Cellular transduction of mechanical oscillations in plants by the plasma-membrane mechanosensitive channel MSL10.

Plants spend most of their life oscillating around 1-3 Hz due to the effect of the wind. Therefore, stems and foliage experience repetitive mechanical stresses through these passive movements. However, the mechanism of the cellular perception and transduction of such recurring mechanical signals remains an open question. Multimeric protein complexes forming mechanosensitive (MS) channels embedded in the membrane provide an efficient system to rapidly convert mechanical tension into an electrical signal. So far, studies have mostly focused on nonoscillatory stretching of these channels. Here, we show that the plasma-membrane MS channel MscS-LIKE 10 (MSL10) from the model plant Arabidopsis thaliana responds to pulsed membrane stretching with rapid activation and relaxation kinetics in the range of 1 s. Under sinusoidal membrane stretching MSL10 presents a greater activity than under static stimulation. We observed this amplification mostly in the range of 0.3-3 Hz. Above these frequencies the channel activity is very close to that under static conditions. With a localization in aerial organs naturally submitted to wind-driven oscillations, our results suggest that the MS channel MSL10, and by extension MS channels sharing similar properties, represents a molecular component allowing the perception of oscillatory mechanical stimulations by plants.

Plant vibrations at all scales: a review.

Plant vibrations is a wide subject that covers topics ranging from the swaying of trees under wind to elastic waves made by an insect on a leaf to communicate with its neighbors. For this reason, the state of the art is somehow fragmented over several communities. This review aims at giving a general overview of the main results and challenges in plant vibrations. Several scales are considered, from the very small and local, in leaves or fruits, to large canopies of many plants.

Foliage motion under wind, from leaf flutter to branch buffeting.

The wind-induced motion of the foliage in a tree is an important phenomenon both for biological issues (photosynthesis, pathogens development or herbivory) and for more subtle effects such as on wi-fi transmission or animal communication. Such foliage motion results from a combination of the motion of the branches that support the leaves, and of the motion of the leaves relative to the branches. Individual leaf dynamics relative to the branch, and branch dynamics have usually been studied separately. Here, in an experimental study on a whole tree in a large-scale wind tunnel, we present the first empirical evidence that foliage motion is actually dominated by individual leaf flutter at low wind velocities, and by branch turbulence buffeting responses at higher velocities. The transition between the two regimes is related to a weak dependence of leaf flutter on wind velocity, while branch turbulent buffeting is strongly dependent on it. Quantitative comparisons with existing engineering-based models of leaf and branch motion confirm the prevalence of these two mechanisms. Simultaneous measurements of the wind-induced drag on the tree and of the light interception by the foliage show the role of an additional mechanism, reconfiguration, whereby leaves bend and overlap, limiting individual leaf flutter. We then discuss the consequences of these findings on the role of wind-mediated phenomena.

Mechanical Criterion for the Rupture of a Cell Membrane under Compression.

We investigate the mechanical conditions leading to the rupture of the plasma membrane of an endothelial cell subjected to a local, compressive force. Membrane rupture is induced by tilted microindentation, a technique used to perform mechanical measurements on adherent cells. In this technique, the applied force can be deduced from the measured horizontal displacement of a microindenter's tip, as imaged with an inverted microscope and without the need for optical sensors to measure the microindenter's deflection. We show that plasma membrane rupture of endothelial cells occurs at a well-defined value of the applied compressive stress. As a point of reference, we use numerical simulations to estimate the magnitude of the compressive stresses exerted on endothelial cells during the deployment of a stent.

Turgidity-dependent petiole flexibility enables efficient water use by a tree subjected to water stress.

Water stress is a major cause of tree mortality. In response to drought, leaves wilt due to an increase in petiole flexibility. We present an analytical model coupling petiole mechanics, thermal balance, and xylem hydraulics to investigate the role of petiole flexibility in protecting a tree from water stress. Our model suggests that turgidity-dependent petiole flexibility can significantly attenuate the minimal xylem pressure and thus reduce the risk of cavitation. Moreover, we show that petiole flexibility increases water use efficiency by trees under water stress.

Comment on "Critical wind speed at which trees break".

Virot et al. [E. Virot et al., Phys. Rev. E 93, 023001 (2016)10.1103/PhysRevE.93.023001] assert that the critical wind speed at which ⩾50% of all trees in a population break is ≈42 m/s, regardless of tree characteristics. We show that empirical data do not support this assertion, and that the assumptions underlying the theory used by Virot et al. are inconsistent with the biomechanics of trees.

Wind and gravity mechanical effects on leaf inclination angles.

In a tree, the distribution of leaf inclination angles plays an important role in photosynthesis and water interception. We investigate here the effect of mechanical deformations of leaves due to wind or their own weight on this distribution. First, the specific role of the geometry of the tree is identified and shown to be weak, using models of idealized tree and tools of statistical mechanics. Then the deformation of individual leaves under gravity or wind is quantified experimentally. New dimensionless parameters are proposed, and used in simple models of these deformations. By combining models of tree geometry and models of leaf deformation, we explore the role of all mechanical parameters on the Leaf Inclination Angle Distributions. These are found to have a significant influence, which is exemplified finally in computations of direct light interception by idealized trees.

Methodological advances in predicting flow-induced dynamics of plants using mechanical-engineering theory.

The modeling of fluid-structure interactions, such as flow-induced vibrations, is a well-developed field of mechanical engineering. Many methods exist, and it seems natural to apply them to model the behavior of plants, and potentially other cantilever-like biological structures, under flow. Overcoming this disciplinary divide, and the application of such models to biological systems, will significantly advance our understanding of ecological patterns and processes and improve our predictive capabilities. Nonetheless, several methodological issues must first be addressed, which I describe here using two practical examples that have strong similarities: one from agricultural sciences and the other from nuclear engineering. Very similar issues arise in both: individual and collective behavior, small and large space and time scales, porous modeling, standard and extreme events, trade-off between the surface of exchange and individual or collective risk of damage, variability, hostile environments and, in some aspects, evolution. The conclusion is that, although similar issues do exist, which need to be exploited in some detail, there is a significant gap that requires new developments. It is obvious that living plants grow in and adapt to their environment, which certainly makes plant biomechanics fundamentally distinct from classical mechanical engineering. Moreover, the selection processes in biology and in human engineering are truly different, making the issue of safety different as well. A thorough understanding of these similarities and differences is needed to work efficiently in the application of a mechanistic approach to ecology.

Flow-induced pruning of branched systems and brittle reconfiguration.

Whereas most plants are flexible structures that undergo large deformations under flow, another process can occur when the plant is broken by heavy fluid-loading. We investigate here the mechanism of such possible breakage, focusing on the flow-induced pruning that can be observed in plants or aquatic vegetation when parts of the structure break under flow. By computation on an actual tree geometry, a 20-yr-old walnut tree (Juglans Regia L.) and comparison with simple models, we analyze the influence of geometrical and physical parameters on the occurrence of branch breakage and on the successive breaking events occurring in a tree-like structure when the flow velocity is increased. We show that both the branching pattern and the slenderness exponent, defining the branch taper, play a major role in the breakage scenario. We identify a criterion for branch breakage to occur before breakage of the trunk. In that case, we show that the successive breakage of peripheral branches allows the plant to sustain higher flow forces. This mechanism is, therefore, similar to elastic reconfiguration, and can be seen as a second strategy to overcome critical events, possibly a widespread solution in plants and benthic organisms.

Transport of wetting liquid plugs in bifurcating microfluidic channels.

A plug of wetting liquid is driven at constant pressure through a bifurcation in a microchannel. For a plug advancing in a straight channel, we find that the viscous dissipation in the bulk may be estimated using Poiseuille's law while Bretherton and Tanner's laws model the additional dissipation occurring at the rear and front interfaces. At a second stage, we focus on the behavior of the plug flowing through a T-junction. Experiments show the existence of a threshold pressure, below which the plug remains blocked at the entrance of the junction. Above this required pressure, the plug enters the bifurcation and either ruptures or splits into two daughter plugs, depending on the applied pressure and on the initial length of the plug. By means of geometrical arguments and the previously cited laws, we propose a global model to predict the transitions between the three observed behaviors.