Download The plant cytoskeleton: its significance in plant

Acta Bot. Neerl.
March
39(1),
1990,
1-18
p.
Review
plant cytoskeleton: its significance in plant
The
development
J.
Derksen F.H.A.
Wilms and E.S.
Pierson
ED
Department of Experimental Botany, University ofNijmegen, Toernooiveld,NL-6525
Nijmegen,
The
Netherlands
CONTENTS
Introduction
1
Structure and
General
composition
organization
of the
of the
The
cytoskeleton
in cell
The
cytoskeleton
in
1
cytoskeleton
4
cytoskeleton
and differentiation
morphogenesis
7
12
plant morphogenesis
remarks
Concluding
12
cell differentiation.
Key-words: cytoskeleton, morphogenesis,
INTRODUCTION
The
of
cytoplasm
It
cytoskeleton.
eukaryotic
connects
cells contains
the various
with each other and with the
in
cesses
the
cell,
cell
and other
cytoplasmic
elements of the cell
membrane and is involved in many
plasma
including
three-dimensionalnetwork of filaments: the
a
organelles
division,
morphogenesis,
dynamic
redistribution
of
pro-
surface
components, endo- and exocytosis and the positioning of cytoplasmic elements (reviews:
Dustin 1984; Lackie
1986; Bershadsky & Vasiliev 1988; plants: Traas 1989).
The three major constituents of this system
mediate filaments.
They
can
be
are
microtubules, microfilaments
based
discriminated,
on
their diameter and
and inter-
by
of
means
immunocytochemistry.
The informationconcerning the
animal cells. However,
to
do
justice
to
all studies
been discussed
(1982).
see
For
Fosket
As
plant
as
concerning
extensively by
a recent
review
on
plant
cells
plant cytoskeleton.
&
Hardham
and
biochemistry
seems
increasing,
Literature
(1982),
genetics
scanty when compared
it will
be
not
prior
Hepler (1985)
of plant
possible
to
to
1980 has
and
Lloyd
cytoskeletal proteins
(1989).
cells
are
and cell expansion
immobile,
a
particular plant shape
by polar growth,
within a tissue must
and
structure
following this
i.e.
the
Gunning
the
cell divisionand cell expansion, i.e.
first
in
cytoskeleton
interest has been rapidly
composition
we will
discuss
embryonic, plants
with
STRUCTURE AND
occur
of the
recent
special
in
a
or
on
reference
only
be obtained
of
by
directional
cell death. Thus, cell division
co-ordinated way. Here
cytoskeleton
results
can
specific
eukaryotic
we
shall describe
cells in
general
and
the organization of the cytoskeleton in higher,
to
COMPOSITION
morphogenesis
OF
THE
and cell differentiation.
CYTOSKELETON
Microtubules
Microtubules
are
average external
tubular
structures
with
diameter of about 25
internal diameter of about
an
nm.
They consist of
1
two
15nm and
evolutionally
an
related
2
J.
a-tubulin and
proteins,
each
p-tubulin,
50 000 kD. The microtubularwall is
numbers
that
Protofilamentsconsist of
occur.
and
asymmetrical
are
microtubule all
respect
Microtubules
assumes
—
and
1978)
steady
a
side. Dynamic
microtubules
proposed
with
with
together
mitotic
dynamics
have been described
Borisy 1988).
Tubulins of
et al.
(Cleveland
1980;
continuously
1978), but
explain
some
may
the relative
herbicides
associate
Olmsted
with
in vivo,
as a
as
see
well relate
&
also
may
play
an
with
1
In
nm
dimers in
a
in
10°
a
of
of
to
the
slowly,
of rapidly
eventually
al.
1984). However,
be much
both
at
in
ends,
behave
to
the
the
growing
according
dynamic instability (e.g.
to
cells of
interphase
stable. In such
more
at
disassembling
their
cases
Sammak &
disappearance
occurrence
1986a).
different
evolutionary
flagella (Cavalier-
of a cell wall. This difference
A
of
variety
may also
largely
has been found
proteins
microtubule-associated
proteins
(MAPs)
determine microtubule
elements and organelles.
enzymes in which Ca
2+
et
stability
/calmodulin
al.
1985,
to
to
(review:
and
Their activity appears
& Vallee 1982; Larsson
(Theurkauf
a
of cilia and
microtubules to colchicine and their sensitivity
MAPs
below).
-(-side and disassembly
population
&
The first model
1984).
appear to be less conservative than in animal cells
plant
the
treadmilling (Margolis
which has been attributed to
Mole-Bajer
role
important
—side.
assemble and disassemble. Two
microtubules appear
tempered
cascade of phosphorylating
a
polar proto-
the
shifted about
polarity
the
at
to
association with other cytoskeletal
regulated by
side
are
& Kirschner
mode of
1989),
insensitivity
(Bajer
in
resulting
processes:
appeared
higher plants
Fosket
et
(Salmon
microtubules:
1986,
these
assembly
pressure. This differencemay result from the
Smith
but different
tubulin dimers
long, a-P
P-tubulin
distinct
a
the existence of a
population
a
spindles
of the microtubules
animals, part
show
explain
to
continuous
a
model
dynamic instability
nm
orientation and
same
dynamic instability (Mitchison
state
the
approximately
protofilaments,
direction,
one
-|-side,
of
weight
ET A L.
1984).
instability predicts
microtubules. In
the
oriented in
called the
static elements but
are no
mechanisms have been
molecular
a
made up of 13
chain of about 8
a
Microtubules thus
left-handed helix (Dustin
Wilson
is
protofilaments have the
each other.
to
all
are
filaments. The a-tubulin side
with
generally
DERKSEN
to
its
be
and cAMP
Schulman
et
al.
1985).
Microtubules have
known role in
been related
movement
of
various types of
to
metaphase
involved in the transport of vesicles and
(Dustin
the
and
dynamics
of the
of
are
reticulum
endoplasmic
their well
cilia/flagella, they
neurons
1984; Bershadsky & Vasiliev 1988). Microtubules
organization
Hotani
like in
organelles,
besides
movements:
chromosomes and
can
be
and other animal cells
also involved in
probably
(Chen
& Lee
1988;
Vale &
1988).
Microfilaments
The backbone
protein
of about 42 kD.
of microfilaments is formed
In the filaments actin molecules
double-stranded twisted
rope.
The
Individual microfilaments have
Microfilaments
considered
are
also
to occur.
dynamic
Bershadsky
cells
& Vasiliev
(review;
Staiger
stress
a
diameter of 5-7
and both
fibres,
1988). They
& Schliwa
are
actin which has
piled
major repeat distance is
Microfilaments often
ation like in muscles and
by
1986).
microscopic preparations represent
treadmilling
occur
where
can
nm
in
they
38
in such
a
a
show
a
way
stable
The microfilaments that
actin filaments, which have
a
can
be
a
polarity.
have been
regular organiz-
as
recently
weight
form
13 molecules.
distinct
(reviews:
also form loose bundles, such
to
as
dynamic instability
bundles with
very
molecular
involving
nm,
and
and
large
are
up
Lackie
in many
seen
1986,
plant
in electron
been confirmed
CYTOSKELETON
for
SIGNIFICANCE IN
cells with
plant
filaments
the
of
use
also form more
can
immunological probes
less dense
or
The different types of association
various associated
2+
Ca
/Ca
2+
Actin is
of actin
(Lancelle
filaments and
play
cells
(Condeelis
1987). Plasma-streaming depends
and vesicle-mediated secretion often appear
in Jackson
1982;
reticulum has been
endoplasmic
& Schliwa
1987; Staiger
stability depend
been identified
thought
to
be actin
proteins
1986;
sensitive
are
to
role.
be actin
to
the
on
(Lackie
et
actin filaments. Also
1987).
Actin
1989).
1974; Parthasarathy
on
movements
Kristen
their
now
important regulatory
an
Hepler
&
associated with membranes.
As in microtubules many associated
which thus
regular component of plant
a
& Schliwa
Staiger
1988).
-calmodulin,
3
networks, often
from which numbers have
proteins
& Vasiliev
Bershadsky
DEVELOPMENT
Also the
al.
1985;
organelle
dependent (reviews
of the
organization
dependent (Quader
et
al.
1987).
Intermediatefilaments
Unlike microtubules and
microfilaments, intermediate filaments
geneous, yet evolutionally related, proteins (reviews in Nagle
In animals they
the
eukaryotic
tissue
are
cell in
specific, indicating
al.
1982).
intermediate
proteins,
filaments.
al.
et
been described
isolated
a
spectrin-like
by Goodbody
et
al.
but do
not
by
and
The
protoplasts (Powell
carrot
Goodbody
et
with
al.
to
nm.
Intermediate
These bundles contain
microtubules
plant
(Dawson
from
plant
part of the proteins detected
al.
et
& Yan
1985;
(1988)
membranes.
at
the
a
with animal
intermediate filaments
(1989). Recently, Wang
ankyrin-like protein
an
nm.
immunological homology
distributions of
extraction-resistant
against
filamental organization
a
P-proteins
also be
diameter of 50-100
co-localize
intermediate filamental proteins,
must
Roop 1988).
this system in
have
have
the
Maybe
membrane
plasma
residues
cell
of
fern
spermatozoids
also co-localize with microtubules in immunofluorescent preparations,
1988)
show
to
hetero-
(1989).
Antibodies raised
al.
a
Distinct
is identical
spectrin-like protein
et
first described in
were
of which show
some
They
1989).
recently
(Marc
cells
plant
bundles with
large
number of different
family of
less conservative character
The diameter of individual intermediate filaments is 7-10
filaments form
Hargreaves
1988;
a
Steiner &
general.
Intermediate filaments of
et
a
are
in
phloem
(Marc
perhaps
or
cells form tubular
regarded, by definition,
as
a
&
Gunning 1988). They might
detect
MAPs.
structures
(Cronshaw
et
al.
intermediate filament
plant-specific
1973),
that
system.
Cytoskeleton-associated proteins
The various associated
their
to
organization
be present in animal systems
plants
(Lackie
few have been identified yet.
possible
1n
of microtubules and microfilaments
proteins
and function. Numerous
proteins
are
known
1986; Bershadsky & Vasiliev 1988), but in higher
They
are
summarized in Table I
with their
together
functions.
higher plants,
the existence of an
but the basis for such
Cytoplasmic
a
acto-myosin
concept has been
set as
1987)
and kinesin
but
expect them
to
be
(Vale
et
present
al.
in
1985)
driven system has still
myosin
microtubule-based motors, such
Vallee
we
cytoskeleton-associated
determine
largely
have
as
not
higher plants
as
is
the
yet
not
been proven,
clearly present.
dynein-like
MAP-1C
been established
&
(Paschal
firmly
in
plants,
well.
The latter may mediate the interactions between microtubules and the tubular endo-
plasmic
reticulum
(e.g.
Vale & Hotani
both actins and microtubules
as
1988). Directional
movement
may also
depend
on
shown for the alga Bryopsis (Menzel & Schliwa 1986).
4
J. DERKSEN
Table
1.
ETAL.
Microtubule (MT) and actin filament (AF) associated proteins that have been identifiedin
the cytoplasm of cells of higher plants
Protein
References
Group
MAPs
MT
Cyr
Kinesin
MT
Moscatelli et
&
Palevitz
Calmodulin
MT
Wick et
Possible role
Microtubule bundling
(1989)
al.
(1988)
Force-generating, organelle transport.
al. (1985)
Ca
2+
-binding protein, regulatory
functions
Troponin
Lim
AF/MT
et
al.
2+
Ca
(1986)
-binding protein binds
to
tropomyosin, regulatory functions
Van
Ankyrin
AF
Wang&
Myosin
AF
Vahey et al. (1982)
Parke
Yan
et
Grolig
AF
Spectrin
The
presence
Yan
(1988)
Connecting
spectrin-like proteins
movements
actin to membrane
proteins
indicates that the associations of
those in animal cells.
to
cytoskeletal proteins
of animal cells will be present somehow in
cells.
GENERAL
ORGANIZATION
The
techniques
used
The
organization
of
OF
Electron
microscopy.
microtubules, microfilaments
ditions used,
during
the
compared
Classical electron
the
and
Northcote
problems
1973; Howard &
& Staehelin
1988).
immunological probes
Large
be
can
surfaces
at
The
embedded material (Wilms
cell parts
can
Light microscopy.
against
(Lloyd
et
animal
(IF) probes
al. 1979; Wick
et
al.
of
use
1985).
serial
to
the
con-
depolymerized
contrasted
poorly
cryo-techniques,
can
be
as
to
study
of the
al.
use
of
by
using cleaving
polyethylene glycol (PEG)
1985)
this
may be useful.
procedure
be evolutionally
spatial
&
1986;
Hepler 1989).
obtained
(Hawes
sectioning, though
appear
et
be conditional for the
Also sections of
mounts
(Hereward
1986; Lancelle
Lancelle &
proteins, especially tubulin,
allow
enable visualiz-
soluble components of the
by
may
(e.g.
analyses
Cytoskeletal elements
Immunofluorescent
the
techniques
and whole
using
only
techniques.
be studied.
by
of these
al.
et
1990)
also be studied
antibodies raised
obscured
1979; Emons & Derksen
quantitative
Traas
become
may
the ultrastructural level
allowing
techniques (Traas 1984;
areas can
use
number of
a
actin filaments, may become
are
or
overcome
Aist
using
intermediate filaments, but due
elements
medium,
small
cytoplasm. Moreover, only
Fixation
fibrous
embedding
CYTOSKELETON
microscopical (EM) techniques
and
cytoskeletal elements, especially
procedure
to
THE
elements has been studied
cytoskeletal
ation of
Craig
intracellular
al. (1989)
Wang &
most
membrane proteins
al. (1988)
et
et
of ankyrin-like and
We expect that
to
(1986)
actin with the membranes may be similar
plant
actin
Connecting
Organelle movement, force generation,
al. (1986)
et al.
Tang
(1988)
Larger
is laborious.
conservative
could be used in
organization
plant
and
cells.
in entire cells
1981) and in sections of PEG-embedded material (Hawes &
CYTOSKELETON SIGNIFICANCE
1. Microtubules in root cortex cells of
Fig.
(1984).
Horne
the
longitudinal axis
though
investigation
techniques
ning
are
the two cells
on
the
as
well
almost
are
1000.
x
three-dimensional
(McCurdy
useful for
Traas el al.
the microtubules
right,
of
et
phalloidin (Wulf
of actin
organization
al.
al.
et
filaments,
1988)).
large scale-studies,
but for
detailed analysis
a
required (e.g. Segaar 1990).
microscopy
light microscopic techniques
(CSLM;
of the
dynamics
Quader
e.g.
image photography (e.g.
understanding
helical, in
of fiuorochrome conjugates
of the
extremely
of advanced
use
laser
enhanced
are
are
Magnification:
antibodies have been used
The IF methods
The
of the cell.
The introduction
1985).
allowed
1979)
EM
Lepidium. Immunofluorescence preparation according to
In the left two cells the microtubules
parallel to
5
IN DEVELOPMENT
&
in
Schnepf
Lichtscheidl & Weiss
of the
cytoskeleton
cells such
plant
1986)
1988)
as
and
confocal
scan-
video/computer
will contribute
to a
better
and its interactions with other cellular
structures.
General
organization
Microtubules
microtubules
in
Gunning
present throughout the cytoplasm, but large arrays of parallel cortical
always present,
Hardham
&
microtubules
throughout
are
are
are
the
and
interconnected and
cell
(Lloyd
1984; Traas
thought
1984). Recently
it
to
Derksen, unpublished
data).
If these
interconnected microtubules could
considerable forces
on
not
only
1989;
form
could be
Nicotiana about 50% of the cortical microtubules is
& J.
in vacuolated cells
especially conspicuous
1982; Lloyd
see
an
also
almost
shown
were
withstand strong
determine the
also present
the
at
the
(reviews
cortical
in
of
(H. Kengen
dynein-type
such
but could even
exert
of
forces,
helix
protoplasts
a
their environment.
At the surface of the nucleus microtubule
not
The
uninterrupted
that
organizing
centres
(MTOCs)
initiatemicrotubule assembly after cell division(e.g. Wick & Duniec
do
1).
interconnected
regularly
interconnections
Fig.
organization
plasma
of the cortical
membrane (Gunning
et
microtubular skeleton may self-assemble into
cytoskeleton,
al.
1978)
and
are
present that
1983). They probably
as
nucleating
in anucleate
sites
are
cytoplasts
highly organized patterns (Bajer
&
J.
6
Fig.
2.
Actin
preparation
x
8000.
filaments
with
in
anucleate
an
rhodamine-phalloidin
of
subprotoplast
as
a
pollen
of
tubes
to Rutten
probe, according
DERKSEN
ET
AL
Nicotiana.
Immunofluorescence
Derksen
(1990). Magnification
&
(Photograph: T, Rutten.)
Mole-Bajer
1986b).
microtubules takes
protoplasts
In
place
at
the
of the
alga Mougeotia reorganization
of the cortical
from the nucleus
plasmalemma, independent
(Galway
&
Hardham 1986).
Like
microtubules,
actin filaments are present in cortical arrays
nucleus is anchored in
with the cells
(review:
basket of actin filaments and
a
periphery (Derksen
Staiger
& Schliwa
1986).
et
al.
microfilaments may show self assembly
Intermediate filaments in
membrane and
fluorescent
be
can
seen
preparations,
seem to connect
as
et
al.
Interactions between
& Derksen
see
in
cytoplasts
also Fig. 2).
associated with the
spindles. Arrays
periphery
interphase
The
plasma streaming
co-localize with microtubules in
those of mitotic
1987).
the nucleus
but in anucleate
1989;
probably present
that
al.
plasma-
immuno-
of filament bundles
cells
(Goodbody
et
al.
1989).
cytoskeletal
cytoskeletal
elements
elements form
Davis 1981; Griffith & Pollard
1986)
are
patches
also in
filaments may be cross-linked
have
cells
(Rutten
et
connect
These bundles reflect
is uncertain,
origin
the nucleus with the cells
1989; Hargreaves
The various
plant
1986b).
Their
(Traas
bundles
large
been observed in both
by
MAPs
1982).
In
an
or
integrated system.
by
plant
actin-associated
cells
they
dry-cleaved preparations
often
et
proteins (e.g.
co-localize,
(Traas
and sections of freeze-substituted material (Tiwari
Microtubules and actin
et
al.
Bennett &
and cross-links
1985; Pierson
al. 1984; Lancelle et al.
et
al.
1987).
CYTOSKELETON SIGNIFICANCE
Fig. 3. Micrograph
of
microfilaments
present
or
are
a
dry-cleaved preparation
at the surface
to accompany microtubules
Single microfilaments
dry
cleaved
data);
see
(J.J.).
of a protoplast from
Often these filaments
(T). Magnification;
were
co-aligned
of Nicotiana
preparations
also
IN DEVELOPMENT
x
59 000.
a
7
Nicotiana cell culture.
seem
to be connected
Numerous
with coated
putative
pits
(\J7),
(Photograph: H. Kengen.)
with microtubules
Fig. 3). However, doubt exists about
distances
over
protoplasts (H. Kengen
to
up
& J. Derksen,
the actual
1 -46 pm in
unpublished
of these filaments
nature
(see below).
A clear co-localization
cent
of
preparations
over
large parts
tubes
pollen
of the cell has been observed in immunofluores-
(Raudaskoski
et
al.
distribution of the microtubules has been reported
distribution(Derksen & Traas
Intermediate filaments of
(Goodbody
filaments that
nect
J.
al.
et
are
1989).
visible in
an
intact actin
microtubule
THE
skeleton,
cells
dry-cleaved
but
may be
et
al.
least
1989)
partly,
and the
on
actin
(Emons&Traas
depends
IN
et
least
at
partly
patchy
a
identical
way
to
cells and that accompany microtubules and
1986; Quadereta/. 1986;
The distribution of the
degradation (Goodbody
CYTOSKELETON
at
co-localize with microtubules in
present proteins
coated pits with microtubules
Derksen, unpublished data).
depend,
1984).
plant
The
Pierson
1987;
to
larger
on
microtubules.
al.
1989).
CELL
bundles is
MORPHOGENESIS
Kengen&
independent
become
They
H.
the
con-
from
dispersed
after
AND
DIFFERENTIATION
Determination of the division plane
The
of
position
microtubular
Prior
to
the
drugs
cell
versa
may
(Burgess
by
bands
bands in nuclear
1988).
may
be
largely
disposition
nucleus will
microtubules
determined
of the nucleus
move
radiating
1970; Pickett-Heaps 1974).
during phragmosome
pre-prophase
cause
division, the
may be determined
vice
nucleus
positioning
The fundamental
is
&
not
regulatory
Libbenga
microtubules,
&
Lloyd
as
anti-
1984).
towards the future division plane, which
from the nucleus
to
the cells
These microtubules may
formationand coincide in time and
(Venverloo
by
(Clayton
place
1987). However,
unquestioned (Clayton
&
periphery
already
with the formationof the
a
role of the
preprophase
Lloyd 1984; Mineyuki
mechanisms are unknown.
and
be present
Also,
et
al.
microfilaments are
8
J.
in the
present
metaphase
preprophase
bands (McCurdy
preprophase
band microtubules
the
and may
filaments remain,
determined
path (Traas
show distinct
et
al.
of cell
al.
et
al.
1987; Lloyd
1990)
but
process,
polarity (Traas
al.
band
but
not
changes
Hormonal control
elements.
causes
Pisum sativum and
a
al.
Vigna
few hours.
In
cortex
ethylene
high
&
Shibaoka
& Shibaoka
growth against
treatment
explants,
(Wilms
1984). However,
Hormones also
(Fragata
may
act
epidermal
the number of
1974;
effects the direction of cell
epidermal
cells of maize
ethylene production (Imaseki
organization
of the
development
Medicago mesophyll
by changing
both
&
the
cells
(Meijer
of
internodes
pea
microtubules and
by gibberellic
depend
of the
pumps
microfilaments (see
acid
the colchicine
on
1984).
Auxin
cytoskeleton.
et
al.
1988).
Since auxin induces
cortical microtubular skeleton
& Simmonds
it
diverse: it may protect
stimulation
is indirect. However, the presence of auxin
a
cause
Gibberellic acid
and the orientation of the cortical micro-
1988).
Hormones may
and channels
1981; Saunders 1986; review:
microtubules and
are
can
it may be concluded that the action of auxin
of
al.
Doonan
1989).
also Mita & Shibaoka
see
et
and low temperature
cremart
organization
expansion
distribution of cation
Hepler
the
coleoptiles (Bergfield
1985),
cytoskeleton
conditional for the
(Saunders
for discussion
on
1982;
cells
transverse
conversely, growth
cells of
Roberts
re-orientation of micro-
Physcomitrella.
the effects of gibberellic acid
indirectly
et
al.
cytoskeletal
epidermis
& Wolters-Arts
cells of
microtubules in
cochicine inhibitionbut
concentration used
tubules in
unknown.
benzylaminopurine (100 gM)
tip-growing
It increases
1987).
1981; Lang
cells of tobacco
may be inhibited by colchicine. The differences however, may
treatment
the
underlying
basically
between hormones and the
of microtubules by colchicine,
prevents depolymerization
(Mita
with the pre-
not
role in cell division
regulatory
cell division are still
concentrations of
rearrangement of cortical
causes
(Akashi
a
re-orientation of cortical microtubules in
of microtubules in
depolymerization
in the establish-
The actual mechanisms
plane.
to
and
phragmoplast,
radiata (Steen & Chadwick
showed that
(1985)
and the
precise relationship
a
tubules is accelerated after
et
involved
are
of the cytoskeletal organization
Ethylene
within
pre-
Lammeren et al. 1989; Traas
(see
which indicates
cytoskeletal organization prior
Little is known about the
1985)
spindle
1985),
in determination of the division
in
the
1989).
& Wick
(Gunning
band actin
along
out
involved in the co-ordination of the
microtubules
probably only
et
1988). During
preprophase
apparatus
ET AL
Both microtubules and actin filaments
probably
are
but the
cytokinetic
1988).
& Traas
1988; Lloyd
disappear
the meiotic divisions
and
Calmodulin is associated with the
prophase
the
guide
to
configurations during
1989; Bednara
meiotic division
ment
et
help
al.
et
DERKSEN
Schnepf
above),
such
on
the
1986).
changes
in
on
seems to
protoplasts
act on
cell
the
be
of
polarity
plasma-membrane
As
Ca
may
2+
also
may
affect
affect
the
organization of cytoskeletal elements.
Controlof cell wall
It is
generally
deposition
believed that the orientationof
nascent
cortical microtubules. Several models have been
trol of microfibril orientation (reviews; Robinson &
All models
imply
that microtubules connected
cellulose microfibrils is controlled by
proposed
to
to
describe microtubular
Quader 1982; Heath & Seagull
the
plasma membrane,
con-
1982).
i.e. the cortical
microtubules, would prevent free diffusionof cellulose microfibril synthesizing complexes
in the
membrane, leading
Herth
1985).
Also the
to
parallelism
insertion of
of microtubulesand
Golgi-vesicles
nascent
microfibrils
(see
also:
with non-cellulosic wall material has
CYTOSKELETON
been
thought
SIGNIFICANCE IN DEVELOPMENT
be under microtubular control
to
9
Roo
(Goosen-de
1973,
also
see
Herth
1985).
As discussed
in
occur
a
clear relationship
been
In
thought
to
Traas
al.
mainly
cases,
al.
et
1984; Emons
1989;
effected
may be
marine algae
and thus
A
& Hoffmann
simultaneous
deposited
will
and
Often such
a
similar
In
1989).
a
other
or
lead
as
drugs
Valonia ventricosa
affect
the
in
factors.
The
also
from
transverse
to
parallel
the
to
be co-incidental.
ation in
so
(Wilms
&
far,
cell
to
cells
elongating
of cellulose
Patterning
instances
some
et
al.
1986), electric
(Roland
number and
(Emons
1985)
1987).
density
evidence for
a
et
al.
1990;
Wilms
be,
e.g. Ca
1988).
2+
et
(Quader
al.
et
It has also been
Particular wall
textures
of cellulose synthesizing
cytoskeleton,
orientation.
vector-sum
nor
If
out
may
expanding
a
absent
In
been
microtubular
cortex
cells of
cell axis
(Wilms
colchicine did
1989). Thus,
common
&
not
such
regulatory
of both microtubules
& Hardham
be
more
1982), might
complicated
1990; Wilms & Kengen
or
al.
may
as
or
by
such
different
a
relationship
be
mechanisms
that microfibrillarorganiz-
in the
exist,
thought
plasma
based
arise from
(Emons 1986).
nascent
they
to
membrane(Emons
be taken
not to
rejected
cell
the internal geometry of the cell
between the orientation of
orienting
on
interfere otherwise. Such
have also been
complexes
1990).
depend
1986), turgor pressure (Derksen
proposed
that co-orientation itself it
relationship
can
determining
Cytoskeleton
the cell’s
pointed
causal
be
within the
or
on
expansion
deposition
spontaneously by self-assembly
al.
cells
mesophyll
changes
Wolters-Arts
in combination with cell dimension and matrix substances
It should be
In
to
fields (Preston
et
In the
the orien-
and relations with microtubular patterns may need reconsider-
thought
ation would occur
wall
1988).
cremart
(Gunning
differentiation. Various factors may be conditional,
factors have been
not
may
microtubule-microfibril interactions may be diverse and
Obviously,
The
do
1988)
and
longitudinal
elimination of microtubules by
orientation with respect
transverse
generally thought
1990).
effect,
microfibrils has
supply
of microtubules and microfibrils
cellulose microfibrils in
nascent
al.
after
deposition
deposition.
al.
et
and
simultaneous changes might be solely co-incidental and depend
and
et
same
deposition
after cessation of auxin
in microfibril orientation
change
exist
cytoplasmic organization
(Hayano
orientation of microtubules
organization
1988). However,
the
has
1985).
change
time interval
same
the
different. Also in
clearly
hairs,
root
(Emons
in cell wall
changes
to
cannot
in microfibril
to
the entire
control of microfibrilorientationhas been inferred (Bergfield
Derksen
Raphanus
change
microtubules and microfibril
coleoptile segments
explants,
relationship
a
relationship
in ordered patterns
microfibrils is
nascent
between
relationship
tobacco
seems to
Also in seed hairs
1982; Emons & Wolters-Arts 1983;
by colchicine,
deposition,
indirectly
Boergesenia forbesii
observed in maize
1987).
hairs: Emons
direct microtubular control
a
tation of microtubules and
(Hahne
al. 1986;
Traas & Derksen
microfibril
on
indicate
necessarily
et
deposition
during xylogenesis.
growing tip cells,
root
but microfibrils were still
occurred,
effect of colchicine
a
in
1985;
of the microtubules
depolymerization
such
(Quader
cells and
obligatory (e.g. Lloyd 1984).
tubes: Derksen
et
exist
seems to
be
number of
a
(pollen
microtubular control of microfibril
by Hepler (1985)
elongating cylindrical cells, guard
on
may
as
pre-requisite
or
microfibrils and the
the
act
absence
as
of
vectors,
co-
the
the orientation of the microfibrils.
and cell expansion
cells
a
periphery.
central vacuole
develops, leaving only
a
small
layer
of
cytoplasm
at
J. DERKSEN
10
In
microtubules generally appear
stretching cells,
tion of cell
expansion (Gunning
be oriented
to
& Hardham
1981; Gunning
transverse
1984; Traas
Traas
ential cell
tip
1989).
of
al.
Traas
1985;
(1984)
expansion,
more or
of
presence
meristematicand
see
that
also
transverse
less
as
in
the
to
in
expanding
pitches (Lloyd
the
1983,
root
of
cells
cortex
of both axial and circumfer-
vector-sum
stretching
randomly organized
cells. The orientation of microtubules in
microtubules
at
et
(Traas
al.
1985; Emons
surfaces, of
non-expanding
cells in these roots, may support this
cortex
the direc-
Fig. 1).
microtubules
cells would be determined in a similar
way
tip-growing
The
1989;
supposed
would be oriented
Raphanus
the
et
al.
et
AL
In many cells,
1982).
microtubular skeleton shows helix-like configurations with different
to
ET
assumption (Derksen
al.
et
1986a).
It
remains open
whether
cell
indirectly, by
This
might
whether these
expansion
either
as
al.
a
Such
observed in
and in Avena
a
the
exact
changes
out
by
pressure.
active
root
cells
force
from
(Traas
transverse
to
et
al.
& Oshima
1984; Hogetsu
&
longitudinal
or
Roberts
of helical patterns
occurrence
epicotyls (Iwata
oblique
more or
expansion (Lloyd 1984;
cell
during
and Pisum
mesocotyls,
would behave
configurations
relate the microtubule orientation
demands
to
more
a
a
i.e.
cytoplasm,
cell
to
1986)
Hogetsu 1988).
occur
expansion
role
at
the
the
one,
In
after
mainly
but fail
point
to
behaviour of microtubules, whereas the
yet needs considerablereorganization
cell axis
immediately
of
during stretching.
orientation of microtubules in
long
appreciable
in cell
(Wilms
change
the
to
without
change
dynamic
for the loss in diameterof the helix
,
Wilms & Derksen took into
that the
rather
of Nicotiana
gradually
play
a
static, passive
longitudinal
to
differentiationand
also
a
compensate
explants
occurs
supposed
or
or
occur
mechanisms.
transverse
might
and
assumption requires
one
In tissue
change
that the helical
and Pisum
Raphanus
the microtubules
from
directly by resisting turgor
or
microtubular skeleton
behaviour cannot be reconciled with the
assumptions
The first
second
of the
expansion,
latter could
has ceased.
elongation
out
deposition,
rigidity
from cell
result
microtubules. The
microtubule-based motors.
coleoptiles
these studies the
these
by
which becomes stretched
spring,
1985).
Both
the
and coworkers assumed
Lloyd
et
by
organizations
helical
determined
the control of cellulose
occur
generation involving
less like
is
after
the cells
changes
explantation.
cell extension and has been related
This
to
de-
polarity. However, ethylene production by wounding
& Derksen
account
the
1988).
To
explain
dynamic properties
in orientation resulted from
plasma membrane, during
a
the mechanism
involved,
of the microtubules.
polarity determining
dynamic phase
They
factors in the
of the microtubulesafter
explantation.
The behaviour of the cortical actin filaments
described,
(Derksen
but the
et
al.
during
organization of the endoplasmic
cell
has
elongation
not
yet been
bundles remain essentially the
same
1985).
Differentiation
Cell
differentiation is
different
functions.
deposition.
Here
we
In
the
event
plants,
will discuss
leading
to
cells
differentiation is
a
few
with
quantitatively
often
examples, namely
accompanied
or
by
qualitatively
a
local
wall
vascular elements, stomatal cells
and statocytes.
The densities of microtubules increase
thickening along
the lateral walls of
young
gradually just
before
sieve elements in
root
the
initiation of
protophloem
wall
of wheat
CYTOSKELETON SIGNIFICANCE
(Eleftheriou
skeletal
11
of the best studied
one
cell differentiation.In
during
in close relation with
locally
is
1987). Xylogenesis
organization
IN DEVELOPMENT
elements
cytoskeletal
for
Zinnia
&
Seagull
(Falconer
studied
in
and
Seagull
particular system (Fukuda
&
et
al.
These cells have
1988).
Fukuda &
The specific bands of microtubules
of actin filaments
the surface.
over
forming
a
transverse
the sites of local wall
at
disappear
orientations
form bundles. The actin dots
are
co-ordinated way.
bundles and wall
of the
deposition
cells take
least
shape
on
of the
1984).
the local
guard
tubules and cellulose
cells
1989;
cells and from radial,
a
prior
in
a
role in the
a
guard
mother
depends
at
kidney-like
the orientation of
clear correlation between micro-
be
to
to
the
firmly established.
deposition
of the
pairs
preceded by
preprophase
of
guard
Hardham
changes
and
transverse
the
bands in the
cells and the
&
1989; Cleary
of the microtubules
over
like in
act
Like in
secondary
1986).
& Wick
the
organization
regions
of microtubules reflects
increases
regular
of microtubule
results in the
finally
Palevitz & Mullinax 1989, and references in these
the
subsidiary
the
divisions of the
radial division of the mothercell is
development,
pattern,
cells. Their function
subsidiary
walls. In these cells
density
(Cho
the
destroys
patterns.
asymmetric
of cortical microtubules and
from mirror images
until
1985). Cytochalasin disrupts
which may indicate
1986),
of wall material which
cell wall. The radial arrays in both the
Palevitz
oblique,
time the microtubules
the microtubule
microfibril orientation appears
asymmetric,
to
changes gradually
same
a
less axial
distributed
regularly
Colchicine
also Herth
al.
et
grasses,
Palevitz 1982; Kristen
(reviews;
radial organization
new
seen
reached via
are
more or
Microtubules and microfilamentsappear to
organization
periclinal
vascular elements, microtubule
The initial,
deposition.
cells and the
deposition
cells. The
guard
cellulose microfibrils in
cell wall
in
development
the
reviewed this
their orientation
At the
microtubule and actin filament
place, forming
partly
wall
deposition (see
deposition (Dauwalder
stomalal
During
initially
are
change
In Zinnia, calmodulin is found between
specific
extensively
present exclusively between the microtubule bands and
are
tubes (Derksen & Traas
changes
dots of actin
actin filaments and also affects
regular pattern of
pollen
large
predominant.
are
finally located under the sites of cell
microtubulepattern and cell wall
the
and
Meanwhile the axial microtubules
oblique
elements
xylem
been
Kobayashi, who recently
network with the actin dots in the darns. This pattern
and
1985).
has also been
Kobayashi 1989).
characteristic sequence of actin and microtubule
patterns. The
patterns
deposited
Herth
1973,
starts
differentiate into
which
culture,
1988; Kobayashi
Falconer &
by
cells
elegans
Roo
deposition
the cyto-
to
wall material is
(Goosen-de
The formation of bands of microtubules before local wall
reported
with respect
cases
xylem cells,
pairs
1989;
plane of
of
to
to
axial in
the
subsidiary
Mullinax &
papers). During
from radial
oblique,
asymmetric,
further
transverse
guard
in
cells. In
Avena, in the last stage of differentiation, both guard cells and subsidiary cells show axial
microtubule
Mullinax
1989). Thus,
patterns (Palevitz &
microtubule patterns
of
Statocytes
Lepidium
situated in the top of the
endoplasmic
reticulum
Sievers
1979).
Hensel
(1985,
stabilizing
co-ordinated
show
cell,
are
a
a
distinct
way
here
cytoplasmic
are
1987).
involved
seems
Microtubules appear to be less
endoplasmic
to
of the nucleus
depend
seems to
reticulum
on
(Hensel
actin filaments
depend
on
a
clear sequence in
organization.
whereas in the distal part of the
present that
too,
in the different cells.
in
The
cell, amyloplasts
nucleus
and
as
is
rough
graviperception (Volkmann
typical organization is entirely actin dependent,
the distal
organization
position
This
in
occurs
has been shown
&
by
involved but may yet contribute in
1984). Thus, endoplasmic
and
not
on
reticulum
microtubules. Also
the
actin filaments here, whereas in other systems it
J. DERK.SEN
12
depends mainly
role of the
reticulum
might
is
also
thought
depend
Thus, cell polarity
part
on a
depend
to
elements.
cytoskeletal
the distal
to
In tobacco
the cortical
must
be
from
separated
perhaps interchangeable
continuous transport of
statocytes (Hensel
of the cell
polarity
each
graviperception,
endoplasmic
1985), graviperception
i.e. microtubules
cytoskeleton,
explants,
cells
PLANT
IN
their
change
itself, however,
(Hensel
involving
a
1985; 1987).
differentpart
the cell. In cells that do
remains
unchanged,
shows meristematic
not
observed
in
Vinca shoot
cortical
a
al.
in
explantation. Initially,
the
longitudinal
different,
are
or
even
et
al.
randomly organized
planes
Selker
1988; Lang
These orientations become
by
before
the
first
Marc & Hacket
meristem may
become
in
aligned
randomly
centres
(Lang
microtubule
as
Selker
patterns
acid
gibberellic
1989; Marc & Hacket
between different cells
Hedera (Marc & Hacket
CONCLUDING
1989)
to
guard
be involved
The
in
the
division
Hedera tunica
intercellularly.
we
in such
a
particular changes
cytoskeletal
Hormones
factors
cell
to
have reviewed
specific
in
they
to
polarity
actions
vivo
needed remains
sequences that
may
explain
as
be
are
with other
partly,
hormone
dependent,
cytoskeleton
appears
as
an
indicator for
the actual mechanisms involved.
may
to
graviperception.
used
occur
plant morphogenesis
but
open,
in
a
highly
early
cell
Changes
co-ordinated way.
at
contacts.
occur
complex
and still
are
also be involved. Whether
The various types of cytoskeletal organization
prove the versatile character of the different cyto-
composition
structures
may
least cell differentiation of tracheids appears
of the various elements, their
and their relation with other cellular
probably
skeleton
least
in the co-ordination within tissues and organs, but other
affect
skeletal elements. The actual
in
that will
show the involvement of the
present clearly
sensory function
cannot
independent from direct cell
specific
at
in different cells
organization
generally thought
and the
the
The micro-
clear co-ordination between
and cell differentiation.The
organization
probably partake
contacts are
be
at
occurs
cells,
1989).
differentiation.However,
in
be,
division
mother cells
promote the process of microtubule pattern formation in
plant morphogenesis
even
may
The
been
and Hedera
REMARKS
The localization studies
cytoskeleton
to
seems
1989).
with
microtubules
have also
parallel
longitudinal
(1988)
One of
planes.
almost
tubular pattern in the tunica cells may indicate the outline of the leaf primordia
develop
axis of
the orientation of the
division planes. However, in Allium
shown
the
occur,
future division
orientation of the division
random
are
As
1989).
microtubule pattern
1989).
preferential
microtubules
et
to
oriented divisions. Meristematic
apices (Sakaguchi
& Hacket
with
regions
(Mineyuki
show
(Marc
parallel
with microtubules that
properties
preferential
do
in
to
apparently randomly
that also
planes
parallel
the
different microtubuleorientations
tunica cells
to
but in three regions where cell divisions
distributed and with
having
several times after
transverse
divide anymore, the orientation of the cortical microtubules
not
cortical microtubules will become
regions
MORPHOGENESIS
polarity
the orientation of microtubules shifts from
the
a
distortionof this transport. The
on
CYTOSKELETON
THE
cells
in
occur
to
seems
As
cytoskeleton.
of the
these
the versatile, and
microtubules, indicating
on
various
ET AL
largely
probably
structures
and
dynamics
and
their mutual inter-
unknown. The interactions of the cyto-
transient and therefore will be difficult
to
CYTOSKELETON
SIGNIFICANCE IN DEVELOPMENT
determine
from
techniques
also appears
However,
static
images
the basis for
is set,
cytoskeleton
particular
As several groups
studies
promises
and
must
The latter may
microtubular control of
interaction with
an
the
synthesizing complexes.
of cytdskeletal
also
are
for those botanists interested in the
exciting
detection and localiz-
proteins.
on
via
occur
expression
function of the cytoskeleton
and function of the
organization
identification,
discussion
pending
differentialgene
studying
are
the
to
be
to
of the
the
light microscopic
developed
cells.
cytoskeleton-associated
control that
a
newly
and that limits lateral diffusion of the cellulose
plasmamembrane
genetic
deposition,
of
plant
understanding
interest also for the still
cellulose microfibril
in
has been made in
ation of intermediate filaments and the
be of
use
promising
further
a
a start
as
the
alone,
be very
to
13
of
cues
and
proteins
the
route,
en
near
future
plant morphogenesis
cell differentiation.
plant
ACKNOWLEDGEMENT
The authors
preparation
indebted
are
of the
Professor M.M.A. Sassen for his critical support
to
the
during
manuscript.
REFERENCES
Akashi, T. & Shibaoka, H. (1987):
the
on
microtubules
Plant Cell
Bajer,
in
&
colchicine
cells
J.
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