Molecular Biology of the Cell by Bruce Alberts, Alexander Johnson, Julian Lewis, David Morgan, Martin Raff, Keith Roberts, Peter Walter by by Bruce Alberts, Alexander Johnson, Julian Lewis, David Morg

1086 Chapter 19: Cell Junctions and the Extracellular Matrix
Microtubules Orient Cell Wall Deposition
An important clue to the mechanism that dictates microfibril orientation came
from observations of the microtubules in plant cells. These are frequently arranged
in the cortical cytoplasm with the same orientation as the cellulose microfibrils
that are currently being deposited in the cell wall in that region. These cortical
microtubules form a cortical array close to the cytosolic face of the plasma membrane,
held there by poorly characterized proteins. The congruent orientation of
the cortical array of microtubules (lying just inside the plasma membrane) and
cellulose microfibrils (lying just outside) is seen in many types and shapes of plant
cells and is present during both primary and secondary cell wall deposition, suggesting
a causal relationship.
This suggestion can be tested by treating a plant tissue with a microtubule-depolymerizing
drug so as to disassemble the entire system of cortical microtubules.
The consequences for subsequent cellulose deposition, however, are not
as straightforward as might be expected. The drug treatment does not disrupt the
production of new cellulose microfibrils, and in some cases cells can continue to
deposit new microfibrils in the preexisting orientation. Any developmental switch
in the orientation of the microfibril pattern that would normally occur between
successive lamellae, however, is invariably blocked. It seems that a preexisting
orientation of microfibrils can be propagated even in the absence of microtubules,
but any change in the deposition of cellulose microfibrils requires that
intact microtubules be present to determine the new orientation.
These observations are consistent with the following model. The cellulose-synthesizing
rosettes embedded in the plasma membrane spin out long cellulose
molecules. As the synthesis of cellulose molecules and their self-assembly into
microfibrils proceeds, the distal end of each microfibril presumably forms indirect
cross-links to the previous layer of wall material, orienting the new microfibril
in parallel with the old ones as it becomes integrated into the texture of the
wall. Since the microfibril is stiff, the rosette at its growing, proximal end has to
move as it deposits the new material. Traveling in the plane of the membrane,
the rosette moves in the direction defined by the way in which the far end of the
microfibril is anchored in the existing wall. In this way, each layer of microfibrils
would tend to be spun out from the membrane in the same orientation as the
layer laid down previously, with the rosettes following the direction of the preexisting
oriented microfibrils outside the cell. Oriented microtubules inside the cell,
however, can force a change in the direction in which the rosettes move: they can
create boundaries in the plasma membrane that act like the banks of a canal to
constrain rosette movement (Figure 19–65). In this view, cellulose synthesis can
occur independently of microtubules; but it is constrained spatially when cortical
microtubules are present to define membrane microdomains within which the
enzyme complex can move.
Figure 19–65 One model of how the
orientation of newly deposited cellulose
microfibrils might be determined by the
orientation of cortical microtubules.
(A) The large cellulose synthase complexes,
or rosettes, are integral membrane
proteins that continuously synthesize
cellulose microfibrils on the outer face of
the plasma membrane. The distal ends
of the stiff microfibrils become integrated
into the texture of the wall, and their
elongation at the proximal end pushes the
synthase complex along in the plane of
the membrane. Because the cortical array
of microtubules is attached to the plasma
membrane in a way that confines this
complex to defined membrane channels,
the orientation of these microtubules—
when they are present—determines the
axis along which the new microfibrils
are laid down. (B, C) Two electron
micrographs show the tight association of
the cortical microtubules with the plasma
membrane. One shows the microtubules
in cross section while the other shows a
microtubule in longitudinal section. Both
emphasize the constant gap of about 20
nm between membrane and microtubule;
the connecting molecules responsible
remain obscure. (B and C, courtesy of
Andrew Staehelin.)
cellulose microfibril being
added to preexisting wall
plasma membrane
(B)
cell wall
microtubules
100 nm
CYTOSOL
(A)
connector
protein
cellulose synthase
complex
microtubule attached
to plasma membrane
0.1 µm
(C)
100 nm