Root cap size and shape influence responses to the physical strength of the growth medium in Arabidopsis thaliana primary roots.

During the progression of root in soil, root cap cells are the first to encounter obstacles and are known to sense environmental cues, thus making the root cap a potential mechanosensing site. In this study, a two-layered growth medium system was developed in order to study root responses to variations in the physical strength of the medium and the importance of the root cap in the establishment of these responses. Root growth and trajectory of primary roots of Arabidopsis seedlings were investigated using in vivo image analysis. After contact with the harder layer of the medium, the root either penetrated it or underwent rapid curvature, thus enabling reorientation of growth. We initially hypothesized that the root-cap structure would affect apex penetration and reorientation, with pointed caps facilitating and domed caps impeding root penetration. This hypothesis was investigated by analysing the responses of Arabidopsis mutants with altered root caps. The primary root of lines of the fez-2 mutant, which has fewer root-cap cell layers and a more pointed root cap than wild-type roots, showed impaired penetration ability. Conversely, smb-3 roots, which display a rectangular-shaped cap, showed enhanced penetration abilities. These results, which contradict our original hypothesis, reveal a role for resistance to buckling in determining root penetration abilities.

Nondestructive and Fast Vibration Phenotyping of Plants.

The frequencies of free oscillations of plants, or plant parts, depend on their geometries, stiffnesses, and masses. Besides direct biomechanical interest, free frequencies also provide insights into plant properties that can usually only be measured destructively or with low-throughput techniques (e.g., change in mass, tissue density, or stiffness over development or with stresses). We propose here a new high-throughput method based on the noncontact measurements of the free frequencies of the standing plant. The plant is excited by short air pulses (typically 100 ms). The resulting motion is recorded by a high speed video camera (100 fps) and processed using fast space and time correlation algorithms. In less than a minute the mechanical behavior of the plant is tested over several directions. The performance and versatility of this method has been tested in three contrasted species: tobacco (Nicotiana benthamian), wheat (Triticum aestivum L.), and poplar (Populus sp.), for a total of more than 4000 data points. In tobacco we show that water stress decreased the free frequency by 15%. In wheat we could detect variations of less than 1 g in the mass of spikes. In poplar we could measure frequencies of both the whole stem and leaves. The work provides insight into new potential directions for development of phenotyping.

A new scenario for gravity detection in plants: the position sensor hypothesis.

The detection of gravity plays a fundamental role during the growth and evolution of plants. Although progress has been made in our understanding of the molecular, cellular and physical mechanisms involved in the gravity detection, a coherent scenario consistent with all the observations is still lacking. In this special issue article, we discuss recent experiments showing that the response to inclination of shoots is independent of the gravity intensity, meaning that the gravity sensor detects an inclination and not a force. This result questions some of the commonly accepted hypotheses and leads to propose a new 'position sensor hypothesis'. The implications of this new scenario are discussed in light of the different observations available in the literature.

Effect of plant interaction on wind-induced crop motion.

Plant motion due to wind affects plant growth, a phenomenon called thigmomorphogenesis. Despite intensive studies of the turbulence over plant canopies, the study of plant motion induced by wind has often been limited to individual trees or cereal plants. Few models of global canopy motions are available. Moreover the numerical analysis of models that are based on individual stems becomes time consuming when dealing with crops. A model of motion within the canopies is proposed here using a wave propagation equation within a homogenized continuous medium, and a forcing function representing turbulent gusts advected over the canopy. This model is derived from a discrete model of a set of plant shoots represented as individual oscillators, including elastic contacts between shoots. Such contacts induce nonlinearities into the wave equation. A new experimental method to measure stem dynamical properties and elastic collision properties is presented with an illustration on alfalfa stems. Results obtained modeling plant motions in an alfalfa crop are presented.

Biomechanical study of the effect of a controlled bending on tomato stem elongation: global mechanical analysis.

An experiment was designed to apply a controlled bending to a tomato stem and simultaneously to measure its effect on stem elongation. Stem elongation was measured over 2 d until steady and equal rates were obtained for the control and the treated plants. Thereafter, the basal part of the stem was submitted to a transient controlled bending at constant displacement rate using a motorized dynamometer. After load removal, stem elongation was again measured for 2 d. The tested plants were mature (height visible internodes) and only the basal part of the stem, which had already finished elongation, was loaded (hypocotyl and the first three internodes). A few minutes after the application of bending, elongation stopped completely for 60 min. Thereafter it took 120-1000 min to recover a rate of elongation similar to the control. The growth response was exclusively due to the bending of the basal part of the stem. It was shown that the side mechanical perturbations on the roots and on the stem tissues interacting directly with the clamp were not significantly involved on the elongation response. These results give evidence for mechanical perception and plant signalling from the basal stem to the upper elongating zone. However, none of the variables characterizing the global mechanical state of the bent part of the stem (i.e. the maximal force, bending moment, inclination, mean curvature of the stem, stored mechanical energy) could quantitatively explain the variability of the growth response. A more local mechanical analysis is therefore needed to elucidate how the mechanical stimulus is perceived.

Biomechanical study of the effect of a controlled bending on tomato stem elongation: local strain sensing and spatial integration of the signal.

In a previous paper it has been demonstrated that tomato stems, submitted to a controlled basal bending, had a reduced terminal primary elongation, indicating mechanosensing and intra plant signalling. The 'intensity' of the growth response, as measured by the time to recover an elongation rate similar to the control, varied hugely between plants. However, no relation was found between the intensity of this response and the mechanical variables characterizing the global mechanical state of the stem. In this paper, a local analysis of mechanical state of each bent stem is performed in the context of beam theory. The spatial distributions of local variables all along the stem (curvature, bending moment, strains and stresses) are established. The validity of hypotheses underlying the mechanical analysis is demonstrated. To investigate the relationships between the mechanical stimulus and the growth response, a novel biomechanical analysis based on spatial integration of the mechanical stimulus is presented. It revealed that the mechanosensing is local and scattered through the stem and that the variability of the growth response is only explained by the integrals of the longitudinal strain field.

Leaves as Shell Structures: Double Curvature, Auto-Stresses, and Minimal Mechanical Energy Constraints on Leaf Rolling in Grasses.

Grass leaves are natural examples of shell structures because they are thin and display a double curvature. An important mechanical property of shells is that changes in longitudinal and transverse curvatures are not independent. The basis of this mechanical coupling is presented using simple diagrams. The relevance of the structural constraints for the processes of hydronastic rolling and developmental unrolling in grass leaves is then reviewed. I show that mechanical constraints can explain a large part of the genetic and developmental variability of hydronastic rolling in grasses, without reference to specific anatomic features such as bulliform cells. Mechanical analysis of a rolled maize mutant also revealed that developmental unrolling is not limited to a pure transverse expansion of hinge cells and involves both longitudinal and transverse dimensional changes in the upper epidermis. Interest in using mechanical models as a tool to reveal structural interactions at the tissue and organ level is discussed, and the importance of Paul Green's biophysical approach to the study of plant morphogenesis is emphasized.

Biomechanical analysis of the Rolled (RLD) leaf phenotype of maize.

The pleiotropic effects of the Rld1-O/+ mutation of Zea mays (Poaceae) on leaf phenotype include a suppression of normal transverse unrolling, a reversed top/bottom epidermal polarity, and an apparently straighter longitudinal shape. According to engineering shell theory, there might be mechanical coupling between transverse and longitudinal habit, i.e., the leaf rolling itself might produce the longitudinal straightening. We tested this possibility with quantitative curvature measurements and mechanical uncoupling experiments. The contributions of elastic bending under self weight, mechanical coupling, and rest state of leaf parts to the longitudinal and transverse habit were assessed in Rld1-O/+ mutants and a population of sibling +/+ segregants. Elastic bending and curvature coupling are shown to be relatively unimportant. The Rld1-O/+ mutation is shown to alter not only the unrolling process, but also the developmental longitudinal curving in the growing leaf, leading to a straighter midrib and a rolled lamina. The Rld1-O/+ mutant is thus a suitable model to study the relation between tissue polarity and differential curvature development in the maize leaf. Since on the abaxial side of the leaf, more abundant sclerenchyma is found in +/+ than in Rld1-O/+, a gradient in sclerification may contribute to the development of midrib curvature.