Abstract
The spindle of the colonial diatom Fragilaria contains two distinct sets of spindle microtubules (MTs): (a) MTs comprising the central spindle, which is composed of two half-spindles interdigitated to form a region of "overlap"; (b) MTs which radiate laterally from the poles. The central spindles from 28 cells are reconstructed by tracking each MT of the central spindle through consecutive serial sections. Because the colonies of Fragilaria are flat ribbons of contiguous cells (clones), it is possible, by using single ribbons of cells, to compare reconstructed spindles at different mitotic stages with minimal intercellular variability. From these reconstructions we have determined: (a) the changes in distribution of MTs along the spindle during mitosis; (b) the change in the total number of MTs during mitosis; (c) the length of each MT (measured by the number of sections each traverses) at different mitotic stages; (d) the frequency of different classes of MTs (i.e., free, continuous, etc.); (e) the spatial arrangement of MTs from opposite poles in the overlap; (f) the approximate number of MTs, separate from the central spindle, which radiate from each spindle pole. From longitudinal sections of the central spindle, the lengths of the whole spindle, half-spindle, and overlap were measured from 80 cells at different mitotic stages. Numerous sources of error may create inaccuracies in these measurements; these problems are discussed. The central spindle at prophase consists predominantly of continuous MTs (pole to pole). Between late prophase and prometaphase, spindle length increases, and the spindle is transformed into two half-spindles (mainly polar MTs) interdigitated to form the overlap. At late anaphase-telophase, the overlap decreases concurrent with spindle elongation. Our interpretation is that the MTs of the central spindle slide past one another at both late prophase and late anaphase. These changes in MT distribution have the effect of elongating the spindle and are not involved in the poleward movement of the chromosomes. Some aspects of tracking spindle MTs, the interaction of MTs in the overlap, formation of the prophase spindle, and our interpretation of rearrangements of MTs, are discussed.
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- Brinkley B. R., Cartwright J., Jr Ultrastructural analysis of mitotic spindle elongation in mammalian cells in vitro. Direct microtubule counts. J Cell Biol. 1971 Aug;50(2):416–431. doi: 10.1083/jcb.50.2.416. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Franke W. W., Reau P. The mitotic apparatus of a zygomycete, Phycomyces blakesleeanus. Arch Mikrobiol. 1973 Mar 26;90(2):121–129. doi: 10.1007/BF00414514. [DOI] [PubMed] [Google Scholar]
- Fuge H. The arrangement of microtubules and the attachment of chromosomes to the spindle during anaphase in tipulid spermatocytes. Chromosoma. 1974 Apr 9;45(3):245–260. doi: 10.1007/BF00283409. [DOI] [PubMed] [Google Scholar]
- Fuge H. Verteilung der Mikrotubuli in Metaphase- und Anaphase-Spindeln der Spermatocyten von Pales ferruginea. Eine quantitative Analyse von Serienquerschnitten. Chromosoma. 1973 Aug 10;43(2):109–143. doi: 10.1007/BF00483375. [DOI] [PubMed] [Google Scholar]
- Heath I. B., Heath M. C. Ultrastructure of mitosis in the cowpea rust fungus Uromyces phaseoli var. Vignae. J Cell Biol. 1976 Sep;70(3):592–607. doi: 10.1083/jcb.70.3.592. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Heath I. B. Mitosis in the fungus Thraustotheca clavata. J Cell Biol. 1974 Jan;60(1):204–220. doi: 10.1083/jcb.60.1.204. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Manton I., Kowallik K., von Stosch H. A. Observations on the fine structure and development of the spindle at mitosis and meiosis in a marine centric diatom (Lithodesmium undulatum). 3. The later stages of meiosis I in male gametogenesis. J Cell Sci. 1970 Jan;6(1):131–157. doi: 10.1242/jcs.6.1.131. [DOI] [PubMed] [Google Scholar]
- Margolis R. L., Wilson L. Opposite end assembly and disassembly of microtubules at steady state in vitro. Cell. 1978 Jan;13(1):1–8. doi: 10.1016/0092-8674(78)90132-0. [DOI] [PubMed] [Google Scholar]
- McCully E. K., Robinow C. F. Mitosis in Mucor hiemalis. A comparative light and electron microscopical study. Arch Mikrobiol. 1973 Dec 21;94(2):133–148. doi: 10.1007/BF00416688. [DOI] [PubMed] [Google Scholar]
- McDonald K., Pickett-Heaps J. D., McIntosh J. R., Tippit D. H. On the mechanism of anaphase spindle elongation in Diatoma vulgare. J Cell Biol. 1977 Aug;74(2):377–388. doi: 10.1083/jcb.74.2.377. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McIntosh J. R., Cande W. Z., Snyder J. A. Structure and physiology of the mammalian mitotic spindle. Soc Gen Physiol Ser. 1975;30:31–76. [PubMed] [Google Scholar]
- McIntosh J. R., Landis S. C. The distribution of spindle microtubules during mitosis in cultured human cells. J Cell Biol. 1971 May 1;49(2):468–497. doi: 10.1083/jcb.49.2.468. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McIntosh J. R., Ogata E. S., Landis S. C. The axostyle of Saccinobaculus. I. Structure of the organism and its microtubule bundle. J Cell Biol. 1973 Feb;56(2):304–323. doi: 10.1083/jcb.56.2.304. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Peterson J. B., Ris H. Electron-microscopic study of the spindle and chromosome movement in the yeast Saccharomyces cerevisiae. J Cell Sci. 1976 Nov;22(2):219–242. doi: 10.1242/jcs.22.2.219. [DOI] [PubMed] [Google Scholar]
- Pickett-Heaps J. D., McDonald K. L., Tippit D. H. Cell division in the pennate diatom Diatoma vulgare. Protoplasma. 1975;86(1-3):205–242. doi: 10.1007/BF01275633. [DOI] [PubMed] [Google Scholar]
- Pickett-Heaps J. D., Tippit D. H. The diatom spindle in perspective. Cell. 1978 Jul;14(3):455–467. doi: 10.1016/0092-8674(78)90232-5. [DOI] [PubMed] [Google Scholar]
- Rieder C., Bajer A. S. Heat-induced reversible hexagonal packing of spindle microtubules. J Cell Biol. 1977 Sep;74(3):717–725. doi: 10.1083/jcb.74.3.717. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Roos U. P. Mitosis in the cellular slime mold Polysphondylium violaceum. J Cell Biol. 1975 Feb;64(2):480–491. doi: 10.1083/jcb.64.2.480. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tippit D. H., Pickett-Heaps J. D. Mitosis in the pennate diatom Surirella ovalis. J Cell Biol. 1977 Jun;73(3):705–727. doi: 10.1083/jcb.73.3.705. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tucker J. B. Shape and pattern specification during microtubule bundle assembly. Nature. 1977 Mar 3;266(5597):22–26. doi: 10.1038/266022a0. [DOI] [PubMed] [Google Scholar]