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PLANTMOVE Report Summary

Project ID: 647384
Funded under: H2020-EU.1.1.

Periodic Reporting for period 1 - PLANTMOVE (Plant movements and mechano-perception: from biophysics to biomimetics)

Reporting period: 2015-07-01 to 2016-12-31

Summary of the context and overall objectives of the project

Unlike animals, plants are sessile organisms that cannot escape their environment to develop. As a consequence, they have evolved a remarkable range of strategies to adapt to external stress, forage for food, water and light or to disperse their offspring. Understanding how these organisms - made mostly of water and cellulose and lacking muscle and nerves - achieve these functions is crucial in agronomy and plant science for better managing plant resource. It also offers a promising path for biomimetic designs in engineering and technologies.
The objective of this project, at the crossroad of plant mechanics and soft matter physics, is to address some of the fundamental mechanisms used by plants to perceive mechanical stimuli and generate motion.

The project focuses on three major issues in plant biophysics, which all involve the coupling between a fluid (water in the vascular network or in the plant cell, cellular cytoplasm) and a solid (plant cell wall, starch grains in gravity-sensing cells):
(i) How mechanical stimuli are perceived and transported within the plant and what is the role of hydraulic signals in this long-distance communication?
(ii) How plants sense and respond to gravity and how this response is related to the granular nature of the gravisensor at the cellular level.
(iii) How plants perform rapid motion and what is the role of osmotic motors and cell wall actuation in this process, using the carnivorous plant Venus flytrap as a paradigm for study?

The overall ambition is (1) To unveil key physical mechanisms involved in basic plant functions (growth, mechano-perception, movements) (2) To develop new strategies in soft matter physics inspired by plant sensors and motility mechanisms (fast soft actuator, active transport of suspension). To achieve this program, we adopt a multi-disciplinary and multi-scale approach, which combines experiments on physical systems that mimic some key features of plant tissue and sensors (soft poroelastic materials, sedimentation in the gravi-sensing cells) and in situ experiments on plants at the organ, tissue and cellular level, using advanced mechanical and imaging tools (3D growth kinematics, live cell imaging, micro-and nano-indentation, cell pressure probe). This approach will be made possible thanks to the expertise of the ERC team members in plant biophysics, granular materials and soft matter physics, and to the collaborations established with well-recognised experts in plant physiology, biomechanics and agronomy.

Work performed from the beginning of the project to the end of the period covered by the report and main results achieved so far

The first part of the work performed during this period concerns plant mechano-perception and long-distance signaling in plants. We designed soft artificial branches perforated with longitudinal liquid-filled channels that mimic the basic features of natural (plant) branches and stems. Using a homemade set-up, we have studied the hydraulic response of these biomimetic branches under bending and observed a strong overpressure generated in the channels. Unexpectedly, this amplitude of this response varies quadratically with the bending strain and scales with the beam elasticity. Inspired by the phenomenon of ovalization in thin elastic tubes, we developed a simple model that enables us to quantitatively predict the experiments and to identify the elastic bulk modulus of the branch as the key physical parameter that controls the generation of the pressure pulse. Further experiments conducted on natural tree branches revealed the same phenomenology. Once rescaled by the model prediction, both the biomimetic and natural branches fall on the same master curve, enlightening the universality of the identified mechanism for the generation of hydraulic signals in plants.

The second part of the project concerns plants gravisensing. In a first stage, we have studied the macroscopic gravitropic response of shoots to different level of gravity and inclination using a centrifugal set-up. We have extended our preliminary tests using wheat coleoptiles to species and organs representative of land angiosperm (lentils, sunflower, arabidopsis). Unexpectedly, all gravitropic responses are shown to be independent of the gravity intensity: they only depend on the inclination. This result implies that shoot gravitropism is stimulated by sensing inclination not gravitational force or acceleration as previously believed. This conclusion led us to formulate a new scenario for gravisensing in plants: the position-sensor hypothesis. To validate this scenario, we then studied the motion of the statoliths (the grains at the origin of gravity detection) in the gravisensing cells under inclination and gravity, using again wheat coleoptile as a model system. The striking result is that, unlike a classical granular medium, statoliths flow like a liquid even at very low angles of inclination, due to their strong random agitation. Biomimetic experiments on microfluidic systems (PDMS) using microbeads show that this agitation does not come from Brownian (thermal) motion, but likely arises from the cytoskeleton activity.

The third work addressed in this period concerns the flow and rheology of colloidal suspensions, following our work on statoliths dynamics in the gravisensing cells. Recent models propose that shear thickening in these suspensions is driven by the activation of friction above an onset stress, arising from short range repulsive forces between particles. Testing this scenario represents a major challenge since classical rheological approaches do not provide access to the frictional properties of suspensions. Here we have adopted a new strategy inspired by pressure-imposed configurations in granular flows that specifically gives access to this information. By investigating the quasistatic avalanche angle, compaction, and dilatancy effects in different nonbuoyant suspensions flowing under gravity, we have demonstrated that particles in shear-thickening suspensions are frictionless under low confining pressure. Moreover, we show that tuning the range of the repulsive force below the particle roughness suppresses the frictionless state and also the shear-thickening behavior of the suspension.

Finally, we have started the part of the project on rapid movements and fast actuation in plants, using the Venus flytrap as a paradigm for study. A set-up involving a nano-indentor and a microscope has been developed and preliminary results have been obtained on the variation of the mechanical properties of the trap during closure.

Progress beyond the state of the art and expected potential impact (including the socio-economic impact and the wider societal implications of the project so far)

Plants are sessile organisms. As such, they have developed specific mechanisms to carry information rapidly throughout their body in response to mechanical stimuli without nerves. Recently, it has been proposed that a first stage of this long-distance signaling could be the propagation of hydraulic signals induced by the mechanical deformation of the plant tissue (bending), but the physical mechanism of this hydro-mechanical coupling remains unknown. Here, we have addressed this issue by combining experiments on natural tree branches and soft biomimetic beams. We have revealed a generic non-linear mechanism responsible for the generation of hydraulic pulses induced by bending in poroelastic branches. Our study gives a first physical basis for long-distance communication in plants based on fast hydraulic signals.

Shoots grow up. Even when a plant is accidentally tipped over the shoot rapidly bends up to recover a vertical position. But how do plants feel gravity? We investigated how shoots respond to changes in the direction and intensity of gravity by measuring how plants grew in a centrifuge using time-lapse photography. We found that shoots do not sense the force of gravity or acceleration as previously believed, but instead measure how far they are tilted from the vertical. This contrasts with the otolith system in the internal ear of vertebrates and explains the robustness of the control of growth direction by plants despite perturbations like wind shaking. Our results will help retarget the search for the molecular mechanism linking shifting statoliths to signal transduction. They could also be useful when learning how to grow plants in space.

The high sensitivity of plants to very low inclinations questions the flowing behavior of the tiny starch grains responsible for gravisensing in plant cells. One of the most spectacular phenomena observed in micrometer-size suspensions like cornstarch is the sudden and severe increase in their viscosity above an onset stress. This shear thickening, which has major implications for industry, is a long-standing puzzle in soft-matter physics. Recently, a frictional transition was conjectured to cause this phenomenon. Using experimental concepts from granular physics, we provide direct evidences that such suspensions are frictionless under low confining pressure, which is key to understanding their shear thickening behavior.
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