DOI QR코드

DOI QR Code

Cell Division in the Absence of Mitosis: The Unusual Case of the Fucoid Ascophyllum nodosum (L.) Le Jolis (Phaeophyceae)

  • Garbary, David J. (Department of Biology, St. Francis Xavier University) ;
  • Lawson, Greg (Department of Biology, St. Francis Xavier University) ;
  • Clement, Kelly (Department of Biology, St. Francis Xavier University) ;
  • Galway, Moira E. (Department of Biology, St. Francis Xavier University)
  • 발행 : 2009.12.01

초록

Fluorescence and electron microscopy were used to examine epidermal shedding in the fucoid alga, Ascophyllum nodosum. Mature meristoderm cells are ca. 50-100 x 30-40 ${\mu}m$ and highly polarized, with a single nucleus and chloroplasts near the base of the cell. Nuclei in these cells undergo mitosis when they are dividing to form a new cortical cell towards the middle of the frond, or anticlinal divisions as part of frond elongation. However, cytokinesis also occurs regularly in these cells when a new periclinal wall is deposited at about 30% of the cell length from the apical end. The newly formed distal cells are anucleate and without chloroplasts. Following cytokinesis the tangential walls then break at the thinnest point. The whole process is synchronous in adjoining epidermal cells across large areas of the frond surface, and this layer dehisces from the thallus. This is the only known plant or algal system in which cytokinesis regularly occurs in the absence of mitosis. We consider this process a novel form of programmed cell death.

키워드

참고문헌

  1. Bisgrove S.R., Henderson D.C. and Kropf D.L. 2003. Asymmetric division in fucoid zygotes is positioned by telophase nuclei. Plant Cell 15: 854-862 https://doi.org/10.1105/tpc.009415
  2. Bisgrove S.R. and Kropf D.L. 2004. Cytokinesis in brown algae: studies of asymmetric division in fucoid zygotes. Protoplasma 223: 163-173 https://doi.org/10.1007/s00709-004-0038-6
  3. Bittner L., Payri C.E., Couloux A., Cruaud C., de Reviers B. and Rousseau F. 2008. Molecular phylogeny of the Dictyotales and their position within the Phaeophyceae, based on nuclear, plastid and mitochondrial DNA sequence data. Mol. Phylogenet. Evol. 49: 211-226 https://doi.org/10.1016/j.ympev.2008.06.018
  4. Carlile M.J., Watkinson S.C. and Gooday G.W. 2001. The Fungi. 2nd ed. Academic Press, San Diego, 588 pp
  5. Deckert R.J. and Garbary D.J. 2005a. Ascophyllum and its symbionts: VI. Microscopic characterization of the Ascophyllum nodosum (Phaeophyceae), Mycophycias ascophylli (Ascomycetes) symbiotum. Algae 20: 225-232 https://doi.org/10.4490/ALGAE.2005.20.3.225
  6. Deckert R.J. and Garbary D.J. 2005b. Ascophyllum and its symbionts: VIII. Interactions among Ascophyllum nodosum (Phaeophyceae), Mycophycias ascophylli (Ascomycetes) and Elachista fucicola (Phaeophyceae). Algae 20: 363-368 https://doi.org/10.4490/ALGAE.2005.20.4.363
  7. De Veylder L., Beeckman T. and Inze D. 2007. The ins and outs of the plant cell cycle. Nature Rev. Mol. Cell Biol. 8: 655-665 https://doi.org/10.1038/nrm2227
  8. Dolan L., Janmaat K., Willemsen V., Linstead P., Poethig S., Roberts K. and Scheres B. 1993. Cellular organisation of the Arabidopsis thaliana root. Development 119: 71-84
  9. Driouich A., Durand C. and Vicre-Gibouin M. 2007. Formation and separation of root border cells. Trends Plant Sci. 12: 14-19 https://doi.org/10.1016/j.tplants.2006.11.003
  10. Filion-Myklebust C. and Norton T.A. 1981. Epidermis shedding in the brown seaweed Ascophyllum nodosum (L.) Le Jolis and its ecological significance. Mar. Biol. Lett. 2: 45-51
  11. Fritsch F.E. 1945. Observations on the anatomical structure of the Fucales. I. New Phytol. 44: 1-16 https://doi.org/10.1111/j.1469-8137.1945.tb05015.x
  12. Fulka J. Jr., Loi P., Fulka H., Ptak G. and Nagai T. 2004. Nucleus transfer in mammals: noninvasive approaches for the preparation of cytoplasts. Trends Biotechnol. 22: 279-283 https://doi.org/10.1016/j.tibtech.2004.04.002
  13. Galway M.E., Hyde G.J. and Hardham A.R. 1994. Capacity for microtubule reorganization and cell wall synthesis in cytoplasts of the green alga Mougeotia. Protoplasma 178: 11-17 https://doi.org/10.1007/BF01404116
  14. Garbary D.J. and Gautam A. 1989. The Ascophyllum, Polysiphonia, Mycosphaerella symbiosis: I. Population ecology of Mycosphaerella from Nova Scotia. Bot. Mar. 32: 181-186 https://doi.org/10.1515/botm.1989.32.2.181
  15. Garbary D.J. and Tam C. 1989. Blidingia minima var. stolonifera var. nov. (Ulvales, Chlorophyta) from British Columbia: systematics, life history and morphogenesis. Nord. J. Bot. 9: 321-328 https://doi.org/10.1111/j.1756-1051.1989.tb01006.x
  16. Garbary D.J. and Belliveau D.J. 1990. Diffuse growth, a new pattern of cell wall deposition for the Rhodophyta. Phycologia 29: 98-102 https://doi.org/10.2216/i0031-8884-29-1-98.1
  17. Garbary D.J. and London F.J. 1995. The Ascophyllum / Polysiphonia / Mycosphaerella symbiosis: V. Fungal infection protect A. nodosum from desiccation. Bot. Mar. 38: 529-533 https://doi.org/10.1515/botm.1995.38.1-6.529
  18. Garbary D.J. and MacDonald K.A. 1995. The Ascophyllum / Polysiphonia / Mycosphaerella symbiosis: IV. Mutualism in the Ascophyllum / Mycosphaerella symbiosis. Bot. Mar. 38: 221-225 https://doi.org/10.1515/botm.1995.38.1-6.221
  19. Garbary D.J. and McDonald A.R. 1996. Actin rings in cytokinesis of apical cells in red algae. Can. J. Bot. 74: 971-974 https://doi.org/10.1139/b96-121
  20. Garbary D.J. and Clarke B. 2001. Apoptosis in trichoblast development in Polysiphonia harveyi (Rhodophyta). Phycologia 40: 324-329 https://doi.org/10.2216/i0031-8884-40-4-324.1
  21. Garbary D.J. and Deckert R.J. 2001. Three part harmony n Ascophyllum and its symbionts. In: Seckbach J. (ed.), Symbiosis: Mechanisms and Model Systems. Kluwer, Dortrecht. pp. 309-321
  22. Garbary D.J. and Clarke B. 2002. Intraplant variation in nuclear DNA content in Laminaria saccharina and Alaria esculenta (Phaeophyceae). Bot. Mar. 45: 211-216 https://doi.org/10.1515/BOT.2002.020
  23. Garbary D.J., Deckert R.J. and Hubbard C.B. 2005. Ascophyllum and its symbionts: VII. Three-way interactions among Ascophyllum nodosum (Phaeophyceae), Mycophycias ascophylli (Ascomycetes) and Vertebrata lanosa (Rhodophyta). Algae 20: 353-361 https://doi.org/10.4490/ALGAE.2005.20.4.353
  24. Graham L.E. and Wilcox L.W. 2000. Algae. Prentice-Hall, Upper Saddle River, New Jersey, 640 pp
  25. Guiry M.D. 1990. Sporangia and spores. In: Cole K.M. and Sheath R.G. (eds), Biology of the Red Algae. Cambridge University Press, Cambridge. pp. 347-376
  26. Gunawardena A.H.L.A.N. 2008. Programmed cell death and tissue remodeling in plants. J. Exp. Bot. 59: 445-451 https://doi.org/10.1093/jxb/erm189
  27. Hamamoto L., Hawes M.C. and Rost T.L. 2006. The production and release of living root cap border cells is a function of root apical meristem type in dicotyledonous angiosperm plants. Ann. Bot. 97: 917-923 https://doi.org/10.1093/aob/mcj602
  28. Hatzold J. and Conradt B. 2008. Control of apoptosis by asymmetric cell division. PLoS Biol. 6: e84 https://doi.org/10.1371/journal.pbio.0060084
  29. Hawes M.C., Brigham L.A., Wen F., Woo H.H. and Zhu Y. 1998. Function of root border cells in plant health: pioneers in the rhizosphere. Annu. Rev. Phytopathol. 36: 311-327 https://doi.org/10.1146/annurev.phyto.36.1.311
  30. Kapraun D.F. and Boone P.W. 1987. Karyological studies of three species of Scytosiphonaceae (Phaeophyta) from coastal North Carolina. J. Phycol. 23: 318-322 https://doi.org/10.1111/j.1529-8817.1987.tb04140.x
  31. Katsaros C., Galatis B. and Mitrakos K. 1983. Fine structural studies on the interphase and dividing apical cells of Sphacelaria tribuloides (Phaeophyta). J. Phycol. 19: 16-30 https://doi.org/10.1111/j.0022-3646.1983.00016.x
  32. Katsaros C., Karyophyllis D. and Galatis B. 2006. Cytoskeleton and morphogenesis in brown algae. Ann. Bot. 97: 679-693 https://doi.org/10.1093/aob/mcl023
  33. Keats D.W., Knight M.A. and Pueschel C.M. 1997. Antifouling effects of epithallial shedding in three crustose coralline algae (Rhodophyta, Corallinales) on a coral reef. J. Exp. Mar. Biol. Ecol. 213: 281-293 https://doi.org/10.1016/S0022-0981(96)02771-2
  34. Kohlmeyer J. and Kohlmeyer E. 1972. Is Ascophyllum nodosum lichenized? Bot. Mar. 15: 109-112 https://doi.org/10.1515/botm.1972.15.2.109
  35. Kopecka M., Gabriel M. and Farkasˇ V. 1987. Some anucleated yeast protoplasts synthesize ${\beta}-(1\rightarrow3)$-d-glucan microfibrils of the cell wall. Naturwissenschaften 74: 389-391 https://doi.org/10.1007/BF00405469
  36. Kroh M. and Knuiman B. 1988. Development of subprotoplasts from in vitro-grown tobacco pollen tubes. Sex. Plant Reprod. 1: 103-113 https://doi.org/10.1007/BF00189269
  37. La Claire J.W. 1982. Light and electron microscopic studies of growth and reproduction in Cutleria (Phaeophyta): III. Nuclear division in the trichothallic meristem of Cutleria cylindrica. Phycologia 21: 273-287 https://doi.org/10.2216/i0031-8884-21-3-273.1
  38. Lorz H. 1984. Enucleation of protoplasts: preparation of cytoplasts and miniprotoplasts. In: Vasil I.K. (ed.), Cell Culture and Somatic Cell Genetics of Plants, Vol. 1. Laboratory Procedures and Their Applications. Academic Press, Orlando. pp. 448-453
  39. Love A.J., Milner J.J. and Sadanandom A. 2008. Timing is everything: regulatory overlap in plant cell death. Trends Plant Sci. 13: 589-595 https://doi.org/10.1016/j.tplants.2008.08.006
  40. McDonald A.R., Garbary D.J. and Duckett J.G. 1993. Rhodamine-phalloidin staining of F-actin in Rhodophyta. Biotech. Histochem. 68: 91-98 https://doi.org/10.3109/10520299309104673
  41. Moss B.L. 1982. The control of epiphytes by Halidrys siliquosa (L.) Lyngb. (Phaeophyta, Cystoseiraceae). Phycologia 21: 185-191 https://doi.org/10.2216/i0031-8884-21-2-185.1
  42. Moss B.L. 1984. 'Skins' and possible relationships in the Fucales. Br. Phycol. J. 19: 198
  43. Motomura T. and Sakai Y. 1985. Ultrastructural studies on nuclear division in the sporophyte of Carpomitra cabrerae (Clemente) Kutzing (Phaeophyta, Sporochnales). Jpn. J. Phycol. 33: 199-209
  44. Nagasato C. and Motomura T. 2002. Influence of the centrosome in cytokinesis of brown algae: polyspermic zygotes of Scytosiphon lomentaria (Scytosiphonales, Phaeophyceae). J. Cell Sci. 115: 2541-2548
  45. Pickett-Heaps J.D. 1975. Green algae: Structure, Reproduction and Evolution in Selected Genera. Sinauer, Sunderland, 606 pp
  46. Pollock F.M. and Pickett-Heaps J.D. 2006. Valve formation without mitosis in the diatom Ditylum recovering from plasmolysis. Nova Hedwig. Beih. 130: 119-126
  47. Pueschel C.M. 1988. Cell sloughing and chloroplast inclusions in Hildenbrandia rubra (Rhodophyta, Hildenbrandiales). Eur. J. Phycol. 23: 17-23 https://doi.org/10.1080/00071618800650021
  48. Pueschel C.M. and Miller T.J. 1996. Reconsidering prey specializations in an algal-limpet grazing mutualism: epithallial cell development in Clathromorphum circumscriptum (Rhodophyta, Corallinales). J. Phycol. 32: 28-36 https://doi.org/10.1111/j.0022-3646.1996.00028.x
  49. Pueschel C.M., Miller T.J. and McCausland B.B. 1996. Development of epithallial cells in Corallina officinalis and Lithophyllum impressum (Corallinales, Rhodophyta). Phycologia 35: 161-169 https://doi.org/10.2216/i0031-8884-35-2-161.1
  50. Reape T.J., Molony E.M. and McCabe P.F. 2008. Programmed cell death in plants: distinguishing between different modes. J. Exp. Bot. 59: 435-444 https://doi.org/10.1093/jxb/erm258
  51. Robinson D.R., Sherwin T., Ploubidou A., Byard E.H. and Gull K. 1995. Microtubule polarity and dynamics in the control of organelle positioning, segregation, and cytokinesis in the trypanosome cell-cycle. J. Cell Biol. 128: 1163-1172 https://doi.org/10.1083/jcb.128.6.1163
  52. Russell G. and Veltkamp C.J. 1984. Epiphyte survival on skinshedding macrophytes. Mar. Ecol. Prog. Ser. 18: 149-153 https://doi.org/10.3354/meps018149
  53. Rutten T.L.M. and Derksen J. 1990. Organization of actin filaments in regenerating and outgrowing subprotoplasts from pollen tubes of Nicotiana tabacum L. Planta 180: 471-479 https://doi.org/10.1007/BF02411443
  54. Schoenwaelder M.E.A. 2008. The biology of phenolic containing vesicles. Algae 23: 163-175 https://doi.org/10.4490/ALGAE.2008.23.3.163
  55. Tarakhovskaya E.R., Maslov Y.I. and Shishova M.F. 2007. Phytohormones in algae. Russian J. Plant Physiol. 54: 163-170 https://doi.org/10.1134/S1021443707020021
  56. Toth R. 1976. The release, settlement and germination of zoospores in Chorda tomentosa (Phaeophyceae, Laminariales). J. Phycol. 12: 222-233 https://doi.org/10.1111/j.0022-3646.1976.00222.x
  57. Uheda E., Akasaka Y. and Daimon H. 1997. Morphological aspects of the shedding of surface layers from peanut roots. Can. J. Bot. 75: 607-611 https://doi.org/10.1139/b97-067
  58. van den Hoek C., Mann D.G. and Jahns H.M. 1995. Algae: An Introduction to Phycology. Cambridge University Press, Cambridge, 623 pp
  59. Xu H., Deckert R.J. and Garbary D.J. 2008. Ascophyllum and its symbionts: X. Ultrastructure of the interaction between A. nodosum (Phaeophyceae) and Mycophycias ascophylli (Ascomycetes). Botany 86: 185-193 https://doi.org/10.1139/B07-122

피인용 문헌

  1. Seaweed extract stimuli in plant science and agriculture vol.23, pp.3, 2011, https://doi.org/10.1007/s10811-010-9560-4
  2. Epidermal shedding inAscophyllum nodosum(Phaeophyceae): seasonality, productivity and relationship to harvesting vol.54, pp.6, 2015, https://doi.org/10.2216/15-32.1
  3. Ascophyllum nodosum and its symbionts: XI. The epiphyte Vertebrata lanosa performs better photosynthetically when attached to Ascophyllum than when alone vol.29, pp.4, 2014, https://doi.org/10.4490/algae.2014.29.4.321
  4. Defense mechanisms of sargassacean species against the epiphytic red algaNeosiphonia harveyi vol.51, pp.4, 2015, https://doi.org/10.1111/jpy.12311
  5. Effects of land-based fish farm effluent on the morphology and growth of Ascophyllum nodosum (Fucales, Phaeophyceae) in southwestern Nova Scotia vol.26, pp.3, 2011, https://doi.org/10.4490/algae.2011.26.3.253
  6. Various defense ability of four sargassacean algae against the red algal epiphyte Neosiphonia harveyi in Wakasa Bay, Japan vol.105, 2013, https://doi.org/10.1016/j.aquabot.2012.10.008