Abstract
The initiation and development of a radial array of microtubules (MTs) in guard cells of A. cepa was studied using immunofluorescence microscopy of tubulin in isolated epidermal layers. Soon after the completion of cytokinesis, MTs originate in the cortex adjacent to a central strip of the new, anticlinically oriented ventral wall separating the two guard cells. Cortical MTs extend from the mid-region of the central strip toward the cell edge where the ventral wall joins the inner periclinal wall. They then spread in a fan-like formation along the periclinal wall and gradually extend along the lateral and end walls as well. Many MTs criss-cross at various angles as they arc past the edge formed by the junction of the ventral and periclinal walls, but they do not terminate there, indicating that, contrary to previous report, the edge is not involved in MT initiation. Instead, the mid-region of the central strip appears to function as a planar MT-organizing zone. Initially, MTs radiate from this zone through the inner cytoplasm as well as the cortex. During cell expansion, however, the cortical MTs increasingly predominate and consolidate into relatively thick, long bundles, while the frequency of non-cortical MTs diminishes. The apparent density of MTs per unit surface area is maintained as the cells expand and gradually flex into an elliptical shape. The guard cells eventually separate completely at the pore site. The entire process is accomplished within about 12 h.
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Abbreviations
- DIC:
-
differential interference contrast
- GC:
-
guard cell
- MT:
-
microtubule
References
Apostolakos, P., Galatis, B. (1985) Studies on the development of the air pores and air chambers of Marchantia paleacea. II. Ultrastructure of the initial aperture formation with particular reference to cortical microtubule organizing centres. Can. J. Bot. 63, 744–756
Busby, C.H., Gunning, B.E.S. (1984) Microtubules and morphogenesis in stomata of the water fern Azolla: an unusual mode of guard cell and pore development. Protoplasma 122, 108–119
Clayton, L., Black, C.M., Lloyd, C.W. (1985) Microtubule nucleating sites in higher plant cells identified by an auto-antibody against pericentriolar material. J. Cell Biol 101, 319–324
Cleary, A.L., Hardham, A.R. (1989) Microtubule organization during development of stomatal complexes in Lolium rigidum. Protoplasma (in press)
Cyr, R.J., Palevitz, B.A (1989) Microtubule-binding proteins from carrot. I. Initial characterization and microtubule bundling. Planta 177, 245–260
Doohan, M.E., Palevitz, B.A. (1980) Microtubules and coated vesicles in guard-cell protoplasts of Allium cepa L. Planta 149, 389–401
Galatis, B. (1980) Microtubules and guard-cell morphogenesis in Zea mays L. J. Cell Sci. 45, 211–244
Galatis, B. (1982) The organization of microtubules in guard cell mother cells of Zea mays. Can. J. Bot. 60, 1148–1166
Galatis, B. (1988) Microtubules and epithem-cell morphogenesis in hydathodes of Pilea cadierei. Planta 176, 287–297
Galatis, B., Mitrakos, K. (1980) The ultrastructural cytology of the differentiating guard cells of Vigna sinensis. Am. J. Bot. 67, 1243–1261
Galatis, B., Apostolakos, P., Katsaros, C. (1983) Microtubules and their organizing centres in differentiating guard cells of Adiantum capillus veneris. Protoplasma 115, 176–192
Giddings, T.H., Jr., Staehelin, L.A. (1988) Spatial relationship between microtubules and plasma-membrane rosettes during the deposition of primary wall microfibrils in Closterium sp. Planta 173, 22–30
Gunning, B.E.S., Hardham, A.R. (1982) Microtubules. Annu. Rev. Plant Physiol 33, 651–698
Hardham, A.R., Gunning, B.E.S. (1978) Structure of cortical microtubule arrays in plant cells. J. Cell Biol 77, 14–34
Hepler, P.K. (1981) Morphogenesis of tracheary elements and guard cells. In: Cytomorphogenesis in plants, pp. 327–347. Kiermayer, O., ed. Springer, Wien New York
Hepler, P.K., Palevitz, B.A. (1986) Metabolic inhibitors block anaphase A in vivo. J. Cell Biol. 102, 1995–2005
Kaufman, P.B., Petering, L.B., Yocum, C.S., Baic, D. (1970) Ultrastructural studies on stomata development in internodes of Avena sativa. Am. J. Bot. 57, 33–49
Kirschner, M., Mitchison, T. (1986) Beyond self-assembly: from microtubules to morphogenesis Cell 45, 329–342
Marc, J., Hackett, P.W. (1989) A new method for immunofluorescent localization of microtubules in surface cell layers: application to the shoot apical meristem of Hedera. Protoplasma 148, 70–79
Marc, J., Mineyuki, Y., Palevitz, B.A. (1989) A planar microtubule-organizing zone in guard cells of Allium: experimental depolymerization and reassembly of microtubules. Planta 179, 530–540
Mishkind, M., Palevitz, B.A., Raikhel, N.V. (1981) Cell wall architecture: normal development and environmental modification of guard cells of the Cyperaceae and related species. Plant Cell Environ. 4, 319–328
Mitchison, T., Kirschner, M. (1984) Microtubule assembly nucleated by isolated centrosomes. Nature 312, 232–237
Palevitz, B.A. (1981a) The structure and development of stomatal cells. In: Stomatal physiology, pp. 1–23, Jarvis, P.E., Mansfield, T.A., eds. Cambridge University Press, Cambridge, UK
Palevitz, B.A. (1981b) Microtubules and possible microtubule nucleation centers in the cortex of stomatal cells as visualized by high voltage electron microscopy. Protoplasma 107, 115–125
Palevitz, B.A. (1982) The stomatalcomplex as a model of cytoskeletal participation in cell differentiation. In: The cytoskeleton in plant growth and development, pp. 345–376, Lloyd, C.W., ed. Academic Press, London
Palevitz, B.A. (1986) Division plane determination in guard mother cells of Allium: video time-lapse analysis of nuclear movements and phragmoplast rotation in the cortex. Dev. Biol. 117, 644–654
Palevitz, B.A., Hepler, P.K. (1976) Cellulose microfibril orientation and cell shaping in developing guard cells of Allium: the role of microtubules and ion accumulation Planta 132, 71–93
Palevitz, B.A., Mullinax, J.B. (1989) Developmental changes in the arrangement of cortical microtubules in stomatal cells of oat (Avena sativa L.). Cell Motil. Cytoskeleton 13, 170–180
Palevitz, B.A., O'Kane, D.J., Kobres, R.E., Raikhel, N.V. (1981) Vacuole movements and changes in morphology in differentiating cells as revealed by epifluorescence, video and electron microscopy. Protoplasma 109, 23–55
Quader, H., Deichgraber, G., Schnepf, E. (1986) The cytoskeleton of Cobaea seed hairs: patterning during cell-wall differentiation. Planta 168, 1–10
Raschke, K. (1979) Movements of stomata. In: Encyclopedia of plant physiology, N.S., vol. 7. Physiology of movements. pp. 385–441, Haupt, W., Feinleib, M.E., eds., Springer, Berlin Heidelberg New York
Sack, F.D., Paolillo, D.J., Jr. (1983) Protoplasmic changes during stomatal development in Funaria. Can. J. Bot. 61, 2515–2526
Schnepf, E. (1984) Pre- and postmitotic reorientation of microtubule arrays in young Sphagnum leaflets: transitional stages and initiation sites. Protoplasma 120, 100–112
Schulze, E., Kirschner, M. (1987) Dynamic and stable populations of microtubules in cells. J. Cell. Biol. 104, 277–288
Singh, A.P., Srivastava, L.M. (1973) The fine structure of pea stomata. Protoplasma 76, 61–82
Srivastava, L.M., Singh, A.P. (1972) Stomatal structure in corn leaves. J. Ultrastruct. Res. 39, 345–363
Wick, S.M. (1985) The higher plant mitotic apparatus: redistribution of microtubules, calmodulin and microtubule initiation material during its establishment. Cytobios 43, 285–294
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Marc, J., Mineyuki, Y. & Palevitz, B.A. The generation and consolidation of a radial array of cortical microtubules in developing guard cells of Allium cepa L.. Planta 179, 516–529 (1989). https://doi.org/10.1007/BF00397591
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DOI: https://doi.org/10.1007/BF00397591