Summary
Tradescantia virginiana leaf epidermal cells were plasmolysed by sequential treatment with 0.8 M and 0.3 M sucrose. Plasmolysis revealed adhesion of the plasma membrane to the cell wall at sites coinciding with cytoskeletal arrays involved in the polarisation of cells undergoing asymmetric divisions — cortical actin patch — and in the establishment and maintenance of the division site —preprophase band of microtubules and filamentous (F) actin. The majority of cells retained adhesions at the actin patch throughout mitosis. However, only approximately 13% of cells formed or retained attachments at the site of the preprophase band. After the breakdown of the nuclear envelope, plasmolysis had a dramatic effect on spindle orientation, cell plate formation, and the plane of cytokinesis. Spindles were rotated at abnormal angles including tilted into the plane of the epidermis. Cell plates formed but were quickly replaced by vacuole-like intercellular compartments containing no Tinopal-stainable cell wall material. This compartment usually opened to the apoplast at one side, and cytokinesis was completed by the furrow extending across the protoplast. This atypical cytokinesis was facilitated by a phragmoplast containing microtubules and F-actin. Progression of the furrow was unaffected by 25 μg of cytochalasin B per ml but inhibited by 10 μM oryzalin. Phragmoplasts were contorted and misguided and cytokinesis prolonged, indicating severe disruption to the guidance mechanisms controlling phragmoplast expansion. These results are discussed in terms of cytoskeleton-plasma membrane-cell wall connections that could be important to the localisation of plasma membrane molecules defining the cortical division site and hence providing positional information to the cytokinetic apparatus, and/or for providing an anchor for cytoplasmic F-actin necessary to generate tension on the phragmoplast and facilitate its directed, planar expansion.
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Abbreviations
- ADZ:
-
actin-depleted zone
- DIC:
-
differential interference contrast
- GMC:
-
guard mother cell
- MT:
-
microtubule
- PPB:
-
preprophase band
- SMC:
-
subsidiary mother cell
References
Allen VW, Kropf DL (1992) Nuclear rotation and lineage specification inPelvetia embryos. Development 115: 873–883
Baskin TI, Cande WZ (1990) The structure and function of the mitotic spindle in flowering plants. Annu Rev Plant Physiol Plant Mol Biol 41: 277–315
Cho S, Wick SM (1989) Microtubule orientation during stomatal differentiation in grasses. J Cell Sci 92: 581–594
— — (1990) Distribution and function of actin in the developing stomatal complex of winter rye (Secale cereale cv. Puma). Protoplasma 157: 154–164
Cleary AL (1995) F-actin redistributions at the division site in livingTradescantia stomatal complexes as revealed by microinjection of rhodamine-phalloidin. Protoplasma 185: 152–165
— (2000) Actin in formation of stomatal complexes. In: Staiger C, Baluska F, Volkmann D, Barlow P (eds) Actin: a dynamic framework for multiple plant cell functions. Kluwer, Dordrecht, pp 411–426
—, Hardham AR (1988) Depolymerization of microtubule arrays in root tip cells by oryzalin and their recovery with modified nucleation patterns. Can J Bot 66: 2353–2366
— — (1989) Microtubule organization during development of stomatal complexes inLolium rigidum. Protoplasma 149: 67–81
—, Mathesius U (1996) Rearrangements of F-actin during stomatogenesis visualised by confocal microscopy in fixed and permeabilisedTradescantia leaf epidermis. Bot Acta 109: 15–24
—, Smith LG (1998) The tangledl gene is required for spatial control of cytoskeletal arrays associated with cell division during maize leaf development. Plant Cell 10: 1875–1888
—, Gunning BES, Wasteneys GO, Hepler PK (1992) Microtubule and F-actin dynamics at the division site in livingTradescantia stamen hair cells. J Cell Sci 103: 977–988
Croxdale J, Smith J, Yandell B, Johnson JB (1992) Stomatal patterning inTradescantia: an evaluation of the cell lineage theory. Dev Biol 149: 158–167
Del Vecchio AJ, Harper JDI, Vaughn KC, Baron AT, Salisbury JL, Overall RL (1997) Centrin homologues in higher plants are prominently associated with the developing cell plate. Protoplasma 196: 224–234
Gens JS, Reuzeau C, Doolittle KW, McNally JG, Pickard BG (1996) Covisualization by computational optical-sectioning microscopy of integrin and associated proteins at the cell membrane of living onion protoplasts. Protoplasma 194: 215–230
Giménez-Abián MI, Panzera F, López-Sáez JF, Giménez-Abián JF, De la Torre C, Giménez-Martin G (1998) Immediate disruption of spindle poles and induction of additional microtubule-organizing centres by a phenycarbamate, during plant mitosis. Protoplasma 204: 119–127
Gu X, Verma DP (1997) Phragmoplastin, a dynamin-like protein associated with cell plate formation in plants. EMBO J 15: 695–704
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
Hecht K (1912) Studien ueber den Vorgang der Plasmolyse. Beitr Biol Pflanzen 11: 137–194
Henry CA, Jordan JR, Kropf DL (1996) Localized membrane-wall adhesions inPelvetia zygotes. Protoplasma 190: 39–52
Herth W, Meyer Y (1978) Cytology of budding and cleavage in tobacco mesophyll protoplasts cultivated in saline medium. Planta 142: 11–21
Kagawa T, Kadota A, Wada M (1992) The junction between the plasma membrane and the cell wall in fern protonemal cells, as visualised after plasmolysis and its dependence on arrays of cortical microtubules. Protoplasma 170: 186–190
Kaminskyj SGW, Heath IB (1995) Integrin and spectrin homologues, and cytoplasm-wall adhesion in tip growth. J Cell Sci 108: 849–856
Kennard JL, Cleary AL (1997) Pre-mitotic nuclear migration in subsidiary mother cells ofTradescantia occurs in G1 of the cell cycle and requires F-actin. Cell Motil Cytoskeleton 36: 55–67
Kropf DL (1994) Cytoskeletal control of cell polarity in a plant zygote. Dev Biol 165: 361–371
Lutz DA, Hamaguchi Y, Inoue S (1988) Micromanipulation studies of the asymmetric positioning of the maturation spindle inCheatopterus sp. oocytes 1: anchorage of the spindle to the cortex and migration of a displaced spindle. Cell Motil Cytoskeleton 11: 83–96
Meyer Y, Abel WO (1975) Importance of the wall for cell division and in the activity of the cytoplasm in cultured tobacco protoplasts. Planta 123: 33–40
Mineyuki Y, Gunning BES (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
—, Palevitz BA (1990) Relationship between preprophase band organization, F-actin and the division site inAllium: fluorescence and morphometric studies on cytochalasin-treated cells. J Cell Sci 97: 283–295
—, Marc J, Palevitz BA (1988) Formation of the oblique spindle in dividing guard mother cells ofAllium. Protoplasma 147: 200–203
— — — (1989) Development of the preprophase band from random cytoplasmic microtubules in guard mother cells ofAllium cepa L. Planta 178: 291–296
—, Karahara I, Murata T, Giddings TH, Staehelin LA (2000) Fine structure of preprophase bands preserved by high pressure freezing. In: Robertson Symposium on plant cell biology, The Australian National University, Canberra, p 40
O'Brien TP (1983) The preprophase band of microtubules: does it block cleavage? Cytobios 37: 101–105
Oparka KJ (1994) Tansley Review no. 67. Plasmolysis: new insights into an old process. New Phytol 126: 571–591
Ôta T (1961) The role of cytoplasm in cytokinesis of plant cells. Cytologia 26: 428–447
Palevitz BA (1993) Morphological plasticity of the mitotic apparatus in plants and its developmental consequences. Plant Cell 5: 1001–1009
—, Hepler PK (1974a) The control of the plane of division during stomatal differentiation inAllium I: spindle reorientation. Chromosoma 46: 297–326
— —, (1974b) The control of the plane of division during stomatal differentiation inAllium II: drug studies. Chromosoma 46: 327–341
Pickett-Heaps JD, Gunning BES, Brown RC, Lemmon BE, Cleary AL (1999) The cytoplast concept in dividing plant cells: cytoplasmic domains and the evolution of spatially organized cell division. Am J Bot 86: 153–172
Roberts AW, Haigier CH (1989) Rise in chlorotetracycline fluorescence accompanies tracheary element differentiation in suspension cultures ofZinnia. Protoplasma 152: 37–45
Robinson DG, Cummins WR (1976) Golgi apparatus secretion in plasmolyzedPisum sativum L. Protoplasma 90: 369–379
Sinnott EW, Bloch R (1941) The relative position of cell walls in developing plant tissues. Am J Bot 28: 607–617
Smith LG (1999) Divide and conquer: cytokinesis in plant cells. Curr Opin Plant Biol 2: 447–453
Sonobe S (1990) Cytochalasin B enhances cytokinetic cleavage in miniprotoplasts isolated from cultured tobacco cells. Protoplasma 155: 239–242
Staehelin LA, Hepler PK (1996) Cytokinesis in higher plants. Cell 84: 821–824
Stebbins GL, Jain SK (1960) Developmental studies of cell differentiation in the epidermis of monocotyledons I:Allium, Rhoeo, andCommelina. Dev Biol 2: 409–426
Traas JA, Bellini C, Nacry P, Kronenberger P, Bouchez D, Caboche M (1995) Normal differentiation patterns in plants lacking microtubular preprophase bands. Nature 375: 676–677
Valster AH, Hepler PK (1997) Caffeine inhibition of cytokinesis: effect on the phragmoplast cytoskeleton in livingTradescantia stamen hair cells. Protoplasma 196: 155–166
White J, Strome S (1996) Cleavage plane specification inC. elegans: how to divide the spoils. Cell 84: 195–198
Wick SM (1991) The preprophase band. In: Lloyd CW (ed) The cytoskeletal basis of plant growth and form. Academic Press, London, pp 231–244
Wyatt SE, Carpita NC (1993) The plant cytoskeleton-cell-wall continuum. Trends Cell Biol 3: 413–417
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Dedicated to Professor Brian E. S. Gunning on the occasion of his 65th birthday
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Cleary, A.L. Plasma membrane-cell wall connections: Roles in mitosis and cytokinesis revealed by plasmolysis ofTradescantia virginiana leaf epidermal cells. Protoplasma 215, 21–34 (2001). https://doi.org/10.1007/BF01280301
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DOI: https://doi.org/10.1007/BF01280301