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Measurement of cytoplasmic streaming in single plant cells by magnetic resonance velocimetry

Published online by Cambridge University Press:  11 December 2009

JAN-WILLEM VAN DE MEENT ,
ANDY J. SEDERMAN ,
LYNN F. GLADDEN  and
RAYMOND E. GOLDSTEIN
JAN-WILLEM VAN DE MEENT
Affiliation:
Instituut-Lorentz, Universiteit Leiden, Postbus 9506, 2300 RA Leiden, The Netherlands Department of Applied Mathematics and Theoretical Physics, University of Cambridge, Wilberforce Road, Cambridge CB3 0WA, UK
ANDY J. SEDERMAN
Affiliation:
Department of Chemical Engineering and Biotechnology, University of Cambridge, Pembroke Street, Cambridge CB2 3RA, UK
LYNN F. GLADDEN
Affiliation:
Department of Chemical Engineering and Biotechnology, University of Cambridge, Pembroke Street, Cambridge CB2 3RA, UK
RAYMOND E. GOLDSTEIN*
Affiliation:
Department of Applied Mathematics and Theoretical Physics, University of Cambridge, Wilberforce Road, Cambridge CB3 0WA, UK
*
†Email address for correspondence: [email protected]
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Abstract

In the giant cylindrical cells found in Characean algae, multitudes of the molecular motor myosin transport the cytoplasm along opposing spiralling bands covering the inside of the cell wall, generating a helical shear flow in the large central vacuole. It has been suggested that such flows enhance mixing within the vacuole (van de Meent, Tuval & Goldstein, Phys. Rev. Lett., vol. 101, 2008, paper no. 178102) and thereby play a role in regulating metabolism. For this to occur the membrane that encloses the vacuole, namely the tonoplast, must transmit efficiently the hydrodynamic shear generated in the cytoplasm. Existing measurements of streaming flows are of insufficient spatial resolution and extent to provide tests of fluid mechanical theories of such flows and information on the shear transmission. Here, using magnetic resonance velocimetry (MRV), we present the first measurements of cytoplasmic streaming velocities in single living cells. The spatial variation of the longitudinal velocity field in cross-sections of internodal cells of Chara corallina is obtained with spatial resolution of 16 μm and is shown to be in quantitative agreement with a recent theoretical analysis (Goldstein, Tuval & van de Meent, Proc. Natl. Acad. Sci. USA, vol. 105, 2008, p. 3663) of rotational cytoplasmic streaming driven by bidirectional helical forcing in the cytoplasm, with direct shear transmission by the tonoplast. These results highlight the open problem of understanding tonoplast motion induced by streaming. Moreover, this study suggests the suitability of MRV in the characterization of streaming flows in a variety of eukaryotic systems and for microfluidic phenomena in general.

JFM classification

Biological Fluid Dynamics: Biological Fluid Dynamics Low-Reynolds-number flows: Low-Reynolds-number flows
Type
Papers
Information
Journal of Fluid Mechanics , Volume 642 , 10 January 2010 , pp. 5 - 14
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Akpa, B. S., Matthews, S. M., Sederman, A. J., Yunus, K., Fisher, A. C., Johns, M. L. & Gladden, L. F. 2007 Study of miscible and immiscible flows in a microchannel using magnetic resonance imaging. Anal. Chem. 79, 6128–6134.CrossRefGoogle Scholar
Aussillous, P., Sederman, A. J., Gladden, L. F., Huppert, H. E. & Worster, M. G. 2006 Magnetic resonance imaging of structure and convection in solidifying mushy layers. J. Fluid Mech. 552, 99–125.CrossRefGoogle Scholar
Callaghan, P. T. 1993 Principles of Nuclear Magnetic Resonance Microscopy. Clarendon.Google Scholar
Choma, M. A., Ellerbee, A. K., Yazdanfar, S. & Izatt, J. A. 2006 Doppler flow imaging of cytoplasmic streaming using spectral domain phase microscopy. J. Biomed. Opt. 11, 024014.CrossRefGoogle ScholarPubMed
Corti, B. 1774 Osservazione Microscopische sulla Tremella e sulla Circulazione del Fluido in Una Planto Acquaguola. Appresso Giuseppe Rocchi.Google Scholar
Cutler, S. R., Ehrhardt, D. W., Griffitts, J. S. & Somerville, C. R. 2000 Random GFP::cDNA fusions enable visualization of subcellular structures in cells of Arabidopsis at a high frequency. Proc. Natl. Acad. Sci. USA 97, 3718–3723.CrossRefGoogle ScholarPubMed
Ding, D. Q., Mimura, T., Amino, S. & Tazawa, M. 1991 Intercellular transport and photosynthetic differentiation in Chara corallina. J. Exp. Bot. 42, 33–38.CrossRefGoogle Scholar
Elkins, C. J. & Alley, M. T. 2007 Magnetic resonance velocimetry: applications of magnetic resonance imaging in the measurement of fluid motion. Exp. Fluids 43, 823–858.CrossRefGoogle Scholar
Esseling-Ozdoba, A., Houtman, D., van Lammeren, A. A. M., Eiser, E. & Emons, A. M. C. 2008 Hydrodynamic flow in the cytoplasm of plant cells. J. Microscopy 231, 274–283.CrossRefGoogle ScholarPubMed
Fischer, T. M., Stohr-Lissen, M. & Schmid-Schonbein, H. 1978 The red cell as a fluid droplet: tank tread-like motion of the human erythrocyte membrane in shear flow. Science 202, 894–896.CrossRefGoogle ScholarPubMed
Forsberg, C. 1965 Nutritional studies of Chara in axenic cultures. Physiol. Plantarum 18, 275–290.CrossRefGoogle Scholar
Goldstein, R. E., Tuval, I. & van de Meent, J. W. 2008 Microfluidics of cytoplasmic streaming and its implications for intracellular transport. Proc. Natl. Acad. Sci. USA 105, 3663–3667.CrossRefGoogle ScholarPubMed
Hochachka, P. W. 1999 The metabolic implications of intracellular circulation. Proc. Natl. Acad. Sci. USA 96, 12233–12239.CrossRefGoogle ScholarPubMed
Houtman, D., Pagonabarraga, I., Lowe, C. P., Esseling-Ozdoba, A., Emons, A. M. C. & Eiser, E. 2007 Hydrodynamic flow caused by active transport along cytoskeletal elements. Europhys. Lett. 78, 18001.CrossRefGoogle Scholar
Huntley, J. M., Martin, T. W., Mantle, M. D., Shattuck, M. D., Sederman, A. J., Wildman, R. D., Gladden, L. F. & Halliwell, N. A. 2007 NMR measurements and hydrodynamics simulations of phase-resolved velocity distributions within three-dimensional vibrofluidized granular bed. Proc. R. Soc. A 463, 2519–2542.CrossRefGoogle Scholar
Kachar, B. 1985 Direct visualization of organelle movement along actin filaments dissociated from characean algae. Science 227 (4692), 1355–1357.CrossRefGoogle ScholarPubMed
Kachar, B. & Reese, T. S. 1988 The mechanism of cytoplasmic streaming in characean algal cells: sliding of endoplasmic reticulum along actin filaments. J. Cell Biol. 106, 1545–1552.CrossRefGoogle ScholarPubMed
Kamiya, N. & Kuroda, K. 1956 Velocity distribution of the protoplasmic streaming in Nitella cells. Bot. Mag. Tokyo 69, 544–554.CrossRefGoogle Scholar
Kantsler, V., Segre, E. & Steinberg, V. 2007 Vesicle dynamics in time-dependent elongation flow: wrinkling instability. Phys. Rev. Lett. 99, 178102.CrossRefGoogle ScholarPubMed
Karol, K. G., McCourt, R. M., Cimino, M. T. & Delwiche, C. F. 2001 The closest living relatives of land plants. Science 294, 2351–2353.CrossRefGoogle ScholarPubMed
Kockenberger, W., De Panfilis, C., Santoro, D., Dahiya, P. & Rawsthorne, S. 2004 High resolution NMR microscopy of plants and fungi. J. Microscopy 214, 182–189.CrossRefGoogle ScholarPubMed
Lucas, W. J. 1975 Photosynthetic fixation of 14carbon by internodal cells of Chara corallina. J. Exp. Bot. 26, 331–346.CrossRefGoogle Scholar
Lucas, W. J. 1995 Plasmodesmata: intercellular channels for macromolecular transport in plants. Curr. Op. Cell Biol. 7, 673–680.CrossRefGoogle ScholarPubMed
van de Meent, J. W., Tuval, I. & Goldstein, R. E. 2008 Nature's microfluidic transporter: rotational cytoplasmic streaming at high Péclet numbers. Phys. Rev. Lett. 101, 178102.CrossRefGoogle ScholarPubMed
Meleshko, V. V., Malyuga, V. S. & Gomilko, A. M. 2000 Steady stokes flow in a finite cylinder. Proc. R. Soc. A 456, 1741–1758.CrossRefGoogle Scholar
Mullin, T., Seddon, J. R. T., Mantle, M. D. & Sederman, A. J. 2009 Bifurcation phenomena in the flow through a sudden expansion in a circular pipe. Phys. Fluids 21, 014110.CrossRefGoogle Scholar
Mustacich, R. V. & Ware, B. R. 1976 A study of protoplasmic streaming in Nitella by laser Doppler spectroscopy. Biophys. J. 16, 373–388.CrossRefGoogle ScholarPubMed
Pickard, W. F. 1972 Further observations on cytoplasmic streaming in Chara braunii. Can. J. Bot. 50, 703–711.CrossRefGoogle Scholar
Pickard, W. F. 1974 Hydrodynamic aspects of protoplasmic streaming in Chara braunii. Protoplasma 82, 321–339.CrossRefGoogle Scholar
Pickard, W. F. 2006 Absorption by a moving spherical organelle in a heterogeneous cytoplasm: implications for the role of trafficking in a symplast. J. Theoret. Biol. 240, 288–301.CrossRefGoogle Scholar
Plieth, C. & Hansen, U. P. 1992 Light dependence of protoplasmic streaming in Nitella flexilis L. as measured by means of laser-velocimetry. Planta 188, 332–339.CrossRefGoogle ScholarPubMed
Scheenen, T. W. J., Vergeldt, F. J., Windt, C. W., de Jager, P. A. & Van As, H. 2001 Microscopic imaging of slow flow and diffusion: a pulsed field gradient stimulated echo sequence combined with turbo spin echo imaging. J. Mag. Res. 151, 94–100.CrossRefGoogle ScholarPubMed
Shimmen, T., Mimura, T., Kikuyama, M. & Tazawa, M. 1994 Characean cells as a tool for studying electrophysiological characteristics of plant cells. Cell Struct. Func. 19, 263–278.CrossRefGoogle ScholarPubMed
Shimmen, T. & Yokota, E. 2004 Cytoplasmic streaming in plants. Curr. Op. Cell Biol. 16, 68–72.CrossRefGoogle ScholarPubMed
Taiz, L. 1992 The plant vacuole. J. Exp. Biol. 172, 113–122.CrossRefGoogle ScholarPubMed
Tazawa, M. 1964 Studies on Nitella having artificial cell sap. Part I. Replacement of the cell sap with artificial solutions. Plant Cell Phys. 5, 33–43.CrossRefGoogle Scholar
Verbelen, J. P. & Tao, W. 1998 Mobile arrays of vacuole ripples are common in plant cells. Plant Cell Rep. 17, 917–920.CrossRefGoogle ScholarPubMed
Windt, C. W., Vergeldt, F. J., De Jager, P. A. & Van As, H. 2006 MRI of long-distance water transport: a comparison of the phloem and xylem flow characteristics and dynamics in poplar, castor bean, tomato and tobacco. Plant Cell Environ. 29, 1715–1729.CrossRefGoogle ScholarPubMed