Abstract
The microtubular cytoskeleton has been studied during development of the zygote, proembryo and free-nuclear endosperm in A. thaliana using immunofluorescence localization of tubulin in enzymatically isolated material. Abundant micro tubules (MTs) are found throughout proembryogenesis. Microtubules in the coenocytic endosperm are mainly internal. By contrast, there is a re-orientation of MTs to a transverse cortical distribution during zygote development, predominantly in a subapical band which accompanies a phase of apical extension. The presence of these cortical arrays coincides with the elongation of the zygote. Cortical arrays also accompany elongation of the cylindrical suspensor. Extensive networks of MTs ramify throughout the cytoplasm of cells in the proembryo proper. Perinuclear arrays are detected in a number of cell types and MTs contribute to typical mitotic configurations during nuclear divisions. Preprophase bands of MTs are absent throughout megasporogenesis and embryo-sac development and do not occur in endosperm cell divisions. We have observed MTs throughout the first division cycle of the zygote. By placing the observed stages in a most probable sequence, we have identified this cell cycle as the point during embryogenesis at which a preprophase band is reinstated as a regular feature of cell division. Preprophase bands were observed to predict planes of cytokinesis in cell divisions up to the octant stage.
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Abbreviations
- DIC:
-
differential interference contrast optics
- MT:
-
microtubule
- PPB:
-
preprophase band of microtubule
References
Caspar, T., Huber, S.C., Somerville, C. (1985) Alterations in growth, photosynthesis, and respiration in a starchless mutant of Arabidopsis thaliana (L.) deficient in chloroplast phosphoglucomutase activity. Plant Physiol. 79, 11–17
Cleary, A.L. (1989) Microtubule organization and nucleation in higher plant cells. Ph.D. thesis, Australian National University, Canberra
Doonan, J.H., Cove, D.J., Corke, F.M.K., Lloyd, C.W. (1987) Pre-prophase band of microtubules, absent from tip-growing moss filaments, arises in leafy shoots during transition to intercalary growth. Cell Motil. Cytoskel. 7, 138–153
Gunning, B.E.S., Hardham, A.R. (1982) Microtubules. Annu. Rev. Plant Physiol. 33, 651–698
Gunning, B.E.S., Sammut, M. (1990) Rearrangements of microtubules involved in establishing cell division planes start immediately after DNA synthesis and are completed just before mitosis. Plant Cell 2, 1273–1282
Hogan, C.J. (1987) Microtubule patterns during meiosis in two higher plant species. Protoplasma 138, 126–136
Huang, B.-Q., Russell, S.D., Strout, G.W., Mao, L.-J. (1990) Organization of isolated embryo sacs and eggs of Plumbago zeylanica (Plumbaginaceae) before and after fertilization. Am. J. Bot. 77, 1401–1410
Johansen, D.A. (1950) Plant Embryology. Embryogeny of the Spermatophyta. Chronica Botanica Co., Waltham, Mass., USA
LaClaire, J.W., II (1987) Microtubule cytoskeleton in intact and wounded coenocytic green algae. Planta 171, 30–42
Mansfield, S.G., Briarty, L.G. (1987) The anatomy and ultrastructure of embryogenesis in Arabidopsis thaliana L. XIV Int. Bot. Congr. (Berlin), Abstr. 17, 243
Marsden, M.P.F., Meinke, D.W. (1985) Abnormal development of the suspensor in an embryo-lethal mutant of Arabidopsis thaliana. Am. J. Bot. 72, 1801–1812
Meinke, D.W., Sussex, I.M. (1979) Embryo-lethal mutants of Arabidopsis thaliana. A model for genetic analysis of plant embryo development. Dev. Biol. 72, 50–61
Misra, R.C. (1962) Contribution to the embryology of Arabidopsis thalianum (Gay et Monn.). Agra Univ. J. Res. 11, 191–199
Murata, T., Kadota, A., Hogetsu, T., Wada, M. (1987) Circular arrangement of cortical microtubules around the subapical part of a tip-growing fern protonema. Protoplasma 141, 135–138
Raghavan, V. (1986) Embryogenesis in angiosperms. A developmental and experimental study. Cambridge University Press, Cambridge, UK
Singh, A.P., Mogensen, H.L. (1975) Fine structure of the zygote and early embryo in Quercus gambelii. Am. J. Bot. 62, 105–115
Van Lammeren, A.A.M. (1988a) Immunocytochemical visualization of the microtubular cytoskeleton in developing kernels of wheat (Triticum aestivum). In: Sexual reproduction in higher plants, pp. 401–406, Cresti, M., Gori, P., Pacini, E., eds. Springer, Berlin Heidelberg New York
Van Lammeren, A.A.M. (1988b) Structure and function of the microtubular cytoskeleton during endosperm development in wheat: an immunofluorescence study. Protoplasma 146, 18–27
Webb, M.C., Gunning, B.E.S. (1990a) Embryo sac development in Arabidopsis thaliana. I. Megasporogenesis, including the microtubular cytoskeleton. Sex. Plant Reprod. 3, 244–256
Webb, M.C., Gunning, B.E.S. (1990b) The cytoskeleton during megagametogenesis, fertilization and proembryo development in Arabidopsis thaliana. In: Proc. XI Int. Symp. “Embryology and Seed Reproduction”, Komarov Bot. Inst. (Acad. Sci. USSR), Leningrad, 3–7 July 1990, in press
Wick, S.M., Duniec, J. (1983) Immunofluorescence microscopy of tubulin and microtubule arrays in plant cells. I. Preprophase band development and concomitant appearance of nuclear envelope-associated tubulin. J. Cell Biol. 97, 235–243
Willemse, M.T.M., Van Lammeren, A.A.M. (1988) Structure and function of the microtubular cytoskeleton during megasporogenesis and embryo sac development in Gasteria verrucosa (Mill.) H. Duval. Sex. Plant Reprod. 1, 74–82
Woodcock, C.L.F. (1971) The anchoring of nuclei by cytoplasmic microtubules in Acetabularia. J. Cell Sci. 8, 611–621
Yakovlev, M.S., Alimova, G.K. (1976) Embryogenesis in Arabidopsis thaliana (L.) Heynh. (Cruciferae). [In russ] Bot. Zh. 61, 12–24
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We thank Ms. Margaret Travers for her helpful English translation of Yakovlev and Alimova (1976) and Mr. James Whitehead for preparation of Fig. 11. M.C.W. was supported by an Australian Postgraduate Research Award.
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Webb, M.C., Gunning, B.E.S. The microtubular cytoskeleton during development of the zygote, proembryo and free-nuclear endosperm in Arabidopsis thaliana (L.) Heynh. Planta 184, 187–195 (1991). https://doi.org/10.1007/BF00197947
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DOI: https://doi.org/10.1007/BF00197947