Cell Patterns Emerge from Coupled Chemical and Physical Fields with Cell Proliferation Dynamics: The Arabidopsis thaliana Root as a Study System

Abstract

A central issue in developmental biology is to uncover the mechanisms by which stem cells maintain their capacity to regenerate, yet at the same time produce daughter cells that differentiate and attain their ultimate fate as a functional part of a tissue or an organ. In this paper we propose that, during development, cells within growing organs obtain positional information from a macroscopic physical field that is produced in space while cells are proliferating. This dynamical interaction triggers and responds to chemical and genetic processes that are specific to each biological system. We chose the root apical meristem of Arabidopsis thaliana to develop our dynamical model because this system is well studied at the molecular, genetic and cellular levels and has the key traits of multicellular stem-cell niches. We built a dynamical model that couples fundamental molecular mechanisms of the cell cycle to a tension physical field and to auxin dynamics, both of which are known to play a role in root development. We perform extensive numerical calculations that allow for quantitative comparison with experimental measurements that consider the cellular patterns at the root tip. Our model recovers, as an emergent pattern, the transition from proliferative to transition and elongation domains, characteristic of stem-cell niches in multicellular organisms. In addition, we successfully predict altered cellular patterns that are expected under various applied auxin treatments or modified physical growth conditions. Our modeling platform may be extended to explicitly consider gene regulatory networks or to treat other developmental systems.

Proteomics in Deciphering the Auxin Commitment in the Arabidopsis thaliana Root Growth

“…[102][103][104] Similar studies suggest that morphogenetic patterns emerge from complex interplaying dynamical processes, acting at different levels of organization and spatiotemporal scales. Barrio et al 105 have modelled a distribution of the concentration of auxins (normalized with its maximum value) similar to the one observed in real roots by Petersson et al 20 .…”

Mathematical Models Light Up Plant Signaling

“…Further technological improvements will bring improved quantitation and opportunities for further modeling of molecular systems underpinning spatial development of A. thaliana ( Figure 4C). In particular, approaches that integrate modeling of tissue mechanics, growth, and molecular regulation promise to aid further study of these systems (Barrio et al, 2013) and contribute toward the development of whole-plant models, as discussed in the next section.…”

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

“…The conceptual and technical tools now available are enabling a more thorough study of their action, as well as their dynamical feedback with biochemical and genetic developmental processes (Newman and Bhat, 2009; Niklas and Kutschera, 2012; Purnell, 2012; Barrio et al, 2013; Mammoto et al, 2013; Bozorg et al, 2014 and references therein). In this review we aim at comparing the role of mechanical forces (e.g., tension and compression) in the generation of positional information and patterns in plant and animal systems.…”

“…Then, rather than just anchoring the cell to the ECM, focal adhesions function as mechanosensors that transmit the mechanical state of the ECM to the cell interior (Engler et al, 2006; Wojtaszek, 2011). The dynamics of cell proliferation, in turn, cause changes in the local tension and compression conditions and feedback to the mechanical state of the tissues (Weiss, 1959; Wojtaszek, 2011; Barrio et al, 2013). In this model, contractile actomyosin filaments, and other cytoskeletal components are the major tension elements that winch in the cytoskeleton against tent peg-like adhesions, and microtubules are considered to resist compression and to balance tensile forces (Ingber, 2008; Wojtaszek, 2011) (Figure 1).…”