Journal of Plant Research

, Volume 110, Issue 1, pp 93–106 | Cite as

The quadripolar microtubule system in lower land plants

  • Roy C. Brown
  • Betty E. Lemmon
Invited Article


The quadripolar microtubule system (QMS) is a complex array that is associated with predivision establishment of quadripolarity in sporocytes of lower plants (bryophytes and lycopsids). The QMS unerringly predicts the polarity of the two meiotic divisions and plays a central role in development of both the mitotic apparatus (MA) and cytokinetic apparatus (CA) which together accomplish quadripartitioning of the sporocyte into four haploid spores. The QMS is typically, but not exclusively, associated with monoplastidy and precocious quadrilobing of the cytoplasm. In early meiotic prophase the single plastid divides and the resultant plastids migrate so that either the tips of two plastids or the four plastids resulting from a second division are located in the future spore domains. Microtubules that emanate from the plastid tips or from individual plastids in the spore domains interact in the future planes of cytokinesis and give rise to the QMS. The QMS, which encages the prophase nucleus, consists of at least four and usually six (when spore domains are in tetrahedral arrangement) bipolar spindle-like arrays of microtubules presumably with minus ends at plastids in spore domains and plus ends interacting in the future plane of cytokinesis. Each of the six arrays is essentially like the single axial microtubule system (AMS) that intersects the division site and is transformed into the spindle in monoplastidic mitosis in hornworts. As comparative data accumulate, it appears that the AMS is not unique to monoplastidic cell division but instead represents a basic microtubule arrangement that survives as spindle and phragmoplast in cell division of higher plants.

Key words

Cytokinesis Evolution Meiosis Microtubules Mitosis Sporogenesis 



axial microtubule system


cytokinetic apparatus


confocal laser scanning microscopy


mitotic apparatus


microtubule converging center


microtubule organizing center


polar organizer


preprophase band of microtubules


quadripolar microtubule system


transmission electron microscopy


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  1. Apostolakos, P. andGalatis, 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. Protoplasma128: 120–135.CrossRefGoogle Scholar
  2. Brown, R.C. andLemmon, B.E. 1982a. Ultrastructure of meiosis in the mossRhynchostegium serrulatum I. Prophasic microtubules and spindle dynamics. Protoplasma110: 23–33.CrossRefGoogle Scholar
  3. Brown, R.C. andLemmon, B.E. 1982b. Ultrastructure of sporogenesis in the moss,Amblystegium riparium I. Meiosis and cytokinesis. Amer. J. Bot.69: 1096–1107.CrossRefGoogle Scholar
  4. Brown, R.C. andLemmon, B.E. 1984. Plastid apportionment and preprophase microtubule bands in monoplastidic root meristem cells ofIsoetes andSelaginella. Protoplasma123: 95–103.CrossRefGoogle Scholar
  5. Brown, R.C. andLemmon, B.E. 1985a. Development of stomata inSelaginella: division polarity and plastid movements. Amer. J. Bot.72: 1914–1925.CrossRefGoogle Scholar
  6. Brown, R.C. andLemmon, B.E. 1985b. A cytoskeletal system predicts division plane in meiosis ofSelaginella. Protoplasma127: 101–109.CrossRefGoogle Scholar
  7. Brown, R.C. andLemmon, B.E. 1987a. Division polarity, development and configuration of microtubule arrays in bryophyte meiosis I. Meiotic prophase to metaphase I. Protoplasma137: 84–99.CrossRefGoogle Scholar
  8. Brown, R.C. andLemmon, B.E. 1987b. Division polarity, development and configuration of microtubule arrays in bryophyte meiosis II. Anaphase I to the tetrad. Protoplasma138: 1–10.CrossRefGoogle Scholar
  9. Brown, R.C. andLemmon, B.E. 1988a. Preprophasic microtubule systems and development of the mitotic spindle in hornworts (Bryophyta). Protoplasma143: 11–21.CrossRefGoogle Scholar
  10. Brown, R.C. andLemmon, B.E. 1988b. Cytokinesis occurs at boundaries of domains delimited by nuclear-based microtubules in sporocytes ofConocephalum conicum (Bryophyta). Cell Motil. Cytoskel.11: 139–146.CrossRefGoogle Scholar
  11. Brown, R.C. andLemmon, B.E. 1989a. Morphogenetic plastid migration and microtubule organization during megasporogenesis inIsoetes. Protoplasma152: 136–147.CrossRefGoogle Scholar
  12. Brown, R.C. andLemmon, B.E. 1989b. Minispindles and cytoplasmic domains in microsporogenesis of orchids. Protoplasma148: 26–32.CrossRefGoogle Scholar
  13. Brown, R.C. andLemmon, B.E. 1990a. Sporogenesis in bryophytes.In S. Blackmore and R.V. Knox, eds., Microspores Evolution and Ontogeny, Academic Press, London, pp. 55–94.Google Scholar
  14. Brown, R.C. andLemmon, B.E. 1990b. Monoplastidic cell division in lower land plants. Amer. J. Bot.77: 559–571.CrossRefGoogle Scholar
  15. Brown, R.C. andLemmon, B.E. 1990c. The quadripolar microtubule system and meiotic spindle ontogeny in hornworts (Bryophyta: Anthocerotae). Amer. J. Bot.77: 1482–1490.CrossRefGoogle Scholar
  16. Brown, R.C. andLemmon, B.E. 1990d. Polar organizers mark division axis prior to preprophase band formation in mitosis of the hepaticReboulia hemispherica (Bryophyta). Protoplasma156: 74–81.CrossRefGoogle Scholar
  17. Brown, R.C. andLemmon, B.E. 1991a. Plastid polarity and meiotic spindle development in microsporogenesis ofSelaginella. Protoplasma161: 168–180.CrossRefGoogle Scholar
  18. Brown, R.C. andLemmon, B.E. 1991b. The cytokinetic apparatus in meiosis: control of division plane in the absence of a preprophase band of microtubules.In C. Lloyd ed. The Cytoskeletal Basis of Plant Growth and Form, Academic Press, London, pp. 259–273.Google Scholar
  19. Brown, R.C. andLemmon, B.E. 1992a. Polar organizers in monoplastidic mitosis of hepatics (Bryophyta). Cell Motil. Cytoskel.22: 72–77.CrossRefGoogle Scholar
  20. Brown, R.C. andLemmon, B.E. 1992b. Cytoplasmic domain: a model for spatial control of cytokinesis in reproductive cells of plants. EMSA Bull.22: 48–53.Google Scholar
  21. Brown, R.C. andLemmon, B.E. 1993. Diversity of cell division in simple land plants holds clues to evolution of the mitotic and cytokinetic apparatus in higher plants. Mem. Torrey Bot. Club25: 45–62.Google Scholar
  22. Brown, R.C., Lemmon, B.E. andCarothers, Z.B. 1982. Spore wall development inSphagnum lescurii. Can. J. Bot.60: 2394–2409.Google Scholar
  23. Brown, R.C., Lemmon, B.E. andGraham, L.E. 1994. Morphogenetic plastid migration and microtubule arrays in mitosis and cytokinesis in the green algaColeochaete orbicularis. Amer. J. Bot.81: 127–133.CrossRefGoogle Scholar
  24. Burr, F.A. 1969. Reduction in chloroplast number during gametophyte regeneration inMegaceros flagellaris. Bryologist72: 200–209.CrossRefGoogle Scholar
  25. Busby, C.H. andGunning, B.E.S. 1988a. Establishment of plastid-based quadripolarity in spore mother cells of the mossFunaria hygrometrica. J. Cell Sci.91: 117–126.Google Scholar
  26. Busby, C.H. andGunning, B.E.S. 1988b. Development of the quadripolar meiotic cytoskeleton in spore mother cells of the mossFunaria hygrometrica. J. Cell. Sci.91: 127–137.Google Scholar
  27. Busby, C.H. andGunning, B.E.S. 1989. Development of the quadripolar meiotic apparatus inFunaria spore mother cells: analysis by means of anti-microtubule drug treatments. J. Cell. Sci.93: 267–277.Google Scholar
  28. Cleary, A.L., Brown, R.C. andLemmon, B.E. 1992a. Establishment of division plane and mitosis in monoplastidic guard cells ofSelaginella. Cell Motil. Cytoskel.23: 89–101.CrossRefGoogle Scholar
  29. Cleary, A.L., Brown, R.C. andLemmon, B.E. 1992b. Microtubule arrays during mitosis in monoplastidic root tip cells ofIsoetes. Protoplasma167: 123–133.CrossRefGoogle Scholar
  30. Crandall-Stoler, B. 1986. Morphogenesis, developmental anatomy and bryophyte phylogenetics: contraindications of monophyly. J. Bryol.14: 1–23.Google Scholar
  31. Dunlop, D.W. 1949. Notes on the cytology of some lycopsids. Bull. Torrey Bot. Club76: 266–277.CrossRefGoogle Scholar
  32. Fowke, L.C. andPickett-Heaps, J.D. 1978. Electron microscope study of vegetative cell division in two species ofMarchantia. Can. J. Bot.56: 467–475.CrossRefGoogle Scholar
  33. Gambardella, R., Duckett, J.G., Alfano, F., Gargiulo, M. andSquillacioti, C. 1993. Studies on the sporogenous lineage in the mossTimmiella barbuloides VII. The microtubule arrays at meiosis. Bot. Acta106: 350–355.Google Scholar
  34. Graham, L.E., Delwiche, C.F. andMishler, B.D. 1991. Phylogenetic connections between the ‘green algae’ and the ‘bryophytes’. Adv. Bryol.4: 213–244.Google Scholar
  35. Heald, R., Tournebize, R., Blank, T., Sandaltzopoulos, R., Becker, P., Hyman, A. andKarsenti, E. 1996. Self-organization of microtubules into bipolar spindles around artificial chromosomes inXenopus egg extracts. Nature382: 420–425.PubMedCrossRefGoogle Scholar
  36. Liu, B. andPalevitz, B.A. 1991. Kinetochore fiber formation in dividing generative cells ofTradescantia. Kinetochore reorientation associated with the transition between lateral microtubule interactions and end-on kinetochore fibers. J. Cell. Sci.98: 475–482.Google Scholar
  37. Lokhorst, G.M., Sluiman, H.J. andStar, W. 1988. The ultrastructure of mitosis and cytokinesis in the sarcinoidChlorokybus atmosphyticus (Chlorophyta, Charophyceae) revealed by rapid freeze fixation and freeze substitution. J. Phycol.24: 237–248.Google Scholar
  38. Mazia, D. 1984. Centrosomes and the mitotic poles. Exp. Cell. Res.153: 1–15.PubMedCrossRefGoogle Scholar
  39. McIntosh, K., Pickett-Heaps, J.D. andGunning, B.E.S. 1995. Cytokinesis inSpirogyra: integration of cleavage and cell-plate formation. Int. J. Plant. Sci.156: 1–8.CrossRefGoogle Scholar
  40. Palevitz, B.A. 1993. Morphological plasticity of the mitotic apparatus in plants and its developmental consequences. Plant Cell5: 1001–1009.PubMedCrossRefGoogle Scholar
  41. Pickett-Heaps, J.D. 1969. The evolution of the mitotic apparatus: an attempt at comparative ultrastructural cytology in dividing plant cells. Cytobios1: 257–280.Google Scholar
  42. Proskauer, J. 1962. OnTakakia, especially its mucilage hairs. J. Hattori Bot. Lab.25: 217–223.Google Scholar
  43. Pryer, K.M., Smith, A.R. andSkog, J.E. 1995. Phylogenetic relationships of extant ferns based on evidence from morphology andrbcL sequences. Amer. Fern. J.85: 205–282.CrossRefGoogle Scholar
  44. Renzaglia, K.S., Brown, R.C., Lemmon, B.E., Duckett, J.G. andLigrone, R. 1994. Occurrence and phylogenetic significance of monoplastidic meiosis in liverworts. Can. J. Bot.72: 65–72.Google Scholar
  45. Segaar, P.J. 1991. The cytokinetic apparatus, the basal body complex, and the spatio-temporal organization of the microtubular cytoskeleton in the cell cycle of green algae. Ph. D. Dissertation, Rijksuniversiteit te Leiden, 301 pp.Google Scholar
  46. Segaar, P.J., Gerrritsen, A.F. andDe Bakker, M.A.G. 1989. The cytokinetic apparatus during sporulation in the unicellular green flagellateGleomonas kupfferi: The phycoplast as a spatio-temporal differentiation of the cortical microtubule array that organizes cytokinesis. Nova Hedw.49: 1–23.Google Scholar
  47. Smirnova, E.A. andBajer, A.S. 1994. Microtubule converging centers and reorganization of the interphase cytoskeleton and the mitotic spindle in higher plantHaemanthus. Cell Motill Cytoskel.27: 219–233.CrossRefGoogle Scholar
  48. Smith, D.K. 1990. Sporophyte ofTakakia discovered. The Bryological Times57/58: 1–4.Google Scholar
  49. Spurck, T. andPickett-Heaps, J.D. 1987. On the mechanism of anaphase A: evidence that ATP is needed for microtubule disassembly and not generation of polewards force. J. Cell Biol.105: 1691–1705.PubMedCrossRefGoogle Scholar
  50. Steer, M.W. 1984. Mitosis in bryophytes. Adv. Bryol.2: 1−23+27 figures.Google Scholar
  51. Takamiya, M., Watanabe, M. andOno, K. 1996. Biosystematic studies on the genusIsoetes (Isoetaceae) in Japan. II. Meiotic behavior and reproductive mode of each cytotype. Amer. J. Bot.83: 1309–1322.CrossRefGoogle Scholar
  52. Uehara, K. andKurita, S. 1991. Ultrastructural study on spore wall morphogenesis inLycopodium clavatum (Lycopodiaceae). Amer. J. Bot.78: 24–36.CrossRefGoogle Scholar

Copyright information

© The Botanical Society of Japan 1997

Authors and Affiliations

  1. 1.Department of BiologyUniversity of Southwestern LouisianaLafayetteUSA

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