Periodic Reporting for period 4 - PLANTMOVE (Plant movements and mechano-perception: from biophysics to biomimetics)
Reporting period: 2020-01-01 to 2020-06-30
(i) How mechanical stimuli are perceived and transported within the plants?
(ii) How plants sense and respond to gravity?
(iii) How plants perform rapid motion?
Several important results were obtained during the project. First, we discovered what could be a new mode of long-distance communication in plants based on hydraulic signals induced by mechanical deformations. We have also explained the remarkable sensitivity of plants to gravity by linking the macroscopic plant response to the sensor mechanics at the cellular level, which involve tiny grains agitated by the cell activity. This knowledge was then used to address the flow of colloidal suspensions, during which we revealed the origin of the dramatic shear-thickening observed in cornstarch or other dense suspensions (‘Oobleck’ effect). Finally, we deciphered the intrinsic actuation mechanism of the iconic carnivorous plant Venus flytrap, solving a longstanding puzzle dating back to Darwin’s time.
The second part of the project concerned plants gravisensing. We first studied the macroscopic gravitropic response of shoots to different level of gravity and inclination using a centrifugal set-up. The response was shown to be sensitive only to inclination (sine law) but not to the gravitational force as previously believed, which lead us to propose a new scenario of graviperception: the position-sensor hypothesis (Chauvet at al Sci. Rep 2016, Pouliquen et al, Phys. Biol 2017). To validate this scenario, we studied the motion of the statoliths (the grains at the origin of gravity detection) in the gravisensing cells. The striking result was that, unlike a classical granular medium, statoliths move and flow like a liquid even at very low angles of inclination. Experiments biomimetic cells revealed that this behavior comes from the strong agitation of the statoliths, whose origin is biological (involving acto-myosin), and not thermal (Bérut et al PNAS 2018, Bizet et al in preparation). We then extended our work to transient stimulation (inclination) and revealed the existence of a memory process in the gravitropic signaling pathway, independent of statolith dynamics. This led us to build a mathematical model that unifies the different laws found in the literature (Chauvet et al J. Exp. Bot 2019).
The third part of the project was about rapid movements and fast actuation in plants (Forterre et al Eur. News 2016). We first unveiled the intrinsic dynamics of closure of the Venus flytrap and showed that its timescale was too short to be explained by a water transport across the traps, as previously proposed. We then probed in-situ the mechanical response of the trap using a micro-indenter and showed that closure is triggering by a rapid softening of the outer layer, providing a generic mechanism for rapid actuation in plants (Ryu et al, in preparation).
Finally, inspired by our work on plant gravitropism, we study the flow of passive Brownian granular piles and found that, unlike a macroscopic granular material, the medium does not stop at a finite pile angle, but slowly creeps until its free surface becomes horizontal—a result we rationalize within a simplified model (Bérut et al Phys Rev Lett 2019). By using the suspension avalanche angle as a proxy for interparticle friction, we also provided the first experimental evidence of the frictional transition scenario proposed to explain the dramatic shear-thickening observed in some dense suspensions (Clavaud et al, PNAS 2017). We confirmed this result by designing an original pressure-imposed rheometer suitable for studying colloidal suspensions (Clavaud et al J Rheol 2020). During this work, we unexpectedly found that viscous dense suspensions exhibit hysteresis of their avalanche angle, while it was previously believed that inertia was required to observe this phenomenon in granular materials (Perrin et al Phys Rev X 2019).