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Structure and Development |
Department of Biological Sciences, Illinois State University, Campus Box 4120, Normal, Illinois 61790-4120 USA
Received for publication June 6, 2003. Accepted for publication October 30, 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, Proceedings of the National Academy of Sciences, USA 99: 2812–2817). It was not known if such a mechanism was unique to flowering plants or whether it occurred more broadly in the plant clade. To determine if a polar mechanism of cell division might have been characteristic of the first plants, differential interference contrast optics were used to examine living cells of the charophycean green alga Coleochaete orbicularis, a close relative of plants, with cytokinesis involving a phragmoplast. By recording images in different focal planes over time, such "polarized" cytokinesis was found in cells dividing either parallel or perpendicular to the edge of this radially symmetrical organism. Previously reported differences between these two types of division in Coleochaete were clarified. Polarized cytokinesis appears to be an ancestral mechanism of plant cell division inherited from the highly vacuolate cells of the charophycean algal ancestors of plants.
Key Words: cell division • cell plate • cell wall • charophycean algae • Coleochaete • cytokinesis • plant evolution • vacuolate cells
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Hepler, 1982
; Samuels et al., 1995
; see Gunning, 1982
; Lloyd, 1991
; and Staehelin and Hepler, 1996
for review). The phragmoplast is usually first observed in the center of the cell, and, as the central part of the plate is complete, the phragmoplast moves centrifugally outward, allowing growth of the cell plate toward the cell periphery, where it finally attaches to the mother cell wall. Recently, using confocal microscopy on living cells, Cutler and Ehrhardt (2002)
described a mechanism in which highly vacuolate shoot cells, as well as some less vacuolate root cells, of Arabidopsis thaliana display so called "polarized" cytokinesis. In these cells, the nucleus is located on one side of a large vacuole. Hence, when the phragmoplast and cell plate move centrifugally outward from the telophase nuclei, they contact and attach to the mother cell wall on one side of the cell first and then move across to the other side of the cell, through the vacuole, rather than expanding uniformly from the cell center. As the phragmoplast and cell plate progress, they remain in contact with the mother cell wall. Cutler and Ehrhardt (2002)
point out that such a cytokinetic mechanism is not unique to Arabidopsis, citing previous reports of cytokinesis in wounded cells, callus, and tissue culture cells of other flowering plants. It was not known, however, how broadly such polar cytokinesis might occur in the plant clade.
To determine whether polar cytokinesis might have been present in the first plants, cytokinesis was examined in the charophycean green alga Coleochaete orbicularis. Plants (embryophytes) are defined by their life cycle, which includes a multicellular diploid embryo that is maintained on and nourished by its haploid parent. Molecular, biochemical, and morphological evidence indicates that the organisms most closely related to the ancestry of plants are the charophycean green algae (Graham et al., 1991
; Mishler et al., 1994
; Karol et al., 2001
). Charophyceans are morphologically diverse, including unicellular forms, unbranched filaments, and more complex branched filaments (for reviews see Graham, 1993
and Graham et al., 2000
). Branched filamentous charophyceans (members of the orders Charales and Coleochaetales) are most closely related to plants (Manhart and Palmer, 1990
; Starke and Gogarten, 1993
; McCourt et al., 1996
; Karol et al., 2001
).
The mechanism of cytokinesis varies among these diverse charophyceans. In unicellular and some unbranched filamentous forms, cytokinesis occurs by means of centripetal infurrowing of the plasma membrane and cell wall (Floyd et al., 1972
; Lokhorst and Star, 1985
; Lokhorst et al., 1988
; reviewed by Graham, 1993
), an apparently ancient method, because it is similar to what occurs in bacteria. In the unbranched filament Spirogyra, cytokinesis involves both centripetal furrowing at the cell periphery and a small central cell plate that forms by vesicle fusion in conjunction with a rudimentary phragmoplast (Fowke and Pickett-Heaps, 1969
; McIntosh et al., 1995
). Cytokinesis in Spirogyra has been interpreted as an intermediate stage in the evolution of cell plate formation involving a phragmoplast (reviewed in Pickett-Heaps et al., 1999
). Cytokinesis in Chara is like that of plants, except that cell plate formation occurs in a patchy manner across the whole cell at once, rather than centrifugally (Pickett-Heaps, 1967a
, b
, 1975
; Cook et al., 1998
).
The complex circular thalloid (disc-shaped) forms of Coleochaete, which include C. scutata and C. orbicularis, consist of a single layer of cells that are attached to a substrate, with growth occurring only at the periphery. Marginal cells may divide in one of two different directions, and, though both involve a phragmoplast, different mechanisms of cytokinesis have been reported in these two division directions (Marchant and Pickett-Heaps, 1973
; Brown et al., 1994
). In radial division, the new cell plate forms perpendicular to the edge of the thallus, and cytokinesis appears to be centrifugal, much like that of plants (though with some centripetal wall formation at the thallus edge), while in circumferential division, the new cell plate forms parallel to the edge of the thallus, and cytokinesis has been described as being centripetal, via vesicle fusion, in the presence of a possibly nonfunctional phragmoplast (Marchant and Pickett-Heaps, 1973
; Brown et al., 1994
). Previous workers interpreted the circumferential division mechanism of complex thalloid species of Coleochaete as an intermediate mechanism in the development of cytokinesis involving a plantlike phragmoplast, but they were puzzled by the combination of features described in circumferential division from their studies of fixed cells (transmission electron microscopy [TEM] or immunofluorescent tubulin) and speculated that the uneven size of the two daughter cells may hamper interpretation of this division (Pickett-Heaps et al., 1999
).
Coleochaete orbicularis was chosen for this study because it divides in association with a phragmoplast and because thalli are only one cell layer thick, facilitating studies of living dividing cells with differential interference contrast (DIC) optics. Live-cell imaging has led to exciting new discoveries of dynamic processes in plant cell biology in general (reviewed by Cutler and Ehrhardt, 2000
) and in plant cytokinesis in particular (Cutler and Ehrhardt, 2002
). Hence studies of living cells might also be expected to shed light on the incongruous characteristics previously described in circumferential cell division of complex thalloid forms of Coleochaete.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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), at 15°C with a 16 h/8 h light cycle. Coverslips were inverted and living thalli examined and photographed using DIC optics on an Olympus BX-60 microscope with either a 40x, 60x, or 100x planfluorite lens. Images were recorded on Fuji Sensia 100 or 400 film and digitized using a Polaroid Sprint Scan 35 film scanner.
Electron microscopy
Specimens were grown on ACLAR plastic (Ted Pella) under the conditions described and preserved via high pressure freezing in a buffered sucrose solution (modified from Ding et al., 1992
). Thalli were immersed for 30–60 min in a 20 mmol/L HEPES buffer solution (pH 8.5) containing 2 mmol/L CaCl2, 2 mmol/L KCl, and 0.2 mol/L sucrose and frozen in this same sucrose solution using a Balzers HPM010 high pressure freezer (Balzers Union, Liechtenstein). Specimens were freeze substituted with 1% osmium in acetone at –80°C for 3 d, –20°C overnight, brought slowly to room temperature over 2 h, rinsed with pure acetone, and infiltrated in three steps with Spurr's resin. Specimens were embedded between a coverslip and a microscope slide, polymerized in a 70°C oven, and glued with epoxy to blocks of hardened Spurr's resin. Thin sections (silver-gold) were stained for 10–15 min with aqueous Reynold's lead citrate and viewed using a Zeiss 10 transmission electron microscope at either 60 or 80 kV.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Radial division
At a single time point approximately midway through radial division (Figs. 1–4), the wall is most substantial near the top of the cell (Fig. 1) and progressively less so as one focuses toward the bottom of the cell (Fig. 4). Near the upper surface of the thallus (Fig. 1), the cell wall is developed across the cell (except at the thallus edge, where the chloroplast has not yet completely divided—discussed in section below entitled ``Chloroplast division and cytokinesis,'' see Fig. 23). At a slightly lower plane of focus (Fig. 2), telophase nuclei with nucleoli are evident (arrowheads), and a developing cell plate (arrow) is present between them. Closer to the bottom of the thallus (Fig. 3), the forming cell plate is more mature toward the edge of the thallus than it is across the rest of the cell, where it appears to be encountering the vacuole. Finally, at the lowest plane of focus (Fig. 4), the wall is present only at the outer edge of the thallus, where it has begun to progress through the vacuole (compare original vacuole shape in Fig. 8). Wall development reflects the position of the single large vacuole, which is located toward the bottom of the cell and the end of the cell away from the edge of the thallus. The developing cell plate forms first near the top of the cell, growing centrifugally from between the telophase nuclei (this early stage not shown), and progresses through the cytoplasm around the outside edge of the thallus where the vacuole is not present. Gradually, it cleaves the large vacuole in order to complete formation of the new cell wall. Because the cell is longer than it is thick, by the time the wall extends completely across the top of the cell (Fig. 1), it has already begun passing through the outer edge of the vacuole (Fig. 4; see Fig. 26).
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Cytokinesis over time
Comparison of forming walls over time in three planes of focus (Figs. 9–20) shows progression of the phragmoplast and cell plate in cells of Coleochaete orbicularis undergoing radial (Fig. 9, R) and circumferential (Fig. 9, C) divisions. In the top plane of focus of the radially dividing cell, the forming cell plate and phragmoplast (Fig. 9) develop into a substantial wall (Figs. 12, 15, 18). In the middle plane of focus, the radial wall progresses through the vacuole from the outside edge of the thallus toward the inside (Figs. 10, 13, 16, 19). In the bottom plane of focus, the radial wall at the initial time period (Fig. 11) is actually more developed than it is at the same time at a higher plane of focus (Fig. 10). This phenomenon is due to the wall being present beneath the vacuole in the lower plane of focus. At subsequent time periods, radial wall development in the middle plane of focus catches up with that in the lower plane of focus (Figs. 16, 17, 19, 20). Wall development in the circumferentially dividing cell progresses similarly over time. The most dramatic example is seen in the bottom plane of focus, where no wall is present at the initial time point (Fig. 11), a hint of a wall is present at the next time point (Fig. 14), and the phragmoplast and maturing cell plate are later visible across the cell (Figs. 17, 20).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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) described for highly vacuolate cells of Arabidopsis thaliana, a derived flowering plant. In both organisms, the nucleus resides at one edge of a large vacuole; hence, cytokinesis begins there between two telophase nuclei. As the cell plate and phragmoplast spread out centrifugally from this position, they contact the mother cell wall on the near side of the cell first, and then progress to the other side of the cell through the vacuole, moving along the mother cell wall on two fronts. Cutler and Ehrhardt (2002
, supplemental data on Proceedings of the National Academy of Sciences website) provide evidence that the forming cell plate is apoplastically connected to the mother cell wall early on during cytokinesis and suggest that in at least some cases peripheral cell wall "stubs" that have sometimes been reported to remain after cytokinesis has been interrupted by caffeine treatment (cited in Cutler and Ehrhardt, 2002
) may be the result of polar cell plate formation that was disrupted early in the process. The TEM observations of polar cytokinesis in cells of C. orbicularis (Figs. 24, 25) show that the forming cell plate is more mature at the edge, where it joins the mother cell wall, than it is in the center of the cell in the same plane of focus, lending support to the suggestion that the cell plate may be less sensitive to disruption where it contacts the mother cell wall.
Differences in the appearance of cytokinesis in Arabidopsis and Coleochaete are caused by variation in cellular organization. The highly vacuolate shoot cells of Arabidopsis studied by Cutler and Ehrhardt (2002)
are long brick-shaped cells, with a similarly shaped vacuole and many small chloroplasts. During cytokinesis in these cells, the forming cell plate encounters a regularly shaped vacuole. In contrast, C. orbicularis has more compact wedge-shaped cells with a single large chloroplast that divides in coordination with the rest of the cell (Brown et al., 1994
). The chloroplast takes up considerable space, preventing the vacuole from following the outline of the cell wall on all sides. Instead, the vacuole is located toward the bottom and inner walls of the cell. The nuclei are located beneath the chloroplast at the top outer edge of the cell; hence, it is in this region that the centrifugally expanding plate first encounters the mother cell wall. While cell plate formation in C. orbicularis generally proceeds from the top of the cell to the bottom, it occurs more rapidly in those places where the vacuole is not present. Hence, in radial division the cell plate forms more rapidly at the peripheral edge, while in circumferential division it forms more rapidly on either side of the vacuole. In addition, the single large chloroplast, at least in the case of radial division, affects the progress of cell plate formation. The chloroplast remains connected well into cytokinesis, and the cell plate forms late in the region of the chloroplast isthmus.
Despite the aforementioned differences due to cell organization, the fundamental process of cytokinesis in Arabidopsis and Coleochaete appears to be the same. The data presented here suggest that "polarized" cytokinesis (Cutler and Ehrhardt, 2002
) is not a derived mechanism unique to Arabidopsis and other flowering plants but rather an ancestral mechanism inherited from the highly vacuolate cells of the charophycean algal ancestors of plants. Examination of cytokinesis in other, morphologically diverse, species of Coleochaete (K. Doty and M. Cook, Illinois State University, unpublished data) supports this finding. Chaetosphaeridium is also a member of the order Coleochaetales and the sister taxon to Coleochaete (Delwiche et al., 2002
). It is not yet known whether this monoplastidic, highly vacuolate organism divides by means of a phragmoplast; study of Chaetosphaeridium is currently underway.
The zygnematalean alga Spirogyra has vacuolate cells that divide partly by means of a microtubular array interpreted as a rudimentary phragmoplast, but the nucleus is suspended in the center of the vacuole on cytoplasmic threads (Fowke and Pickett-Heaps, 1969
; McIntosh et al., 1995
), and cytokinesis is not polar. The only other order of extant charophycean green algae whose members are known to possess a plantlike phragmoplast are the Charales, the sister taxon to plants (Karol et al., 2001
). Dividing cells of members of the Charales are polyplastidic and not highly vacuolate (Pickett-Heaps, 1967a
). Cytokinesis occurs across the whole cell at once in a patchy manner in Chara (Pickett-Heaps, 1967a
, b
, 1975
; Cook et al., 1998
), with the cell plate attaching to the mother cell wall last (Cook et al., 1998
), as it does in centrifugal cytokinesis of plants (Samuels et al., 1995
). It is likely that a common ancestor of the Coleochaetales, Charales, and plants passed on both polar cytokinesis and strictly centrifugal cytokinesis to these advanced charophycean algae and to members of the plant clade. Hence, members of the Coleochaetales and Charales may serve as simple model organisms for studying cytokinesis in plants.
Studies of microtubular arrays associated with monoplastidic mitosis in some cells of bryophytes and vascular plants (see Brown and Lemmon, 1990
, 1993
, 1997
for review) have not focused on the presence of vacuoles or their position with respect to other cellular organelles, hence further observations are required to determine whether cytokinesis in these cells is polar. Such observations are essential for meaningful comparison of cytokinesis in charophycean algae and plants. For example, cytokinesis in monoplastidic cells of the liverwort Monoclea has been reported to involve both infurrowing and cell plate development by means of a phragmoplast, a combination of mechanisms compared with those in cytokinesis of Coleochaete (Brown and Lemmon, 1992
). Perhaps these cytokinetic features in Monoclea can be attributed to polar cytokinesis as they were here in Coleochaete. Comparisons of cytokinesis in charophycean algae and early divergent plants may contribute to our understanding of the evolution of cytokinesis in the plant lineage.
Cytokinesis in Coleochaete orbicularis
This study of living, dividing cells of Coleochaete orbicularis demonstrates that cytokinesis is similar not only in Coleochaete and Arabidopsis, but also in radial and circumferential division of Coleochaete. It also helps explain differences described previously (Marchant and Pickett-Heaps, 1973
; Brown et al., 1994
) between these two types of dividing cells in complex circular thalloid forms of Coleochaete. Because dividing cells of C. orbicularis are located at the periphery of a circular thallus that is attached to a substrate, they have both dorsal/ventral and peripheral/inner polarity. Though the process of cell division is basically the same in all peripheral cells, these different types of polarity in conjunction with the presence of a large vacuole and a single large chloroplast cause some differences in the appearance of cytokinesis in radially and circumferentially dividing cells. The present study corroborates some findings of previous studies and clarifies other observations that were previously puzzling.
The present observations that the chloroplast is located on the top and outer sides of peripheral cells in Coleochaete orbicularis and that the nucleus lies underneath the top portion of the chloroplast is consistent with previous findings for C. scutata (Marchant and Pickett-Heaps, 1973
), but contrary to a previous report for C. orbicularis (Brown et al., 1994
) that the chloroplast in circumferentially dividing cells is located on the edge and bottom of the cell with the nucleus above it. When a thallus is growing on a coverslip that is inverted for observation, it can be difficult to infer which surface represents the top of the thallus. Perhaps such confusion explains the previous report for C. orbicularis. The present light microscope observation that the nucleus is closely associated with the incised chloroplast in dividing cells agrees with previous TEM observation of a radially dividing cell (Graham and Kaneko, 1991
). A previous study of Coleochaete scutata, a close relative of C. orbicularis as inferred from molecular phylogenetic data (Delwiche et al., 2002
), demonstrated that the chloroplast divides during interphase (Marchant and Pickett-Heaps, 1973
). Here it was shown that in C. orbicularis the chloroplast remains connected at a narrow isthmus well into cytokinesis and that the cell plate forms late in the region of the chloroplast isthmus, at least in radial division.
Two uncertainties previously concerning cytokinesis in Coleochaete orbicularis are resolved by the present study: (1) cell division is shown to be polar overall, with the cell plate moving out centrifugally from between the daughter nuclei and then generally proceeding from the top side of the cell to the bottom in both radial and circumferential division, and (2) cytokinesis is shown to be accomplished by means of a phragmoplast that is located along the plane of the forming cell plate in both types of division. Hence, Coleochaete does not have two types of division that represent an evolutionary transition from centripetal furrowing to a centrifugal phragmoplast as previously suggested. The related alga Spirogyra, which undergoes cytokinesis involving both furrowing and a cell plate formed via a phragmoplast precursor (Fowke and Pickett-Heaps, 1969
; McIntosh et al., 1995
), would instead be a potential model organism for understanding the transition from centripetal furrowing to centrifugal cell plate formation in the charophycean ancestors of plants.
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FOOTNOTES |
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2 E-mail: <mecook1{at}ilstu.edu
>
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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