How to make a centriole or basal body (Iris Diaphragm Model).
[See ref 12,
The microtubular skeleton of centrioles and basal bodies is characterized by the following features:
Their formation has frequently been associated with the following observations
- Cylindrical structure
- Taper of the cylinder
- Ninefold rotational symmetry
- Blades composed of one complete and two incomplete microtubules
- Convex shape of the blades
- Pitch of the blades
- Clockwise rotational slant of the blades seen from the distal end
- The increasingly tangential slant of the blades towards the distal end.
The main feature of the model is its reduction of the universal and quite complex geometry of centrioles and basal bodies to only four basic numbers.
It is described in much greater detail and with the pertinant references in ref 12:
- Fibrous coils of - 120 nm diameter have frequently been seen to precede centriole and basal body formation
- The inner and outer diameter grows during maturation of centrioles and basal bodies
- The initially radial slant of the blades turns more tangential as centrioles and basal bodies mature
- The slant of the blades is more tangential at the distal than at the proximal end.
- Connecting fibers appear to span the distance between adjacent blades in centrioles and basal bodies
- The A tubule of the forming blades is the first of the three blade microtubules to grow in length, followed by the B and C tubule
For example, the bud structure results from the microtubular radius and the ninefold symmetry. The blade curvature is a consequence of the radius and the 13-fold symmetry of the microtubules. The arm structure
and location of the hinges follows from the microtubular radius, the ninefold symmetry, and the number 4 of the segments covered by the arm, and so forth.
- the radius of microtubules (12 nm),
- the rotational symmetry of centrioles (ninefold),
- the rotational symmetry of microtubules (13-fold), and
- the number of segments of the initial ring structure covered by the arm (four segments).
We assume that the formation of a centriole (basal
body) begins with a ring of nine short microtubules or
precursors to microtubules spaced in a wall-to-wall configuration in the densest possible packing. The second and third row conists of incomplete microtubules as in actual centrioles.
This structure will be called the bud.
Based on a microtubular radius of = 12 nm, the bud
diameter D = 94nm. The bud is likely to resemble a coil of fibers that hold the
Fig.1. Bud formation by adding in the form of densest packing 2 rows of Incomplete microtubules (precursors)to an initial ring of 9 microtubules (precursor)
Assuming that centriolar microtubules and basal body microtubules are composed of 13 protofilaments,
like ordinary microtubules, important constraints on the shape of the future blades result. For example, the B
tubule must share two of the protofilaments with the A tubule. Since the number 13 of protofilaments
is odd, the C tubules cannot be attached along the straight line that connects the centers of A and B. It must turn aside in order to share the protofilaments.
The resulting triplet is curved similar to the shape of blades of actual centrioles and basal bodies. The blade curvature can be described
by the angle τ, which measures how much the center C of the C tubules is shifted away from the midline
connecting the A and B tubules.
There is a second possibility to attach the C tubule.In this case, the angle of the blade curvature is 3τ.
In addition to these two possibilities, the blade curvatures
could assume values of -τ and -3τ, which correspond
to the mirror images of the blade structures described
above. Ultimately, these blade curvatures would
require to mirror image every other structure of the bud,
hence the entire centriole structure. However, mirror image centrioles have never been observed.
Fig.2. Two possible ways of connecting 3 microtubules with shared protofilaments (black dots. )
Formation of the swivel arms.
A major postulate of the model is the formation of fibrous arms that extend around the perimeter of the bud along 4 microtubular diameters. One of the nine arms is
drawn in red as a polygon of 4 segments that stretch
from center to center of five consecutive microtubular
precursors. The number of segments covered by each
arm is essential for the model. If one changes it to three
or five, the resulting structures are markedly different
from actual centrioles and basal bodies.
The model assumes that each of the nine arms is
rigidly connected to the three specific microtubular precursors drawn in red ('blade')
Thus, it divides the bud into nine identical structures, called
swivel arms, one of which is drawn in red. The
free end of each arm is assumed to be able to swivel
around a hinge. It should be noted that each hinge coincides
with the center of one of the microtubular precursors of
The main idea of the iris diaphragm model of
centriole (and basal body) formation is expressed in the
following two postulates:
- The nine hinges remain fixed in their relative position by an assumed special
- The nine arms remain rigid while swiveling around their hinges (marked 'swivel point'). The formation of the arm and its connection to the
three future blades requires a template. Therefore, one may prefer to combine the two postulates of a bud structure and of nine swiwel arms into one postulate,
i.e., that that the bud and the arms are formed together by
a template of appropriate shape and dimensions. We will
show that the known microtubular skeleton results from
the above postulates in surprisingly accurate detail.
Fig.3. Formation of rigid swivel arms that connect the blades with the centers of 4 innermost microtubules (precursors)in the bud. One is drawn in red.
Unfolding of the bud
The model postulates that each rigid arm will rotate in only one direction around its hinge,namely clockwise.
Counterclockwise rotation would result in a compression
of the microtubular precursors beyond their densest
packing which is not possible. By contrast, the clockwise
rotation of the arms opens up the array similar to the
opening of the individual segments of an iris diaphragm.
Fig.4. Unfolding of the bud to form a mature centriole by each arm swiveling around its hnge. )
The necessity of connectors between blades
Consecutive blades have to be connected by
flexible fibers (connector) whose length corresponded to
the maximal distance between adjacent blades. Otherwise the swiveling arms may get entangled. Mechanical model demonstrated how the connectors prevented the tangle: If a
blade approached the preceding one, it had to stretch the
connector behind it, thus pulling up the rear blade. This,
in turn, pulled up the blade 2 places behind it, and so
forth, all around the circle, until the pull had reached the
blade in front, which now pulled away from the approaching
blade and cleared the space. In this way, entangling
of the arms was impossible and an even opening
of the array guaranteed. Many such connectors must be
attached along the entire lengths of the blades in order to
Consistent with the model, such connectors are
regularly seen between the blades of centrioles and basal
Fig.5. Connectors between the blades.(a) Entangling between blades, if their swivel speed is not exactly matched. (b)Prevention of entanglement by connectors (white lines; arrow). (c) Eletron micrograph of the connectors of a basal body (arrow)
Axial growth of the blade microtubules
As is well known from the literature, the pro-centrioles and pro-basal bodies grow
in length while their diameter increases. .
The first microtubule to grow is the A tubule, followed
by the B and C tubules.
According to our model, the arms are still in the
process of swiveling while the blade microtubules grow
in lengt. We assumes that the
blade tubules grow downward; i.e., the array of arms
will eventually become the distal end of the mature centriole
or basal body. This assumption is not vital for the
validity of the model but, as pointed out in the next
section, it allows a simple explanation for the pitch of the
blades, the taper of the entire structure, and perhaps even
the swiveling mechanism itself.
Pitch of the blades and taper of the centriole
The model assumes that the swiveling action occurs at the future distal
end of the centriole. Consequently, it is reasonable to
assume that mechanical resistance of the surrounding cytoplasm
will cause the blades at the proximal end to lag
behind in their rotation. The lag will not correspond to a
large difference in swivel angle because the connectors
all along the blades can be expected to couple the movement
of the blades reasonably well to each other. Nevertheless,
a lag of some size must be expected, and it
entails a number of important consequences.
For example, (1) the blades are pitched by 10-15o as in actual
centrioles and basal bodies (2) the diameter of the proximal end is larger than
the diameter of the distal end ('taper' )
Fig.6. Formation of pitched blades and the taper. (a) Electron micrograph of an oblique section through a centriole to show the pitch of the blades. (b)Taper and the pitch of the blades of centrioles and basal bodies as a resultof a lag of the swiveling at the distal end compared to the basal end
Fig.7. Conceivable way to create the initial ring of 9 microtubules (precursors)by templating them from the densest packing of circles.