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Plants are able to sense and respond to minute tilt from the vertical direction of the gravity, which is key to maintain their upright posture during development. However, gravisensing in plants relies on a peculiar sensor made of microsize starch-filled grains (statoliths) that sediment and form tiny granular piles at the bottom of the cell. How such a sensor can detect inclination is unclear, as granular materials like sand are known to display flow threshold and finite avalanche angle due to friction and interparticle jamming. Here, we address this issue by combining direct visualization of statolith avalanches in plant cells and experiments in biomimetic cells made of microfluidic cavities filled with a suspension of heavy Brownian particles. We show that, despite their granular nature, statoliths move and respond to the weakest angle, as a liquid clinometer would do. Comparison between the biological and biomimetic systems reveals that this liquid-like behavior comes from the cell activity, which agitates statoliths with an apparent temperature one order of magnitude larger than actual temperature. Our results shed light on the key role of active fluctuations of statoliths for explaining the remarkable sensitivity of plants to inclination. Our study also provides support to a recent scenario of gravity perception in plants, by bridging the active granular rheology of statoliths at the microscopic level to the macroscopic gravitropic response of the plant.

Gravisensors in plant cells behave like an active granular liquid