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The relationship between carbon and water transport in single cells ofChara corallina

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Summary

The hydraulic resistance of the plasma membrane was measured on single internodal cells ofChara corallina using the method of transcellular osmosis. The hydraulic resistance of the plasma membrane of high CO2-grown cells was significantly higher than the hydraulic resistance of the plasma membrane in low CO2-grown cells. Therefore we tested the possibility that the “bicarbonate transport system”, postulated to be present in low CO2-grown cells, serves as a water channel that lowers the hydraulic resistance of the plasma membrane. We were unable to find any correlation between agents that inhibited the “bicarbonate transport system” and agents that increased the hydraulic resistance of low CO2-grown cells. We did, however, find a correlation between the permeability of the cell to water and CO2. We propose that the reduced hydraulic resistance of the plasma membrane of the low CO2-grown cells is a function of a change in either the structural properties of the lipid bilayer or the activity of a CO2 transport protein so that under conditions of reduced inorganic carbon, the plasma membrane becomes more permeable to CO2, and consequently to other small molecules, including H2O, methanol and ethanol.

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References

  • Adams RJ, Pollard TD (1989) Binding of myosin-I to membrane lipids. Nature 340: 565–588

    PubMed  Google Scholar 

  • Aizawa, K, Miyachi S (1986) Carbonic anhydrase and CO2 concentrating mechanisms in microalgae and cyanobacteria. FEMS Microbiol Rev 39: 215–233

    Google Scholar 

  • Aloia RC (ed) (1983) Membrane fluidity in biology, vol 2, general principles. Academic Press, New York

    Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase inBeta vulgaris. Plant Physiol 24: 1–15

    Google Scholar 

  • Badger MR (1987) The CO2-concentrating mechanism in aquatic phototrophs In: Hatch MD, Boardman NK (eds) The biochemistry of plants. A comprehensive treatise, vol 10, photosynthesis. Academic Press, San Diego, pp 219–274

    Google Scholar 

  • Barber RF, Thompson JE (1980) Senescence-dependent increase in the permeability of liposomes prepared from bean cotyledon membranes. J Exp Bot 31: 1305–1313

    Google Scholar 

  • Benga G (1989) Water exchange through the erythrocyte membrane. Int Rev Cytol 114: 273–316

    PubMed  Google Scholar 

  • Boyer JS (1990) Photosynthesis in dehydrating plants. Bot Mag (Special Issue 2): 73–85

  • Brechignac F, Lucas WJ (1987) Photorespiration and internal CO2 accumulation inChara corallina as inferred from the influence of DIC and O2 on photosynthesis. Plant Physiol 83: 163–169

    Google Scholar 

  • Cass A, Finkelstein A (1967) Water permeability of thin lipid membrane. J Gen Physiol 50: 1765–1784

    PubMed  Google Scholar 

  • Chang HT, Loomis WE (1945) Effect of carbon dioxide on absorption of water and nutrients by roots. Plant Physiol 20: 221–232

    Google Scholar 

  • Cullis PR, de Kruijff B, Hope MJ, Verkleij AJ, Nayar R, Farren SB, Tilcock C, Madden TD, Bally MB (1983) Structural properties of lipids and their functional roles in biological membranes. In: Aloia RC (ed) Membrane fluidity in biology, vol 1, concepts of membrane structures. Academic Press, New York, pp 39–81

    Google Scholar 

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

    Google Scholar 

  • — (1964) Osmotic flow. Symp Soc Exp Biol 19: 75–85

    Google Scholar 

  • —, Ginzburg B (1964 a) The measurement of hydraulic conductivity (osmotic permeability to water) of internodal characean cells by means of transcellular osmosis. Biochim Biophys Acta 79: 102–111

    PubMed  Google Scholar 

  • — — (1964 b) The permeability of the cell membranes ofNitella translucens to urea and the effect of high concentrations of succrose on this permeability. Biochim Biophys Acta 79: 112–121

    PubMed  Google Scholar 

  • — — (1964 c) The reflection coefficient of plant cell membranes for certain solutes. Biochim Biophys Acta 79: 129–137

    PubMed  Google Scholar 

  • —, Hope AB (1959) The water permeability of cells ofChara australis R Br. Aust J Biol Sci 12: 136–145

    Google Scholar 

  • Ding D-Q, Mimura T, Amino S, Tazawa M (1991) Intracellular transport and photosynthetic differentiation inChara corallina. J Exp Bot 42: 33–38

    Google Scholar 

  • —, Amino S, Mimura T, Sakano K, Nagata T, Tazawa M (1992) Quantitative analysis of intracellularly transported photoassimilates inChara corallina. J Exp Bot 43: 1045–1051

    Google Scholar 

  • Ferrier JM (1980) Apparent bicarbonate uptake and possible plasmalemma proton efflux inChara corallina. Plant Physiol 66: 1198–1199

    Google Scholar 

  • Findenegg GR (1974) Beziehungen zwischen Carboanhydraseaktivität und Aufnahme von HCO3 − und C1− bei der Photosynthese vonScenedesmus obliquus. Planta 116: 123–131

    Google Scholar 

  • Finkelstein A (1987) Water movement through lipid bilayers, pores, and plasma membranes. Theory and reality. Wiley, New York (Distinguished lecture series of the Society of General Physiologists, vol 4)

    Google Scholar 

  • Gimmler H, Weiss C, Baier M, Hartung W (1990) The conductance of the plasmalemma for carbon dioxide. J Exp Bot 41: 785–794

    Google Scholar 

  • Ginzburg BZ, Katchalsky A (1963) The frictional coefficients of the flows of non-electrolytes through artificial membranes. J Gen Physiol 47: 403–418

    PubMed  Google Scholar 

  • Glinka Z, Reinhold L (1962) Rapid changes in permeability of cell membranes to water brought about by carbon dioxide and oxygen. Plant Physiol 37: 481–486

    Google Scholar 

  • Grassl SM, Holohan PD, Ross CR (1987) HCO3 − transport in basolateral membrane vesicles isolated from rat renal cortex. J Biol Chem 262: 2682–2687

    PubMed  Google Scholar 

  • Graziani Y, Livne A (1972) Water permeability of bilayer lipid membranes: sterol-lipid interaction. J Membr Biol 7: 275–284

    Google Scholar 

  • Gutknecht J, Bisson MA, Tosteson DC (1977) Diffusion of carbon dioxide through lipid bilayer membranes: effects of carbonic anhydrase, bicarbonate and unstirred layers. J Gen Physiol 69: 779–794

    PubMed  Google Scholar 

  • Hayden SM, Wolenski JS, Mooseker MS (1990) Binding of brush border myosin I to phospholipid vesicles. J Cell Biol 111: 443–451

    PubMed  Google Scholar 

  • Hill R, Whittingham CP (1955) Photosynthesis. Methuen, London

    Google Scholar 

  • Holz R, Finkelstein A (1970) The water and nonelectrolyte permeability induced in thin lipid membranes by the polyene antibiotics nystatin and amphotericin B. J Gen Physiol 56: 125–145

    PubMed  Google Scholar 

  • Jain MK (1972) The bimolecular lipid membrane: a system. Van Nostrand Reinhold, New York

    Google Scholar 

  • — (1983) Nonrandom lateral organization in bilayers and biomembranes. In: Aloia RC (ed) Membrane fluidity in biology, vol 1, concepts of membrane structure. Academic Press, New York, pp 1–37

    Google Scholar 

  • Kamiya N, Tazawa M (1956) Studies on the water permeability of a single plant cell by means of transcellular osmosis. Protoplasma 46: 394–422

    Google Scholar 

  • Kasamo K (1990) Mechanism for the activation of the plasma membrane H+ -ATPase from rice (Oryza saliva L.) culture cells by molecular species of a phospholipid. Plant Physiol 93: 1049–1053

    Google Scholar 

  • —, Kagita F, Yamanishi H, Sakaki T (1992) Low temperature-induced changes in the thermotropic properties and fatty acid composition of the plasma membrane and tonoplast of cultured rice (Oryza sativa L.) cells. Plant Cell Physiol 33: 609–616

    Google Scholar 

  • Keifer DW, Franceschi VR, Lucas WJ (1982) Plasmalemma chloride transport inChara corallina. Inhibition by 4,4′diisothiocyano-2,2′-disulfonic acid stilbene. Plant Physiol 70: 1327–1334

    Google Scholar 

  • Kiyosawa K (1993) Permeability of theChara cell membrane for ethylene glycol, glycerol, meso-erythritol, xylitol and mannitol. Physiol Plant 88: 366–371

    Google Scholar 

  • —, Tazawa M (1972) Influence of intracellular and extracellular tonicities on water permeability in characean cells. Protoplasma 74: 257–270

    Google Scholar 

  • — — (1973) Rectification characteristics ofNitella membranes in respect to water permeability. Protoplasma 78: 203–214

    Google Scholar 

  • — — (1977) Hydraulic conductivity of tonoplast-freeChara cells. J Membr Biol 37: 157–166

    Google Scholar 

  • Lucas WJ (1975) Photosynthetic fixation of14carbon by internodal cells ofChara corallina. J Exp Bot 26: 331–336

    Google Scholar 

  • — (1976) The influence of Ca2+ and K+ on H14CO3 − influx in internodal cells ofChara corallina. J Exp Bot 27: 32–42

    Google Scholar 

  • — (1977) Analogue inhibiton of the active HCO3 transport site in the characean plasma membrane. J Exp Bot 28: 1321–1336

    Google Scholar 

  • — (1979) Alkaline band formation inChara corallina. Due to OH− efflux or H+ influx? Plant Physiol 63: 248–254

    Google Scholar 

  • —, Alexander JM (1981) Influence of turgor pressure manipulation on plasmalemma transport of HCO3 and OH− inChara corallina. Plant Physiol 68: 553–559

    Google Scholar 

  • —, Dainty J (1977 a) HCO3 − influx across the plasmalemma ofChara corallina. Divalent cation requirement. Plant Physiol 60: 862–867

    Google Scholar 

  • — — (1977 b) Spatial distribution of functional OH− carriers along a characean internodal cell: determined by the effect of cytochalasin B on H14CO3 −. J Membr Biol 32: 75–92

    PubMed  Google Scholar 

  • —, Shimmen T (1981) Intracellular perfusion and cell centrifugation studies on plasmalemma transport processes inChara corallina. J Membr Biol 58: 227–237

    Google Scholar 

  • —, Spanswick RM, Dainty J (1978) HCO3 influx across the plasmalemma ofChara corallina. Plant Physiol 61: 487–493

    Google Scholar 

  • —, Keifer DW, Pesacreta TC (1986) Influence of culture medium pH on charasome development and chloride transport inChara corallina. Protoplasma 130: 5–11

    Google Scholar 

  • Lynch DV, Steponkus PL (1987) Plasma membrane lipid alterations associated with cold acclimation of winter rye seedlings (Secale cereale L. cv Puma). Plant Physiol 83: 761–767

    Google Scholar 

  • McElhaney RN (1985) The effect of membrane lipids on permeability and transport in prokaryotes. In: Benga G (ed) Structure and properties of cell membrane, vol 2. CRC Press, Boca Raton, pp 19–51

    Google Scholar 

  • Maren TH (1988) The kinetics of HCO3 − synthesis related to fluid secretion, pH control, and CO2 elimination. Annu Rev Physiol 50: 695–717

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Mimura T, Tazawa M (1983) Effect of intracellular Ca2+ on membrane potential and membrane resistance in tonoplast-free cells ofNitellopsis obtusa. Protoplasma 118: 49–55

    Google Scholar 

  • —, Shimmen T, Tazawa M (1983) Dependence of the membrane potential on intracellular ATP concentration in tonoplast-free cells ofNitellopsis obtusa. Planta 162: 77–84

    Google Scholar 

  • —, Müller R, Kaiser WM, Shimmen T, Dietz K-J (1993) ATP-dependent carbon transport in perfusedChara cells. Plant Cell Environ 16: 653–661

    Google Scholar 

  • Miyata H, Bowers B, Korn ED (1989) Plasma membrane association ofAcanthamoeba myosin I. J Cell Biol 109: 1519–1528

    PubMed  Google Scholar 

  • Nielsen S, Smith BL, Christensen EI, Knepper MA, Agre P (1993) CHIP28 water channels are localized in constitutively water-permeable segments of the nephron. J Cell Biol 120: 371–383

    PubMed  Google Scholar 

  • Nobel PS (1991) Physicochemical and environmental plant physiology. Academic Press, San Diego

    Google Scholar 

  • Osterhaut WJV (1949) Movement of water in cells ofNitella. J Gen Physiol 32: 553–558

    Google Scholar 

  • Price GD, Badger MR (1985) Inhibition by proton buffers of photosynthetic utilization of bicarbonate inChara corallina. Aust J Plant Physiol 12: 257–267

    Google Scholar 

  • —, Badger MR, Bassett ME, Whitecross MI (1985) Involvement of plasmalemmasomes and carbonic anhydrase in photosynthetic utilization of bicarbonate inChara corallina. Aust J Plant Physiol 12: 241–256

    Google Scholar 

  • Raven JA (1984) Energetics and transport in aquatic plants. AR Liss, New York

    Google Scholar 

  • Reinhold L, Volokita M, Zenvirth D, Kaplan A (1984) Is HCO3 − transport inAnabaena a Na+ symport? Plant Physiol 76: 1090–1092

    Google Scholar 

  • Rygol J, Arnold WM, Zimmerman U (1992) Zinc and salinity effects on membrane transport inChara connivens. Plant Cell Environ 15: 11–23

    Google Scholar 

  • Sanders D (1980) Control of C1 influx inChara by cytoplasmic C1− concentration. J Membr Biol 52: 51–60

    Google Scholar 

  • Shinitzky M (1984) Membrane fluidity and cellular functions. In: Shinitzky M (ed) Physiology of membrane fluidity, vol 1. CRC Press, Boca Raton, pp 1–51

    Google Scholar 

  • Shiraiwa Y, Kikuyama M (1989) Role of carbonic anhydrase and identification of the active species of inorganic carbon utilized for photosynthesis inChara corallina. Plant Cell Physiol 30: 581–587

    Google Scholar 

  • Smith FA, Walker NA (1980) Effects of ammonia and methylamine on C1− transport and on the pH changes and circulating electric currents associated with HCO3 − assimilation. J Exp Bot 31: 119–133

    Google Scholar 

  • Solomon AK (1989) Transport pathways: water movement across cell membranes. In: Tosteson DC (ed) Membrane transport. People and ideas. American Physiological Society, Bethesda, pp 125–153

    Google Scholar 

  • Staves MP, Wayne R (1993) The touch-induced action potential inChara: inquiry into the ionic basis and the mechanoreceptor. Aust J Plant Physiol 20: 471–488

    Google Scholar 

  • — —, Leopold AC (1992) Hydrostatic pressure mimics gravitational pressure in characean cells. Protoplasma 168: 141–152

    PubMed  Google Scholar 

  • Stein WD (1986) Transport and diffusion across cell membranes. Academic Press, San Diego

    Google Scholar 

  • Steudle E, Tyerman SD (1983) Determination of permeability coefficients, reflection coefficients, and hydraulic conductivity ofChara corallina using pressure probe: effects of solute concentration. J Membr Biol 75: 85–96

    Google Scholar 

  • Tazawa M (1972) Membrane characteristics as revealed by water and ionic relations of algal cells. Protoplasma 75: 427–460

    PubMed  Google Scholar 

  • —, Kamiya N (1965) Water relations of characean internodal cell. Annu Rep Biol Works Fac Sci Osaka Univ 13: 123–157

    Google Scholar 

  • — — (1966) Water permeability of a characean internodal cell with special reference to its polarity. Aust J Biol Sci 19: 399–419

    Google Scholar 

  • —, Kiyosawa K (1970) Water movement in a plant cell on application of hydrostatic pressure. Annu Rep Biol Works Fac Sci Osaka Univ 18: 57–70

    Google Scholar 

  • —, Shimmen T (1987) Cell motility and ionic relations in characean cells as revealed by internal perfusion and cell models. Int Rev Cytol 109: 259–312

    Google Scholar 

  • —, Kikuyama M, Shimmen T (1976) Electric characteristics and cytoplasmic streaming of Characeae cells lacking tonoplast. Cell Struct Funct 1: 165–176

    Google Scholar 

  • —, Shimmen T, Mimura T (1987) Membrane control in the Characeae. Annu Rev Plant Physiol 38: 95–117

    Google Scholar 

  • Tolbert NE, Zill LP (1954) Photosynthesis by protoplasm extruded fromChara andNitella. J Gen Physiol 37: 575–589

    PubMed  Google Scholar 

  • Tsutsui I, Ohkawa T (1993) N-Ethylmaleimide blocks the H+ pump in the plasma membrane ofChara corallina internodal cells. Plant Cell Physiol 34: 1159–1162

    Google Scholar 

  • Van Deenen LLM (1969) Membrane lipids and lipophilic proteins. In: Tosteson DC, (ed) The molecular basis of membrane function. Prentice-Hall, Englewood Cliffs, pp 47–78

    Google Scholar 

  • Verkman AS (1992) Water channels in cell membranes. Annu Rev Physiol 54: 97–108

    PubMed  Google Scholar 

  • Verbavatz J-M, Brown D, Sabolic I, Valenti G, Ausiello DA, van Hoek AN, Ma T, Verkman AS (1993) Tetrameric assembly of CHIP28 water channels in liposomes and cell membranes: a freeze-fracture study. J Cell Biol. 123: 605–618

    PubMed  Google Scholar 

  • Wade NL, Campbell LC, Bishop DG (1980) Tissue permeability and membrane lipid composition of ripening banana fruits. J Exp Bot 31: 975–982

    Google Scholar 

  • Walker NA (1985) The carbon species taken up byChara: a question of unstirred layers. In: Lucas WJ, Berry JA (eds) Inorganic carbon uptake by aquatic photosynthetic organisms. American Society of Plant Physiologists, Rockville, MD, pp 31–37

    Google Scholar 

  • —, Smith FA, Cathers IR (1980) Bicarbonate assimilation by fresh water charophytes and higher plants. I. Membrane transport of bicarbonate is not proven. J Membr Biol 57: 51–58

    Google Scholar 

  • Wayne R (1985) The contribution of calcium ions and hydrogen ions to the signal transduction chain in phytochrome-mediated fern spore germination. PhD Thesis, University of Massachusetts, Amherst, MA

    Google Scholar 

  • —, Tazawa M (1988) The actin cytoskeleton and polar water permeability in characean cells. Protoplasma [Suppl 2]: 116–130

    Google Scholar 

  • — — (1990) Nature of the water channels in the internodal cells ofNitellopsis. J Membr Biol 116: 31–39

    PubMed  Google Scholar 

  • —, Staves M, Moriyasu Y (1990) Calcium, cytoplasmic streaming, and gravity. In: Leonard RT, Hepler PK (eds) Calcium in plant growth and development. American Society of Plant Physiologists, Rockville, MD, pp 86–92 (American Society of Plant Physiologists series, vol 4)

    Google Scholar 

  • Woodbury DJ (1989) Pure lipid vesicles can induce channel-like conductances in planar bilayers. J Membr Biol 109: 145–150

    PubMed  Google Scholar 

  • Yeoh HH, Badger MR, Watson L (1981) Variations in kinetic properties of ribulose-l,5-bisphosphate carboxylases among plants. Plant Physiol. 67: 1151–1155

    Google Scholar 

  • Zenvirth D, Kaplan A (1981) Uptake and efflux of inorganic carbon inDunaliella satina. Planta 152: 8–12

    Google Scholar 

  • Zhang R, Skach W, Hasegawa H, van Hoek AN, Verkman AS (1993) Cloning, functional analysis and cell localization of a kidney proximal tubule water transporter homologous to CHIP28. J Cell Biol 120: 359–369

    PubMed  Google Scholar 

  • Zot HG, Doberstein SK, Pollard TD (1992) Myosin-I moves actin filaments on a phospholipid substrate: implications for membrane targeting. J Cell Biol 116: 367–376

    PubMed  Google Scholar 

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Authors and Affiliations

  1. Laboratory of Molecular Biomechanics, Department of Life Science, Faculty of Science, Himeji Institute of Technology, Harima Science Park City, Hyogo

    R. Wayne, T. Mimura & T. Shimmen

  2. Section of Plant Biology, Cornell University, 14853, Ithaca, NY, USA

    R. Wayne

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  2. T. Mimura
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Dedicated to our teacher, Professor Masashi Tazawa, on the occasion of his 65th birthday

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Wayne, R., Mimura, T. & Shimmen, T. The relationship between carbon and water transport in single cells ofChara corallina . Protoplasma 180, 118–135 (1994). https://doi.org/10.1007/BF01507848

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