Seasonal courses of maximum hydraulic conductance in shoots of six temperate deciduous tree species
Krõõt Aasamaa A C and Anu Sõber BA Department of Silviculture, Estonian Agricultural University, Kreutzwaldi 5, Tartu 51014, Estonia.
B Institute of Botany and Ecology, University of Tartu, Lai 40, Tartu 51005, Estonia.
C Corresponding author. Email: kroot@eau.ee
Functional Plant Biology 32(12) 1077-1087 https://doi.org/10.1071/FP05088
Submitted: 12 April 2005 Accepted: 11 July 2005 Published: 1 December 2005
Abstract
The seasonal course of maximum hydraulic conductance of leaf laminae (K lamina) of shoots correlated strongly with the seasonal course of the maximum hydraulic conductance of leaf laminae of HgCl2-treated shoots (K lamina(HgCl2)), and with the seasonal course of the difference (dK lamina) between K lamina and K lamina(HgCl2). However, it did not correlate strongly with the seasonal course of the hydraulic conductance of stem and petioles of the shoot (K stpt) in six temperate deciduous tree species. The species ranked according to K lamina as follows: Populus tremula L. > Salix caprea L. > Padus avium Mill. > Quercus robur L. > Tilia cordata Mill. > Acer platanoides L. The species-specific maxima of K lamina correlated positively with the simultaneous values of K lamina(HgCl2), dK lamina and K stpt; the correlation was strongest with K lamina(HgCl2). It was concluded that the seasonal dynamics of maximum hydraulic conductance of leaf laminae was determined almost equally by the seasonal dynamics of the hydraulic conductance of foliar protoplasts and apoplast, but the inter-specific differences in K lamina were mainly caused by the different apoplastic hydraulic conductance in leaves of these species. The relative contribution of dK lamina (in K lamina) was highest in slow-growing species (~55% in A. platanoides) and the lowest in fast-growers (~30% in S. caprea).
Keywords: HgCl2, hydraulic conductance of leaf laminae, inter-specific variability, leaf dry mass per area.
Acknowledgments
The study was financed by the Estonian Ministry of Education and Science (grants no. 0172100s02 and 0172619s03) and the Estonian Science Foundation (grant no. 5305).
Aasamaa K, Sõber A
(2001) Hydraulic conductance and stomatal sensitivity to changes of leaf water status in six deciduous tree species. Biologia Plantarum 44, 65–73.
| Crossref | GoogleScholarGoogle Scholar |
Aasamaa K,
Sõber A, Rahi M
(2001) Leaf anatomical characteristics associated with shoot hydraulic conductance, stomatal conductance and stomatal sensitivity to changes of leaf water status in temperate deciduous trees. Australian Journal of Plant Physiology 28, 765–774.
Aasamaa K,
Sõber A,
Hartung W, Niinemets Ü
(2002) Rate of stomatal opening, shoot hydraulic conductance and photosynthetic characteristics in relation to leaf abscisic acid concentration in six temperate deciduous trees. Tree Physiology 22, 267–276.
| PubMed |
Aasamaa K,
Sõber A,
Hartung W, Niinemets Ü
(2004) Drought acclimation of two deciduous tree species of different layers in a temperate forest canopy. Trees (Berlin) 18, 93–101.
Becker P,
Tyree MT, Tsuda M
(1999) Hydraulic conductances of angiosperms versus conifers: similar transport sufficiency at the whole-plant level. Tree Physiology 19, 445–452.
| PubMed |
Biela A,
Grote K,
Otto B,
Hoth S,
Hedrich R, Kaldenhoff R
(1999) The Nicotiana tabacum plasma membrane aquaporin NtAQP1 is mercury-insensitive and permeable for glycerol. The Plant Journal 18, 565–570.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Brodribb TJ, Holbrook NM
(2004) Stomatal protection against hydraulic failure: a comparison of coexisting ferns and angiosperms. New Phytologist 162, 663–670.
| Crossref | GoogleScholarGoogle Scholar |
Bucci SJ,
Scholz FG,
Goldstein G,
Meinzer FC, Sternberg L da SL
(2003) Dynamic changes in hydraulic conductivity in petioles of two savanna tree species: factors and mechanisms contributing to the refilling of embolized vessels. Plant, Cell & Environment 26, 1633–1645.
| Crossref | GoogleScholarGoogle Scholar |
Catesson AM
(1994) Cambial ultrastructure and biochemistry: changes in relation to vascular tissue differentiation and seasonal cycle. International Journal of Plant Sciences 155, 251–261.
| Crossref | GoogleScholarGoogle Scholar |
Chaumont F,
Barrieu F,
Wojcik E,
Chrispeels MJ, Jung R
(2001) Aquaporins constitute a large and highly divergent protein family in maize. Plant Physiology 125, 1206–1215.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Cochard H, Tyree MT
(1990) Xylem dysfunction in Quercus: vessel sizes, tyloses, cavitation and seasonal changes in embolism. Tree Physiology 6, 393–407.
| PubMed |
Cochard H,
Nardini A, Coll L
(2004) Hydraulic architecture of leaf blades: where is the main resistance? Plant, Cell & Environment 27, 1257–1267.
| Crossref | GoogleScholarGoogle Scholar |
Dickison, WC (2000).
Domec JC, Gartner BL
(2002) How do water transport and water storage differ in coniferous earlywood and latewood? Journal of Experimental Botany 53, 2369–2379.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Eckert M,
Biela A,
Siefritz F, Kaldenhoff R
(1999) New aspects of plant aquaporin regulation and specificity. Journal of Experimental Botany 50, 1541–1545.
| Crossref | GoogleScholarGoogle Scholar |
Esau, K (1965).
Fettiplace R, Haydon DA
(1980) Water permeability of lipid membranes. Physiological Reviews 60, 510–550.
| PubMed |
Gascó A,
Nardini A, Salleo S
(2004) Resistance to water flow through leaves of Coffea arabica is dominated by extra-vascular tissues. Functional Plant Biology 31, 1161–1168.
| Crossref | GoogleScholarGoogle Scholar |
Hill AE,
Shachar-Hill B, Shachar-Hill Y
(2004) What are aquaporins for? Journal of Membrane Biology 197, 1–32.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Jaquish LL, Ewers FW
(2001) Seasonal conductivity and embolism in the roots and stems of two clonal ring-porous trees, Sassafras albidum (Lauraceae) and Rhus typhina (Anacardiaceae). American Journal of Botany 88, 206–212.
| PubMed |
Javot H, Maurel C
(2002) The role of aquaporins in root water uptake. Annals of Botany 90, 301–313.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Laas, E (1987).
Lersten NR
(1997) Occurrence of endodermis with a Casparian strip in stem and leaf. Botanical Review 63, 265–272.
Lin J,
He X,
Hu Y,
Kuang T, Ceulemans R
(2002) Lignification and lignin heterogeneity for various age classes of bamboo (Phylostachys pubescens) stems. Physiologia Plantarum 114, 296–302.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lu Z, Neumann PM
(1999) Water stress inhibits hydraulic conductance and leaf growth in rice seedlings but not the transport of water via mercury-sensitive water channels in the root. Plant Physiology 120, 143–152.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Macinnis-Ng C,
McClenahan K, Eamus D
(2004) Convergence in hydraulic architecture, water relations and primary productivity amongst habitats and across seasons in Sydney. Functional Plant Biology 31, 429–439.
| Crossref | GoogleScholarGoogle Scholar |
Martre P,
Morillon R,
Barrieu F,
North GB,
Nobel PS, Chrispeels MJ
(2002) Plasma membrane aquaporins play a significant role during recovery from water deficit. Plant Physiology 130, 2101–2110.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Mathiesen, A (1934).
Matzner S, Comstock J
(2001) The temperature dependence of shoot hydraulic resistance: implications for stomatal behaviour and hydraulic limitation. Plant, Cell & Environment 24, 1299–1307.
| Crossref | GoogleScholarGoogle Scholar |
Mederski HJ
(1961) Determination of internal water status of plants by beta ray gauging. Soil Science 92, 143–146.
Morillon R, Chrispeels MJ
(2001) The role of ABA and the transpiration stream in the regulation of the osmotic water permeability of leaf cells. Proceedings of National Academy of Sciences USA 98, 14138–14143.
| Crossref | GoogleScholarGoogle Scholar |
Nardini A
(2001) Are sclerophylls and malacophylls hydraulically different? Biologia Plantarum 44, 239–245.
| Crossref | GoogleScholarGoogle Scholar |
Nardini A, Pitt F
(1999) Drought resistance of Quercus pubescens as a function of root hydraulic conductance, xylem embolism and hydraulic architecture. New Phytologist 143, 485–493.
| Crossref | GoogleScholarGoogle Scholar |
Niinemets Ü,
Kull O, Tenhunen JD
(1998) An analysis of light effects on foliar morphology, physiology, and light interception in temperate deciduous woody species of contrasting shade tolerance. Tree Physiology 18, 681–696.
| PubMed |
North GB,
Martre P, Nobel PS
(2004) Aquaporins account for variations in hydraulic conductance for metabolically active root regions of Agave deserti in wet, dry, and rewetted soil. Plant, Cell & Environment 27, 219–228.
| Crossref | GoogleScholarGoogle Scholar |
Otto B, Kaldenhoff R
(2000) Cell-specific expression of the mercury-insensitive plasma membrane aquaporin NtAQP1 from Nicotiana tabacum.
Planta 211, 167–172..
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pääkönen E,
Günthardt-Goerg MS, Holopainen T
(1998) Responses of leaf processes in a sensitive birch (Betula pendula Roth.) clone to ozone combined with drought. Annals of Botany 82, 49–59.
| Crossref | GoogleScholarGoogle Scholar |
Prior LD, Eamus D
(2000) Seasonal changes in hydraulic conductance, xylem embolism and leaf area in Eucalyptus tetrodonta and Eucalyptus miniata saplings in a north Australian savanna. Plant, Cell & Environment 23, 955–965.
| Crossref | GoogleScholarGoogle Scholar |
Ranathunge K,
Kotula L,
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. Journal of Experimental Botany 55, 433–447.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Rüdinger M,
Hallgren SW,
Steudle E, Schulze ED
(1994) Hydraulic and osmotic properties of spruce roots. Journal of Experimental Botany 45, 1413–1425.
Sack L,
Melcher PJ,
Zwieniecki MA, Holbrook NM
(2002) The hydraulic conductance of the angiosperm leaf lamina: a comparison of three measurement methods. Journal of Experimental Botany 53, 2177–2184.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sack L,
Cowan PD,
Jaikumar N, Holbrook NM
(2003) The ‘hydrology’ of leaves: co-ordination of structure and function in temperate woody species. Plant, Cell & Environment 26, 1343–1356.
| Crossref | GoogleScholarGoogle Scholar |
Sack L,
Streeter CM, Holbrook NM
(2004) Hydraulic analysis of water flow through leaves of sugar maple and red oak. Plant Physiology 134, 1824–1833.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sack L,
Tyree MT, Holbrook NM
(2005) Leaf hydraulic architecture correlates with regeneration irradiance in tropical rainforest trees. New Phytologist 167, 403–413.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Salleo S, Nardini A
(2000) Sclerophylly: evolutionary advantage or mere epiphenomenon? Plant Biosystems 134, 247–259.
| Crossref |
Salleo S,
Raimondo F,
Trifilò P, Nardini A
(2003) Axial-to-radial water permeability of leaf major veins: a possible determinant of the impact of vein embolism on leaf hydraulics? Plant, Cell & Environment 26, 1749–1758.
| Crossref | GoogleScholarGoogle Scholar |
Sõber A
(1996) Simultaneous measurement of leaf hydraulic and stomatal conductances by pressure bomb, gas exchange and β-gauge techniques. Proceedings of Estonian Academy of Sciences. Biology 45, 35–43.
Sõber A, Moldau H
(1977) An apparatus with separate conditioning of the plant and the leaf for determination of stomatal resistance and leaf water content. Fiziologia Rastenii [In Russian] 24, 1301–1307.
Steppe K, Lemeur R
(2004) An experimental system for analysis of the dynamic sap-flow characteristics in young trees: results of a beech tree. Functional Plant Biology 31, 83–92.
| Crossref | GoogleScholarGoogle Scholar |
Steudle E
(2000) Water uptake by plant roots: an integration of views. Plant and Soil 226, 45–56.
| Crossref | GoogleScholarGoogle Scholar |
Steudle E, Peterson CA
(1998) How does water get through roots? Journal of Experimental Botany 49, 775–788.
| Crossref | GoogleScholarGoogle Scholar |
Suga S,
Murai M,
Kuwagata T, Maeshima M
(2003) Differences in aquaporin levels among cell types of radish and measurement of osmotic water permeability of individual protoplast. Plant & Cell Physiology 44, 277–286.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Trifilò P,
Gascó A,
Raimondo F,
Nardini A, Salleo S
(2003) Kinetics of recovery of leaf hydraulic conductance and vein functionality from cavitation-induced embolism in sunflower. Journal of Experimental Botany 54, 2323–2330.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tyree MT, Cheung YNS
(1977) Resistance to water flow in Fagus grandifolia leaves. Canadian Journal of Botany 55, 2591–2599.
Tyree MT,
Sinclair B,
Lu P, Granier A
(1993) Whole-shoot hydraulic resistance in Quercus species measured with a new high-pressure flowmeter. Annals of Science 50, 417–423.
Tyree MT,
Velez V, Dalling JW
(1998) Growth dynamics of root and shoot hydraulic conductance in seedlings of five neotropical tree species: scaling to show possible adaptation to differing light regimes. Oecologia 114, 293–298.
| Crossref | GoogleScholarGoogle Scholar |
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 Physiology 120, 11–21.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tyree MT,
Nardini A,
Salleo S,
Sack L, El Omari B
(2005) The dependence of leaf hydraulic conductance on irradiance during HPFM measurements: any role for stomatal response? Journal of Experimental Botany 56, 737–744.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Uemura A,
Ishida A,
Tobias DJ,
Koike N, Matsumoto Y
(2004) Linkage between seasonal gas exchange and hydraulic acclimation in the top canopy leaves of Fagus trees in a mesic forest in Japan. Trees (Berlin) 18, 452–459.
Vogt UK
(2001) Hydraulic vulnerability, vessel refilling, and seasonal courses of stem water potential of Sorbus aucuparia L. and Sambucus nigra L. Journal of Experimental Botany 52, 1527–1536.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wu XQ,
Lin JX,
Zhu JM,
Hu YX,
Hartmann K, Schreiber L
(2003) Casparian strips in needles of Pinus bungeana: isolation and chemical characterization. Physiologia Plantarum 117, 421–424.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Yakir D,
DeNiro MJ, Gat JR
(1990) Natural deuterium and oxygen-18 enrichment of leaf water of cotton plants grown under wet and dry conditions: evidence for water compartmentation and its dynamics. Plant, Cell & Environment 13, 49–56.
Yang S,
Maeshima M,
Tanaka Y, Komatsu S
(2003) Modulation of vacuolar H+-pumps and aquaporin by phytohormones in rice seedling leaf sheaths. Biological & Pharmaceutical Bulletin 26, 88–92.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Zwieniecki MA,
Melcher PJ,
Boyce CK,
Sack L, Holbrook NM
(2002) Hydraulic architecture of leaf venation in Laurus nobilis L. Plant, Cell & Environment 25, 1445–1450.
| Crossref | GoogleScholarGoogle Scholar |