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231 Ada 801. Neerl. 36 November (3-4), 231-245 1987, p. division in the green Cell Marvania geminata: role of coated autosporogenesis, pit-microtubule systematic H.J. 1 2 1 Sluiman Rijksherbarium, Universite de and complexes, significance 2 and O.L. P.O. Box Reymond 2300 RA 9514, Institut Lausanne, microalga semi-exogenous Leiden, The Netherlands. d’Histologie et d’Embryologie, Rue du Bugnon 9, CH-1005 Lausanne, Switzerland. SUMMARY Cell division electron the cell in the unicellular microscopy. Unlike has part of the intact. The expanded appears a coated and in at the break spindle is not associated site at the before division is initiated. pit-like septum. Cells original the cell cleavage furrow. after the During mitosis events, in be may seem is marked grow by near a to be wall particular considered as a the absent along escape of envelope remains throughout with invaginates the short the cell is broken of a forms a at the broadly to form microtubule, furrowing mechanism, member not before the cortical microtubule which daughter cell layer transmission occurs involves the nuclear short with mitosis the microtubule inward common studied algae, expansion After furrowing, each old, It is concluded geminata Cell centrioles, which membrane septum. A model explaining cytokinetic that M. volume. The plasma membrane separate has been geminata wall. The latter continues to structure. effect constitutes the new in M. in other coccoid green cycle with plasma alga green about twice its protoplastthrough a The division cycle. until coccoid the division wall level layer of the is presented. conceived order Chlorococcales. 1. INTRODUCTION features of the external Light microscopical zation of the a plant body (including dominantrole in tion of green current text algae (example: non-flagellated forms are its book Ettl morphology presentations 1980). For generally assigned few will doubt that the order thus conceived is not be defined held by sharp, those coccoid Especially together due which results in trate the complexity to the more difficulty what appears The to be of a unambiguous green persistence or forms and those with to to the continue higher-level unicellular and colonial order Chlorococcales, artificial, heterogenous, products and or yet can- 1983). of cell division of extra-cellular substances discrete play to classifica- criteria (cf., Komarek & Fott virtual continuum of of how of the example, in which the less coherent tissue- establishing among the green question algae and the cellular organi- reproductive structures) filament-like complexes, illus- morphological categories (taxa) increasing are (mucilage, walls) levels of in morphological algae. distinguish higher grades between multicellular chlorococcalean of organization like filaments and tissue-like 232 H. has led Bold and co-workers complexes systematic value of the patterns This resulted in the ‘desmoschisis’, include to to be capable cell basic two division, and as ‘eleutheroschisis’, well critical The taxonomic problematic filamentous green The ‘filament’ algae The spherical assigned to summ- and Ettl & Komarek 1982 for a the special in to occur for that cell in case (Hindak microalga green point sense, as diad-forming view, Marvania geminata Hin- that illustrates the mentioned problems suggest an affinity with chlorococ- mode of cell division only 1976; Heynig 1980; Reymond in any member of the Chlorococcales, nor involving al. et in any can should be be produced classified, at led Hindak least (1976, tentatively, 1978) a 1986) other The fact that under certain conditions linear matter. complexes geminata the inabi- more on considered to be filamentous in Hindak’s are characteristic and is ment-like) (e.g., cell division patterns. specific broad a truly Hindak the taxonomic delimitation of the order Chlorococcales. The mechanism alga, of occurrence by in the order Ulotrichales. budding-like known Ulotrichales primitive of the Chlorococcales is based obviously applied was algae, yet its that M. on cell features of Marvania obviously vegetative green be a recent natural link between Chlorococcales and unicellularnon-motile concerning calean 1982, of the so-called position a concept placed dak 1976, presents above non-vegeta- or to has been discussed in various papers like Elakatothrix and therefore are not as form filaments than term green algae) His 1962,1978,1982). to algae. discussion.) (which might be regarded lity potential and that those known would have separate order Chlorosarcinales (see Bold & Wynne 1985 for ary, and Silva 1982, Tschermak-Woess a the types of cell division exist, viz. by eleutheroschisis, desmoschisis by to that the order Chlorococcales would be restricted proposed divide to that that divide solely algae as a was focus their attention to REYMOND of cell division that occur in coccoid green recognition vegetative or tive division. It J, SLUIMAN AND O. L. (fila- conclude to in the order Ulotri- chales. It now seems ‘natural’ higher ral and al. (1986), a features and biochemical, preliminary et doubt that for the establishment of green micro-algae, taxonomic levels, it is essential reproductive cally beyond classification of at to study of M. geminata seemingly exotic a more stable and intermediate and morphological markers, both was undertaken by and structu- reason, a Reymond method of cell division is basi- Our present report examines the ultra- autosporogenesis. structural aspects of cell division in M. 2. gross search for novel taxonomic who found that its form of de-emphasize at cellular and macromolecular levels. For this ultrastructural special to especially geminata in more detail. MATERIALS AND METHODS A strain of Marvania geminata Bratislava, Czechoslovakia) Hole MBL medium 2 mM HEPES Hindak, (nr. was following grown as a Nichols 1978/21, isolated by unialgal (1973), Dr. F. Hindak, culture in aerated Woods with TR1S being replaced by (N-2-hydroxyethylpiperazine-N’-2-ethanesulfonic acid) at 16 °C CELL DIVISION IN MAR VANIA Fig. 1. new Marvania (inner) x51000. wall 233 GEMINATA geminata. Advanced layers clearly visible. stage of cell expansion prior to cell division, with C, chloroplast; G, Golgi body; M, mitochondrion;N, old and nucleus, 234 H. under 16 h a numbers of the at light: 3500 cells dividing for 5 rpm in 30- 50 noted being at followed followed that the by during that the in agar (galloyl glucose, in medium. The acidified a took distilled MW 1701.21, electron (Lausanne) at table a of the using centrifuge (1 % glutaralde- temperature for room cells in pelleted 3 mm taken As (3) and 0.05% blocks, were embedded in using Philips at room warm temperature in method (1), except in medium, and that in method glutaraldehyde, Polysciences) in c. 8 cut As (2) glutaraldehyde of 0.2% 2,4-dimethoxypropane, photographs in 4 ml fixative c. highest the sixth h of light) samples 7.2) water. Reichert Ultracut-E microtome and made and in pH after osmication. place specimens, cultures light period (the 1 % aqueous Os0 4 for 90 min wash in fixative consisted primary 10 ml by embedding fixative consisted of 0.2% primary embedding in thorough a L. REYMOND of the immobilized cells in medium containing 0.1 repeated washing postfixation the approximately M HEPES, AND O. Exponentially growing by resuspension 0.1 containing min; centrifugation M HEPES; using followed min, medium 1.5% agar; 3. photoperiod. following protocols. (1) Centrifugation of hyde or 8 h darkness for electron microscopy sampled were J. SLUIMAN (2), except 0.2% tannic acid saponin (Polysciences) dehydrated Spurr’s resin, with acetone and sectioned diamondknife. Observations a EM-300 (Leiden) were and Zeiss EM-10 microscopes. RESULTS The ultrastructure of M. geminata has been the general study (Reymond will focus a thin wall is plast. The wall in deposited less with the the ‘isthmus’ cell has reached having the nucleolus the occurs, (MT) to indicate the not was than 5 or at a length two presence a and semi-cells and short a previous the at irregular plasma the out At the of the same bulging part chloroplast. is effected seemingly time, a new of the proto- shows (which sign no By what might After of the time original diameter, organization (fig. 2). the a is established, and be described chloroplast as has condensation of chromatin entering prophase. membrane (PM) associated micro- ‘isthmus’ transverse at passes expansion Golgi-body having duplicated, (fig. 4). This MT is visible sections. Most observations single cortical MT, position As the nucleus (fig. 1). position level of the one protoplast of about twice its that the nucleus is the of of the intracellular central a 6 consecutive noted in similar shown). of increase in volume of the elongating parietal disappears, indicating appears no more an cell, including symmetrical assumed between in MT subject in the present report which contains the nucleus and the At this first stage of mitosis tubule repeated fashion initially single mitochondrion nucleus patches yet) mirror-like the cleaved, be not bulging budding-like a expanding cytoplasm the expanded or a all around the imminent mitosis more will cell until it has doubled in size. This cell break in the cell wall and rigid encasing an 1986), and stage of each division cycle involves initially spherical by al. the details of cell division. on The first et opposite but on one occasion side of the nucleus through prometaphase during a seem second (micrograph which a much CELL Fig. DIVISION IN 2. M. chondria geminata. Cell expansion (M) reduced is and bodies (G) a is completed, have and mitosis has been initiated duplicated, and chloroplast division minute indentation or PM is associated with particularly acid is ing Golgi is a associated with a two some a abluminal proteins evidence MTs instead of are a one MT. fixative major (not shown) coat that 52000. x the cortical diameter of less than 50 primary aldehyde This suggests that material. There is with densely staining well visible when employed. pit Mito- (prophase). underway, spindle apparatus is developed (figs. 3, 5) the PM subtending MT forms pit 235 MARVANIA GEMINATA nm. The (figs. 6-8), which containing tannic constituentof the the coated pit coat- may be 236 H. M. Figs. 3,4. (arrow), (arrow) x geminata. Fig. 40000. marks the Fig. 3. Prophase 4. Cel! at nucleus in in prophase division site, presumptive period, of the cell any stage After to of the by an intact nuclear or the now elongated PM furrow, at just completed septum with cytokinetic 1 or time have being are formed microtubule not observed most during invagination proceeds an at the front end associated MT is shown MTs been observed during cleavage, apart 2 MTs just described. of the Immediately following completion some REYMOND least until about half of the internuclear cytop- in fig. 9. At from the L. envelope during coating material/MT complex persists lasm has been bisected. A no microtubules membrane-associated Centrioles were permanently. of mitosis inward. The invagination not spindle plasma O. cycle. completion grow if a SLUIMAN AND 42000. x The mitotic apparatus is enclosed of the division which which J. in each daughter cell begins trans-side, containing amorphous septum (shown in fig. 10) the dictyo- release to a steady flow of vesicles from its electron dense material. These vesicles mi- grate towards the septum where the amorphous substance is discharged via cytosis (figs. 10-13). wall the in the layer dictyosomes tion from shown in the the a new to septum, fig. 10 initially but after to a bi-layer layers similar at the septum texture and differentiatebetween old and period are has apparently not restricted a delicate exo- single wall is formed. The transibeen captured activity to this is most region in the cell evident at alone since continuous with layers deposited elsewhere. staining properties, new of of intense vesicle traffic from wall formation septum, it is certainly the development double-layered a (arrow). Although wall in the some the septum PM to single layer transverse Due This results layers where they however, are it is difficult to closely appressed (fig. CELL DIVISION Fig. 5-8. M. IN geminata. Fig. envelope. Furrowing membrane, showing with coated advanced coated 237 MARVANIA GEMINATA one or by the formation two associated pit (arrow) pit, 5. The mitotic nucleus has started with in more (metaphase?) is of microtubules, detail, x 80000. associated microtubule a coated x 47000. surrounded Fig. 6. x an 60000. intact nuclear of the Enlarged portion Figs. 7,8. Non-adjacent (arrows), by pit-like invagination serial plasma of sections fig. 5, of an 238 H. Figs. 9,10. after M. plane (arrow), Fig. body geminata. Fig. telophase. 10. Early x A 9. A just completed, delicate septum septum-associated microtubule can be seen J. SLUIMAN AND O. L. spans the intemuclear about halfway across REYMOND cytoplasm the division 44000. stage of septum wall ofeach cell. Part of the new formation, with wall has wall precursors being produced by already become bi-layered (arrow), x 35000. the Golgi 239 CELL DIVISION IN MAR VANIAGEMINATA II, As inset). the wall two layers cell wall that encloses outer the the septum increase in at septum (fig. 12-13, arrows). This allows the cells shape, 4. and eventually to to old level of the to a more spherical separate. DISCUSSION 4.1. and Morphological taxonomic On the basis of the present observations bined with information obtained the division cycle of this alga of the division site formation of (5) site marked of the the now coated a 1 or 2 MTs, MTs other than those of the by separation The larly informative of the aspects the of the to as PM resulting new associated wall layers at cell division cell be to appears expansion and more the of al. of M. 1986). Assignment be contradicted cell cycle 1983). tion of the quence is Cell geminata seen: after gradual occurs at least cell two period is the Chlorococ- geminata represents important respects. expansion, in the by a of nuclear an inactivity, or apparently the prolonged followed after rupture progeny However, in M. geminata some the during autospor- to within the confines of the mother cell wall expansion mother wall. and particu- The over-all unique although in Chlorococcales is characterized cytokinetic inactivity cleavages occurring & Fott are not algae. any of the other features listed. Ne- by the chlorococcalean pattern in typical daughter cells; two following cleavage it is obvious that the cell division mechnism of M. First, with the level of the septum, followed vertheless, period apically distinct wall layers by two its taxonomic affinities among green to the of septum that separates the not seem MTs; at absence of cytokinetic the formationof walls in Chlorococcales et cycle; cleavage; (7) cales does on membrane plasma invagination in cell deposition during ogenesis (Reymond variation of the cell short cortical cells. ‘budding-like’ same as (‘bud- and mito- prometaphase; (6) following telophase, ingrowth pit-like the rest two one or com- structural features: following details noted in M. geminata and listed above pattern of cell wall essentially at two geminata, it is concluded that (1986), mitosis and the during prophase by at common outer of the cytokinetic al. chloroplast, Golgi apparatus, mentioned; (8) deposition Golgi activity (9) rupture at coated elongated co-migrating enhanced of the pit-like invagination cortical MTs by et is characterized by the absence of centrioles chondrion; (3) cell division in M. Reymond by ding’); (2) pre-mitotic duplication (4) marking considerations on of the cell and localized rupture of the cell wall (1) pre-mitotic expansion a the at convert the thickness, cells breaks daughter two by two or (Komarek desintegra- reversed beginning of se- a new division cycle is marked by expansion of the protoplast, causing rupture of the cell wall, with subsequent been doubled. This M. geminata cytokinesis seems to and in Chlorococcales A second deviation of M. pattern is of cells as are geminata the formation of only multiple daughter being delayed indicate that the cell two until the cell cycle fundamentally volume has control mechanisms in different. from the usual chlorococcalean division cells per division cycle. reported by Hindak (1976) was (The not formation observed in 240 Fig. H. 11. M. geminata. of wall material via Inset: More advanced Golgi-derived Enlarged portion of stage vesicles of septum (arrows). wall SLUIMAN AND O. formation, with The wall is now fig. 11, showing the junction J. L. REYMOND continued excretion bilayered throughout, of transverse and lateral walls. x 39000. x59000. CELL DIVISION IN MARVANIA 241 GEMINATA Figs. 12,13. M. geminata.Golgi-derived vesicles apparently fuse thereby discharging the 13). septum (asterisk x 37000, x their in 45000. electron fig. 12), dense and contents (arrows). their remnants remain with the Old wall visible for septum plasma membrane, layers some break time at the level (asterisk in of fig. 242 our H. This cultures). division resulting mentous forms one related Microspora ) closely of pair that appear grounds (Sluiman to well, for ment order, be the expanding more If this to SLUIMAN AND O. exist in other geminata belongs less or with the simple this pseudo-fila- (Sphaeroplea, Chlorococcales more (which fila- loosely organized or is taken as an argu- limits of morphology-based accepted to in occurs Radiofilum, Fusola, Fottea) currently REYMOND structural and ultrastructural on affinity L. apparent than real. Cell more typically ( Cylindrocapsa ) Chlorococcales to like Elakatothrix, it is clear that M. cells daughter 1984, 1985). future EM studies may reveal ments as may be deviation, however, in J. the conceived order broadly Chlorococcales. On the basis of all information now available cell division of M. paper), geminata appears division patterns of Chlorococcales than initial (Hindak 1976) cales is the M. would is formation of probably et best spores, the type present the known observations in Chlorococ- division pattern formation of ‘semi-exogenous as 1986, to light microscopic multiple described al. similar more Whereas thebasic cell division suggest. endogenous geminata (Reymond be to in auto- spore diads’. 4.2. The role of coated In M. pears geminata, and at electron-dense of ‘coated the same pits’, Although i.e. PM a the coated helpful Coated to sign of the arise in M. geminata development as a discussion, does not of coated its site ap- is highly give reminiscent in the forma- implicated see face with cytoplasmic Emons & Traas rise to a coated 1986). vesicle, in other systems pits/vesicles of PM bilayer helps (or, induces) cytoplasmic vesicle (Darnell can believed that the the al. the PM in cause predetermined curve into clear, but the consistent presence at a et along the latter 1986; proteins, cytoplasmic to of assembly invaginate surface and Heuser & Evans to 1980; 1969). A similar mechanism may pit that are coated with regions clathrin. It is lattice of clathrin from triskelions Kanaseki & Kadota a on structure that have been references and by invagination phospholipid bud off cleavage understand its role in the process of cell cleavage. pits cage-like cleavage determination of the resulting specializations pit a PM-associated MT is formed. The PM then inva- a the best characterized of which is the microtubules in of time becomes associated (for with the comparison and material. The coating tion of coated vesicles be when during prophase ginates pits the first visible site. of a dividing How this cells of M. cleavage MT before the pit site is has geminata fixed is developed, to not and its close and persistent association with the coating material suggests that there is microtubular involvement in the a the cleavage formation at this known tant site. According to (Ockleford 1981), specific site from the clustering the membrane the protein subtending microtuble/monomer interaction, parts of the PM, and arrive of the fluid membrane bilayer. at the of coat motility monomers cortical or pit may site by protein monomers may be inserted in the PM cytoplasm through be at model of coated vesicle incorporated in some un- more lateral transport in the dis- plane CELL DIVISION The fact that rather persists sors the that MTs lular play a role in material. This stopped cell. the Although (fig. 9) may association Coated scribed graphs actual the be taken might pit-like as et al. In that in M. of material coat MT geminata at alongside the the presence by the apical could not has coat of to side of the opposite be observed just completed septum a this site the close at subcel- as a It is understood that coated disassembly coat a involved with clearly are coccoid green plant visible in PM/coat/MT- algae. also the figures, conerning MT aeria (fig. (MTs?) cytokinetic division to been de- 11 1-3 in Deason (figs. the not electron micro- Tetracystis pit-associated useful comparison a published These include of detailed information organisms prevents cell division have few a and Friedmannia israelensis 1979), of these some Lack present. in these process structures dividing 1979). be The observed co-mi- with other membranes fusing implies indirect evidence that in Deason & O’Kelley to explained certain radius have ended. before, yet they of once a 1981). of the integrity microscope. the presence of study, vesicle but may be the addition of new PM precur- Ockleford be disassembled before the furrow reaches the PM in the present coated a and its associated MT into the cell again suggests maintaining from prevented are coating coat form to invagination has interrupting membrane (cf. PM PM assembly visible in the electron structure vesicles the apical narrow coat off pinched not without reached, invaginating of the gration is pit ever-elongating an is curvature to the coated as that the process of by assuming of pit 243 IN MARVANIA GEMINATA events seems process in M. gemi- nata. It is known that green plants cellular division by localized or Golgi-derived vesicles), man 1984). many green described in growth and is often any detail; in published by on the referred the particular, reported to as precise Domozych through ingression mechanism in the cleavage (1987). physically ponent (ER, Golgi apparatus) furrow whose apical presents the first to a green of PM cell evidence of the been an and detailed Carteria were division is effected on the lack of critical endomembrane com- M. geminata, intrinsic, never recently, very based membrane-associated positive port-dependent invagination an has flagellate conclusion that the furrow PM. be characteristic of mechanism of membrane Only was (invagination) (Slui- to ‘furrowing’, transferred from PM bears nizable marker in the form of therefore, His of existing PM into the cell evidence that membraneis a in of lateral PM which has been casually septum membranes during of endomembraneelements (i.e., ER- in the furrow has received little attention. observations duces new transverse by folding or The latter process, algae form incorporation however, ultrastructurally coat. The present occurrence during cellular division in a of lateral green pro- recog- study, trans- alga. ACKNOWLEDGEMENTS This work for the was made possible with support from the Netherlands Advancement of Pure Research (Z.W.O.), grant Organization H 86-88. Thanks are 244 H. due to Dr. F. Hindak P.-A. Dr. B. Hickel (Bratislava), Milliquet (Lausanne) the (Leiden) SLUIMAN AND O. L. REYMOND Prof. B. Droz and Mr. (Pldn), for their assistance C. Kalkman and Dr. G. M. Lokhorst J. in various ways, for their helpful and Prof. to comments on manuscript. REFERENCES H. C. & M. J. Wynne Bold, edition. Darnell, J., W. H. coccoid and R. & J. C. P. R., cleavage E. O’Kelly A. M. C. — J. Ryals, C. H. (1980): and O’Kelly (1982): reproduction. Second Scientific American Books, in several cleavage during zoosporogenesis Bullock Phycol. 15: 452-457. division in Carteria crucifera Fine (1979): (Chlorophyta): the of mitosis structure role ofthe endomem- 170-182. 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