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Some New Aspects of the Microtubular Organization of the Mitotic Spindle and the Phragmoplast Spindle

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Some New Aspects of the Microtubular Organization of the Mitotic Spindle and the Phragmoplast Spindle 1969 163 Some New Aspects of the Microtubular Organization of the Mitotic Spindle and the Phragmoplast Spindle L. V. Olah Botany Department, Southern Illinois University Carbondale, Illinois, U. S. A. Received June 24, 1968 With the great influx of ultrastructural investigations carried out in the last decade, the classical concepts concerning the organization and function of the mitotic spindle and the phragmoplast have become untenable, and their revision is an inevitable necessity. It has become apparent that there are several functionally different microtubules of separate purposes in plant cells: a) cortical microtubules of two assumed different functions (Ledbetter and Porter 1963, 1964), b) microtubules constituting a preprophase band around the nucleus before the onset of mitosis (Pickett-Heaps and Northcote 1966 a, b), c) mitotic spindle microtubules constituting chromosomal fibers and continuous fibers, and d) microtubules constituting the phragmoplast spindle (Olah 1966, Ledbetter 1967). Regardless of their function, all microtubules seem to display identical or closely similar structure on the submicroscopical level (Ledbetter and Porter 1963, 1964, Harris 1962, Roth and Daniels 1962). Descriptions of the fine structures of all microtubules of animal and plant organisms agree that microtubules seem to be structurally related to cilium and flagellum (Ledbetter and Porter 1964, Manton 1952). Both are composed of 11-14 subunits 40A in diameter forming a cylindrical sheath around a hollow space. The subunits seem to be built of a proteinaceous material by polymerization of a monomer available throughout the cell. Observable cross striations indicate the existence of a spiral pattern (Harris 1962). The cortical microtubules may have two separate functions: 1. They may serve to orient cellulose microfibrils during primary and secondary cell wall formation (Ledbetter and Porter 1963, 1964, Green 1962). 2. They may participate in the process of cyclosis generated by their undulating movement (Ledbetter and Porter 1963, 1914, Jarosch 1958). Their proximity to the plasmalemma and their parallel orientation to the microfibrils strongly support the first assumption. Their similarity in structure to cilium and flagellum supports the second assumption. Instead of cortical microtubules present in preprophase, Northcote and Pickett-Heaps recently detected a band of microtubules located near the plasma lemma which encircles the nucleus (Pickett-Heaps and Northcote 1966 a, b). They noted that the future cell plate joins the mother wall at the same area 11* 164 L. V. Olah Cytologia 34 in which the band is located. In other words, the position of the cell plate is predetermined by the position of the microtubular preprophase band. Microtubules of the mitotic spindle constituting the chromosomal fibers are directly involved in chromosomal movement. They are formed in late prophase and disappear in telophase. The microtubules constituting the con tinuous fibers of the mitotic spindle were believed to participate in phragmo plast formation. Some authors supposed. that the transformation of the spindle to the phragmoplast was due to a condensation of continuous fibers (Sato 1959, Inoue and Bajer 1961) (Figs. 1, 2). Most of the above observations indicate that microtubules are short-living elements, their polymerization and de-polymerization being a rapid process. The monomer for polymerization seems to be available throughout the cell (Ledbetter 1967). Our investigations were focused on the particular interrelationship between mitotic spindle and phragmoplast. A new mitotic agent was found which specifically dissociated these two organelles in meristematic cells. The effect of this agent, a foaming saponin of steroid structure called digitonion, was studied on both optical and ultrastructural levels (Olah 1963, 1965, Under brink and Olah 1963, 1965, 1967). As a result, a new concept was proposed (Olah 1966). According to this concept, all or almost all the microtubules constituting continuous fibers disappear until telophase. The development of the phragmoplast begins with the formation of newly polymerized microtubules. That is, the spindle continuous fibers do not transform into a phragmoplast. Rather, in higher plants, there are two entirely independent microtubular organells; one in the mitotic spindle formed at late prophase and abolished until telophase, and the other is the phragmoplast spindle formed during late anaphase and telophase. Inoue and Bajer observed that birefringency almost disappears in late anaphase in the interzonal region. However, a strong birefringency reappears in early telophase on both sides of the forming cell plate (Fig. 1 right, 2 left). The birefringency progresses along side the cell plate (Fig. 2 left). Birefringency decreases in strength over the established portion of the cell plate (Fig. 2 right), and disappears when the cell plate joins the maternal wall. The authors believed that the condensation of continuous fibers causes the increasing birefringency. According to our interpretation, the appearance of strong birefringency is due to the formation of a newly synthesized microtubular system (i.e., the phragmoplast spindle). Thus, the transfor mation of continuous fibers by condensation into phragmoplast is an untenable concept. In meristematic cells in which the cell plate formation usually begins in the central part of the equatorial plane, the new phragmoplast mie_??_ules first appear over this region. As the cell plate develops like an _??_ing diaphragm, new microtubules are formed successively along the growi_??_ge 1969 Some New Aspects of the Microtubular Organization of Spindles 165 Figs. 1-9. 1, development of the phragmoplast in Haemanthus katherinae according to Inoue and Bajer. Left picture: early telophase. Continuous fibers are birefringent in the interzonal region. Lower corner of equatorial region shows a strongly birefringent spot, indicating the initiation of the cell plate. Right picture: forty minutes later, portion of the cell plate became visible, and both sides of the plate is strongly birefringent. 2, left picture: more advanced stage of cell plate development. Note the strongly birefring ent region covering both sides of the growing cell plate. Right picture: fourteen minutes later, showing cell plate almost reaching the periphery of the cell. Birefringency is di minishing in the mid-region. 3 and 4, syncytial endosperm of Iris pseudacorus, shown by Jungers. 5, syncytial endosperm development shown by Strasburger in Agrimonia eupatoria. 6, two developmental stages of syncytial endosperm in Sequoia gigantea shown by Bucholz. 7, multi-spindled system formed between interphase sister and non-sister nuclei in Iris pseudacorus, shown by Jungers. 8, fine structure of a meristematic cell (longitudinal section) fixed in CdCl2 by Wada. Fibrillar (microtubular) system has dis appeared over the established region of the cell plate. However, a doughnut-shaped micro tubular ring of the phragmoplast spindle is still visible (a-b) around the growing edge of the plate. Courtesy of B. Wada. 9, schematic representation of the meiosis of a PMC with simultaneous development of the separating cell walls by Gottschalk. 166 L. V. Olah Cytologia 34 of the cell plate. At the same time, when the central circular segment of the cell plate is completely established, the phragmoplast microtubules succes sively disappear. If the cell plate is already bordered on both sides by plasmalemma, the phragmoplast microtubules are no longer present. Thus, a doughnut-shaped fibrillar structure composed of microtubules is observable during the development of the cell plate. With the expanding plate, this ring-like structure expands centrifugally by the addition of new microtubules on the outer surface and by the abolishment of those in the inner surface. When the cell plate joins the mother wall, all microtubules disappear (Olah 1966, Ledbetter 1967, Wada 1966) (Fig. 8). Thus, in meristematic cells, mitotic and phragmoplast spindles overlap each other. However, there are at least two biological systems in which the dissociation of these organelles in time and space is complete. These systems are: syncytial1 endosperm of Iris pseudacorus (Jungers 1931) (Figs. 3, 4), Agrimonia eupatoria (Strasburger 1934) (Fig. 5), Sequoia gigantea (Bucholz 1939) (Fig. 6), and those pollen mother cells in which cell plate formation occurs simultaneously during the second meiotic division. The first description about syncytial endosperm came from Jungers in 1931. Reinvestigating the described phenomenon, we found further evidence of the validity of his observations. In the syncytial endosperm, a series of mitoses occurs in which cell plate formation is omitted. If a certain number of nuclei are produced to build up a syncytium, a multi-spindled system appears almost simultaneously to connect sister and non-sister nuclei equally (Fig. 7). On optical level, these phragmoplast spindles connecting interphase nuclei seem to be almost structurally identical with mitotic spindles. However, it is clear that the phragmoplast spindles have no relationship to chromosomal movement and their function is exclusively related to the process of cell plate formation. In the simultaneously dividing PMC's, a similar phenomenon occurs. During second division, four spindles are present connecting sister and non sister nuclei (Gottschalk 1954) (Fig. 9). Cell plate is formed in all four equatorial regions of these spindles. Moreover, we found in Dodecatheon
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