress trajectories dictated by the Lamé-Maxwell equations on a surface subjected to compression. In this case, the v curves are the compression trajectories. The singularity corresponds to the unique region on the surface at which growth rates are nearly zero, meaning that stresses are also almost null at this point.

Figure 4

Localization of plant meristems. Localization of plant meristems. Apical and axillary meristems (arrowheads) of (A) Arabidopsis embryo, and (B) Marchantia gametophyte, respectively. (C) Vascular meristems that generate xylem and phloem tissues during radial growth are located within a narrow ring (dashed line). (D) Lintilhac (1974a,b) showed the points of stress concentration generated by notches. He also predicted that ring-like geometries (dashed line) would be zones where forces of tension and compression nullify (E). We hypothesize that the mechanical properties of these regions are part of a potentially generic mechanism for the localization and maintenance of SCNs in multicellular organisms.