Plant and Soil

, Volume 226, Issue 1, pp 45–56 | Cite as

Water uptake by plant roots: an integration of views

  • Ernst Steudle


A COMPOSITE TRANSPORT MODEL is presented which explains the variability in the ability of roots to take up water and responses of water uptake to different factors. The model is based on detailed measurements of 'root hydraulics' both at the level of excised roots (root hydraulic conductivity, Lpr) and root cells (membrane level; cell Lp) using pressure probes and other techniques. The composite transport model integrates apoplastic and cellular components of radial water flow across the root cylinder. It explains why the hydraulic conductivity of roots changes in response to the nature (osmotic vs. hydraulic) and intensity of water flow. The model provides an explanation of the adaptation of plants to conditions of drought and other stresses by allowing for a `coarse regulation of water uptake' according to the demands from the shoot which is favorable to the plant. Coarse regulation is physical in nature, but strongly depends on root anatomy, e.g. on the existence of apoplastic barriers in the exo- and endodermis. Composite transport is based on the composite structure of roots. A `fine regulation' results from the activity of water channels (aquaporins) in root cell membranes which is assumed to be under metabolic and other control.

apoplast composite transport model endodermis exodermis hydraulic conductivity root water channels water flow 


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  1. Azaizeh H, Gunse B and Steudle E 1992 Effects of NaCl and CaCl2 on water transport across root cells of maize (Zea mays L.) seedlings. Plant Physiology 99, 886–894.Google Scholar
  2. Azaizeh H and Steudle E. 1991 Effects of salinity on water transport of excised maize (Zea mays L.) roots. Plant Physiology 99, 1136–1145.Google Scholar
  3. Birner T P and Steudle E 1993 Effects of anaerobic conditions on water and solute relations and active transport in root of maize (Zea mays L.). Planta 190, 474–483.Google Scholar
  4. Brewig A 1937 Permeabilitätsänderungen der Wurzelgewebe, die vom Spross beeinflusst werden. Zeitschrift für Botanik 31, 481–540.Google Scholar
  5. Brouwer R 1954 The regulating influence of transpiration and suction tension on the water and salt uptake by roots of intact Vicia faba plants. Acta Botanica Neerlandica 3, 264–312.Google Scholar
  6. Carvajal M, Cooke D T and Clarkson D T 1996 Responses of wheat plants to nutrition deprivation may involve the regulation of water-channel function. Planta 199: 372–381.Google Scholar
  7. Cheng A C, van Hoek A N, Yeager M, Verkman A S and Mitra A K 1997 Three-dimensional organization of a human water channel. Nature 387, 627–630.Google Scholar
  8. Chrispeels M J and Maurel C 1994 Aquaporins: the molecular basis of facilitated water movement through living plant cells. Plant Physiology 105, 9–15.Google Scholar
  9. Cruz R T, Jordan W R and Drew M C (1992 Structural changes and associated reduction of hydraulic conductance in roots of Sorghum bicolor L. following exposure to water deficit. Plant Physiology 99, 203–212.Google Scholar
  10. Fiscus E L 1975 The interaction of osmotic-and pressure-induced water flow in plant roots. Plant Physiology 55: 917–922.Google Scholar
  11. Fiscus E L 1986 Diurnal changes in volume and solute transport coefficients of Phaseolus roots. Plant Physiology 80, 752–759.Google Scholar
  12. Frensch J and Steudle E 1989 Axial and radial hydraulic resistance to roots of maize (Zea mays L.). Plant Physiology 91, 719–726.Google Scholar
  13. Frensch J, Hsiao T C and Steudle E 1996 Water and solute transport along developing maize roots. Planta 198, 348–355.Google Scholar
  14. Freundl E, Steudle E and Hartung W 1998 Water uptake by roots of maize and sunflower affects the radial transport of abscisic acid and its concentration in the xylem. Planta 207, 8–19.Google Scholar
  15. Freundl E, Steudle E and Harting W (1999) Apoplastic transport of abscisic acid through roots of maize: effects of the exodermis. Planta (In press).Google Scholar
  16. Guerrero F D, Jones J T and Mullet J E 1990 Turgor-responsive gene transcription and RNA levels increase rapidly when pea shoots are wilted. Sequence and expression of three inducible genes. Plant Molecular Biology 15, 11–26.Google Scholar
  17. van den Honert T H 1948 Water transport in plants as a catenary process. Discussions of the Faraday Society 3, 146–53.Google Scholar
  18. Henzler T and Steudle E 1995 Reversible closing of water channels in Chara internodes provides evidence for a composite transport model of the plasma membrane. J Exper. Bot. 46, 199–209.Google Scholar
  19. Henzler T, Carvajal M, Smyth A, Cooke D T and Clarkson D T 1998 Diurnal variation in root hydraulics and aquaporin genehomologue expression in Lotus japonicus. J. Exper. Bot. 49 S: 10.Google Scholar
  20. Hertel A and Steudle E 1997 The function of water channels in Chara: the temperature dependence of water and solute flows provides evidence for composite membrane transport and for a slippage of small organic solutes across water channels. Planta 202, 324–335.Google Scholar
  21. Jap B K and Li H 1995 Structure of the osmoregulated H2O-channel, AQP-CHIP, in projection at 3.5 Å resolution. J. Molec. Biol. 251, 413–420.Google Scholar
  22. Johansson I, Larsson C, Ek B and Kjellbom P 1996 The major integral proteins of spinach leaf plasma membranes are putative aquaporins and are phoshorylated in response to Ca2+ and apoplastic water potential. Plant Cell 8, 1181–1191Google Scholar
  23. Jones H, Tomos A D, Leigh R A and Wyn Jones R G 1983 Waterrelation parameters of epidermal and cortical cells in the primary root of Triticum aestivum L. Planta 158, 230–6.Google Scholar
  24. Jung J S, Preston G M, Smith B L, Guggino W B and Agre P 1994 Molecular structure of the channel activity of the seed specific aquaporin α-TIP. EMBO Journal 14, 3028–35.Google Scholar
  25. Kramer P J and Boyer J S 1995 Water relations of plants and soils. Academic Press, Orlando.Google Scholar
  26. Maggio A and Joly R J 1995 Effects of mercuric chloride on the hydraulic conductivity of tomato root systems: evidence for a channel-mediated pathway. Plant Physiology 109, 331–335.Google Scholar
  27. Maurel C, Reizer J, Schroeder J L and Chrispeels M J 1993 The vacuolar membrane protein γ-TIP creates water specific channels in Xenopus oocytes. EMBO Journal 12, 2241–2247.Google Scholar
  28. Maurel C 1997 Aquaporins and water permeability of plant membranes. Annu. Rev. Plant Physiol. Plant Molec. Biol. 48, 399–429.Google Scholar
  29. Melchior W and Steudle E 1993 Water transport in onion (Allium cepa L.) roots. Changes of axial and radial hydraulic conductivities during root development. Plant Physiol. 101, 1305–1315.Google Scholar
  30. Melchior W and Steudle E 1995 Hydrostatic and osmotic hydraulic conductivities and reflection coefficients of onion (Allium cepa L.) roots. In Structure and Function of Roots. Eds. Baluska F, Ciamporova M, Gasparikova O, Barlow P W. pp 209–213. Kluwer Academic Press Publ., Dordrecht, The NetherlandsGoogle Scholar
  31. Miller D M 1985 Studies of root function in Zea mays. III. Xylem sap composition at maximum root pressure provides evidence of active transport into the xylem and a measurement of the reflection coefficient of the root. Plant Physiol. 77, 162–167.Google Scholar
  32. Murphy R and Smith J A C 1998 Determination of cell waterrelation parameters using the presure probe: extended theory and practice of the pressure-clamp technique. Plant Cell Environ. 21, 637–657.Google Scholar
  33. Newman E I 1973 Permeability to water of five herbaceous species. New Phytologist 72, 547–555.Google Scholar
  34. Nielson S and Agre P 1995 The aquaporin family of water channels in kidney. Annual Kidney International 48, 1057–1068.Google Scholar
  35. North G B and Nobel P S 1991 Changes in hydraulic conductivity and anatomy caused by drying and rewetting roots of Agave desertii (Agavaceae). Am. J. Bot. 78, 906–915.Google Scholar
  36. Park J H and Saier M H 1996 Phyolgentic characterization of the MIP family of transmembrane channel proteins. J. Membrane Biol. 153, 171–180.Google Scholar
  37. Passioura J B 1988 Water transport in and to roots. Annu. Rev. Plant Physiol. Plant Molec. Biol. 39, 245–56.Google Scholar
  38. Peterson C A and Enstone D E 1996 Functions of passage cells in the endodermis and exodermis of roots. Physiologia Plantarum 97, 592–598.Google Scholar
  39. Peterson C A, Murrmann M and Steudle E 1993 Location of major barriers to water and ion movement in young roots of Zea mays L. Planta 190, 127–136.Google Scholar
  40. Peyrano G, Taleisnik E, Quiroga M, de Forchetti S M and Tigier H 1997 Salinity effects on hydraulic conductance, lignin content and peroxidase activity in tomato roots. Plant Physiol. Biochem. 35, 387–393.Google Scholar
  41. Preston G M, Carroll T P, Guggino W B and Agre P 1992 Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science 256, 385–387.Google Scholar
  42. Reizer J, Reizer A and Saier M H 1993 The MIP family of integral membrane channel proteins: sequence comparisons, evolutionary relationships, reconstructed pathway evolution, and proposed functional differentation of the two repeated halves of the proteins. Critical Reviews in Biochemistry and Molecular Biology 28, 235–257.Google Scholar
  43. Rüdinger M, Hallgren S W, Steudle E and Schulze E D 1994 Hydraulic and osmotic püroperties of spruce roots. J. Exper. Bot. 45, 1413–1425.Google Scholar
  44. Schäffner A R 1998 Aquaporin function, structure and expression: are there more surprises to surface in plant water relations. Planta 204, 131–9.Google Scholar
  45. Schütz K and Tyerman S D 1997 Water channels in Chara corallina. J. Exper. Bot. 48, 1511–1518.Google Scholar
  46. Stavosky E and Peterson C A 1993 Effects of drought and subsequent rehydration on the structure, vitality and permeability of Allium cepa adventitious roots. Can. J. B. 71, 700–7.Google Scholar
  47. Steudle E 1989 Water flow in plants and its coupling to other processes: an overview. Methods of Enzymology 174: 183–225.Google Scholar
  48. Steudle E 1993 Pressure ropbe techniques: basic principles and application to studies of water and solute relations at the cell, tissue and organ level. In Water deficits: plant responses from cell to community. Eds. J A C Smith and H Griffiths. pp 5–36. Bios Scientific Publ. Ltd., Oxford.Google Scholar
  49. Steudle E 1994 Water transport across roots. Plant Soil 167, 79–90.Google Scholar
  50. Steudle E 1995 Trees under tension. Nature 378, 663–4.Google Scholar
  51. Steudle E 1997 Water transport across plant tissue: role of water channels. Biology of the Cell 89, 259–273.Google Scholar
  52. Steudle E and Brinckmann E 1989 The osmometer model of the root: water and solute relations of Phaseolus coccineus. Botanica Acta 102, 85–95.Google Scholar
  53. Steudle E and Frensch J 1989 Osmotic responses of maize roots. Water and solute relations. Planta 177, 281–295.Google Scholar
  54. Steudle E and Frensch J 1996 Water transport in plants: role of the apoplast. Plant Soil 187, 67–79.Google Scholar
  55. Steudle E and Henzler T 1995 Water channels in plants: do basic concepts of water transport change? J. Exper. Bot. 46, 1067–1076.Google Scholar
  56. Steudle E and Heydt H 1997 Water transport across tree roots. In Trees - Contributions to Modern Tree Physiology. Eds. Rennenberg H, Eschrich W, Ziegler H. pp 239–255. Backhuys Publishers, Leiden, The Netherlands.Google Scholar
  57. Steudle E and Jeschke W D 1983 Water transport in barley roots. Planta 158, 237–248.Google Scholar
  58. Steudle E and Meshcheryakov A B 1996 Hydraulic and osmotic properties of oak roots. J. Exper. Bot. 47, 387–401.Google Scholar
  59. Steudle E, Murrmann M and Peterson C A 1993 Transport of water and solutes across maize roots modified by puncturing the endodermis. Further evidence for the composite transport model of the root. Plant Physiology 103, 335–349.Google Scholar
  60. Steudle E, Oren R and Schulze 1987 Water transport in maize roots. Plant Physiol. 84, 1220–1232.Google Scholar
  61. Steudle E and Peterson C A 1998 How does water get through roots? J. Exper. Bot. 49, 775–788.Google Scholar
  62. Tazawa M, Asai K and Iwasaki N 1996 Characteristics of Hg-and Zn-sensitive water channels in the plasmamembrane of Chara cells. Botanica Acta 109, 388–96.Google Scholar
  63. Tyerman, S D, Bohnert H, Maurel C, Steudle E and Smith J A C 1999 Plant water channels: molecular biology meets biophysics. J. Exper. Bot. (In press).Google Scholar
  64. Tyree M T 1977 The cohesion-tension theory of sap ascent: current controversies. J. Exper. Bot. 48, 1753–65.Google Scholar
  65. Verkman A S, van Hoek A N, Ma T, Frigeri A and Skach W R 1996 Water transport across mammalian cell membranes. Am. J. Physiol. 270, C12–C30.Google Scholar
  66. Walz T, Typke D, Smith B L, Agre P and Engel A 1995 Projection map of aquaporin-1 determined by electron crystallography. Nature Structural Biology 2, 730–32.Google Scholar
  67. Walz T, Hirai T, Murata K, Heymann J B, Mitsuoka K, Fujiyioshi Y, Smith B L, Agre P and Engel A 1997 The three-dimensional structure of aquaporin-1. Nature 387, 624–627.Google Scholar
  68. Wayne R and Tazawa M 1990 Nature of the water channels in the internodal cells of Nitellopsis. J. Membrane Biol. 116, 31–39.Google Scholar
  69. Weatherley P E 1982 Water uptake and flow into roots. In Encyclopedia of Plant Physiology Vol 12B. Eds. Lange O L, Nobel P S, Osmond C B, Ziegler H pp 79–109. Springer-Verlag, Berlin.Google Scholar
  70. Zhang W H and Tyerman S D 1991 Effect of low O2 concentration and azide on hydraulic conductivity and osmotic volume of the cortical cells of wheat roots. Australian J. Plant Physiol. 18, 603–613.Google Scholar
  71. Zhu GL and Steudle E 1991 Water transport across maize roots. Plant Physiol. 95, 305–315.Google Scholar
  72. Zimmermann H M and Steudle E 1998 Apoplastic transport across young maize roots: effect of the exodermis. Planta 206, 7–19.Google Scholar

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© Kluwer Academic Publishers 2000

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  • Ernst Steudle

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