Amyloplast sedimentation dynamics in maize columella cells support a new model for the gravity-sensing apparatus of roots

Quantitative analysis of statolith sedimentation behavior was accomplished using videomicroscopy of living columella cells of corn (Zen mays) roots, w hich displayed no systematic cytoplasmic streaming. Following 90 degrees ro tation of the root, the statoliths moved downward along the distal wall and then spread out along the bottom with an average velocity of 1.7 mum min(- 1). When statolith trajectories traversed the complete width or length of t he cell, they initially moved horizontally toward channel-initiation sites and then moved vertically through the channels to the lower side of the reo riented cell where they again dispersed. These statoliths exhibited a signi ficantly lower average velocity than those sedimenting on distal-to-side tr ajectories. In addition, although statoliths undergoing distal-to-side sedi mentation began at their highest velocity and slowed monotonically as they approached the lower cell membrane, statoliths crossing the cell's central region remained slow initially and accelerated to maximum speed once they r eached a channel. The statoliths accelerated sooner, and the channeling eff ect was less pronounced in roots treated with cytochalasin D. Parallel ultr astructural studies of high-pressure frozen-freeze-substituted columella ce lls suggest that the low-resistance statolith pathway in the cell periphery corresponds to the sharp interface between the endoplasmic reticulum (ER)- rich cortical and the ER-devoid central region of these cells. The central region is also shown to contain an actin-based cytoskeletal network in whic h the individual, straight, actin-like filaments are randomly distributed. To explain these findings as well as the results of physical simulation exp eriments, we have formulated a new, tensegrity-based model of gravity sensi ng in columella cells. This model envisages the cytoplasm as pervaded by an actin-based cytoskeletal network that is denser in the ER-devoid central r egion than in the ER-rich cell cortex and is linked to stretch receptors in the plasma membrane. Sedimenting statoliths are postulated to produce a di rectional signal by locally disrupting the network and thereby altering the balance of forces acting on the receptors in different plasma membrane reg ions.