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Microtubule and actin filament organization during acentral divisions in potato suspension culture cells

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Summary

Microtubule and filamentous(F)-actin organization in the potato suspension culture line HH260 was studied by fluorescence microscopy in double-labelled cells. During interphase, microtubules and F-actin were randomly arrayed in isodiametric cells but were aligned transversely to the direction of growth in elongated cells. Microtubules and F-actin coaligned in preprophase bands which were, however, comparatively rare and diffuse. Interestingly, more than half of the cells in telophase contained phragmoplasts that were either horseshoe-shaped or straight, instead of being round. We traced the cause of this difference to preprophase, where misplaced nuclear localization away from the central axis of cells may give rise to acentrally placed spindles and, subsequently, to acentrally placed phragmoplasts and cell plates. Further, we hypothesize that it is the uneven fusion of the expanding cell plates with the parent plasma membrane, and the accompanying depolymerization of those parts of the phragmoplasts, that gives the incomplete phragmoplasts observed.

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Abbreviations

DAPI:

4′,6-diamidino-2-phenylindole

MBS:

3-maleimidobenzoyl-N-hydroxy-succinimidester

PMSF:

phenyl-methylsulfonyl fluoride

SB:

stabilization buffer

References

  • Baskin TI, Cande WZ (1990) The structure and function of the mitotic spindle in flowering plants. Annu Rev Plant Physiol 41: 277–315

    Google Scholar 

  • Binding H, Nehls R, Schieder O, Sopory SK, Wenzel G (1978) Regeneration of mesophyll protoplasts isolated from dihaploid clones ofSolanum tuberosum. Physiol Plant 43: 52–54

    Google Scholar 

  • Cleary AL (1995) F-actin redistributions at the dividing site in livingTradescantia stomatal complexes as revealed by microinjection of rhodamine-phalloidin. Protoplasma 185: 152–165

    Google Scholar 

  • —, Hardham AR (1989) Microtubule organization during development of stomatal complexes inLilium rigidum. Protoplasma 149: 67–81

    Google Scholar 

  • —, Mathesius U (1996) Rearrangements of F-actin during stomato-genesis visualized by confocal microscopy in fixed and permeabilizedTradescantia leaf epidermis. Bot Acta 109: 15–24

    Google Scholar 

  • Fowke LC, Gamborg OL (1980) Applications of protoplasts to the study of plant cells. Int Rev Cytol 68: 9–51

    Google Scholar 

  • Gilissen LJW, Sree Ramulu K, Flipse E, Meinen E, Stiekema WJ (1991) Transformation of diploid potato genotypes throughAgrobacterium vectors and expression of T-DNA markers in root clones, regenerated plants and suspension cells. Acta Bot Neerl 40: 53–61

    Google Scholar 

  • Gorst J, Wernicke W, Gunning BES (1986) Is the preprophase band of microtubules a marker of organization in suspension cultures? Protoplasma 134: 130–140

    Google Scholar 

  • Gunning BES (1982) The cytokinetic apparatus: its development and spatial regulation. In: Lloyd CW (ed) The cytoskeleton in plant growth and development. Academic Press, London, pp 229–292

    Google Scholar 

  • Holy TE, Dogterom M, Yurke B, Leibler S (1997) Assembly and positioning of microtubule asters in microfabricated chambers. Proc Natl Acad Sci USA 94: 6228–6231

    Google Scholar 

  • Kakimoto T, Shibaoka H (1987a) A new method for preservation of actin filaments in higher plant cells. Plant Cell Physiol 28: 1581–1585

    Google Scholar 

  • — — (1987b) Actin filaments and microtubules in the preprophase band and phragmoplast of tobacco cells. Protoplasma 140: 151–156

    Google Scholar 

  • — — (1988) Cytoskeletal ultrastructure of phragmoplast-nuclei complexes isolated from cultured tobacco cells. Protoplasma Suppl 2: 95–103

    Google Scholar 

  • Katsuta J, Shibaoka H (1988) The roles of the cytoskeleton and the cell wall in nuclear positioning in tobacco BY-2 cells. Plant Cell Physiol 29: 403–413

    Google Scholar 

  • —, Hashiguchi Y, Shibaoka H (1990) The role of the cytoskeleton in positioning of the nucleus in premitotic tobacco BY-2 cells. J Cell Sci 95: 413–422

    Google Scholar 

  • Lambert A (1995) Microtubule-organizing centres in higher plants: evolving concepts. Bot Acta 108: 535–537

    Google Scholar 

  • Lehrer SS (1981) Damage to actin filaments by glutaraldehyde: protection by tropomyosin. J Cell Biol 90: 459–466

    Google Scholar 

  • Lloyd CW, Slabas AR, Powell AJ, Lowe SB (1980) Microtubules, protoplasts and plant cell shape. Planta 147: 500–506

    Google Scholar 

  • Mahlberg PG, Turner FR, Walkinshaw C, Venketeswaran S, Mehrota B (1975) Observations of incomplete cytokinesis in callus cells. Bot Gaz 136: 189–195

    Google Scholar 

  • Marc J (1997) Microtubule-organizing centres in plants. Trends Plant Sci 2: 223–230

    Google Scholar 

  • McCurdy DW, Gunning BES (1990) Reorganization of cortical actin microfilaments and microtubules at preprophase and mitosis in wheat root-tip cells: a double label immunofluorescence study. Cell Motil Cytoskeleton 15: 76–87

    Google Scholar 

  • Molé-Bajer J, Bajer AS, Inoué S (1988) Three-dimensional localization and redistribution of F-actin in higher plant mitosis and cell plate formation. Cell Motil Cytoskeleton 10: 217–228

    Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15: 473–497

    Google Scholar 

  • Nagata T, Okada K, Takebe I, Matsui C (1981) Delivery of tobacco mosaic virus RNA into plant protoplasts mediated by reverse-phase evaporation vesicles (liposomes). Mol Gen Genet 184: 161–165

    Google Scholar 

  • Panteris E, Apostolakos P, Galatis B (1992) The organization of F-actin in root tip cells ofAdiantum capillus veneris throughout the cell cycle. Protoplasma 170: 128–137

    Google Scholar 

  • Parthasarathy MV, Perdue TD, Witztum A, Alvernaz J (1985) Actin network as a normal component of the cytoskeleton in many vascular plant cells. Am J Bot 72: 1318–1323

    Google Scholar 

  • Schellenbaum P, Vantard M, Peter C, Lambert A (1993) Co-assembly properties of higher plant microtubule-associated proteins with purified brain and plant tubulins. Plant J 3: 253–260

    Google Scholar 

  • Schmit A, Lambert A (1990) Microinjected fluorescent phalloidin in vivo reveals the F-actin dynamics and assembly of higher plant mitotic cells. Plant Cell 2: 129–138

    Google Scholar 

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

    Google Scholar 

  • Simmonds DH (1986) Prophase bands of microtubules occur in protoplast cultures ofVicia hajastana Grossh. Planta 167: 469–472

    Google Scholar 

  • —, 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

    Google Scholar 

  • Sinnott EW, Bloch R (1940) Cytoplasmic behavior during division of vacuolate plant cells. Proc Natl Acad Sci USA 26: 223–227

    Google Scholar 

  • Smith LG, Hake S, Sylvester AW (1996) Thetangled-1 mutation alters cell division orientations throughout maize leaf development without altering leaf shape. Development 122: 481–489

    Google Scholar 

  • Sonobe S, Shibaoka H (1989) Cortical fine actin filaments in higher plant cells visualized by rhodamine-phalloidin after pretreatment withm-maleimidobenzoyl N-hydroxysuccinimide ester. Protoplasma 148: 80–86

    Google Scholar 

  • Staiger CJ, Lloyd CW (1991) The plant cytoskeleton. Curr Opin Cell Biol 3: 33–42

    Google Scholar 

  • Tautorus TE, Wang H, Fowke LC, Dunstan DI (1992) Microtubule pattern and the occurrence of preprophase bands in embryogenic cultures of black spruce (Picea mariana Mill.) and nonembryogenic cultures of jack pine (Pinus banksiana Lamb.). Plant Cell Rep 11: 419–423

    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 dividing nucleus. J Cell Biol 105: 387–395

    Google Scholar 

  • Venverloo CJ, Hovenkamp PH, Weeda AJ, Lbbenga KR (1980) Cell division inNautilocalyx explants I: phragmosome, preprophase band and plane of division. Z Pflanzenphysiol 100: 161–174

    Google Scholar 

  • Wareing PF, Phillips IDJ (1981) Growth and differentiation in plants, 3rd edn. Pergamon Press, Oxford

    Google Scholar 

  • Yasuhara H, Sonobe S, Shibaoka H (1993) Effects of taxol on the development of the cell plate and of the phragmoplast in tobacco BY-2 cells. Plant Cell Physiol 34: 21–29

    Google Scholar 

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  1. David A. Collings

    Present address: Department of Botany, North Carolina State University, Raleigh, North Carolina, USA

Authors and Affiliations

  1. Laboratory of Plant Cytology and Morphology, Wageningen University, Arboretumlaan 4, 6703 BD, Wageningen, The Netherlands

    David A. Collings & Anne Mie C. Emons

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  1. David A. Collings
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  2. Anne Mie C. Emons
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Correspondence to Anne Mie C. Emons.

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Collings, D.A., Emons, A.M.C. Microtubule and actin filament organization during acentral divisions in potato suspension culture cells. Protoplasma 207, 158–168 (1999). https://doi.org/10.1007/BF01282996

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