Skip to main content
SpringerLink
Log in

Microtubule disassembly enhances reversible cytochalasin-dependent disruption of actin bundles in characean internodes

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

Summary

Parallel bundles of actin filaments at the cortex-endoplasm interface provide tracks for myosin-generated cytoplasmic streaming in characean internodes. These bundles resist disassembly or structural modification when exposed to 10 μM cytochalasin D (CD) even though this concentration of CD rapidly (within minutes) but reversibly arrests streaming. Unexpectedly, we discovered that prolonged treatment with lower concentrations of CD could partially disassemble the subcortical actin bundles. Actin bundles became discontinuous following one- to several-day treatment with concentrations (6 μM) that reduced but did not arrest streaming, and the residual fragments mostly remained parallel to the chloroplast files. When microtubules were concurrently disassembled with tubulin-specific drugs, however, low CD concentrations (2.5–3 μM) completely arrested bulk streaming, disrupted the largely 2-dimensional actin bundle array and caused the formation of a coarse, thick-meshed actin network that extended from the cortex to the endoplasm. Despite such massive reconstruction, drug removal enabled cells to recover continuous parallel bundles and streaming. Recovery was possible if both or just one of the drugs were removed. In recovered cells, the streaming pattern frequently redeveloped in new directions that did not follow the chloroplast files, and later, chloroplast files readjusted to the new polarity established by the actin bundles. This first report on the complete and reversible disassembly of characean actin bundles provides new insights into the mechanism of actin bundle assembly and organization and supports the idea of indirect interactions between actin filaments and microtubules.

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

AFW:

artificial fresh water

CD:

cytochalasin D

MBS:

m-maleimidobenzoyl N-hydroxysuccinimide ester

References

  • Bradley MO (1973) Microfilaments and cytoplasmic streaming: inhibition of streaming with cytochalasin. J Cell Sci 12: 327–343

    PubMed  CAS  Google Scholar 

  • Braun M, Sievers A (1994) Role of the microtubule cytoskeleton in gravisensingChara rhizoids. Eur J Cell Biol 63: 289–298

    PubMed  CAS  Google Scholar 

  • Collings DA, Wasteneys GO, Miyazaki M, Williamson RE (1994) Elongation factor lα is a component of the subcortical actin bundles of characean algae. Cell Biol Int 18: 1019–1024

    Article  PubMed  CAS  Google Scholar 

  • — —, Williamson RE (1995) Cytochalasin rearranges cortical actin of the algaNitella into short, stable rods. Plant Cell Physiol 36: 765–772

    CAS  Google Scholar 

  • — — — (1996) Actin-microtubule interactions in the algaNitella: analysis of the mechanism by which microtubule depolymerization potentiates cytochalasin’s effects on streaming. Protoplasma 191: 178–190

    Article  CAS  Google Scholar 

  • —, Asada T, Allen NS, Shibaoka H (1998) Plasma membrane-associated actin in bright yellow 2 tobacco cells. Plant Physiol 118: 917–928

    Article  PubMed  CAS  Google Scholar 

  • Cooper JA (1987) Effects of cytochalasin and phalloidin on actin. J Cell Biol 105: 1473–1478

    Article  PubMed  CAS  Google Scholar 

  • Durso NA, Cyr RJ (1994) Beyond translation: elongation factor-1-alpha and the cytoskeleton. Protoplasma 180: 99–105

    Article  CAS  Google Scholar 

  • Foissner I, Wasteneys GO (1994) Injury toNitella internodal cells alters microtubule organization but microtubules are not involved in the wound response. Protoplasma 182: 102–114

    Article  Google Scholar 

  • — — (1997) A cytochalasin-sensitive actin filament meshwork is a prerequisite for local wound wall deposition inNitella internodal cells. Protoplasma 200: 17–30

    Article  CAS  Google Scholar 

  • — — (1998) Taxol stabilizes microtubules in characean internodal cells but does not prevent their disassembly at wound sites. Cell Biol Int 21: 866–868 (1997)

    Google Scholar 

  • — — (1999) Microtubules at wound sites ofNitella internodal cells passively co-align with actin bundles when exposed to hydrodynamic forces generated by cytoplasmic streaming. Planta 208: 480–490

    Article  CAS  Google Scholar 

  • — — (2000) Actin in characean internodal cells. In: Baluska F, Barlow PW, Staiger CJ, Volkmann D (eds) Actin: a dynamic framework for multiple plant cell functions. Kluwer, Dordrecht, pp 259–274

    Google Scholar 

  • —, Lichtscheidl IK, Wasteneys GO (1996) Actin-based vesicle dynamics and exocytosis during wound wall formation in characean internodal cells. Cell Motil Cytoskeleton 35: 35–48

    Article  PubMed  CAS  Google Scholar 

  • Heslop-Harrison J, Heslop-Harrison Y (1991) Restoration of movement and apical growth in the angiosperm pollen tube following cytochalasin-induced paralysis. Philos Trans R Soc Lond B Biol Sci 331: 225–235

    Google Scholar 

  • Goode BL, Drubin DG, Barnes G (2000) Functional cooperation between the microtubule and actin cytoskeletons. Curr Opin Cell Biol 12: 63–71

    Article  PubMed  CAS  Google Scholar 

  • Grolig F, Pierson ES (2000) Cytoplasmic streaming: from flow to track. In: Baluska F, Barlow PW, Staiger CJ, Volkmann D (eds) Actin: a dynamic framework for multiple plant cell functions. Kluwer, Dordrecht, pp 165–190

    Google Scholar 

  • Jarosch R (1976) Dynamic behaviour of the actin fibrils ofNitella based on rapid filament rotation. Biochem Physiol Pflanzen 170: 111–131

    Google Scholar 

  • Kamitsubo E (1972) A “window technique” for detailed observation of characean cytoplasmic streaming. Exp Cell Res 74: 613–616

    Article  PubMed  CAS  Google Scholar 

  • Kersey YM, Hepler PK, Palevitz BA, Wessells NK (1976) Polarity of actin filaments in characean algae. Proc Natl Acad Sci USA 73: 165–167

    Article  PubMed  CAS  Google Scholar 

  • Kuroda K (1990) Cytoplasmic streaming in plant cells. Int Rev Cytol 121: 267–307

    Article  CAS  Google Scholar 

  • Lancelle SA, Hepler PK (1988) Cytochalasin-induced structural alterations inNicotiana pollen tubes. Protoplasma Suppl 2: 65–75

    Google Scholar 

  • Leung CL, Sun DM, Zhang M, Knowles DR, Liem RKH (1999) Microtubule actin cross-linking factor (MACF): a hybrid of dystonin and dystrophin that can interact with the actin and microtubule cytoskeletons. J Cell Biol 147, 1275–1285

    Article  PubMed  CAS  Google Scholar 

  • Lichtscheidl IK (1995) Organelle motility in plant cells:Allium cepa inner epidermis. Wiss Film 47: 111–125

    Google Scholar 

  • Miller DD, de Ruijter NCA, Bisseling T, Emons AMC (1999) The role of actin in root hair morphogenesis: studies with lipochitooligosaccharide as a growth stimulator and cytochalasin as an actin perturbing drug. Plant J 17: 141–154

    Article  CAS  Google Scholar 

  • Moore RC, Durso NA, Cyr RJ (1998) Elongation factor-1 alpha stabilizes microtubules in a calcium/calmodulin-dependent manner. Cell Motil Cytoskeleton 41: 168–180

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Palevitz BA (1988) Cytochalasin-induced reorganization of actin inAllium root cells. Cell Motil Cytoskeleton 9: 283–298

    Article  CAS  Google Scholar 

  • Sawitzky H, Liebe S, Willingale-Theune J, Menzel D (1999) The antiproliferative agent jasplakinolide rearranges the actin cytoskeleton of plant cells. Eur J Cell Biol 78: 424–433

    PubMed  CAS  Google Scholar 

  • Shimmen T, Yokota E (1994) Physiological and biochemical aspects of cytoplasmic streaming. Int Rev Cytol 155: 97–139

    CAS  Google Scholar 

  • Sider JR, Mandato CA, Weber KL, Zandy AJ, Beach D, Finst RJ, Skoble J, Bement WM (1999) Direct observations of microtubule-f-actin interaction in cell free lysates. J Cell Sci 112: 1947–1956

    PubMed  CAS  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 

  • Spector I, Braet F, Shochet NR, Bubb MR (1999) New anti-actin drugs in the study of the organization and function of the actin cytoskeleton. Microsc Res Tech 47: 18–37

    Article  PubMed  CAS  Google Scholar 

  • Suda M, Fukui M, Sogabe Y, Sato K, Morimatsu A, Arai R, Motegi F, Miyakawa T, Mabuchi I, Hirata D (1999) Overproduction of elongation factor 1 alpha, an essential translational component, causes aberrant cell morphology by affecting the control of growth polarity in fission yeast. Genes Cells 4: 517–527

    Article  PubMed  CAS  Google Scholar 

  • Tominaga M, Morita K, Sonobe E, Yokata E, Shimmen T (1997) Microtubules regulate the organization of actin filaments at the cortical region in root hair cells ofHydrocharis. Protoplasma 199: 83–92

    CAS  Google Scholar 

  • Wasteneys GO, Williamson RW (1991) Endoplasmic microtubules and nucleus-associated actin rings inNitella internodal cells. Protoplasma 162: 86–98

    Google Scholar 

  • —, Collings DA, Gunning BES, Hepler PK, Menzel D (1996) Actin in living and fixed characean internodal cells: identification of a cortical array of fine actin strands and chloroplast actin rings. Protoplasma 190: 25–38

    Article  CAS  Google Scholar 

  • Williamson RE (1975) Cytoplasmic streaming in Chara: a cell model activated by ATP and inhibited by cytochalasin B. J Cell Sci 17: 655–668

    PubMed  CAS  Google Scholar 

  • — (1978) Cytochalasin B stabilises the sub-cortical actin bundles ofChara against a solution of low ionic strength. Cytobiologie 18: 107–113

    PubMed  CAS  Google Scholar 

  • — (1985) Immobilisation of organelles and actin bundles in the cortical cytoplasm of the algaChara corallina Klein ex Wild. Planta 163: 1–8

    Article  CAS  Google Scholar 

  • — (1992) Cytoplasmic streaming in characean algae: mechanism, regulation by Ca2+, and organization. In: Melkonian M (ed) Algal cell motility. New York, Chapman and Hall, pp 73–98

    Google Scholar 

  • Williamson RE, Hurley UA (1986) Growth and regrowth of actin bundles inChara: bundle assembly by mechanisms differing in sensitivity to cytochalasin. J Cell Sci 85: 21–32

    PubMed  CAS  Google Scholar 

  • — —, Perkin JL (1984) Regeneration of actin bundles inChara: polarized growth and orientation by endoplasmic flow. Eur J Cell Biol 34: 221–228

    PubMed  CAS  Google Scholar 

  • —, Grolig F, Hurley UA, Jablonski PP, McCurdy DW, Wasteneys GO (1989) Methods for studying the plant cytoskeleton. In: Linskens HF, Jackson JF (eds) Plant fibers. Springer, Berlin Heidelberg New York Tokyo, pp 203–218 (Linskens HF, Jackson JF [eds] Modern methods of plant analysis, new series, vol 10)

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut für Pflanzenphysiologie, Universität Salzburg, Hellbrunnerstrasse 34, A-5020, Salzburg, Austria

    I. Foissner

  2. Plant Cell Biology Group, Research School of Biological Sciences, Australian National University, Canberra

    G. O. Wasteneys

Authors
  1. I. Foissner
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. G. O. Wasteneys
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to I. Foissner.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Foissner, I., Wasteneys, G.O. Microtubule disassembly enhances reversible cytochalasin-dependent disruption of actin bundles in characean internodes. Protoplasma 214, 33–44 (2000). https://doi.org/10.1007/BF02524260

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02524260

Keywords

Search

Navigation