Skip to main content
Log in

Measuring the Osmotic Water Permeability of the Plant Protoplast Plasma Membrane: Implication of the Nonosmotic Volume

  • Published:
Journal of Membrane Biology Aims and scope Submit manuscript

Abstract

Starting from the original theoretical descriptions of osmotically induced water volume flow in membrane systems, a convenient procedure to determine the osmotic water permeability coefficient (P os) and the relative nonosmotic volume (β) of individual protoplasts is presented. Measurements performed on protoplasts prepared from pollen grains and pollen tubes of Lilium longiflorum cv. Thunb. and from mesophyll cells of Nicotiana tabacum L. and Arabidopsis thaliana revealed low values for the osmotic water permeability coefficient in the range 5–20 μm · s−1 with significant differences in P os, depending on whether β is considered or not. The value of β was determined using two different methods: by interpolation from Boyle-van’t Hoff plots or by fitting a solution of the theoretical equation for water volume flow to the whole volume transients measured during osmotic swelling. The values determined with the second method were less affected by the heterogeneity of the protoplast samples and were around 30% of the respective isoosmotic protoplast volume. It is therefore important to consider nonosmotic volume in the calculation of P os as plant protoplasts behave as nonideal osmometers.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Notes

  1. The term “osmotic active surface” is introduced in accordance to the term “osmotic volume,” although we are aware that a surface area is not osmotically active in a physical sense.

References

  • Ackerson RC, Hebert RR (1981) Osmoregulation in cotton in response to water stress. I. Alterations in photosynthesis, leaf conductance, translocation and ultrastructure. Plant Physiol 67:487–488

    Google Scholar 

  • Chaumont F, Barrieu F, Herman EM, Chrispeels MJ (1998) Characterisation of a maize tonoplast aquaporin expressed in zones of cell division and elongation. Plant Physiol 117:1143–1152

    Article  PubMed  CAS  Google Scholar 

  • Chaumont F, Moshelion M, Daniels MJ (2005) Regulation of plant aquaporin activity. Biol Cell 97:749–764

    Article  PubMed  CAS  Google Scholar 

  • Comparot S, Morillon R, Badot P-M (2000) Water permeability and revolving movement in Phaseolus vulgaris L. twinning shoots. Plant Cell Physiol 41:114–118

    PubMed  CAS  Google Scholar 

  • Dainty J (1963) Water relations in plant cells. Adv Bot Res 1:279–326

    Article  CAS  Google Scholar 

  • Daniels MJ, Mirkov TE, Chrispeels MJ (1994) The plasma membrane of Arabidopsis thaliana contains a mercury-insensitive aquaporin that is a homolog of the tonoplast water channel protein TIP. Plant Physiol 106:1325–1333

    Article  PubMed  CAS  Google Scholar 

  • Denker BM, Smith BL, Kuhaida FP, Agre P (1988) Identification, purification and partial characterization of a novel Mr 28,000 integral membrane protein from erythrocytes and renal tubules. J Biol Chem 263:15634–15642

    PubMed  CAS  Google Scholar 

  • Ding X, Iwasaki I, Kitagawa Y (2004) Overexpression of a lily PIP1 gene in tobacco increased the osmotic water permeability of leaf cells. Plant Cell Environ 27:177–186

    Article  CAS  Google Scholar 

  • Doroshenko P (1999) High intracellular chloride delays the activation of the volume-sensitive chloride conductance in mouse L-fibroblasts. J Physiol 514.2:437–446

    Article  Google Scholar 

  • Dowgert MF, Steponkus PL (1983) Effect of cold acclimation on intracellular ice formation in isolated protoplasts. Plant Physiol 72:978–988

    PubMed  Google Scholar 

  • Echevarria M, Verkman AS (1992) Optical measurement of osmotic water transport in cultured cells. Role of glucose transporters. J Gen Physiol 99:573–89

    Article  PubMed  CAS  Google Scholar 

  • Griessner M, Obermeyer G (2003) Characterization of whole-cell K+ currents across the plasma membrane of pollen grain and tube protoplasts of Lilium longiflorum. J Membr Biol 193:99–108

    Article  PubMed  CAS  Google Scholar 

  • Hill AE, Shachar-Hill B, Shachar-Hill Y (2004) What are aquaporins for? J Membr Biol 197:1–32

    Article  PubMed  CAS  Google Scholar 

  • Homann U (1998) Fusion and fission of plasma membrane material accommodates for osmotically induced changes in the surface area of guard-cell protoplasts. Planta 206:329–333

    Article  CAS  Google Scholar 

  • Hurst AC, Meckel T, Tayefeh S, Thiel G, Homann U (2004) Trafficking of the plant potassium inward rectifier KAT1 in guard cell protoplasts of Vicia faba. Plant J 37:391–397

    Article  PubMed  CAS  Google Scholar 

  • Kaldenhoff R, Grote K, Zhu J-J, Zimmermann U (1998) Significance of plasmalemma aquaporins for water transport in Arabidopsis thaliana. Plant J 14:121–128

    Article  PubMed  CAS  Google Scholar 

  • Kamerloher W, Fisher U, Piechottka GP, Schäffner AR (1994) Water channels in the plant plasma membrane cloned by immunoselection from a mammalian expression system. Plant J 6:187–199

    Article  Google Scholar 

  • Kedem O, Katchalsky A (1958) Thermodynamic analysis of the permeability of biological membranes to non-electrolytes. Biochim Biophys Acta 27:229–246

    Article  PubMed  CAS  Google Scholar 

  • Kirch H-H, Vera-Estrella R, Golldack D, Quigley F, Michalowski B, Barkla BJ, Bohnert HJ (2000) Expression of water channel proteins in Mesembryanthemum crystallinum. Plant Physiol 123:111–124

    Article  PubMed  CAS  Google Scholar 

  • Kubitscheck U, Homann U, Thiel G (2000) Osmotically evoked shrinking of guard-cell protoplasts causes vesicular retrieval of plasma membrane into the cytoplasm. Planta 210:423–431

    Article  PubMed  CAS  Google Scholar 

  • Maurel C, Reizer J, Schroeder JI, Chrispeels MJ (1993) The vacuolar membrane protein γ-TIP creates water specific channels in Xenopus oocytes. EMBO J 12:2241–2247

    PubMed  CAS  Google Scholar 

  • Maurel C, Tacnet F, Güclü J, Guern J, Ripoche P (1997) Purified vesicles of tobacco cell vacuolar and plasma membranes exhibit dramatically different water permeability and water channel activity. Proc Natl Acad Sci USA 94:7103–7108

    Article  PubMed  CAS  Google Scholar 

  • Mlekoday HJ, Moore R, Levitt DG (1983) Osmotic water permeability of human red cell. Dependence on direction of water flow and cell volume. J Gen Physiol 81:213–220

    Article  PubMed  CAS  Google Scholar 

  • Morillon R, Chrispeels MJ (2001) The role of ABA and the transpiration stream in the regulation of the osmotic water permeability of leaf cells. Proc Natl Acad Sci USA 98:14138–14143

    Article  PubMed  CAS  Google Scholar 

  • Morillon R, Lassalles J-P (2002) Water deficit during root development: effects on the growth of roots and on water permeability of isolated root protoplasts. Planta 214:392–399

    Article  PubMed  CAS  Google Scholar 

  • Morris CE, Homann U (2001) Cell surface area regulation and membrane tension. J Membr Biol 179:79–102

    PubMed  CAS  Google Scholar 

  • Moshelion M, Becker D, Biela A, Uehlein N, Hedrich R, Otto B, Levi H, Moran N, Kaldenhoff R (2002) Plasma membrane aquaporins in the motor cells of Samanea saman: diurnal and circadian regulation. Plant Cell 14:727–739

    Article  PubMed  CAS  Google Scholar 

  • Moshelion M, Moran N, Chaumont F (2004) Dynamic changes in the osmotic water permeability of protoplast plasma membrane. Plant Physiol 135:2301–2317

    Article  PubMed  CAS  Google Scholar 

  • Niemietz CM, Tyerman SD (1997) Characterization of water channels in wheat root membrane vesicles. Plant Physiol 115:561–567

    PubMed  CAS  Google Scholar 

  • Ohshima Y, Iwasaki I, Suga S, Murakami M, Inoue K, Maeshima M (2001) Low aquaporin content and low osmotic water permeability of the plasma and vacuolar membranes of a CAM plant Graptopetalum paraguayense: comparison with radish. Plant Cell Physiol 42:1119–1129

    Article  PubMed  CAS  Google Scholar 

  • Olbrich K, Rawicz W, Needham D, Evans E (2000) Water permeability and mechanical strength of polyunsaturated lipid bilayers. Biophys J 79:321–327

    PubMed  CAS  Google Scholar 

  • Preston GM, Carroll TP, Guggino WB, Agre P (1992) Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science 256:385–387

    Article  PubMed  CAS  Google Scholar 

  • Quigley F, Rosenberg JM, Shachar-Hill Y, Bohnert HJ (2001) From genome to function: the Arabidopsis aquaporins. Genom Biol 3:1–17

    Google Scholar 

  • Rabinowitch S, Grover NB, Ginzburg BZ (1975) Cation effects on volume and water permeability in the halophilic algae Dunaliella parva. J Membr Biol 22:211–230

    Article  PubMed  CAS  Google Scholar 

  • Ramahaleo T, Morillon R, Alexandre J, Lasalles J-P (1999) Osmotic water permeability of isolated protoplasts. Modifications during development. Plant Physiol 119:885–896

    Article  PubMed  CAS  Google Scholar 

  • Raucher D, Sheetz M (1999) Characteristics of a membrane reservoir buffering membrane tension. Biophys J 77:1992–2002

    PubMed  CAS  Google Scholar 

  • Reed RH, Chudek JA, Foster R, Gadd GM (1987) Osmotic significance of glycerol accumulation in exponentially growing yeasts. Appl Environ Microbiol 53:2119–2123

    PubMed  CAS  Google Scholar 

  • Shope JC, DeWald DB, Mott KA (2003) Changes in surface area of intact guard cells are correlated with membrane internalization. Plant Physiol 133:1314–1321

    Article  PubMed  CAS  Google Scholar 

  • Siefritz F, Biela A, Eckert M, Otto B, Uehlein N, Kaldenhoff R (2001) The tobacco plasma membrane aquaporin NtAQP1. J Exp Bot 52:1953–1957

    Article  PubMed  CAS  Google Scholar 

  • Steponkus PL (1984) Role of the plasma membrane in freezing injury and cold acclimation. Annu Rev Plant Physiol 35:543–584

    Article  CAS  Google Scholar 

  • Suga S, Murai M, Kuwagata T, Maeshima M (2003) Differences in aquaporin levels among cell types of radish and measurement of osmotic water permeability of individual protoplasts. Plant Cell Physiol 44:277–286

    Article  PubMed  CAS  Google Scholar 

  • Terwilliger TC, Solomon AK (1981) Osmotic water permeability of human red cells. J Gen Physiol 77:549–570

    Article  PubMed  CAS  Google Scholar 

  • Thiel G, Sutter J-U, Homann U (2000) Ca2+-sensitive and Ca2+-insensitive exocytosis in maize coleotile protoplasts. Pflugers Arch 439:R152–R153

    Article  PubMed  CAS  Google Scholar 

  • Tyerman SD, Bohnert HJ, Maurel C, Steudle E, Smith JAC (1999) Plant aquaporins: their molecular biology, biophysics and significance for plant water relations. J Exp Bot 58:1055–1071

    Article  Google Scholar 

  • van Heeswijk MPE, van Os CH (1986) Osmotic water permeabilities of brush border and basolateral membrane vesicles from rat renal cortex and small intestine. J Membr Biol 92:183–193

    Article  PubMed  Google Scholar 

  • Vera-Estrella R, Barkla BJ, Bohnert HJ, Pantoja O (2004) Novel regulation of aquaporins during osmotic stress. Plant Physiol 135:2318–2329

    Article  PubMed  CAS  Google Scholar 

  • Weyers JDB, Fitzsimons PJ (1982) The nonosmotic volume of Commelina guard cells. Plant Cell Environ 5:417–421

    Article  Google Scholar 

  • Wiest SC, Steponkus PL (1978) Freeze-thaw injury to isolated spinach protoplasts and its simulation at above freezing temperatures. Plant Physiol 62:699–705

    Article  PubMed  CAS  Google Scholar 

  • Williams JM, Williams RJ (1976) Osmotic factors of dehardening in Cornus florida L. Plant Physiol 58:243–247

    PubMed  Google Scholar 

  • Wolfe J, Dowgert MF, Steponkus PL (1986) Mechanical study of the deformation and rupture of the plasma membranes of protoplasts during osmotic expansions. J Membr Biol 93:63–74

    Article  Google Scholar 

  • Zelenina M, Brismar H (2000) Osmotic water permeability measurements using confocal laser scanning microscopy. Eur Biophys J 29:165–171

    Article  PubMed  CAS  Google Scholar 

  • Zhang R, Logee KA, Verkman AS (1990) Expression of mRNA coding for kidney and red cell water channels in Xenopus oocytes. J Biol Chem 265:15375–15378

    PubMed  CAS  Google Scholar 

  • Zhang R, Verkman AS (1991) Water and urea permeability properties of Xenopus oocytes: expression of mRNA from toad urinary bladder. Am J Physiol 260:C26–C34

    PubMed  CAS  Google Scholar 

  • Zimmermann U (1978) Physics of turgor- and osmoregulation. Annu Rev Plant Physiol 29:121–148

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to Prof. Dr. Steve Tyerman (Adelaide University, Australia) and Prof. Dr. Anton Schäffner (GSF-Forschungszentrum für Umwelt und gesundheit, Neuherberg, Germany) for valuable discussions. This work was partially financed by grants from the Austrian Research Foundation FWF-Fond FW Förderung des Wissenschaftlichen Forschung (P 13064, P 17227).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gerhard Obermeyer.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sommer, A., Mahlknecht, G. & Obermeyer, G. Measuring the Osmotic Water Permeability of the Plant Protoplast Plasma Membrane: Implication of the Nonosmotic Volume. J Membrane Biol 215, 111–123 (2007). https://doi.org/10.1007/s00232-007-9011-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00232-007-9011-6

Keywords

Navigation