(see Box 23.

1), values for threshold intensity for Avena

coleoptiles and roots were found to be 1.4 × 10-3 g and
1.4 × 10-4 g. Values calculated for lettuce seedling
hypocotyl and roots in experiments aboard the Salyut 7
spacecraft were 2.9 × 10-3 g and 1.5 × 10-4 g, respectively. It is apparent that many
plants are very sensitive
to gravitational stimulus.
23.2.3 ROOT GRAVITROPISM OCCURS
IN FOUR PHASES
Virtually all of the studies on root gravitropism have
focused on primary roots and have identified four successive phases: perception,
transduction, transmission,
and growth response (Figure 23.11). Although the actual
timing may vary depending on the conditions of the
experiment, the initial perception phase occurs within
perhaps one second of orienting a root off the vertical
and involves biophysical mechanisms (e.g., pressure) for
sensing the direction of gravitational pull. The transduction phase, occurring between 1
and 10 seconds
following reorientation, involves the conversion of the
biophysical single to a biochemical signal. The transmission phase occurs between 10
seconds and 10 minutes
of reorientation and involves a redistribution of auxin
within the root tip. The growth response, due to the
unequal distribution of auxin, causes curvature of the
root toward a more vertical orientation.
23.2.3.1 Gravity is perceived by the columella
cells in the root cap. Gravitropic perception in the
root is localized in the root cap, a thimble-like mass of
cells that covers the tip of the root. The root cap consists
of a central core of cells (the columella) arranged in
regular tiers and one or more outer layers of peripheral
cells. Traditionally, the function of the root cap was
thought to be twofold; it provides physical protection
for the root apical meristem and its peripheral cells
secrete a mucilaginous polysaccharide that lubricates
the path of the growing root.
A third function, that of gravity perception, has
been established by experiments in which the root cap
is wholly or partially surgically removed (Figure 23.12).
Complete removal of the root cap does not interfere with
the elongation of the root but completely abolishes any
gravitropic response. Decapped roots will recover sensitivity to gravity after about 24
hours, which correlates
with the regeneration of a new cap. Surgical experiments
have also indicated that removal of the central core, or
columella, cells caused the strongest inhibition of the
response to gravity. Individual cells or pairs of columella
cells can be selectively removed or ablated (L. ablatus, to
take away) with a nitrogen laser, in conjunction with an
optical microscope. Ablation of the innermost columella
cells has the greatest impact on root curvature, without
affecting overall growth rate of the root (Figure 23.13).
Laser ablation of the root cap peripheral cells, on the
other hand, has no effect on the gravitropic response.
A.
B.
FIGURE 23.12 The role of the root cap in curvature of
vertically oriented roots. (A) Control root. Growth is
uniform when the root cap is left intact. (B) When the
root cap is surgically removed from one-half of the
root, the root grows toward the side with the cap
remaining.
402 Chapter 23 / Tropisms and Nastic Movements: Orienting Plants in Space
S1 S1
CI
CI CI CI
Qc
Qc Qc Qc
S2
S3
S3 S3 S3
S2
S2 S2
S1 S1
FIGURE 23.13 Diagram of an Arabidopsis root cap showing the quiescent center (QC),
columella initials (CI),
and three ranks of columella cells. Colored cells indicate
the cells that are sensitive to gravistimulation, based on
laser ablation experiments. Relative sensitivity is indicated by the intensity of color.
(Based on Perbal and
Driss-Ecole, 2003).
23.2.3.2 Gravity perception involves displacement of starch-filled
amyloplasts. A response to
gravity must almost certainly involve sedimentation
of some physical structure within the cell. F. Noll
was the first to suggest, in 1892, that plants might
sense gravity in a manner similar to some animals.
Crustaceans, molluscs, and many other invertebrates
have gravity-sensing organs called statocysts, small
innervated cavities lined with sensory hairs. Within
the cavity are one or more statoliths, tiny granules of
sand or calcium carbonate that are pulled downward
by gravity. When the statocyst changes position, the
statoliths also shift position, bending the sensory hairs
and sending an action potential to inform the central
nervous system of the change.
In 1900, G. Haberlandt and E. Nemec independently adapted the statolith theory to
account for plant
responses to gravity. Based on careful cytological studies, they proposed the starch-
statolith hypothesis in
which starch grains found in specialized tissues function as statoliths. Statocytes are
cells containing sedimentable starch grains. Tissues that contain statocytes
are known as statenchyma. Support for the statolith
hypothesis was found in earlier reports by Darwin and
others that removal of the root tip, where most of the
starch grains are found, resulted in a loss of gravitropic response. Nonetheless, the
hypothesis was not
universally accepted and over the decades a number of
investigators have attempted to prove or disprove it.
A statolith is not a naked starch grain, but a group
of starch grains contained within a membrane, called an
amyloplast (Figure 23.14). There may be 1 to several
individual grains within an amyloplast and as many as a
dozen amyloplasts in each statocyte. This compares with
the single large grains characteristic of starch storage
organs. Not all amyloplasts in all cells are readily mobile.
In fact, detection of putative statoliths, or readily mobile
amyloplasts, appears to be largely confined to regions of
high gravitropic sensitivity. These include the mass of
columella cells in the central core of the root cap and, in
hypocotyls, a zone of endodermal cells that sheath the
vascular tissues (also referred to as the starch sheath).
Mobile amyloplasts may also be found in the inner
cortical cells of aerial organs and the pulvini, or motor
organs in the nodes of grass stems that are responsive to
gravity.
Any gravity-sensing mechanism involving particle
sedimentation would have to operate with a speed and
sensitivity consistent with the known speed and sensitivity of the response. In the 1960s,
L. J. Audus undertook
a careful examination of various subcellular particles.
Audus concluded that, of all the cellular organelles, only
starch grains have the mass and density to move through
the viscous cytoplasm within known presentation times.
Ultrastructural examination has shown that other cellular organelles, such as the
endoplasmic reticulum,
may become shifted in cells subjected to gravitationa