Skip to main content
Log in

The microtubular cytoskeleton during development of the zygote, proembryo and free-nuclear endosperm in Arabidopsis thaliana (L.) Heynh

  • Published:
Planta Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

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

    Article  CAS  Google Scholar 

  • Cleary, A.L. (1989) Microtubule organization and nucleation in higher plant cells. Ph.D. thesis, Australian National University, Canberra

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Gunning, B.E.S., Hardham, A.R. (1982) Microtubules. Annu. Rev. Plant Physiol. 33, 651–698

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Hogan, C.J. (1987) Microtubule patterns during meiosis in two higher plant species. Protoplasma 138, 126–136

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Johansen, D.A. (1950) Plant Embryology. Embryogeny of the Spermatophyta. Chronica Botanica Co., Waltham, Mass., USA

    Google Scholar 

  • LaClaire, J.W., II (1987) Microtubule cytoskeleton in intact and wounded coenocytic green algae. Planta 171, 30–42

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Misra, R.C. (1962) Contribution to the embryology of Arabidopsis thalianum (Gay et Monn.). Agra Univ. J. Res. 11, 191–199

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Raghavan, V. (1986) Embryogenesis in angiosperms. A developmental and experimental study. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Singh, A.P., Mogensen, H.L. (1975) Fine structure of the zygote and early embryo in Quercus gambelii. Am. J. Bot. 62, 105–115

    Article  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Woodcock, C.L.F. (1971) The anchoring of nuclei by cytoplasmic microtubules in Acetabularia. J. Cell Sci. 8, 611–621

    CAS  PubMed  Google Scholar 

  • Yakovlev, M.S., Alimova, G.K. (1976) Embryogenesis in Arabidopsis thaliana (L.) Heynh. (Cruciferae). [In russ] Bot. Zh. 61, 12–24

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

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.

Rights and permissions

Reprints and permissions

About this article

Cite this article

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

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00197947

Key words

Navigation