Skip to main content
SpringerLink
Log in

Cytoplasmic streaming enables the distribution of molecules and vesicles in large plant cells

  • New Ideas in Cell Biology
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

Recent studies of aquatic and land plants show that similar phenomena determine intracellular transport of organelles and vesicles. This suggests that aspects of cell signaling involved in development and response to external stimuli are conserved across species. The movement of molecular motors along cytoskeletal filaments directly or indirectly entrains the fluid cytosol, driving cyclosis (i.e., cytoplasmic streaming) and affecting gradients of molecular species within the cell, with potentially important metabolic implications as a driving force for cell expansion. Research has shown that myosin XI functions in organelle movement driving cytoplasmic streaming in aquatic and land plants. Despite the conserved cytoskeletal machinery propelling organelle movement among aquatic and land plants, the velocities of cyclosis in plant cells varies according to cell types, developmental stage of the cell, and plant species. Here, we synthesize recent insights into cytoplasmic streaming, molecular gradients, cytoskeletal and membrane dynamics, and expand current cellular models to identify important gaps in current research.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Allen N, Allen R (1978a) Cytoplasmic streaming in green plants. Annu Rev Biophys Bioeng 7:497–526

    Article  CAS  PubMed  Google Scholar 

  • Allen R, Allen N (1978b) Cytoplasmic streaming in ameboid movement. Annu Rev Biophys Bioeng 7:469–495

    Article  CAS  PubMed  Google Scholar 

  • Avisar D, Prokhnevsky AI, Makarova KS, Koonin EV, Dolja VV (2008) Myosin XI-K Is required for rapid trafficking of Golgi stacks, peroxisomes, and mitochondria in leaf cells of Nicotiana benthamiana. Plant Physiol 146(3):1098–1108

    Article  CAS  PubMed  Google Scholar 

  • Cardenas L, Lovy-Wheeler A, Wilsen KL, Hepler PK (2005) Actin polymerization promotes the reversal of streaming in the apex of pollen tubes. Cell Motil Cytoskeleton 61(2):112–127

    Article  CAS  PubMed  Google Scholar 

  • Cardenas L, Lovy-Wheeler A, Kunkel JG, Hepler PK (2008) Pollen tube growth oscillations and intracellular calcium levels are reversibly modulated by actin polymerization. Plant Physiol 146(4):1611–1621

    Article  CAS  PubMed  Google Scholar 

  • Chen KM, Wu GL, Wang YH, Tian CT, Samaj J, Baluska F, Lin JX (2008) The block of intracellular calcium release affects the pollen tube development of Picea wilsonii by changing the deposition of cell wall components. Protoplasma 233(1–2):39–49

    Article  CAS  PubMed  Google Scholar 

  • Cole L, Orlovich D, Ashford A (1998) Structure, function, and motility of vacuoles in filamentous fungi. Fungal Genet Biol 24:86–100

    Article  PubMed  Google Scholar 

  • Ellgaard L, Helenius A (2001) ER quality control: towards an understanding at the molecular level. Curr Opin Cell Biol 13(4):431–437

    Article  CAS  PubMed  Google Scholar 

  • Emons AMC (1987) The cytoskeleton and secretory vesicles in root hairs of Equisetum and Limnobium and cytoplasmic streaming in root hairs of Equisetum. Annu Bot 60:625–632

    Google Scholar 

  • Esseling-Ozdoba A, Houtman D, Van Lammeren AAM, Eiser E, Emons AMC (2008) Hydrodynamic flow in the cytoplasm of plant cells. J Microscopy 231:274–283

    Article  CAS  Google Scholar 

  • Foissner I, Wasteneys GO (2007) Wide-ranging effects of eight cytochalasins and latrunculin A and B on intracellular motility and actin filament reorganization in characean internodal cells. Plant Cell Physiol 48(4):585–597

    Article  CAS  PubMed  Google Scholar 

  • Goldstein RE, Tuval I, van de Meent JW (2008) Microfluidics of cytoplasmic streaming and its implications for intracellular transport. Proc Natl Acad Sci USA 105(10):3663–3667

    Article  CAS  PubMed  Google Scholar 

  • Hancock J (1968) Effect of infection by Hypomyces solani f. sp. Cucurbitae on apparent free space, cell membrane permeability, and respiration of squash hypocotyls. Plant Physiol 43:1666–1672

    Article  CAS  PubMed  Google Scholar 

  • Hayashi T, Takagi S (2003) Ca2+-dependent cessation of cytoplasmic streaming induced by hypertonic treatment in Vallisneria mesophyll cells: possible role of cell wall-plasma membrane adhesion. Plant Cell Physiol 44(10):1027–1036

    Article  CAS  PubMed  Google Scholar 

  • Hepler PK, Vidali L, Cheung AY (2001) Polarized cell growth in higher plants. Annu Rev Cell Dev Biol 17:159–187

    Article  CAS  PubMed  Google Scholar 

  • Hochachka PW (1999) The metabolic implications of intracellular circulation. Proc Natl Acad Sci USA 96:12233–12239

    Article  CAS  PubMed  Google Scholar 

  • Ihara-Ohori Y, Nagano M, Muto S, Uchimiya H, Kawai-Yamada M (2007) Cell death suppressor Arabidopsis bax inhibitor-1 is associated with calmodulin binding and ion homeostasis. Plant Physiol 143(2):650–660

    Article  CAS  PubMed  Google Scholar 

  • Ito K, Ikebe M, Kashiyama T, Mogami T, Kon T, Yamamoto K (2007) Kinetic mechanism of the fastest motor protein, Chara myosin. J Biol Chem 282(27):19534–19545

    Article  CAS  PubMed  Google Scholar 

  • Jedd G, Chua NH (2002) Visualization of peroxisomes in living plant cells reveals acto-myosin-dependent cytoplasmic streaming and peroxisome budding. Plant Cell Physiol 43(4):384–392

    Article  CAS  PubMed  Google Scholar 

  • Justus CD, Anderhag P, Goins JL, Lazzaro MD (2004) Microtubules and microfilaments coordinate to direct a fountain streaming pattern in elongating conifer pollen tube tips. Planta 219(1):103–109

    Article  CAS  PubMed  Google Scholar 

  • Kachar B (1985) Direct visualization of organelle movement along actin filaments dissociated from characean algae. Science 227:1355–1357

    Article  CAS  PubMed  Google Scholar 

  • Kachar B, Reese T (1988) The mechanism of cytoplasmic streaming in characean algal cells: sliding of endoplasmic reticulum along actin filaments. J Cell Biol 106:1545–1552

    Article  CAS  PubMed  Google Scholar 

  • Kamiya N, Kuroda K (1956) Velocity distribution of the protoplasmic streaming in Nitella cells. Bot Mag Tokyo 69:544–554

    Google Scholar 

  • Lazzaro MD, Cardenas L, Bhatt AP, Justus CD, Phillips MS, Holdaway-Clarke TL, Hepler PK (2005) Calcium gradients in conifer pollen tubes; dynamic properties differ from those seen in angiosperms. J Exp Bot 56:2619–2628

    Article  CAS  PubMed  Google Scholar 

  • Li JF, Nebenfuhr A (2008) Inter-dependence of dimerization and organelle binding in myosin XI. Plant J 55(3):478–490

    Article  CAS  PubMed  Google Scholar 

  • Mertz S, Arntzen C (1977) Selective inhibition of K+, Na+, Cl-, and PO 3-4 uptake in Zea mays L. by Bipolaris (Helminthosporium) maydis Race T pathotoxin. Plant Physiol 60:363–369

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Moutinho A, Trewavas AJ, Malho R (1998) Relocation of a Ca2+-dependent protein kinase activity during pollen tube reorientation. Plant Cell 10(9):1499–1510

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Navazio L, Mariani P, Sanders D (2001) Mobilization of Ca2+ by cyclic ADP-ribose from the endoplasmic reticulum of cauliflower florets. Plant Physiol 125(4):2129–2138

    Article  CAS  PubMed  Google Scholar 

  • Nebenfuhr A, Gallagher L, Dunahay T, Frohlick J, Mazurkiewicz A, Meehl J, LA S (1999) Stop-and-go movements of plant Golgi stacks are mediated by the acto-myosin system. Plant Physiol 121(14):1127–1142

    Article  CAS  PubMed  Google Scholar 

  • Nieman R, Willis C (1971) Correlation between the suppression of glucose and phosphate uptake and the release of protein from viable carrot root cells treated with monovalent cations. Plant Physiol 1971:287–293

    Article  Google Scholar 

  • Obermeyer G, Weisenseel MH (1991) Calcium channel blocker and calmodulin antagonists affect the gradient of free calcium ions in lily pollen tubes. Eur J Cell Biol 56(2):319–327

    CAS  PubMed  Google Scholar 

  • Parton RM, Fischer-Parton S, Trewavas AJ, Watahiki MK (2003) Pollen tubes exhibit regular periodic membrane trafficking events in the absence of apical extension. J Cell Sci 116(Pt 13):2707–2719

    Article  CAS  PubMed  Google Scholar 

  • Peremyslov VV, Prokhnevsky AI, Avisar D, Dolja VV (2008) Two class XI myosins function in organelle trafficking and root hair development in Arabidopsis. Plant Physiol 146(3):1109–1116

    Article  CAS  PubMed  Google Scholar 

  • Pickard BG, Ding JP (1993) The mechanosensory calcium-selective ion channel: key component of a plasmalemmal control centre? Aust J Plant Physiol 20:439–459

    Article  CAS  PubMed  Google Scholar 

  • Pickard W (2003) The role of cytoplasmic streaming in symplastic transport. Plant Cell Environ 26:1–15

    Article  CAS  Google Scholar 

  • Pickard WF (2006) Absorption by a moving spherical organelle in a heterogeneous cytoplasm: implications for the role of trafficking in a symplast. J Theor Biol 240:288–301

    Article  PubMed  Google Scholar 

  • Pike SM, Zhang XC, Gassmann W (2005) Electrophysiological characterization of the Arabidopsis avrRpt2-specific hypersensitive response in the absence of other bacterial signals. Plant Physiol 138(2):1009–1017

    Article  CAS  PubMed  Google Scholar 

  • Prokhnevsky AI, Peremyslov VV, Dolja VV (2008) Overlapping functions of the four class XI myosins in Arabidopsis growth, root hair elongation, and organelle motility. Proc Natl Acad Sci USA 105(50):19744–19749

    Article  CAS  PubMed  Google Scholar 

  • Romeis T, Ludwig AA, Martin R, Jones JD (2001) Calcium-dependent protein kinases play an essential role in a plant defence response. Embo J 20(20):5556–5567

    Article  CAS  PubMed  Google Scholar 

  • Sattarzadeh A, Franzen R, Schmelzer E (2008) The Arabidopsis class VIII myosin ATM2 is involved in endocytosis. Cell Motil Cytoskeleton 65(6):457–468

    Article  CAS  PubMed  Google Scholar 

  • Shimmen T, Yokota E (2004) Cytoplasmic streaming in plants. Curr Opin Cell Biol 16(1):68–72

    Article  CAS  PubMed  Google Scholar 

  • Sieber B, Emons AMC (2000) Cytoarchitecture and pattern of cytoplasmic streaming in root hairs of Medicago truncatula during development and deformation by nodulation factors. Protoplasma 214:118–127

    Article  Google Scholar 

  • Sparkes IA, Teanby NA, Hawes C (2008) Truncated myosin XI tail fusions inhibit peroxisome, Golgi, and mitochondrial movement in tobacco leaf epidermal cells: a genetic tool for the next generation. J Exp Bot 59(9):2499–2512

    Article  CAS  PubMed  Google Scholar 

  • Sumiyoshi H, Ooguchi M, Ooi A, Okagaki T, Higashi-Fujime S (2007) Insight into the mechanism of fast movement of myosin from Chara corallina. Cell Motil Cytoskeleton 64(2):131–142

    Article  CAS  PubMed  Google Scholar 

  • Takagi S, Kong SG, Mineyuki Y, Furuya M (2003) Regulation of actin-dependent cytoplasmic motility by type II phytochrome occurs within seconds in Vallisneria gigantea epidermal cells. Plant Cell 15(2):331–345

    Article  CAS  PubMed  Google Scholar 

  • van de Meent JW, Tuval I, Goldstein RE (2008) Nature's microfluidic transporter: rotational cytoplasmic streaming at high Peclet numbers. Phys Rev Lett 101(17):178102

    Article  PubMed  Google Scholar 

  • van de Meent JW, Sederman AJ, Gladden LF, Goldstein RE (2010) Measurement of cytoplasmic streaming in single plant cells by magnetic resonance velocimetry. J Fluid Mech. (in press)

  • Vidali L, McKenna ST, Hepler PK (2001) Actin polymerization is essential for pollen tube growth. Mol Biol Cell 12(8):2534–2545

    CAS  PubMed  Google Scholar 

  • Volkmann D, Mori T, Tirlapur UK, Konig K, Fujiwara T, Kendrick-Jones J, Baluska F (2003) Unconventional myosins of the plant-specific class VIII: endocytosis, cytokinesis, plasmodesmata/pit-fields, and cell-to-cell coupling. Cell Biol Int 27(3):289–291

    Article  CAS  PubMed  Google Scholar 

  • Walter N, Holweg CL (2008) Head-neck domain of Arabidopsis myosin XI, MYA2, fused with GFP produces F-actin patterns that coincide with fast organelle streaming in different plant cells. BMC Plant Biol 8:74

    Article  PubMed  Google Scholar 

  • Yamamoto K, Shimada K, Ito K, Hamada S, Ishijima A, Tsuchiya T, Tazawa M (2006) Chara myosin and the energy of cytoplasmic streaming. Plant Cell Physiol 47(10):1427–1431

    Article  CAS  PubMed  Google Scholar 

  • Yokota E, Muto S, Shimmen T (1999) Inhibitory regulation of higher-plant myosin by Ca2+ ions. Plant Physiol 119(1):231–240

    Article  CAS  PubMed  Google Scholar 

  • Zhang K, Kaufman RJ (2006) The unfolded protein response: a stress signaling pathway critical for health and disease. Neurology 66(2 Suppl 1):S102–S109

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank an anonymous reviewer for excellent and careful edits and suggestions and are grateful to J. Carr, J. Davies, E. MacRobbie, I. Tuval, J.-W. van de Meent, and A. Webb for important discussions. This work was supported in part by a USDA CSREES-NRI-2007-01530 Research Sabbatical Grant and OCAST ONAP08-018 (J.V.L.), the Leverhulme Trust and the Schlumberger Chair Fund (R.E.G.), and Oklahoma Center for Advancement of Science and Technology Contract number 7141.

Conflict of Interest

The authors have no conflict of interest. We have no financial relationship with the organization that sponsored the research.

Author information

Authors and Affiliations

  1. Department of Entomology and Plant Pathology, Oklahoma State University, Stillwater, OK, 74078, USA

    Jeanmarie Verchot-Lubicz

  2. Department of Applied Mathematics and Theoretical Physics, Centre for Mathematical Sciences, University of Cambridge, Wilberforce Road, Cambridge, CB3 0WA, UK

    Raymond E. Goldstein

Authors
  1. Jeanmarie Verchot-Lubicz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Raymond E. Goldstein
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jeanmarie Verchot-Lubicz.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Verchot-Lubicz, J., Goldstein, R.E. Cytoplasmic streaming enables the distribution of molecules and vesicles in large plant cells. Protoplasma 240, 99–107 (2010). https://doi.org/10.1007/s00709-009-0088-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-009-0088-x

Keywords

Search

Navigation