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Type: Article
Published: 2022-12-30
Page range: 75–84
Abstract views: 454
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Microtubule organization and plastid distribution during meiosis of Haplomitrium mnioides (Haplomitriopsida)

Graduate School of Integrated Sciences for Life, Hiroshima University, Kagamiyama 1-3-1, Higashi-Hiroshima 739-8526, Japan
microtubules GBM QMS meiosis sporogenesis plastids Haplomitrium

Abstract

The organization of microtubules and plastid distribution of the liverwort, Haplomitrium mnioides (Haplomitriopsida), was studied during the meiotic phase lasting for six months. In the late fall, the cytoplasm of early sporocytes forms four lobes of future spore domains before meiotic prophase. Microtubules align at the cytoplasmic cleavage furrow regions as girdling bands in the four-lobed sporocytes. Finally, the cleavage furrows are proximal to the nucleus positioned in the center of the sporocyte, and the girdling bands of the microtubule (GBM) disappear. Subsequently, the nucleus moves into one of the cytoplasmic lobes, and sporocytes pass the winter season at this stage. In early spring, the nucleus returns to the central position of the lobed cytoplasm, concurrent with plastid repositioning around the nucleus. Plastids are then distributed equally to each of the four lobes as a plastid cluster. Astral microtubules emanate from the plastid cluster in each spore domain and encage prophase nuclei as a quadripolar microtubule system (QMS). The QMS changes into a twisted spindle of metaphase I with broad poles, while spindles of metaphase II also emanate from the four plastid clusters. Cytokinesis is completed through the centrifugal cell plate formation in telophase II. The division axes of two successive nuclear divisions appear to be determined by plastid-based QMS, and the future site of cytokinesis is marked by cytoplasmic furrows associated with GBM. The phylogenetic distribution of GBM and QMS suggests that the meiotic system involving these structures is an ancestral trait of liverworts. Long-term dormancy in diploid sporocytes rather than haploid spores may represent transitional traits from charophycean green algae to land plants.

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References

  1. Bartholomew-Began S.E. (1991) A morphogenetic re-evaluation of Haplomitrium Nees (Hepatophyta). Bryophytorum Bibliotheca 41: 1–297.

  2. Brown, R.C. & Lemmon, B.E. (1987) Division polarity, development and configuration of microtubules arrays in bryophyte meiosis. I. Meiotic prophase to Metaphase I. Protoplasma 137: 84­99.  https://doi.org/10.1007/BF01281144

  3. Brown, R.C. & Lemmon, B.E. (1988) Sporogenesis in Bryophytes. Advances in Bryology 3: 159–223.

  4. Brown, R.C. & Lemmon, B.E. (1990) Sporogenesis in bryophytes. In: Blackmore, S. & Knox, R.B. (Eds.) Microspores, evolution and ontogeny. Academic Press, London, pp. 55–94.  https://doi.org/10.1016/B978-0-12-103458-0.50007-9

  5. Brown, R.C. & Lemmon, B.E. (1997) The quadripolar microtubule system in lower land plants. Journal of Plant Research 110: 93–106.  https://doi.org/10.1007/BF02506848

  6. Brown, R.C. & Lemmon, B.E. (2006) Polar organizers and girdling bands of microtubules are associated with γ-tubulin and act in establishment of meiotic quadripolarity in the hepatic Aneura pinguis (Bryophyta). Protoplasma 227: 77–85.  https://doi.org/10.1007/s00709-006-0148-4

  7. Brown, R.C. & Lemmon, B.E. (2009) Pre-meiotic bands and novel meiotic spindle ontogeny in quadrilobed sporocytes of leafy liverworts (Jungermannidae, Bryophyta). Protoplasma 237: 41.  https://doi.org/10.1007/s00709-009-0073-4

  8. Brown, R.C. & Lemmon, B.E. (2011) Spores before sporophytes: hypothesizing the origin of sporogenesis at the algal–plant transition. New Phytologist 190: 875–881.  https://doi.org/10.1111/j.1469-8137.2011.03709.x

  9. Brown, R.C., Lemmon, B.E. & Shimamura, M. (2010) Diversity in meiotic spindle origin and determination of cytokinetic planes in sporogenesis of complex thalloid liverworts (Marchantiopsida). Journal of Plant Research 123: 589–605.  https://doi.org/10.1007/s10265-009-0286-9

  10. Brown, R.C. & Lemmon, B.E. (2013) Sporogenesis in bryophytes: Patterns and diversity in meiosis. Botanical Review 79: 178–280.  https://doi.org/10.1007/s12229-012-9115-2

  11. Busby, C.H. & Gunning, B.E.S. (1988a) Establishment of plastid based quadripolarity in spore mother cells of the moss Funaria hygrometrica. Journal of Cell Science 91: 117–126.  https://doi.org/10.1242/jcs.91.1.117

  12. Busby, C.H. & Gunning, B.E.S. (1988b) Development of the quadripolar meiotic cytoskeleton in spore mother cells of the moss Funaria hygrometrica. Journal of Cell Science 91: 127–137.  https://doi.org/10.1242/jcs.91.1.127

  13. Carafa, A., Duckett, J.G. & Ligrone, R. (2003) Subterranean gametophytic axes in the primitive liverwort Haplomitrium harbour a unique type of endophytic association with aseptate fungi. New Phytologist 160: 185-197.  https://doi.org/10.1046/j.1469-8137.2003.00849.x

  14. Duckett, J.G. & Renzaglia, K.S. (1993) The reproductive biology of the liverwort Blasia pusilla L. Journal of Bryology 17: 541–552.  https://doi.org/10.1179/jbr.1993.17.4.541

  15. Field, KJ., Rimington, W.R, Bidartondo, M.I, Allinson, K.E, Beerling, D.J, Cameron, D.D, Duckett, J.G., Leake, J.R. & Pressel, S. (2015) First evidence of mutualism between ancient plant lineages (Haplomitriopsida liverworts) and Mucoromycotina fungi and its response to simulated Palaeozoic changes in atmospheric CO2. New Phytologist 205: 743–756.  https://doi.org/10.1111/nph.13024

  16. Forrest, L.L. & Crandall-Stotler, B.J. (2005) Progress towards a robust phylogeny for the liverworts, with particular focus on the simple thalloids. Journal of Hattori Botanical Laboratory 97: 127–159.

  17. Forrest, L.L., Davis, E.C., Long, D.G., Crandall-Stotler, B.J., Clark, A. & Hollingsworth, M.L. (2006) Unraveling the evolutionary history of the liverworts (Marchantiophyta)—multiple taxa, genomes, and analyses. Bryologist 109: 303–334.  https://doi.org/10.1639/0007-2745(2006)109[303:UTEHOT]2.0.CO;2

  18. Gottsche, C.M., Lindenberg, J.B.W. & Nees von Esenbeck, C.G.D. (1846) Synopsis Hepaticarum, fasc. 4. Meissner, Hamburg, pp. 465–624.

  19. Graham, L.E. (1993) Origin of land plants. John Wiley & Sons, New York, 287 pp.

  20. Hunt, T. (1989) Embryology. Under arrest in the cell cycle. Nature 342: 483–484.  https://doi.org/10.1038/342483a0

  21. Kremer, C. & Drinnan, A. (2003) Secondary wall formation in elaters of liverworts and the hornwort Megaceros. International Journal of Plant Sciences 164: 823–824.  https://doi.org/10.1086/378651

  22. Lindberg, S.O. (1874) Manipulus muscorum secundus. Notiser ur Sällskapets pro Fauna et Flora Fennica Förhandlingar 13: 351­417.

  23. Linnaeus C. (1753) Species plantarum 2. Impensis Laurentii Salvii, Stockholm, Sweden, pp. 561–1200.

  24. Masui Y., & Markert, C.L. (1971) Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes. Journal of Experimental Zoology 177: 129–145.  https://doi.org/10.1002/jez.1401770202

  25. Nees von Esenbeck, C.G.D. (1833) Naturgeschichte der Europäischen Lebermoose 1. August Rücker, Breslau, 348 pp.

  26. Neidhart, H.V. (1979) Comparative studies of sporogenesis in Bryophytes. In: Clarke, G.C.S. & Duckett, J.G. (Eds.) Bryophyte Systematics. Academic Press, London, pp. 251-280.

  27. Nurse, P. (1990) Universal control mechanism regulating onset of M-phase. Nature 344: 503–508.  https://doi.org/10.1038/344503a0

  28. Renzaglia, K.S., Brown, R.C., Lemmon, B.E., Duckett, J.G. & Lignone, R. (1994) Occurrence and phylogenetic significance of monoplastidic meiosis in liverworts. Canadian Journal of Botany 72: 65–72. https://doi.org/10.1139/b94-009

  29. Schuster, R.M. (1963) Studies on antipodal Hepaticae. I. Annotated keys to the genera of antipodal Hepaticae with special reference to New Zealand and Tasmania. Journal of the Hattori Botanical Laboratory 26: 185­309.

  30. Schuster, R.M. (1983) Evolution, phylogeny and classification of the Hepaticae. In: Schuster, R.M. (Ed.) New Manual of Bryology: The Hattori Botanical Laboratory. Nichinan, Japan, pp. 892–1070.

  31. Shimamura, M., Deguchi, H. & Mineyuki, Y. (2003) A review of the occurrence of monoplastidic meiosis in liverworts. The Journal of of the Hattori Botanical Laboratory 94: 179–186.

  32. Shimamura, M., Itouga, M. & Tsubota, H. (2012) Evolution of apolar sporocytes in marchantialean liverworts: implications from molecular phylogeny. Journal of Plant Research 125: 197–206.  https://doi.org/10.1007/s10265-011-0425-y

  33. Shimamura, M. (2015) Whole-mount immunofluorescence staining of plant cells and tissues. In: Yeung, E. (Ed.) Plant Microtechniques and Protocols. Springer, Switzerland, pp. 181–196. https://doi.org/10.1007/978-3-319-19944-3_11

  34. Shimamura, M., Brown, R.C., Lemmon, B.E., Akashi, T., Mizuno, K., Nishihara, N., Tomizawa, K.-I., Yoshimoto, K., Deguchi, H., Hosoya, H., Horio, T. & Mineyuki, Y. (2004) γ-Tubulin in basal land plants: characterization, localization and implication in the evolution of acentriolar microtubule organizing centers. Plant Cell 16: 45-59.  https://doi.org/10.1105/tpc.016501

  35. Yamamoto, K., Shimamura, M., Degawa, Y. & Yamada, A (2019) Dual colonization of Mucoromycotina and Glomeromycotina fungi in the basal liverwort, Haplomitrium mnioides (Haplomitriopsida). (2019). Journal of Plant Research 132: 777–788.  https://doi.org/10.1007/s10265-019-01145-3