Advertisement

Protoplasma

, Volume 180, Issue 3–4, pp 118–135 | Cite as

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

  • R. Wayne
  • T. Mimura
  • T. Shimmen
Original Papers

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.

Keywords

Carbon transport Chara corallina CO2 permeability Hydraulic resistance Plasma membrane Water transport 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Adams RJ, Pollard TD (1989) Binding of myosin-I to membrane lipids. Nature 340: 565–588PubMedGoogle Scholar
  2. Aizawa, K, Miyachi S (1986) Carbonic anhydrase and CO2 concentrating mechanisms in microalgae and cyanobacteria. FEMS Microbiol Rev 39: 215–233Google Scholar
  3. Aloia RC (ed) (1983) Membrane fluidity in biology, vol 2, general principles. Academic Press, New YorkGoogle Scholar
  4. Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase inBeta vulgaris. Plant Physiol 24: 1–15Google Scholar
  5. 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 219–274Google Scholar
  6. Barber RF, Thompson JE (1980) Senescence-dependent increase in the permeability of liposomes prepared from bean cotyledon membranes. J Exp Bot 31: 1305–1313Google Scholar
  7. Benga G (1989) Water exchange through the erythrocyte membrane. Int Rev Cytol 114: 273–316PubMedGoogle Scholar
  8. Boyer JS (1990) Photosynthesis in dehydrating plants. Bot Mag (Special Issue 2): 73–85Google Scholar
  9. 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: 163–169Google Scholar
  10. Cass A, Finkelstein A (1967) Water permeability of thin lipid membrane. J Gen Physiol 50: 1765–1784PubMedGoogle Scholar
  11. Chang HT, Loomis WE (1945) Effect of carbon dioxide on absorption of water and nutrients by roots. Plant Physiol 20: 221–232Google Scholar
  12. 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 39–81Google Scholar
  13. Dainty J (1963) Water relations of plant cells. Adv Bot Res 1: 279–326Google Scholar
  14. — (1964) Osmotic flow. Symp Soc Exp Biol 19: 75–85Google Scholar
  15. —, 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: 102–111PubMedGoogle Scholar
  16. — — (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: 112–121PubMedGoogle Scholar
  17. — — (1964 c) The reflection coefficient of plant cell membranes for certain solutes. Biochim Biophys Acta 79: 129–137PubMedGoogle Scholar
  18. —, Hope AB (1959) The water permeability of cells ofChara australis R Br. Aust J Biol Sci 12: 136–145Google Scholar
  19. Ding D-Q, Mimura T, Amino S, Tazawa M (1991) Intracellular transport and photosynthetic differentiation inChara corallina. J Exp Bot 42: 33–38Google Scholar
  20. —, Amino S, Mimura T, Sakano K, Nagata T, Tazawa M (1992) Quantitative analysis of intracellularly transported photoassimilates inChara corallina. J Exp Bot 43: 1045–1051Google Scholar
  21. Ferrier JM (1980) Apparent bicarbonate uptake and possible plasmalemma proton efflux inChara corallina. Plant Physiol 66: 1198–1199Google Scholar
  22. Findenegg GR (1974) Beziehungen zwischen Carboanhydraseaktivität und Aufnahme von HCO3 und C1 bei der Photosynthese vonScenedesmus obliquus. Planta 116: 123–131Google Scholar
  23. 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
  24. Gimmler H, Weiss C, Baier M, Hartung W (1990) The conductance of the plasmalemma for carbon dioxide. J Exp Bot 41: 785–794Google Scholar
  25. Ginzburg BZ, Katchalsky A (1963) The frictional coefficients of the flows of non-electrolytes through artificial membranes. J Gen Physiol 47: 403–418PubMedGoogle Scholar
  26. Glinka Z, Reinhold L (1962) Rapid changes in permeability of cell membranes to water brought about by carbon dioxide and oxygen. Plant Physiol 37: 481–486Google Scholar
  27. Grassl SM, Holohan PD, Ross CR (1987) HCO3 transport in basolateral membrane vesicles isolated from rat renal cortex. J Biol Chem 262: 2682–2687PubMedGoogle Scholar
  28. Graziani Y, Livne A (1972) Water permeability of bilayer lipid membranes: sterol-lipid interaction. J Membr Biol 7: 275–284Google Scholar
  29. 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: 779–794PubMedGoogle Scholar
  30. Hayden SM, Wolenski JS, Mooseker MS (1990) Binding of brush border myosin I to phospholipid vesicles. J Cell Biol 111: 443–451PubMedGoogle Scholar
  31. Hill R, Whittingham CP (1955) Photosynthesis. Methuen, LondonGoogle Scholar
  32. 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: 125–145PubMedGoogle Scholar
  33. Jain MK (1972) The bimolecular lipid membrane: a system. Van Nostrand Reinhold, New YorkGoogle Scholar
  34. — (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 1–37Google Scholar
  35. Kamiya N, Tazawa M (1956) Studies on the water permeability of a single plant cell by means of transcellular osmosis. Protoplasma 46: 394–422Google Scholar
  36. 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: 1049–1053Google Scholar
  37. —, 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: 609–616Google Scholar
  38. 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: 1327–1334Google Scholar
  39. Kiyosawa K (1993) Permeability of theChara cell membrane for ethylene glycol, glycerol, meso-erythritol, xylitol and mannitol. Physiol Plant 88: 366–371Google Scholar
  40. —, Tazawa M (1972) Influence of intracellular and extracellular tonicities on water permeability in characean cells. Protoplasma 74: 257–270Google Scholar
  41. — — (1973) Rectification characteristics ofNitella membranes in respect to water permeability. Protoplasma 78: 203–214Google Scholar
  42. — — (1977) Hydraulic conductivity of tonoplast-freeChara cells. J Membr Biol 37: 157–166Google Scholar
  43. Lucas WJ (1975) Photosynthetic fixation of14carbon by internodal cells ofChara corallina. J Exp Bot 26: 331–336Google Scholar
  44. — (1976) The influence of Ca2+ and K+ on H14CO3 influx in internodal cells ofChara corallina. J Exp Bot 27: 32–42Google Scholar
  45. — (1977) Analogue inhibiton of the active HCO3 transport site in the characean plasma membrane. J Exp Bot 28: 1321–1336Google Scholar
  46. — (1979) Alkaline band formation inChara corallina. Due to OH efflux or H+ influx? Plant Physiol 63: 248–254Google Scholar
  47. —, Alexander JM (1981) Influence of turgor pressure manipulation on plasmalemma transport of HCO3 and OH inChara corallina. Plant Physiol 68: 553–559Google Scholar
  48. —, Dainty J (1977 a) HCO3 influx across the plasmalemma ofChara corallina. Divalent cation requirement. Plant Physiol 60: 862–867Google Scholar
  49. — — (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: 75–92PubMedGoogle Scholar
  50. —, Shimmen T (1981) Intracellular perfusion and cell centrifugation studies on plasmalemma transport processes inChara corallina. J Membr Biol 58: 227–237Google Scholar
  51. —, Spanswick RM, Dainty J (1978) HCO3 influx across the plasmalemma ofChara corallina. Plant Physiol 61: 487–493Google Scholar
  52. —, Keifer DW, Pesacreta TC (1986) Influence of culture medium pH on charasome development and chloride transport inChara corallina. Protoplasma 130: 5–11Google Scholar
  53. 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: 761–767Google Scholar
  54. 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 19–51Google Scholar
  55. Maren TH (1988) The kinetics of HCO3 synthesis related to fluid secretion, pH control, and CO2 elimination. Annu Rev Physiol 50: 695–717PubMedGoogle Scholar
  56. Maurel C, Reizer J, Schroeder JI, Chrispeels MJ (1993) The vacuolar membrane protein γ-TIP creates water specific channels inXenopus oocytes. EMBO J 12: 2241–2247PubMedGoogle Scholar
  57. Mimura T, Tazawa M (1983) Effect of intracellular Ca2+ on membrane potential and membrane resistance in tonoplast-free cells ofNitellopsis obtusa. Protoplasma 118: 49–55Google Scholar
  58. —, Shimmen T, Tazawa M (1983) Dependence of the membrane potential on intracellular ATP concentration in tonoplast-free cells ofNitellopsis obtusa. Planta 162: 77–84Google Scholar
  59. —, Müller R, Kaiser WM, Shimmen T, Dietz K-J (1993) ATP-dependent carbon transport in perfusedChara cells. Plant Cell Environ 16: 653–661Google Scholar
  60. Miyata H, Bowers B, Korn ED (1989) Plasma membrane association ofAcanthamoeba myosin I. J Cell Biol 109: 1519–1528PubMedGoogle Scholar
  61. 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: 371–383PubMedGoogle Scholar
  62. Nobel PS (1991) Physicochemical and environmental plant physiology. Academic Press, San DiegoGoogle Scholar
  63. Osterhaut WJV (1949) Movement of water in cells ofNitella. J Gen Physiol 32: 553–558Google Scholar
  64. Price GD, Badger MR (1985) Inhibition by proton buffers of photosynthetic utilization of bicarbonate inChara corallina. Aust J Plant Physiol 12: 257–267Google Scholar
  65. —, 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: 241–256Google Scholar
  66. Raven JA (1984) Energetics and transport in aquatic plants. AR Liss, New YorkGoogle Scholar
  67. Reinhold L, Volokita M, Zenvirth D, Kaplan A (1984) Is HCO3 transport inAnabaena a Na+ symport? Plant Physiol 76: 1090–1092Google Scholar
  68. Rygol J, Arnold WM, Zimmerman U (1992) Zinc and salinity effects on membrane transport inChara connivens. Plant Cell Environ 15: 11–23Google Scholar
  69. Sanders D (1980) Control of C1 influx inChara by cytoplasmic C1 concentration. J Membr Biol 52: 51–60Google Scholar
  70. Shinitzky M (1984) Membrane fluidity and cellular functions. In: Shinitzky M (ed) Physiology of membrane fluidity, vol 1. CRC Press, Boca Raton, pp 1–51Google Scholar
  71. 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: 581–587Google Scholar
  72. 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: 119–133Google Scholar
  73. Solomon AK (1989) Transport pathways: water movement across cell membranes. In: Tosteson DC (ed) Membrane transport. People and ideas. American Physiological Society, Bethesda, pp 125–153Google Scholar
  74. Staves MP, Wayne R (1993) The touch-induced action potential inChara: inquiry into the ionic basis and the mechanoreceptor. Aust J Plant Physiol 20: 471–488Google Scholar
  75. — —, Leopold AC (1992) Hydrostatic pressure mimics gravitational pressure in characean cells. Protoplasma 168: 141–152PubMedGoogle Scholar
  76. Stein WD (1986) Transport and diffusion across cell membranes. Academic Press, San DiegoGoogle Scholar
  77. 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: 85–96Google Scholar
  78. Tazawa M (1972) Membrane characteristics as revealed by water and ionic relations of algal cells. Protoplasma 75: 427–460PubMedGoogle Scholar
  79. —, Kamiya N (1965) Water relations of characean internodal cell. Annu Rep Biol Works Fac Sci Osaka Univ 13: 123–157Google Scholar
  80. — — (1966) Water permeability of a characean internodal cell with special reference to its polarity. Aust J Biol Sci 19: 399–419Google Scholar
  81. —, Kiyosawa K (1970) Water movement in a plant cell on application of hydrostatic pressure. Annu Rep Biol Works Fac Sci Osaka Univ 18: 57–70Google Scholar
  82. —, Shimmen T (1987) Cell motility and ionic relations in characean cells as revealed by internal perfusion and cell models. Int Rev Cytol 109: 259–312Google Scholar
  83. —, Kikuyama M, Shimmen T (1976) Electric characteristics and cytoplasmic streaming of Characeae cells lacking tonoplast. Cell Struct Funct 1: 165–176Google Scholar
  84. —, Shimmen T, Mimura T (1987) Membrane control in the Characeae. Annu Rev Plant Physiol 38: 95–117Google Scholar
  85. Tolbert NE, Zill LP (1954) Photosynthesis by protoplasm extruded fromChara andNitella. J Gen Physiol 37: 575–589PubMedGoogle Scholar
  86. Tsutsui I, Ohkawa T (1993) N-Ethylmaleimide blocks the H+ pump in the plasma membrane ofChara corallina internodal cells. Plant Cell Physiol 34: 1159–1162Google Scholar
  87. Van Deenen LLM (1969) Membrane lipids and lipophilic proteins. In: Tosteson DC, (ed) The molecular basis of membrane function. Prentice-Hall, Englewood Cliffs, pp 47–78Google Scholar
  88. Verkman AS (1992) Water channels in cell membranes. Annu Rev Physiol 54: 97–108PubMedGoogle Scholar
  89. 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: 605–618PubMedGoogle Scholar
  90. Wade NL, Campbell LC, Bishop DG (1980) Tissue permeability and membrane lipid composition of ripening banana fruits. J Exp Bot 31: 975–982Google Scholar
  91. 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 31–37Google Scholar
  92. —, 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: 51–58Google Scholar
  93. 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, MAGoogle Scholar
  94. —, Tazawa M (1988) The actin cytoskeleton and polar water permeability in characean cells. Protoplasma [Suppl 2]: 116–130Google Scholar
  95. — — (1990) Nature of the water channels in the internodal cells ofNitellopsis. J Membr Biol 116: 31–39PubMedGoogle Scholar
  96. —, 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
  97. Woodbury DJ (1989) Pure lipid vesicles can induce channel-like conductances in planar bilayers. J Membr Biol 109: 145–150PubMedGoogle Scholar
  98. Yeoh HH, Badger MR, Watson L (1981) Variations in kinetic properties of ribulose-l,5-bisphosphate carboxylases among plants. Plant Physiol. 67: 1151–1155Google Scholar
  99. Zenvirth D, Kaplan A (1981) Uptake and efflux of inorganic carbon inDunaliella satina. Planta 152: 8–12Google Scholar
  100. 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: 359–369PubMedGoogle Scholar
  101. Zot HG, Doberstein SK, Pollard TD (1992) Myosin-I moves actin filaments on a phospholipid substrate: implications for membrane targeting. J Cell Biol 116: 367–376PubMedGoogle Scholar

Copyright information

© Springer-Verlag 1994

Authors and Affiliations

  • R. Wayne
    • 1
    • 2
  • T. Mimura
    • 1
  • T. Shimmen
    • 1
  1. 1.Laboratory of Molecular Biomechanics, Department of Life Science, Faculty of ScienceHimeji Institute of TechnologyHyogo
  2. 2.Section of Plant BiologyCornell UniversityIthacaUSA

Personalised recommendations