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The role of microtubules in establishing nuclear spatial patterns in multinucleate green algae

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In uninucleate cells, cytokinesis follows karyokinesis, thereby reestablishing a specific nucleus-to-cytoplasm ratio. In multinucleate cells, cytokinesis is absent or infrequent; no plasmalemma boundary defines the cytoplasmic territory of an individual nucleus. Several genera of large multinucleate green algae were examined with epifluorescence light microscopy to determine whether the patterns of cytoplasmic organization establish nuclear cytoplasmic domains. Randomly spaced nuclei, singular mitotic events and cytoplasmic streaming characterize the organization of two genera,Derbesia andBryopsis (Caulerpales). The cells ofValonia, Valoniopsis, Boergesenia, Ventricaria (Siphonocladales), andHydrodictyon (Chlorococcales) display regularly spaced nuclei which undergo synchronous divisions in a stationary cytoplasm. In the cytoplasm of genera with regularly spaced nuclei, microtubules radiate from all nuclei in late telophase-early interphase. These internuclear microtubule arrays are not found in algal genera with randomly spaced nuclei. It is hypothesized that these microtubule arrays play a role in establishing the cytoplasmic domain of each nucleus in genera with regularly spaced nuclei. Loss of microtubule arrays during the events of mitosis correlated positively with the increasing randomization of nuclear patterns in algae grown in microtubule inhibitors. Cytoplasmic domains were maintained when cells were grown in the same media in the dark. This suggests that, after a round of division, regular nuclear spacing in certain multinucleate algae is reestablished by internuclear microtubule arrays, which are not, however, required to maintain spacing during interphase.

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References

  • Bajer AJ, Molé-Bajer J (1986) Drugs with colchicine-like effects that specifically disassemble plant but not animal microtubules. In: Soifer D (ed) Dynamic aspects of microtubule biology. Ann NY Acad Sci 466: 767–781

  • Bakhuizen R, van Spronsen PC, Sluiman-den Hertog FAJ, Venverloo CJ, Goosen-de Roo L (1985) Nuclear envelope radiating microtubules in plant cells during interphase mitosis transition. Protoplasma 128: 43–51

    Google Scholar 

  • Bold HC and Wynne MJ (1985) Introduction to the algae. Prentice-Hall, Englewood Cliffs, NJ

    Google Scholar 

  • Brown RC, Lemmon BE (1988) Cytokinesis occurs at boundaries of domains delimited by nuclear-based microtubules in sporocytes ofConocephalum conicum (Bryophyta). Cell Mot Cytoskeleton 11: 139–146

    Google Scholar 

  • — — (1989) Minispindles and cytoplasmic domains in microsporogenesis of orchids. Protoplasma 148: 26–132

    Google Scholar 

  • Caron JM, Jones AL, Kirschner MW (1985) Autoregulation of tubulin synthesis in hepatocytes and fibroblasts. J Cell Biol 101: 1763–1772

    Google Scholar 

  • Clark PJ, Evans FC (1954) Distance to nearest neighbor as a measure of spatial relationships in populations. Ecology 35: 445–453

    Google Scholar 

  • Clutterbuck AJ (1969) Cell volume per nucleus in haploid and diploid strains ofAspergillus nidulans. J Gen Microbiol 55: 291–299

    Google Scholar 

  • Collis PS, Weeks DP (1978) Selective inhibition of tubulin synthesis by amiprophos-methyl during flagellar regeneration inChlamydomonas reinhardii. Science 202: 440–442

    Google Scholar 

  • Cyr RJ (1986) Expression of tubulin proteins in higher plants during growth and development. PhD dissertation University of California, Irvine, CA

    Google Scholar 

  • —, Tochi L, Fosket DE (1984) Immunological studies on plant tubulin isolated from divers cell lines. Protoplasma 134: 30–42

    Google Scholar 

  • Doonan JH, Cove DJ, Lloyd CW (1985) Immunofluorescence microscopy of microtubules in intact cell lineages of the moss,Physcomitrella patens. J Cell Sci 75: 131–147

    Google Scholar 

  • Falconer MM, Seagull RW (1987) Amiprophos-methyl (APM): A rapid, reversible, anti-microtubule agent for plant cell cultures. Protoplasma 136: 118–124

    Google Scholar 

  • Fantes PA, Grant WD, Pritchard RH, Sudbery PE, Wheals AE (1975) The regulation of cell size and the control of mitosis. J Theoret Biol 50: 213–244

    Google Scholar 

  • Giloh H, Sedat JW (1982) Fluorescence microscopy: reduced photobleaching of rhodamine and fluorescein protein conjugates by n-propyl gallate. Science 217: 1252–1255

    Google Scholar 

  • Goff LJ, Coleman AW (1984) Elucidation of fertilization and development in a red alga by quantitative DNA microspectrofluorometry. Dev Biol 102: 173–194

    Google Scholar 

  • — (1987) The solution to the cytological paradox of isomorphy. J Cell Biol 104: 739–748

    Google Scholar 

  • Gunning BES, Hardham AR (1982) Microtubules. Annu Rev Plant Physiol 33: 651–698

    Google Scholar 

  • Hartmann M (1928) Über experimentelle Unsterblichkeit von Protozoen-Individuen. Zoo Jb 45: 973–987

    Google Scholar 

  • Hori T, Enomoto S (1978) Electron microscope observations on the nuclear division inValonia ventricosa (Chlorophyceae, Siphonocladales). Phycologia 17: 33–42

    Google Scholar 

  • Hudson PR, Waaland JR (1974) Ultrastructure of mitosis and cytokinesis in the multinucleate green algaAcrosiphonia. J Cell Biol 62: 274–294

    Google Scholar 

  • Johnson RT, Rao PN (1971) Nucleo-cytoplasmic interactions in the achievement of nuclear synchrony in DNA synthesis and mitosis in multinucleate cells. Biol Rev 46: 97–155

    Google Scholar 

  • Kilmartin JV, Adams AEM (1984) Structural rearrangements of tubulin and actin during the cell cycle of the yeastSaccharomyces. J Cell Biol 98: 922–933

    Google Scholar 

  • Kiermayer O, Fedtke C (1977) Strong anti-microtubule action of amiprophos-methyl (APM) inMicrasterias. Protoplasma 92: 163–166

    Google Scholar 

  • La Claire II JW (1987) Microtubule cytoskeleton in intact and wounded coenocytic green algae. Planta 171: 30–42

    Google Scholar 

  • Laskey RA, Fairman MP, Blow JJ (1989) S phase of the cell cycle. Science 246: 609–614

    Google Scholar 

  • Lewin J (1966) Silicon metabolism in diatoms. V. Germanium dioxide, a specific inhibitor of diatom growth. Phycologia 6: 1–12

    Google Scholar 

  • Maclachlan J (1973) Growth media-marine. In: Stein JR (ed) Handbook of phycological methods. Culture methods and growth measurements. Cambridge University Press, London, pp 25–51

    Google Scholar 

  • Marchant HJ, Pickett-Heaps JD (1970) Ultrastructure and differentiation ofHydrodictyon reticulatum I. Mitosis in the coenobium. Aust J Biol Sci 23: 1173–1186

    Google Scholar 

  • Mazia D (1961) Mitosis and the physiology of cell division. In: Brachet J, Mirsky AE (eds) The cell, vol 3. Academic Press, New York, pp 77–412

    Google Scholar 

  • Menzel D, Schliwa M (1986 a) Motility in the siphonous green algaBryopsis. I. Spatial organization of the cytoskeleton and organelle movements. Eur J Cell Biol 40: 275–285

    Google Scholar 

  • — — (1986 b) Motility in the siphonous green algaBryopsis. II. Chloroplast movement requires organized arrays of both microtubules and actin filaments. Eur J Cell Biol 40: 286–295

    Google Scholar 

  • Mizukami M, Wada S (1983) Morphological anomalies induced by antimicrotubule agents inBryopsis plumosa. Protoplasma 114: 151–162

    Google Scholar 

  • Morejohn LC, Fosket DE (1984) Inhibition of plant microtubule polymerization in vitro by the phosphoric amide herbicide amiprophos-methyl. Science 224: 874–976

    Google Scholar 

  • Murray AW, Kirschner MW (1989) Dominoes and clocks: the union of two views of the cell cycle. Science 246: 614–621

    Google Scholar 

  • Olsen JL, West JA (1988)Ventricaria (Siphonocladales-Cladophorales complex,Chlorophyta), a new genus forValonia ventricosa. Phycologia 27: 103–108

    Google Scholar 

  • Pardee AB (1989) G1 events and regulation of cell proliferation. Science 246: 603–608

    Google Scholar 

  • Shihira-Ishikawa I (1987) Cytoskeleton in cell morphogenesis of the coenocytic green algaValonia ventricosa I. Two microtubule systems and their roles in positioning of chloroplasts and nuclei. Jap J Phycol (Sorui) 35: 251–258

    Google Scholar 

  • Starr RC (1978) The Culture Collection at the University of Texas at Austin. J Phycol [Suppl] 14: 92–96

    Google Scholar 

  • Staves M, La Claire III JW (1985) Nuclear synchrony inValonia macrophysa (Chlorophyta): light microscopy and flow cytometry. J Phycol 21: 68–71

    Google Scholar 

  • Warn RM, Warn A (1986) Microtubule arrays present during the syncytial and cellular blastoderm stages of the earlyDrosophila embryo. Exp Cell Res 163: 201–210

    Google Scholar 

  • Wick SM, Duniec J (1984) Immunofluorescence microscopy of tubulin and microtubule arrays in plant cells. II. Transition between the pre-prophase band and the mitotic spindle. Protoplasma 122: 45–55

    Google Scholar 

  • Woodcock CLF (1971) The anchoring of nuclei in cytoplasmic microtubules inAcetabularia. J Cell Sci 8: 611–621

    Google Scholar 

  • Wordeman L, McDonald KL, Cande WZ (1986) The distribution of cytoplasmic microtubules throughout the cell cycle of the centric diatomStephanopyxis turris: their role in nuclear migration and positioning the mitotic spindle during cytokinesis. J Cell Biol 102: 1688–1698

    Google Scholar 

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  1. Department of Biology and Institute of Marine Studies, University of California, 95064, Santa Cruz, CA, USA

    Eugenia E. McNaughton & Lynda J. Goff

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  1. Eugenia E. McNaughton
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  2. Lynda J. Goff
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Dedicated to the memory of Professor Oswald Kiermayer

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McNaughton, E.E., Goff, L.J. The role of microtubules in establishing nuclear spatial patterns in multinucleate green algae. Protoplasma 157, 19–37 (1990). https://doi.org/10.1007/BF01322636

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  • DOI: https://doi.org/10.1007/BF01322636

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