MACRONUCLEAR DIFFERENTIATION DURING ORAL REGENERATION IN STENTOR COERULEUS
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1 J. Cell Sci. 19, 53i-54t (i975) 531 Printed in Great Britain MACRONUCLEAR DIFFERENTIATION DURING ORAL REGENERATION IN STENTOR COERULEUS J.J.PAULIN AND A. SUSAN BROOKS Department of Zoology, University of Georgia, Athens, Georgia 30602, U.S.A. SUMMARY The moniliform macronucleus of Stentor coeruleus coalesces and renodulates during division, reorganization and regeneration. These nuclear events are spatially and temporally synchronized with oral primordium development occurring at stages six and seven of membranellar morphogenesis. Coalesced, elongating and early renodulating macronuclei at stages six and seven contained microtubules within double membrane-bound channels, passing through the nucleus parallel to the long axis. The number of microtubules per channel varied between 4 and 23. Microtubules were also found in the perinuclear cytoplasm at these stages, forming a loose network around the nucleus. The microtubules and channels are absent in control cells and macronuclei of regenerating cells prior to stage six. These transient microtubules and channels appearing in late stage six and stage seven may provide the axial plane on which elongation of the macronucleus proceeds. INTRODUCTION During division the large heterotrich ciliate Stentor coeruleus produces a new membranellar band for the opisthe; the prater retains its feeding organelles. Eight welldefined stages of membranellar morphogenesis, each lasting about one hour, can be identified from the onset of primordium formation to completion of the new membranellar band (Tartar, 1961; Paulin & Bussey, 1971). The developmental stages observed in the formation of the membranellar band in division are mimicked in reorganization and regeneration (Tartar, 1961; deterra, 1969). Regeneration of oral membranelles is inducible by surgical removal of existing membranelles (Tartar, 1961) or by placement of stentors in various chemical agents (e.g. 12% sucrose, 4% urea; Tartar, 1957) causing them to shed their membranelles, providing populations of regenerating stentors for critical analysis of cortical and cytoplasmic events. Excellent reviews have been published on these events based on morphogenetic studies (Tartar, 1961; Margulis, 1973; deterra, 1974) and electron microscopy (Paulin & Bussey, 1971). Concomitant with the cortical events (i.e. formation of the membranellar band) the moniliform macronucleus begins to coalesce at stage six, becoming unitary and ovoid in appearance by stage seven with subsequent elongation and renodulation by late stage seven; the membranellar band is completely differentiated at this time. Consequently oral replacement and nuclear events are spatially and temporally synchronized (Tartar, 1961; deterra, 1969, 1974). The present investigation explores the possible mechanism(s) responsible for the
2 532 J.J. Paulin and A. S. Brooks coalescence and renodulation of the macronucleus during regeneration. A light and electron-optical study of interphase, coalescing, clumped and renodulating macronuclei was initiated in an attempt to reveal the structural basis for the kinetic event. An abstract of this work has been published elsewhere (Paulin, 1973). MATERIALS AND METHODS Stentor cocruleus originally obtained from Carolina Biological Supply (Burlington, North Carolina) were maintained in a modified Peter's solution (Hetherington, 1934) and fed Euglena sp. every 3 days. Stentors were induced to shed their oral membranelles in 12% sucrose (w/v, in distilled H 2 O), washed and resuspended in conditioned media. Regenerating stentors were removed at i-h intervals after shedding up to a period of 8 h and viewed in a Zeiss Photomicroscope II with phase optics to determine the specific stage of regeneration based on membranellar band differentiation and macronuclear configurations. Control cells (interphase cells) and experimentals were prepared by the Feulgen nuclear reaction (Galigher & Kozloff, 1964) and photographed in the Zeiss Photomicroscope II utilizing Kodak Panatomic X, 35-mm film. The procedures for fixation and embedding for electron microscopy have been described elsewhere (Paulin & Bussey, 1971). Cells were prepared by these methods at each stage of regeneration and flat-embedded. Thus, specific stages based on membranelle differentiation and macronuclear configurations could be selected and properly oriented before sectioning. Thin sections were obtained on a Porter Blum-MT. microtome utilizing diamond knives. The sections were stained for 15 min with saturated uranyl acetate (w/v, in distilled water) followed by Reynolds' lead citrate (2 min) and viewed in a Siemens 101 electron microscope at 80 kev with a 35-/im objective aperture. RESULTS Light microscopy The interphase moniliform macronucleus of Stentor coeruleus consists of ovoid nodes (X 7-6 per cell, ea. X i6-2x 14-5 /tm, 53 cells counted) linked together and contained by the nuclear membrane which often forms tenuous constrictions between nodes (arrow, Fig. 1). If cells are induced to shed their oral membranelles and allowed to regenerate, the moniliform macronucleus remains quiescent until early stage 6 of membranellar regeneration; the membranellar band at this stage is well differentiated, and the buccal cavity is beginning to regress (see Paulin & Bussey, 1971). At this point in regeneration the macronuclear nodes begin to coalesce, nodes at the extremities fusing first. Fig. 2 shows 2 macronuclear clumps formed by such fusions. This process continues until the once moniliform nucleus forms a single large mass (Fig. 3) by early stage 7. By late stage 7 the macronucleus has begun to elongate and renodulate. Fig. 4 shows the initial nodes being formed by constrictions around the elongating macronucleus. Nodulation begins at both extremities and progresses to the centre. All nodes are reconstituted by stage 8 in concert with completion of oral regeneration or just after cytokinesis in dividing stentors. Electron microscopy Control cell macronuclear nodes are encapsulated by 2 unit membranes (Figs. 5-8) perforated with numerous pores (p, Fig. 6). Portions of 3 nodes from a control cell
3 Macronuclear differentiation 533 are depicted in Fig. 5. The cytoplasm around the nucleus is often vacuolated and contains numerous mitochondria (m, Fig. 5). The karyoplasm contains dense amorphous masses of chromatin (c, Fig. 5) and numerous nucleoli (n, Fig. 5). Macronuclei of cells regenerating oral membranelles examined at i-h intervals after the stimulus to regenerate to mid-stage 6, when nodal fusion is near completion, appear ultrastructurally similar to control cell nuclei (see above). However, late stage 6 and early stage 7 macronuclei, those fully clumped and beginning to elongate, possess microtubules either in double membrane-bound channels (Figs. 6-10) or forming a network around the nucleus (Figs. 8, 9). Channels containing the microtubules are found near the periphery of elongating nuclei, running parallel to the long axis of the nucleus (Figs. 7, 9, 10). The number of microtubules per channel varies between 4 and 23 (Fig. 6), and at high magnification they do not appear to be cross-linked (Fig. 8). The microtubules are continuous through the channels and appear to radiate from the channels at the periphery of the nucleus (Fig. 9). Their terminus in the cytoplasm cannot be ascertained. After nodulation has begun in late stage 7 there is a noticeable reduction in the number of microtubule-bearing channels and microtubules in juxtaposition to the nuclear membrane. In Fig. 10 a node-forming furrow (small arrow) can be seen bisecting a portion of the nucleus. A portion of a channel (large arrow) is reflected to the axis of the furrow which is at right angles to the channels. By stage 8 channels and microtubules are nearly absent. DISCUSSION The presence of channels containing microtubules through elongating macronuclei of Stentor is surprising. Microtubules have been found in dividing macronuclei in a number of ciliates (e.g. Nassula, Tetrahymena and Diplodinium to name a few, see reviews by Falk, Wunderlich & Franke, 1968; Raikov, 1969). However, the microtubules are contained within the karyoplasm, not membrane-bound, forming a compact bundle or 'pushing body' which has been postulated to be the kinetic element associated with elongation of the macronucleus in division (Tucker, 1967; Raikov, 1969). These bundles of microtubules are aligned parallel to the axis of elongation. Jenkins (1969) has found in the heterotrich ciliate Blepharisma sp. microtubules external and adjacent to the macronuclear membrane during elongation of the macronucleus in division. No microtubules were found in the karyoplasm or in coalescing nuclei. Colchicine (5 x io~ 3 M) blocks elongation of the macronucleus but not coalescence or cell division (Jenkins, 1969). Cytoplasmic channels containing microtubules have been found in a number of dinoflagellates (Hollande, 1972). In Gyrodinium cohnii the channels are perpendicular to the division furrow, forming the axis on which the nucleus elongates (Kubai & Ris, 1969). The situation is similar in Amphidinium; however, Oakely & Dodge (1974) found the microtubules within the channels to be attached to kinetochore-like plaques on the nuclear membrane serving as attachment sites for chromosomes and thus functioning as spindle microtubules. In the dinoflagellates as in regenerating stentors
4 534 J- J- Paulin and A. S. Brooks the microtubules exiting from the channels terminate in the perinuclear cytoplasm and are not associated with kinetosomes or centrioles What then is the function of the microtubules found within the channels and around the macronucleus in regenerating cells? We can rule out a mitotic function since the macronucleus is polyploid, and no condensed chromosomes (polytene) have been observed in Stentor macronuclei (Tartar, 1961), and no chromatinic association has been found. Whether they function as a pushing body as in other ciliates cannot be ruled out, but in all other ciliates studied to date the pushing bodies have been intranuclear. The most plausible possibility is that the channels containing microtubules and perinuclear microtubules form the axial plane for elongation and are the kinetic element responsible for elongation. Tartar (1961) has indicated that some intrinsic impulse to nodulate resides in the macronucleus, due to the fact that clumped nuclei isolated in a small volume of cytoplasm from dividing cells elongate and attempt to renodulate. The timing of the nuclear events (e.g. clumping, elongation and renodulation) has been shown to reside in the cortex (Tartar, 1961; deterra, 1969, 1974). Consequently, it may be hypothesized that the stimulus to form a primordium in regeneration (loss of cortical membranelles) may at a specific time (stage 6) initiate macronuclear channel and microtubular formation triggering elongation and initial renodulation (intrinsic impulse of Tartar, 1961) of the nucleus which is completed under continued cortical feedback. Whether these channels and microtubules are present in clumped and elongating macronuclei of dividing cells needs to be explored. By serial sectioning techniques we may be able to establish unequivocally whether there is a link between the nuclear microtubules and the cortex, a situation not resolvable in this study. Serial sectioning will also demonstrate the continuity of the channels with the nuclear membrane, eliminating the remote possibility of the channels being intranuclear vesicles containing microtubules. The continuity of the files of microtubules in the channels and perinuclear cytoplasm seen in Fig. 9 supports the hypothesis that they are indeed continuous through the nucleus. The authors acknowledge the financial support of a Brown-Hazen Grant from Research Corporation and the technical assistance of Mr William Henk II. REFERENCES DETERRA, N. (1969), Differential growth in the cortical fibrillar system as the trigger for oral differentiation and cell division in Stentor. Expl Cell Res. 56, DETERRA, N. (1974). Cortical control of cell division. Science, N.Y. 184, FALK, H., WUNDERLICH, F. & FRANKE, W. (1968). Microtubular structures in macronuclei of synchronously dividing Tetrahymena pyrifonnis. J. Protozool. 15, GALIGHER, A. & KOZLOFF, E. (1964). Essentials of Practical Microteclmique, pp Philadelphia: Lea and Febiger. HETHERINGTON, A. (1934). The role of bacteria in the growth of Colpidium colpoda. Physiol. Zool. 7, HOLLANDE, A. (1972). Le d^roulement de la cryptomitose et les modalite's de la segregation des chromatides dans quelques groupes de protozaires. Atmls Biol. 11,
5 Macronuclear differentiation 535 JENKINS, R. (1969). The role of microtubules in macronuclear division in Blepharisma. jf. Protozool. I6J, 10 (Abstr.). KUBAI, D. & Ris, H. (1969). Division of the dinoflagellate Gyrodinium cohnii (Schiller). J. Cell Biol. 40, MARGULIS, L. (1973). Colchicine-sensitive microtubules. Int. Rev. Cytol. 34, OAKELY, B. & DODGE, J. (1974). Kinetochores associated with the nuclear envelope in the mitosis of a dinoflagellate. J. Cell Biol. 63, PAULIN, J. (1973). Macronuclear reorganization during regeneration of oral membranelles in Stentor coeruleus. In Progress in Protozoology: IVth Int. Congr. Protozool. (e&: P. de Puytorac), p France: Clermont-Ferrand. PAULIN, J. & BUSSEY, J. (1971). Oral regeneration in the ciliate Stentor coeruleus: a scanning and transmission electron optical study. Jf. Protozool. 18, RAIKOV, I. (1969). The macronucleus of ciliates. In Research in Protozoology (ed. T. Chen), pp New York: Pergamon. TARTAR, V. (1957). Reactions of Stentor coeruleus to certain substances added to the medium. Expl Cell Res. 13, TARTAR, V. (1961). The Biology of Stentor. New York: Pergamon. TUCKER, J. (1967). Changes in nuclear structure during binary fission in the ciliate Nassula. J. Cell Set. 3, (Received 15 May 1975)
6 536 J. J. Paulin and A. S. Brooks Figs Light micrographs of Feulgen preparations of successive stages of macronuclear reorganization. Fig. 1. Control moniliform macronucleus with tenuous constriction between nodes (arrow) and pigment stripes of cortex are evident in this optical section, x Fig. 2. Clumping macronucleus; 2 enlarged nodes formed by the fusion of other nodes are evident, x Fig. 3. Clumped macronucleus. x Fig. 4. Elongating macronucleus; constriction furrow delineating new node can be seen (arrow), x Fig. 5. Survey electron micrograph through 3 macronuclear nodes from control cell; nucleoli (n) and chromatin clumps (c) are dispersed throughout the nodes and numerous mitochondria (in) are seen between the nodes, x 7600.
7 Macronuclear differentiation 537 \ «CEL 19
8 538 J. J. Paulin and A. S. Brooks Fig. 6. Cross-section through a portion of an elongating nucleus (stage 7); numerous double membrane-bound channels containing microtubules are found in the nucleus, note pore (p) in the double nuclear membrane, x Fig. 7. Intranuclear channel cut in longitudinal section; note its close proximity to the periphery of the nucleus, x Fig. 8. High magnification of intranuclear channel; microtubules are present in the lumen of the channel and outside the double nuclear membrane (arrow), x
9 Macronuclear differentiation
10 54 J. J. Paulin and A. S. Brooks Fig. 9. Grazing section through nodulating macronucleus; note intranuclear channels containing microtubules and microtubules forming a network around the nuclear membrane (arrows), x Fig. 10. Cytoplasmic furrow (small arrow) and channels (large arrow) containing microtubules are both seen in this micrograph, x
11 Macronuclear differentiation 54'
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