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Endoplasmic microtubules and nucleus-associated actin rings inNitella internodal cells

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Summary

The view that microtubules are confined to the cortex of characean internodal cells has been disproved by the discovery of microtubules in the endoplasm ofNitella by immunofluorescence. By cutting open cells so that they could be viewed from the inside out, clear observations of nuclei, microtubules, and actin-containing elements (preserved by glutaraldehyde) in the endoplasm have been made. Microtubules were found in the subcortical layer, aligned and possibly associated with the prominent actin bundles. The abundant nuclei, located in the streaming endoplasm were also examined and a system of actin rings—possibly involved in nuclear rotation—was discovered. Some nuclei displayed peripheral microtubules but no spindle-like structures were observed. Contrary to earlier published findings, we have demonstrated that microtubule disassembly significantly impedes the cell's ability to recover from cytochalasin-induced streaming arrest, indicating that microtubules or microtubule proteins can in some still unknown way influence cytoplasmic streaming.

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Abbreviations

BSA:

bovine serum albumin

DMSO:

dimethylsulfoxide

FITC:

fluorescein isothiocyanate

PBS:

phosphate buffered saline

PE:

phycoerythrin

SA:

streptavidin

References

  • Bradley MO (1973) Microfilaments and cytoplasmic streaming: inhibition of streaming by cytochalasin. J Cell Sci 12: 327–343

    PubMed  CAS  Google Scholar 

  • Clayton L, Lloyd CW (1985) Actin organisation during the cell cycle in meristematic plant cells. Actin is present in the cytokinetic phragmoplast. Exp Cell Res 156: 231–238

    Article  PubMed  CAS  Google Scholar 

  • Derksen J, Traas J, Oostendorp T (1986) Distribution of actin filaments in differentiating cells ofEquisetum hyemale root tips. Plant Sci 43: 77–81

    Article  CAS  Google Scholar 

  • Green PB (1954) The spiral growth pattern of the cell wall inNitella axillaris. Amer J Bot 41: 403–409

    Article  Google Scholar 

  • — (1962) Mechanisms for plant cellular morphogenesis. Science 138: 1404–1405

    Article  Google Scholar 

  • — (1964) Cinematic observations on the growth and division of chloroplasts inNitella. Amer J Bot 51: 334–342

    Article  Google Scholar 

  • Grolig F, Williamson RE, Parke J, Miller C, Anderton BH (1988) Myosin and Ca2+-sensitive streaming in the algaChara: detection of two polypeptides reacting with a monoclonal anti-myosin and their localisation in the streaming endoplasm. Eur J Cell Biol 47: 22–31

    PubMed  CAS  Google Scholar 

  • Gunning BES, Wick SM (1985) Preprophase bands, phragmoplasts and spatial control of cytokinesis. J Cell Sci [Suppl] 2: 157–179

    CAS  Google Scholar 

  • Harmon AC, McCurdy DW (1990) Calcium-dependent protein kinase and its possible role in the regulation of the cytoskeleton. Curr Top Plant Biochem Physiol 9: 119–128

    CAS  Google Scholar 

  • Jarosch R (1956a) Aktiv bewegungsfähige Plasmaelemente und Chloroplastenrotation beiCharaceen. Anz Österr Akad Wiss 6: 58–60

    Google Scholar 

  • — (1965b) Plasmaströmung und Chloroplastenrotation beiCharaceen. Phyton (Buenos Aires), 6: 87–108

    Google Scholar 

  • — (1957) Zur Mechanik der Protoplasmafibrillenbewegung. Biochim Biophys Acta 25: 204–205

    Article  PubMed  CAS  Google Scholar 

  • — (1958) Die Protoplasmafibrillen derCharaceen. Protoplasma 50: 93–108

    Article  Google Scholar 

  • Kachar B, Reese TS (1988) The mechanism of cytoplasmic streaming in characean algal cells: sliding of endoplasmic reticulum along actin filaments. J Cell Biol 106: 1545–1552

    Article  PubMed  CAS  Google Scholar 

  • Kakimoto T, Shibaoka H (1987) Actin filaments and microtubules in the preprophase band and phragmoplast of tobacco cells. Protoplasma 140: 151–156

    Article  Google Scholar 

  • —— (1987) A new method for preservation of actin filaments in higher plant cells. Cell Physiol 28: 1581–1585

    CAS  Google Scholar 

  • Kamiya N (1962) Protoplasmic streaming. In: Bünning E (ed) Physiologie der Bewegungen. Bewegungen durch Einflüsse der Temperatur, Schwerkraft, chemischer Faktoren und aus inneren Ursachen. Springer, Berlin Göttingen Heidelberg, pp 979–1035 [Ruhland W (ed) Handbuch der Pflanzenphysiologie, vol 17, part 2]

    Google Scholar 

  • — (1986) Cytoplasmic streaming in giant algal cells: a historical survey of experimental approaches. Bot Mag Tokyo 99: 441–467

    Article  CAS  Google Scholar 

  • Kobayashi H, Fukuda H, Shibaoka H (1987) Reorganization of actin filaments associated with the differentiation of tracheary elements inZinnia mesophyll cells. Protoplasma 138: 69–71

    Article  Google Scholar 

  • Kuroda K (1964) The behaviour of naked cytoplasmic drops isolated from plant cells. In: Allen RD, Kamiya N (eds) Primitive motile systems in cell biology: Academic Press, New York, pp 31–41

    Google Scholar 

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

    Article  Google Scholar 

  • Laloue M, Courtois D, Manigault P (1980) Convenient and rapid fluorescent staining of plant cell nuclei with “33258” Hoechst. Plant Sci Lett 17: 175–179

    Article  CAS  Google Scholar 

  • Lessard JL (1988) Two monoclonal antibodies to actin: one muscle selective and one generally reactive. Cell Motil Cytoskeleton 10: 349–362

    Article  PubMed  CAS  Google Scholar 

  • Ludwig SR, Oppenheimer DG, Silflow CD, Snustad DP (1987) Characterization of the α-tubulin gene family ofArabidopsis thaliana. Proc Natl Acad Sci USA 84: 5833–5837

    Article  PubMed  CAS  Google Scholar 

  • McLean B, Juniper BE (1986) The plasma membrane of youngChara internodal cells revealed by rapid freezing. Planta 169: 153–161

    Article  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Nagai R, Rebhun LI (1966) Cytoplasmic microfilaments in streamingNitella cells. J Ultrastruct Res 14: 571–589

    Article  PubMed  CAS  Google Scholar 

  • Palevitz BA (1987) Actin in the preprophase band ofAllium cepa. J Cell Biol 104: 1515–1519

    Article  PubMed  CAS  Google Scholar 

  • Parke J, Miller C, Anderton BH (1986) Higher plant myosin heavy-chain identified using a monoclonal antibody. Eur J Cell Biol 41: 9–13

    CAS  Google Scholar 

  • Pickett-Heaps JD (1967) Ultrastructure and differentiation inChara sp. I. Vegetative cells. Aust J Biol Sci 20: 539–551

    Google Scholar 

  • Pollard TD, Selden SC, Maupin P (1984) Interaction of actin microfilaments with microtubules. J Cell Biol 99: 33s-37s

    Article  PubMed  CAS  Google Scholar 

  • Putnam-Evans C, Harmon A, Palevitz B, Fechheimer M, Cormier M (1988) Calcium-dependent protein kinase is localized with F-actin in plant cells. Cell Motil Cytoskeleton 12: 12–22

    Article  Google Scholar 

  • Richmond PA (1983) Patterns of cellulose microfibril deposition and rearrangement inNitella: in vivo analysis by a birefringence index. J Appl Polymer Sci Appl Polymer Symp 37: 107–122

    CAS  Google Scholar 

  • Schroeder M, Wehland J, Weber K (1985) Immunofluorescence microscopy of microtubules in plant cells; stabilization by dimethylsulfoxide. Eur J Cell Biol 38: 211–218

    Google Scholar 

  • Seagull RW, Falconer MM, Weerdenburg CA (1987) Microfilaments: dynamic arrays in higher plant cells. J Cell Biol 104: 995–1004

    Article  PubMed  CAS  Google Scholar 

  • Segaar PJ, Lokhorst GM (1988) Dynamics of the microtubular cytoskeleton in the green algaAphanochaete magna (Chlorophyta). I. Late mitotic stages and the origin and development of the phycoplast. Protoplasma 142: 176–187

    Article  Google Scholar 

  • Simmonds D, Setterfield G, Brown DL (1983) Organization of microtubules in dividing and elongating cells ofVicia hajastana Grossh. in suspension culture. Eur J Cell Biol 32: 59–66

    PubMed  CAS  Google Scholar 

  • Tewinkel M, Volkmann D (1987) Observations of dividing plastids in the protonema of the mossFunaria hygrometrica Sibth. Arrangement of microtubules and filaments. Planta 172: 309–320

    Article  Google Scholar 

  • Tiwari SC, Polito VS (1988) Spatial and temporal organization of actin during hydration, activation, and germination of pollen inPyrus communis L.: a population study. Protoplasma 147: 5–15

    Article  Google Scholar 

  • Traas JA, Doonan JH, Rawlins DJ, Shaw PJ, Watts J, Lloyd CW (1987) An actin network is present in the cytoplasm throughout the cell cycle of carrot cells and associates with the nucleus. J Cell Biol 105: 387–395

    Article  PubMed  CAS  Google Scholar 

  • Wasteneys GO, Williamson RE (1987) Microtubule orientation in developing internodal cells ofNitella: a quantitative analysis. Eur J Cell Biol 43: 14–22

    Google Scholar 

  • —— (1989) Reassembly of microtubules inNitella tasmanica: assembly of cortical microtubules in branching clusters and its relevance to steady state microtubule assembly. J Cell Sci 93: 705–714

    Google Scholar 

  • —, Jablonsky PP, Williamson RE (1989) Assembly of purified brain tubulin at cortical and endoplasmic sites in perfused internodal cells of the algaNitella tasmanica. Cell Biol Int Rep 13: 513–528

    Article  CAS  Google Scholar 

  • Wick SM, 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  PubMed  CAS  Google Scholar 

  • Williamson RE (1972) A light microscope study of the action of cytochalasin B on the cells and isolated cytoplasm of theCharaceae. J Cell Sci 10: 811–819

    PubMed  CAS  Google Scholar 

  • —, Hurley UA, Perkin JL (1984) Regeneration of actin bundles inChara: polarized growth and orientation by endoplasmic flow. Eur J Cell Biol 34: 221–228

    PubMed  CAS  Google Scholar 

  • —, Perkin JL, McCurdy DW, Craig S, Hurley UA (1986) Production and use of monoclonal antibodies to study the cytoskeleton and other components of the cortical cytoplasm ofChara. Eur J Cell Biol 41: 1–8

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

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Wasteneys, G.O., Williamson, R.E. Endoplasmic microtubules and nucleus-associated actin rings inNitella internodal cells. Protoplasma 162, 86–98 (1991). https://doi.org/10.1007/BF02562552

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  • DOI: https://doi.org/10.1007/BF02562552

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