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(American Journal of Botany. 2008;95:643-654.) doi: 10.3732/ajb.2007210 © 2008 Botanical Society of America, Inc. |
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Anatomy and Morphology |
2 Cullman Program for Molecular Systematics Studies, New York Botanical Garden, Bronx, New York 10458 USA 3 Department of Botany, Academy of Natural Sciences, 1900 Benjamin Franklin Parkway, Philadelphia, Pennsylvania 19103 USA 4 Department of Cell Biology and Molecular Genetics, University of Maryland, College Park, Maryland 20742 USA
Received for publication 8 July 2007. Accepted for publication 7 March 2008.
ABSTRACT
Patterns of cell division and cross wall formation vary among the charophytes, green algae closely related to land plants. One group of charophytes, the conjugating green algae (Zygnematophyceae), is species-rich and is known to vary substantially in the mode of cell division, but the details of these cell division patterns and their phylogenetic distribution remain poorly understood. We studied cross wall development in filamentous Desmidiaceae (a clade of conjugating green algae) using differential interference contrast and fluorescence light microscopy. All strains investigated had centripetal encroachment of a septum, but with several different developmental patterns. In most cases, cell wall formation was delayed with respect to the Cosmarium-type of cell division, and the cross wall was modified considerably after deposition in a manner specific to the particular clade of filamentous desmids. These characteristics were mapped on a phylogeny estimated from a data set of two organellar genes, and the evolutionary implications of the character state distribution were evaluated. The data suggest a complex history of evolution of cell division in this lineage and also imply that Desmidium and Spondylosium are polyphyletic. These results indicate that many features of the cell shape are determined at the time of cell division in conjugating green algae.
Key Words: Desmidiaceae • cell division • coxIII • development • rbcL • septum formation • Zygnematophyceae
Cell division is a fundamental process critical to the proliferation of all cells. In plants and many algae, cytokinesis is simultaneous with the construction of a new extracellular wall. Land plants generally share a single mode of cell division involving the formation of a phragmoplast, but their close algal relatives, the charophytes, have many differences in their modes of cell division.
The nature of cell wall deposition plays an important role in determining the shape of the cell or, in unicellular species, the structure of the organism. Changes in the process of cell division are considered important steps in the evolution of complex cellular organization (Graham et al., 2000
). In Coleochaete, for example, the ability to control the plane of cell wall deposition allows the filaments to bifurcate and leads to the branched thallus characteristic of the genus. Transitions from unicellular to filamentous forms have occurred many times in the evolution of the conjugating green algae (Zygnematophyceae) (McCourt et al., 1995; Gontcharov et al., 2003). Their close relationship to land plants makes the Zygnematophyceae an exceptional model for studying the process of cell division and morphogenesis and provides insight into the evolution of multicellularity in the lineage that gave rise to land plants (Karol et al., 2001; Turmel et al., 2006; Hall and Delwiche, 2007).
Many algae lack a cell wall, but all charophytes (except Mesostigma, which has scales), have a cellulosic cell wall (Graham and Wilcox, 2000). Among charophytes, cell wall formation proceeds by centrifugal growth of a cell plate (land plants and Coleochaetales) (Cook, 2004), uniform deposition of material along the cross wall (Chara) (Cook et al., 1998), or by centripetal encroachment of a peripheral septum (Zygnematophyceae, Klebsormidiophyceae, and Chlorokybus) (Graham et al., 2000). The Zygnematophyceae, however, are known to have several different variations of centripetal cell division (Brook, 1981). The diversity of patterns of cell division among the conjugating green algae is far greater than that found among land plants, but has received little investigation.
Some Zygnematophyceae, such as Zygnema, apparently undergo cell division exactly as Klebsormidium and Chlorokybus do. However, many constricted species—that is, those that are divided into semicells connected by a narrow cytoplasmic isthmus—have the "Cosmarium-type" cell division. In this mode, the division septum forms soon after mitosis, and before any substantial cellular elongation. The two new semicells then expand, and the secondary wall is not deposited until the semicell is nearly fully formed (Pickett-Heaps, 1972; Meindl, 1993). In the Desmidiaceae, one of four families of conjugating green algae commonly referred to as desmids, the primary wall is subsequently shed in its entirety or in fragments leaving only the secondary wall in mature cells (Pickett-Heaps, 1972). Details of the Cosmarium-type cell division are relatively well understood, and a number of interesting cytoskeletal and nuclear phenomena have been described (Meindl, 1983, 1986, 1988; Holzinger and Lutz-Meindl, 2002, 2003).
Although the Cosmarium-type of cell division is common among constricted desmids, it is not the only means of division known for constricted cells. In Onychonema laeve, a filamentous desmid with constricted cells, a common vesicle (termed a division vesicle by Krupp and Lang [1985b]) forms between the semicells. This vesicle enlarges to nearly the size of an adult semicell before a division septum forms. Once the new cross wall forms, the semicells continue to grow and take the shape of their parent cell, in this case forming apical processes and lateral spines. The filamentous habit is maintained by the persistence of a fragment of primary wall between adjacent cells; however, most of the primary wall is jettisoned as in other Desmidiaceae (Krupp and Lang, 1985b).
Perhaps the most remarkable variation of centripetal cell division is represented by Bambusina borreri. In this alga, after the new cell wall forms during cytokinesis, a cylinder of primary and secondary cell wall is deposited in the center of the cell. This cylinder results in what appears to be folds, termed replications (Brook, 1981), in the cross wall. As the cells elongate, these cylinders evert and flatten, which results in a nearly full-size cell with a complete wall (Gerrath, 1973; Krupp and Lang, 1985a). This kind of cell division was thought to be typical of many filamentous desmid genera, specifically Bambusina, Desmidium, Streptonema, and Haplozyga (Krupp and Lang, 1985b).
Still other forms of cell division are known among the filamentous desmids. Hyalotheca, for example, uses centripetal cell division similar to Zygnema and Mougeotia (Acton, 1916; Krupp, 1980). This mode differs, however, in the accumulation of a band of "membrane" around the midregion before cytokinesis (Hauptfleisch, 1888).
Cell division has not been explicitly studied in a number of filamentous Desmidiaceae. In these taxa, the mode of cell division is inferred from the presence of cross walls of a particular shape, or cell division is assumed to be the same as that of superficially similar unicellular and filamentous species. All known cell division patterns in Zygnematophyceae are variations of centripetal cell division shared with Klebsormidium and Chlorokybus.
In the course of a molecular survey of the conjugating green algae and extensive field study, we observed undocumented variation in cell division among filamentous Desmidiaceae. To understand the phylogenetic and developmental significance of this variation, we undertook a broad preliminary survey of cell division in these taxa and placed that diversity in the context of molecular phylogenetic data. In addition to reporting characteristics of cell division for a number of genera and species, we also explored evidence concerning the evolution of centripetal cell division within the Zygnematophyceae as inferred from chloroplast and mitochondrial gene phylogenies.
MATERIALS AND METHODS
Terminology
For the purpose of this paper, "cell division" refers to the entire process of division from premitotic elongation of cells through chloroplast division, mitosis, cytokinesis; the primary and secondary walls could not be differentiated with the techniques used. However, wall material deposited during cytokinesis is assumed to be primary wall. Subsequent thickening of this wall is presumed to be the result of secondary wall deposition. Chloroplast and nuclear divisions, when observed, are referred to separately. A "cross wall" refers not only to the primary wall or the position of wall deposition, but rather to the wall (sometimes with, presumably, both primary and secondary materials) that is deposited before a final stage of elongation in filamentous species. We follow previous authors in using terminology that parallels wall terminology for plants (Gerrath, 1973; Krupp and Lang, 1985a). The first wall deposited during cytokinesis is referred to as the primary wall and the subsequent thickened layer deposited inside the first wall as a secondary wall.
An isthmus is considered elongated if a constricted cell (those with a defined isthmus) noticeably deposits wall material along the isthmus, resulting in a tube connecting semicells. An inflated vesicle results when this tube increases in width to form a larger, semicell-shaped space. This inflated isthmus was termed a division vesicle by Krupp and Lang (1985b), and we follow that terminology.
Culture conditions
Strains were obtained from public culture collections or isolated from the wild (Table 1). All strains were grown in Guillard’s Woods Hole medium (Nichols, 1973) in a Percival (Perry, Iowa, USA) growth chamber under Sylvania (Danvers, Massachusetts, USA) Cool White fluorescent lamps with irradiance of 30 µE on a 16 h : 8 h light : dark cycle at 15°C. Cells were observed at several times throughout the day with many cross walls visible 
2 h into the light cycle. Dividing cells could be found at any time of day.
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) and sequenced using Big Dye Terminator sequencing technology on an Applied Biosystems (Foster City, California, USA) 3100 capillary sequencer. Fragments were sequenced in both directions and assembled using the program Sequencher version 4.2 (GeneCodes, Ann Arbor, Michigan, USA). Sequences were aligned with the program MacClade version 4.7 (Maddison and Maddison, 2000). Phylogenetic analyses were performed using the program PAUP* (Swofford, 2003). Under the maximum parsimony criterion (MP), a heuristic search with 10 random taxon addition sequences and tree-bisection-reconnection (TBR) branch swapping was used. Support for taxon bipartitions was estimated using the nonparametric bootstrap (BS), with 500 pseudoreplicates and 10 random taxon addition sequences in each pseudoreplicate. Under the maximum likelihood criterion (ML) we used the GTR+I+G model of sequence evolution, as recommended by the program MrModeltest 2.2 (Nylander, 2004), with parameters estimated from the data. One hundred bootstrap replicates were run with three random taxon addition sequences per replicate. Two analyses in MrBayes (BI), each using four chains sampled for four million generations, sampled every 100 generations, were used to estimate the topology and posterior probabilities (PP) of the taxon bipartitions. The first 2000 trees were discarded as burnin, the point at which the likelihood had reached stationarity.
Light microscopy
Living cells were observed at various stages of cell division using a Zeiss (Thornwood, New York, USA) Axioskop microscope. Image data were recorded as digital micrographs using an AxioCam HRc CCD camera (Zeiss). Many cells at different stages of cell division were observed, and when possible a single cell was followed through a division cycle. In most cases, cross walls were visible using DIC microscopy; however, some stages were recorded by staining the cells with the cellulose-specific fluorochrome Calcofluor. When staining, cells were harvested by gentle centrifugation and fixed with 3% glutaraldehyde (v/v) in Guillard’s Woods Hole medium for 20 min. Cells were allowed to settle and rinsed once in the medium, and stained for 1 h with 1% Calcofluor (w/v). Cells were rinsed for 10 min three times in the medium and viewed on the same microscope using an HBO 50 Mercury arc lamp (excitation near 395 nm) and a long-pass emission filter of 470 nm.
RESULTS
Cross walls
The order of cellular events such as cell wall deposition differed among the species. All cross walls formed by the centripetal encroachment of a peripheral septum. Complex features of the cross wall formed after cytokinesis and the initial deposition of wall material. Many differences in cross wall structure were only apparent in the fully mature cross walls (that is, cross walls just before the cells elongated to form mature semicells). Calcofluor effectively stained material interpreted to be secondary wall material; however, the first walls deposited were not always visible when stained with Calcofluor, even when they were visible with DIC. This difficulty was particularly noticeable in Hyalotheca spp., Spondylosium pulchellum, Teilingia granulata, and Spondylosium tetragonum.
Teilingia granulata
Teilingia cells are somewhat rectangular, and the semicells are connected across a narrow isthmus. In strains of T. granulata, after chloroplast division, the cells elongated at the isthmus to form a narrow tubular connection approximately the width of the isthmus (Figs. 1J3, 3D). A cross wall then formed across this elongated isthmus. The resulting semicells further elongated, and the new semicell enlarged, forming the mirror image of the parent semicell when fully developed (Fig. 1 J4).
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Hyalotheca dissiliens and H. mucosa
Hyalotheca cells are cylindrical and very subtly constricted in the midregion. In both species, cells elongated somewhat before a cross wall was deposited. The new cross wall, formed before and during cytokinesis, was observed to be much thinner than the parent semicell walls and stained poorly with Calcofluor. Encroachment of a peripheral septum was observed. This cross wall was irregular initially, but became linear as it thickened. The daughter cells then further elongated and walls on the new semicell thickened.
Groenbladia taylorii
Cells of G. taylorii are cylindrical and not noticeably constricted. When G. taylorii elongated before cytokinesis, it was apparent in some Calcofluor-stained cells that new wall material was deposited at the isthmus (Fig. 3B). Before cross wall deposition, an accumulation of light-transparent material formed along the inner surface of the cell at the site of cross wall formation (Fig. 3A, arrow). Encroachment of a peripheral septum was observed. Following cytokinesis, the newly formed semicells further elongated. Often, the chloroplast would then divide, leaving two chloroplasts in the interphase cells.
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for details.
Desmidium grevillei
Cells of D. grevillei are cylindrical, broader than long, and connected along the entire apex. Early in cell division, cells of D. grevillei elongated at the median constriction, sometimes resulting in what appeared to be a shared vesicle (Fig. 1E4). After elongation, the cell deposited a cross wall and then a cylinder (replication) of cell wall material was deposited in the center (Fig. 2C, D). These cylinders were about 2–3 µm in amplitude compared to the nearly 5 µm cylinders found in B. borreri.
Onychonema laeve var. micracanthum and O. filiforme
Semicells of Onychonema are reniform and connected by a narrow isthmus. Before cytokinesis, the isthmus of Onychonema cells elongate and inflate to form a large shared vesicle (division vesicle) between the semicells (Fig. 3E, F; Krupp and Lang, 1985b). Subsequently, a division septum divided the vesicle somewhat asymmetrically at an oblique angle (Fig. 3E, F). Once separated, the new daughter semicells rounded at the angles and continued to expand. After the wall was deposited, the apical processes characteristic of Onychonema became apparent.
Desmidium aptogonum, D. aptogonum var. ehrenbergii, D. baileyi, and D. swartzii
Cells of these species are angular (usually triangular) in apical view, broader than long and connected by apical processes leaving open space between adjacent cells. Before cytokinesis, cells elongated at the isthmus (Fig. 1C3, 2E–H). In species with a median constriction, elongation resulted in what appeared to be a division vesicle, which was then divided by a plane cross wall. Unlike Bambusina, a cylinder of cell wall material was deposited at each angle of the semicell where the cells would be connected by apical processes, rather than in the center of the cell (Fig. 2E–H). The number of such cylinders correlated to the number of apical processes found in the cell: the biradiate Desmidium aptogonum var. ehrenbergii had two, the triradiate D. baileyi had three, and quadriradiate forms of Desmidium had four (not shown). The size of these cylinders was approximately proportional to the length of the apical processes of the mature cells and generally much smaller in diameter than those of Bambusina and D. grevillei. Desmidium baileyi, which has long process (>5 µm), had the largest fold (also >5 µm). Desmidium swartzii, which has very short processes, also had very short replicate folds, each fold being between 1 and 2 µm long. These cylinders were apparent when the cells were stained with Calcofluor but difficult to see in untreated cells. With DIC, the folds were visible but were often obscured by cytoplasmic contents in living cells. Division cylinders among these species differ from those of Bambusina and D. grevillei in number, position, relative size, and, most importantly, in their association with apical processes.
Spondylosium pulchrum
Cells of S. pulchrum are very deeply constricted and have a small apical process that is the point of connection between adjacent cells. Cell division in S. pulchrum differed from that of other Spondylosium species investigated. In this species, the cells initially elongated at the isthmus, and the isthmus inflated into a division vesicle similar to that found in Onychonema. It is not known whether karyokinesis takes place in this vesicle. A cross wall then divided the vesicle, and a small cylinder of cell wall material was deposited in the center of the cross wall. This cylinder was very small and appeared, as in Desmidium swartzii, as a small bubble on the cross wall (Fig. 2I, J). This mode of cell division was most similar to that of D. baileyi, differing primarily in the scale of the features.
Micrasterias foliacea, Phymatodocis, Heimansia, and Cosmocladium
Cell division patterns of two filamentous and two colonial desmids included in the phylogeny (Phymatodocis, Micrasterias foliacea, Heimansia, and Cosmocladium) were not investigated. Only division in M. foliacea has been studied in detail (Lorch and Engels, 1979) and was found to be of the Cosmarium-type. These are all thought to use the Cosmarium-type cell division (see Spondylosium pulchellum in this study). Our observations were consistent with this hypothesis but insufficient to confirm it.
Molecular phylogenetic analyses
Phylogenetic analyses were performed on a data set containing nearly full-length fragments of the chloroplast gene rbcL and the mitochondrial gene coxIII. Outgroup species were selected from a previous study (Hall et al., 2008), and species within the filamentous clade were added to this analysis. Many other strains of filamentous Desmidiaceae were screened for differences in cross walls.
With the exception of Phymatodocis and Micrasterias foliacea, the filamentous and colonial species were found in a single lineage (Fig. 4) (90/98/1.0; MP/ML/PP). Within this clade, two lineages were resolved: one containing Teilingia granulata, Spondylosium tetragonum, and Cosmocladium saxonicum and the other containing the remaining filamentous or colonial species (Fig. 4). In the first lineage, Cosmocladium, a colonial desmid connected by delicate cell wall strands, diverged first. Spondylosium tetragonum was sibling to a clade of Teilingia granulata. Teilingia strains had some sequence and structural diversity (see Discussion).
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DISCUSSION
Cell division is of fundamental importance to living organisms. The processes of cell division and cell wall formation are thought to be highly conserved between even distantly related taxa. For example, aspects of cell division and mitosis (along with other cytological characteristics) led Mattox and Stewart (1984) to conclude that charophytes and land plants were closely related. Differences in cell division among living species of charophytes provide much insight into the variability possible in this important process. Developmental similarities may also indicate which aspects of cell division are conserved.
Several modes of cell division are well characterized among the conjugating green algae (Brook, 1981). Of the two orders of conjugating green algae, the Zygnematales and the Desmidiales (Mix, 1972; Hall et al., 2008), this diversity is concentrated among the latter. The filamentous Zygnematales, use simple centripetal cell division involving the encroachment of a peripheral septum. In at least some species of Spirogyra and probably some Mougeotia, cell division also involves a cytoskeletal array similar to a phragmoplast (Fowke and Pickett-Heaps, 1969a,b; Galway and Hardham, 1991). Among the Desmidiales, the most common form of cell division is the Cosmarium-type. The filamentous Desmidiales have still more diversity in their modes of cell division, and these modes are compared to the Cosmarium-type for convenience.
Among the filamentous Desmidiales, the Cosmarium-type cell division has now been observed in Spondylosium pulchellum, Cosmocladium saxonicum, and the distantly related Micrasterias foliaceae and Phymatodocis nordstedtiana. Besides those species using the Cosmarium-type cell division, all filamentous Desmidiaceae delay deposition of cell wall material with respect to the Cosmarium-type. The differences among these modes of cell division mostly hinge on the order and extent of cellular processes.
We observed that Teilingia granulata and Spondylosium tetragonum delay primary wall deposition until after an initial phase of elongation. This delay results in the formation of an elongated isthmus in Teilingia and elongated cells in Spondylosium tetragonum. These "vesicles" do not inflate, which distinguishes them from similar structures in Onychonema and S. pulchrum. In all other aspects, cell division in Teilingia and S. tetragonum seems to be very similar to the Cosmarium-type.
Besides the Cosmarium-type cell division, there are four modes of cell division known among the filamentous Desmidiaceae: the Hyalotheca type, Bambusina type, Desmidium type, and the Onychonema type. Cell division in Groenbladia taylorii is similar to that in Hyalotheca as described by Hauptfleisch (1888). In these species, cells elongate without forming an inflated division vesicle. Hauptfleisch (1888) observed a ring of "membrane" that formed along the inner surface of the cells of Hyalotheca in the region of the isthmus during cell division. A similar observation was made in G. taylorii (Fig. 3A, arrow), although we are not certain of the composition of the aggregation.
In Onychonema, deposition of wall material is delayed until after an initial phase of elongation (Krupp and Lang, 1985b). The resulting vesicle increases in width to nearly the size of a mature semicell before it is divided transversely by a wall. The inflated vesicle of Onychonema is similar to the early developing semicells of Cosmarium in that the vesicle consists of mostly primary wall material (Krupp and Lang, 1985b).
The cylinders of cell wall material deposited on the mature cross walls of Desmidium and Bambusina share no known homologs among green algae. A similar structure is found in some Spirogyra (Transeau, 1951); however, in that organism the cylinders are present on the mature cells and are not part of the process of cell division as in Desmidium and Bambusina. Convergence of two lineages of desmids on this similar mechanism would be surprising and the apparent distribution of the characteristic may be the result of losses rather than convergence. Nevertheless, these lineages are separated phylogenetically by organisms with other modes of cell division (Fig. 4). Additionally, species in these two lineages differ somewhat in the placement of the cylinders on the mature cross wall. In the case of Bambusina borreri and Desmidium grevillei, a single cylinder is found in the center of the cell. In Spondylosium pulchrum and the Desmidium II clade, the cylinders are positioned at the site of future apical processes and vary in number as a function of the number of apical processes.
Cell division in Spondylosium pulchrum had not been previously described in detail. The only known reference to its mode of cell division is found in Scott and Prescott (1958) where it is compared to cell division in Streptonema trilobatum Wallich. Although somewhat indirect, Scott and Prescott (p. 71) posit that a division cylinder is formed after a cross wall is deposited, but that it forms by the "infolding of the apical wall." While mostly consistent with our data, the folds do not seem to form from the infolding of the wall, but rather from the deposition of new wall material in a cylindric form as described for Bambusina (Gerrath, 1973; Krupp and Lang, 1985a). Spondylosium pulchrum is somewhat unlike most other filamentous desmids in that spaces are sometimes observed between adjacent cells in a filament. Scott and Prescott (1958) suggested that filaments are held together by mucilagenous pads. Connection by mucilaginous pads would not be expected since, in those species that have been characterized by TEM—Bambusina, Desmidium, Hyalotheca and Onychonema—the cells in the filament are held together by shared primary wall (Gerrath, 1973; Krupp, 1980; Krupp and Lang, 1985a, b).
These observations are supported by dozens of published images of cells in the process of division (Table 2). Only two drawings appear to be inconsistent with our results. In one case, the drawing may depict a cell that has almost completed cell division (Förster, 1974). In the other case (Förster, 1964), there is no obvious explanation for the discrepancy except to say that the diagnostic characteristics in that species would be very small, and the report was based on fixed material and most likely a single cell. Other images showing a flat cross wall in Desmidium and Bambusina would seem to be inconsistent with our results; however, in these species a flat cross wall is initially deposited and the characteristic cylinders of cell wall material develop later. The association of division cylinders with an apical process (a cellular projection) was anecdotally observed (Croasdale et al., 1983), but the developmental significance and taxonomic implications were not discussed.
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). In the case of Teilingia, cells were followed through a division cycle and found to separate normally. It has been shown experimentally that cytokinesis is delayed when cells are grown at elevated temperatures (Meindl, 1990). In this study, all observations were made on strains grown at 15°C, so the delay in cytokinesis is unlikely to be temperature induced.
Most filamentous Desmidiaceae were resolved in a single lineage in this analysis; however, another study based on 18S rDNA sequences found two clades of filamentous desmids (Gontcharov et al., 2003). These two clades are probably analogous to the clades described here as clade 1 and 2 (Fig. 4). Although cell division in Groenbladia and Teilingia are superficially similar, these species were resolved in separate clades among organisms with other modes of cell division (Fig. 5).
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).
Two previous studies showed that species of Spondylosium were polyphyletic (Gontcharov et al., 2003, 2004). Part of this confusion was the result of the misidentification of two strains of Teilingia (previously reported as S. planum and S. secedens) (Hall et al., 2008). A polyphyletic Spondylosium was also found in this study. We believe that our strains are correctly identified, and the apparent phylogenetic relationships of the organisms are supported by the observation that the three lineages have three different kinds of cell division (Fig. 5). The clade of Teilingia granulata has more sequence diversity than is found in other desmid species (J. Hall, unpublished data). In addition to this sequence diversity, there were also structural differences among the strains. Strains differed in cell sizes and the degree of constriction (data not shown). Within each strain, some cells lacked the apical granules characteristic of the genus.
Although several modes of cell division were known for conjugating green algae, the species investigated in this study are unique in that they are filamentous representatives of a species-rich and mostly unicellular family, the Desmidiaceae. Accordingly, cell division in this lineage brings some evidence to bear on the evolution of multicellularity in charophytes. Few desmid lineages contain filamentous species. Phymatodocis nordstedtiana is a filamentous organism that seems to represent an entirely independent occurrence of the filamentous state. Micrasterias foliacea, which also forms filaments, is a second instance. However, in this species the filaments are held together by the interlocking of apical processes, not by means of a shared primary wall (Lorch and Engels, 1979). It is also true that the "filamentous" lineage here discussed contains organisms that are better described as colonial, namely, Cosmocladium saxonicum and Heimansia pusilla. Cells of these species are more loosely connected (Gerrath, 1970).
It is not clear why there are so few transitions from the unicellular to the colonial and filamentous forms among the desmids. In a related group, the Zygnematales, organisms have made the transition between unicellular and filamentous forms several times (McCourt et al., 1995, 2000; Gontcharov et al., 2003, 2004; Hall et al., 2008). The filamentous Desmidiaceae are embedded in the lineage of the Desmidiales and the Desmidiaceae whose cell walls are very different from those of the Zygnematales (Mix, 1972; Pickett-Heaps, 1972). Perhaps the cell wall composition of the ancestor of the Desmidiaceae has been a factor.
These results provide some indication of the variability possible in the process of cell division. While the cells in filamentous Desmidiaceae most likely do not share cytoplasmic connections, the cells, at the very least cooperate with one another to form filaments of diverse shape. The differences in cell division are the product of not only changes in the degree and order of cellular events, but also of the evolution of novel structures. Our results demonstrate that considerable variation is possible in processes as complex and critical as cell division.
The data presented suggest that aspects of the mature cell wall are determined at the time of cell division. Desmidium baileyi, for instance, deposits cylinders of cell wall material on the cross wall several hours before the cell elongated to form a mature, mirror image of the semicell. Our findings are consistent with the hypothesis put forward by Kiermayer (1970, 1981) that the cell pattern is in part determined at the time of cell division.
It is clear that there is much diversity of cell division among the filamentous conjugating green algae, but the exact details of these differences remain obscure. We investigated the formation of cross walls as structural characteristics, but other aspects of cell division are important for understanding the evolution of these cell division syndromes. Timing of chloroplast and nuclear division, and the fate of the primary wall, all require more in-depth study of each species and probably the employment of different methods such as TEM. This study is only the beginning of such an investigation. Future work may reveal information that will be useful in determining the evolutionary history of cell division in this unique group of organisms.
FOOTNOTES
1 This work was supported by NSF grant DEB-9978117 to C.F.D. and by a USDA-CSREES graduate training fellowship 2005-3842015761 to J.D.H. 
5 Author for correspondence (e-mail: jhall{at}nybg.org)
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