Download Cytokinesis in flowering plants: cellular process

486
Cytokinesis in flowering plants: cellular process and
developmental integration
Maren Heese, Ulrike Mayer and Gerd Jürgens*
In phragmoplast-assisted cytokinesis of somatic cells, vesicle
fusion generates a cell plate that matures into a new cell wall
and its flanking plasma membranes. Insight into this dynamic
process has been gained in the past few years and additional
molecular components of the basic machinery of cytokinesis
have been identified. Specialized modes of cytokinesis occur in
meiosis and gametophyte development, and recent studies
indicate that they are genetically distinct from somatic
cytokinesis.
Addresses
Lehrstuhl für Entwicklungsgenetik, Universität Tübingen, Auf der
Morgenstelle 1, D-72076 Tübingen, Federal Republic of Germany
*e-mail: [email protected]
Current Opinion in Plant Biology 1998, 1:486–491
http://biomednet.com/elecref/1369526600100486
© Current Biology Ltd ISSN 1369-5266
Abbreviations
BFA
Brefeldin A
FS
fenestrated membrane sheet
FT
fusion tubes
KatAp kinesin-like protein A, Arabidopsis thaliana
KCBP kinesin-like calmodulin binding protein
MTOC microtubule organizing center
PPB
preprophase band
TN
tubular network
TVN
tubulo-vesicular network
ZAD
zone of actin depletion
Introduction
The textbook-type of flowering plant cytokinesis is usually contrasted with the animal type: center-out mode in
plants versus periphery-in mode in animals. In reality,
however, the situation in plants is more complex as there
are different ways of splitting a cell in two. Most dividing
somatic cells from embryogenesis to the flowering stage
display a preprophase band (PPB) and use phragmoplastassisted cell plate formation, while cellularising
endosperm, meiocytes and gametophytic cells each undergo cytokinesis in their own specific ways. Somatic
cytokinesis has been studied most thoroughly in a number
of model systems, including the synchronisable tobacco
BY-2 cell culture, Tradescantia stamen hair cells, which are
well suited for injection experiments, and the two genetic
model organisms, Arabidopsis and maize. Although BY-2
cells and stamen hair cells are ideal to analyze cellular
mechanisms of cytokinesis, Arabidopsis and maize offer the
additional possibility of studying how cytokinesis is integrated in developmental processes and subject to
intercellular controls.
Cytokinesis of somatic cells: the basic
machinery
Somatic cytokinesis progresses from the center to the
periphery of the cell, forming a new cell wall and flanking
plasma membranes de novo [1,2]. This dynamic process is
initiated in late anaphase with the formation of the phragmoplast — a complex array of microtubules, actin
microfilaments and different membrane compartments.
The phragmoplast appears in the interzone between the
two sets of daughter chromosomes and mediates the accumulation of vesicles which fuse with each other to form the
so-called cell plate (Figure 1). The cell plate undergoes a
profound maturation process, changing from an aggregate
of locally fused vesicles to a flat membranous disk with cell
wall material in its lumen. While maturing, the cell plate
expands laterally until its growing margin reaches and
fuses with the parental cell walls. The expanding cell plate
seems to be guided to the cortical division site by actin
microfilaments [3•].
The phragmoplast cytoskeleton consists of two oppositelyoriented sets of microtubules overlapping with their plus
ends in the plane of cell division and of two sets of actin
microfilaments which show the same orientation as the
microtubules but do not overlap. The microtubules are in
part recruited from the mitotic spindle and in part polymerized anew, forming a cylinder which consolidates by
shortening in length and widening in girth [3 •].
Subsequently, the microtubules depolymerize in the center and repolymerize along the edge, transforming the
phragmoplast into a barrel-like structure which marks the
growing margin of the cell plate (Figure 1b). Several lines
of evidence suggest that microtubules are involved in the
transport of vesicles to the plane of cell division [2], whereas the role of phragmoplast actin microfilaments is less
clear. Depolymerization of actin by profilin injection into
Tradescantia dividing stamen hair cells results in delayed
cell plate formation or disintegration of a cell plate already
formed. These results are compatible with a stabilizing
role of actin but an involvement in vesicle transport has
been suggested as well [4].
Additional proteins have recently been localized to the
phragmoplast/cell plate, using antibodies generated
against MTOC (microtubule organizing center) components in other systems. The anti-γ-tubulin antibody
associates with the early phragmoplast near the minus ends
of microtubules which, at least in other systems, are generally embedded in MTOCs. By contrast, the labeling is
more dispersed in the expanding phragmoplast [5].
Antibodies against yeast and animal MTOC phosphoproteins, such as MPM-2 [6] and anti-cerin [7] antibody, label
the phragmoplast and the forming cell plate. The proteins
Cytokinesis in flowering plants Heese, Mayer and Jürgens
487
Figure 1
Formation and expansion of cell plate.
(a) Initial stage of cell plate formation. Golgiderived vesicles are transported along
phragmoplast microtubules by an unidentified
plus-end directed motor and accumulate in
the center of the plane of cell division.
Membrane fusion requires the cytokinesis
specific t-SNARE KN and a hypothetical
v-SNARE. The GTPase phragmoplastin may
be involved in the formation of 20 nm fusion
tubes (FT) at an early stage in cell-plate
formation (modified after [46]). The
organization of phragmoplast microtubules
(MT) is presumably facilitated by the plus-end
directed kinesin TKRP125. Cell-plate
formation can be inhibited by brefeldin A
(BFA) treatment. KN, KNOLLE syntaxin;
TKRP125, tobacco kinesin-related
polypeptide of 125 kD; V, Golgi-derived
vesicle. (b) Lateral expansion of the cell plate.
The cell plate expands from the centre (left) to
the periphery (right) and eventually fuses with
the parental cell wall (PCW) at the zone of
cortical actin depletion (ZAD). Cell-plate
expansion is guided by microfilaments (MF)
and involves translocation of phragmoplast
microtubules (MT) which can be blocked by
the MT-stabilising drug, taxol. (Note:
microfilaments of the phragmoplast are not
shown.) While expanding by continuous
vesicle fusion at leading edge, the cell plate
undergoes maturation. Successive steps are
marked at the top: free vesicles (FV), fusion
tubes (FT), tubulo-vesicular network (TVN),
tubular network (TN), fenestrated sheet (FS)
(modified after [46]). Putative sites of action
of inhibitors, such as 2,6-dichlorobenzonitrile
(DCB), caffeine and taxol, are indicated. The
appearance of clathrin-coated buds (CB) may
suggest removal of membrane material from
the maturing cell plate.
(a) Vesicle transport
Membrane fusion
-
KN
(t-SNARE)
Golgi
BFA
motor?
-
+
v-SNARE?
+
MT organisation
-
FT formation
+
-
V
MT
+
-
phragmoplastin?
TKRP125
(b)
caffeine
DCB
FS
TN
FT+FV
TVN
MT
CB
MF
ZAD
MT
tr an
sl ocati on
PCW
taxol
Current Opinion in Plant Biology
recognized by these antibodies may thus play as yet undefined special roles in flowering-plant cytokinesis.
Cell plate maturation
The forming cell plate undergoes a complex series of maturation steps which have been revealed by high pressure
freezing/freeze-substitution electron microscopy (Figure 1;
[1]). Vesicles start to fuse with one another via 20 nm
fusion tubes, generating a membranous network which
seems to be stabilized by the assembly of a fibrous coat.
Formation of the fusion tubes (FT) may involve phragmoplastin (also called ADL1), a dynamin-like GTPase which
accumulates in the forming cell plate [8•,9•]. Continuing
membrane fusion leads to a tubulo-vesicular network
(TVN) which further transforms into a tubular network
(TN) and then into a fenestrated membrane sheet (FS,
Figure 1b). During the TVN-to-TN transformation the
dense membrane coat and the associated microtubules of
the phragmoplast are disassembled. The centrifugally
expanding cell plate displays successive stages of maturation from the growing margin, where new vesicles
continuously fuse, to the most mature parts in the center of
the cell (Figure 1b). Soon after fusion of the growing margin with the parental cell walls, the wavy cell plate flattens
and stiffens, indicating ongoing maturation of the newlyformed cell wall [10].
Vesicle trafficking along the phragmoplast
The cell plate appears to originate from Golgi-derived
vesicles, as Brefeldin A (BFA) treatment of telophase cells
488
Cell biology
results in Golgi disintegration and inhibition of cell plate
growth (Figure 1a; [11]). The vesicles deliver specific
cargo, such as callose synthase which is active in the cell
plate during maturation [12]. Plasma membrane ATPase
which decorates the plasma membrane of the interphase
cell [9•] is not found in the cell plate, suggesting a different trafficking route. Accumulation of cytokinetic vesicles
in the equatorial plane of the phragmoplast is increased by
taxol stabilization of microtubules, suggesting that vesicles
traffic by translocation along, rather than treadmilling of,
microtubules [13]. Vesicle transport to the division plane
should thus involve plus-end directed motor molecules
which, however, have not been identified (Figure 1a; [14]).
Two kinesin-like proteins associated with the phragmoplast —KatAp (kinesin-like protein A, Arabidopsis thaliana;
[15]) and KCBP (kinesin-like calmodulin binding protein,
tobacco; [16]) — are putative minus-end directed motors
and may be involved in stabilization or reorganization of
the phragmoplast. A similar role has been proposed for the
plus-end directed motor TKRP125 (tobacco kinesinrelated polypeptide of 125 kD), on the basis of
immunolocalization studies and inhibition of microtubule
translocation by antibodies against its motor domain
(Figure 1a; [17•]).
Vesicle fusion in the plane of cell division
The Arabidopsis KNOLLE gene encodes a cytokinesisspecific syntaxin, which suggests that cell plate formation
proceeds by vesicle fusion involving components of the
v-SNARE/t-SNARE vesicle-docking machinery [9•,18].
According to the SNARE model of membrane fusion,
which is based on studies in a variety of organisms, matching pairs of syntaxin (t-SNARE) and synaptobrevin
(v-SNARE) contribute to the specificity of a particular
fusion process [19]. In the absence of KNOLLE protein,
vesicles accumulate in the plane of division and bind
ADL1 but are strongly impaired in fusion. Assuming a
homogeneous vesicle population, KNOLLE syntaxin
would be involved in homotypic fusion during cell plate
formation. Whether KNOLLE protein also participates,
maybe by interacting with a different partner, in the heterotypic fusion of the cell plate membrane with the
plasma membrane remains to be resolved. The
Arabidopsis homologue of yeast Cdc48p, an ATPase
involved in membrane fusion, has been localized to the
phragmoplast of dividing cells [20]. The functional role of
AtCdc48, however, has not been determined. Additional
specific components of the cytokinetic process should be
identified by cloning genes that mutate to give cytokinesis-defect phenotypes, such as CYD from pea [21] and
KEULE from Arabidopsis [22].
translocation of the phragmoplast and arrests cell plate
expansion [13]. In the presence of caffeine, the initial
fusion of vesicles takes place but the fragile fusion-tube
generated network is not transformed into the more stable TVN and callose is not deposited in the lumen
(Figure 1b; [23]). Caffeine does not seem to interfere
with the consolidation of the phragmoplast but blocks its
lateral progression [3•]. Although the effects of caffeine
on cell plate formation have been described in detail, its
primary site(s) of action is still not known. The herbicide
DCB, a presumed inhibitor of cellulose synthesis, affects
cell plate maturation after the formation of the tubular
network (TN; Figure 1b; [12]). Although the cell plate
fuses with the parental cell wall it does not stiffen and
contains abnormally high levels of callose.
Regulation of the division plane
The cell plate fuses with the parental cell walls at a narrow
zone that is largely devoid of actin (‘zone of actin depletion’; ZAD in Figure 1). The ZAD, or cortical division site,
determines the plane of somatic cell division. During lateral expansion, microfilaments appear to extend from the
ZAD to the expanding phragmoplast and aid in guiding
cell plate growth as indicated by the fact that obliquely
positioned phragmoplasts can reorient towards the cortical
division site [3•]. The cortical division site corresponds to
the position of the PPB of cortical microtubules which
transiently appeared at the onset of mitosis. The PPB may
thus play a role in determining the plane of cell division by
marking the cortical division site. This is consistent with
the abnormal planes of cell division in Arabidopsis fass and
tonneau mutants which lack the PPB microtubules [24].
These mutants, however, also display abnormal cortical
microtubule arrays during interphase and may thus be
indirectly affected in the plane of cell division. Recent
experiments addressed this issue by analyzing cells with
two PPBs. Some synchronized BY-2 cells form two parallel
PPBs, corresponding to two potential cortical division sites,
but later the single phragmoplast is linked by microfilaments with the cortex such that an oblique cell plate
connects the two different cortical sites [25]. Caffeineinduced binucleate cells appear to utilize the cortical
division site from the previous cycle, sites marked by the
new PPBs or both in a stochastic manner, depending on
the relative proximity of the PPB-marked cortical sites to
the expanding cell plate [26•]. The persistence through
mitosis of the cortical division site may involve local modification of the cortex (see [27•] for discussion). In
summary, the PPB is not necessary for somatic cytokinesis
per se but appears to correlate with the cortical division site
to which a nearby phragmoplast is guided and thus, the
position of the PPB predicts the plane of division.
Lateral progression of cell plate formation:
inhibitor studies
Cytokinesis and the cell cycle
Centrifugal progression of cytokinesis
plex interplay between cell plate
expansion of both phragmoplast and
microtubule-stabilizing drug taxol
In most somatic cells, mitosis (nuclear division) and cytokinesis are tightly coupled. The KNOLLE syntaxin gene is
expressed in a cell cycle-dependent manner [18]. KNOLLE
syntaxin, however, does not accumulate in tapetum cells of
involves a commaturation and
cell plate. The
inhibits lateral
Cytokinesis in flowering plants Heese, Mayer and Jürgens
the Arabidopsis anther, which undergo nuclear division without cytoplasmic partitioning [9•]. This indicates that mitosis
does not necessarily trigger cytokinesis and rather suggests
that both events are subject to cell-cycle controls. Active
cdc2/cyclin B complex not only drives mitotic progression
but also causes rapid disassembly of the PPB when injected
into Tradescantia stamen hair cells, revealing the PPB as a
target for cell-cycle control [28]. In addition, cdc2At has
been localized to the PPB and to the phragmoplast [29,30•].
In maize, where different cyclin isoforms can be distinguished by specific antibodies, cyclin Ib and II associate
with the PPB, and cyclins II and III co-localize with the
phragmoplast [30•]. This persistence of cdc2 and cyclin into
cytokinesis suggest a plant-specific cell-cycle regulation.
Specialized modes of cytokinesis
Meiotic and gametophytic cells have long been known to
divide differently than somatic cells. Recent studies may
shed light on the mechanisms being involved. In
Arabidopsis, as in many plant species, male meiotic
cytokinesis produces the four microspores simultaneously, no PPB marks the division site and no cell plate
forms. Instead, the new cell walls are initiated at the cell
surface and grow, presumably by vesicle fusion, along
the interfaces of microtubule arrays that radiate from the
four telophase nuclei [31]. KNOLLE syntaxin does not
accumulate during this cytokinesis [9•]. Mutations which
possibly affect the same gene, stud [32] and tetraspore (tes,
[33]), specifically block male meiotic cytokinesis, resulting in a single microspore with four nuclei. This
tetrakaryotic cell can give rise to a functional pollen tube
with up to eight sperm cells. Female meiotic cytokinesis
is not affected by stud and tes mutations, suggesting a
sex-specific genetic regulation [32,33]. The male and
female gametophytic divisions occur normally in all
cytokinesis mutants analyzed — knolle, keule, stud, tes and
cyd, implying that other as yet unidentified components
are involved.
Endosperm cellularisation is a unique kind of cytokinesis
(reviewed in [34]). The endosperm nuclei initially undergo a series of rapid synchronous divisions within a single
cell before cell walls are simultaneously laid down around
each nucleus from the cell surface. Formally, endosperm
cellularisation is similar to blastoderm cellularisation in the
Drosophila embryo: both involve ingrowth of cell membrane from the surface. The two processes differ in their
cytoskeletal support systems, however, and in the delivery
site of new membrane material although syntaxins are
involved in both cases. In Drosophila, an actomyosin-based
ring pulls in the membrane and while expanding, the
membrane receives new material by syntaxin1-mediated
vesicle fusion at its base, not at its tip [35]. By contrast, the
Arabidopsis cellularising endosperm appears to involve tip
growth: microtubule-associated membrane vesicles accumulate in front of the ingrowing membrane [36], and only
the newly-forming membrane contains the cytokinesisspecific KNOLLE syntaxin [9•].
489
Cytokinesis in development
Cytokinesis partitions the cytoplasm of the dividing cell,
resulting in potentially different micro-environments for
the daughter nuclei, due to the segregation of intrinsic factors or, more often, in response to signals from their
neighbors. Cytokinesis mutants disrupt tissue specification
in embryo, cotyledon or floral organ development
[18,21,22,37]. Other mutants display uncoordinated cell
divisions and eventually die [38,39]. Thus, to make a functional multicellular organism cytokinesis not only has to be
completed but also needs to be integrated, in time and
space, with developmental processes.
Oriented cell divisions are associated with pattern formation in the Arabidopsis embryo. Mutations affecting
apical–basal or radial patterning can be recognized by their
abnormal cell division patterns in specific regions or tissue
layers (reviewed in [40]). In scarecrow and short root
mutants, for example, only a single layer of cortex/endodermis cells is made in the embryo, in lateral roots and in
adventitious roots grown from callus. Ablation studies performed on wild-type seedling roots suggest that signals
from the mature tissue influence the orientation of the
division plane in the daughter cells of cortex/endodermis
initials [41]. A role for oriented cell divisions in morphogenesis, the shaping of embryos and organs, has been
inferred from the analysis of the Arabidopsis mutants fass
and tonneau, in which randomly oriented cell divisions
result in stunted plants with abnormally shaped organs
[24]. In the maize mutants tangled and warty, however, the
orientation of cell division can be perturbed without significantly affecting the overall shape of the leaf [42,43].
These results suggest that organ development is largely
controlled at a supracellular level. The Arabidopsis results
are consistent with the opposite notion that the orientation
of cell division influences organ shape.
A special function of cytokinesis in development is asymmetric cell division, which appears to segregate cell fates.
For example, microspore cytokinesis yields a large vegetative and a small generative cell. That this asymmetric
division is indeed associated with cell fate segregation has
been recently demonstrated. If this division is blocked by
colchicine treatment, a unicellular pollen expresses a vegetative cell-specific marker and forms a growing pollen
tube [44]. Lower levels of colchicine result in a symmetric
division producing two vegetative cells. The sidecar pollen
mutation of Arabidopsis also alters the microspore division
[45]. Of the two equal-sized daughter cells, one undergoes
the normal gametophytic divisions and the other becomes
an extra vegetative cell within the same pollen grain.
Conclusions
Substantial progress has been made in the analysis of
somatic cytokinesis. The high pressure freezing/freezesubstitution technique has revealed the dynamics of cell
plate maturation. A number of molecules have been implicated in cytokinesis but their precise roles have yet to be
490
Cell biology
9.
Lauber MH, Waizenegger I, Steinmann T, Schwarz H, Mayer U,
Hwang I, Lukowitz W, Jürgens G: The Arabidopsis KNOLLE protein
is a cytokinesis-specific syntaxin. J Cell Biol 1997, 139:14851493.
Detailed immunofluorescence study reveals KNOLLE distribution during the
cell cycle, including during cell plate formation, and in various tissues which
exhibit different modes of cytokinesis. Electron microscope analysis of knolle
mutant cells indicates that vesicle fusion is impaired.
determined by functional analysis. The characterisation of
additional cytokinesis mutants and the genes affected is
likely to address various aspects of this complex cellular
process. For example, if cell plate formation results from
SNARE-mediated homotypic fusion of Golgi-derived
vesicles, what are the other components of the vesiclefusion machinery? What motor molecules translocate the
vesicles along the phragmoplast microtubules? How does
the cell plate fuse with the plasma membrane at the lateral surface? How cytokinesis is regulated in time and space
is still poorly understood. Cytokinesis is linked to cellcycle progression but the mechanism is not known.
Analysis of the regulation of KNOLLE syntaxin gene
expression may help to clarify this point. Another critical
question is how the division plane is determined. In particular, the nature of persisting cortical signals for
positioning the plane of division needs to be addressed.
Regarding the developmental integration of cytokinesis,
further insights may be expected from the molecular
analysis of developmental regulators influencing the rate
or plane of division in specific developmental contexts.
11. Yasuhara H, Sonobe S, Shibaoka H: Effects of brefeldin A on the
formation of the cell plate in tobacco BY-2 cells. Eur J Cell Biol
1995, 66:274-281.
Acknowledgements
17.
We thank Markus Grebe, Ulrike Folkers, Arp Schnittger and Axel Völker
for critically reading the manuscript.
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