Posture control in land plants: growth, position sensing, proprioception, balance, and elasticity

Abstract

The colonization of the atmosphere by land plants was a major evolutionary step. The mechanisms that allow for vertical growth through air and the establishment and control of a stable erect habit are just starting to be understood. A key mechanism was found to be continuous posture control to counterbalance the mechanical and developmental challenges of maintaining a growing upright structure. An interdisciplinary systems biology approach was invaluable in understanding the underlying principles and in designing pertinent experiments. Since this discovery previously held views of gravitropic perception had to be reexamined and this has led to the description of proprioception in plants. In this review, we take a purposefully pedagogical approach to present the dynamics involved from the cellular to whole-plant level. We show how the textbook model of how plants sense gravitational force has been replaced by a model of position sensing, a clinometer mechanism that involves both passive avalanches and active motion of statoliths, granular starch-filled plastids, in statocytes. Moreover, there is a transmission of information between statocytes and other specialized cells that sense the degree of organ curvature and reset asymmetric growth to straighten and realign the structure. We give an overview of how plants have used the interplay of active posture control and elastic sagging to generate a whole range of spatial displays during their life cycles. Finally, a position-integrating mechanism has been discovered that prevents directional plant growth from being disrupted by wind-induced oscillations.

Atmospheric CO2 and VPD alter the diel oscillation of leaf elongation in perennial ryegrass: compensation of hydraulic limitation by stored‐growth

“…Certainly, the diel elongation responses found in this work warrant more detailed mechanistic studies with spatio-temporal detail at the level of expanding tissue, including the kinematics of growth, cell division, expansion and associated metabolic processes (e.g. Green et al, 1971;Nonami & Boyer, 1993;Martre et al, 1999;Fricke & Peters, 2002;Moulia et al, 2019).…”

Architectural analyses of tree forking habit with single-image photogrammetry: a case study of post-mature temperate oaks

“…Nonetheless, agreement between both methods was rather high (87%), and branching ratio may still be recognised a simple and useful 340 measure of TF. Furthermore, inclusion of the branch and stem shape metrics (Moulia et al, 2019;Moulia & Fournier, 2009) in the quantitative analysis could potentially resolve described ambiguities. Several cues point to a general finding, that the tree-level causes of fork formation dominated here over the shoot-level (traumatic) ones.…”

“…Here, the measured diameters best disentangled the investigated branching habits. Second, trees control their posture as a whole (Moulia et al, 2019), 365 and as they grow large, with heavy branches, the posture control must be an important issue. Stable patterns in branching systems may be found in even much older trees than those studied here .…”

Spatio-temporal kinematic analysis of shoot gravitropism in <i>Arabidopsis thaliana</i>

“…A major advantage of a theoretical approach is that mechanical parameters can be systematically changed to predict what happens with the filament-shaped material. Previous studies (Chelakkot and Mahadevan 2017) were able to characterize various types of bending processes by changing the dimensionless parameters that indicate the bending strength and the balance between growth, elasticity, and gravity (Chelakkot and Mahadevan 2017;Moulia et al 2019). Thus, the theoretical model might explain mechanical aspects of shoot gravitropism that cannot be observed in experiments.…”