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Cytokinesis: The Art of Partitioning

Gerd Jürgens
Gerd Jürgens
Center of Plant Molecular Biology University of Tübingen Auf der Morgenstelle 1 D-72076 Tübingen Germany
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Published June 2000. DOI: https://doi.org/10.1105/tpc.12.6.827

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In higher plants, cytokinesis partitions the cytoplasm of a dividing cell by forming a new cell wall between the two sets of daughter chromosomes. Although conceptually simple, this process involves a sequence of well-orchestrated events, starting with the determination of the division plane before the onset of mitosis (reviewed in Staehelin and Hepler, 1996; Heese et al., 1998; Smith, 1999). A transient preprophase band of microtubules and actin microfilaments marks a cortical division site which is in the same plane as the dividing nucleus. Following disintegration of the nuclear envelope and formation of the mitotic spindle, the chromosomes condense, align, and separate before the spindle moves the daughter chromosomes away from the division plane. Remnants of the spindle are incorporated into the phragmoplast, which appears in the interzone in late anaphase. The phragmoplast consists of two opposing sets of microtubules and actin microfilaments with their plus ends toward the plane of division. The phragmoplast mediates the translocation of Golgi-derived vesicles to the division plane where the vesicles fuse with one another to form the cell plate, a transient membrane compartment. The disc-shaped cell plate expands from the center of the division plane to the periphery and eventually fuses with the lateral cell wall at the cortical division site. During cell plate expansion, the phragmoplast microtubules depolymerize in the center and repolymerize along the edge such that additional Golgi-derived vesicles are targeted to the margin of the cell plate. While expanding, the cell plate undergoes a complex transformation from an initial network of thin fusion tubes to a solid plate, with polysaccharides secreted into its lumen (Samuels et al., 1995). In summary, somatic cytokinesis is a phragmoplast-assisted process of cell plate formation and expansion driven by targeted vesicle fusion.

The dynamics of the cell division process are not well understood, although a number of proteins have been localized either to the cytoskeletal arrays involved in cell division or to the forming cell plate. For example, the large GTPase phragmoplastin (also called Arabidopsis dynamin-like protein) accumulates in the cell plate (Gu and Verma, 1997; Lauber et al., 1997). However, it is not known whether this protein plays a role in the formation of thin fusion tubes from vesicles and/or is needed in the removal of excess membrane from the maturing cell plate. Another example is a MAP kinase that is activated in mitosis and localized to the cell plate (Bögre et al., 1999). Although the localization data suggest a role in cell division, the functional analysis of proteins requires some sort of bioassay. On pages 979–990 of this issue of THE PLANT CELL, Vos et al. report on use of microinjection into living stamen hair cells of Tradescantia to determine the role of the kinesin-like calmodulin binding protein (KCBP) in the process of cell division. KCBP is a minus-end directed microtubule motor protein (Song et al., 1997) that localizes to the cytoskeletal arrays associated with cell division, such as preprophase band, mitotic spindle and phragmoplast, but does not colocalize with cortical microtubules during interphase (Bowser and Reddy, 1997; Smirnova et al., 1998). KCBP interacts with microtubules in vitro, and this interaction is inhibited by calmodulin (CaM). The inhibition is abolished by an antibody raised against a peptide derived from the calmodulin binding domain of KCBP, suggesting that the antibody may keep KCBP in a constitutively active form (Narasimhulu and Reddy, 1998). To test this idea, the authors microinjected the anti-KCBP antibody into stamen hair cells at different stages of the cell cycle.

The authors report that injection into interphase cells does not block cytoplasmic streaming—in contrast to an anti-CaM antibody—thus ruling out nonspecific interference with physiologic processes. Injection into mitotic cells has differential effects. Late prophase cells are induced to break down the nuclear envelope precociously. Cells at prometaphase do not progress to anaphase. Their chromosomes condense as if arrested at metaphase, although the chromosomes do not subsequently stay aligned. By contrast, cells injected at late metaphase or early anaphase complete anaphase, and a considerable proportion displays telophase arrest without forming a phragmoplast or a cell plate. To test whether the microtubule cytoskeleton had been destroyed, the authors injected rhodamine-labeled tubulin prior to injection with the anti-KCBP antibody. Although the nuclear envelope break down precociously and the cells are subsequently arrested at prometaphase, rhodamine-labeled microtubules are still present. These results suggest that KCBP is involved in microtubule organization during M phase. The authors present a model in which they propose a role for KCBP in microtubule bundling and spindle assembly. Because KCBP shares sequence similarity with Xenopus XCTK2 and Drosophila Ncd, two proteins associated with the spindle poles and involved in the formation of convergent bipolar spindles, the authors propose that KCBP plays a similar role. Another interesting feature discussed by the authors relates to the role of calcium in cell division. Specifically, CaM inhibits the interaction of KCBP with microtubules in vitro only in the presence of calcium. To explain the stage-specific effects of the anti-KCBP antibody, one could postulate that calcium is released from internal stores, such as from the ER, differentially and locally during M phase. In any event, the present report suggests a mechanistically plausible model of how calcium concentration could be involved in the reorganization of the microtubule cytoskeleton during cell division.

Although cytokinesis is usually tightly coupled to nuclear division, this is not always the case. One obvious exception occurs in the endosperm, which originates from the triploid fusion product of a sperm cell with the large central cell of the embryo sac. Initially, several rounds of synchronous nuclear divisions proceed without cytokinesis (Mansfield and Briarty, 1990; Olsen et al., 1995; Berger, 1999; Brown et al., 1999). The syncytial endosperm is then cellularized by the formation of anticlinal (radial) cell walls between the nuclei which have migrated toward the cell surface (Mansfield and Briarty, 1990; Olsen et al., 1995; Brown et al., 1999). How the cytoplasm of the large cell is partitioned to the nonmitotic nuclei has been controversial. According to the prevailing view, membrane furrows grow inward from the surface and separate neighboring nuclei. Such a process would be formally similar to cellularization of the Drosophila syncytial blastoderm embryo, during which membrane material is delivered to the base of inwardly growing furrows in a syntaxin-mediated manner (Burgess et al., 1997). In the Arabidopsis endosperm, microtubules and vesicles have been observed at the tips of inwardly growing membrane furrows (Mansfield and Briarty, 1990), suggesting that the anticlinal cell walls are formed by tip growth. Similar observations have been reported for other species (reviewed in Olsen et al., 1995); however, there is also evidence supporting the alternative view that anticlinal cell wall formation resembles cytokinesis of somatic cells. In the cellularizing wheat endosperm, membrane vesicles accumulate between adjacent nuclei and form a cell plate which then expands toward the surface of the central cell while its opposing “free” end grows toward the vacuole (Fineran et al., 1982). Compatible with either view is the observation that the newly forming cell membranes of the cellularizing Arabidopsis endosperm accumulate the cytokinesis-specific KNOLLE syntaxin (Lauber et al., 1997). This result also suggests that endosperm cellularization is mechanistically related to phragmoplast-assisted cytokinesis of somatic cells.

On pages 933–947 of this issue of THE PLANT CELL, Otegui and Staehelin take a fresh look at cell wall formation in the syncytial endosperm of Arabidopsis. The authors take advantage of the high-pressure freezing/freeze substitution technique, which better preserves membrane structure than does chemical fixation (Samuels et al., 1995). In addition, they focus on the micropylar zone of endosperm surrounding the developing embryo, where the single layer of nuclei is in a two-dimensional array parallel to the surface of the large central cell. In this region, cellularization results in a honeycomb-like organization of new anticlinal cell walls. At the time of cellularization, no mitotic spindles are present, but microtubules radiate from the surface of the nonmitotic nuclei. The process of cellularization is resolved in exquisite detail. Small groups of oppositely oriented microtubules, called mini-phragmoplasts, are assembled and assist in the formation of a special type of cell plate (syncytial-type) between sister and nonsister nuclei. Unlike the directional expansion and maturation of the cell plate in somatic cytokinesis, a patchwork of local cell plates is formed simultaneously by multiple mini-phragmoplasts. Initially, Golgi-derived vesicles fuse to form hourglass-shaped intermediates, which give rise to 45-nm wide tubules, unlike the narrow fusion tubes observed in somatic cells. The wide tubules coalesce into networks, and adjacent wide tubular networks merge into a coherent cell plate network that undergoes maturation in a patchy pattern. The authors also analyzed the composition of syncytial-type cell plates and endosperm cell walls using specific antibodies. Two distinctive features of this analysis are the lack of fucosyl residues on xyloglucans and the persistence of callose in the cell walls after the cell plate has fused with the parental plasma membrane, which may be related to the role of the endosperm in seed development.

So what is the take-home message? In a simplified view, partitioning of the cytoplasm appears to be comparable in endosperm cellularization and somatic cytokinesis, although the details differ. In both processes, Golgi-derived vesicles are translocated to the plane of partitioning by phragmoplast microtubules, and vesicle fusion, mediated by the cytokinesis-specific KNOLLE syntaxin, results in cell plate formation. In this way, endosperm cellularization can be viewed as a variant of somatic cytokinesis. It may thus be worthwhile to reexamine, with the high-pressure freezing/freeze substitution technique, other modes of cytokinesis that have been described for meiotic and gametophytic cells, to elucidate their similarities and dissimilarities to somatic cytokinesis.

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Cytokinesis: The Art of Partitioning
Gerd Jürgens
The Plant Cell Jun 2000, 12 (6) 827-829; DOI: 10.1105/tpc.12.6.827

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Cytokinesis: The Art of Partitioning
Gerd Jürgens
The Plant Cell Jun 2000, 12 (6) 827-829; DOI: 10.1105/tpc.12.6.827
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The Plant Cell Online: 12 (6)
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Jun 2000
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