Skip to main content
SpringerLink
Log in

Protease-sensitive anchoring of microfilament bundles provides tracks for cytoplasmic streaming inVallisneria

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

Summary

In mesophyll cells of the aquatic angiospermVallisneria gigantea Graebner, the endoplasm streams rotationally along the cell walls normal to the leaf surface in situ. Bundles of microfilaments anchored in the ectoplasm serve as tracks for the cytoplasmic streaming. In single mesophyll cells isolated by enzymatic digestion, hypertonic treatment induces abnormal streaming concomitant with plasmolysis, specifically at one or both of the shorter sides of an approximate rectangle. The disorderly arrangement of microfilaments in such cells has been confirmed by fluorescence microscopy of cells stained with FITC-phalloidin. While inhibitors of proteases added to the enzyme solution used for isolation of cells suppress the disturbance of rotational streaming, exogenously applied protease promotes it. The results suggest that bundles of microfilaments in the ectoplasm are stabilized by protease-sensitive factor(s) in the presence of the cell wall.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

APMSF:

(p-amidinophenyl)methanesulfonyl fluoride hydrochloride

ATP:

adenosine 5′-triphosphate

BS:

basal solution

EGTA:

ethyleneglycol-bis(2-aminoethylether)-N,N,N′,N′-tetraacetic acid

F-actin:

fibrous actin

FITC:

fluorescein isothiocyanate

FTC:

fluorescein thiocarbamoyl derivative

G-actin:

globular actin

MS:

Murashige and Skoog

Pipes:

piperazine-N,N′-bis (2-ethanesulfonic acid)

Tris:

tris(hydroxymethyl)aminomethane

References

  • Akashi T, Shibaoka H (1991) Involvement of transmembrane proteins in the association of cortical microtubules with the plasma membrane in tobacco BY-2 cells. J Cell Sci 98 (in press)

  • —, Kawasaki S, Shibaoka H (1990) Stabilization of cortical microtubules by the cell wall in cultured tobacco cells: effects of extensin on the cold-stability of cortical microtubules. Planta 182: 363–369

    Article  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  PubMed  CAS  Google Scholar 

  • Burridge K, Fath K, Kelly T, Nuckolls G, Turner C (1988) Focal adhesions: transmembrane junctions between the extracellular matrix and the cytoskeleton. Annu Rev Cell Biol 4: 487–525

    Article  PubMed  CAS  Google Scholar 

  • Forde J, Steer MW (1976) Cytoplasmic streaming inElodea. Can J Bot 54: 2688–2694

    Article  Google Scholar 

  • Grolig F, Williamson RE, Parke J, Miller C, Anderton BH (1988) Myosin and Ca2+-sensitive streaming in the algaChara: detection of two polypeptides reacting with a monoclonal antimyosin and their localization in the streaming endoplasm. Eur J Cell Biol 47: 22–31

    PubMed  CAS  Google Scholar 

  • Hayashi T, Kamitsubo E (1959) Plasmolysis in Characeae. Bot Mag 72: 309–315

    Google Scholar 

  • Ishigami M, Nagai R (1980) Motile apparatus inVallisneria leaf cells. II. Effects of cytochalasin B and lead acetate on the rate and direction of streaming. Cell Struct Funct 5: 13–20

    Article  CAS  Google Scholar 

  • Izutani Y, Takagi S, Nagai R (1990) Orientation movements of chloroplasts inVallisneria epidermal cells: different effects of light at low- and high-fluence rate. Photochem Photobiol 51: 105–111

    CAS  Google Scholar 

  • Kakimoto T, Shibaoka H (1987) Actin filaments and microtubules in the preprophase band and phragmoplast of tobacco cells. Protoplasma 140: 151–156

    Article  Google Scholar 

  • Kamitsubo E (1966) Motile protoplasmic fibrils ofCharaceae. II. Linear fibrillar structure and its bearing on protoplasmic streaming Proc Jap Acad 42: 640–643

    Google Scholar 

  • Kamiya N (1959) Protoplasmic streaming. Springer, Wien [Heilbrunn LV, Weber F (eds) Protoplasmatologia, vol VIII 3 a]

    Google Scholar 

  • — Kuroda K (1956) Velocity distribution of protoplasmic streaming inNitella cells. Bot Mag 69: 543–554

    Google Scholar 

  • Kato T, Tonomura Y (1977) Identification of myosin inNitella flexilis. J Biochem 82: 777–782

    PubMed  CAS  Google Scholar 

  • Kropf DL, Kloareg B, Quatrano RS (1988) Cell wall is required for fixation of the embryonic axis inFucus zygotes. Science 239: 187–190

    Article  PubMed  CAS  Google Scholar 

  • Kuroda K (1983) Cytoplasmic streaming in Characean cells cut open by microsurgery. Proc Jp Acad (B) 59: 126–130

    Google Scholar 

  • Küster E (1910) Über Inhaltsverlagerungen in plasmolysierten Zellen. Flora 100: 267–287

    Google Scholar 

  • Lichtscheidl IK, Lancelle SA, Hepler PK (1990) Actin-endoplasmic reticulum complexes inDrosera. Their structural relationship with the plasmalemma, nucleus, and organelles in cells prepared by high pressure freezing. Protoplasma 155: 116–126

    Article  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15: 473–497

    Article  CAS  Google Scholar 

  • Nagai R, Hayama T (1979) Ultrastructure of the endoplasmic factor responsible for cytoplasmic streaming inChara internodal cells. J Cell Sci 36: 121–136

    PubMed  CAS  Google Scholar 

  • —, Rebhum LI (1966) Cytoplasmic microfilaments in streamingNitella cells. J Ultrastruct Res 14: 571–589

    Article  PubMed  CAS  Google Scholar 

  • Ohsuka K, Inoue A (1979) Identification of myosin in a flowering plant,Egeria densa. J Biochem 85: 375–378

    PubMed  CAS  Google Scholar 

  • Palevitz BA, Ash JF, Hepler PK (1974) Actin in the green alga,Nitella. Proc Natl Acad Sci USA 71: 363–366

    Article  PubMed  CAS  Google Scholar 

  • Schindler M, Meiners S, Cheresh DA (1989) RGD-dependent linkage between plant cell wall and plasma membrane: consequences for growth. J Cell Biol 108: 1955–1965

    Article  PubMed  CAS  Google Scholar 

  • Sheetz MP, Spudich JA (1983) Movement of myosin-coated fluorescent beads on actin cables in vitro. Nature 303: 31–35

    Article  PubMed  CAS  Google Scholar 

  • Shimmen T, Yano Y (1984) Active sliding movement of latex beads coated with skeletal muscle myosin onChara actin bundles. Protoplasma 121: 132–137

    Article  CAS  Google Scholar 

  • Shinmi T, Hase T, Sugiyama T (1989) Effect of ATP on the trypsin proteolysis of plasma membrane ATPase from corn roots. In: Tazawa M, Katsumi M, Masuda Y, Okamoto H (eds). Plant water relations and growth under stress. MYU K.K., Tokyo, pp 446–448

    Google Scholar 

  • Sonobe S, Shibaoka H (1989) Cortical fine actin filaments in higher plant cells visualized by rhodamine-phalloidin after pretreatment with m-maleimidobenzoyl N-hydroxysuccinimide ester. Protoplasma 148:80–86

    Article  Google Scholar 

  • Takagi S, Nagai R (1983) Regulation of cytoplasmic streaming inVallisneria mesophyll cells. J Cell Sci 62: 385–405

    PubMed  CAS  Google Scholar 

  • Traas JA, Doonan JH, Rawlins DJ, Shaw PJ, Watts J, Lloyd CW (1987) An actin network is present in the cytoplasm throughout the cell cycle of carrot cells and associates with the dividing nucleus. J Cell Biol 105: 387–395

    Article  PubMed  CAS  Google Scholar 

  • Twining SS (1984) Fluorescein isothiocyanate-labeled casein assay for proteolytic enzymes. Anal Biochem 143: 30–34

    Article  PubMed  CAS  Google Scholar 

  • Williamson RE (1974) Actin in the alga,Chara corallina. Nature 248: 801–802

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi Y, Nagai R (1981) Motile apparatus inVallisneria leaf cells. I. Organization of microfilaments. J Cell Sci 48: 193–205

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biology, College of General Education, Osaka University, Machikane-yama 1-1, 560, Toyonaka, Osaka, Japan

    Y. Masuda, S. Takagi & R. Nagai

Authors
  1. Y. Masuda
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Takagi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. R. Nagai
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Masuda, Y., Takagi, S. & Nagai, R. Protease-sensitive anchoring of microfilament bundles provides tracks for cytoplasmic streaming inVallisneria . Protoplasma 162, 151–159 (1991). https://doi.org/10.1007/BF02562558

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02562558

Keywords

Search

Navigation