Abstract
The science of plant water transport is equal parts of physics and biology. Plants have evolved a complex wick system that harnesses the cohesive hydrogen bond energy of liquid water and suppresses the heterogeneous nucleation of cavitation. Trade-offs between making the wick safe against cavitation and implosion, yet efficient in moving water, result in the process being limiting to plant performance. Cavitation limits the range of negative pressures that can be harnessed to move water, and the hydraulic conductance of the wick limits the flow rate that can be moved at a given negative pressure gradient. Both limits constrain CO2 uptake via the water-for-carbon trade-off at the stomatal interface. Research in the area concerns the mechanisms of cavitation, its reversal by embolism repair, consequences for plant ecology and evolution, and the coupling of water transport to plant productivity. Very little is known of the molecular biology underlying xylem physiology.
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References
Alder NN, Pockman WT, Sperry JS, Nuismer S (1997) Use of centrifugal force in the study of xylem cavitation. J Exp Bot 48:665–674
Baas P (1986) Ecological patterns of xylem anatomy. In: Givnish TJ (ed) On the economy of plant form and function. Cambridge University Press, Cambridge, pp 327–351
Bailey IW, Tupper WW (1918) Size variation in tracheary cells. I. A comparison between the secondary xylems of vascular cryptograms, gymnosperms and angiosperms. Proc Am Acad Arts Sci 54:149–204
Boyer JS, Cavalieri AJ, Schulze ED (1985) Control of the rate of cell enlargement: excision, wall relaxation, and growth-induced water potentials. Planta 163:527–543
Briggs LJ (1950) Limiting negative pressure of water. J Appl Phys 21:721–722
Brodribb TJ, Cochard H (2009) Hydraulic failure defines the recovery and point of death in water-stressed conifers. Plant Physiol 149:575–584
Brodribb TJ, Feild TS (2010) A surge in leaf photosynthetic capacity during early angiosperm diversification. Ecol Lett. doi:10.1111/j.1461-0248.2009.01410.x
Brodribb TJ, Holbrook NM (2004) Stomatal protection against hydraulic failure: a comparison of coexisting ferns and angiosperms. New Phytol 162:663–670
Brodribb TJ, Holbrook NM (2005) Water stress deforms tracheids peripheral to the leaf vein of a tropical conifer. Plant Physiol 137:1139–1146
Brodribb TJ, Holbrook NM, Zwieniecki MA, Palma B (2005) Leaf hydraulic capacity in ferns, conifers, and angiosperms: impacts on photosynthetic maxima. New Phytol 165:839–846
Brodribb TJ, Feild TS, Jordan GJ (2007) Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiol 144:1890–1898
Bucci SJ, Scholz FG, Goldstein G, Meinzer FC, Sternberg LDSL (2003) Dynamic changes in hydraulic conductivity in petioles of two savanna species: factors and mechanisms contributing to the refilling of embolized vessels. Plant Cell Environ 26:1633–1645
Canny MJ (1990) What becomes of the transpiration stream? New Phytol 114:341–368
Carlquist S (1988) Comparative wood anatomy. Springer, Berlin
Carlquist S (1992) Pit membrane remnants in perforation plates of primitive dicotyledons and their significance. Am J Bot 79:660–672
Cavender-Bares J (2005) Impacts of freezing on long distance transport in woody plants. In: Holbrook NM, Zwieniecki MA (eds) Vascular transport in plants. Academic, Amsterdam, pp 401–424
Choat B, Lahr EC, Melcher PJ, Zwieniecki MA, Holbrook NM (2005) The spatial pattern of air-seeding thresholds in mature sugar maple trees. Plant Cell Environ 28:1082–1089
Choat B, Cobb AR, Jansen S (2008) Structure and function of bordered pits: new discoveries and impacts on whole-plant hydraulic function. New Phytol 177:608–626
Christman MA, Sperry JS (2010) Single vessel flow measurements indicate scalariform perforation plates confer higher resistance to flow than previously estimated. Plant Cell Environ 33:431–433
Christman MA, Sperry JS, Adler FR (2009) Testing the rare pit hypothesis in three species of Acer. New Phytol 182:664–674
Cochard H (2002) A technique for measuring xylem hydraulic conductance under high negative pressures. Plant Cell Environ 25:815–819
Cochard H, Tyree MT (1990) Xylem dysfunction in Quercus: vessel sizes, tyloses, cavitation and seasonal changes in embolism. Tree Physiol 6:393–408
Cochard H, Cruiziat P, Tyree MT (1992) Use of positive pressures to establish vulnerability curves: further support for the air-seeding hypothesis and implications for pressure-volume analysis. Plant Physiol 100:205–209
Cochard H, Ewers FW, Tyree MT (1994) Water relations of a tropical vine-like bamboo (Rhipidocladum racemiflorum): root pressures, vulnerability to cavitation and seasonal changes in embolism. J Exp Bot 45:1085–1089
Cochard H, Ameglio T, Cruiziat P (2001) The cohesion theory debate continues. Trends Plant Sci 6:456
Cochard H, Froux F, Mayr S, Coutand C (2004) Xylem wall collapse in water-stressed pine needles. Plant Physiol 134:401–408
Cochard H, Gaelle D, Bodet C, Tharwat I, Poirier M, Ameglio T (2005) Evaluation of a new centrifuge technique for rapid generation of xylem vulnerability curves. Physiol Plant 124:410–418
Cox RM, Malcolm JM (1997) Effects of duration of a simulated winter thaw on dieback and xylem conductivity of Betula papyrifera. Tree Physiol 17:389–396
Crombie DS, Hipkins MF, Milburn JA (1985) Gas penetration of pit membranes in the xylem of Rhododendron as the cause of acoustically detectable sap cavitation. Aust J Plant Physiol 12:445–454
Cuevas LE (1969) Shrinkage and collapse studies on Eucalyptus viminalis. J Inst Wood Sci 4:29–38
Davis SD, Sperry JS, Hacke UG (1999a) The relationship between xylem conduit diameter and cavitation caused by freezing. Am J Bot 86:1367
Davis SD, Ewers FW, Wood J, Reeves JJ, Kolb KJ (1999b) Differential susceptibility to xylem cavitation among three pairs of Ceanothus species in the Transverse Mountain ranges of Southern California. Ecoscience 6:180–186
Davis SD, Ewers FW, Portwood KA, Sperry JS, Crocker MC, Adams GC (2002) Shoot dieback during prolonged drought in Ceanothus chaparral in California: a possible case of hydraulic failure. Am J Bot 89:820–828
Debenedetti PG (1996) Metastable liquids. Princeton University Press, Princeton, NJ
Ellmore GS, Ewers FW (1986) Fluid flow in the outermost xylem increment of a ring-porous tree, Ulmus americana. Am J Bot 73:1771–1774
Enquist BJ, West GB, Brown JH (2000) Quarter-power allometric scaling in vascular plants: Functional basis and ecological consequences. In: West GB, Brown JH (eds) Scaling in biology. Oxford University Press, Oxford, pp 167–198
Franks PJ, Drake PL, Froend RH (2007) Anisohydric but isohydrodynamic: seasonally constant plant water potential gradient explained by a stomatal control mechanism incorporating variable plant hydraulic conductance. Plant Cell Environ 30:19–30
Grace J (1993) Refilling of embolized xylem. In: Grace J, Raschi A, Borghetti M (eds) Water transport in plants under climatic stress. Cambridge University Press, Cambridge, pp 52–62
Hacke U, Sauter JJ (1996) Xylem dysfunction during winter and recovery of hydraulic conductivity in diffuse-porous and ring-porous trees. Oecologia 105:435–439
Hacke UG, Sperry JS (2003) Limits to xylem refilling under negative pressure in Laurus nobilis and Acer negundo. Plant Cell Environ 26:303–311
Hacke UG, Sperry JS, Pockman WP, Davis SD, McCulloh KA (2001) Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure. Oecologia 126:457–461
Hacke UG, Sperry JS, Wheeler JK, Castro L (2006) Scaling of angiosperm xylem structure with safety and efficiency. Tree Physiol 26:689–701
Hammel HT (1967) Freezing of xylem sap without cavitation. Plant Physiol 42:55–66
Holbrook NM, Zwieniecki MA (1999) Embolism repair and xylem tension: do we need a miracle? Plant Physiol 120:7–10
Holbrook NM, Ahrens ET, Burns MJ, Zwieniecki MA (2001) In vivo observation of cavitation and embolism repair using magnetic resonance imaging. Plant Physiol 126:27–31
Hudson PJ, Razanatsoa J, Feild TS (2010) Early vessel evolution and the diversification of wood function – insights from Malagasy Canellales. Am J Bot 97:80
Jackson RB, Sperry JS, Dawson TE (2000) Root water uptake and transport: using physiological processes in global predictions. Trends Plant Sci 5:482–488
Jacobsen AL, Ewers FW, Pratt RB, Paddock WA, Davis SD (2005) Do xylem fibers affect vessel cavitation resistance? Plant Physiol 139:546–556
Jacobson AL, Pratt RB, Ewers FW, Davis SD (2007) Cavitation resistance among 26 chaparral species of southern California. Ecol Monogr 77:99–115
Kolb KJ, Sperry JS (1999) Differences in drought adaptation between subspecies of sagebrush (Artemisia tridentata). Ecology 80:2373–2384
Kwak H, Panton RL (1985) Tensile strength of simple liquids predicted by a model of molecular interactions. J Phys Appl Phys 18:647–659
Li Y, Sperry JS, Bush SE, Hacke UG (2008) Evaluation of centrifugal methods for measuring xylem cavitation in conifers, diffuse- and ring-porous angiosperms. New Phytol 177:558–568
Lopez OR, Farris-Lopez K, Montgomery RA, Givnish TJ (2008) Leaf phenology in relation to canopy closure in southern Appalachian trees. Am J Bot 95:1395–1407
Maherali H, Pockman WT, Jackson RB (2003) Adaptive variation in the vulnerability of woody plants to xylem cavitation. Ecology 85:2184–2199
Mayr S, Sperry JS (2010) Freeze-thaw induced embolism in Pinus contorta: centrifuge experiments validate the “thaw-expansion” hypothesis but conflict with ultrasonic data. New Phytol 185:1016–1024
McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry JS, West A, Williams DG, Yepez EA (2008) Mechanisms of plant survival and mortality during drought. Why do some plants survive while others succumb to drought? New Phytol 178:719–739
Mencuccini M (2003) The ecological significance of long-distance water transport: short-term regulation, long-term acclimation and the hydraulic costs of stature across plant life forms. Plant Cell Environ 26:163–182
Milburn JA, McLaughlin ME (1974) Studies of cavitation in isolated vascular bundles and whole leaves of Plantago major L. New Phytol 73:861–871
Oertli JJ (1971) The stability of water under tension in the xylem. Z Pflanzenphysiol 65:195–209
Pickard WF (1981) The ascent of sap in plants. Progr Biophys Mol Biol 37:181–229
Piquemal J, LaPierre C, Myton K, O’Connel A, Schuch W, Grima-Pettenati J, Boudet AM (1998) Down-regulation of cinnamoyl-CoA reductase induces significant changes of lignin profiles in transgenic tobacco plants. Plant J 13:71–83
Pittermann J, Sperry JS (2003) Tracheid diameter is the key trait determining extent of freezing-induced cavitation in conifers. Tree Physiol 23:907–914
Pittermann J, Sperry JS (2006) Analysis of freeze-thaw embolism in conifers: the interaction between cavitation pressure and tracheid size. Plant Physiol 140:374–382
Pittermann J, Sperry JS, Hacke UG, Wheeler JK, Sikkema EH (2005) Torus-margo pits help conifers compete with angiosperms. Science 310:1924
Pockman WT, Sperry JS (1997) Freezing-induced xylem cavitation and the northern limit of Larrea tridentata. Oecologia 109:19–27
Pockman WT, Sperry JS (2000) Vulnerability to cavitaiton and the distribution of Sonoran desert vegetation. Am J Bot 87:1287–1299
Pockman WT, Sperry JS, O’Leary JW (1995) Sustained and significant negative water pressure in xylem. Nature 378:715–716
Rand RH (1978) The dynamics of and evaporating meniscus. Acta Mechanica 29:135–146
Raven JA (1987) The evolution of vascular land plants in relation to supracellular transport processes. Adv Bot Res 5:153–219
Rice KJ, Matzner SL, Byer W, Brown JR (2004) Patterns of tree dieback in Queensland, Australia: the importance of drought stress and the role of resistance to cavitation. Oecologia 139:190–198
Rood SB, Patino S, Coombs K, Tyree MT (2000) Branch sacrifice: cavitation-associated drought adaptation of riparian cottonwoods. Trees 14:248–257
Ryan MG, Phillips N, Bond BJ (2006) The hydraulic limitation hypothesis revisited. Plant Cell Environ 29:367–381
Salleo S, Lo Gullo MA, De Paoli 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, Trifilo P, LoGullo MA (2006) Phloem as a possible major determinant of rapid cavitation reversal in Laurus nobilis (laurel). Funct Plant Biol 33:1063–1074
Salleo S, Trifilo P, Esposito S, Nardini A, LoGullo MA (2009) Starch-to-sugar conversion in wood parenchyma of field-growing Laurus nobilis plants: a component of the signal pathway for embolism repair? Funct Plant Biol 36:815–825
Schlesinger WH (1997) Biogeochemistry. Academic, San Diego
Shen F, Rongfu G, Liu W, Zhang W (2002) Physical analysis of the process of cavitation in xylem sap. Tree Physiol 22:655–659
Sperry JS (1986) Relationship of xylem embolism to xylem pressure potential, stomatal closure, and shoot morphology in the palm Rhapis excelsa. Plant Physiol 80:110–116
Sperry JS (2000) Hydraulic constraints on plant gas exchange. Agric For Meteorol 2831:1–11
Sperry JS, Robson DJ (2001) Xylem cavitation and freezing in conifers. In: Colombo SJ, Bigras FJ (eds) Conifer cold hardiness. Kluwer, Dordrecht, pp 121–136
Sperry JS, Sullivan JEM (1992) Xylem embolism in response to freeze-thaw cycles and water stress in ring-porous, diffuse-porous, and conifer species. Plant Physiol 100:605–613
Sperry JS, Tyree MT (1988) Mechanism of water stress-induced xylem embolism. Plant Physiol 88:581–587
Sperry JS, Tyree MT (1990) Water-stress-induced xylem embolism in three species of conifers. Plant Cell Environ 13:427–436
Sperry JS, Holbrook NM, Zimmermann MH, Tyree MT (1987) Spring filling of xylem vessels in wild grapevine. Plant Physiol 83:414–417
Sperry JS, Donnelly JR, Tyree MT (1988) Seasonal occurrence of xylem embolism in sugar maple (Acer saccharum). Am J Bot 75:1212–1218
Sperry JS, Saliendra NZ, Pockman WT, Cochard H, Cruiziat P, Davis SD, Ewers FW, Tyree MT (1996) New evidence for large negative xylem pressures and their measurement by the pressure chamber method. Plant Cell Environ 19:427–436
Sperry JS, Adler FR, Campbell GS, Comstock JP (1998) Limitation of plant water use by rhizosphere and xylem conductance: results from a model. Plant Cell Environ 21:347–359
Sperry JS, Hacke UG, Pittermann J (2006) Size and function in conifer tracheids and angiosperm vessels. Am J Bot 93:1490–1500
Sperry JS, Hacke UG, Feild TS, Sano Y, Sikkema EH (2007) Hydraulic consequences of vessel evolution in angiosperms. Int J Plant Sci 168:1127–1139
Steudle E (1994) Water transport across roots. Plant Soil 167:79–90
Stiller V, Lafitte HR, Sperry JS (2005) Embolized conduits of rice (Oryza sativa L.) refill despite negative xylem pressure. Am J Bot 92:1970–1974
Sucoff E (1969) Freezing of conifer xylem and the cohesion-tension theory. Physiol Plant 22:424–431
Sutcliffe JF (1968) Plants and water. Edward Arnold, London
Taneda H, Sperry JS (2008) A case-study of water transport in co-occurring ring- versus diffuse-porous tresses: contrasts in water-status, conducting capacity, cavitation and vessel refilling. Tree Physiol 28:1641–1652
Tardieu F, Davies W (1993) Integration of hydraulic and chemical signalling in the control of stomatal conductance and water status of droughted plants. Plant Cell Environ 16:341–349
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 40:19–38
Tyree M, Davis S, Cochard H (1994) Biophysical perspectives of xylem evolution – is there a tradeoff of hydraulic efficiency for vulnerability to dysfunction? IAWA J 15:335–360
Tyree MT, Salleo S, Nardini A, Lo Gullo MA, Mosca R (1999) Refilling of embolized vessels in young stems of laurel. Do we need a new paradigm? Plant Physiol 102:11–21
Vesala T, Holtta T, Peramaki M, Nikinmaa E (2003) Refilling of a hydraulically isolated embolized xylem vessel: model calculations. Ann Bot 91:419–428
Vogel S (1988) Life’s devices. Princeton University Press, Princeton
Vogel S (1994) Life in moving fluids: the physical biology of flow, 2nd edn. Princeton University Press, Princeton, NJ
Wang J, Ives NE, Lechowicz MJ (1992) The relation of foliar phenology to xylem embolism in trees. Funct Ecol 6:469–475
West AG, Hultine KR, Sperry JS, Bush SE, Ehleringer JR (2008) Transpiration and hydraulic strategies in a pinyon-juniper woodland. Ecol Appl 18:911–927
Wheeler JK, Sperry JS, Hacke UG, Hoang N (2005) Inter-vessel pitting and cavitation in woody Rosaceae and other vesselled plants: a basis for a safety vs. efficiency trade-off in xylem transport. Plant Cell Environ 28:800–812
Willson C, Jackson RB (2006) Xylem cavitation caused by drought and freezing stress in four co-occurring Juniperus species. Physiol Plant 127:374–382
Yang S, Tyree MT (1992) A theoretical model of hydraulic conductivity recovery from embolism with comparison to experimental data on Acer saccharum. Plant Cell Environ 15:633–643
Young WC (1989) Roark’s formulas for stress and strain. McGraw Hill, New York
Zimmermann MH (1983) Xylem structure and the ascent of sap. Springer, Berlin
Zwieniecki MA, Hutyra L, Thompson MV, Holbrook NM (2000) Dynamic changes in petiole specific conductivity in red maple (Acer rubrum L.), tulip tree (Liriodendron tulipifera L.) and northern fox grape (Vitis labrusca L.). Plant Cell Environ 23:407–414
Zwieniecki MA, Melcher PJ, Boyce KC, Sack L, Holbrook NM (2002) Hydraulic architecture of leaf venation in Laurus nobilis L. Plant Cell Environ 25:1445–1450
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Sperry, J.S. (2011). Hydraulics of Vascular Water Transport. In: Wojtaszek, P. (eds) Mechanical Integration of Plant Cells and Plants. Signaling and Communication in Plants, vol 9. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-19091-9_12
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