Abstract
We investigated the potential links between stomatal control of transpiration and the risk of embolism in root and shoot xylem of seedlings of three Mediterranean conifers (Cupressus sempervirens, Pinus halepensis and P. nigra) grown in a greenhouse under semi-controlled conditions. We measured the intrinsic vulnerability to embolism in roots and current year shoots by the air injection method. Root and shoot segments were subjected to increasing pressures, and the induced loss of hydraulic conductivity recorded. The three species displayed very different vulnerabilities in shoots, with P. nigra being much more vulnerable than P. halepensis and C. sempervirens. Roots were distinctly more vulnerable than shoots in C. sempervirens and P. halepensis (50% loss of conductivity induced at 3.0 MPa and 1.7 MPa higher xylem water potential in roots vs shoots). In P. nigra, no significant difference of vulnerability between shoots and roots was found. Seedlings were subjected to soil drought, and stomatal conductance, twig hydraulic conductivity and needle water potential were measured. The water potential resulting in almost complete stomatal closure (90%) was very close to the threshold water potential inducing loss of conductivity (10%) in twigs in P nigra, resulting in a very narrow safety margin between stomatal closure and embolism induction. The safety margin was larger in P. halepensis and greatest in C. sempervirens. Unexpectedly, this water potential threshold produced a 30–50% loss of conductivity in 3–5 mm diameter roots, depending on the species. The implications of this finding are discussed.
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References
Alder NN, Sperry JS, Pockman WT (1996) Root and stem xylem embolism, stomatal conductance, and leaf turgor in Acer grandidentatum populations along a soil moisture gradient. Oecologia 105:293–301
Cochard H (2002) Xylem embolism and drought-induced stomatal closure in maize. Planta 215:466–471
Cochard H, Bréda N, Granier A (1996) Whole tree hydraulic conductance and water loss regulation in Quercus during drought: evidence for stomatal control of embolism? Ann For Sci 53:197–206
Cochard H, Coll L, Le Roux X, Améglio T (2002) Unraveling the effects of plant hydraulics on stomatal closure during water stress in walnut. Plant Physiol 128:282–290
Edwards WRN, Jarvis AJ, Grace J, Moncrieff JB (1994) Reversing cavitation in tracheids of Pinus sylvestris L. under negative water potentials. Plant Cell Environ 17:389–397
Ewers FW, North GB, Nobel PS (1992) Root-stem junctions of a desert monocotyledon and a dicotyledon: hydraulic consequences under wet conditions and during drought. New Phytol 121:377–385
Ewers FW, Cochard H, Tyree MT (1997) A survey of root pressures in vines of a tropical lowland forest. Oecologia 110:191–196
Fisher JB, Guillermo AA, Ewers FW, Lopez-Portillo J (1997) Survey of root pressure in tropical vines and woody species. Int J Plant Sci 158:44–50
Froux F, Huc R, Ducrey M, Dreyer E (2002) Xylem hydraulic efficiency versus vulnerability in seedlings of four contrasting Mediterranean tree species (Cedrus atlantica, Cupressus sempervirens, Pinus halepensis and Pinus nigra). Ann For Sci 59:409–418
Hacke UG, Sauter JJ (1996) Drought-induced xylem dysfunction in petioles, branches, and roots of Populus balsamifera L. and Alnus glutinosa (L.) Gaertn. Plant Physiol 111:413–417
Hacke UG, Sperry JS, Ewers BE, Ellsworth DS, Schäfer KVR, Oren R (2000a) Influence of soil porosity on water use in Pinus taeda. Oecologia 124:495–505
Hacke UG, Sperry JS, Pittermann J (2000b) Drought experience and cavitation resistance in six shrubs from the Great Basin, Utah. Basic Appl Ecol 1:31–41
Holbrook NM, Burns MJ, Field CB (1995) Negative xylem pressure in plants: a test of balancing pressure technique. Science 270:1193–1194
Hsiao TC, Xu L-K (2000) Sensitivity of growth of roots versus leaves to water stress: biophysical analysis and relation to water transport. J Exp Bot 51:1595–1616
Hubbart RM, Ryan MG, Stiller V, Sperry JS (2001) Stomatal conductance and photosynthesis vary linearly with plant hydraulic conductance in ponderosa pine. Plant Cell Environ 24:113–121
Jones HG, Sutherland RA (1991) Stomatal control of xylem embolism. Plant Cell Environ 14:607–612
Kavanagh KL, Bond BJ, Aitken SN, Gartner BL, Knowe S (1999) Shoot and root vulnerability to xylem cavitation in four populations of Douglas-fir seedlings. Tree Physiol 19:31–37
Lu P, Biron P, Granier A, Cochard H (1996) Water relations of adult Norway spruce (Picea abies (L) Karst) under soil drought in the Vosges mountains: whole-tree hydraulic conductance, xylem embolism and water loss regulation. Ann For Sci 53:113–121
Martinez-Vilalta J, Prat E, Oliveras J, Piñol J (2002) Xylem hydraulic properties in roots and stems of nine Mediterranean woody species. Oecologia 133:19–29
Nardini A, Salleo S (2000) Limitation of stomatal conductance by hydraulic traits: sensing or preventing xylem cavitation? Trees 15:14–24
Nardini A, Tyree MT, Salleo S (2001) Xylem cavitation in the leaf of Prunus laurocerasus and its impact on leaf hydraulics. Plant Physiol 125:1700–1709
North GB, Nobel PS (1996) Radial hydraulic conductivity of individual root tissues of Opuntia ficus-indica (L.) Miller as soil moisture varies. Ann Bot 77:133–142
Passioura JB (1988) Water transport in and to roots. Annu Rev Plant Physiol Plant Mol Biol 39:245–265
Pockman WT, Sperry JS (2000) Vulnerability to xylem cavitation and the distribution of Sonoran Desert vegetation. Am J Bot 87:1297–1299
Saliendra NZ, Sperry JS, Comstock JP (1995) Influence of leaf water status on stomatal response to humidity, hydraulic conductance, and soil drought in Betula occidentalis. Planta 196:357–366
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, Nardini A, Pitt F, Lo Gullo MA (2000) Xylem cavitation and hydraulic control of stomatal conductance in Laurel (Laurus nobilis L.). Plant Cell Environ 23:71–79
Sobrado MA, Grace J, Jarvis PG (1992) The limits to xylem embolism recovery in Pinus sylvestris L. J Exp Bot 251:831–836
Sparks JP, Black RA (1999) Regulation of water loss in populations of Populus trichocarpa: the role of stomatal control in preventing xylem cavitation. Tree Physiol 19:453–459
Sperry JS, Ikeda T (1997) Xylem cavitation in roots and stems of Douglas-fir and white fir. Tree Physiol 17:275–280
Sperry JS, Pockman WT (1993) Limitation of transpiration by hydraulic conductance and xylem cavitation in Betula occidentalis. Plant Cell Environ 16:279–287
Sperry JS, Saliendra NZ (1994) Intra- and inter-plant variation in xylem cavitation in Betula occidentalis. Plant Cell Environ 17:1233–1241
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, Donnelly JR, Tyree MT (1988) A method for measuring hydraulic conductivity and embolism in xylem. Plant Cell Environ 11:35–40
Sperry JS, Alder NN, Eastlack SE (1993) The effect of reduced hydraulic conductance on stomatal conductance and xylem cavitation. J Exp Bot 44:1075–1082
Sperry JS, Hacke UG, Oren R, Comstock JP (2002) Water deficits and hydraulic limits to leaf water supply. Plant Cell Environ 25:251–263
Steudle E (2000) Water uptake by roots: effects of water deficit. J Exp Bot 51:1531–1542
Tardieu F, Davies WJ (1993) Integration of hydraulic and chemical signaling in the control of stomatal conductance and water status of droughted plants. Plant Cell Environ 16:341–349
Tsuda M, Tyree MT (1997) Whole-plant hydraulic resistance and vulnerability segmentation in Acer saccharinum. Tree Physiol 17:351–357
Tyree MT, Ewers FW (1991) Tansley Review No. 34. The hydraulic architecture of trees and other woody plants. New Phytol 119:345–360
Tyree MT, Ewers FW (1996) Hydraulic architecture of woody tropical plants. In: Mulkey SS, Chazdon RL, Smith AP (eds) Tropical forest plant ecophysiology. Chapman and Hall, London, pp 218–241
Tyree MT, Sperry JS (1988) Do woody plants operate near the point of catastrophic xylem dysfunction caused by dynamic water stress? Plant Physiol 88:574–580
Tyree MT, Yang S (1992) Hydraulic conductivity recovery versus water pressure in xylem of Acer saccharum. Plant Physiol 100:669–676
Tyree MT, Cochard H, Cruiziat P, Sinclair B, Ameglio T (1993) Drought-induced leaf shedding in walnut. Evidence for vulnerability segmentation. Plant Cell Environ 16:879–882
Acknowledgements
F.F. was supported by a PhD grant of the French Ministry of Education. We are indebted to Mr. Didier Betored and Mr. Arnaud Jouineau for their technical assistance in growing the plants and maintaining the experiment. We thank Dr. Hervé Cochard for very helpful advice and comments on an early draft of the paper, and Dr. Jean-Marc Guehl and Prof. Dr. Pierre Dizengremel for fruitful discussions. We are grateful to Dr. Stephen Hallgren for English language review and comments on the manuscript.
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Froux, F., Ducrey, M., Dreyer, E. et al. Vulnerability to embolism differs in roots and shoots and among three Mediterranean conifers: consequences for stomatal regulation of water loss?. Trees 19, 137–144 (2005). https://doi.org/10.1007/s00468-004-0372-5
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DOI: https://doi.org/10.1007/s00468-004-0372-5