Protoplasma

, Volume 157, Issue 1–3, pp 52–63 | Cite as

The microtubule cytoskeleton in developing cysts of the green algaAcetabularia: Involvement in cell wall differentiation

  • D. Menzel
  • Christine Elsner-Menzel
Article

Summary

Cysts of the green algaAcetabularia develop a unique lid structure to enable the release of gametes. This lid is separated from the rest of the thick cellulose cell wall by a circular fault line formed within the fibrillar texture of the wall. By immunofluorescence microscopy, we show that, prior to the first division of the single cyst nucleus, the radially symmetrical, perinuclear microtubule system which is a remnant carried over from previous developmental stages of cyst morphogenesis transforms into a circular microtubule band (CMB) around the nucleus. This band consisting of only a few bundled microtubules beneath the plasma membrane encircles the cyst nucleus at a distance of 75 to 100μm. In a previous fine structural study, a lid-forming apparatus (LFA) was described as a circular band of rod-like structures in the plane of the plasma membrane, demarcating the contour of the future lid. Both the CMB and the LFA are superimposed on the rim of the lid. We therefore propose that the microtubule band is a component of the LFA identical with the rod-like structures. Formation of the CMB and, hence, lid formation are blocked by the microtubule-specific herbicide Oryzalin but not by the actin filament-disrupting inhibitor cytochalasin D. Upon recovery from Oryzalin treatment, the nuclei but not the prospective sites of the CMBs serve as nucleation centers, indicating that the CMB is not formed by a pre-existing template in the plasma membrane. This suggests that the dynamic behavior of the microtubules within the perinuclear microtubule cytoskeleton gives rise to the CMB. Since the stage of CMB assembly marks the beginning of cell wall formation, it is proposed that the CMB determines the position of the lid by spatially controlling cell wall deposition. On the basis of current hypotheses, two scenarios for the role of the LFA/CMB in lid formation are discussed.

Keywords

Acetabularia Chlorophyceae Cytoskeleton Cell wall Dasycladaceae Immunofluorescence Microtubules Morphogenesis 

Abbreviations

CMB

circular microtubule band

EGTA

ethylene glycol bis-(β-aminoethyl ether) N,N,N′,N′-tetraacetic acid

FITC

fluorescein isothiocyanate

LFA

lid-forming-apparatus

MAP

microtubule-associated protein

MT

microtubule

MTOC

microtubuleorganizing center

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References

  1. Bakhuizen R, van Spronsen PC, Sluiman-den Hertog AJ, Venverloo CJ, Goosen-DeRoo DL (1985) Nuclear envelope radiating microtubules in plant cells during interphase mitosis transition. Protoplasma 128: 43–51Google Scholar
  2. Bonotto S (1988) Recent progress in research onAcetabularia and related Dasycladales. Prog Phycol Res 6: 59–235Google Scholar
  3. Brown RC, Lemmon BE (1988) Cytokinesis occurs at boundaries of domains delimited by nuclear-based microtubules in sporophytes ofConocephalum conicum (Bryophyta). Cell Motil Cytoskeleton 11: 139–146Google Scholar
  4. — — (1988) Microtubules associated with simultaneous cytokinesis of coenocytic microsporocytes. Amer J Bot 75: 1848–1856Google Scholar
  5. — — (1989) Minispindles and cytoplasmic domains in microsporogenesis of orchids. Protoplasma 148: 26–32Google Scholar
  6. Elinson RP, Rowning B (1988) A transient array of parallel microtubules in frog eggs. Potential tracks for a cytoplasmic rotation that specifies the dorso-ventral axis. Dev Biol 128: 185–197Google Scholar
  7. Godward MBE, Beth K, Pacey J (1979) Nuclear division in the cyst, and white spot nuclei preceding cyst formation, inAcetabularia wettsteinii. Protoplasma 101: 37–46Google Scholar
  8. Harris P, Osborn M, Weber K (1980) A spiral array of microtubules in the fertilized sea urchin egg cortex examined by indirect immunofluorescence and electron microscopy. Exp Cell Res 126: 227–236Google Scholar
  9. Heath IB (1974) A unifying hypothesis for the role of membrane bound enzyme complexes and microtubules in plant cell wall synthesis. J Theor Biol 48: 445–449Google Scholar
  10. —, Seagull RW (1982) Oriented cellulose fibrils and the cytoskeleton: a critical comparison of models. In: Lloyd CW (ed) The cytoskeleton in plant growth and development. Academic Press, LondonGoogle Scholar
  11. Herth W (1985) Plant cell wall formation. In: Robards AW (ed) Botanical microscopy 1985. Oxford University Press, OxfordGoogle Scholar
  12. Koop H-U (1975) Germination of cysts inAcetabularia mediterranea. Protoplasma 84: 137–146Google Scholar
  13. McNaughton EE, Goff L (1988) Nuclear spatial organization in coenocytic green algae. Do microtubules establish cytoplasmic domains. Am Zool 28: 66Google Scholar
  14. Mizuta S, Okuda K (1987)Boodlea cell wall microfibril orientation unrelated to cortical microtubule arrangement. Bot Gaz 148: 297–307Google Scholar
  15. Menzel D (1986) Visualization of cytoskeletal changes through the life cycle inAcetabularia. Protoplasma 134: 30–42Google Scholar
  16. — (1988) Perturbation of cytoskeletal assemblies in cyst domain morphogenesis in the green algaAcetabularia. Eur J Cell Biol 46: 217–226Google Scholar
  17. —, Elsner-Menzel C (1989) Maintenance and dynamic of cytoplasmic organization controlled by cytoskeletal assemblies inAcetabularia. In: Stein J, Coleman AW, Goff LJ (eds) Algae as experimental systems in cell biology. AR Liss, New York, pp 71–92Google Scholar
  18. — — (1990) Cytoskeletal dynamics in the reproductive cycle ofAcetabularia (Dasycladaceae, Chlorophyceae) — cyst morphogenesis and delayed cytokinesis. In: Wiessner W, Robinson DG, Starr R (eds) Recent advances in experimental phycology. Springer, Berlin Heidelberg New York Tokyo (in press)Google Scholar
  19. Montezinos D (1982) The role of the plasma membrane in cellulose microfibril assembly. In: Lloyd CW (ed) The cytoskeleton in plant growth and development. Academic Press, LondonGoogle Scholar
  20. Morejohn LC, Bureau TE, Mole-Bajer L, Bajer AS, Fosket DE (1987) Oryzalin, a dinitroaniline herbicide, binds to plant tubulin and inhibits microtubule polymerization in vitro. Planta 172: 252–264Google Scholar
  21. Neuhaus-Url G, Schweiger H-G (1984) The lid forming apparatus in cysts of the green algaAcetabularia mediterranea. Protoplasma 122: 120–124Google Scholar
  22. Nisizawa K, Kuroda K, Tomita Y, Shimahara H (1974) Main cell wall constituents of the cysts ofAcetabularia. Botanica Marina 17: 16–19Google Scholar
  23. Olmsted JB (1986) Microtubule-associated proteins. Annu Rev Cell Biol 2: 421–457Google Scholar
  24. Puiseux-Dao S (1970)Acetabularia and cell biology. Logos Press, LondonGoogle Scholar
  25. Seagull RW (1989) The plant cytoskeleton. Crit Rev Plant Sci 8: 131–167Google Scholar
  26. Shihira-Ishikawa I (1987) Cytoskeleton in cell morphogenesis of the coenocytic green algaValonia ventricosa. I. Two microtubule systems and their role in positioning of chloroplasts and nuclei. Jap J Phycol 35: 251–258Google Scholar
  27. Traas JA, Derksen J (1989) Microtubules and cellulose microfibrils in plant cells. Simultaneous demonstration in dry cleave preparations. Eur J Cell Biol 48: 159–164Google Scholar
  28. Vallee RB, Bloom GS, Theurkauf WE (1984) Microtubule-associated proteins: subunits of the cytomatrix. J Cell Biol 99: 38 s-44 sGoogle Scholar
  29. Van Lammeren AAM (1988) Structure and function of the microtubular cytoskeleton during endosperm development in wheat: an immunofluorescence study. Protoplasma 146: 18–27Google Scholar
  30. —, Keijzer CJ, Willemse MTM, Kieft H (1985) Structure and function of the microtubular cytoskeleton during pollen development inGasteria verrucosa (Mill.) H. Duval. Planta 165: 1–11Google Scholar
  31. Woodcock CLF, Miller GJ (1973) Ultrastructural features of the life cycle ofAcetabularia mediterranea. II. Events associated with the division of the primary nucleus and the formation of cysts. Protoplasma 77: 331–341Google Scholar
  32. — — (1973) Ultrastructural features of the life cycle ofAcetabularia mediterranea. I. Gametogenesis. Protoplasma 77: 313–329Google Scholar
  33. Zimmer B, Werz G (1980) Concanavalin A affects polysaccharide wall formation and mitotic activity inPolyphysa (Acetabularia) cliftonii protoplasts. Exp Cell Res 126: 299–310Google Scholar
  34. — — (1981) Cytoskeletal elements and their involvement inPolyphysa (Acetabularia) protoplast differentiation. Cytoskeleton modifiers and concanavalin A-mediated effects. Exptl Cell Res 131: 105–113Google Scholar

Copyright information

© Springer-Verlag 1990

Authors and Affiliations

  • D. Menzel
    • 1
  • Christine Elsner-Menzel
    • 1
  1. 1.Max-Planck-Institut für ZellbiologieLadenburgFederal Republic of Germany

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