Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Tubular and filamentous structures in pollen tubes: Possible involvement as guide elements in protoplasmic streaming and vectorial migration of secretory vesicles

Summary

An ultrastructural study of the pollen tubes of Lilium and Clivia has demonstrated three different classes of longitudinal structures which could influence patterns of protoplasmic streaming and/or serve as “guide elements” in the vectorial migration of secretory vesicles: (a), cortical and noncortical microtubules; (b), microfilaments; and (c), subcortical tubules and cisternae of the endoplasmic reticulum (“subsurface cisternae”). Morphological details of these structures are described. Colchicine concentrations which lead to the complete disappearance of the microtubules affect neither germination of the pollen nor cytoplasmic streaming and tip growth of the elongating pollen tubes. Tip growth is initially uninhibited by cycloheximide, and cytoplasmic streaming is insensitive to this inhibitor. However, both of these processes are sensitive to cytochalasin B and vinblastine. Our results suggest that neither microtubules nor subsurface cisternae are essential for cytoplasmic streaming and directional secretion of cell surface materials in the pollen tube but would be consistent with an involvement of microfilamentous structures in these processes. Additionally, the possible importance of the lateral cross-link elements interconnecting all three types of structures is discussed.

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

References

  1. Allen, R. D.: A reinvestigation of cross sections of cilia. J. Cell Biol. 37, 825–831 (1968).

  2. Allen, R. D.: Fine structure of membraneous and microfibrillar systems in the cortex of Paramecium caudatum. J. Cell Biol. 49, 1–20 (1971).

  3. Anderson, G. W., Brenner, R. M.: The formation of basal bodies (centrioles) in rhesus monkey oviduct. J. Cell Biol. 50, 10–34 (1971).

  4. Bikle, D., Tilney, L. G., Porter, K. R.: Microtubules and pigment migration in the melanophores of Fundulus heteroclitus. Protoplasma (Wien) 61, 322–345 (1966).

  5. Brown, R. M., Franke, W. W., Kleinig, H., Falk, H., Sitte, P.: Scale formation in chrysophycean algae. I. Cellulosic and noncellulosic components made by the Golgi apparatus. J. Cell Biol. 45, 246–271 (1970).

  6. Campbell, R. D., Campbell, J. H.: Origin and continuity of desmosomes. In: Origin and continuity of cell organelles. Results and problems in cell differentiation, ed. by Reinert, J., Ursprung, H., vol. 2, p. 261–298. Berlin-Heidelberg-New York: Springer 1971.

  7. Crang, R. E., Miles, G. B.: An electron microscope study of germinating Lychnis alba pollen. Amer. J. Bot. 56, 398–405 (1969).

  8. Cronshaw, J.: Tracheid differentiation in tobacco pith cultures. Planta (Berl.) 72, 78–90 (1967).

  9. Dahlström, A.: In: Cellular dynamics of the neuron, ed. Barondes, S. H., p. 153–174. New York and London: Academic Press 1969.

  10. Darlington, C. D., LaCour, L. F.: Methoden der Chromosomenuntersuchung, S. 76. Stuttgart: Kosmos-Verlag 1963.

  11. Dashek, W. V., Rosen, W. G.: Electron microscopical localisation of chemical components in the growth zone of lily pollen tubes. Protoplasma (Wien) 61, 192–204 (1966).

  12. Dickson, M. R., Mercer, E. H.: Fine structure of the pedal gland of Philodina roseola (Rotifera). J. Microscopie 5, 81–90 (1966).

  13. Dirksen, E. R.: Centriole morphogenesis in developing ciliated epithelium of the mouse oviduct. J. Cell Biol. 51, 286–302 (1971).

  14. Franke, W. W.: Cytoplasmic microtubules linked to endoplasmic reticulum with cross-bridges. Exp. Cell Res. 66, 486–489 (1971a).

  15. Franke, W. W.: Membrane-microtubule-microfilament relationship in the ciliate pellicle. Cytobiologie 4, 307–316 (1971b).

  16. Franke, W. W.: Relationship of nuclear membranes with filaments and microtubules. Protoplasma (Wien) 73, 263–292 (1971c).

  17. Franke, W. W., Kartenbeck, J., Zentgraf, H., Scheer, U., Falk, H.: Membrane-tomembrane cross-bridges. A means to orientation and interaction of membrane faces. J. Cell Biol. 51, 881–888 (1971).

  18. Freed, J. J., Lebowitz, M. M.: The association of a class of saltatory movements with microtubules in cultured cells. J. Cell Biol. 45, 334–354 (1970).

  19. Goldman, R. D., Follett, E. A. C.: The structure of the major cell processes of isolated BHK 21 fibroblasts. Exptl. Cell Res. 57, 263–276 (1969).

  20. Grimstone, A. V., Cleveland, L. R.: The fine structure and function of the contractile axostyles of certain flagellates. J. Cell Biol. 24, 387–400 (1965).

  21. Grove, S. N., Bracker, C. E., Morré, D. J.: An ultrastructural basis for hyphal tip growth in Pythium ultimum. Amer. J. Bot. 57, 245–266 (1970).

  22. Gullvåg, B. M.: The fine structure of pollen grains and spores: A selective review from the last twenty years of research. Phytomorphol. 16, 211–227 (1966).

  23. Hanaoka, H., Friedman, B.: Paired cisternae in human tumor cells. J. Ultrastruct. Res. 32, 323–333 (1970).

  24. Hepler, P. K., Jackson, W. T.: Microtubules and early stages of cell-plate formation in the endosperm of Haemanthus katherinae Baker. J. Cell Biol. 38, 437–446 (1968).

  25. Hepler, P. K., McIntosh, J., Cleland, S.: Intermicrotubule bridges in mitotic spindle apparatus. J. Cell Biol. 45, 438–444 (1970).

  26. Herth, W., Franke, W. W., VanDerWoude, W. J.: Cytochalasin stops tip growth in plants. Naturwissenschaften 59, 38a (1972).

  27. Hoefert, L. L.: Ultrastructure of Beta pollen. Amer. J. Bot. 56, 363–368 (1969).

  28. Hoefert, L. L.: Fine structure of sperm cells in pollen grains of Beta. Protoplasma (Wien) 68, 237–240 (1969).

  29. Hoffmann-Berling, H.: Adenosintriphosphat als Betriebsstoff von Zellbewegungen. Biochim. biophys. Acta (Amst.) 14, 182–194 (1954).

  30. Hufnagel, L. A.: Cortical ultrastructure of Paramecium aurelia: studies on isolated pellicles. J. Cell Biol. 40, 779–801 (1969).

  31. Kamiya, N.: Motilität des Plasmas. In: Die Zelle, Struktur und Funktion, ed. Metzner, H., S. 373–404. Stuttgart: Wissenschaftliche Verlagsgesellschaft 1971).

  32. Kiermayer, O.: The distribution of microbules in differentiating cells of Micrasterias denticulata. Planta (Berl.) 83, 223–236 (1968).

  33. Komnick, H., Stockem, W., Wohlfahrt-Bottermann, K. E.: Weitreichende fibrilläre Protoplasmadifferenzierungen und ihre Bedeutung für die Protoplasmaströmung. Z. Zellforsch. 109, 420–430 (1970).

  34. Kreutzberg, G. W.: Neuronal dynamics and axonal flow. IV. Blockage of intraaxonal enzyme transport by colchicine. Proc. nat. Acad. Sci. (Wash.) 62, 722–728 (1969).

  35. Krishan, A.: Fine structure of cytochalasine induced multinucleated cells. J. Ultrastruct. Res. 36, 191–204 (1971).

  36. Krishan, A., Hsu, D.: Observations on the association of helical polyribosomes and filaments with vincristine-induced cristals in Earle's L-cell fibroblasts. J. Cell Biol. 43, 553–563 (1969).

  37. Kumegawa, M., Cattoni, M., Rose, G. G.: Electron microscopy of oral cells in vitro. II. Subsurface and intracytoplasmic confronting cisternae in strain KB cells. J. Cell Biol. 36, 443–452 (1968).

  38. Larson, D. A.: Fine-structural changes in the cytoplasm of germinating pollen. Amer. J. Bot. 52, 139–154 (1965).

  39. Lentz, T. L.: The fine structure of differentiating interstitial cells in Hydra. Z. Zellforsch. 67, 547–560 (1965).

  40. Lentz, T. L.: Rhabdite formation in Planaria: The role of microtubules. J. Ultrastruct. Res. 17, 114–126 (1967).

  41. Luykx, P.: Cellular mechanisms of chromosome distribution. Int. Rev. Cytol. 2, 1–171 (1970).

  42. Maitra, S. C., De, D. N.: Role of microtubules in secondary thickening of differentiating xylem element. J. Ultrastruct. Res. 34, 15–22 (1971).

  43. Malaisse-Lagae, F., Greider, M. H., Malaisse, W. J., Lacy, P. E.: The stimulussecretion coupling of glucose-induced insulin release. IV. The effect of vincristine and deuterium oxide on the microtubular system of the pancreatic beta cell. J. Cell Biol. 49, 530–535 (1971).

  44. Malawista, S. E., Sato, H., Creasy, W. A., Bensch, K. G.: Vinblastine produces uniaxial, birefringent crystals in starfish oocytes. Fed. Proc. 28, 875 (1969).

  45. Marantz, R., Shelanski, M. L.: Structure of microtubular crystals induced by vinblastine in vitro. J. Cell Biol. 44, 234–238 (1970).

  46. Mazia, D., Ruby, A.: Dissolution of erythrocyte membranes in water and comparison of the membrane protein with other structural proteins. Proc. nat. Acad. Sci. (Wash.) 61, 1005–1012 (1968).

  47. McIntosh, J. R., Hepler, P. K., Van Wie, D. G.: Model for mitosis. Nature (Lond.) 224, 659–663 (1969).

  48. Mollenhauer, H. H., Morré, D. J.: Golgi apparatus and plant secretion. Ann. Rev. Plant Physiol. 17, 27–46 (1966).

  49. Morré, D. J., VanDerWoude, W. J.: Origin and growth of cell surface components. Develop. Biol., in press.

  50. Mühlethaler, K.: Ultrastructure and formation of plant cell walls. Ann. Rev. Plant Physiol. 18, 1–24 (1967).

  51. Nagai, R., Rebhun, L. I.: Cytoplasmic microfilaments in streaming Nitella cells. J. Ultrastruct. Res. 14, 571–589 (1966).

  52. Newcomb, E. H.: Plant microtubules. Ann. Rev. Plant Physiol. 20, 253–288 (1969).

  53. Northcote, D. H.: Organization of structure, synthesis and transport within the plant during cell division and growth. Symp. Soc. exp. Biol. 25, 51–69 (1971).

  54. Northcote, D. H., Pickett-Heaps, J. D.: A function of the Golgi apparatus in polysaccharide synthesis and transport in the root-cap cells of wheat. Biochem. J. 98, 159–167 (1966).

  55. O'Brien, T. P., Thimann, K. V.: Intracellular fibers in oat coleoptile cells and their possible significance in cytoplasmic streaming. Proc. nat. Acad. Sci. (Wash.) 56, 888–894 (1966).

  56. Olson, L. W., Kochert, G.: Ultrastructure of Volvox carteri. I. The kinetosome. Arch. Mikrobiol. 74, 31–40 (1970).

  57. Pickett-Heaps, J. D.: Ultrastructure and differentiation in Chara sp. I. Vegetative cells. Aust. J. biol. Sci. 20, 539–551 (1967).

  58. Pickett-Heaps, J. D.: Xylem wall deposition. Radioautographic investigations using lignin precursors. Protoplasma (Wien) 65, 181–205 (1968).

  59. Pitelka, D. R.: Fibrillar systems in protozoa. In: Research in protozoology, Tze Tuan Chen, ed., vol. 3, p. 279–388. Oxford: Pergamon Press 1969.

  60. Pollard, T. D., Korn, E. D.: Filaments of Amoeba proteus. II. Binding of heavy meromyosin by thin filaments in motile cytoplasmic extracts. J. Cell Biol. 48, 216–219 (1971).

  61. Rebhun, L. I.: Saltatory particle movements and their relation to the mitotic apparatus. In: The cell in mitosis, ed. by Levine p. L., 67–106. New York-London: Acad. Press 1963.

  62. Robards, A. W.: On the ultrastructure of differentiating secondary xylem in willow. Protoplasma (Wien) 65, 449–464 (1971).

  63. Rosen, W. G.: Ultrastructure and physiology of pollen. Ann. Rev. Plant Physiol. 19, 435–462 (1968).

  64. Sabnis, D. D., Jacobs, W. P.: Cytoplasmic streaming and microtubules in the coenocytic marine alga Caulerpa prolifera. J. Cell Sci. 2, 465–472 (1967).

  65. Schmitt, F. O.: Fibrous proteins neuronal organelles. Proc. nat. Acad. Sci. 60, 1092–1101 (1968).

  66. Simard-Duquesne, N., Coullard, P.: Ameboid movement. I. Reactivation of glycerinated models of ameba proteus with adenosin triphosphate. Exp. Cell Res. 28, 92–98 (1962).

  67. Smith, D. S.: Bridges between vesicles and axoplasmic microtubules. J. Cell Biol. 47, 195a (1970).

  68. Smith, D. S., Järlfors, U., Beranek, R.: The organization of synaptic axoplasm in the lamprey (Petromyzon marinus) central nervous system. J. Cell Biol. 46, 199–219 (1970).

  69. Stadler, J., Franke, W. W.: Colchicine binding protein in chromatin and membranes. Nature (Lond.), in press.

  70. Tilney, L. G.: Origin and continuity of microtubules. In: Origin and continuity of cell organelles, ed. by Reinert, J., Ursprung, H., p. 222–260. Berlin-Heidelberg-New York: Springer 1971.

  71. VanDerWoude, W. J., Morré, D. J., Bracker, C. E.: Isolation and characterization of secretory vesicles in germinated pollen of Lilium longiflorum. J. Cell Sci. 8, 331–351 (1971).

  72. Warner, F. D.: New observations on flagellar fine structure. The relationship between matrix structure and the microtubule component of the axoneme. J. Cell Biol. 47, 159–182 (1970).

  73. Weihing, R. R., Korn, E. D.: Acanthamoeba actin. Isolation and properties. Biochemistry 10, 590–600 (1971).

  74. Wessels, N. K., Spooner, B. S., Ash, J. F., Bradley, M. O., Luduena, M. A., Taylor, E. L., Wrenn, J. T., Yamada, K. M.: Microfilaments in cellular and developmental processes. Contractile microfilament machinery of many cell types is reversibly inhibited by cytochalasin B. Science 171, 135–140 (1971).

  75. Wilson, L., Bryan, J., Ruby, A., Mazia, D.: Precipitation of proteins by vinblastine and calcium ions. Proc. nat. Acad. Sci. (Wash.) 66, 807–814 (1970).

  76. Wooley, D. E.: An actin-like protein from amoeba of Dictyostelium discoideum. Fed. Proc. 29, 667 A (1970).

  77. Yamada, K. M., Spooner, B. S., Wessels, N. K.: Ultrastructure and function of growth cones and axons of cultured nerve cells. J. Cell Biol. 49, 614–635 (1971).

Download references

Author information

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Franke, W.W., Herth, W., VanDerWoude, W.J. et al. Tubular and filamentous structures in pollen tubes: Possible involvement as guide elements in protoplasmic streaming and vectorial migration of secretory vesicles. Planta 105, 317–341 (1972). https://doi.org/10.1007/BF00386769

Download citation

Keywords

  • Pollen Tube
  • Colchicine
  • Vinblastine
  • Cytochalasin
  • Secretory Vesicle