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Apparent Amitosis in the Binucleate Dinoflagellate Peridinium Balticum

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Apparent Amitosis in the Binucleate Dinoflagellate Peridinium Balticum J. Cell Set. 31, 273-289 (1976) 273 Printed in Great Britain APPARENT AMITOSIS IN THE BINUCLEATE DINOFLAGELLATE PERIDINIUM BALTICUM D. H. TIPPIT AND J. D. PICKETT-HEAPS Department of Molecular Cellular and Developmental Biology, University of Colorado, Boulder, Colorado 80302, U.S.A. SUMMARY Mitosis and cytokinesis in the free-living binucleate dinoflagellate Peridiniuvi balticum are described. P. balticum contains 2 nuclei; one is a typical dinoflagellate nucleus and the other resembles the interphase nuclei of some eucaryotic cells and is here named the supernumerary nucleus (formerly called the eucaryotic nucleus). The dinoflagellate nucleus divides in the characteristic manner already described for certain other dinofiagellates. The supernumerary nucleus does not undergo normal mitosis; its chromatin does not condense, a spindle is not differentiated for its division, nor are any microtubules present inside the nucleus during any stage of its division. Instead the supernumerary nucleus divides by simple cleavage, which is concurrent with cytoplasmic cleavage. The nucleus cleaves first on its side facing the wall, but later it cleaves circumferentially as the cytoplasmic cleavage furrow draws closer. Invariably at late cytokinesis, a portion of the dividing nucleus passes through the only remaining uncleaved area of the cell. The final separation of the supernumerary nucleus is probably accomplished by the ingrowing furrow pinching the nucleus in two. There is no apparent precise segregation of genetic material during division, nor are there any structural changes inside the dividing nucleus which distinguish it from the interphase nucleus. Certain aspects of amitosis, and pre- viously postulated theories concerning the endosymbiont origin of the second nucleus, are discussed. INTRODUCTION Many dinofiagellates (Dinophyceae) possess unusual nuclei which display what appear to be primitive features, including the attachment of permanently condensed chromosomes to the nuclear envelope during mitosis (Kubai & Ris, 1969), and very low levels of acid-soluble protein associated with the chromosomes; this protein is different from the histones of more typical eucaryotic cells (Rizzo & Nooden, 1974). Recently, dinofiagellates have been discovered which contain two nuclei; one is the normal dinoflagellate nucleus, and the other has been called a 'eucaryotic' nucleus (Dodge, 1971) because it resembles the interphase nucleus of other eucaryotic cells. This 'eucaryotic' nucleus is bounded by the usual nuclear envelope with pores, it stains positively with the Feulgen, azure B and acetocarmine reagents, and it contains at least one nucleolus-like structure. Thus far, 2 species of such binucleate dino- fiagellates have been reported: Glenodinium foliaceum (Dodge, 1971; S. W. Jeffery & M. Vesk, in preparation) and Peridinium balticum (Tomas, Cox & Steidinger, 1973). G. foliaceum has a varied taxonomic history; most recently placed in the genus Glenodinium, it had previously been included in other genera, including Peridinium. Every cell of P. balticum and G. foliaceum so far examined, contains two nuclei, and the 'eucaryotic' nucleus is structurally similar in both species. 274 D. H. Tippit andj. D. Pickett-Heaps The cells of P. balticum and G. foliaceum examined by these workers appear to have been vegetative, and not in any stage of sexual reproduction. This is significant since certain heterotrophic dinoflagellates produce gametes which contain the typical dinoflagellate nucleus, while the vegetative cells of these same organisms have a nu- cleus like that of other eucaryotic cells (Zingmark, 1970; Soyer, 1971). One might conclude that the cells of P. balticum and G.foliaceum examined were at some stage in gametogenesis with the dinoflagellate nucleus being related to, or created for sexual reproduction. This possibility is refuted by Tomas & Cox (1973) who concluded that both nuclei are present during the vegetative life cycle. Tomas & Cox (1973) also postulate that the eucaryotic nucleus, along with numerous organelles, are derived from an endosymbiont of chrysophyte origin living within the dinoflagellate. Nuclear division has been examined in G. foliaceum using the light microscope (Blanchard-Babillot, 1972); the eucaryotic nucleus is characterized by unusual division since there is not precise staining of individual chromosomes and the nucleus simply constricts or pinches in two during division. The status and function of the 'eucaryotic' nucleus within these dinoflagellates is not clear. Several possibilities may be proposed, for example: (i) it may belong to an endosymbiont as proposed by Tomas & Cox; (ii) it may be related to some aspect of sexual reproduction; (iii) it may be analogous to or have features in common with the macronucleus of ciliated protozoa; or (iv) it could be a structure unique to these particular dinoflagellates. We have examined the division of the 'eucaryotic' nucleus to clarify these possibilities; the formation of a mitotic apparatus for its division would indicate whether it is truly a eucaryotic nucleus, and the type of spindle might then suggest the origin of the postulated endosymbiont, i.e. if it is of chrysophyte origin, then we might expect it to have a mitotic apparatus similar to that of other chrysophytes. ABBREVIATIONS ON PLATES c chromosomes no nucleolus cf cleavage furrow P pores d dinoflagellate nucleus t microtubules 8 girdle tr trichocy8ts n supernumerary nucleus V vacuole Fig. 1. Scanning micrograph of P. balticum with the characteristic girdle (g) encircling the cell, x 2800. Fig. 2. Cell surface, containing numerous pores (p); small vesicle-like structures (v) sometimes surmount the pores, but more frequently line the sutures, x 7100. Figs. 3, 4. Interphase vegetative cells stained with acetocarmine. Each contained 2 strongly staining bodies, the supernumerary nucleus (n) and the dinoflagellate nucleus (d). The permanently condensed chromosomes of the dinoflagellate nucleus give it a striated appearance. The interphase supernumerary nucleus is highly irregular in shape; sometimes it is composed of interconnecting lobes (Fig. 3), or it may be ovoid as in Fig. 4. x 2000. Division in Peridinium 276 D. H. Tippit andj. D. Pickett-Heaps Division in Peridinium 277 MATERIALS AND METHODS Peridinium balticum from the Culture Collection of Algae at Indiana University (Cat. no. LB1563), was grown in Erdschreiber medium (James, 1969) at 18 °C on a 15/9 h light/dark cycle. The cells were illuminated at a range of 30-1 era (12 in.) with General Electric Fluores- cent plant lights (13 W). For transmission microscopy, cells were fixed in 1 % glutaraldehyde for 30 min in culture medium, washed in culture medium and then fixed in 1 % osmium tetroxide, also in culture medium for 1 h, and finally washed in distilled water. The cells were dehydrated in acetone and then embedded in Spurr's (1969) resin. Preselected cells were remounted and sectioned; the sections were collected on Formvar-coated grids and stained with lead and uranium, then viewed in a Philips EM 200 electron microscope. For scanning microscopy, the cells were collected on a Solvinert Millipore filter, treated with 1 % Glusulase (Endo Labs., Garden City,. New York) for 30 min and then fixed in 1 % osmium tetroxide for 30 min. The cells were de- hydrated in acetone, passed through the critical point drying procedure (as in Marchant, 1973), coated with carbon and gold and examined at 20 kV in a Cambridge Stereoscan S4 scanning electron microscope. For light microscopy, cells were fixed in 3 :1 absolute ethanol: acetic acid for 1 h, stained with acetocarmine (Jensen, 1962) and photographed with Zeiss-Nomarski differential interference contrast optics. RESULTS Dodge (1971) tentatively named the second nucleus of the binucleate dinoflagellates^ the 'eucaryotic' nucleus based upon upon its interphase structure. We will show that this 'eucaryotic' nucleus does not divide like typical eucaryotic nuclei, nor does it differentiate condensed chromosomes during its division. Hence we now feel that the term 'eucaryotic' is misleading and until more is known about the function of this nucleus, we prefer the neutral term 'supernumerary nucleus' to describe it. We continue to call this structure a nucleus as did Dodge (1971) and Tomas et al. (1973), based upon its morphological appearance and the presence of DNA within it demon- strable by histochemical techniques. The interphase cell A scanning micrograph of an interphase cell is shown in Fig. 1. Details of the theca (Fig. 2) show the pores and blisters already described in Peridinium trochoideum (Kalley &Bisalputra, 1970). There is an additional feature on the surface of P. balticumy Fig. 5. Interphase cell, similar to that in Fig. 3. The supernumerary nucleus (fi) is lobed. Within the dinoflagellate nucleus are characteristic, permanently condensed chromosomes (c) and a prominent nucleolus (no). Numerous vacuoles (v) line the cell periphery, and trichocysts (tr) are common near the vacuoles. The girdle (jg) shown in Figs. 1 and 4, is clearly seen in longitudinal section, x 6500. Fig. 6. Mid-division of the dinoflagellate nucleus. Channels (small arrows) containing microtubules extend through the nucleus, perpendicular to the cleavage furrow. The supernumerary nucleus (n) is always ovoid and elongated prior to division, and under- goes no structural changes during division of the dinoflagellate nucleus. Nucleolar material (large arrow heads) is scattered through the supernumerary nucleus, x 3900.
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