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Cell Division in the Scaly Green Flagellate Heteromastix Angulata and Its Bearing on the Origin of the Chlorophyceae Author(S): Karl R

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Cell Division in the Scaly Green Flagellate Heteromastix Angulata and Its Bearing on the Origin of the Chlorophyceae Author(S): Karl R Cell Division in the Scaly Green Flagellate Heteromastix angulata and Its Bearing on the Origin of the Chlorophyceae Author(s): Karl R. Mattox and Kenneth D. Stewart Source: American Journal of Botany, Vol. 64, No. 8 (Sep., 1977), pp. 931-945 Published by: Wiley Stable URL: https://www.jstor.org/stable/2442248 Accessed: 13-02-2019 18:06 UTC REFERENCES Linked references are available on JSTOR for this article: https://www.jstor.org/stable/2442248?seq=1&cid=pdf-reference#references_tab_contents You may need to log in to JSTOR to access the linked references. JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at https://about.jstor.org/terms Wiley is collaborating with JSTOR to digitize, preserve and extend access to American Journal of Botany This content downloaded from 132.248.28.28 on Wed, 13 Feb 2019 18:06:24 UTC All use subject to https://about.jstor.org/terms Amer. J. Bot. 64(8): 931-945. 1977. CELL DIVISION IN THE SCALY GREEN FLAGELLATE HETEROMASTIX ANGULATA AND ITS BEARING ON THE ORIGIN OF THE CHLOROPHYCEAE1 KARL R. MATTOX AND KENNETH D. STEWART Department of Botany, Miami University, Oxford, Ohio 45056 AB S TRACT H. angulata is a scale-covered, asymmetrical green unicell with two laterally attached, anisokont flagella. In recent years it has been classified in the Prasinophyceae. The flagellar apparatus replicates, and the cell begins to cleave at the side opposite the flagella before the nucleus can be perceived to be in prophase. The flagellar apparatuses separate, and the extra- nuclear development of the spindle occurs from the regions occupied by rhizoplasts. Rhizo- plasts or partial rhizoplasts lie at the flat metaphase spindle poles. By metaphase, the cell has already elongated to the extent that it is nearly twice as long as at interphase. The spindle and the cell itself elongate greatly during anaphase with a concomitant further separation of the flagellar pairs. Although the interzonal spindle persists during cytokinesis as in charo- phycean algae, H. angulata is similar in flagellar scale morphology and other characteristics to the chlorophycean Platymonas, which hag a collapsing interzonal spindle at telophase, a phycoplast, and a wall-like theca, which develops by the fusion of small stellate scales. It is hypothesized that the collapsing telophase spindle and phycoplast evolved in green flagellates similar to Platymonas, in which cell and spindle elongation became restricted by a cell wall that evolved from stellate scales similar to those in Heteromastix. Such walled flagellates are then visualized as having eventually given rise to Chlamydomonas and to the entire range of chlorophycean algae with phycoplasts. It is pointed out that the hypothesis has a number of implications by which its validity could be judged when sufficient information becomes avail- able. THE STATEMENT has often been made, even re- but differ conspicuously from Heteromastix in cently, that the motile cells of green algae are being nearly symmetrical and in having four an- characterized by anteriorly inserted, isokont fla- teriorly inserted, equal flagella. Even the Pra- gella. While this statement is at least approxi- sinophyceae are still occasionally characterized as mately accurate for most genera and seems to having anterior flagella (e.g., Dodge, 1973, p. provide an additional distinguishing criterion, it 16), presumably because genera such as Prasino- is an oversimplification that leads readers to un- cladus and Pyramimonas were among the earliest derestimate the diversity of green algae. In the to be assigned to the class. early sixties, Manton and Parke (Manton, 1959; We have pointed out that the Prasinophyceae Manton and Parke, 1960) showed that certain is not easily separated from other green algae by scaly or naked asymmetrical flagellates thereto- any set of characteristics (Mattox and Stewart, fore considered to belong to other algal groups 1973; Birkbeck, Stewart, and Mattox, 1974; are, in fact, green algae. The scale-covered Het- Stewart, Mattox, and Chandler, 1974; Stewart eromastix Korshikov has always been considered and Mattox, 1975a). There are, however, sev- a green alga, but it has laterally attached flagella eral presumably primitive characteristics that oc- which differ in length and manner of motion (see cur in various combinations in prasinophycean Manton et al., 1965). genera (Stewart and Mattox, 1975b). Cellular In recent years, Heteromastix and other asym- asymmetry, anisokonty, scales, and an interzonal metrical green flagellates have usually been clas- spindle that persists throughout cytokinesis are sified in the Prasinophyceae, along with Platy- features that might be considered primitive be- monas G. S. West, Prasinocladus Kuckuck and cause they are more typical of other algal classes, Pyramimonas Schmarda, which also bear scales certain fungi and protozoa than of most of the advanced green algal genera. More advanced, 1 Received for publication 5 November 1976; revisionspecialized, or less common characteristics such accepted 1 June 1977. as a collapsing telophase spindle, a phycoplast, This research was made possible by National Science approximate radial symmetry, isokonty, and a Foundation Grant DEB76-08822 and by a special alloca- tion from Miami University for the purchase of an wall-like theca are also found in prasinophycean electron microscope. genera. Scaly green flagellates could be the ex- 931 This content downloaded from 132.248.28.28 on Wed, 13 Feb 2019 18:06:24 UTC All use subject to https://about.jstor.org/terms 932 AMERICAN JOURNAL OF BOTANY [Vol. 64 tant remnants of early green algae which under- (Fig. 3). These microtubules do not extend be- went extensive evolutionary diversification in cel- yond the nucleus. lular organization, symmetry, cell covering, and The flagellar apparatus includes two superficial the details of cell division (cf. Stewart and Mat- microtubular roots, which start near the basal tox, 1975a, b). The diversity found in cell divi- bodies and extend to either side of the flagellar sion in the three scaly or naked green flagellates apparatus parallel to the long axis of the cell. studied, Platymonas (Stewart et al., 1974), One root contains seven microtubules and the Pedinomonas (Pickett-Heaps and Ott, 1974) other two or three (Manton et al., 1965, and and Pyramimonas (Pearson and Norris, 1975), present results). A rhizoplast extends from the strongly support this view. The scaly green fla- basal bodies inwardly through the cell to the gellates are clearly important to the understand- vicinity of the chloroplast and makes contact with ing of the evolutionary origin of the different the nuclear envelope for much of its length (Fig. groups of higher green algae and land plants and 9). The rhizoplast is narrow and delicate; it perhaps even in assessing the relationship of green and its cross-striations stain lightly so that they algae to other eucaryotic microorganisms. A are sometimes only faintly visible. At the point minimal effort should include careful fine struc- where the rhizoplast terminates near the chloro- tural studies of at least one species of each of the plast, it is attached to the cell's small, single small number of known genera. microbody (Fig. 6). The microbody is often ex- tensively lobed and sometimes appears, in a MATERIALS AND METHODS-Heteromastix an- single section, to be a group of small microbodies gulata Korshikov was obtained from the Indiana (cf. Fig. 5, 7). University Culture Collection of Algae (IUCC An unusual feature is the presence of a pyre- #1026, Starr, 1964). Stock cultures were main- noid-like region at the outer periphery of the tained in soil-water bottles. Algae to be studied chloroplast (Fig. 1, 2), although a definite, more were grown in Fernbach Lo-Form culture flasks typical, pyrenoid with traversing thylakoids oc- in a medium consisting of nine parts BBM (Nich- curs elsewhere in the chloroplast (Fig. 1, 2). ols and Bold, 1965) and one part soil-water ex- tract. The cultures were maintained for 12 days Prophase-The first sign of the onset of mito- at 20 C and on a 16/8 lt/dk regime. A few divid- sis is a slight cleavage in the chloroplast (Fig. ing cells were present at all times, but there ap- 7, 10). The microbody lies in or near the chlo- peared to be a greater number from 2 to 4 h after roplast cleavage (Fig. 7, 10). The cell itself de- the onset of darkness. velops a conspicuous early cleavage before there Cultures were killed with equal volumes of 2% is any indication that the nucleus has reached glutaraldehyde and fresh growth medium. After prophase (Fig. 10, 11). centrifugation, the cells were rinsed in sterile By prophase, the flagellar apparatus has been medium and resuspended in 2% aqueous OS04. replicated, but the two new flagella are noticeably After OS04 treatment, the cells were rinsed with shorter than the old ones and remain shorter un- water, pelleted in BEEM capsules, and brought til at least telophase. Each daughter cell receives through dehydration to embedment in Spurr's one of the original flagella and one new one Low Viscosity Medium. (Fig. 4; also see Manton et al., 1965). During prophase the two pairs of flagella begin to move RESULTS-Cellular organization during inter- apart (Fig. 8, 12). Early in prophase, there- phase-Interphase cells of Heteromastix have fore, a group of four flagella is observed close been described by Manton et al. (1965). We together near a shallow cleavage. A drawing of shall mention those aspects of cellular organiza- that stage in Manton et al.
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