THE BEHAVIOUR OF CHLOROPLASTS DURING CELL DIVISION OF ISOETES LACUSTRIS L.
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1 New Phytol (1974) 73, THE BEHAVIOUR OF CHLOROPLASTS DURING CELL DIVISION OF ISOETES LACUSTRIS L. BY JEAN M. WHATLEY Botany School, University of Oxford (Received 2 July 1973) SUMMARY Cells in the meristematic tissue of Isoetes lacustris contain a single chloroplast which divides when the cells divide. Details of this process, as seen by electron microscopy, are described. INTRODUCTION Earlier workers using the light microscope have described in some detail the behaviour of chloroplasts of Isoetes species during the course of cell division. The polarity of these plastids during cell division was first described by Marquette (1907) for /. macrospora and later by Ma (1928) for /. melanopoda, and by Stewart (1948) for /. macrospora and /. muricata var. braunii. Paolillo (1962) using both the light and electron microscope observed the structure of plastids oil. howellii in a variety of tissues, including meristems, but his electron micrographs do not include any showing chloroplasts during cell division. The sequence of events associated with cell division seems to be similar within the meristematic regions of all the above species. This sequence has been described as follows. 1I) Resting cells of meristematic tissue contain a single chloroplast. (2) The plastid elongates and eventually divides following the appearance of a central constriction. The final separation of the chloroplast into two daughter plastids may occur prior to prophase or may be delayed even until the onset of metaphase. (3) The elongated plastid or daughter plastids lie closely appressed to the nucleus. (4) During division the daughter plastids migrate, one to each pole where they remain until the nuclei are reformed. When plastid division is delayed until metaphase, connections between the polar plastid portions are maintained on either side of the spindle. Examples of these various stages, first described under the light microscope, have been observed under the electron microscope and are recorded here. MATERIALS AND METHODS Segments of tissue from the zone of intercalary meristem in the basal portion of young leaves of Isoetes lacustris were prepared for examination under the electron microscope. The tissue was fixed in glutaraldehyde, stained with osmium tetroxide, and after dehydration in an alcohol series, embedded in Araldite; post staining was carried out using uranyl acetate and lead citrate. 139
2 140 JEAN M. WHATLEY OBSERVATIONS Plastids in intercalary meristem cells By use of the light microscope observations of earlier workers as a basis, it was possible to build up a series of electron micrographs showing the changes in chloroplast appearance and position within the cell during the course of cell division in Isoetes lacustris. (1) At interphase the cell contains a single plastid. It is small (compared with plastid size at other stages) and simple in outline. Some starch is present and there is a fairly restricted lamellar system. Vesicles similar to those described for angiosperm plastids as resulting from invaginations of the inner chloroplast membranes are also present (Plate I, No. i). (2) Light microscope observations show that the plastid elongates. The outline remains simple and internal structure is unchanged. The plastid lies close to but never attached to the nucleus (Plate i. No. 2). II I I Nucleu; I I Cytoplasm tv'^ Plasrid Fig. I. Model showing close relationship of amoeboid chloroplast to nucleus. The model is based on serial sections. (3) Before division the elongated plastid becomes highly amoeboid in shape. Broad areas of stroma are cut across by a still limited lamellar system. The position of the plastid close to the nucleus remains unchanged (Plate i. No. 3). (4) After plastid division the two daughter plastids generally remain close to the nucleus and frequently intertwine with it, for at this stage the nucleus also appears to be amoeboid in shape (Plate i. No. 4; Fig. i). No potential division figures of constricted plastids, as seen under the light microscope, could be found, but the amoeboid nature of the plastids made observation of this type of pattern particularly difficult. That division occurs at the amoeboid stage seems fairly certain, however. Observations of chloroplast numbers per cell were made with the high voltage electron microscope using thick serial sections. Cells with amoeboid plastids contained either one or two plastids. Other cells contained only single plastids. In /. lacustris, therefore, plastid division occurs perhaps as early as interphase but certainly before the onset of metaphase. (5) By metaphase, plastids have lost their amoeboid character and have taken up positions at the two poles on either side of the central chromosome band (Plate i. No. 5). (6) During anaphase the plastids remain at the poles (Plate i. No. 6). (7) During telophase the plastids remain at the poles as do some small rounded mitochondria. Other elongated mitochondria appear to be in process of migration and
3 Chloroplasts in Isoetes 141 occupy positions parallel to microtubules and at right angles to the cell plate (Plate 2, Nos. 7 and 9). (8) As cell division is completed, the plastids largely retain their former polar positions, lying at the ends of the daughter cells farthest from the new cell wall (Plate 2, No. 8). Plastids in cells of roots or mature leaves Plastids of roots (Plate 2, No. 10) and mature leaves (Plate 2, No. 11) differ considerably in appearance from those of meristematic tissue. Root plastids may contain some starch, but their most characteristic features are general lack of lamellar development and the presence of vesicles and osmiophilic bodies. The latter do not appear as regular in shape as the osmiophilic globules generally seen in plastids of other species. Their staining is less dense and they are sometimes as large as starch grains. Mature leaf plastids are very elongated, generally narrow at the extremities, and have a starch-filled centre. Conventional lamellar development is limited and granal stacking minimal. In contrast to the heavily stained thylakoid system, the plastids also contain a double membrane system which is much less electron dense, is arranged in concentric rings and which is associated with numerous vesicles (Plate 2, No. 12 insert). These plastids are quite different from those observed by Paolillo in the mature leaf of /. howellii. The latter have a shape and a well-developed granal-thylakoid system much more similar to those of conventional higher plant plastids. DISCUSSION The pattern of chloroplast behaviour during cell division in the genus Isoetes is of considerable interest. Because the non-dividing meristematic cells contain only a single plastid, chloroplast behaviour can be followed through subsequent cell division much more easily than in those plants with more numerous plastids in each cell. In the meristem of plants of this genus there appears to be a high degree of synchrony between nuclear division and chloroplast division. Such synchrony does not appear to occur in most higher plants, e.g. Phaseolus vulgaris (at present under study). The synchrony of plastid and nuclear division in /. lacustris does not, however, appear to be absolute. Metaphase was easy to distinguish and many cells were clearly recognizable as at interphase. Between these two stages it was found that chloroplast state and nuclear state did not keep in phase. It is suggested that the chloroplasts pass through the following stages: (i) simple, single and small; (2) simple, single and elongated; (3) amoeboid and single; (4) an amoeboid pair. In association with these four chloroplast states, nuclei occurred which ranged in state from those with dispersed chromatin to those with aggregated chromatin. The degree of dispersion or aggregation of chromatin in the nucleus appeared to be quite unrelated to the state of the adjacent chloroplast. Chloroplast division, therefore, may occur at some indeterminate time during late interphase or early prophase. Although chloroplast behaviour in Isoetes is distinctive, there appear to be certain features in common with dividing plastids of angiosperms. The constriction division pattern earlier reported for Isoetes from light microscope observations is identical with the pattern usually accepted as typical for angiosperms. Secondly, the tortuous shape of the supposedly dividing plastids of Isoetes corresponds to a similar amoeboid stage identified in 3-day-old primary leaves of Phaseolus vulgaris during the early stages of plastid division (J. M. Whatley, unpublished). It is at this stage also that lamellar de-
4 142 JEAN M. WHATLEY velopment is limited, a little starch is present, and vesicles are common within the stroma in chloroplasts of both Isoetes and immature Phaseolus. However, prolamellar body remnants present at this stage of Phaseolus development were absent in Isoetes chloroplasts. Although the synchrony of plastid and cell division in Isoetes does not appear to occur in the multi-plastid angiosperms nevertheless these two very different groups of plants do show some similarity in chloroplast structure at the time of division of immature plastids. ACKNOWLEDGMENTS I am grateful to Mr H. Edge for excellent technical assistance in preparing the serial sections and to the Science Research Council for financial support. REFERENCES MA, R. M. (1928). The chloroplasts of Isoetes melanopoda. Am. y. Bot., 15, 277. MARQUETTE, W. (1907). Manifestations of polarity in plant cells which apparently are without centrosomes. Beih. bot. Zbl., 21, 281. PAOLILLO, D. J. JR (1962). The plastids of Isoetes howellii. Am. y. Bot., 49, 590. STEWART, W. N. (1948). A study of the plastids in the cells of the mature sporophyte oi Isoetes. Bot. Gaz., no, 281. EXPLANATION OF PLATES Key to lettering: Ch, Chromosome; CP, cell plate; L, lamellar system; M, mitochondrion; MS, membrane system; Mt, microtubules; N, nucleus; O, oil droplet; OB, osmiophilic body; P, plastid; St, starch; V, vesicle. PLATE I No. I. Interphase cell with single small simple plastid. x No. 2. Elongated simple plastid at first stage of plastid division, x No. 3. Elongated amoeboid plastid at second stage of plastid division, x No. 4. Two amoeboid plastids closely associated with an amoeboid nucleus following plastid division, x No. 5. Metaphase cell with plastids, no longer amoeboid, occupying polar positions, x No. 6. Anaphase cell with the only plastid included in the section situated at a pole, x PLATE 2 No. 7. Telophase cell showing the continued polar position of the plastid as its cell plate is formed. Some elongated mitochondria appear to be migrating towards the cell plate, x No. 8. Daughter cells have plastids at the ends of the cells away from the newly formed cell wall. X No. 9. Enlargement of part of the telophase cell showing the microtubules extending at right angles to and across the cell plate. The elongated mitochondria lie parallel to the microtubules. X 15,000. No. 10. Root plastid with almost no lamellar system. Vesicles and osmiophilic bodies are present, x No. II. Plastid from a mature leaf cell sbowing a massive central concentration of starch grains. The elongated plastid contains a limited, densely stained thylakoid system in addition to a second less densely stained membrane system, x No. 12. Enlargement of part of a mature leaf plastid showing the concentric pattern of the second membrane system and associated vesicles, x 10,000.
5 THE NEW PHYTOLOGIST, 73, i PLATE I JEAN M. WHAThEY CHOROPLASTS JN ISOETES {facing page 142)
6 THE NEW PHYTOLOGIST, 73, i PLATE 2 JEAN M. V^'H\Tl.Y.Y CHOROPLASTS IN ISOETES
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