Statolith Sedimentation Kinetics and Force Transduction to the Cortical Endoplasmic Reticulum in Gravity-SensingArabidopsisColumella Cells  

Abstract

The starch statolith hypothesis of gravity sensing in plants postulates that the sedimentation of statoliths in specialized statocytes (columella cells) provides the means for converting the gravitational potential energy into a biochemical signal. We have analyzed the sedimentation kinetics of statoliths in the central S2 columella cells of Arabidopsis thaliana. The statoliths can form compact aggregates with gap sizes between statoliths approaching <30 nm. Significant intra-aggregate sliding motions of individual statoliths suggest a contribution of hydrodynamic forces to the motion of statoliths. The reorientation of the columella cells accelerates the statoliths toward the central cytoplasm within <1 s of reorientation. During the subsequent sedimentation phase, the statoliths tend to move at a distance to the cortical endoplasmic reticulum (ER) boundary and interact only transiently with the ER. Statoliths moved by laser tweezers against the ER boundary experience an elastic lift force upon release from the optical trap. High-resolution electron tomography analysis of statolith-to-ER contact sites indicate that the weight of statoliths is sufficient to locally deform the ER membranes that can potentially activate mechanosensitive ion channels. We suggest that in root columella cells, the transduction of the kinetic energy of sedimenting statoliths into a biochemical signal involves a combination of statolith-driven motion of the cytosol, statolith-induced deformation of the ER membranes, and a rapid release of kinetic energy from the ER during reorientation to activate mechanosensitive sites within the central columella cells.

Effects of mechanostimulation on gravitropism and signal persistence in flax roots

“…statocytes. 40 Although flax and Arabidopsis may have similar sedimentation kinetics, the saturation of the graviresponse after 10 min is also supported by our observation of maximal curvature after 10 min reorientation. Investigations with excess starch mutants indicate that gravisensing is not saturated 41 and studies of the presentation time show that much shorter reorientation times than signal saturation are sufficient to induce curvature and suggest that amyloplast sedimentation is not necessary for the initiation of gravitropism.…”

“…Investigations with excess starch mutants indicate that gravisensing is not saturated 41 and studies of the presentation time show that much shorter reorientation times than signal saturation are sufficient to induce curvature and suggest that amyloplast sedimentation is not necessary for the initiation of gravitropism. 40 While earlier studies focused on the detection limit (presentation time) that is sufficient to induce curvature, 28,35 this study demonstrates saturation of the gravity stimulus likely coincides with the amyloplast sedimentation. Studies on gravity-induced gene expression, hormone redistribution and signal transduction should use this time as reference point for maximal effects of a (single) acceleration or reorientation stimulus.…”

Root gravitropism is regulated by a transient lateral auxin gradient controlled by a tipping-point mechanism

“…This result may represent the angle statoliths move within columella cells at the midpoint of a root gravitropic response (33). Live imaging revealed that the initial 908 gravity stimulus causes statoliths to be displaced from the rootward (apical) end of columella cells to the new lower cell wall (26). However, at a root angle of ∼408 statoliths return to the rootward face of columella cells (Fig.…”

“…Specialized starch-filled organelles termed statoliths move within 5 min of a gravity stimulus in gravity-sensing columella cells (26,27). It has been proposed that statolith sedimentation onto the lower side of these cells triggers the formation of the lateral auxin gradient (28,29).…”

The root as a drill

“…5,6 The physical signal of statolith sedimentation is converted to physiological information by a mechanism still to be fully deciphered, and transmitted to the root elongation zone located at a distance from the root cap. Several constituents of this physiological response have been identified including changes in pH, reactive oxygen species, Ca +2 induced signaling, and modulation of auxin transport.…”