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Preprophasic microtubule systems and development of the mitotic spindle in hornworts (Bryophyta)

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Summary

Studies of monoplastidic mitosis in hornworts (Bryophyta) using transmission electron microscopy and indirect immunofluorescence staining of microtubules have revealed that two mutually perpendicular microtubule systems predict division polarity in preprophase. Events of cytoplasmic reorganization in preparation for division occur in the following order: migration of the single plastid to a position perpendicular to the division site, constriction of the plastid where its midpoint intersects the division site, development of an axial system of microtubules parallel to the elongating plastid isthmus, and appearance of an atypical preprophase band of microtubules (PPB). The PPB is asymmetrical with a tight band of microtubules on the side over the plastid isthmus and a broad band of widely spaced microtubules over the nucleus. The axial system contributes directly to development of the spindle. In prometaphase, the axial system separates at the equator and additional microtubule bundles project from polar regions, creating two opposing halfspindles. The PPB is still present during asymmetrical organization of the spindle and microtubules extending from the broad portion of the PPB to poles appear to be incorporated into the developing spindle. Dynamic changes in the microtubular cytoskeleton demonstrate (1) intimate relationship of plastid and nuclear division, (2) contribution of preprophase/prophase microtubule systems to spindle development in monoplastidic cells, and (3) dynamic reorientation of microtubules from one system to another.

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References

  • Apostolakos P, Galatis B (1985) Studies on the development of the air pores and air chambers ofMarchantia paleacea III. Microtubule organization in preprophase-prophase initial aperture cells-formation of incomplete preprophase microtubule bands. Protoplasma 128: 120–135

    Google Scholar 

  • Brown RC, Lemmon BE (1984) Plastid apportionment and preprophase microtubule bands in monoplastidic root meristem cells ofIsoetes andSelaginella. Protoplasma 123: 95–103

    Google Scholar 

  • — (1985 a) Preprophasic establishment of division polarity in monoplastidic mitosis of hornworts. Protoplasma 124: 175–183

    Google Scholar 

  • — (1985 b) Development of stomata inSelaginella. Division polarity and plastid movements. Am J Bot 72: 1914–1925

    Google Scholar 

  • — (1985 c) A cytoskeletal system predicts division plane in meiosis ofSelaginella. Protoplasma 127: 101–109

    Google Scholar 

  • — (1987 a) Division polarity, development and configuration of microtubule arrays in bryophyte meiosis I. Meiotic prophase to metaphase I. Protoplasma 137: 84–99

    Google Scholar 

  • — (1987 b) Division polarity, development and configuration of microtubule arrays in bryophyte meiosis II. Anaphase I to the tetrad. Protoplasma 138: 1–10

    Google Scholar 

  • Buchen B, Sievers A (1981) Sporogenesis and pollen grain formation. In:Kiermayer O (ed) Cytomorphogenesis in plants. Springer, Wien New York, pp 349–376

    Google Scholar 

  • Busby CH (1986) Development of the meiotic cytoskeleton in bryophytes. MS Thesis, Australian National University, Canberra

    Google Scholar 

  • Calarco-Gillam PD, Siebert MC, Hubble R, Mitchison T, Kirschner M (1983) Centrosome development in early mouse embryos as defined by an auto-antibody against pericentriolar material. Cell 35: 621–629

    PubMed  Google Scholar 

  • Clayton L, Black CM, Lloyd CW (1985) Microtubule nucleating sites in higher plant cells identified by an auto-antibody against pericentriolar material. J Cell Biol 101: 319–324

    Google Scholar 

  • Crandall-Stotler B (1980) Morphogenetic designs and a theory of bryophyte origins and divergence. Bioscience 30: 580–585

    Google Scholar 

  • Doonan JH, Cove DJ, Lloyd CW (1985) Immunofluorescence microscopy of microtubules in intact cell lineages in the moss,Phycomitrella patens I. Normal and CIPC-treated tip cells. J Cell Sci 75: 131–147

    PubMed  Google Scholar 

  • —,Cove DJ, Corke FMK, Lloyd CW (1987) Pre-prophase band of microtubules, absent from tip-growing moss filaments, arises in leafy shoots during transition to intercalary growth. Cell Motil Cytoskel 7: 138–153

    Google Scholar 

  • Dunlop DW (1949) Notes on the cytology of some lycopsids. Bull Torrey Bot Club 76: 266–277

    Google Scholar 

  • Euteneuer U, McIntosh JR (1980) Polarity of midbody and phragmoplast microtubules. J Cell Biol 87: 509–515

    PubMed  Google Scholar 

  • Fowke LC, Pickett-Heaps JD (1978) Electron microscope study of vegetative cell division in two species ofMarchantia. Can J Bot 56: 467–475

    Google Scholar 

  • Galatis B, Apostolakos P (1977) On the fine structure of differentiating mucilage papillae ofMarchantia. Can J Bot 55: 772–795

    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 New York, pp 229–292

    Google Scholar 

  • Lander CA (1935) The relation of the plastid to nuclear division inAnthoceros laevis. Am J Bot 22: 42–51

    Google Scholar 

  • Marchant HJ, Pickett-Heaps JD (1973) Mitosis and cytokinesis inColeochaete scutata. J Phycol 9: 461–471

    Google Scholar 

  • McIntosh JR (1981) Microtubule polarity and interaction in mitotic spindle function. In:Schweiger HG (ed) International cell biology 1980–1981. Springer, Berlin Heidelberg New York, pp 359–368

    Google Scholar 

  • —,Euteneuer U (1984) Tubulin hooks as probes for microtubule polarity: an analysis of the method and an evaluation of data on microtubule polarity in the mitotic spindle. J Cell Biol 98: 525–533

    PubMed  Google Scholar 

  • Mitchison T, Kirschner M (1984) Microtubule assembly nucleated by isolated centrosomes. Nature (London) 312: 232–236

    Google Scholar 

  • Mole-Bajer J, Baser AS (1968) Studies of selected endosperm cells with the light and electron microscope. The technique. Cellule 67: 257–265 + 5 pl

    Google Scholar 

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

    Google Scholar 

  • — (1974) Plant microtubules. In:Robards AW (ed) Dynamic aspects of plant ultrastructure. McGraw-Hill, London New York, pp 219–255

    Google Scholar 

  • —,Tippit DH, Cohn SA, Spurck TP (1986) Microtubule dynamics in the spindle. Theoretical aspects of assembly/disassembly reactionsin vivo. J Theor Biol 118: 153–169

    PubMed  Google Scholar 

  • Sack FD, Paollilo DJ (1985) Incomplete cytokinesis inFunaria stomata. Am J Bot 72: 1325–1333

    Google Scholar 

  • Schliwa M, van Blerkom J (1981) Structural interaction of cytoskeletal components. J Cell Biol 90: 222–235

    PubMed  Google Scholar 

  • Schmiedel G, Reiss H-D, Schnepf E (1981) Associations between membranes and microtubules during mitosis and cytokinesis in caulonema tip cells of the mossFunaria hygrometrica. Protoplasma 108: 173–190

    Google Scholar 

  • Schnepf E(1973) Mikrotubulus-Anordnung und -Umordnung, Wandbildung und Zellmorphogenese in jungenSphagnum-Blättchen. Protoplasma 78: 145–173

    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 

  • Steer MW (1984) Mitosis in Bryophytes. AdvBryol 2: 1–23 + 27 figs

    Google Scholar 

  • Telzer BR, Haimo LT (1981) Decoration of spindle microtubules with dynein: evidence for uniform polarity. J Cell Biol 89: 373–378

    PubMed  Google Scholar 

  • Wick SM (1985) Immunofluorescence microscopy of tubulin and microtubule arrays in plant cells. III. Transition between mitotic/ cytokinetic and interphase microtubule arrays. Cell Biol Int Rep 9: 357–371

    PubMed  Google Scholar 

  • —,Duniec J (1983) Immunofluorescence microscopy of tubulin and microtubule arrays in plant cells. I. Preprophase band development and concomitant appearance of nuclear envelope-as-sociated tubulin. J Cell Biol 97: 235–243

    Google Scholar 

  • — — (1984) Immunofluorescence microscopy of tubulin and microtubule arrays in plant cells. II. Transition between the preprophase band and the mitotic spindle. Protoplasma 122: 45–55

    Google Scholar 

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Brown, R.C., Lemmon, B.E. Preprophasic microtubule systems and development of the mitotic spindle in hornworts (Bryophyta). Protoplasma 143, 11–21 (1988). https://doi.org/10.1007/BF01282954

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