Investigating water transport through the xylem network in vascular plants

Journal of Experimental Botany

Volumn 65, Issue 7, 2014, Pages 1895-1904

  Kim, Hae Koo ^a   Park, Joonghyuk ^b   Hwang, Ildoo ^b  

^a International Maize and Wheat Improvement Center (CIMMYT)   (Ethiopia)

^b Pohang University of Science and Technology (POSTECH)   (South Korea)

Author keywords

cohesion tension theory; efficiency safety trade off; embolism.; hydraulic regulation; sap flow dynamics; Water flow

Indexed keywords

WATER;

METABOLISM; PLANT; TRANSPORT AT THE CELLULAR LEVEL; XYLEM;

BIOLOGICAL TRANSPORT; PLANTS; WATER; XYLEM;

EID: 84898897470     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/eru075     Document Type: Review

References (121)

1. Angeles G, Bond B, Boyer JS, et al. 2004. The cohesion-tension theory. New Phytologist 163, 451-452.
2. Apol MEF, Etienne RS, Olff H. 2008. Revisiting the evolutionary origin of allometric metabolic scaling in biology. Functional Ecology 22, 1070-1080.
3. 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.
4. Boehm H. 1893. Capillaritat und saftsteigen. Berichte der Deutschen Botanischen Gesellschaft 11, 203-212.
5. Botha CEJ, Aoki N, Scofield GN, Liu L, Furbank RT, White RG. 2008. A xylem sap retrieval pathway in rice leaf blades: evidence of a role for endocytosis? Journal of Experimental Botany 59, 2945-2954.
6. Brodersen CR. 2013. Visualizing water transport in roots: advanced maging tools for an expanding field. Plant and Soil 366, 29-32.
7. Brodersen CR, McElrone AJ. 2013. Maintenance of xylem network transport capacity: a review of embolism repair in vascular plants. Frontiers in plant science 4, 108.
8. Brodersen CR, McElrone AJ, Choat B, Lee EF, Shackel KA, Matthews MA. 2013. In vivo visualizations of drought-induced embolism spread in Vitis vinifera. Plant Physiology 161, 1820-1829.
9. Brodersen CR, McElrone AJ, Choat B, Matthews MA, Shackel KA. 2010. The dynamics of embolism repair in xylem: in vivo visualizations using high-resolution computed tomography. Plant Physiology 154, 1088-1095.
10. Brodribb TJ. 2009. Xylem hydraulic physiology: The functional backbone of terrestrial plant productivity. Plant Science 177, 245-251.
11. Burgess SSO, Adams MA, Turner NC, Beverly CR, Ong CK, Khan AAH, Bleby TM. 2001. An improved heat pulse method to measure low and reverse rates of sap fow in woody plants. Tree Physiology 21, 589-598.
12. Canny MJ. 1995. A new theory for the ascent of sap-cohesion supported by tissue pressure. Annals of Botany 75, 343-357.
13. Choat B, Ball M, Luly J, Holtum J. 2003. Pit membrane porosity and water stress-induced cavitation in four co-existing dry rainforest tree species. Plant Physiology 131, 41-48.
14. Cochard H. 2006. Cavitation in trees. Comptes Rendus Physique 7, 1018-1026.
15. Cochard H, Nardini A, Coll L. 2004. Hydraulic architecture of leaf blades: where is the main resistance? Plant, Cell & Environment 27, 1257-1267.
16. Cochard H, Badel E, Herbette S, Delzon S, Choat B, Jansen S. 2013. Methods for measuring plant vulnerability to cavitation: a critical review. Journal of Experimental Botany 64, 4779-4791.
17. Cohen Y, Fuchs M, Green GC. 1981. Improvement of the heat pulse method for determining sap fow in trees. Plant, Cell & Environment 4, 391-397.
18. Coomes DA. 2006. Challenges to the generality of WBE theory. Trends in Ecology & Evolution 21, 593-596.
19. Cruiziat P, Cochard H, Ameglio T. 2002. Hydraulic architecture of trees: main concepts and results. Annals of Forest Science 59, 723-752.
20. De Faÿ E, Vacher V, Humbert F. 2000. Water-related phenomena in winter buds and twigs of Picea abies L. (Karst.) until bud-burst: a biological, histological and NMR study. Annals of Botany 86, 1097-1107.
21. De Swaef T, Hanssens J, Cornelis A, Steppe K. 2013. Non-destructive estimation of root pressure using sap fow, stem diameter measurements and mechanistic modelling. Annals of Botany 111, 271-282.
22. Dimond AE. 1966. Pressure and fow relations in vascular bundles of the tomato plant. Plant Physiology 41, 119-131.
23. Dixon HH, Joly J. 1894. On the ascent of sap. Annals of Botany 8, 468-470.
24. Dodds PS, Rothman DH, Weitz JS. 2001. Re-examination of the "3/4-law" of metabolism. Journal of Theoretical Biology 209, 9-27.
25. Dye PJ, Olbrich BW, Calder IR. 1992. A comparison of the heat pulse method and deuterium tracing method for measuring transpiration from Eucalyptus grandis trees. Journal of Experimental Botany 43, 337-343.
26. Ehrenberger W, Rüger S, Fitzke R, Vollenweider P, Günthardt-Goerg M, Kuster T, Zimmermann U, Arend M. 2012. Concomitant dendrometer and leaf patch pressure probe measurements reveal the effect of microclimate and soil moisture on diurnal stem water and leaf turgor variations in young oak trees. Functional Plant Biology 39, 297-305.
27. Ellmore GS, Ewers FW. 1986. Fluid fow in the outermost xylem ncrement of a ring-porous tree, Ulmus americana. American Journal Botany 73:1771-1774.
28. Fitzgibbon J, Bell K, King E, Oparka K. 2010. Super-resolution maging of plasmodesmata using three-dimensional structured illumination microscopy. Plant Physiology 153, 1453-1463.
29. Fukuda, H. 1997. Tracheary element differentiation. The Plant Cell, 9, 1147.
30. Geitmann A. 2006. Experimental approaches used to quantify physical parameters at cellular and subcellular levels. American Journal of Botany 93, 1380-1390.
31. Green S, Clothier B, Jardine B. 2003. Theory and practical application of heat pulse to measure sap fow. Agronomy Journal 95, 1371-1379.
32. Hacke UG, Sperry JS. 2001. Functional and ecological xylem anatomy. Perspectives in Plant Ecology, Evolution and Systematics 4, 97-115.
33. Hacke UG, Sperry JS, Wheeler JK, Castro L. 2006. Scaling of angiosperm xylem structure with safety and effciency. Tree Physiology 26, 689-701.
34. Hargrave KR, Kolb KJ, Ewers FW, Davis SD. 1994. Conduit diameter and drought-induced embolism in Salvia mellifera Greene (Labiatae). New Phytologist 126, 695-705.
35. Harris JM. 1961. Water-conduction in the stems of certain conifers. Nature 189, 678-679.
36. Heine RW, Farr DJ. 1973. Comparison of heat-pulse and radioisotope tracer methods for determining sap-fow velocity in stem segments of poplar. Journal of Experimental Botany 24, 649-654.
37. Herbert E, Balibar S, Caupin F. 2006. Cavitation pressure in water. Physical Review E (Statistical, Nonlinear, and Soft Matter Physics) 74, 041603-041622.
38. Holbrook NM, Zwieniecki MA. 1999. Embolism repair and xylem tension: Do we need a miracle? Plant Physiology 120, 7-10.
39. Holbrook NM, Zwieniecki MA. 2005. Vascular transport in plants. Amsterdam: Elsevier Academic Press.
40. Höltta T, Cochard H, Nikinmaa E, Mencuccini M. 2009. Capacitive effect of cavitation in xylem conduits: results from a dynamic model. Plant Cell and Environment 32, 10-21.
41. Höltta T, Mencuccini M, Nikinmaa E. 2011. A carbon cost-gain model explains the observed patterns of xylem safety and effciency. Plant, Cell & Environment 34, 1819-1834.
42. James SA, Meinzer FC, Goldstein G, Woodruff D, Jones T, Restom T, Mejia M, Clearwater M, Campanello P. 2003. Axial and radial water transport and internal water storage in tropical forest canopy trees. Oecologia 134, 37-45.
43. Huber B. 1932. Beobachtungen und Messungen pfanzlicher Saftströme. Berichte der Deutsch Botanischen Gesellschaft 50, 89-109
44. Jeje AYA, Zimmermann MH. 1979. Resistance to water fow in xylem vessels. Journal of Experimental Botany 30, 817-827.
45. Kim HK, Lee SJ. 2010. Synchrotron X-ray imaging for nondestructive monitoring of sap fow dynamics through xylem vessel elements in rice leaves. New Phytologist 188, 1085-1098.
46. Kimura T, Geya Y, Terada Y, Kose K, Haishi T, Gemma H, Sekozawa Y. 2011. Development of a mobile magnetic resonance imaging system for outdoor tree measurements. Review of Scientifc Instruments 82, 053704.
47. Koch GW, Sillett SC, Jennings GM, Davis SD. 2004. The limits to tree height. Nature 428, 851-854.
48. Kozlowski TT, Winget CH. 1963. Patterns of water movement in forest trees. Botanical Gazette 124, 301-311.
49. Kramer PJ, Kozlowski TT. 1960. Physiology of trees. McGraw-Hill Book Company, New York.
50. Lancashire JR, Ennos AR. 2002. Modelling the hydrodynamic resistance of bordered pits. Journal of Experimental Botany 53, 1485-1493.
51. Lee EF, Matthews MA, McElrone AJ, Phillips RJ, Shackel KA, Brodersen CR. 2013a. Analysis of HRCT-derived xylem network reveals reverse fow in some vessels. Journal of Theoretical Biology 333, 146-155.
52. Lee SJ, Hwang BG, Kim HK. 2013b. Hydraulic characteristics of water-reflling process in excised roots of Arabidopsis. Planta 238, 307-315.
53. Lens F, Tixier A, Cochard H, Sperry JS, Jansen S, Herbette S. 2013. Embolism resistance as a key mechanism to understand adaptive plant strategies. Current Opinion in Plant Biology 16, 287-292.
54. Lewis AM, Boose ER. 1995. Estimating volume fow-rates through xylem conduits. American Journal of Botany 82, 1112-1116.
55. Loepfe L, Martinez-Vilalta J, Pinol J, Mencuccini M. 2007. The relevance of xylem network structure for plant hydraulic effciency and safety. Journal of Theoretical Biology 247, 788-803.
56. Lubczynski MW, Chavarro-Rincon D, Roy J. 2012. Novel, cyclic heat dissipation method for the correction of natural temperature gradients in sap fow measurements. Part 1. Theory and application. Tree Physiology 32, 894-912.
57. Lucas WJ, Groover A, Lichtenberger R, Furuta K, Yadav SR, Helariutta Y, He XQ, Fukuda H, Kang J, Brady SM. 2013. The plant vascular system: evolution, development and functions. Journal of Integrative Plant Biology 55, 294-388.
58. Murata K, Mitsuoka K, Hirai T, Walz T, Agre P, Heymann JB, Engel A, Fujiyoshi Y. 2000. Structural determinants of water permeation through aquaporin-1. Nature 407, 599-605.
59. McCulloh K, Sperry JS, Lachenbruch B, Meinzer FC, Reich PB, Voelker S. 2010. Moving water well: comparing hydraulic effciency in twigs and trunks of coniferous, ring-porous, and diffuse-porous saplings from temperate and tropical forests. New Phytologist 186, 439-450.
60. McCully ME, Canny MJ, Huang CX. 2009. Cryo-scanning electron microscopy (CSEM) in the advancement of functional plant biology. Morphological and anatomical applications. Functional Plant Biology 36, 97-124.
61. Meinzer FC, Clearwater MJ, Goldstein G. 2001. Water transport in trees: current perspectives, new insights and some controversies. Environmental and Experimental Botany 45, 239-262.
62. Melcher P, Meinzer F, Yount D, 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. Journal of Experimental Botany 49, 1757-1760.
63. Milburn JA. 1996. Sap ascent in vascular plants: challengers to the cohesion theory ignore the signifcance of immature xylem and the recycling of munch water. Annals of Botany 78, 399-407.
64. Niklas KJ, Spatz H-C, Vincent J. 2006. Plant biomechanics: an overview and prospectus. American Journal of Botany 93, 1369-1378.
65. Oda Y, Hasezawa S. 2006. Cytoskeletal organization during xylem cell differentiation. Journal of Plant Research 119, 167-177.
66. Page GFM, Liu JIE, Grierson PF. 2011. Three-dimensional xylem networks and phyllode properties of co-occurring Acacia. Plant, Cell & Environment 34, 2149-2158.
67. Passioura JB. 1988. Water Transport in and to roots. Annual Review of Plant Physiology and Plant Molecular Biology 39, 245-265.
68. Passioura JB, Munns R. 1984. Hydraulic resistance of plants. II Effects of rooting medium, and time of day, in barley and lupin. Australian Journal of Plant Physiology 11, 341-350.
69. Pennisi E. 2008. Plant genetics: the blue revolution, drop by drop, gene by gene. Science 320, 171-173.
70. Petit G, Anfodillo T. 2009. Plant physiology in theory and practice: An analysis of the WBE model for vascular plants. Journal of Theoretical Biology 259, 1-4.
71. Pittermann J. 2010. The evolution of water transport in plants: an integrated approach. Geobiology 8, 112-139.
72. Pittermann J, Sperry JS, Hacke UG, Wheeler JK, Sikkema EH. 2005. Torus-margo pits help conifers compete with angiosperms. Science 310, 1924.
73. Pockman WT, Sperry JS, Oleary JW. 1995. Sustained and signifcant negative water-pressure in xylem. Nature 378, 715-716.
74. Renner O. 1911. Experimentelle beiträge zur kenntnis der wasserbewegung. Flora 103, 171-247.
75. Ryan MG, Phillips N, Bond BJ. 2006. The hydraulic limitation hypothesis revisited. Plant, Cell & Environment 29, 367-381.
76. Sack L, Dietrich EM, Streeter CM, Sanchez-Gomez D, Holbrook NM. 2008. Leaf palmate venation and vascular redundancy confer tolerance of hydraulic disruption. Proceedings of the National Academy of Sciences, USA 105, 1567-1572.
77. Sano Y, Okamura Y, Utsumi Y. 2005. Visualizing water-conduction pathways of living trees: selection of dyes and tissue preparation methods. Tree Physiology 25, 269-275.
78. Savage VM, Bentley LP, Enquist BJ, Sperry JS, Smith DD, Reich PB, von Allmen EI. 2010. Hydraulic trade-offs and space flling enable better predictions of vascular structure and function in plants. Proceedings of the National Academy of Sciences, USA 107, 22722-22727.
79. Scheenen T, Vergeldt F, Heemskerk A, Van As H. 2007. Intact plant magnetic resonance imaging to study dynamics in long-distance sap fow and fow-conducting surface area. Plant Physiology 144, 1157-1165.
80. Scholander PF, Bradstreet ED, Hemmingsen EA, Hammel HT. 1965. Sap pressure in vascular plants: negative hydrostatic pressure can be measured in plants. Science 148, 339-346.
81. Schulte PJ, Castle AL. 1993. Water fow through vessel perforation plates-the effects of plate angle and thickness for Liriodendron tulipifera. Journal of Experimental Botany 44, 1143-1148.
82. Schulte PJ, Gibson AC, Nobel PS. 1989. Water Flow in vessels with simple or compound perforation plates. Annals of Botany 64, 171-178.
83. Scoffoni C, Rawls M, McKown A, Cochard H, Sack L. 2011. Decline of leaf hydraulic conductance with dehydration: relationship to leaf size and venation architecture. Plant Physiology 156, 832-843.
84. Shinozaki K, Kyoji Y, Hozumi K, Kira T. 1964. A quantitative analysis of plant form. Pipe model theory. I. Basic analysis. Japanese Journal of Ecology 14, 133-139.
85. Smith DM, Allen SJ. 1996. Measurement of sap fow in plant stems. Journal of Experimental Botany 47, 1833-1844.
86. Somerville C, Bauer S, Brininstool G, Facette M, Hamann T, Milne J, Osborne E, Paredez A, Persson S, Raab T, Vorwerk S, Youngs H. 2004. Toward a systems approach to understanding plant cell walls. Science 306, 2206-2211.
87. Sperry JS. 2003. Evolution of water transport and xylem structure. International Journal of Plant Sciences 164, S115-S127.
88. Sperry JS, Hacke UG, Feild TS, Sano Y, Sikkema EH. 2007. Hydraulic consequences of vessel evolution in angiosperms. International Journal of Plant Sciences 168, 1127-1139.
89. Sperry JS, Meinzer FC, McCulloh KA. 2008. Safety and effciency conficts in hydraulic architecture: scaling from tissues to trees. Plant, Cell & Environment 31, 632-645.
90. Tang A-C, Boyer JS. 2002. Xylem tension affects growth-induced water potential and daily elongation of maize leaves. Journal of Experimental Botany 53, 489-503.
91. Turner NC, Spurway RA, Schulze E-D. 1984. Comparison of water potentials measured by in situ psychrometry and pressure chamber in morphologically different species. Plant Physiology 74, 316-319.
92. Tyree MT. 1997. The Cohesion-tension theory of sap ascent: current controversies. Journal of Experimental Botany 48, 1753-1765.
93. Tyree MT. 2003. Plant hydraulics: The ascent of water. Nature 423, 923-923.
94. Tyree MT, Ewers FW. 1991. The hydraulic architecture of trees and other woody plants. New Phytologist 119, 345-360.
95. Tyree MT, Sperry JS. 1989. Vulnerability of xylem to cavitation and embolism. Annual Review of Plant Physiology and Plant Molecular Biology 40, 19-36.
96. Tyree MT, Zimmermann MH. 2002. Xylem structure and the ascent of sap. Berlin: Springer-Verlag.
97. Umebayashi T, Utsumi Y, Koga S, Inoue S, Shiiba Y, Arakawa K, Matsumura J, Oda K. 2007. Optimal conditions for visualizing water-conducting pathways in a living tree by the dye injection method. Tree Physiology 27, 993-999.
98. Vandegehuchte MW, Steppe K. 2012a. Sapfow+: a four-needle heat-pulse sap fow sensor enabling nonempirical sap fux density and water content measurements. New Phytologist 196, 306-317.
99. Vandegehuchte MW, Steppe K. 2012b. Use of the correct heat conduction-convection equation as basis for heat-pulse sap fow methods in anisotropic wood. Journal of Experimental Botany 63, 2833-2839.
100. van den Honert. 1948. Water transport in plants as a caternary process. Discussion of the Faraday Society 3, 146-153.
101. Vieweg GH, Ziegler H. 1960. Thermoelektrische registrierung der geschwindigkeit des transpirationsstromes. Berichte der Deutsch Botanischen Gesellschaft 73, 221-226.
102. von Allmen EI, Sperry JS, Smith DD, Savage VM, Enquist BJ, Reich PB, Bentley LP. 2012. A species-level model for metabolic scaling of trees II. Testing in a ring-and diffuse-porous species. Functional Ecology 26, 1066-1076.
103. Warren J, Bilheux H, Kang M, Voisin S, Cheng C-L, Horita J, Perfect E. 2013. Neutron imaging reveals internal plant water dynamics. Plant and Soil 366, 683-693.
104. Wei C, Steudle E, Tyree MT. 1999a. Water ascent in plants: do ongoing controversies have a sound basis? Trends in Plant Science 4, 372-375.
105. Wei C, Steudle E, Tyree MT, Lintilhac PM. 2001. The essentials of direct xylem pressure measurement. Plant, Cell & Environment 24, 549-555.
106. Wei C, Tyree MT, Steudle E. 1999b. Direct measurement of xylem pressure in leaves of intact maize plants. A test of the cohesion-tension theory taking hydraulic architecture into consideration. Plant Physiology 121, 1191-1205.
107. West GB, Brown JH, Enquist BJ. 1999. A general model for the structure and allometry of plant vascular systems. Nature 400, 664-667.
108. Wheeler TD, Stroock AD. 2008. The transpiration of water at negative pressures in a synthetic tree. Nature 455, 208-212.
109. Wheeler JK, Huggett BA, Tofte AN, Rockwell FE, Holbrook NM. 2013. Cutting xylem under tension or supersaturated with gas can generate PLC and the appearance of rapid recovery from embolism. Plant Cell Environment 36, 1938-1949.
110. Wistuba N, Reich R, Wagner HJ, Zhu JJ, Schneider H, Bentrup FW, Haase A, Zimmermann U. 2000. Xylem fow and its driving forces in a tropical liana: concomitant fow-sensitive NMR imaging and pressure probe measurements. Plant Biology 2, 579-582.
111. Wuyts N, Palauqui J-C, Conejero G, Verdeil J-L, Granier C, Massonnet C. 2010. High-contrast three-dimensional imaging of the Arabidopsis leaf enables the analysis of cell dimensions in the epidermis and mesophyll. Plant Methods 6, 17.
112. Zanne AE, Westoby M, Falster DS, Ackerly DD, Loarie SR, Arnold SE, Coomes DA. 2010. Angiosperm wood structure: Global patterns in vessel anatomy and their relation to wood density and potential conductivity. American Journal of Botany 97, 207-215.
113. Zehbe R, Haibel A, Riesemeier H, Gross U, Kirkpatrick CJ, Schubert H, Brochhausen C. 2010. Going beyond histology. Synchrotron micro-computed tomography as a methodology for biological tissue characterization: from tissue morphology to individual cells. Journal of The Royal Society Interface 7, 49-59.
114. Ziegler H, Weber J, Lüttge U. 2009. Thermal dissipation probe measurements of sap fow in the xylem of trees documenting dynamic relations to variable transpiration given by instantaneous weather changes and the activities of a mistletoe xylem parasite. Trees 23, 441-450.
115. Zimmermann D, Reuss R, Westhoff M, Gessner P, Bauer W, Bamberg E, Bentrup F-W, Zimmermann U. 2008. A novel, non-invasive, online-monitoring, versatile and easy plant-based probe for measuring leaf water status. Journal of Experimental Botany 59, 3157-3167.
116. Zimmermann MH. 1983. Xylem structure and the ascent of sap. New York: Springer-Verlag.
117. Zimmermann MH, Brown CL, Tyree MT. 1971. Trees: Structure and Function. Berlin: Springer-Verlag.
118. Zimmermann U, Meinzer FC, Benkert R, Zhu JJ, Schneider H, Goldstein G, Kuchenbrod E, Haase A. 1994. Xylem water transport: is the available evidence consistent with the cohesion theory? Plant, Cell & Environment 17, 1169-1181.
119. Zimmermann U, Schneider H, Wegner LH, Haase A. 2004. Water ascent in tall trees: does evolution of land plants rely on a highly metastable state? New Phytologist 162, 575-615.
120. Zwieniecki MA, Holbrook NM. 1998. Diurnal variation in xylem hydraulic conductivity in white ash (Fraxinus americana L.), red maple (Acer rubrum L.) and red spruce (Picea rubens Sarg.). Plant, Cell & Environment 21, 1173-1180.
121. Zwieniecki MA, Holbrook NM. 2009. Confronting Maxwell's demon: biophysics of xylem embolism repair. Trends in Plant Science 14, 530-534.