Abstract
When vascular plants are subjected to drought and eventually desiccate, they use different mechanisms to protect against water losses. Within the liquid phase, changes in hydraulics refer to part of these mechanisms of stress avoidance, which exclude the major role of gas exchange. At the input side, the water uptake by plant roots is governed by the composite structure of roots, which provides different pathways across the root cylinder. These are affected by the action of aquaporins (AQPs) in the cell membranes and apoplastic barriers along the cell wall path. The composite transport model is shown to provide mechanisms of short-term adaptation to water shortage. Composite transport and apoplastic barriers in roots should also be involved during the rehydration of resurrection plants, but this was not yet considered. Long-distance transport in the xylem according to the cohesion/tension (CT) mechanism is subject to cavitation, although xylem can withstand rather large tensions before vessels embolize. The problem is the refilling, where mechanisms have been proposed, but clues for solving the problem are missing. It is pointed out that, in resurrection plants, mechanisms of refilling appear to be more simple in that there is no refilling of empty xylem in the presence of a surrounding that has a water potential, which is more negative than that within the vessels. In the leaf, the major constraint with respect to hydraulic conductance is again cavitation, but detailed quantitative measurements are missing here to really provide physical models of the leaf hydraulic architecture. In both stem flow and leaf hydraulics, the role of living cells of xylem parenchyma is much discussed not only during refilling, but also during uptake and loss of water into or from vessels. Evidence for the action of AQPs in living tissue around xylem vessels comes from the temperature and light dependence of shoot hydraulic conductivity, which are hard to understand in terms of just viscose flow across vessels.
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Azaizeh H, Gunse B, Steudle E (1992) Effects of NaCl and CaCl2 on water transport across root cells of maize (Zea mays L.) seedlings. Plant Physiol 99:886–894
Balling A, Zimmermann U (1990) Comparative measurements of the xylem pressure of Nicotiana plants by means of the pressure bomb and pressure probe. Planta 182:325–338
Birner T, Steudle E (1993) Effects of anaerobic conditions on water and solute relations, and on active transport in roots of maize (Zea mays L.). Planta 190:474–483
Brewig A (1937) Permeabilitätsänderungen der Wurzelgewebe, die vom Spross beeinflusst werden. Z Bot 31:481–540
Brodribb TJ, Holbrook NM (2003a) Diurnal depression of leaf hydraulic conductance in a tropical tree species. Plant Cell Environ 27:820–827
Brodribb TJ, Holbrook NM (2003b) Stomatal closure during leaf dehydration, correlation with other leaf physiological traits. Plant Physiol 132:2166–2177
Brodribb TJ, Holbrook NM (2006) Diurnal depression of leaf hydraulic conductance in a tropical tree species. Plant Cell Environ 27:820–827
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 Bot Neerl 3:264–312
Burykin A, Warshel A (2004) On the origin of the electrostatic barrier for proton transport in aquaporin. FEBS Lett 570:41–46
Canny MJ (2000) Water transport at the extreme – restoring the hydraulic system in a resurrection plant. New Phytol 148:187–189
Canny MJ (2001) Contributions to the debate on water transport. Am J Bot 88:43–46
Canny MJ, McCully ME, Huang CX (2001) Cryo-scanning electron microscopy observations of vessel content during transpiration in walnut petioles. Facts or artefacts? Plant Physiol Biochem 39:7–8
Carvajal M, Cooke DT, Clarkson DT (1996) Responses of wheat plants to nutrition deprivation may involve the regulation of water-channel function. Planta 199:372–381
Clarkson DT, Robards AW, Stephens JE, Stark M (1987) Suberinlamellae in the hypodermis of maize (Zea mays) roots: development and factors affecting the permeability of hypodermal layers. Plant Cell Environ 10:83–93
Cochard H (2002) Xylem embolism and drought-induced stomatal closure in maize. Planta 215:466–471
Cochard H, Coll L, Le Roux X, Ameglio T (2002) Unraveling the effects of plant hydraulics on stomatal closure during water stress in walnut. Plant Physiol 128:282–290
Cochard H, Venisse JS, Barigah TS, Brunel N, Herbette S, Guilliot A, Tyree MT, Sakr S (2007) Putative role of aquaporins in variable conductance of leaves in response to light. Plant Physiol 143:122–133
Cowan IR (1977) Stomatal behaviour and environment. Adv Bot Res 4:117–228
Denker BM, Smith BL, Kuhadja FP, Agre P (1988) Identification, purification, and partial characterization of a novel MW 28, 000 integral membrane-protein from erythrocytes and renal tubules. J Biol Chem 263:15634–15642
Faiz SMA, Weatherley PE (1978) Further investigation into the location and magnitude of the hydraulic resistances in the soil–plant system. New Phytol 81:19–28
Fiscus EL (1975) The interaction between osmotic- and pressure-induced water flow in plant roots. Plant Physiol 55:917–922
Frensch J, Steudle E (1989) Axial and radial hydraulic resistance to roots of maize (Zea mays L.). Plant Physiol 91:719–726
Frensch J, Hsiao TC, Steudle E (1996) Water and solute transport along developing maize roots. Planta 198:348–355
Freundl E, Steudle E, Hartung W (1998) Water uptake by roots of maize and sunflower affects the radial transport of abscisic acid and the ABA concentration in the xylem. Planta 207:8–19
Hacke U, Sauter JJ (1996) Drought-inuced xylem dysfunction in petioles, branches, and roots of Populus balsamifera L. and Alnus glutinosa (L.) Gaertn. Plant Physiol 111:413–417
Henzler T, Waterhouse RN, Smyth AJ, Carvajal M, Cooke DT, Schäffner AR, Steudle E, Clarkson DT (1999) Diurnal variations in hydraulic conductivity and root pressure can be correlated with the expression of putative aquaporins in the root of Lotus japonicus. Planta 210:50–60
Henzler T, Ye Q, Steudle E (2004) Oxidative gating of water channels (aquaporins) in Chara by hydroxyl radicals. Plant Cell Environ 27:1184–1195
Herkelrath WN, Miller EE, Gardner WR (1977) Water uptake by plants. II. The root contact model. Soil Sci Soc Am J 41:1039–1043
Holbrook NM, Ahrens ET, Burns MJ, CB ZMA (2001) In vivo observation of cavitation and embolism repair using magnetic resonance imaging. Plant Physiol 126:27–31
Hose E, Steudle E, Hartung W (2000) Abscisic acid and the hydraulic conductivity of roots: a cell- and root-pressure probe study. Planta 211:874–882
Hose E, Clarkson DT, Steudle E, Schreiber L, Hartung W (2001) The exodermis: a variable apoplastic barrier. J Exp Bot 52:2245–2264
Kedem O, Katchalsky A (1963) Permeability of composite membranes. Part 2. Parallel elements. Trans Faraday Soc 59:1931–1940
Kenrick FB, Wismer KL, Wyatt KS (1924) Supersaturation of gases in liquids. J Phys Chem 28:1308–1315
Kim YX, Steudle E (2007) Light and turgor affect the water permeability (aquaporins) of parenchyma cells in the midrib of leaves of Zea mays. J Exp Bot 58:4119–4129
Kim YX, Steudle E (2009) Gating of aquaporins by light and reactive oxygen species in leaf parenchyma cells of the midrib of Zea mays. J Exp Bot 60:547–556
Kramer PJ, Boyer JS (1995) Water relations of plants and soils. Academic, Orlando
Lange OL, Schulze ED, Koch W (1970) Experimentell-ökologische Untersuchungen an Flechten der Negev-Wüste. II. CO2-Gaswechsel und Wasserhaushalt von Ramalina maciformis (Del.) Bory am natürlichen Standort während der sommerlichen Trockenperiode. Flora 159:38–62
Larcher W (1995) Physiological plant ecology. Springer, Berlin
Lee SH, Chung GC, Steudle E (2005a) Gating of aquaporins by low temperature in roots of chilling-sensitive cucumber and chilling-tolerant figleaf gourd. J Exp Bot 56:985–995
Lee SH, Chung GC, Steudle E (2005b) Low temperature and mechanical stresses differently gate aquaporins of root cortical cells of chilling-sensitive cucumber and -resistant figleaf gourd. Plant Cell Environ 28:1191–1202
Logullo MA, Nardini A, Trifilo P, Salleo S (2003) Changes in leaf hydraulics and stomatal conductance following drought stress and irrigation in Ceratonia siliqua (caob tree). Physiol Plant 117:186–194
Maggio A, Joly RJ (1995) Effects of mercuric chloride on the hydraulic conductivity of tomato root systems: evidence for a channel-mediated pathway. Plant Physiol 109:332–335
Maurel C (1997) Aquaporins and water permeability of plant membranes. Annu Rev Plant Physiol Plant Mol Biol 48:399–429
Maurel C, Santoni V, Luu DT, Wudick MM, Verdoucq L (2009) The cellular dynamics of plant aquaporin expression and functions. Curr Opin Plant Biol 12:690–698
Melcher PJ, Meinzer FC, Yount DE, Goldstein G, Zimmermann U (1998) Comparative measurements of xylem pressure in transpiring and non-transpiring leaves by means of the pressure chamber and the xylem pressure probe. J Exp Bot 49:1757–1760
Melchior W, Steudle E (1993) Water transport in onion (Allium cepa L.) roots. Changes of axial and radial hydraulic conductivity during root development. Plant Physiol 101:1305–1315
Meyer CJ, Peterson CA, Steudle E (2011) Permeability of Iris germanica’s multiseriate exodermis to water, NaCl and ethanol. J Exp Bot 62, Publ. online Dec. 3, 2010. doi: 10.1093/jxb/erg380
Molz FJ, Ferrier JM (1982) Mathematical treatment of water movement in plant cells and tissues: a review. Plant Cell Environ 5:191–206
Molz FJ, Ikenberry E (1974) Water transport through plant cells and walls: theoretical development. Soil Sci Am Proc 38:699–704
Munns R, Passioura JB (1984) Hydraulic resistance of plants. III. Effects of NaCl in barley and lupin. Aust J Plant Physiol 11:351–359
Nardini A, Salleo S, Raimondo F (2003) Changes in leaf hydraulic conductance correlate with leaf vein embolism in Cercis siliquatrum L. Trees 17:529–534
Nobel PS (1999) Physiochemical and environmental plant physiology. Academic, San Diego
North GB, Nobel PS (1991) Hydraulic conductivity of concentric root tissue of Agave desertii Engelm. Under wet and drying conditions. New Phytol 130:47–57
Peterson CA, Steudle E (1993) Lateral hydraulic conductivity of early metaxylem vessels in Zea mays L. roots. Planta 189:288–297
Peterson CA, Murrmann M, Steudle E (1993) Location of major barriers to water and ion movement in young roots of Zea mays L. Planta 190:127–136
Peyrano G, Taleisnik E, Quiroga M, de Forchetti SM, Tigker H (1997) Salinity effects on hydraulic conductance, lignin content and peroxydase activity in tomato roots. Plant Physiol Biochem 35:387–393
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
Ranathunge K, Steudle E, Lafitte R (2003) Control of water uptake by rice (Oryza sativa L.): role of the older part of the root. Planta 217:193–205
Ranathunge K, Steudle E, Lafitte R (2004) Water permeability and reflection coefficient of the outer part of young rice roots are differently affected by closure of water channels (aquaporins) or blockage of apoplastic pores. J Exp Bot 55:433–447
Ranathunge K, Steudle E, Lafitte R (2005a) Blockage of apoplastic bypass-flow of water in rice roots by insoluble salt precipitates analogous to a Pfeffer cell. Plant Cell Environ 28:121–133
Ranathunge K, Steudle E, Lafitte R (2005b) A new precipitation technique provides evidence for the permeability of Casparian bands to ions in young roots of corn (Zea mays L.) and rice (Oryza sativa L.). Plant Cell Environ 28:1450–1462
Rieger M, Litvin P (1999) Root system hydraulic conductivity in species with contrasting root anatomy. J Exp Bot 50:201–209
Sack L, Holbrook NM (2006) Leaf hydraulics. Annu Rev Plant Physiol Plant Mol Biol 57:361–381
Sack L, Melcher PJ, Zwieniecki MA, Holbrook NM (2002) The hydraulic conductance of the angiosperm leaf lamina: a comparison of three measurement methods. J Exp Bot 53:2177–2184
Salleo S, LoGullo MA, DePaoli D, Zippo M (1996) Xylem recovery from cavitation-induced embolism in young plants of Laurus nobilis: a possible mechanism. New Phytol 132:47–56
Salleo S, LoGullo MA, Raimondo F, Nardini A (2001) Vulnerability to cavitation of leaf minor veins: any impact on leaf gas exchange? Plant Cell Environ 24:851–859
Sanderson J (1983) Water uptake by different regions of the barley root. Pathways for radial flow in relation to development of the endodermis. J Exp Bot 34:240–253
Schneider H, Thürmer F, Zhu JJ, Wistuba N, Gessner P, Lindner K, Herrmann B, Zimmermann G, Hartung W, Bentrup FW, Zimmermann U (1999) Diurnal changes in xylem pressure off the hydrated resurrection plant Myrothamnus flabellifolia: evidence for lipid bodies in conducting xylem vessels. New Phytol 143:471–484
Schneider H, Manz B, Westhoff M, Mimietz S, Szimtenings M, Neuberger T, Faber C, Krohne G, Haase A, Volke F, Zimmermann U (2003) The impact of lipid distribution, composition and mobility on xylem water refilling of the resurrection plant Myrothamnus flabellifolia. New Phytol 159:487–505
Schreiber L, Breiner HW, Riederer M, Düggelin M, Guggenheim R (1994) The Casparian strip of Clivia miniata Reg. roos: fine structure and chemical nature. Bot Acta 107:353–361
Schreiber L, Hartmann K, Skrabs M, Zeier J (1999) Apoplastic barriers in roots: chemical composition of endodermal and hypodermal cell walls. J Exp Bot 50:1267–1280
Schulze ED (1986) Carbon dioxide and water vapor exchange in response to drought in the atmosphere and soil. Annu Rev Plant Physiol 37:247–274
Sherwin HW, Pammenter NW, February E, van der Willigen C, Farrant JM (1998) Xylem hydraulic characteristics, water relations and wood anatomy of the resurrection plant Myrothamnus flabellifolia Welw. Ann Bot 81:567–575
Stasovsky E, Peterson CA (1993) Effects of drought and subsequent rehydration on the structure, vitality and permeability of Allium cepa adventitious roots. Can J Bot 71:700–707
Steudle E (1989) Water flows in plants and its coupling with other processes: an overview. Meth Enzymol 174:183–225
Steudle E (1992) The biophysics of plant water: compartmentation: coupling with metabolic processes, and flow of water in plant roots. In: Somero GN, Osmond CB, Bolis CL (eds) Water and life: comparative analysis of water relationships at the organismic, cellular, and molecular levels. Springer, Heidelberg, pp 173–204
Steudle E (1994) Water transport across roots. Plant Soil 167:79–90
Steudle E (2000a) Water uptake by roots: effects of water deficit. J Exp Bot 51:1532–1542
Steudle E (2000b) Water uptake by plant roots: an integration of views. Plant Soil 226:45–56
Steudle E (2001) The cohesion-tension mechanism and the acquisistion of water by plant roots. Annu Rev Plant Physiol Plant Mol Biol 52:847–875
Steudle E, Frensch J (1996) Water transport in plants: role of the apoplast. Plant Soil 187:67–79
Steudle E, Henzler T (1995) Water channels in plants: do basic concepts of water transport change? J Exp Bot 46:1067–1076
Steudle E, Jeschke WD (1983) Water transport in barley roots. Planta 158:237–248
Steudle E, Peterson CA (1998) How does water get through roots? J Exp Bot 49:775–788
Steudle E, Murrmann M, Peterson CA (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 Physiol 103:335–349
Taleisnik E, Peyrano G, Cordoba A, Arias C (1999) Water retention capacity in root segments differing in the degree of exodermis development. Ann Bot 83:19–27
Trifilo P, Gasco A, Raimondo F, Nardini A, Salleo S (2003) Kinetics of recovery of leaf hydraulic conductance and vein functionality from cavitation-induced embolism in sunflower. J Exp Bot 119:4009–4417
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 50:1055–1071
Tyree MT (1997) The cohesion-tension theory of sap ascent. Current controversies. J Exp Bot 48:1753–1765
Tyree MT, Sperry JS (1989) Vulnerability of xylem to cavitation and embolism. Annu Rev Plant Physiol Plant Mol Biol 14:19–38
Tyree MT, Zimmermann MH (2002) Xylem structure and the ascent of sap. Springer, Berlin
Tyree MT, Davis SD, Cochard H (1994) Biophysical perspectives of xylem evolution: is there a tradeoff of hydraulic efficiency for vulnerability dysfunction? IAWA J 15:335–360
Tyree MT, Patino S, Bennink J, Alexander J (1995) Dynamic measurements of root hydraulic conductance using a high-pressure flow meter in the laboratory and field. J Exp Bot 46:83–94
van Ieperen W, van Meeren U, van Gelder H (2000) Fluid ionic composition influences hydraulic conductance of xylem conduits. J Exp Bot 51:769–776
Vieweg GH, Ziegler H (1969) Zur Physiologie von Myrothamnus flabelliflora. Ber. Dtsch. Bot. Ges. 82:29–36
Wan X, Steudle E, Hartung W (2004) Gating of water channels (aquaporins) in cortical cells of young corn roots by mechanical stimuli (pressure pulses): effects of ABA and of HgCl2. J Exp Bot 55:411–422
Weatherley PE (1982) Water uptake and flow into roots. In: Lange OL, Nobel PS, Osmond CB, Ziegler H (eds) Encyclopedia of plant physiology, vol 12B. Springer, Berlin, pp 79–109
Wei C, Steudle E, Tyree MT (1999a) Water ascent in plants: do ongoing controversies have a sound basis? Trends Plant Sci 4:372–375
Wei C, Tyree MT, Steudle E (1999b) Direct measurement of xylem pressure in leaves of intact maize plants: a test of cohesion-tension theory taking into account hydraulic architecture. Plant Physiol 121:1191–1205
Westgate ME, Steudle E (1985) Water transport in the midrib tissue of maize leaves. Direct Maesurement of the propagation of changes in cell turgor across a plant tissue. Plant Physiol 78:183–191
Ye Q, Steudle E (2006) Oxidative gating of water channels (aquaporins) in corn roots. Plant Cell Environ 29:459–470
Ye Q, Wiera B, Steudle E (2004) A cohesion/tension mechanism explains the gating of water channels (aquaporins) in Chara internodes by high concentration. J Exp Bot 55:449–461
Ye Q, Muhr J, Steudle E (2005) A cohesion/tension model for the gating of aquaporins allows estimation of water channel pore volumes in Chara. Plant Cell Environ 28:525–535
Zeidel ML, Ambudakar SV, Bl S, Agre P (1992) Reconstitution of functional water channels in liposomes containing purified red-cell CHIP28 protein. Biochemistry 31:7436–7440
Zeier J, Schreiber L (1998) Comparative investigation of primary and tertiary endodermal cell walls isolated from the roots of five monocotyledoneous species: chemical composition in relation to root fine structure. Planta 206:349–361
Zheng Q, Durben DJ, Wolf GH, Angell CA (1991) Liquids at large negative pressures: water at the homogenous nucleation limit. Science 254:829–832
Zhu GL, Steudle E (1991) Water transport across maize roots: simultaneous measurement of flows at the cell and root level by double pressure probe technique. Plant Physiol 95:305–315
Zimmermann MH (1978) Hydraulic architecture of some diffuse-porous trees. Can J Bot 56:2286–2295
Zimmermann HM, Steudle E (1998) Apoplastic transport across young maize roots: effects of the exodermis. Planta 206:7–19
Zwieniecki MA, Hutyra L, Thompson MV, Holbrook NM (2000) Dynamic changes in petiole specific conductivity in red maple (Acer rubrum L.), tulip tree (Liriodendon tulipifera L.) and northern fox grape (Vitis labrusca L.). Plant Cell Environ 23:407–414
Zwieniecki MA, Melcher PJ, Holbrook NM (2001) Hydrogel control of xylem hydraulic resistance in plants. Science 291:1059–1062
Acknowledgment
I thank Drs. Yangmin Kim, Department of Soil Physics, Helmholtz Centre for Environmental Research, Halle, Germany, and Kosala Ranathunge, Institute of Cellular and Molecular Botany, University of Bonn, Germany, for reading and discussing the manuscript.
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Steudle, E. (2011). Hydraulic Architecture of Vascular Plants. In: Lüttge, U., Beck, E., Bartels, D. (eds) Plant Desiccation Tolerance. Ecological Studies, vol 215. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-19106-0_10
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