Plant Biol (Stuttg) 2001; 3(1): 4-16
DOI: 10.1055/s-2001-11749
Review Article
Georg Thieme Verlag Stuttgart ·New York

Dynamic Organization of Microtubules and Microfilaments during Cell Cycle Progression in Higher Plant Cells

F. Kumagai, S. Hasezawa
  • Department of Integrated Biosciences, Graduate School of Frontier Sciences, The University of Tokyo, Hongo, Bunkyo-ku, Tokyo 113-0033, Japan
Further Information

Publication History

September 7, 2000

December 8, 2000

Publication Date:
31 December 2001 (online)

Abstract

The cytoskeleton, which mainly consists of microtubules (MTs) and actin microfilaments (MFs), plays various significant roles that are indispensable for eukaryotic viability, including determination of cell shape, cell movement, nuclear division, and cytokinesis. In animal cells, MFs appear to be of more importance than MTs, except for spindle formation in nuclear division. In contrast, higher plants have a rigid cell wall around their cells, and have thus evolved elegant systems of MTs to control the direction of cellulose microfibrils (CMFs) deposited in the cell wall, and to divide centrifugally in a physically limited space. Dynamic changes in MTs during cell cycle progression in higher plant cells have been observed over several decades, including cortical MTs (CMTs) during interphase, preprophase bands (PPBs) from late G2 phase to prophase, spindles from prometaphase to anaphase, and phragmoplasts at telophase. The MFs also show some changes not as obvious as MT dynamics. However, questions regarding the process of formation of these arrays, and the precise mechanisms by which they fulfill their roles, remain unsolved. In this article, we present an outline of the changes in the cytoskeleton based on our studies with highly-synchronized tobacco BY-2 cells. Some candidate molecules that could play roles in cytoskeletal dynamics are discussed. We also hope to draw attention to recent attempts at visualization of cytoskeletons with molecular techniques, and to some examples of genetic approaches in this field.

Abbreviations

ADZ: actin-depleted zone

CMF: cellulose microfibril

CMT: cortical microtubule

CSC: cellulose synthesizing complex

GFP: green fluorescent protein

MAP: microtubule associated protein

MT: microtubule

MF: microfilament

MTOC: microtubule organizing centre

PPB: preprophase band

References

  • 01 Andersen,  S. S. L.. (1999);  Molecular characteristics of the centrosome.  Int. Rev. Cytol.. 187 51-109
  • 02 Andersen,  S. S. L.,, Ashford,  A. J.,, Tournebize,  R.,, Gavet,  O.,, Sobel,  A.,, Hyman,  A. A.,, and Karsenti,  E.. (1997);  Mitotic chromatin regulates phosphorylation of Stathmin/Op 18.  Nature. 389 640-643
  • 03 Arioli,  T.,, Peng,  L.,, Betzer,  A. S.,, Burn,  J.,, Wittke,  W.,, Heath,  W.,, Camilleri,  C.,, Hoffe,  H.,, Plazinski,  J.,, Birch,  R.,, Cork,  A.,, Glover,  J.,, Redmond,  J.,, and Williamson,  R. E.. (1998);  Molecular analysis of cellulose biosynthesis in Arabidopsis. .  Science. 279 717-720
  • 04 Asada,  T.,, Sonobe,  S.,, and Shibaoka,  H.. (1991);  Microtubule translocation in the cytokinetic apparatus of cultured tobacco cells.  Nature. 350 238-241
  • 05 Asada,  T., and Shibaoka,  H.. (1994);  Isolation of polypeptides with microtubule-translocating activity from phragmoplasts of tobacco BY-2 cells.  J. Cell Sci.. 107 2249-2257
  • 06 Baluška,  F.,, Volkmann,  D.,, and Barlow,  P. W.. (1997);  Nuclear components with microtubule-organizing properties in multicellular eukaryotes: function and evolutionary considerations.  Int. Rev. Cytol.. 175 91-135
  • 07 Baluška,  F.,, Volkmann,  D.,, and Barlow,  P. W.. (2000);  Actin-based domains of the “cell periphery complex” and their associations with polarized “cell bodies” in higher plants.  Plant Biol.. 2 253-267
  • 08 Baskin,  T. I., and Cande,  W. Z.. (1990);  The structures and function of the mitotic spindle in flowering plants.  Annu. Rev. Plant Physiol. Plant Mol. Biol.. 41 277-315
  • 09 Binarová,  F.,, DoleŽel,  J.,, Dráber,  P.,, Heberle-Bors,  E.,, Strnad,  M.,, and Bögre,  M. S. L.. (1998);  Treatment of Vicia faba root tip cells with specific inhibitors to cyclin-dependent kinases leads to abnormal spindle formation.  Plant J.. 16 697-707
  • 10 Binarová,  P.,, Cenklová,  V.,, Hause,  B.,, Kubátová,  E.,, Lysák,  M.,, DoleŽel,  J.,, Bögre,  L.,, and Dráber,  P.. (2000);  Nuclear γ-tubulin during acentriolar plant mitosis.  Plant Cell. 12 433-442
  • 11 Blackman,  L. M.,, Harper,  J. D. I.,, and Overall,  R. L.. (1999);  Localization of a centrin-like protein to higher plant plasmodesmata.  Eur. J. Cell Biol.. 78 297-304
  • 12 Chan,  J.,, Jensen,  C. G.,, Jensen,  L. C. W.,, Bush,  M.,, and Lloyd,  C. W.. (1999);  The 65-kDa carrot microtubule-associated protein forms regularly arranged filamentous cross-bridges between microfibrils.  Proc. Natl. Acad. Sci. USA. 96 14931-14936
  • 13 Clark,  S. W., and Meyer,  D. I.. (1992);  Centractin is an actin homologue associated with centrosome.  Nature. 359 246-250
  • 14 Cleary,  A. L.,, Gunning,  B. E. S.,, Wasteneys,  G. O.,, and Hepler,  P. K.. (1992);  Microtubule and F-actin dynamics at the division site in living Tradescantia stamen hair cells.  J. Cell Sci.. 103 977-988
  • 15 Cleary,  A. L.. (1995);  F-actin redistributions at the division site in living Tradescantia stomata complexes as revealed by microinjection of rhodamine-phalloidin.  Protoplasma. 185 152-165
  • 16 Cleary,  A. L., and Smith,  L. G.. (1998);  The Tangled1 gene is required for spatial control of cytoskeleton arrays associated with cell division during maize leaf development.  Plant Cell. 10 1875-1888
  • 17 Colasanti,  J.,, Cho,  S.-O.,, Wick,  S.,, and Sunderesan,  V.. (1993);  Localization of the functional p34cdc2 homolog of maize in root tip and stomatal complex cells.  Plant Cell. 5 1101-1111
  • 18 Collings,  D. A.,, Asada,  T.,, Allen,  N. S.,, and Shibaoka,  H.. (1998);  Plasma membrane-associated actin in Bright Yellow 2 tobacco cells.  Plant Physiol.. 118 917-928
  • 19 Compton,  D. A., and Cleveland,  D. W.. (1994);  NuMA, a nuclear protein involved in mitosis and nuclear reformation.  Curr. Opin. Cell Biol.. 6 343-346
  • 20 de Ruijter,  N. C. A., and Emons,  A. M. C.. (1999);  Actin-binding proteins in plant cells.  Plant Biol.. 1 26-35
  • 21 Del Vecchio,  A. J.,, Harper,  J. D. I.,, Vaughn,  K. C.,, Baron,  A. T.,, Salisbury,  J. L.,, and Overall,  R. L.. (1997);  Centrin homologues in higher plants are prominently associated with the developing cell plate.  Protoplasma. 196 224-234
  • 22 Delmer,  D. P., and Amor,  Y.. (1995);  Cellulose biosynthesis.  Plant Cell. 7 987-1000
  • 23 Doxsey,  S. J.,, Stein,  P.,, Evans,  L.,, Calarco,  P. D.,, and Kirschner,  M.. (1994);  Pericentrin, a highly conserved centrosome protein involved in microtubule organization.  Cell. 76 639-650
  • 24 Erickson,  H. P.. (2000);  γ-Tubulin nucleation: template or protofilament?.  Nature Cell Biol.. 2 E93-E96
  • 25 Gervais,  C.,, Simmonds,  D. H.,, and Newcomb,  W.. (1994);  Actin microfilament organization during pollen development of Brassica napus cv. Topas.  Protoplasma. 183 67-76
  • 26 Giddings,  T. H., and Staehelin,  L. A.. (1988);  Spatial relationship between microtubules and plasma membrane rosettes during the deposition of primary wall microfibrils in Closterium sp.  Planta. 173 22-30
  • 27 Giddings,  T. H., and Staehelin,  L. A.. (1991) Microtubule-mediated control of microfibril deposition: a re-examination of the hypothesis. The cytoskeletal basis of plant growth and form. Lloyd, C. W., ed. San Diego; Academic Press pp. 85-100
  • 28 Granger,  C. L., and Cyr,  R. J.. (2000);  Microtubule reorganization in tobacco BY-2 cells stably expressing GFP-MBD.  Planta. 210 502-509
  • 29 Hasezawa,  S.,, Marc,  J.,, and Palevitz,  B. A.. (1991);  Microtubule reorganization during the cell cycle in synchronized BY-2 tobacco suspensions.  Cell Motil. Cytoskel.. 18 94-106
  • 30 Hasezawa,  S., and Nagata,  T.. (1991);  Dynamic organization of plant microtubules at the three distinct transition points during the cell cycle progression of synchronized tobacco BY-2 cells.  Bot. Acta. 104 206-211
  • 31 Hasezawa,  S., and Nagata,  T.. (1993);  Microtubule organizing centers in plant cells: localization of a 49 kDa protein that is immunologically cross-reactive to a 51 kDa protein from sea urchin centrosomes in synchronized tobacco BY-2 cells.  Protoplasma. 176 64-74
  • 32 Hasezawa,  S.,, Kumagai,  F.,, and Nagata,  T.. (1997);  Sites of microtubule reorganization in tobacco BY-2 cells during cell-cycle progression.  Protoplasma. 198 202-209
  • 33 Hasezawa,  S.,, Sano,  T.,, and Nagata,  T.. (1998);  The role of microfilaments in the organization and orientation of microtubules during the cell cycle transition from M phase to G1 phase in tobacco BY-2 cells.  Protoplasma. 202 105-114
  • 34 Hasezawa,  S., and Nozaki,  H.. (1999);  Role of cortical microtubules in the orientation of cellulose microfibril deposition in higher-plant cells.  Protoplasma. 209 98-104
  • 35 Hasezawa,  S.,, Ueda,  K.,, and Kumagai,  F.. (2000);  Time-sequence observation of microtubule dynamics throughout mitosis in living cell suspensions of stable transgenic Arabidopsis-direct evidence for the origin of cortical microtubules at M/G1 interphase.  Plant Cell Physiol.. 41 244-250
  • 36 Heald,  R.,, Tournebize,  C.,, Blank,  T.,, Sandantzopoulos,  R.,, Becken,  P.,, Hyman,  A. R.,, and Karsenti,  E.. (1996);  Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopus egg extracts.  Nature. 385 420-425
  • 37 Heath,  I. B.. (1974);  A unified hypothesis for the role of membrane bound enzyme complexes and microtubules in plant cell wall synthesis.  J. Theor. Biol.. 48 445-449
  • 38 Hepler,  P. K., and Gunning,  B. E. S.. (1998);  Confocal fluorescence microscopy of plant cells.  Protoplasma. 201 121-157
  • 39 Huang,  J.-D.,, Brady,  S. T.,, Richards,  B. W.,, Stenojen,  D.,, Resau,  J. H.,, Copeland,  N. G.,, and Jenkins,  N. A.. (1999);  Direct interaction of microtubule- and actin-based transport motors.  Nature. 397 267-270
  • 40 Igarashi,  H.,, Orii,  H.,, Mori,  H.,, Shimmen,  T.,, and Sonobe,  S.. (2000);  Isolation of a novel 190 kDa protein from tobacco BY-2 cells: Possible involvement in the interaction between actin filaments and microtubules.  Plant Cell Physiol.. 41 920-931
  • 41 Jeng,  R., and Stearns,  T.. (1999);  γ-Tubulin complexes: size does matter.  Trends Cell Biol.. 9 339-342
  • 42 Jiang,  C.-J., and Sonobe,  S.. (1993);  Identification of preliminary characterization of a 65 kDa higher-plant microtubule-associated protein.  J. Cell Sci.. 105 891-901
  • 43 Kahana,  J. A., and Cleveland,  D. W.. (1999);  Beyond nuclear transport: Ran-GTP as a determinant of spindle assembly.  J. Cell Biol.. 146 1205-1209
  • 44 Kakimoto,  T., and Shibaoka,  H.. (1988);  Cytoskeletal ultrastructure of phragmoplast-nuclei complexes isolated from cultured tobacco cells.  Protoplasma,. Suppl. 2 95-103
  • 45 Katsuta,  J., and 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
  • 46 Katsuta,  J.,, Hashiguchi,  Y.,, and 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
  • 47 Keating,  T. J., and Borisy,  G. G.. (2000);  Immunostructural evidence for the template mechanism of microtubule nucleation.  Nature Cell Biol.. 2 352-357
  • 48 Kengen,  H. M. P.,, Eygensteyn,  J.,, and von Amstel,  T. N. M.. (1995);  F-actin in mitotic spindles of synchronized suspension culture cells of tobacco visualized by confocal laser scanning microscopy.  Cell Biol. Int.. 19 585-592
  • 49 Kimura,  S.,, Laosinchai,  W.,, Itoh,  T.,, Cui,  X.,, Linder,  C. R.,, and Malcolm Brown,  J. R.. (1999);  Immunogold labeling of rosette terminal cellulose-synthesizing complexes in the vascular plant Vigna angularis. .  Plant Cell. 11 2075-2085
  • 50 Kost,  B.,, Spielhofer,  P.,, and Chua,  N.-H.. (1998);  A GFP-mouse talin fusion protein labels plant actin filaments in vivo and visualizes the actin cytoskeleton in growing pollen tubes.  Plant J.. 16 393-401
  • 51 Kumagai,  F.,, Hasezawa,  S.,, Takahashi,  Y.,, and Nagata,  T.. (1995);  The involvement of protein synthesis elongation factor 1α in the organization of microtubules on the perinuclear region during the cell cycle transition from M phase to G1 phase in tobacco BY-2 cells.  Bot. Acta. 108 467-473
  • 52 Kumagai,  F.,, Hasezawa,  S.,, and Nagata,  T.. (1999);  Putative involvement of a 49 kDa protein in microtubule assembly in vitro. .  Eur. J. Cell Biol.. 78 109-116
  • 53 Lambert,  A.-M.,, Vantard,  M.,, Schmit,  A.-C.,, and Stoeckel,  H.. (1991) Mitosis in plants. The cytoskeletal basis of plant growth and form. Lloyd C. W., ed. London; Academic Press pp. 199-208
  • 54 Lambert,  A.-M.. (1993);  Microtubule-organizing centers in higher plants.  Curr. Opin. Cell Biol.. 5 116-122
  • 55 Lambert,  A.-M.,, and Lloyd,  C. W.. (1994) The higher plant microtubule cycle. Microtubule. Hyams, J. S., and Lloyd, C. W., eds. New York; Wiley-Liss pp. 325-341
  • 56 Lambert,  A.-M.,. (1995);  Microtubule-organizing centers in higher plants: evolving concepts.  Bot. Acta. 108 535-537
  • 57 Lantz,  V. A., and Miller,  K. G.. (1998);  A class VI unconventional myosin is associated with a homologue of a microtubule-binding protein, cytoplasmic linker protein-170, in neurons and at the posterior pole of Drosophila embryos.  The J. Cell Biol.. 140 897-910
  • 58 Ledbetter,  M. C., and Porter,  K. R.. (1963);  A “microtubule” in plant fine structure.  J. Cell Biol.. 19 239-250
  • 59 Leguy,  R.,, Melki,  R.,, Pantaloni,  D.,, and Carlier,  M.-F.. (2000);  Monomeric γ-tubulin nucleates microtubules.  J. Biol. Chem.. 275 21975-21980
  • 60 Leung,  C. L.,, Sun,  D.,, Zheng,  M.,, Knowles,  D. R.,, and Liem,  R. K. H.. (1999);  Microtubule actin cross-linking factor (MACF): a hybrid of dystonin and dystrophin that can interact with the actin and microtubule cytoskeletons.  J. Cell Biol.. 147 1275-1285
  • 61 Liu,  B., and Palevitz,  B. A.. (1992);  Organization of cortical microfilaments in dividing root cells.  Cell Motil. Cytoskel.. 23 252-264
  • 62 Liu,  B.,, Marc,  J.,, Joshi,  H. C.,, and Palevitz,  B. A.. (1993);  A γ-tubulin related protein associated with the microtubule arrays of higher plant cells in a cell cycle-dependent manner.  J. Cell Sci.. 104 1217-1228
  • 63 Liu,  B.,, Joshi,  H. C.,, Wilson,  T. J.,, Silflow,  C. D.,, Palevitz,  B. A.,, and Snustad,  D. P.. (1994);  γ-Tubulin in Arabidopsis: gene sequence, immunoblot, and immunofluorescence studies.  Plant Cell. 6 303-314
  • 64 Ludin,  B., and Matus,  A.. (1998);  GFP illuminates the cytoskeleton.  Trends Cell Biol.. 8 72-77
  • 65 Marc,  J.,, Granger,  C. L.,, Brincat,  J.,, Fisher,  D. D.,, Kao,  T.,, McCubbin,  A. G.,, and Cyr,  R. J.. (1998);  A GFP-MAP4 reporter gene for visualizing cortical microtubule rearrangements in living epidermal cells.  Plant Cell. 10 1927-1939
  • 66 Marchesi,  V. T., and Ngo,  N.. (1993);  In vitro assembly of multiprotein complexes containing α, β, and γ tubulin, heat shock protein HSP70, and elongation factor 1α.  Proc. Natl. Acad. Sci. USA. 90 3028-3032
  • 67 Mathur,  J., and Chua,  N.-H.. (2000);  Microtubule stabilization leads to growth reorientation in Arabidopsis trichomes.  Plant Cell. 12 465-478
  • 68 Mazia,  D.. (1987);  The chromosome cycle and the centrosome cycle in the mitotic cycle.  Int. Rev. Cytol.. 100 49-92
  • 69 McClinton,  R. S., and Sung,  Z. R.. (1997);  Organization of cortical microtubules at the plasma membrane in Arabidopsis. .  Planta. 201 252-260
  • 70 McCurdy,  D. W., and Gunning,  B. E. S.. (1990);  Reorganization of cortical actin microfilaments and microtubules at preprophase and mitosis in wheat root-tip cells: a double label immunofluorescence study.  Cell Motil. Cytoskel.. 15 76-87
  • 71 Mews,  M.,, Sek,  F. J.,, Moore,  R.,, Volkmann,  D.,, Gunning,  B. E. S.,, and John,  P. C. L.. (1997);  Mitotic cyclin distribution during maize cell division: implications for the sequence diversity and function of cyclins in plants.  Protoplasma. 200 128-145
  • 72 Mineyuki,  Y., and Gunning,  B. E. S.. (1990);  A role for preprophase bands of microtubules in maturation of new cell walls, and a general proposal on the function of preprophase band sites in cell division in higher plants.  J. Cell Sci.. 97 527-537
  • 73 Mineyuki,  Y., and Palevitz,  B. A.. (1990);  Relationship between preprophase band organization, F-actin and the division site in Allium. .  J. Cell Sci.. 97 283-295
  • 74 Mineyuki,  Y.. (1999);  The preprophase band of microtubules: its function as a cytokinetic apparatus in higher plants.  Int. Rev. Cytol.. 187 1-49
  • 75 Mitsui,  H.,, Hasezawa,  S.,, Nagata,  T.,, and Takahashi,  H.. (1996);  Cell cycle dependent accumulation of a kinesin-like protein, Kat B/C, in synchronized tobacco BY-2 cells.  Plant Mol. Biol.. 30 177-181
  • 76 Miyake,  T.,, Hasezawa,  S.,, and Nagata,  T.. (1997);  Role of cytoskeletal components in the migration of nuclei during the cell cycle transition from G1 phase to S phase of tobacco BY-2 cells.  J. Plant Physiol.. 150 528-536
  • 77 Mizutani,  T.,, Katsuta,  J.,, and Shibaoka,  H.. (1993);  Nuclear-cycle dependence of the development of the preprophase band in tobacco BY-2 cells.  Plant Cell Physiol.. 34 215-219
  • 78 Molé-Bajer,  J., and Bajer,  A. S.. (1988);  Relation of F-actin organization to microtubules in drug treated Haemanthus mitosis.  Protoplasma,. Suppl. 1 99-112
  • 79 Moritz,  M.,, Braunfeld,  M. B.,, Guénebaut,  V.,, Heuse,  J.,, and Agard,  D. A.. (2000);  Structure of the γ-tubulin ring complex: a template for microtubule nucleation.  Nature Cell Biol.. 2 365-370
  • 80 Nagata,  T.,, Okada,  K.,, and Takebe,  I.. (1982);  Mitotic protoplasts and their infection with tobacco mosaic virus RNA encapsulated in liposomes.  Plant Cell Rep.. 1 250-252
  • 81 Nagata,  T.,, Nemoto,  Y.,, and Hasezawa,  S.. (1992);  Tobacco BY-2 cell line as the “HeLa” cell in the cell biology of higher plants.  Int. Rev. Cytol.. 132 1-30
  • 82 Nagata,  T.,, Kumagai,  F.,, and Hasezawa,  S.. (1994);  The origin and organization of cortical microtubules during the transition between M and G1 phases of the cell cycle as observed in highly synchronized cells of tobacco BY-2.  Planta. 193 567-572
  • 83 Nagata,  T.,, and Kumagai,  F.. (1999);  Plant cell biology through the window of the highly synchronized tobacco BY-2 cell line.  Meth. Cell Sci.. 21 123-127
  • 84 Nasmyth,  K.,, Peters,  J.-M.,, and Uhlmann,  F.. (2000);  Splitting the chromosome: cutting the ties that bind sister chromatids.  Science. 288 1379-1384
  • 85 Nishimoto,  T.. (1999);  A new role of Ran GTPase.  Biochem. Biophys. Res. Comm.. 262 571-574
  • 86 Oakley,  B. R.,, Oakley,  C. E.,, Yoon,  Y.,, and Jung,  M. K.. (1990);  γ-Tubulin is a component of the spindle pole body that is essential for microtubule function in Aspergillus nidulans. .  Cell. 61 1289-1301
  • 87 Oakley,  B. R.. (1995);  A nice ring to the centrosome.  Nature. 378 555-556
  • 88 Ohta,  K.,, Toriyama,  M.,, Miyazaki,  M.,, Murofushi,  H.,, Hosoda,  S.,, Endo,  S.,, and Sakai,  H.. (1990);  The mitotic apparatus-associated 51-kDa protein from sea urchin eggs is a GTP-binding protein and is immunologically related to yeast polypeptide elongation factor 1α.  J. Biol. Chem.. 265 3240-3247
  • 89 Olsen,  O.-A.,, Brown,  R. C.,, and Lemmon,  B. E.. (1995);  Pattern and process of wall formation in developing endosperm.  Bioessays. 17 803-812
  • 90 Ookata,  K.,, Hisanaga,  S.,, Bulinski,  J. C.,, Murofushi,  H.,, Aizawa,  H.,, Itoh,  T. J.,, Hotani,  H.,, Okumura,  E.,, Tachibana,  K.,, and Kishimoto,  T.. (1995);  Cyclin B interaction with microtubule-associated protein 4 (MAP4) targets p34cdc2 kinase to microtubules and is a potential regulator of M-phase microtubule dynamics.  J. Cell Biol.. 128 849-862
  • 91 Pear,  J. R.,, Kawagoe,  Y.,, Schrechkengost,  W. E.,, Delmer,  D. P.,, and Stalker,  D. M.. (1996);  Higher plants contain homologs of the bacterial celA genes encoding the catalytic subunit of cellulose synthase.  Proc. Natl. Acad. Sci. USA. 93 12637-12642
  • 92 Pedrotti,  B.,, Colombo,  R.,, and Islam,  K.. (1994);  Microtubule associated protein MAP1A is an actin-binding and crosslinking protein.  Cell Motil. Cytoskel.. 29 110-116
  • 93 Pickett-Heaps,  J. D.,, Gunning,  B. E. S.,, Brown,  R. C.,, Lemmon,  B. E.,, and Cleary,  A. L.. (1999);  The cytoplast concept in dividing plant cells: cytoplasmic domains and the evolution of spatially organized cell division.  Amer. J. Bot.. 86 153-172
  • 94 Sattilaro,  R. F.. (1986);  Interaction of microtubule-associated protein 2 with actin filaments.  Biochemistry. 25 2003-2009
  • 95 Schiebel,  E., and Bornens,  M.. (1995);  In search of a function for centrins.  Trends Cell Biol.. 5 197-201
  • 96 Schiebel,  E.. (2000);  γ-Tubulin complexes: binding to the centrosome, regulation and microtubule nucleation.  Curr. Opin. Cell Biol.. 12 113-118
  • 97 Schmit,  A.-C., and Lambert,  A.-M.. (1987);  Characterization and dynamics of cytoplasmic F-actin in higher plant endosperm cells during interphase, mitosis, and cytokinesis.  J. Cell Biol.. 105 2157-2166
  • 98 Schmit,  A.-C., and Lambert,  A.-M.. (1988);  Plant actin filament and microtubule interactions during anaphase-telophase transition: effects of antagonist drugs.  Biol. Cell. 64 309-319
  • 99 Seagull,  R. W.,, Falconer,  M. M.,, and Weerdenburg,  C. A.. (1987);  Microfilaments: dynamic arrays in higher plant cells.  J. Cell Biol.. 104 995-1004
  • 100 Shibaoka,  H.. (1994);  Plant hormone-induced changes in the orientation of cortical microtubules: alterations in the cross-linking between microtubules and the plasma membrane.  Ann. Rev. Plant Physiol. Plant Mol. Biol. . 45 527-544
  • 101 Shibaoka,  H., and Nagai,  R.. (1994);  The plant cytoskeleton.  Curr. Opin. Cell Biol.. 6 10-15
  • 102 Smirnova,  E. A.,, Cox,  D. L.,, and Bajer,  A. S.. (1995);  Antibody against phosphorylated proteins (MPM-2) recognizes mitotic microtubules in endosperm cells of higher plant Haemanthus. .  Cell Motil. Cytoskel.. 31 34-44
  • 103 Smith,  L. G.,, Hake,  S.,, and Sylvester,  A. W.. (1996);  The tangled-1 mutation alters cell division orientations throughout maize leaf development without altering leaf shape.  Development. 122 481-489
  • 104 Staehelin,  L. A., and Hepler,  P. K.. (1996);  Cytokinesis in higher plants.  Cell. 84 821-824
  • 105 Staiger,  C. J., and Lloyd,  C. W.. (1991);  The plant cytoskeleton.  Curr. Opin. Cell Biol.. 3 33-42
  • 106 Stoppin-Mellet,  V.,, Canaday,  J.,, and Lambert,  A.-M.. (1999);  Characterization of microsome-associated tobacco BY-2 centrins.  Eur. J. Cell Biol.. 78 842-848
  • 107 Stoppin-Mellet,  V.,, Peter,  C.,, and Lambert,  A.-M.. (2000);  Distribution of γ-tubulin in plant cells: cytosolic γ-tubulin is part of high molecular weight complexes.  Plant Biol.. 2 290-296
  • 108 Toriyama,  M.,, Ohta,  K.,, Endo,  S.,, and Sakai,  H.. (1988);  51-kd protein, a component of microtubule-organizing granules in the mitotic apparatus involved in aster formation in vitro. .  Cell Motil. Cytoskel.. 9 117-128
  • 109 Traas,  J. A.,, Doonan,  J. H.,, Rawlins,  D. J.,, Shaw,  P. J.,, Watts,  J.,, and Lloyd,  C. W.. (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
  • 110 Traas,  J.,, Bellini,  C.,, Nacry,  P.,, Kronenberger,  J.,, Bouchez,  D.,, and Cabosche,  M.. (1995);  Normal differentiation patterns in plants lacking microtubular preprophase bands.  Nature. 375 676-677
  • 111 Ueda,  K.,, Matsuyama,  T.,, and Hashimoto,  T.. (1999);  Visualization of microtubules in living cells of transgenic Arabidopsis thaliana. .  Protoplasma. 206 201-206
  • 112 Vandré,  D. D.,, Davis,  F. M.,, Rao,  P. N.,, and Borisy,  G. G.. (1986);  Distribution of cytoskeletal proteins sharing a conserved phosphorylated epitope.  Eur. J. Cell Biol.. 41 72-81
  • 113 Vaughan,  K. T.,, Tynan,  S. H.,, Faulkner,  N. E.,, Echeverri,  C. J.,, and Vallee,  R. B.. (1999);  Colocalization of cytoplasmic dynein with dynactin and CLIP-170 at microtubule distal ends.  J. Cell Sci.. 112 1437-1447
  • 114 Vaughn,  K. C., and Harper,  J. D. I.. (1998);  Microtubule-organizing centers and nucleating sites in land plants.  Int. Rev. Cytol.. 181 75-149
  • 115 Wiese,  C., and Zheng,  Y.. (2000);  A new function for the γ-tubulin ring complex as a microtubule minus-end cap.  Nature Cell Biol.. 2 358-364
  • 116 Yang,  Y.,, Bauer,  C.,, Strasser,  G.,, Wollman,  R.,, Julien,  J.-P.,, and Fuchs,  E.. (1999);  Integrators of the cytoskeleton that stabilize microtubules.  Cell. 98 229-238
  • 117 Yasuhara,  H.,, Sonobe,  S.,, and 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
  • 118 Yu,  W., and de.la. Espina,  S. M. D.. (1999);  The plant nucleoskeleton: ultrastructural organization and identification of NuMA homologues in the nuclear matrix and mitotic spindle of plant cells.  Exp. Cell Res.. 246 516-526
  • 119 Zhang,  D.,, Wadsworth,  P.,, and Hepler,  P. K.. (1993);  Dynamics of microfilaments are similar, but distinct from microtubules during cytokinesis in living, dividing plant cells.  Cell Motil. Cytoskel.. 24 151-155

F. Kumagai

Department of Integrated Biosciences
Graduate School of Frontier Sciences
The University of Tokyo

Hongo, Bunkyo-ku
Tokyo 113-0033, Japan

Email: kumagai@biol.s.u-tokyo.ac.jp

Section Editor: T. Nagata

    >