Biologia plantarum 2013, 57:531-539 | DOI: 10.1007/s10535-013-0316-2
Impact of phloem girdling on leaf gas exchange and hydraulic conductance in hybrid aspen
- 1 Institute of Ecology and Earth Sciences, University of Tartu, Tartu, Estonia
We investigated phloem-xylem interactions in relation to leaf hydraulic capacity in hybrid aspen (Populus tremula L. × P. tremuloides Michx.) by using phloem girdling method. Removal of bark tissues (phloem girdling) at the branch base resulted in a substantial decline in stomatal conductance (gS), net photosynthetic rate (PN), and leaf hydraulic efficiency, and in increase of leaf water potential (ΨL). Although gS declined more than PN (83 versus 78 %), the ratio of intercellular to ambient CO2 concentrations (ci/ca) increased from 0.67 to 0.87 in three days after girdling. Girdling induced a decrease in leaf hydraulic conductance (KL) on average by 43 % (P = 0.006). The changes in gS and leaf conductance to water vapour were co-ordinated with KL only in girdled branches whereas intrinsic water-use efficiency was invariant to KL. The declines in KL with girdling were not accompanied by changes in potassium ion concentration ([K+]), electrical conductivity, or pH of xylem sap. The results suggest that phloem girdling at the branch base does not influence the recirculation of ions between the phloem and xylem in hybrid aspen and the decrease of KL in response to the manipulation is not related to changes in [K+] and total ionic content of xylem sap.
Keywords: leaf water potential; net photosynthetic rate; phloem-xylem interactions; potassium; stomatal conductance; water-use efficiency; xylem sap
Subjects: phloem girdling; hydraulic conductance; water transport; water potential; net photosynthetic rate; potassium; stomatal conductance; water use efficiency; xylem; carbon dioxide concentration; transpiration rate; hybrid aspen
Species: Populus tremula × Populus tremuloides
Received: May 11, 2012; Accepted: November 20, 2012; Published: September 1, 2013Show citation
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References
- Brodribb, T.J., Holbrook, N.M.: Changes in leaf hydraulic conductance during leaf shedding in seasonally dry tropical forest. - New Phytol. 158: 295-303, 2003. Go to original source...
- Cernusak, L.A., Marshall, J.D.: Responses of foliar δ13C, gas exchange and leaf morphology to reduced hydraulic conductivity in Pinus monticola branches. - Tree Physiol. 21: 1215-1222, 2001. Go to original source...
- Chen, J.-W., Zhang, Q., Cao, K.-F.: Inter-species variation of photosynthetic and xylem hydraulic traits in the deciduous and evergreen Euphorbiaceae tree species from a seasonally tropical forest in south-western China. - Ecol. Res. 24: 65-73, 2009. Go to original source...
- Christman, M.A., Sperry, J.S., Smith, D.D.: Rare pits, large vessels and extreme vulnerability to cavitation in a ringporous tree species. - New Phytol. 193: 713-720, 2012. Go to original source...
- Cochard, H., Herbette, S., Hernández, E., Hölttä, T., Mencuccini, M.: The effects of sap ionic composition on xylem vulnerability to cavitation. - J. exp. Bot. 61: 275-285, 2010. Go to original source...
- De Boer, A.H., Volkov, V.: Logistics of water and salt transport through the plant: structure and functioning of the xylem. - Plant Cell Environ. 26: 87-101, 2003. Go to original source...
- Dickmann, D.I., Kuzovkina, J.: Poplars and Willows of the World, with Emphasis on Silviculturally Important Species. - FAO, Rome 2008.
- Di Vaio, C., Petito, A., Buccheri, M.: Effect of girdling on gas exchanges and leaf mineral content in the 'Independence' nectarine. - J. Plant Nutr. 24: 1047-1060, 2001. Go to original source...
- Domec, J.-C., Pruyn, M.L.: Bole girdling affects metabolic properties and root, trunk and branch hydraulics of young ponderosa pine trees. - Tree Physiol. 28: 1493-1504, 2008. Go to original source...
- Esau, K.: Anatomy of Seed Plants. - John Wiley & Sons, New York 1977.
- Farquhar, G.D., Ehleringer, J.R., Hubick, K.T.: Carbon isotope discrimination and photosynthesis. - Annu. Rev. Plant Physiol. Plant mol. Biol. 40: 503-537, 1989. Go to original source...
- Fumuro, M.: Effects of trunk girdling during early shoot elongation period on tree growth, mineral absorption, water stress, and root respiration in Japanese persimmon (Diospyros kaki L.) cv. Nishimurawase. - J. jap. Soc. hort. Sci. 67: 219-227, 1998. Go to original source...
- Gascó, A., Gortan, E., Salleo, S., Nardini, A.: Changes of pH of solutions during perfusion through stem segments: further evidence for hydrogel regulation of xylem hydraulic properties? - Biol. Plant. 52: 502-506, 2008. Go to original source...
- Gascó, A., Nardini, A., Gortan, E., Salleo, S.: Ion-mediated increase in the xylem hydraulic conductivity: role of pits and consequences for the impact of cavitation on water transport in plants. - Plant Cell Environ. 29: 1946-1955, 2006.
- Hubbard, R.M., Ryan, M.G., Stiller, V., Sperry, J.S.: Stomatal conductance and photosynthesis vary linearly with plant hydraulic conductance in ponderosa pine. - Plant Cell Environ. 24: 113-121, 2001. Go to original source...
- Jang, J.-C., Leon, P., Zhou, L., Sheen, J.: Hexokinase as a sugar sensor in higher plants. - Plant Cell 9: 5-19, 1997. Go to original source...
- Jeschke, D.W., Pate, J.S.: Cation and chloride partitioning through xylem and phloem within the whole plant of Ricinus communis L. under conditions of salt stress. - J. exp. Bot. 42: 1105-1116, 1991. Go to original source...
- Kanai, S., Moghaieb, R.E., El-Shemy, H.A., Panigrahi, R., Mohapatra, P.K., Ito, J., Nguyen, N.T., Saneoka, H., Fujita, K.: Potassium deficiency affects water status and photosynthetic rate of the vegetative sink in green house tomato prior to its effects on source activity. - Plant Sci. 180: 368-374, 2011. Go to original source...
- Kupper, P., Sõber, J., Sellin, A., Lõhmus, K., Tullus, A., Räim, O., Lubenets, K., Tulva, I., Uri, V., Zobel, M., Kull, O., Sõber, A.: An experimental facility for Free Air Humidity Manipulation (FAHM) can alter water flux through deciduous tree canopy. - Environ. exp. Bot. 72: 432-438, 2011. Go to original source...
- Kuwagata, T., Ishikawa-Sakurai, J., Hayashi, H., Nagasuga, K., Fukushi, K., Ahamed, A., Takasugi, K., Katsuhara, M., Murai-Hatano, M.: Influence of low air humidity and low root temperature on water uptake, growth and aquaporin expression in rice plants. - Plant Cell Physiol. 53: 1418-1431, 2012. Go to original source...
- Lee, J., Holbrook, N.M., Zwieniecki, M.A. Ion induced changes in the structure of bordered pit membranes. - Front. Plant Sci. 3: 55. doi: 10.3389/fpls.2012.00055, 2012. Go to original source...
- Levin, M., Lemcoff, J.H., Cohen, S., Kapulnik, Y.: Low air humidity increases leaf-specific hydraulic conductance of Arabidopsis thaliana (L.) Heynh (Brassicaceae). - J. exp. Bot. 58: 3711-3718, 2007. Go to original source...
- Maunoury-Danger, F., Fresneau, C., Eglin, T., Berveiller, D., François, C., Lelarge-Trouverie, C., Damesin, C.: Impact of carbohydrate supply on stem growth, wood and respired CO2 δ13C: assessment by experimental girdling. - Tree Physiol. 30: 818-830, 2010. Go to original source...
- Murakami, P.F., Schaberg, P.G., Shane, J.B.: Stem girdling manipulates leaf sugar concentrations and anthocyanin expression in sugar maple trees during autumn. - Tree Physiol. 28: 1467-1473, 2008. Go to original source...
- Myers, D.A., Thomas, R.B., DeLucia, E.H.: Photosynthetic responses of loblolly pine (Pinus taeda) needles to experimental reduction in sink demand. - Tree Physiol. 19: 235-242, 1999. Go to original source...
- Nardini, A., Gasco, A., Trifilo, 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. Go to original source...
- Nardini, A., Grego, F., Trifilò, P., Salleo, S.: Changes of xylem sap ionic content and stem hydraulics in response to irradiance in Laurus nobilis. - Tree Physiol. 30: 628-635, 2010. Go to original source...
- Nardini, A., Tyree, M.T., Salleo, S.: Xylem cavitation in the leaf of Prunus laurocerasus and its impact on leaf hydraulics. - Plant Physiol. 125: 1700-1709, 2001. Go to original source...
- Nemec, S.: Vessel blockage by myelin forms in citrus with and without rough-lemon decline symptoms. - Can. J. Bot. 53: 102-108, 1975. Go to original source...
- Neumann, P.M, Weissman, R., Stefano, G., Mancuso, S.: Accumulation of xylem transported protein at pit membranes and associated reductions in hydraulic conductance. - J. exp. Bot. 61: 1711-1717, 2010. Go to original source...
- Noel, A.R.A.: The girdled tree. - Bot. Rev. 36: 162-195, 1970. Go to original source...
- Offler, C.E., McCurdy, D.W., Patrick, J.W., Talbot, M.J.: Transfer cells: cells specialized for a special purpose. - Annu. Rev. Plant Biol. 54: 431-454, 2002.
- Pate, J.S., Jeschke, W.D.: 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, San Diego 1995.
- Rivas, F., Gravina, A., Agustí, M.: Girdling effects on fruit set and quantum yield efficiency of PSII in two Citrus cultivars. - Tree Physiol. 27: 527-535, 2007. Go to original source...
- Ryden, P., MacDougall, A.J., Tibbits, C.W., Ring, S.G.: Hydration of pectic polysaccharides. - Biopolymers 54: 398-405, 2000. Go to original source...
- Sack, L., Holbrook, N.M.: Leaf hydraulics. - Annu. Rev. Plant Biol. 57: 361-381, 2006. Go to original source...
- Sack, L., Tyree, M.T., Holbrook, N.M.: Leaf hydraulic architecture correlates with regeneration irradiance in tropical rainforest trees. - New Phytol. 167: 403-413, 2005. Go to original source...
- Salleo, S., Lo Gullo, M.A., De Paoli, D., Zippo, M.: Xylem recovery from cavitation-induced embolism in young plants of Laurus nobilis: a possible mechanism. - New Phytol. 132: 47-56, 1996. Go to original source...
- Salleo, S., Lo Gullo, M.A., Trifilò, P., Nardini, A.: New evidence for a role of vessel-associated cells and phloem in the rapid xylem refilling of cavitated stems of Laurus nobilis L. - Plant Cell Environ. 27: 1065-1076, 2004. Go to original source...
- Santiago, L.S., Goldstein, G., Meinzer, F.C., Fisher, J.B., Machado, K., Woodruff, D., Jones, T.: Leaf photosynthetic traits scale with hydraulic conductivity and wood density in Panamanian forest canopy trees. - Oecologia 140: 543-550, 2004. Go to original source...
- Sellin, A.: Does pre-dawn water potential reflect conditions of equilibrium in plant and soil water status? - Acta oecol. 20: 51-59, 1999. Go to original source...
- Sellin, A., Eensalu, E., Niglas, A.: Is distribution of hydraulic constraints within tree crowns reflected in photosynthetic water-use efficiency? An example of Betula pendula. - Ecol. Res. 25: 173-183, 2010b. Go to original source...
- Sellin, A., Õunapuu, E., Karusion, A.: Experimental evidence supporting the concept of light-mediated modulation of stem hydraulic conductance. - Tree Physiol. 30: 1528-1535, 2010a. Go to original source...
- Sellin, A., Õunapuu, E., Kupper, P.: Effects of light intensity and duration on leaf hydraulic conductance and distribution of resistance in shoots of silver birch (Betula pendula). - Physiol. Plant. 134: 412-420, 2008. Go to original source...
- Sellin, A., Sack, L., Õunapuu, E., Karusion, A.: Impact of light quality on leaf and shoot hydraulic properties: a case study in silver birch (Betula pendula). - Plant Cell Environ. 34: 1079-1087, 2011. Go to original source...
- Setter, T.L., Brun, W.A., Brenner, M.L.: Effect of obstructed translocation of leaf abscisic acid on associated stomatal closure and photosynthesis decline. - Plant Physiol. 65: 1111-1115, 1980. Go to original source...
- Sevanto, S., Hölttä, T., Holbrook, N.M.: Effects of the hydraulic coupling between xylem and phloem on diurnal phloem diameter variation. - Plant Cell Environ. 34: 690-703, 2011. Go to original source...
- 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. Go to original source...
- Sokal, R.R., Rohlf, F.J.: Biometry: the Principles and Practice of Statistics in Biological Research. - W. H. Freeman and Co, New York 1995.
- Sperry, J.S., Tyree, M.T.: Mechanism of water stress-induced xylem embolism. - Plant Physiol. 88: 581-587, 1988. Go to original source...
- Sperry, J.S., Donnelly, J.R., Tyree, M.T.: A method for measuring hydraulic conductivity and embolism in xylem. - Plant Cell Environ. 11: 35-40, 1988. Go to original source...
- Stark, N., Spitzner, C., Essig, D.: Xylem sap analysis for determining the nutritional status of trees: Pseudotsuga menziesii. - Can. J. Forest. Res. 15: 429-437, 1985. Go to original source...
- Taylor, D., Eamus, D.: Coordinating leaf functional traits with branch hydraulic conductivity: resource substitution and implications for carbon gain. - Tree Physiol. 28: 1169-1177, 2008. Go to original source...
- Tyree, M.T., Zimmermann, M.H.: Xylem Structure and the Ascent of Sap. - Springer-Verlag, Berlin 2002.
- Urban, L., Alphonsout, L.: Girdling decreases photosynthetic electron fluxes and induces sustained photoprotection in mango leaves. - Tree Physiol. 27: 345-352, 2007. Go to original source...
- Van Bel, A.J.E.: Xylem-phloem exchange via the rays: the undervalued route of transport. - J. exp. Bot. 41: 631-644, 1990. Go to original source...
- Van Doorn, W.G., Hiemstra, T., Fanourakis, D.: Hydrogel regulation of xylem water flow: an alternative hypothesis. - Plant Physiol. 157: 1642-1649, 2011. Go to original source...
- Van Ieperen, W.: Ion-mediated changes of xylem hydraulic resistance in planta: fact or fiction? - Trends Plant Sci. 12: 137-142, 2007. Go to original source...
- 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. Go to original source...
- Wilson, B.F., Gartner, B.L.: Effects of phloem girdling in conifers on apical control of branches, growth allocation and air in wood. - Tree Physiol. 22: 347-353, 2002. Go to original source...
- Williams, L.E., Ayars, J.E.: Water use of Thompson Seedless grapevines as affected by the application of gibberellic acid (GA3) and trunk girdling - practices to increase berry size. - Agr. Forest. Meteorol. 129: 85-94, 2005. Go to original source...
- Williams, L.E., Retzlaff, W.A., Yang, W.G., Biscay, P.J., Ebisuda, N.: Effect of girdling on leaf gas exchange, water status, and non-structural carbohydrates of field-grown Vitis vinifera L. (cv. Flame Seedless). - Amer. J. Enol. Viticult. 51: 49-54, 2000.
- Wullschleger, S.D., Meinzer, F.C., Vertessy, R.A.: A review of whole-plant water use studies in trees. - Tree Physiol. 18: 499-512, 1998. Go to original source...
- Zhang, J.-L., Cao, K.-F.: Stem hydraulics mediates leaf water status, carbon gain, nutrient use efficiencies and plant growth rates across dipterocarp species. - Funct. Ecol. 23: 658-667, 2009. Go to original source...
- Zweifel, R., Item, H., Häsler, R.: Stem radius changes and their relation to stored water in stems of young Norway spruce trees. - Trees 15: 50-57, 2000. Go to original source...
- 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. Go to original source...
- Zwieniecki, M.A., Melcher, P.J., Feild, 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. Go to original source...
- Zwieniecki, M.A., Melcher, P.J., Holbrook, N.M.: Hydrogel control of xylem hydraulic resistance in plants. - Science 291: 1059-1062, 2001. Go to original source...