Skip to main content

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

Abstract

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.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Abbreviations

EFC:

Expanded flat cisterna

ER:

Endoplasmic reticulum

FC:

Flat cisterna

GV:

Golgi-derived vesicle

LB:

Latrunculin B

MN:

Membranous network

MS:

Membranous sac

MT:

Microtubule

References

  • Belanger KD, Quatrano RS (2000a) Polarity: the role of localized secretion. Curr Opin Plant Biol 3:67–72

    Article  CAS  PubMed  Google Scholar 

  • Belanger KD, Quatrano RS (2000b) Membrane recycling occurs during asymmetric tip growth and cell plate formation in Fucus distichus zygotes. Protoplasma 212:24–37

    Article  Google Scholar 

  • Bisgrove SR, Kropf DL (1998) Alignment of centrosomal and growth axes is a late event during polarization of Pelvetia compressa zygote. Dev Biol 194:246–256

    Google Scholar 

  • Bisgrove SR, Kropf DL (2004) Cytokinesis in brown algae: studies of asymmetric division in fucoid zygotes. Protoplasma 223:163–173

    Article  CAS  PubMed  Google Scholar 

  • Bisgrove SR, Henderson DC, Kropf DL (2003) Asymmetric division in fucoid zygotes is positioned by telophase nuclei. Plant Cell 15:854–862

    Article  CAS  PubMed  Google Scholar 

  • 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 180:537–547

    Article  CAS  Google Scholar 

  • 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 8:189–201

    Article  CAS  PubMed  Google Scholar 

  • 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 73:193–205

    Article  CAS  PubMed  Google Scholar 

  • 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 100:1173–1184

    Article  CAS  PubMed  Google Scholar 

  • Brawley SH, Quatrano RS, Wetherbee R (1977) Fine-structural studies of the gametes and embryo of Fucus vesiculosus L. (Phaeophyta). J Cell Sci 24:275–294

    CAS  PubMed  Google Scholar 

  • Callow ME, Coughlan SJ, Evans LV (1978) The role of Golgi bodies in polysaccharide sulphation in Fucus zygotes. J Cell Sci 32:337–356

    CAS  PubMed  Google Scholar 

  • 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 47:53–60

    Article  CAS  Google Scholar 

  • 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 10:137–150

    Article  CAS  PubMed  Google Scholar 

  • Engqvist-Goldstein AEY, Drubin DG (2003) Actin assembly and endocytosis: from yeast to mammals. Annu Rev Cell Dev Biol 19:287–332

    Article  CAS  PubMed  Google Scholar 

  • Evans LV, Simpson M, Callow ME (1973) Sulfated polysaccharide synthesis in brown algae. Planta 110:237–252

    Article  CAS  Google Scholar 

  • Hable WE, Miller NR, Kropf DL (2003) Polarity establishment requires dynamic actin in fucoid zygotes. Protoplasma 221:193–204

    CAS  PubMed  Google Scholar 

  • Haug A, Larsen B, Smidsrod O (1966) A study of the constitution of alginate by partial acid hydrolysis. Acta Chem Scand 20:183–190

    Article  CAS  Google Scholar 

  • Hepler PK (1982) Endoplasmic reticulum in formation of the cell plate and plasmodesmata. Protoplasma 111:121–123

    Article  Google Scholar 

  • Hepler PK, Newcomb EH (1967) Fine structure of cell plate formation in the apical meristem of Phaseolus roots. J Ultrastruct Res 19:498–513

    Article  CAS  PubMed  Google Scholar 

  • Karyophyllis D, Katsaros C, Dimitriadis I, Galatis B (2000) F-actin organization during the cell cycle of Sphacelaria rigidula (Phaeophyceae). Eur J Phycol 35:25–33

    Google Scholar 

  • Katsaros C, Galatis B, Mitrakos K (1983) Fine structural studies of the interphase and dividing apical cells of Sphacelaria tribuloides (Phaeophyta). J Phycol 19:16–30

    Article  Google Scholar 

  • Katsaros C, Motomura T, Nagasato C, Galatis B (2009) Diaphragm development in cytokinetic vegetative cells of brown algae. Bot Mar 52:150–161

    Article  Google Scholar 

  • Kiermayer O (1981) Cytoplasmic basis of morphogenesis in Micrasterias. In: Kiermayer O (ed) Cytomorphogenesis in plants. Cell biology monographs, vol 8. Springer, Wien, pp 147–189

    Google Scholar 

  • 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 26:259–315

    Google Scholar 

  • Kloareg B, Demarty M, Mabeau S (1986) Polyanionic characteristics of purified sulphated homofucans from brown algae. Int J Biol Macromol 8:380–386

    Article  CAS  Google Scholar 

  • Kropf DL (1992) Establishment and expression of cellular polarity in fucoid zygotes. Microbiol Rev 56:316–339

    CAS  PubMed  Google Scholar 

  • La Claire II JW (1981) Occurrence of plasmodesmata during infurrowing in a brown alga. Biol Cell 40:139–142

    Google Scholar 

  • Markey DR, Wilce RT (1975) The ultrastructure of reproduction in the brown alga Pylaiella littoralis I. Mitosis and cytokinesis in the plurilocular gametangia. Protoplasma 85:219–241

    Article  CAS  PubMed  Google Scholar 

  • 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 73:335–338

    Article  CAS  PubMed  Google Scholar 

  • 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 174:433–445

    Article  CAS  Google Scholar 

  • Nagasato C, Motomura T (2002a) Influence of the centrosome in cytokinesis of brown algae: polyspermic zygotes of Scytosiphon lomentaria (Scytosiphonales, Phaeophyceae). J Cell Sci 115:2541–2548

    CAS  PubMed  Google Scholar 

  • Nagasato C, Motomura T (2002b) Ultrastructural study on mitosis and cytokinesis in Scytosiphon lomentaria zygotes (Scytosiphonales, Phaeophyceae) by freeze-substitution. Protoplasma 219:140–149

    Article  CAS  PubMed  Google Scholar 

  • 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 45:404–412

    Article  CAS  Google Scholar 

  • Novotny AM, Forman M (1974) The relationship between changes in cell wall composition and the establishment of polarity in Fucus embryos. Dev Biol 40:162–173

    Article  CAS  PubMed  Google Scholar 

  • Otegui MS, Staehelin LA (2000a) Syncytial-type cell plates: a novel kind of cell plate involved in endosperm cellularization of Arabidopsis. Plant Cell 12:933–947

    Article  CAS  PubMed  Google Scholar 

  • Otegui MS, Staehelin LA (2000b) Cytokinesis in flowering plants: more than one way to divide a cell. Curr Opin Plant Biol 3:493–502

    Article  CAS  PubMed  Google Scholar 

  • 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 13:2033–2051

    Article  CAS  PubMed  Google Scholar 

  • 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 29:93–101

    Article  Google Scholar 

  • Quatrano RS, Crayton MA (1973) Sulfation of fucoidan in Fucus embryos. I. Possible role in localization. Dev Biol 30:29–41

    Article  CAS  PubMed  Google Scholar 

  • Quatrano RS, Stevens PT (1976) Cell wall assembly in Fucus zygotes. I. Characterization of the polysaccharide components. Plant Physiol 58:224–231

    Article  CAS  PubMed  Google Scholar 

  • Ragan MA (1976) Physodes and the phenolic compounds of brown algae. Composition and significance of physodes in vivo. Bot Mar 19:145–154

    Article  CAS  Google Scholar 

  • Rutte TLM, Knuiman B (1993) Brefeldin A effects on tobacco pollen tubes. Eur J Cell Biol 61:247–255

    Google Scholar 

  • 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 130:1345–1357

    Article  CAS  PubMed  Google Scholar 

  • Saxene IM, Brown MR Jr (2005) Cellulose biosynthesis: current views and evolving concepts. Ann Bot London 96:9–21

    Article  CAS  Google Scholar 

  • 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 34:969–980

    Article  CAS  Google Scholar 

  • Schoenwaelder MEA, Clayton MN (1998b) The role of the cytoskeleton in brown algal physode movement. Eur J Phycol 34:223–229

    Article  Google Scholar 

  • Schoenwaelder MEA, Clayton MN (1999) The presence of phenolic compounds in isolated cell walls of brown algae. Phycologia 38:161–166

    Article  Google Scholar 

  • Schoenwaelder MEA, Wiencke C (2000) Phenolic compounds in the embryo development of several northern hemisphere fucoids. Plant Biol 2:24–33

    Article  CAS  Google Scholar 

  • Schopfer CR, Hepler PK (1991) Distribution of membranes and the cytoskeleton during cell plate formation in pollen mother cells of Tradescantia. J Cell Sci 100:717–728

    Google Scholar 

  • 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 16:836–856

    Article  PubMed  CAS  Google Scholar 

  • Tatewaki M (1966) Formation of a crustaceous sporophyte with unilocular sporangia in Scytosiphon lomentaria. Phycologia 6:62–66

    Google Scholar 

  • 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 58:13–26

    Article  CAS  Google Scholar 

  • 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 41:300–310

    CAS  PubMed  Google Scholar 

  • 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 66:274–281

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Dr. C. Katsaros, University of Athens, Faculty of Biology, Department of Botany and Dr. J.M. Cock, Station Biologique de Roscoff for their critical reading of the manuscript and helpful suggestions. This study was supported by a Grant-in-Aid for Scientific Research from the Ministry of Education, Science and Culture, Japan (21770065, 20370025), and by the Research and Development Program for New Bio-industry Initiatives (2006-2010) of Bio-oriented Technology Research Advancement Institution (BRAIN), Japan.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Chikako Nagasato.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Nagasato, C., Inoue, A., Mizuno, M. et al. Membrane fusion process and assembly of cell wall during cytokinesis in the brown alga, Silvetia babingtonii (Fucales, Phaeophyceae). Planta 232, 287–298 (2010). https://doi.org/10.1007/s00425-010-1188-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-010-1188-8

Keywords

  • Brown algae
  • Cell wall
  • Cytokinesis
  • Flat cisternae
  • Golgi-derived vesicles