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: gerd.juergens@uni-tuebingen.de
Current Opinion in Plant Biology1998, 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 usual-ly 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 phragmoplast-assisted cell plate formation, while cellularising endosperm, meiocytes and gametophytic cells each under-go 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, Tradescantiastamen 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, Arabidopsisand maize offer the additional possibility of studying how cytokinesis is inte-grated 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 phrag-moplast — 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 accu-mulation 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 oppositely-oriented 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 poly-merized anew, forming a cylinder which consolidates by shortening in length and widening in girth [3•].
Subsequently, the microtubules depolymerize in the cen-ter 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], where-as the role of phragmoplwhere-ast 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) compo-nents 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 gener-ally embedded in MTOCs. By contrast, the labeling is more dispersed in the expanding phragmoplast [5]. Antibodies against yeast and animal MTOC phosphopro-teins, such as MPM-2 [6] and anti-cerin [7] antibody, label the phragmoplast and the forming cell plate. The proteins
Cytokinesis in flowering plants: cellular process and
developmental integration
recognized by these antibodies may thus play as yet unde-fined special roles in flowering-plant cytokinesis.
Cell plate maturation
The forming cell plate undergoes a complex series of mat-uration 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 phragmo-plastin (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 matura-tion 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 mar-gin with the parental cell walls, the wavy cell plate flattens and stiffens, indicating ongoing maturation of the newly-formed 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
Figure 1
Formation and expansion of cell plate.
(a)Initial stage of cell plate formation. Golgi-derived 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.
PCW MF
M Ttr ansloca
tion
FS TN FT+FV
taxol
ZAD
DCB caffeine
TVN
CB MT
FT formation Golgi
BFA
MT V
phragmoplastin? KN
(t-SNARE) Membrane fusion Vesicle transport
motor? +
-+
-MT organisation
TKRP125
-+ +
-v-SNARE?
(a)
(b)
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
differ-ent 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 phragmo-plast —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 kinesin-related 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 cytokinesis-specific 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, match-ing 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 het-erotypic 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 cytokine-sis-defect phenotypes, such as CYD from pea [21] and KEULEfrom Arabidopsis[22].
Lateral progression of cell plate formation:
inhibitor studies
Centrifugal progression of cytokinesis involves a com-plex interplay between cell plate maturation and expansion of both phragmoplast and cell plate. The microtubule-stabilizing drug taxol inhibits lateral
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 sta-ble 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 deple-tion’; ZAD in Figure 1). The ZAD, or cortical division site, determines the plane of somatic cell division. During lat-eral 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 fassand 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 microfila-ments with the cortex such that an oblique cell plate connects the two different cortical sites [25]. Caffeine-induced 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 mod-ification of the cortex (see [27•] for discussion). In
summary, the PPB is not necessary for somatic cytokinesis per sebut 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.
Cytokinesis and the cell cycle
the Arabidopsisanther, which undergo nuclear division with-out 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 distin-guished 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 simultaneous-ly, 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, result-ing in a sresult-ingle 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, tesand 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 under-go 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 mem-brane 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 Arabidopsiscellularising endosperm appears to involve tip growth: microtubule-associated membrane vesicles accu-mulate in front of the ingrowing membrane [36], and only the newly-forming membrane contains the cytokinesis-specific KNOLLE syntaxin [9•].
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 fac-tors 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 func-tional 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 forma-tion 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/endo-dermis cells is made in the embryo, in lateral roots and in adventitious roots grown from callus. Ablation studies per-formed 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 morpho-genesis, the shaping of embryos and organs, has been inferred from the analysis of the Arabidopsismutants fass and tonneau, in which randomly oriented cell divisions result in stunted plants with abnormally shaped organs [24]. In the maize mutants tangledand warty, however, the orientation of cell division can be perturbed without sig-nificantly affecting the overall shape of the leaf [42,43]. These results suggest that organ development is largely controlled at a supracellular level. The Arabidopsisresults are consistent with the opposite notion that the orientation of cell division influences organ shape.
A special function of cytokinesis in development is asym-metric cell division, which appears to segregate cell fates. For example, microspore cytokinesis yields a large vegeta-tive and a small generavegeta-tive 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 veg-etative 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 Arabidopsisalso 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
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 vesicle-fusion machinery? What motor molecules translocate the vesicles along the phragmoplast microtubules? How does the cell plate fuse with the plasma membrane at the later-al surface? How cytokinesis is regulated in time and space is still poorly understood. Cytokinesis is linked to cell-cycle 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 par-ticular, 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.
Acknowledgements
We thank Markus Grebe, Ulrike Folkers, Arp Schnittger and Axel Völker for critically reading the manuscript.
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