, Volume 232, Issue 2, pp 287–298

Membrane fusion process and assembly of cell wall during cytokinesis in the brown alga, Silvetia babingtonii (Fucales, Phaeophyceae)

  • Chikako Nagasato
  • Akira Inoue
  • Masashi Mizuno
  • Kazuki Kanazawa
  • Takao Ojima
  • Kazuo Okuda
  • Taizo Motomura


During cytokinesis in brown algal cells, Golgi-derived vesicles (GVs) and flat cisternae (FCs) are involved in building the new cell partition membrane. In this study, we followed the membrane fusion process in Silvetia babingtonii zygotes using electron microscopy together with rapid freezing and freeze substitution. After mitosis, many FCs were formed around endoplasmic reticulum clusters and these then spread toward the future cytokinetic plane. Actin depolymerization using latrunculin B prevented the appearance of the FCs. Fusion of GVs to FCs resulted in structures that were thicker and more elongated (EFCs; expanded flat cisternae). Some complicated membranous structures (MN; membranous network) were formed by interconnection of EFCs and following the arrival of additional GVs. The MN grew into membranous sacs (MSs) as gaps between the MNs disappeared. The MSs were observed in patches along the cytokinetic plane. Neighboring MSs were united to form the new cell partition membrane. An immunocytochemical analysis indicated that fucoidan was synthesized in Golgi bodies and transported by vesicles to the future cytokinetic plane, where the vesicles fused with the FCs. Alginate was not detected until the MS phase. Incubation of sections with cellulase-gold showed that the cellulose content of the new cross wall was not comparable to that of the parent cell wall.


Brown algae Cell wall Cytokinesis Flat cisternae Golgi-derived vesicles 



Expanded flat cisterna


Endoplasmic reticulum


Flat cisterna


Golgi-derived vesicle


Latrunculin B


Membranous network


Membranous sac




  1. Belanger KD, Quatrano RS (2000a) Polarity: the role of localized secretion. Curr Opin Plant Biol 3:67–72CrossRefPubMedGoogle Scholar
  2. Belanger KD, Quatrano RS (2000b) Membrane recycling occurs during asymmetric tip growth and cell plate formation in Fucus distichus zygotes. Protoplasma 212:24–37CrossRefGoogle Scholar
  3. Bisgrove SR, Kropf DL (1998) Alignment of centrosomal and growth axes is a late event during polarization of Pelvetia compressa zygote. Dev Biol 194:246–256Google Scholar
  4. Bisgrove SR, Kropf DL (2004) Cytokinesis in brown algae: studies of asymmetric division in fucoid zygotes. Protoplasma 223:163–173CrossRefPubMedGoogle Scholar
  5. Bisgrove SR, Henderson DC, Kropf DL (2003) Asymmetric division in fucoid zygotes is positioned by telophase nuclei. Plant Cell 15:854–862CrossRefPubMedGoogle Scholar
  6. Bonfante-Fasolo P, Vian B, Perotto S, Faccio A, Knox JP (1990) Cellulose and pectin localization in roots of mycorrhizal Allium porrum: labelling continuity between host cell wall and interfacial material. Planta 180:537–547CrossRefGoogle Scholar
  7. Bouget FY, Gerttula S, Shaw SL, Quatrano RS (1996) Localization of actin mRNA during the establishment of cell polarity and early cell division in Fucus embryos. Plant Cell 8:189–201CrossRefPubMedGoogle Scholar
  8. Brawley SH, Quatrano RS (1979) Sulfation of fucoidin in Fucus embryos. IV. Autoradiographic investigations of fucoidin sulfation and secretion during differentiation and the effect of cytochalasin treatment. Dev Biol 73:193–205CrossRefPubMedGoogle Scholar
  9. Brawley SH, Robinson KR (1985) Cytochalasin treatment disrupts the endogenous currents associated with cell polarization in fucoid zygotes: studies of the role of F-actin in embryogenesis. J Cell Biol 100:1173–1184CrossRefPubMedGoogle Scholar
  10. Brawley SH, Quatrano RS, Wetherbee R (1977) Fine-structural studies of the gametes and embryo of Fucus vesiculosus L. (Phaeophyta). J Cell Sci 24:275–294PubMedGoogle Scholar
  11. Callow ME, Coughlan SJ, Evans LV (1978) The role of Golgi bodies in polysaccharide sulphation in Fucus zygotes. J Cell Sci 32:337–356PubMedGoogle Scholar
  12. Chi E-S, Henry EC, Kawai H, Okuda K (1999) Immunogold-labeling analysis of alginate distributions in the cell walls of chromophyte algae. Phycol Res 47:53–60CrossRefGoogle Scholar
  13. Dhonukshe P, Baluska F, Schlicht M, Hlavacka A, Samaj J, Friml J, Gadella TWJ Jr (2006) Endocytosis of cell surface material mediates cell plate formation during plant cytokinesis. Dev Cell 10:137–150CrossRefPubMedGoogle Scholar
  14. Engqvist-Goldstein AEY, Drubin DG (2003) Actin assembly and endocytosis: from yeast to mammals. Annu Rev Cell Dev Biol 19:287–332CrossRefPubMedGoogle Scholar
  15. Evans LV, Simpson M, Callow ME (1973) Sulfated polysaccharide synthesis in brown algae. Planta 110:237–252CrossRefGoogle Scholar
  16. Hable WE, Miller NR, Kropf DL (2003) Polarity establishment requires dynamic actin in fucoid zygotes. Protoplasma 221:193–204PubMedGoogle Scholar
  17. Haug A, Larsen B, Smidsrod O (1966) A study of the constitution of alginate by partial acid hydrolysis. Acta Chem Scand 20:183–190CrossRefGoogle Scholar
  18. Hepler PK (1982) Endoplasmic reticulum in formation of the cell plate and plasmodesmata. Protoplasma 111:121–123CrossRefGoogle Scholar
  19. Hepler PK, Newcomb EH (1967) Fine structure of cell plate formation in the apical meristem of Phaseolus roots. J Ultrastruct Res 19:498–513CrossRefPubMedGoogle Scholar
  20. Karyophyllis D, Katsaros C, Dimitriadis I, Galatis B (2000) F-actin organization during the cell cycle of Sphacelaria rigidula (Phaeophyceae). Eur J Phycol 35:25–33Google Scholar
  21. Katsaros C, Galatis B, Mitrakos K (1983) Fine structural studies of the interphase and dividing apical cells of Sphacelaria tribuloides (Phaeophyta). J Phycol 19:16–30CrossRefGoogle Scholar
  22. Katsaros C, Motomura T, Nagasato C, Galatis B (2009) Diaphragm development in cytokinetic vegetative cells of brown algae. Bot Mar 52:150–161CrossRefGoogle Scholar
  23. Kiermayer O (1981) Cytoplasmic basis of morphogenesis in Micrasterias. In: Kiermayer O (ed) Cytomorphogenesis in plants. Cell biology monographs, vol 8. Springer, Wien, pp 147–189Google Scholar
  24. Kloareg B, Quatrano RS (1988) Structure of the cell walls of marine algae and ecophysiological functions of the matrix of polysaccharides. Oceanogr Mar Biol Annu Rev 26:259–315Google Scholar
  25. Kloareg B, Demarty M, Mabeau S (1986) Polyanionic characteristics of purified sulphated homofucans from brown algae. Int J Biol Macromol 8:380–386CrossRefGoogle Scholar
  26. Kropf DL (1992) Establishment and expression of cellular polarity in fucoid zygotes. Microbiol Rev 56:316–339PubMedGoogle Scholar
  27. La Claire II JW (1981) Occurrence of plasmodesmata during infurrowing in a brown alga. Biol Cell 40:139–142Google Scholar
  28. Markey DR, Wilce RT (1975) The ultrastructure of reproduction in the brown alga Pylaiella littoralis I. Mitosis and cytokinesis in the plurilocular gametangia. Protoplasma 85:219–241CrossRefPubMedGoogle Scholar
  29. Mizuno M, Nishitani Y, Tanoue T, Matoba Y, Ojima T, Hashimoto T, Kanazawa K (2009) Quantification and localization of fucoidan in Laminaria japonica using a novel antibody. Biosci Biotechnol Biochem 73:335–338CrossRefPubMedGoogle Scholar
  30. Moore PJ, Staehelin LA (1988) Immunogold localization of the cell-wall-matrix polysaccharides rhamnogalacturonan I and xyloglucan during cell expansion and cytokinesis in Trifolium pratense L.: implication for secretory pathways. Planta 174:433–445CrossRefGoogle Scholar
  31. Nagasato C, Motomura T (2002a) Influence of the centrosome in cytokinesis of brown algae: polyspermic zygotes of Scytosiphon lomentaria (Scytosiphonales, Phaeophyceae). J Cell Sci 115:2541–2548PubMedGoogle Scholar
  32. Nagasato C, Motomura T (2002b) Ultrastructural study on mitosis and cytokinesis in Scytosiphon lomentaria zygotes (Scytosiphonales, Phaeophyceae) by freeze-substitution. Protoplasma 219:140–149CrossRefPubMedGoogle Scholar
  33. Nagasato C, Motomura T (2009) Effect of latrunculin B and brefeldin A on cytokinesis in the brown alga Scytosiphon lomentaria zygotes (Scytosiphonales, Phaeophyceae). J Phycol 45:404–412CrossRefGoogle Scholar
  34. Novotny AM, Forman M (1974) The relationship between changes in cell wall composition and the establishment of polarity in Fucus embryos. Dev Biol 40:162–173CrossRefPubMedGoogle Scholar
  35. Otegui MS, Staehelin LA (2000a) Syncytial-type cell plates: a novel kind of cell plate involved in endosperm cellularization of Arabidopsis. Plant Cell 12:933–947CrossRefPubMedGoogle Scholar
  36. Otegui MS, Staehelin LA (2000b) Cytokinesis in flowering plants: more than one way to divide a cell. Curr Opin Plant Biol 3:493–502CrossRefPubMedGoogle Scholar
  37. Otegui MS, Mastronarde DN, Kang B-H, Bednarek SY, Staehelin LA (2001) Three-dimensional analysis of syncytial-type cell plates during endosperm cellularization visualized by high resolution electron tomography. Plant Cell 13:2033–2051CrossRefPubMedGoogle Scholar
  38. Phillips JA, Clayton MN, Harvey AS (1994) Comparative studies on sporangial distribution and structure in species of Zonaria, Lobophora and Homoeostrichus (Dictyotales, Phaeophyceae) from Australia. Eur J Phycol 29:93–101CrossRefGoogle Scholar
  39. Quatrano RS, Crayton MA (1973) Sulfation of fucoidan in Fucus embryos. I. Possible role in localization. Dev Biol 30:29–41CrossRefPubMedGoogle Scholar
  40. Quatrano RS, Stevens PT (1976) Cell wall assembly in Fucus zygotes. I. Characterization of the polysaccharide components. Plant Physiol 58:224–231CrossRefPubMedGoogle Scholar
  41. Ragan MA (1976) Physodes and the phenolic compounds of brown algae. Composition and significance of physodes in vivo. Bot Mar 19:145–154CrossRefGoogle Scholar
  42. Rutte TLM, Knuiman B (1993) Brefeldin A effects on tobacco pollen tubes. Eur J Cell Biol 61:247–255Google Scholar
  43. Samuels AL, Giddings TH, Staehelin LA (1995) Cytokinesis in Tobacco BY-2 and root tip cells: a new model of cell plate formation in higher plants. J Cell Biol 130:1345–1357CrossRefPubMedGoogle Scholar
  44. Saxene IM, Brown MR Jr (2005) Cellulose biosynthesis: current views and evolving concepts. Ann Bot London 96:9–21CrossRefGoogle Scholar
  45. Schoenwaelder MEA, Clayton MN (1998a) Secretion of phenolic substances into the zygote wall and cell plate in embryos of Hormosira and Acrocarpia (Fucales, Phaeophyceae). J Phycol 34:969–980CrossRefGoogle Scholar
  46. Schoenwaelder MEA, Clayton MN (1998b) The role of the cytoskeleton in brown algal physode movement. Eur J Phycol 34:223–229CrossRefGoogle Scholar
  47. Schoenwaelder MEA, Clayton MN (1999) The presence of phenolic compounds in isolated cell walls of brown algae. Phycologia 38:161–166CrossRefGoogle Scholar
  48. Schoenwaelder MEA, Wiencke C (2000) Phenolic compounds in the embryo development of several northern hemisphere fucoids. Plant Biol 2:24–33CrossRefGoogle Scholar
  49. Schopfer CR, Hepler PK (1991) Distribution of membranes and the cytoskeleton during cell plate formation in pollen mother cells of Tradescantia. J Cell Sci 100:717–728Google Scholar
  50. Seguí-Simarro JM, Austin JR II, White EA, Staehelin LA (2004) Electron tomographic analysis of somatic cell plate formation in meristematic cells of Arabidopsis preserved by high-pressure freezing. Plant Cell 16:836–856CrossRefPubMedGoogle Scholar
  51. Tatewaki M (1966) Formation of a crustaceous sporophyte with unilocular sporangia in Scytosiphon lomentaria. Phycologia 6:62–66Google Scholar
  52. Thiele K, Wanner G, Kindzierski V, Jürgens G, Mayer U, Pachl F, Assaad FF (2009) The timely deposition of callose is essential for cytokinesis in Arabidopsis. Plant J 58:13–26CrossRefGoogle Scholar
  53. Yasuhara H, Shibaoka H (2000) Inhibition of cell-plate formation by brefeldin A inhibited the depolymerization of microtubules in the central region of the phragmoplast. Plant Cell Physiol 41:300–310PubMedGoogle Scholar
  54. Yasuhara H, Sonobe S, Shibaoka H (1995) Effects of brefeldin A on the formation of the cell plate in tobacco BY-2 cells. Eur J Cell Biol 66:274–281PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Chikako Nagasato
    • 1
  • Akira Inoue
    • 2
  • Masashi Mizuno
    • 3
  • Kazuki Kanazawa
    • 3
  • Takao Ojima
    • 2
  • Kazuo Okuda
    • 4
  • Taizo Motomura
    • 1
  1. 1.Muroran Marine Station, Field Science Center for Northern BiosphereHokkaido UniversityMuroranJapan
  2. 2.Graduate School of Fisheries ScienceHokkaido UniversityHakodateJapan
  3. 3.Graduate School of Agricultural ScienceKobe UniversityKobeJapan
  4. 4.Graduate School of Kuroshio ScienceKochi UniversityKochiJapan

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