Skip to main content
Log in

Membrane recycling occurs during asymmetric tip growth and cell plate formation inFucus distichus zygotes

  • Original Papers
  • Published:
Protoplasma Aims and scope Submit manuscript

Summary

Zygotes of the brown algaFucus distichus undergo a series of intracellular changes resulting in the establishment of a polar growth axis prior to the first embryonic cell division. In order to examine the dynamics of membrane recycling which occur in the zygote during polar growth of the rhizoid, we probed living Fucus zygotes with the vital stain FM4-64, N-(3-triethylammoniumpropyl)-4-(6-(4-(diethylammo)phenyl)hexatrienyl)pyridinium dibromide. In newly fertilized, spherical zygotes, FM4-64 staining is symmetric and predominantly in the perinuclear region which is rich in endoplasmic reticulum, Golgi, and vacuolar membranes. As rhizoid or tip growth is initiated, this population of stained membranes becomes asymmetrically redistributed, concentrating at the rhizoid tip and extending centrally to the perinuclear region. This asymmetric localization is maintained in the zygote throughout polar growth of the rhizoid and during karyokinesis. Subsequently, FM4-64 staining also begins to accumulate in a central location between the daughter nuclei. As cytokinesis proceeds, this region of stain expands laterally from this central location, perpendicular to the plane of polar rhizoid outgrowth. The staining pattern thus delineates the formation of a cell plate, similar spatially to the accumulation of nascent plate membranes of higher plants. Treatment of Fucus zygotes with brefeldin-A inhibits both asymmetric growth of the rhizoid and formation of a new cell plate. These data suggest that inF. distichus FM4-64 is labeling a Golgi-derived membrane fraction that appears to be recycling between the site of tip growth, perinuclear region, and new cell plate.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

AF:

after fertilization

ASW:

artificial seawater

BFA:

brefeldin A

ER:

endoplasmic reticulum

FM4-64:

N-(3-triethylam-moniumpropyl)-4-(6-(4-(diethylamino)phenyl)hexatrienyl)pyridinium dibromide

References

  • Becker BN, Cheng H-F, Burns KD, Harris RC (1995) Polarized rabbit type 1 angiotensin II receptors manifest differential rates of endocytosis and recycling. Am J Physiol 269: C1048-C1056

    Google Scholar 

  • Beireiter-Hahn J (1996) Dimethylaminostyrylmethylpyridimiumiodide (DASPMI) as a fluorescent probe for mitochondria in situ. Biochim Biophys Acta 423: 1–14

    Google Scholar 

  • Berger F, Taylor A, Brownlee C (1994) Cell fate determination by the cell wall in early Fucus development. Science 263: 1421–1423

    Google Scholar 

  • Betz WJ, Mao F, Bewick GS (1992) Activity-dependent fluorescent staining and destaining of living vertebrate motor nerve terminals. J Neurosci 12: 363–375

    Google Scholar 

  • — —, Smith CB (1996) Imaging exocytosis and endocytosis. Curr Opin Neurobiol 6: 365

    Google Scholar 

  • Bouget F-Y, Gerttula S, Shaw SL, Quatrano RS (1996) Localization of actin mRNA during the establishment of cell polarity and early cell divisions in Fucus embryos. Plant Cell 8: 189–201

    Google Scholar 

  • Brawley SH, Quatrano RS, Wetherbee R (1976) Fine-structural studies of the gametes and embryo ofFucus esiculosus L (Phaeophyta) II: the cytoplasm of the egg and young zygote. J Cell Sci 20: 255–271

    Google Scholar 

  • — — — (1977) Fine-structural studies of the gametes and embryo ofFucus esiculosus L (Phaeophyta) III: cytokinesis and the multicellular embryo. J Cell Sci 24: 275–294

    Google Scholar 

  • Bretscher A, Drees B, Harsay E, Schott D, Wang T (1994) What are the basic functions of microfilaments? Insights from studies in budding yeast. J Cell Biol 126: 821–825

    Google Scholar 

  • Brodsky FM (1988) Living with clathrin: its role in intracellular membrane traffic. Science 242: 1396–1402

    Google Scholar 

  • Chang F, Drubin DG (1996) Cell division: why daughters cannot be like their mothers. Curr Biol 6: 651–654

    Google Scholar 

  • Drubin DG, Nelson WJ (1996) Origins of cell polarity. Cell 84: 335–344

    Google Scholar 

  • Eady C, Lindsey K, Twell D (1995) The significance of microspore division and division symmetry for vegetative cell-specific transcription and generative cell differentiation. Plant Cell 7: 65–74

    Google Scholar 

  • Fowke LC, Pickett-Heaps JD (1969a) Cell division in Spirogyra I: mitosis. J Phycol 5: 240–259

    Google Scholar 

  • — — (1969b) Cell division in Spirogyra II: cytokinesis. J Phycol 5: 273–281

    Google Scholar 

  • Fowler J, Quatrano RS (1997) Plant cell morphogenesis: plasma membrane interactions with the cytoskeleton and cell wall. Annu Rev Cell Dev Biol 13: 697–743

    Google Scholar 

  • Goodner B, Quatrano RS (1993) Fucus embryogenesis: a model to study the establishment of polarity. Plant Cell 5: 1471–1481

    Google Scholar 

  • Grabski S, de Feijter AW, Schindler M (1993) Endoplasmic reticulum forms a dynamic continuum for lipid diffusion between contiguous soybean root cells. Plant Cell 5: 25–38

    Google Scholar 

  • Griffing LR (1997) Flying into the plant cell: 3D reconstruction of early endocytosis. Plant Physiol 114: 69–70

    Google Scholar 

  • Guo S, Kemphues KJ (1996) A non-muscle myosin required for embryonic polarity inCaenorhabditis elegans. Nature 382: 455–458

    Google Scholar 

  • Hable WE, Kropf DL (1998) Roles of secretion and the cytoskeleton in cell adhesion and polarity establishment inPel etia compressa zygotes. Dev Biol 198: 45–56

    Google Scholar 

  • Hawes C, Satiat-Jeunemaitre B (1996) Stacks of questions: how does the plant Golgi work? Trends Plant Sci 1: 395–401

    Google Scholar 

  • Hepler PK, Bonsignore C (1990) Caffeine inhibition of cytokinesis: ultrastructure of cell plate formation/degradation. Protoplasma 157: 182–192

    Google Scholar 

  • Heuser J, Zhu Q, Clarke M (1993) Proton pumps populate the contractile vacuoles of Dictyostelium amoebae. J Cell Biol 121: 1311–1327

    Google Scholar 

  • Horvitz HR, Herskowitz I (1992) Mechanisms of asymmetric cell division: two Bs or not two Bs, that is the question. Cell 68: 237–255

    Google Scholar 

  • Kropf DL (1997) Induction of polarity in fucoid zygotes. Plant Cell 9: 1011–1020

    Google Scholar 

  • —, Berge SK, Quatrano RS (1989) Actin localization during Fucus embryogenesis. Plant Cell 1: 191–200

    Google Scholar 

  • —, Maddock A, Gard DL (1990) Microtubule distribution and function in early Pelvetia development. J Cell Sci 97: 545–552

    Google Scholar 

  • Mayer U, Buttner G, Jurgens G (1993) Apical-basal pattern formation in the Arabidopsis embryo: studies on the role of thegnom gene. Development 117: 149–162

    Google Scholar 

  • McIntosh K, Pickett-Heaps JD, Gunning B (1995) Cytokinesis in Spirogyra: integration of cleavage and cell plate formation. Int J Plant Sci 156: 1–8

    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

    Google Scholar 

  • Nuccitelli R (1978) Ooplasmic segregation and secretion in Pelvetia egg is accompanied by the membrane-generated electrical current. Dev Biol 62: 13–33

    Google Scholar 

  • Phillips GD, Preshaw C, Steer MW (1988) Dictyosome vesicle production and plasma membrane turnover in auxin-stimulated outer epidermal cells of coleoptile segments fromA ena sati a (L.). Protoplasma 125: 59–65

    Google Scholar 

  • Pickett-Heaps JD (1975) Green algae: structure, reproduction and evolution in selected genera. Sinauer Associates, Sunderland, Mass

    Google Scholar 

  • Quatrano RS (1982) Cell-wall formation in Fucus zygotes: a model system to study the assembly and location of wall polymers. In: Brown RM (ed) Cellulose and other natural polymer systems. Plenum, London, pp 45–59

    Google Scholar 

  • —, (1997) Cortical asymmetries direct the establishment of cell polarity and the plane of cell division in Fucus embryos. Cold Spring Harbor Symp Quant Biol 62: 65–70

    Google Scholar 

  • —, Crayton MA (1973) Sulfation of fucoidan in Fucus embryos I: possible role in localization. Dev Biol 30: 29–35

    Google Scholar 

  • —, Shaw S (1997) Role of the cell wall in the determination of cell polarity and the plane of cell division in Fucus embryos. Trends Plant Sci 2: 15–21

    Google Scholar 

  • —, Griffing LR, Huber-Walchli V, Doubet S (1985) Cytological and biochemical requirements for the establishment of a polar cell. J Cell Sci Suppl 2: 129–141

    Google Scholar 

  • Rawlence D (1973) Some aspects of the ultrastructure ofAscopyllum nodosum (L.) Le Jolis (Phaeophyceae, Fucales) including observations on cell plate formation. Phycologia 12: 17–28

    Google Scholar 

  • Robinson DG, Hillmer S (1990) Endocytosis in plants. Physiol Plant 79: 96–104

    Google Scholar 

  • Samuels AL, Bisalputra T (1990) Endocytosis in elongating root cells ofLobelia erinus. J Cell Sci 97: 1153–1166

    Google Scholar 

  • —, 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

    Google Scholar 

  • Sawitsky H, Grolig F (1995) Phragmoplast of the green alga Spirogyra is functionally distinct from the higher plant phragmoplast. J Cell Biol 130: 1359–1371

    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 

  • Shaw SL, Quatrano RS (1996a) Polar localization of a dihydropyridine receptor on living Fucus zygotes. J Cell Sci 109: 335–342

    Google Scholar 

  • — — (1996b) The role of targeted secretion in the establishment of cell polarity and the orientation of the division plane in Fucus zygotes. Development 122: 2623–2630

    Google Scholar 

  • Staehelin LA, Hepler PK (1996) Cytokinesis in higher plants. Cell 84: 821–824

    Google Scholar 

  • Tanchak MA, Griffing LR, Mersey BG, Fowke LC (1984) Endocytosis of cationized ferritin by coated vesicles of soybean protoplasts. Planta 162: 481–486

    Google Scholar 

  • Vida TA, Emr SD (1995) A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J Cell Biol 128: 779–792

    Google Scholar 

  • Wagner VT, Brian L, Quatrano RS (1992) Role of vitronectin-like molecule in embryo adhesion of the brown alga Fucus. Proc Natl Acad Sci USA 89: 3644–3648

    Google Scholar 

  • Wardlaw CW (1968) Morphogenesis in plants. Methuen, London

    Google Scholar 

  • Wick S (1991) Spatial aspects of cytokinesis in plant cells. Curr Opin Cell Biol 3: 253–260

    Google Scholar 

  • Zhang D, Wadsworth P, Hepler PK (1993) Dynamics of microfilaments are similar, but distinct from microtubules during cytokinesis in living, dividing plant cells. Cell Motil Cytoskeleton 24: 151–155

    Google Scholar 

  • Zhong W, Feder JN, Jiang MM, Jan LY, Jan YN (1996) Asymmetric localization of a mammalian numb homolog during mouse cortical neurogenesis. Neuron 17: 43–53

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Belanger, K.D., Quatrano, R.S. Membrane recycling occurs during asymmetric tip growth and cell plate formation inFucus distichus zygotes. Protoplasma 212, 24–37 (2000). https://doi.org/10.1007/BF01279344

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01279344

Keywords

Navigation