Abstract
Hydraulic conductance of stem and petioles increased in response to an increase in xylem sap ion concentration, and decreased in response to a decrease in the ion concentration in six temperate deciduous tree species. The ion sensitivity of hydraulic conductance of stem and petioles was higher than the ion sensitivity of the stem alone. The ion sensitivity was lowest in the earliest developmental stages of the xylem, and had a seasonal maximum in the second half of summer. The ion sensitivity was highest in slow-growing species and lowest in fast-growing species. The ion sensitivity correlated negatively with mean radius of xylem conduits, hydraulic conductance of stem and petioles, hydraulic conductance of leaf laminae, and stomatal conductance, and positively with response of the hydraulic conductance of leaf laminae to HgCl2, and stomatal response to a decrease in leaf water potential or abscisic acid. It was concluded that the high ion sensitivity of xylem hydraulic conductance is a relevant characteristic of slow growth and a conservative water use strategy.
Similar content being viewed by others
Abbreviations
- cion :
-
xylem sap ion concentration
- EC:
-
electrical conductivity
- Ks :
-
hydraulic conductance of shoot stem
- Ksp :
-
hydraulic conductance of shoot stem and petioles
- Ss :
-
ion sensitivity of hydraulic conductance of shoot stem
- Ssp :
-
ion sensitivity of hydraulic conductance of shoot stem and petioles
References
Aasamaa, K., Niinemets, Ü., Sõber, A.: Leaf hydraulic conductance in relation to anatomical and functional traits during Populus tremula leaf ontogeny. — Tree Physiol. 25:1409–1418, 2005.
Aasamaa, K., Sõber, A.: Hydraulic conductance and stomatal sensitivity to changes of leaf water status in six deciduous tree species. — Biol. Plant. 44: 65–73, 2001.
Aasamaa, K., Sõber, A.: Seasonal courses of maximum hydraulic conductance in shoots of six temperate deciduous tree species. — Funct. Plant. Biol. 32: 1077–1087, 2005.
Aasamaa, K., Sõber, A., Hartung, W., Niinemets, Ü.: Drought acclimation of two deciduous tree species of different layers in a temperate forest canopy. — Trees 18: 93–101, 2004.
Aasamaa, K., Sõber, A., Rahi, M.: Leaf anatomical characteristics associated with shoot hydraulic conductance, stomatal conductance and stomatal sensitivity to changes of leaf water status in temperate deciduous trees. — Aust. J. Plant Physiol. 28: 765–774, 2001.
Bahrun, A., Jensen, C.R., Asch, F., Mogensen, V.O.: Drought-induced changes in xylem pH, ionic composition, and ABA concentration act as early signals in field-grown maize (Zea mays L.) — J. exp. Bot. 53: 251–263, 2002.
Boyce, C.K., Zwieniecki, M.A., Cody, G.D., Jacobsen, C., Wirick, S., Knoll, A.H., Holbrook, N.M.: Evolution of xylem lignification and hydrogel transport regulation. — Proc. nat. Acad. Sci. Plant Biol. 101: 17555–17558, 2004.
Brett, C.T., Waldron, K.W. (ed.): Physiology and Biochemistry of Plant Cell Walls. — Chapman & Hall, London 1996.
Castro-Díez, P., Navarro, J., Pintado, A., Sancho, L.G., Maestro, M.: Interactive effects of shade and irrigation on the performance of seedlings of three Mediterranean Quercus species. — Tree Physiol. 26: 389–400, 2006.
Chapin, F.S., III, Autumn, K., Pugnaire, F.: Evolution of suites of traits in response to environmental stress. — Amer. Natur. 142: S78–S92, 1993.
Choat, B., Jansen, S., Zwieniecki, M.A., Smets, E., Holbrook, N.M.: Changes in pit membrane porosity due to deflection and stretching: the role of vestured pits. — J. exp. Bot. 55: 1569–1575, 2004.
Choat, B., Brodie, T.W., Cobb, A.R., Zwieniecki, M.A., Holbrook, N.M.: Direct measurements of intervessel pit membrane hydraulic resistance in two angiosperm tree species. — Amer. J. Bot. 93: 993–1000, 2006.
Cochard, H., Tyree, M.T.: Xylem dysfunction in Quercus: vessel sizes, tyloses, cavitation and seasonal changes in embolism. — Tree Physiol. 6: 393–407, 1990.
Dickison, W.C.: Integrative Plant Anatomy. — Academic Press, San Diego — San Francisco — New York — Boston — London — Toronto — Sydney — Tokyo 2000.
Donovan, L.A., West, J.B., McLeod, K.W.: Quercus species differ in water and nutrient characteristics in a resource-limited fall-line sandhill habitat. — Tree Physiol. 20: 929–936, 2000.
Ellmore, G.S., Zanne, A.E., Orians, C.M.: Comparative sectoriality in temperate hardwoods: hydraulics and xylem anatomy. — Bot. J. Linn. Soc. 150: 61–71, 2006.
Ewers, F.W., Fisher, J.B.: Variation in vessel length and diameter in stems of six tropical and subtropical lianas. — Amer. J. Bot. 76: 1452–1459, 1989.
Gajardo-Caviedes, P.A., Espinosa, M.A., González, U. del T., Ríos, D.G.: The influence of thinning and tree size on the sapwood area / leaf area ratio in coigue. — Can. J. Forest Res. 35: 1679–1685, 2005.
Galmés, J., Cifre, J., Medrano, H., Flexas, J.: Modulation of relative growth rate and its components by water stress in Mediterranean species with different growth forms. — Oecologia 145: 21–31, 2005.
Gascó, A., Gortan, E., Salleo, S., Nardini, A.: Changes of pH solutions during perfusion through stem segments: further evidence for hydrogel regulation of xylem hydraulic properties? — Biol. Plant. 52: 502–506, 2008.
Gascó, A., Nardini, A., Gortan, E., Salleo, S.: Ion-mediated increase in the hydraulic conductivity of laurel stems: role of pits and consequences for the impact of cavitation on water transport. — Plant Cell Environ. 29: 1946–1955, 2006.
Gascó, A., Salleo, S., Gortan, E., Nardini, A.: Seasonal changes in the ion-mediated increase of xylem hydraulic conductivity in stems of three evergreens: any functional role? — Physiol. Plant. 129: 597–606, 2007.
Gorsuch, D.M., Oberbauer, S.F.: Effects of mid-season frost and elevated growing season temperature on stomatal and specific xylem conductance of the arctic shrub, Salix pulchra. — Tree Physiol. 22: 1027–1034, 2002.
Grignon, C., Sentenac, H.: pH and ionic conditions in the apoplast. — Annu. Rev. Plant Physiol. Plant mol. Biol. 42: 103–128, 1991.
Hacke, U.G., Sperry, J.S., Wheeler, J.K., Castro, L.: Scaling of angiosperm xylem structure with safety and efficiency. — Tree Physiol. 26: 689–701, 2006.
Herdel, K., Schmidt, P., Feil, R., Mohr, A., Schurr, U.: Dynamics of concentration and nutrient fluxes in the xylem of Ricinus communis — diurnal course, impact of nutrient availability and nutrient uptake. — Plant Cell Environ. 24: 41–52, 2001.
Holbrook, N.M., Zwieniecki, M.A., Melcher, P.J.: The dynamics of “dead” wood: maintenance of water transport through plant stems. — Integr. Comp. Biol. 42: 492–496, 2002.
Huber, B., Merz, W.: [Meaning of bordered pits for axial water conductivity of resinous woods.] — Planta 51: 645–672, 1958. [In German]
Jarbeau, J.A., Ewers, F.W., Davis, S.D.: The mechanism of water-stress-induced embolism in two species of chaparral shrubs. — Plant Cell Environ. 18: 189–196, 1995.
Johansson, S., Tuomela, K.: Growth of sixteen provenances of Eucalyptus microtheca in regularly irrigated plantation in eastern Kenya. — Forest Ecol. Manage. 82: 11–18, 1996.
Kozlowsky, T.T., Pallardy, S.G.: Physiology of Woody Plants. — Academic Press, San Diego — London — Boston — New York — Sydney — Tokyo — Toronto 1997.
Laas, E.: Dendroloogia [Dendrology.] — Valgus, Tallinn 1987. [In Estonian]
Li, C.: Carbon isotope composition, water-use efficiency and biomass productivity of Eucalyptus microtheca populations under different water supplies. — Plant Soil 214: 165–171, 1999.
Loewenstein, N.J., Pallardy, S.G.: Drought tolerance, xylem sap abscisic acid and stomatal conductance during soil drying: a comparison of canopy trees of three temperate deciduous angiosperms. — Tree Physiol. 18: 431–439, 1998.
López-Portillo, J., Ewers, F.W., Angeles, G.: Sap salinity effects on xylem conductivity in two mangrove species. — Plant Cell Environ. 28: 1285–1292, 2005.
Maillette, L.: Seasonal model of modular growth in plants. — J. Ecol. 80: 123–130, 1992.
Marron, N., Dreyer, E., Boudouresque, E., Delay, D., Petit, J.-M., Delmotte, F.M., Brignolas, F.: Impact of successive drought and re-watering cycles on growth and specific leaf area of two Populus ×canadensis (Moench) clones, ‘Dorskamp’ and ‘Luisa_Avanzo’. — Tree Physiol. 23: 1225–1235, 2003.
Mathiesen, A.: Dendroloogia. [Dendrology.] — Estonian Acad. Forest. Soc., Tartu 1934. [In Estonian]
Miller, D.M.: 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, 1985.
Nardini, A., Gasco, A., Trifilò, P., Lo Gullo, M.A., Salleo, S.: Ion-mediated enhancement of xylem hydraulic conductivity is not always suppressed by the presence of Ca2+ in the sap. — J. exp. Bot. 58: 2609–2615, 2007.
Nardini, A., Pitt, F.: Drought resistance of Quercus pubescens as a function of root hydraulic conductance, xylem embolism and hydraulic architecture. — New Phytol. 143: 485–493, 1999.
Orians, C.M., Babst, B.B., Zanne, A.E.: Vascular constraints and long-distance transport in dicots. — In: Holbrook, N.M., Zwieniecki, M.A. (ed.): Vascular Transport in Plants. Pp. 355–371. Elsevier Academic Press, Amsterdam — Boston — Heidelberg — London — New York — Oxford — Paris — San Diego — San Francisco — Singapore — Sydney — Tokyo 2005.
Passioura, J.B.: Water in the soil-plant-atmosphere continuum. — In: Lange, O.L., Nobel, P.L., Osmond, C.B., Ziegler, H. (ed.): Encyclopedia of Plant Physiology, New Series: Physiological Plant Ecology II, Vol. 12 B. Pp. 5–33. Springer-Verlag, Berlin — Heidelberg — New York 1982.
Pate, J.S., Jeschke, W.D.: The role of stems in transport, storage and circulation of ions and metabolites by the whole plant. — In: Gartner, B.L. (ed.): Plant Stems. Physiology and Functional Morphology. Pp. 177–204. Academic Press, London — San Diego 1995.
Peuke, A.D., Jeschke, W.D., Hartung, W.: Flows of elements, ions and abscisic acid in Ricinus communis under potassium limitation. — J. exp. Bot. 53: 241–250, 2002.
Querejeta, J.I., Barea, J.M., Allen, M.F., Caravaca, F., Roldán, A.: Differential response of δ13C and water use efficiency to arbuscular mycorrhizal infection in two aridland woody plant species. — Oecologia 135: 510–515, 2003.
Ridley, B.L., O’Neill, M.A., Mohnen, D.: Pectins: structure, biosynthesis, and oligogalacturonide-related signalling. — Phytochemistry 57: 929–967, 2001.
Ryden, P., MacDougall, A.J., Tibbits, C.W., Ring, S.G.: Hydration of pectic polysaccharides. — Biopolymers 54: 398–405, 2000.
Salleo, S., Raimondo, F., Trifilò, P., Nardini, A.: Axial-to-radial water permeability of leaf major veins: a possible determinant of the impact of vein embolism on leaf hydraulics? — Plant Cell Environ. 26: 1749–1758, 2003.
Salleo, S., Trifilò, P., Lo Gullo, M.A.: Phloem as a possible major determinant of rapid cavitation reversal in stems of Laurus nobilis (laurel) — Funct. Plant Biol. 33: 1063–1074, 2006.
Sano, Y.: Inter- and intraspecific structural variations among intervascular pit membranes, as revealed by field-emission scanning electron microscopy. — Amer. J. Bot. 92: 1077–1084, 2005.
Schurr, U., Schulze, E.-D.: The concentration of xylem sap in root exudate, and in sap from intact transpiring castor bean plants (Ricinus communis L.). — Plant Cell Environ. 18: 409–420, 1995.
Siebrecht, S., Herdel, K., Schurr, U., Tischner, R.: Nutrient translocation in the xylem of poplar — diurnal variations and spatial distribution along the shoot axis. — Planta 217: 783–793, 2003.
Sperry, J.S., Nichols, K.L., Sullivan, J.E.M., Eastlack, S.E.: Xylem embolism in ring-porous, diffuse-porous, and coniferous trees of northern Utah and interior Alaska. — Ecology 75: 1736–1752, 1994.
Sperry, J.S., Hacke, U.G., Wheeler, J.K.: Comparative analysis of end wall resistivity in xylem conduits. — Plant Cell Environ. 28: 456–465, 2005.
Sperry, J.S., Hacke, U.G., Pittermann, J.: Size and function in conifer tracheids and angiosperm vessels. — Amer. J. Bot. 93: 1490–1500, 2006.
Thakur, B.R., Singh, A.K., Handa, A.K.: Chemistry and use of pectin — a review. — Crit. Rev. Food Sci. Nutr. 37: 47–73, 1997.
Trifilò, P., Lo Gullo, M.A., Salleo, S., Callea, K., Nardini, A.: Xylem embolism alleviated by ion-mediated increase in hydraulic conductivity of functional xylem: insights from field measurements. — Tree Physiol. 28: 1505–1512, 2008.
Tyree, M.T., Salleo, S., Nardini, A., Lo Gullo, M.A., Mosca, R.: Refilling of embolized vessels in young stems of laurel. Do we need a new paradigm? — Plant Physiol. 120: 11–21, 1999.
Van Ieperen, W., Van Gelder, A.: Ion-mediated flow changes suppressed by minimal calcium presence in xylem sap in Chrysanthemum and Prunus laurocerasus. — J. Exp. Bot. 57: 2743–2750, 2006.
Van Ieperen, W., Van Meeteren, U., Van Gelder, H.: Fluid ionic composition influences hydraulic conductance of xylem conduits. — J. exp. Bot. 51: 769–776, 2000.
Weih, M.: Evidence for increased sensitivity to nutrient and water stress in a fast-growing hybrid willow compared with a natural willow clone. — Tree Physiol. 21: 1141–1148, 2001.
Wheeler, J.K., Sperry, J.S., Hacke, U.G., Huang, N.: Intervessel pitting and cavitation in woody Rosaceae and other vesseled plants: a basis for a safety vs. efficiency trade-off in xylem transport. — Plant Cell Environ. 28: 800–812, 2005.
Zanne, A.E., Sweeney, K., Sharma, M., Orians, C.M.: Patterns and consequences of differential vascular sectoriality in 18 temperate tree and shrub species. — Funct. Ecol. 20: 200–206, 2006.
Zimmermann, M.H.: Hydraulic architecture of some diffuse-porous trees. — Can. J. Bot. 56: 2286–2295, 1978.
Zimmermann, M.H., Jeje, A.A.: Vessel length distribution of some American woody plants. — Can. J. Bot. 59: 1882–1892, 1981.
Zwieniecki, M.A., Hutyra, L., Thompson, M.V., Holbrook, N.M.: 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, 2000.
Zwieniecki, M.A., Melcher, P.J., Field, T.S., Holbrook, N.M.: A potential role for xylem-phloem interactions in the hydraulic architecture of trees: effects of phloem girdling on xylem hydraulic conductance. — Tree Physiol. 24: 911–917, 2004.
Zwieniecki, M.A., Melcher, P.J., Holbrook, N.M.: Hydrogel control of xylem hydraulic resistance in plants. — Science 291: 1059–1062, 2001.
Acknowledgement
The study was financed by the Estonian Science Foundation (grants no. 6823 and 6969), and by the Estonian Ministry of Science and Education (target-financed themes no. 0172100s02 and 0170021s08). We also thank the staff of the Department of Food Science and Hygiene (at the Estonian University of Life Sciences) for permitting us to use their laboratory equipment.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Aasamaa, K., Sõber, A. Sensitivity of stem and petiole hydraulic conductance of deciduous trees to xylem sap ion concentration. Biol Plant 54, 299–307 (2010). https://doi.org/10.1007/s10535-010-0052-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10535-010-0052-9