Gravisensors in plant cells behave like an active granular liquid

Abstract

SignificanceThe sensor of gravity in plants consists of tiny starch-rich grains called statoliths that sediment and form miniature granular piles at the bottom of the gravisensing cells. How such a sensor could be a reliable clinometer is unclear, as granular materials are known to display jamming and finite avalanche angles. Here we address this issue by comparing statolith avalanches in plant cells to microfluidic avalanches of Brownian particles in biomimetic cells. We reveal that statoliths behave like a liquid, not a granular material, due to the cell activity that strongly agitates statoliths. Our study elucidates the physical grounds of the high sensitivity of plants to gravity and bridges the active microrheology of statoliths to the macroscopic response of the plant.

The Role of the Primary Cell Wall in Plant Morphogenesis

“…These observations connect gravitropism with a rapid increase of cytosolic Ca 2+ [ 51 ] and the following conclusion [ 91 ]: “Thus, the identified tight link between the cell wall and cell polarity provides the conceptual possibility for regulation of signal fluxes and, ultimately, plant development via signaling from the extracellular matrix.” Such evidence suggests that auxin-based mechanoperception and subsequent root morphogenesis involve the Hechtian growth oscillator. This fundamental phenomenon supersedes textbook dogma and hypotheses in highly contentious and confusing fields [ 49 , 92 , 93 , 94 ] that struggle to disentangle cause from effect. As a prime example, consider the challenge to identify the gravity sensor.…”

Brownian Granular Flows Down Heaps

“…This phenomenon is reminiscent of the relaxation observed in macroscopic granular materials submitted to external perturbations, such as vibration [11,12], thermal cycling [36], shear below yield stress [37], or fluid-injection below the fluidization threshold [38]. It is also analogous to the mechanism found in the gravity sensing cells of plants, where the gravisensors are made of tiny heavy grains, which are agitated by the cytoskeleton activity to promote their mobility under gravity [39]. To describe this creep regime, we have proposed a one-dimensional thermally activated model based on a Kramers' escape rate.…”

Settling for Less: Do Statoliths Modulate Gravity Perception?

“…A recent study by Bérut et al [27] showed that statolith sedimentation in gravistimulated endodermal cells quickly responds even to small changes in bending angle. Statoliths therefore behave less like a pile of stones and more like a liquid.…”

“…It has been hypothesized that cell-generated active (non-Brownian) fluctuations strongly modulate statoliths movements to achieve this effect. Cytoskeletal network dynamics are good candidates for modulating this agitation [27]. Though its regulation has not been linked to changes in the sensitivity of gravitropic responses, it seems possible that local changes in cytoplasmic streaming affect statoliths sedimentation rates.…”