Báo cáo khoa học: "Use of pressure volume curves in water relation analysis on woody shoots: influence of rehydration and comparison of four European oak species"

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Original article Use of pressure volume in water relation curves shoots: analysis woody on influence of rehydration and comparison of four European oak species 12 Dreyer F Bousquet 2 Ducrey E M 1 d’Écophysiologie INRA, Laboratoire de Bioclimatologie et Forestières, Champenoux, 54280 Seichamps; 2 Station de Sylviculture Méditerranéenne, avenue Vivaldi, INRA, 86000 Avignon, France 7 November 1989; accepted 7 May 1990) (Received Summary - Pressure volume analyses were undertaken on leafy shoots of 4 European oak species (Quercus robur, Q petraea, Q pubescens and Q ilex) in order to determine the re- lationship between leaf water potential, average osmotic potential and volume averaged tur- gor. Some technical limitations of pressure volume analysis, as shown by the influence of the resaturation method on computed turgor, were overcome by accounting for losses of intercellular water during the first stages of dehydration. Variations in leaf to stem ratio, which are very important between large leaved oaks and small leaved evergreens, surprisingly did not influence the relative symplasmic volume of our samples. Differences in mean osmotic potential at full turgor (Π were related to species, with higher values in drought adapted ) 0 species, and to leaf age and growing conditions. Values of volumetric modulus of elasticity (ϵ did not significantly influence the relations between leaf water potential (Ψ and turgor ) o ) w (P) in different species. This relationship was mostly related to Π Finally, tolerance to drought . 0 appeared to be related more to the ability to osmotically adjust in response to changes in environment rather than to the absolute values of Π . 0 water relations / Quercus sp / / turgor / water pressure-volume potential curve Résumé - Utilisation de courbes pression/volume dans l’analyse des relations hydri- ques de rameaux feuillés: influence de la réhydratation et comparaison de quatre es- pèces de chênes européens. Une analyse des relations hydriques de rameaux feuillés de 4 espèces de chêne (Quercus robur, Q petraea, Q pubescens, Q ilex) a été entreprise à l’aide de la technique des courbes pression-volume, afin de préciser les relations existant entre le potentiel hydrique foliaire, le potentiel osmotique moyen et la pression de turgescence moyenne. Un certain nombre de limites techniques dues par exemple, à la méthode de réhydratation des échantillons végétaux, ont été dépassées par la prise en compte des pertes * and Correspondence reprints
d’eau intercellulaire se produisant durant les premiers stades de déssèchement Des variations importantes du rapport des biomasses feuilles/tiges, liéesà la morphologie des espèces (grandes feuilles des chênes médioeuropéens par rapport aux sclérophylles des chênes verts), n’ont pas eu d’influence sur l’estimation du volume symplasmique relatif. Des différences importantes appa- raissent dans les valeurs de potentiel osmotiqueà pleine turgescence (Π0), en premier lieu entre espèces, avec des valeurs plus élevées pour des chênes adaptés à la sécheresse, mais aussi en fonction de l’âge des feuilles et des conditions dans lesquelles s’est efffectuée la croissance des arbres. Les valeurs prises par le module d’élasticité volumique (o n’influencent que peu les )ϵ relations entre potentiel hydrique foliaire (Ψ et turgescence (P), qui en fait dépendent étroitement ) w de celle de Π Enfin, les différences dans le degré de tolérance de périodes de sécheresse . 0 paraissent plus liées à la capacité des arbresà mettre en &oelig;uvre un ajustement osmotique en réponse aux perturbations de leur environnement qu’aux valeurs absolues de Π . 0 / turgescence / courbe pres- relations hydriques / Quercus sp / potentiel hydrique sion-volume INTRODUCTION Tolerance of leaf water deficits is mainly related to elastic properties of cell walls and to osmotic water potential The genus Quercus contains a wide at full turgor (Π Larger values of Π 0 ). 0 variety of species that exhibit very differ- imply a better maintenance of cell tur- ent ecological habits. In Europe, the most gor (P) at a given leaf water potential important species for forestry are Quer- (Ψ (Tyree and Jarvis, 1982). A larger ) w cus robur L and Q petraea (Matt) Liebl. cell wall elasticity limits decreases in P Both species belong to the section robur with decreasing Ψ Variability of Π in 0 . w of the subgenus Lepidobalanus (Krus- a great range of American hardwoods mann, 1978), and are mostly found in re- has been reviewed recently by Abrams gions with few and limited periods of (1988b). He emphasized that variations drought. Other species, such as Q pubes- within a given species are often larger cens Willd (subgenus Lepidobalanus than those between species, and that section robur) and Q ilex (an evergreen variations were related to leaf age, local sclerophyll, subgenus Lepidobalanus stand conditions, and physiological section ilex), are located on drier sites adaptation to recurrent drought through in Southern Europe. osmo-regulation. Water relation parameters are most Ecological studies conducted in oak often obtained by establishing so-called differences be- shown stands have "pressure-volume relations" (Tyree and tween Q petraea and Q robur in their Hammel, 1972). However, the use of this ability to survive a severe summer technique with woody shoots may yield drought, such as the drought of 1976 some artifacts due to the variable ratio in Western Europe when the former of foliar to associated stem tissues in species was observed to be more re- samples (Neufeld and Teskey, 1986), sistant than the latter (Becker and Lévy, and, therefore, to the presence of larger 1982). A variety of mechanisms may be amounts of apoplastic water in stem ver- responsible for these differences; these sus leaf tissues. include better soil colonization by roots, In this paper, we describe the water re- efficient control of water loss more lations obtained with the pressure-volume during stress periods, and/or a better method on leafy shoots of 4 oak spe- ability to tolerate leaf water deficits.
cies growing under a given set of en- vironmental conditions. Before undertaking interspecific comparisons, the effects of re- hydration techniques on computed water relation parameters were evaluated and these results were used to adjust values of the parameters used to develop the spe- cies comparison. MATERIAL AND METHODS potential isotherms were established Water using the transpiration method described by Hinckley et al (1980), where a shoot is tran- spiring freely, and its weight and water po- tential are recorded at regular intervals. Theory Theory of pressure-volume curves has been established by Tyree and Hammel (1972). Pairs of values of leaf water potential Ψ and w leaf saturation deficit D, corresponding to suc- cessive states of dehydration, are plotted as: This expression relies on the hypothesis that all changes in leaf water content are due to changes in symplasmic water content, and that the apoplastic and intercellular wa- ter content remain constant. Such a curve, as shown in figure 1, displays a linear re- gion where turgor is equal to 0. A linear re- gression (least squares analysis) through the points of this straight segment results where Π is the osmotic pressure at full turgor. 0 in equation (1): The significance of both regression coefficients in equation (1) appears clearly: where Π is the volume averaged osmotic pressure of the leaf, a the slope of the fit- where Fs is the symplasm fraction of the leaf. ted line, b the Y-axis intercept, Vsi the ac- This estimation is obtained through an ex- tual symplasmic volume of the leaf, N the s trapolation of the linear regression toward total number of moles of solutes present in the X-axis (fig 1). There is, however, some the vacuoles, R the gas constant and T the uncertainty regarding this value (Tyree and absolute temperature. Richter, 1982). Because: is de- The non-linear fraction of the curve scribed by: volume at full where V is the symplasmic s turgor and V the apoplastic volume, equa- a tion (1) may be transformed into: where Π is derived from equation (1) and P is the volume averaged turgor. The beha- viour of P with changes in D is related to
National des Forêts nursery at Villers-lès- elasticity. The volumetric modulus of cellular Nancy and were grown for 4 years in pots elasticity is estimated as (Tyree and Jarvis, containing 30 I of a sandy-loam, in a green- 1982; Fanjul and Rosher, 1984): house, at Champenoux (near Nancy); irriga- tion was manual. Both species were visually changes in D in P with and changes as: differentiated based on their leaf mor- phology, Q petraea by its differentiated substitution: and by petiole and Q robur by its well defined ears on the base of the lamina. In order to assess which may be approximated by: the effect of natural stand conditions, 30- year-old Q petraea trees (dominant height: At full turgor, RWC is equal to 1, and about 12 m) grown in Champenoux "Forêt volumetric modulus of elasticity at full turgor Domaniale" were also used. Shoots were col- lected on 4 different individuals by rifle shoot- ϵ is calculated as: o ing; only leaves exposed to full light were selected. Collection was undertaken in The function P= f(D) is fitted to a second August-September after a period of natural + alpha;D 2 &βD+χ, and the modulus order polynom shortage. water of elasticity therefore corresponds to the value of the derivated function 2αD+β for trees of Q pubescens Thirty-year-old Willd and Q ilex L growing in natural stands D=0, that is β. near Avignon in Southern France were studied. Only well developed adult leaves Plant material were used for the measurements. However, in the case of the sempervirent species Measurements were taken partly in Avignon Q ilex, measurements were made either on and partly in Nancy on leafy shoots of the previous year leaves (in April), later called following species: "old" leaves, or on current-year leaves (in July, "young" leaves). For all species, leafy Quercus robur L and Q petraea (Matt) bearing 4-10 leaves, were Liebl (measurements in Nancy). Seedlings of shoots, harvested at the end of the afternoon. these 2 species originated from the Office
rehydrated (ie, through the stem) and the Rehydration techniques other from a twig completely immersed for Three different rehydration techniques were 12 h. These data were used to compute tested on Q ilex shoots during April prior to the relationship between leaf saturation extensive experiments (table I): deficit (D) and measured water potential standard method: the cut stem was plung- - (Ψ as shown in figure 2b. A considerable ) w ed into tap water and stored at 4-10 °C, in difference exists between the 2 curves; the darkness for 12 h; first steps of dehydration for the immersed 24 h rehydration: the same technique was - applied, but rehydration last for 24 h; sample are not accompanied by any sig- immersion: the leafy shoot was completely - nificant change in Ψ After these initial de- . w immersed under water at 4-10 °C in dark- hydration steps, the pattern of both curves ness for 12 h. is similar, and may be described by a second order polynomial. Intersection of Pressure-volume parameters each curve with the Y-axis approximates the shift δ in D due to water losses without Pressure-volume relations were established appreciable changes in Ψ This shift is . w follows: water was carefully removed from as present for immersed samples alone and a rehydrated shoot, and the shoot was then is absent for most stem rehydrated weighed to establish full turgor fresh weight (FW The corresponding water potential samples. This difference is probably due ). ft was measured with a pressure chamber, in to an oversaturation of apoplasmic and in- which pressure was gradually increased tercellular spaces in leaves and stems be- ) -1 min until the appearence of a (+0.3 MPa cause of immersion. sap meniscus at the cut end occurred. The Plotting the results obtained with an balance pressure was recorded with a pres- sure transducer Protais CPM 20 and a milli- immersed sample on a Höfler diagram Voltmeter. Pressure was released at the (fig 2c) shows the spurious effects of same low rate, and the shoot was allowed over resaturation on calculated turgor to transpire for about 20 min. This procedure pressure (P): a long plateau appears was repeated until water potential reached before the typical decrease in P with D. values of about -4 MPa. We may correct the values of D for the The absence of any significant weight loss during pressurization was verified. After shift (δ), using the following equation: reaching -4.0 MPa, leaves and stems were desiccated at 85 °C for 48 h, and weighed where D is the new value of leaf cor separately. The dry weight ratio of water deficit. D will be below 0 for cor leaves/stem (L/S) was calculated, and the saturation deficit corresponding to succes- all points corresponding to oversatura- sive dehydrations was estimated from: tion. These points have been eliminated from all subsequent calculations. DW weight and where FW is the shoot fresh Recalculation of parameters using the dry weight. corrected values of D results in a mod- ified Höfler diagram as shown in figure 2c: the plateau in P has completely dis- RESULTS appeared, and P evolution is similar to the general model. Effects of rehydration technique on Statistical results shown in tables II calculated water relation parameters and III confirm that these shifts (δ) ap- (Quercus ilex, old leaves) pear in all pressure-volume data ob- tained with immersed samples. They Figure 2a shows 2 pressure-volume attain a mean value of 0.3 with im- curves, 1 obtained from a twig "normally"
is not affected but all other parameters mersed samples, and values of less Osmotic potential at full turgor (Π ) 0 than 0.1 with stem rehydrated samples. are. is underestimated while the volumetric Even the stem rehydration technique elastic modulus at full turgor (o and the ) ϵ may result in oversaturation, but with leaf saturation deficit at turgor loss (D ) tl relatively small effects on calculated P. are underestimated (table II). Consequences of this oversaturation arti- When corrected values of D are used, fact on calculated parameters are impor- these artifacts are minimized. Table III turgor loss) (water potential at tant: Ψ wti
Effects of leaf age in Quercus ilex comparison of water relation shows a parameters obtained with corrected Results in table IV show that water re- values D no significant differences ; cor lation parameters of non-current leaves appear anymore, except for &o . epsiv; of the previous year differ markedly In the following analyses, we will use from those of current year leaves: Π , 0 for old leaves of Quercus ilex mean Ψ are much lower and D is much tl wtl values calculated using stem rehydra- higher while &o and Fs are not affected. epsiv; tion (12 or 24 h) and corrected values Therefore both groups will be con- of D whenever needed.
sidered separately for the inter- second, the expected relationship be- general species analysis. F and the leaf/stem dry weight s tween ratio (L/S) does not occur; third, the species with lowest L/S also display the largest values of F Finally, no statisti- . s between Comparison and species growth conditions cal correlation was noted between F s and L/S values of individual twigs for given species-treatment (r 0.11). = 2 a There are many differences between Figure 3 illustrates the relations be- the study species (table IV). Major re- tween P and Ψ obtained with 3 differ- w sults will be noted briefly. ent Q pubescens and Q petraea 0 Π is highest for Q robur and Q petraea - individuals. These relationships are ap- grown under a greenhouse environment. It is significantly lower in Q petraea and Q pubescens growing in stands; and the latter values appear intermediate between those of curvent and previous year leaves of Q ilex. The lowest value of Π is ob- 0 served on old foliage of Q ilex; the same ranking is noted for Ψ wtl - and D however, differences between ; tl species for these parameters, although still significant, were smaller because of increased variability; differences in &o are not consistently epsiv; - significant; &o seems to be lower for epsiv; Q robur and Q petraea grown under greenhouse environment; a most striking are the results concern- - ing relative symplasmic volume (Fs). First, the greatest values of F are s noted in Southern, small-leaved oaks; by linear regressions proximated &clearly t 2 (rhat, ge;0.99). This representation shows for a given Ψ P is much , w greater in Q pubescens than in Q petraea. For Q petraea, this differ- ence is mainly the result of a lower Π . 0 Mean tissue elasticity does not signifi- cantly affect the relationship. We used the fact that the P/Ψ re- w lationship is nearly linear to present our results in a synthesis diagram: mean values of Π for each species, which 0 are equal to the mean maximal P, are connected by a straight line to the mean values of Ψ This line approxi- . wtl
only occasionally with normal stem re- relationship between P mates the mean hydrated shoots. As suggested by for all species (fig 4). Differ- and Ψ w others (eg, Parker and Pallardy, 1987), ences between groups are largely due these results indicate that the changes to variations in the estimate pressure- in D without a change in Ψ are due w volume parameters. to an oversaturation of intercellular volumes in leaves and stems during re- hydration, and that this water is lost DISCUSSION during the first steps of dehydration. This artifact stongly affects the rela- leafy Pressure volume relations on tionship between P and D, resulting in shoots from woody species a "plateau" before decreasing normally with increasing D. Such plateaus have Possible artifacts arising from the use of been directly or indirectly described by the pressure-volume technique to esti- other investigators (Kandiko et al, 1980; mate water relation parameters for woody Parker et al, 1982; Dreyer, 1984; Ritchie twigs have been frequently discussed and Shula, 1984; Guyon, 1987), but (Neufeld and Teskey, 1986; Turner, 1988). have never been convincingly ex- The choice of the free transpiration ver- plained. Correcting the values of D for sus the within chamber pressurization the oversaturation with our method method is not clear as discrepancies with yields results of the same magnitude as both methods have been noted (Ritchie those obtained with standard methods, and Roden, 1985; Parker and Pallardy exhibiting an immediate decrease of P 1988a; Hardegree, 1989). These discre- with increasing D. pancies were mostly minor and both It should be noted that light oversat- methods are now generally accepted. uration effects also occur with standard One criticism of the free transpira- stem rehydration; we may therefore con- tion method is the fact that intercellular clude, as did Turner (1988), that short re- water content in leaves may change hydration periods of a few hours should during measurement. In fact, we have be used when possible. In addition, demonstrated that such changes occur, Meinzer et al (1986) have demonstrated and that they depend largely on the that resaturation may eliminate any tran- technique used for sample rehydration. sitory diurnal osmotic adjustment. During the first steps of dehydration, Varying leaf/stem ratio (L/S), for ex- apparent leaf water deficit (D) in- ample with smallleaved shoots of Q ilex creases without a parallel decrease in vs large leaved shoots of Q petraea or water potential (Ψ These findings ). w Q robur, could possibly modify some confirm those of Ritchie and Shula estimated parameters, because the (1984) and Parker and Pallardy (1987). ratio of symplasmic to total water Such behavior was attributed by Turner volume (F probably varies. However, ) s (1988) to membrane damage caused Neufeld and Teskey (1986) examined by the high turgor pressure in cells. In the effects of defoliating twigs (ie mod- the case of xeric plants displaying very ifying L/S); Π and Ψ estimates did o wtl low Ψ rehydration is also accompanied , w not change significantly. They also ob- by solute transfers causing changes in tained a curious result: their defolia- Π (Evans et al, 1990). In our case, the 0 tions did not promote a reduction in the appeared most effects observed estimate of the relative symplasmic frequently with immersed shoots, and
volume F In our study no significant . s perienced by the stand during the year correlation was detected between in- of measurement. Active adjustment of dividual values of L/S and F The effect . s 0 Π in response to drought has been re- of varying stem volumes on F esti- s ported for various tree species, but ad- mates remains a major problem of pres- justments are typically less than 0.5 MPa. sure-volume analyses on woody shoots. The following values have been reported for a wide set of species: 0.50, 0.54 and 0.26 MPa for Quercus alba, Q macro- Effects of leaf age carpa and Q stellata respectively (Parker and Pallardy, 1988b), 0.60, 0.23 and 0.13 A comparison between 2 age classes MPa for Q acutissima, Q alba and Q stel- of Q ilex leaves (current year leaves in lata (Ki and Pallardy, 1989), 0.4 MPa in July and previous year leaves in April) Tsuga heterophylla (Kandiko et al, 1980), confirms previous results regarding the 0.3 to 0.4 in Malus domestica (Fanjul and effects of leaf age: both Π and Ψ 0 wtl Rosher, 1984), 0.3 to 0.4 in Eucalyptus decreased (Roberts et al, 1980; Doi et microcarpa (Myers and Neales, 1986) al, 1986), and the volumetric modulus and 0.2 in Rosa hybrida (Auge et al, of elasticity &o remained relatively con- epsiv; 1986). In our case, a simple osmotic ad- (Roberts et al, 1980; Parker et al, stant justment may not account fully for the 1982). It is not clear whether these ef- large differences between greenhouse fects are due to leaf ageing alone, or saplings and mature trees. Light regime to drought preconditioning during the and possibly mineral nutrition may also previous summer. have a strong effect on water relation parameters. These results indicate that further data concerning drought precon- oak Comparing species ditioning are needed for oak seedlings; such data would be very important in un- Our results allow a clear separation of derstanding the production of drought studied species into 2 groups. The 1st hardened seedlings for transplanting. group is composed of both mesic spe- These large differences in Π which , 0 cies from Northern France, Q robur and appeared in response to changing en- Q petraea, cultivated under a green- vironmental conditions (greenhouse ver- house environment with optimal watering. sus stand), reveal an important plasticity The 2nd group is composed of Q petraea among species; it is therefore very risky under stand conditions and the more to compare tree species on the basis of xeric species from Southern France published data on Π and other water 0 (Q pubescens and Q ilex). The 1st group relation parameters. Nevertheless, a showed very similar results, while greater quick glance at Π and Ψ values in 0 wtl variability appeared in the 2nd. different oak species (table V) allows a The most striking result is the large schematic ranking of species. Values for difference between young trees growing our greenhouse trees appear high as in a greenhouse and older trees growing compared to those of most other oak in a stand as shown by results from species; only Q ellipsoidalis showed Q petraea. The difference between green- higher values. Other mesic species have house saplings and mature trees was 0.8 a similar range of values, eg, Juglans MPa for Π and 1.0 MPa for Ψ These 0 . wtl nigra (-1.47 and -2.04 MPa, Parker and very large differences may be due to ac- Pallardy, 1985), Juglans regia (-1.3 and climation to the summer drought ex-
ability to maintain a high turgor P when -1.9 MPa, Dreyer, 1984), Acer sach- transpiration or soil water conditions harinum (-1.4 and -2.3 MPa, Cheung et impose a low leaf water potential Ψ w al, 1975). Stand grown trees of Q petraea between (Turner, 1988). Relationships and the 2 mediterranean species have values of P and Ψ show clear w much lower values of Π and Ψ than 0 wtl mean differences between species in this re- those of most species. Similar low values gard. The degree of desiccation toler- have been observed in Malus domestica ance is rather obvious: Q ilex’s older (-2.2 and -3.3 MPa, Fanjul and Rosher, leaves are the most tolerant, followed 1984) and Olea oleaster (-2.0 and -2.9 by Q pubescens and Q petraea in MPa, Lo Gullo and Salleo, 1988). stands then Q ilex young leaves, and Significant differences appear be- finally by Q petrae and Q robur grown tween species in the volumetric mod- greenhouse. in a ulus of elasticity (ϵ Its values are ). o lower (higher elasticity) in Q robur and What can be the role of observed Q petraea than in Q pubescens and differences in Π and Ψ in the ability wtl 0 of tree species to tolerate dry environ- Q ilex, due to the greater sclerophylly of Southern oaks. The leaf saturation ments? These differences may be less important than generally suggested. In deficit at turgor loss (D is also higher ) tl fact, the large plasticy observed with in the Southern oaks. the species Q petraea suggests a It is generally accepted that the best major role of environmental conditions criterion for desiccation tolerance is the
in hardwood species in north eastern promoting adjustments to drought. Kansas. For Sci, 32, 687-696 Furthermore, the fact that Q petraea in Auge RM, Schekel KA, Wample RL (1986) stands at Nancy and Q pubescens at Osmotic adjustment in leaves of VA-my- Avignon have about the same Π and 0 corrhizal and non-mycorrhizal rose plants Ψ values indicates that these para- wtl in response to drought stress. Plant Phys- meters only play a minor role in drought iol 82, 765-770 tolerance. As also stated by Lo Gullo Bahari ZA, Pallardy SG, Parker WC (1985) and Salleo (1988) with sclerophyllous Photosynthesis, water relations, and plants, osmotic potential per se may drought adaptation in six woody species of oak-hickory forests in central Missouri. not be an index of drought tolerance. For Sci 31, 557-569 Other physiological parameters should Becker M, Lévy G (1982) Le dépérissement be tested, such as the stability of water du chêne en Forêt de Tronçais. Les conduction under drought, or even in- cause écologiques. Ann Sci For 36, 439- teractions between water and carbon 444 budgets. These conclusions need to be Cheung YNS, Tyree MT, Dainty J (1975) confirmed in further studies on oak Water relation parameters on single stress physiology, in which the plastic- leaves obtained in a pressure bomb and ity of water relations and hydraulic some ecological considerations. Can J Bot 53, 1342-1346 functions should be examined in paral- lel. Doi K, Morikawa K, Hinckley TM (1986) Sea- sonal trends of several water relation par- in ameters Cryptomeria japonica seedlings. Can J For Res 16, 74-77 ACKNOWLEDGEMENTS Dreyer E (1984) Cornportement d’une plante pérenne soumiseà des contraintes hy- driques: réponses physiologiques de The authors wish to thank P Gross, JM jeunes noyersà des périodes de séch- Gioria and JM Desjeunes for technical eresse. Thèse Docteur-Ingénieur, Univer- sité de Clermont Ferrand. assistance, and JM Guehl, A Granier and G Aussenac for discussions during Evans RD, Black RA, Link SO (1990) Rehy- dration-induced changes in pressure- this work. They are grateful to TM volume relationships of Artemisia Hinckley for considerable help in manu- tridentata Nutt ssp tridentata. Plant Cell script editing, and to both TM Hinckley Environ (in press) and P Cruiziat for helpful criticism of a Fanjul L, Rosher PH (1984) Effects of water first version of the manuscript. stress internal water relations of apple on leaves. Physiol Plant 62, 321-328 Guyon JP (1987) Étude des courbes pres- REFERENCES sion-volume de rameaux de 3 espèces forestières. Acta Oecol Oecol Appl 8, 363-370 Abrams MD (1988a) Comparative water re- SP Hardegree (1989) Discrepancies be- lations of three successional hardwood tween water potential isotherm measure- species in central Wisconsin. Tree Physiol ments on Pinus ponderosa seedling 4, 263-273. shoots: xylem hysteresis and apoplasmic Abrams MD (1988b) Sources of variation in osmotic potentials. Plant Cell Environ 12, osmotic potentials with special reference 57-62 to North American tree species. For Sci Hinckley TM, Duhme F, Hinckley AR, Richter 34, 1030-1046 H (1980) Water relations of drought hardy Abrams MD, Knapp AK (1986) Seasonal shrubs: osmotic potential and stomatal water relations of three gallery forest reactivity. Plant Cell Environ 3, 131-140
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