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Plant Physiol, February 2001, Vol. 125, pp. 1045-1060
Amyloplast Sedimentation Dynamics in Maize Columella Cells
Support a New Model for the Gravity-Sensing Apparatus of
Roots1
Thomas L.
Yoder,
Hui-qiong
Zheng,
Paul
Todd, and
L. Andrew
Staehelin*
Department of Astronautical Engineering, United States Air Force
Academy, Colorado Springs, Colorado 80840 (T.L.Y.); BioServe Space
Technologies Center, Department of Aerospace Engineering Sciences,
University of Colorado, Boulder, Colorado 80309-0429 (T.L.Y., P.T.);
MCD Biology, University of Colorado, Boulder, Colorado 80309 (H.-q.Z.,
L.A.S.); and Chemical Engineering, University of Colorado, Boulder,
Colorado 80309 (P.T.)
Quantitative analysis of statolith sedimentation behavior was
accomplished using videomicroscopy of living columella cells of corn
(Zea mays) roots, which displayed no systematic
cytoplasmic streaming. Following 90° rotation 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 µm
min 1. When statolith trajectories traversed the complete
width or length of the cell, they initially moved horizontally toward
channel-initiation sites and then moved vertically through the channels
to the lower side of the reoriented cell where they again dispersed.
These statoliths exhibited a significantly lower average velocity than those sedimenting on distal-to-side trajectories. In addition, although
statoliths undergoing distal-to-side sedimentation 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 reached a
channel. The statoliths accelerated sooner, and the channeling effect
was less pronounced in roots treated with cytochalasin D. Parallel
ultrastructural studies of high-pressure frozen-freeze-substituted
columella cells 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 which the individual, straight,
actin-like filaments are randomly distributed. To explain these
findings as well as the results of physical simulation experiments, we
have formulated a new, tensegrity-based model of gravity sensing in
columella cells. This model envisages the cytoplasm as pervaded by an
actin-based cytoskeletal network that is denser in the ER-devoid
central region than in the ER-rich cell cortex and is linked to stretch
receptors in the plasma membrane. Sedimenting statoliths are postulated to produce a directional signal by locally disrupting the network and
thereby altering the balance of forces acting on the receptors in
different plasma membrane regions.
1
This research was supported by the National
Aeronautics and Space Administration (grant nos. NAG 5-3967 and NCC
8-131), University of Colorado, Boulder.
*
Corresponding author; e-mail staeheli{at}spot.colorado.edu; fax
303-492-7744.
© 2001 American Society of Plant Physiologists
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