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.
Highlights
Plants can sense and redirect their growth in response to gravity (Darwin, 1907)
We have focused our studies on the response of statoliths to the gravitational force in the central tier (S2) cells of growing roots reoriented up to angles of 1358
The findings reported here are representative of the light microscopic recordings of >50 roots and on the analysis of ;20 roots preserved by high-pressure freezing for electron microscopy
Summary
The sites of gravity perception in plant roots are columella cells. These specialized sensory cells function as statocytes, which are cells that can both detect and respond to the gravitational force (Sack, 1991; Sievers et al, 1991; Kiss, 2000; Boonsirichai et al, 2002). The columella cells are the only cells in roots that exhibit structural polarity with respect to gravity and can transmit the sensory information related to the gravitational force to the root elongation zone (Driss-Ecole et al, 2003). Statoliths, specialized starch-containing plastids (amyloplasts), primarily respond to the force of gravity. According to the starch statolith hypothesis (Haberlandt, 1900; Nemec, 1900), displacement of the statoliths in the gravitational field provides a means for converting the gravitational potential energy into sensor-
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