Summary
Changes in the pattern of microtubules during the cell cycle of the hepaticReboulia hemisphaerica (Bryophyta) were studied by indirect immunofluorescence using conventional and confocal laser scanning microscopy (CLSM). The first indication that a cell is preparing for division is fusiform shaping of the nucleus accompanied by the appearance of well-defined polar organizers (POs) at the future spindle poles. Microtubules emanating from the POs ensheath the nucleus and eventually develop into the half-spindles of mitosis. Some of the microtubules from each PO pass tangential to the nucleus and interact in the region of the future mitotic equator. A preprophase band (PPB) forms in this region later in prophase and coexists with the prophase spindle. Thus, the plane of division appears to be determined by interaction of opposing arrays of microtubules emanating from POs. Prometaphase is marked by disappearance of the POs, loss of astral microtubules, and conversion of the fusiform spindle of prophase to a truncated, barrel-shaped spindle more typical of higher plants. Restoration of cortical microtubules in daughter cell occurs on the cell side distal to the new cell plate, but nucleation of microtubules is associated with the nuclear envelope and not with organized POs. At the next division POs appear at opposite poles of preprophase nuclei with no evidence of division and migration that is characteristic of cells with centriolar centrosomes. These data lend additional support for the view that mitosis in hepatics is transitional between green algae and higher plants.
Similar content being viewed by others
Abbreviations
- AMS:
-
axial microtubule system
- CLSM:
-
confocal laser scanning microscopy
- MTOC:
-
microtubule organizing center
- PO:
-
polar organizer
- PPB:
-
preprophase band of microtubules
- QMS:
-
quadripolar microtubule system
- TEM:
-
transmission electron microscopy
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
Bakhuizen R, van Spronsen PC, Sluiman-den Hertog FAJ, Venverloo CJ, Goosen-de Roo L (1985) Nuclear envelope radiating microtubules in plant cells during interphase mitosis transition. Protoplasma 128: 43–51
Brown RC, Lemmon BE (1982) Ultrastructure of meiosis in the mossRhynchostegium serrulatum I. Prophasic microtubules and spindle dynamics. Protoplasma 110: 23–33
— — (1987 a) Division polarity, development and configuration of microtubule arrays in bryophyte meiosis I. Meiotic prophase to metaphase I. Protoplasma 137: 84–99
— — (1987 b) Division polarity, development and configuration of microtubule arrays in bryophyte meiosis II. Anaphase I to the tetrad. Protoplasma 138: 1–10
— — (1988 a) Preprophasic microtubule systems and development of the mitotic spindle in hornworts (Bryophyta). Protoplasma 143: 11–21
— — (1988 b) Microtubules associated with simultaneous cytokinesis of coenocytic microsporocytes. Amer J Bot 75: 1848–1856
— — (1989) Minispindles and cytoplasmic domains in microsporogenesis of orchids. Protoplasma 148: 26–32
— — (1990) Monoplastidic cell division in lower land plants. Amer J Bot 77: 559–571
Busby CH, Gunning BES (1988 a) Establishment of plastid-based quadripolarity in spore mother cells of the mossFunaria hygrometrica. J Cell Sci 91: 117–126
— — (1988 b) Development of the quadripolar meiotic cytoskeleton in spore mother cells of the mossFunaria hygrometrica. J Cell Sci 91: 127–137
Cho SO, Wick SM (1989) Microtubule orientation during stomatal differentiation in grasses. J Cell Sci 92: 581–594
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
Cleary AL, Hardham AR (1989) Microtubule organization during development of stomatal complexes ofLolium rigidum. Protoplasma 149: 67–81
Doonan JH, Duckett JG (1988) The bryophyte cytoskeleton: experimental and immunofluorescence studies of morphogenesis. Adv Bryol 3: 1–31
—, 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 Cytoskeleton 7: 138–153
—, Lloyd CW, Duckett JG (1986) Anti-tubulin antibodies locate the blepharoplast during spermatogenesis in the fernPlatyzoma microphyllum R. Br.: a correlated immunofluorescence and electronmicroscopic study. J Cell Sci 81: 243–265
Duckett JG (1986) Ultrastructure in bryophyte systematics and evolution: an evaluation. J Bryol 14: 25–42
Farmer JB (1895) On spore-formation and nuclear division in the Hepaticae. Ann Bot 9: 470–523 + 3 plates
—, Reeves J (1894) On the occurrence of centrospheres inPellia epiphylla Nees. Ann Bot 8: 219–224 + 1 plate
Fowke LC, Pickett-Heaps JD (1978) Electron microscope study of vegetative cell division in two species ofMarchantia. Canad J Bot 56: 467–475
Galatis B, Apostolakos P (1977) On the fine structure of differentiating mucilage papillae ofMarchantia. Canad J Bot 55: 772–795
Gifford EM, Foster AS (1989) Morphology and evolution of vascular plants. Freeman, New York
Graham LE (1984)Coleochaete and the origin of land plants. Amer J Bot 71: 603–608
Gunning BES (1982) The cytokinetic apparatus: its development and spatial regulation. In: Lloyd CW (ed) Cytoskeleton in plant growth and development. Academic Press, London, pp 229–292
Mullinax JB, Palevitz BA (1989) Microtubule reorganization accompanying preprophase band formation in guard mother cells ofAvena sativa L. Protoplasma 149: 89–94
Marc J, Gunning BES (1986) Immunofluorescent localization of cytoskeletal tubulin and actin during spermatogenesis inPteridium aquilinum (L.) Kuhn. Protoplasma 134: 163–177
Marchant HJ, Pickett-Heaps JD (1973) Mitosis and cytokinesis inColeochaete scutata. J Phycol 9: 461–471
Robbins RR (1984) Origin and behavior of bicentriolar centrosomes in the bryophyteRiella americana. Protoplasma 121: 114–119
Schnepf E (1982) Morphogenesis in moss protonemata. In: Lloyd CW (ed) Cytoskeleton in plant growth and development. Academic Press, London, pp 321–344
— (1984) Pre- and postmitotic reorientation of microtubule arrays in youngSphagnum leaflets: traditional stages and initiation sites. Protoplasma 120: 100–112
Schmiedel G, Reiss HD, Schnepf E (1981) Associations between membranes and microtubules during mitosis and cytokinesis in caulonema tip cells of the mossFunaria hygrometrica. Protoplasma 108: 173–190
Steer MW (1984) Mitosis in bryophytes. Adv Bryol 2: 1–23 + 27 figures
Van Hook JM (1900) Notes on the division of the cell and nucleus in liverworts. Bot Gaz 30: 394–399
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
—, Duniec J (1983) Immunofluorescence microscopy of tubulin and microtubule arrays in plant cells. I. Pre-prophase band development and concomitant appearance of nuclear envelope-associated tubulin. J Cell Biol 97: 235–243
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Brown, R.C., Lemmon, B.E. Polar organizers mark division axis prior to preprophase band formation in mitosis of the hepaticReboulia hemisphaerica (Bryophyta). Protoplasma 156, 74–81 (1990). https://doi.org/10.1007/BF01666508
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01666508