The canopy water relations of old-growth Douglas-fir trees

 We investigated whole tree water relations in 56–65 m tall, old-growth Pseudotsuga menziesii trees within the Wind River Canopy Crane site, Carson, Washington, USA. We measured at predawn and solar noon the vertical gradients in xylem pressure potential using a pressure chamber. On an Abies amabilis sapling located in the understory at the base of one of the study trees, predawn and solar noon xylem pressure potentials were also measured. Xylem pressure potential data were measured from late June through early September 1996 on foliage sampled from 1 to 64.5 m. Over this height gradient, predawn water potentials ranged from –0.23 to –1.10 MPa. Solar noon values showed an even greater range (from –0.44 to –2.51 MPa). At predawn, the water potential gradient approached the theoretical hydrostatic gradient (–0.0105 vs –0.010 MPa m^–1). The gradient at solar noon was steeper (–0.0331 MPa m^–1). Instantaneous stomatal conductances were not greatly different between young, sapling-sized and old-growth trees [0.094±0.033 (SD) vs 0.086±0.045 cm s^–1, respectively]. Stomata of both size classes of trees appeared very sensitive to increasing vapor pressure deficits. A comparison of stable carbon isotope values from the old-growth and sapling-sized trees indicated lower stomatal conductances in the old-growth. This study provides sound documentation regarding the utility of the cohesion theory in the interpretation of water potential gradients. This study also emphasizes inherent differences between sapling-sized and tall, old-growth trees. Received: 10 January 1998 / Accepted: 12 October 1998     

Does turgor limit growth in tall trees?

The gravitational component of water potential contributes a standing 0.01 MPa m^?1 to the xylem tension gradient in plants. In tall trees, this contribution can significantly reduce the water potential near the tree tops. The turgor of cells in buds and leaves is expected to decrease in direct proportion with leaf water potential along a height gradient unless osmotic adjustment occurs. The pressure–volume technique was used to characterize height‐dependent variation in leaf tissue water relations and shoot growth characteristics in young and old Douglas‐fir trees to determine the extent to which growth limitation with increasing height may be linked to the influence of the gravitational water potential gradient on leaf turgor. Values of leaf water potential (Ψ_l), bulk osmotic potential at full and zero turgor, and other key tissue water relations characteristics were estimated on foliage obtained at 13.5 m near the tops of young (approximately 25‐year‐old) trees and at 34.7, 44.2 and 55.6 m in the crowns of old‐growth (approximately 450‐year‐old) trees during portions of three consecutive growing seasons. The sampling periods coincided with bud swelling, expansion and maturation of new foliage. Vertical gradients of Ψ_l and pressure–volume analyses indicated that turgor decreased with increasing height, particularly during the late spring when vegetative buds began to swell. Vertical trends in branch elongation, leaf dimensions and leaf mass per area were consistent with increasing turgor limitation on shoot growth with increasing height. During the late spring (May), no osmotic adjustment to compensate for the gravitational gradient of Ψ_l was observed. By July, osmotic adjustment had occurred, but it was not sufficient to fully compensate for the vertical gradient of Ψ_l. In tall trees, the gravitational component of Ψ_l is superimposed on phenologically driven changes in leaf water relations characteristics, imposing potential constraints on turgor that may be indistinguishable from those associated with soil water deficits.     

Hydraulic limitation on maximum height of Pinus strobus trees in northern Minnesota,USA

Key message

Using comparisons within and between trees, the authors show evidence for hydraulic limitation of tree height in a humid-climate species that is far from the global maximum tree height.

Abstract

We measured water status and two indicators of drought stress as a function of height within the canopies of four tall (32–35 m) eastern white pines (Pinus strobus) at an old-growth site in northern Minnesota, USA. Pre-dawn and midday xylem pressure potential measured on terminal shoots (Ψ _shoot), needle length, and foliar carbon isotope discrimination (δ ¹³C) all showed within-canopy gradients consistent with increasing drought stress with height. Midday Ψ _shoot near tree tops was ?1.8 MPa, close to values associated with stomatal closure for other temperate conifers. Pre-dawn Ψ _shoot decreased with height at >2× the gradient in gravitational potential. δ ¹³C was strongly correlated with height and weakly correlated with light. Needles were 15–25 % shorter at canopy top compared to the bottom of the canopy. Midday Ψ _shoot and needle length showed significant differences in regression model coefficients from tree to tree. The patterns are consistent with hydraulic constraints on height growth of white pine at this site.     

Xylem water transport: is the available evidence consistent with the cohesion theory?

Since its introduction in the late 19th century, the so-called cohesion theory has become widely accepted as explaining the mechanism of the ascent of sap. According to the cohesion theory, the minimum standing vertical xylem tension gradient should be 0·01 MPa m⁻¹. When transpiration is occurring, frictional resistances are expected to make this gradient considerably steeper. The results of numerous pressure chamber measurements reported in the literature are generally regarded as corroborating the cohesion theory. Nevertheless, several reports of pressure chamber measurements in tall trees appear to be incompatible with predictions of the cohesion theory. Furthermore, the pressure chamber is an indirect method for inferring xylem pressure, which, until recently, has not been validated by comparison against a direct method. The xylem pressure probe provides a means of testing the validity of the pressure chamber and other indirect techniques for estimating xylem pressure. We discuss here the results of concurrent measurements made with the pressure chamber and the xylem pressure probe, particularly recent measurements made at the top of a tall tropical tree during the rainy season. These measurements indicate that the pressure chamber often substantially overestimates the tension previously existing in the xylem, especially in the partially dehydrated tissue of droughted plants. We also discuss other evidence obtained from classical and recent approaches for studying water transport. We conclude that the available evidence derived from a wide range of independent approaches warrants a critical reappraisal of tension-driven water transport as the exclusive mechanism of long-distance water transport in plants.     

Evaluation of water stress control with polyethylene glycols by analysis of guttation

The water relations of pepper plants (Capsicum frutescens L.) under conditions conducive to guttation were studied to evaluate the control of plant water stress with polyethylene glycols. The addition of polyethylene glycol 6000 to the nutrient solution resulted in water relations similar to those expected in soil at the same water potentials. Specifically, xylem pressure potential in the root and leaf became more negative during a 24-hour treatment period, while osmotic potential of the root xylem sap remained constant. The decrease in pressure potential was closely correlated with the decrease in osmotic potential of the nutrient solution. In contrast, the addition of polyethylene glycol 400 to the nutrient medium resulted in a reduction of osmotic potential in the root xylem sap; this osmotic adjustment in the xylem was large enough to establish an osmotic gradient for entry of water and cause guttation at a nutrient solution osmotic potential of −4.8 bars. Pressure potential in the root and leaf xylem became negative only at nutrient solution osmotic potentials lower than −4.8 bars. About half of the xylem osmotic adjustment in the presence of polyethylene glycol 400 was caused by increased accumulation of K⁺, Na⁺, Ca²⁺, and Mg²⁺ in the root xylem. These studies indicate that larger polyethylene glycol molecules such as polyethylene glycol 6000 are more useful for simulating soil water stress than smaller molecules such as polyethylene glycol 400.     

Morphological adaptations of tracheid structure to water stress gradients in the crown of Sequoiadendron giganteum

Summary Mean radial diameter of tracheids in young branches of a 90 m Sequoiadendron giganteum decreases linearly with height along a gradient correlated linearly with decreasing xylem pressure potential. These smaller tracheid diameters provide strength to resist strong mechanical tensions in the xylem column and hypothetically allow greater efficiencies of water conduction. Tracheid length is not significantly correlated with either water stress or tracheid diameter.     

Water Transport in the Liana Bauhinia fassoglensis (Fabaceae)

To determine the efficiency of xylem conductance in the liana (woody vine) Bauhinia fassoglensis Kotschy ex Schweinf., we measured hydraulic conductance per unit stem length (measured K_h), leaf-specific conductivity (LSC = K_h/distal leaf area), transpiration rate (E), xylem water potential (ε), vessel number, and vessel diameter. The measured K_h was 49% (se = 7%) of the predicted K_h from Poiseuille's law. The mean LSC for unbranched stem segments was 1.10 × 10⁻⁸ square meters per megapascal per second (se = 0.07). LSCs were much lower (about 0.2) at branch junctions. At midday, with E at 7 × 10⁻⁸ meters per second, the measured drop in ε was about 0.08 megapascal per meter along the stems and branches and about 0.27 megapascal in going from stem to leaf. In addition, there was a drop of about 0.20 megapascal at branch junctions as predicted by E/LSC. In diurnal measurements leaf ε never dropped below about −1.2 megapascal. For long (e.g. 16 meters) stems, the predicted mid-day drop in ε through the xylem transport system might be great enough to have substantial physiological impact.     

Morphological and reproductive responses of dominant plant species to local conditions in herbaceous successional stages of a calcareous hillside

Secondary succession on calcareous hillsides, initiated following the abandonment of agro-pastoral practices, is characterized by the transformation of initial short sward into tall herbaceous vegetation and finally woody formations. These structural changes are accompanied by modifications in ecological conditions but some species are able to persist and flower along the successional gradient. In this study, we compare reproductive and morphological traits of seven perennial species present in three successional stages [short grassland (SG), tall grassland (TG), and encroached grassland (EG)] to test if plant species present modifications along the successional gradient. The results show that morphological traits as height, leaf area and leaf dry mass increase for all studied species. Along the successional gradient, Teucrium chamaedrys increases ramet biomass more than twice (+145%) while Brachypodium pinnatum increases it even more (+340%). Maximum specific leaf area was observed in Brachypodium pinnatum (SLA = 20.4 mm² mg⁻¹) in SG, whereas Helianthemum nummularium and Teucrium chamaedrys have both rising SLA and falling leaf dry matter content in TG and EG. Concurrently, Helianthemum nummularium, Hippocrepis comosa and Teucrium chamaedrys show a clear decrease in sexual reproduction, with between 18 and 40% fewer flowers during the progress of succession. By contrast, Festuca lemanii, Sesleria caerulea and Brachypodium pinnatum increase their flower numbers per inflorescence (×3.6, ×3.3, and ×3.5, respectively). Festuca lemanii and Sesleria caerulea increase seed production to a maximum in TG, and Brachypodium pinnatum and Carex flacca increase seed output in TG and EG (×4.5, ×5.5, respectively). Changes in plants traits underscore the idea that species allocate resources differently probably because of increasing competition and decreasing edaphic constraints. This study also implies the potential existence of specific responses allowing plants to maintain existence within a plant community and explaining their contrasting performance during the succession.     

Direct and indirect measurements of Phloem turgor pressure in white ash

Direct determinations and indirect calculations of phloem turgor pressure were compared in white ash (Fraxinus americana L.). Direct measurements of trunk phloem turgor were made using a modified Hammel-type phloem needle connected to a pressure transducer. Turgor at the site of the direct measurements was calculated from the osmotic potential of the phloem sap and from the water potential of the xylem. It was assumed that the water potentials of the phloem and xylem were close to equilibrium at any one trunk location, at least under certain conditions. The water potential of the xylem was determined from the osmotic potential of xylem sap and from the xylem tension of previously bagged leaves, measured with a pressure chamber. The xylem tension of bagged leaves on a branch adjacent to the site of the direct measurements was considered equivalent to the xylem tension of the trunk at that point. While both the direct and indirect measurements of phloem turgor showed clear diurnal changes, the directly measured pressures were consistently lower than the calculated values. It is not clear at present whether the discrepancy between the two values lies primarily in the calculated or in the measured pressures, and thus, the results from both methods as described here must be regarded as estimates of true phloem turgor.     

Effect of osmotic stress on abscisic acid levels in xylem sap of sunflower (Helianthus annuus L.)

Summary Addition of an osmoticum (-12 bars) to the rooting medium of sunflowers (Helianthus annuus L.) caused an increase in the level of abscisic acid (ABA) present in xylem exudate subsequently collected from cut shoots. Using tall and dwarf plants it was shown that there was a time lag in the appearance of increased levels of ABA in tall plants when compared with dwarf plants. The results indicate that the leaves, rather than the roots are the site of synthesis of ABA present in the xylem sap of osmotically stressed sunflower plants.Abbreviation ABA abscisic acid     

How Does Water Ascend in Tall Trees and Other Vascular Plants?

Since the Cohesion Theory was first introduced, a series ofincompatible observations has appeared in the literature. Directmeasurements of xylem pressure in single vessels of higher plantsand tall trees by means of the xylem pressure probe techniqueindicate that xylem tension in the leaves of intact, transpiringplants is often much smaller than that predicted for transpiration-drivenwater ascent through continuous water columns. We conclude thatthe available evidence warrants a critical reappraisal of tension-drivenwater transport as the exclusive mechanism of long-distancewater transport in plants.Copyright 1995, 1999 Academic Press Cohesion Theory, higher plants, long-distance transport, trees, water ascent, xylem pressure probe     

Common DNA variants predict tall stature in Europeans

Genomic prediction of the extreme forms of adult body height or stature is of practical relevance in several areas such as pediatric endocrinology and forensic investigations. Here, we examine 770 extremely tall cases and 9,591 normal height controls in a population-based Dutch European sample to evaluate the capability of known height-associated DNA variants in predicting tall stature. Among the 180 normal height-associated single nucleotide polymorphisms (SNPs) previously reported by the Genetic Investigation of ANthropocentric Traits (GIANT) genome-wide association study on normal stature, in our data 166 (92.2 %) showed directionally consistent effects and 75 (41.7 %) showed nominally significant association with tall stature, indicating that the 180 GIANT SNPs are informative for tall stature in our Dutch sample. A prediction analysis based on the weighted allele sums method demonstrated a substantially improved potential for predicting tall stature (AUC = 0.75; 95 % CI 0.72–0.79) compared to a previous attempt using 54 height-associated SNPs (AUC = 0.65). The achieved accuracy is approaching practical relevance such as in pediatrics and forensics. Furthermore, a reanalysis of all SNPs at the 180 GIANT loci in our data identified novel secondary association signals for extreme tall stature at TGFB2 (P = 1.8 × 10^?13) and PCSK5 (P = 7.8 × 10^?11) suggesting the existence of allelic heterogeneity and underlining the importance of fine analysis of already discovered loci. Extrapolating from our results suggests that the genomic prediction of at least the extreme forms of common complex traits in humans including common diseases are likely to be informative if large numbers of trait-associated common DNA variants are available.     

The mechanisms of refilling of xylem conduits and bleeding of tall birch during spring

Seasonal variations in osmolality and components of xylem sap in tall birch trees were determined using several techniques. Xylem sap was extracted from branch and trunk sections of 58 trees using the very rapid gas bubble-based jet-discharge method. The 5-cm long wood pieces were taken at short intervals over the entire tree height. The data show that large biphasic osmolality gradients temporarily exist within the conducting xylem conduits during leaf emergence (up to 272 mosmol x kg(-1) at the apex). These gradients (arising mainly from glucose and fructose) were clearly held within the xylem conduit as demonstrated by (1)H NMR imaging of intact twigs. Refilling experiments with benzene, sucrose infusion, electron and light microscopy, as well as (1)H NMR chemical shift microimaging provided evidence that the xylem of birch represents a compartment confined by solute-reflecting barriers (radial: lipid linings/lipid bodies; axial: presumably air-filled spaces). These features allow transformation of osmolality gradients into osmotic pressure gradients. Refilling of the xylem occurs by a dual mechanism: from the base (by root pressure) and from the top (by hydrostatic pressure generated by xylem-bound osmotic pressure). The generation of osmotic pressure gradients was accompanied by bleeding. Bleeding could be observed at a height of up to 21 m. Bleeding rates measured at a given height decreased exponentially with time. Evidence is presented that the driving force for bleeding is the weight of the static water columns above the bleeding point. The pressure exerted by the water columns and the bleeding volume depend on the water-filling status of (communicating) vessels.     

Function and structure of leaves contributing to increasing water storage with height in the tallest <Emphasis Type="Italic">Cryptomeria japonica</Emphasis> trees of Japan

Key message

In Cryptomeria japonica , transfusion tissue in leaves may have functions of water storage and supply, which could compensate for hydraulic constraints with increasing height.

Abstract

The tallest trees of Cryptomeria japonica occur in climatic regions similar to the world’s tallest trees. We hypothesized that tall C. japonica trees would have evolved adaptive mechanisms to overcome height growth limitation. Here, we focused on foliar water storage, a mechanism recently discovered in Sequoia sempervirens. In C. japonica, leaf water potential at turgor loss did not change with height or light availability, while leaf hydraulic capacitance and succulence (water content per leaf surface area) increased, suggesting hydraulic compensation. Plasticity of leaf morphology could contribute to avoiding negative effects of height on photosynthesis. We also focused on the structure and function of transfusion tissue in leaves and its role in water storage and supply. Cross-sectional area of transfusion tissue increased with height, whereas that of xylem was constant. We confirmed that water flowed from vascular bundle to mesophyll via the transfusion tissue. Cryo-scanning electron microscopy images of leaf cross sections showed that transfusion cells were flattened, but not fully dehydrated when leaf water potential decreased in situ and by experimental dehydration, and cell deformation was more marked for treetop leaves than for lower-crown leaves. The shape of transfusion cells recovered at predawn as well as after experimental rehydration. As in S. sempervirens, transfusion tissue of C. japonica may function as a hydraulic buffer, absorbing and releasing water according to leaf water status. Anatomical and hydraulic properties contributing to foliar water storage may be an adaptive mechanism acquired by tall Cupressaceae trees to overcome the hydraulic constraints on physiological function with increasing height.

     

Occurrence of Inverted Water Potential Gradients between Soil and Bean Roots

Measurements with a pressure chamber were made of the xylem water potential of leaves, shoots and roots from bean plants (Pkaseolus vulgaris L. cv. Processor) grown with a 12 hour dark period and natural or artificial light conditions during the day. The water potentials were measured at the end of a dark period and during the light period. Measurements taken at the end of the dark period indicated normal potential gradients within the soil/plant system (leaf < shoot < root < soil), when the matric potential of soil water was relatively high (above ?0.02 bar), and the gradients then also remained normal during the day (natural light). When the soil water potential was ?1 bar or lower in the morning, however, the root xylem water potential was higher than the soil water potential; at very low soil water potentials (< ?4 bar) it remained higher during most of the day. In this case also leaf and shoot xylem water potentials were higher than the soil water potential in the early morning, although decreasing rapidly in daylight. Under artificial light, both leaf and root water potentials were higher than the soil water potential throughout the whole diurnal cycle when the latter potential was below ?4 bar. From measurements of stomatal diffusion resistance, transpiration, relative water content of leaves and of changes in the matric potential of soil water, it was concluded that when the matric potential of soil water was low, water could be taken up by the plant against a water potential gradient. Because leaf xylem water potential was always lower than root xylem water potential, the mechanism involved in the inversion of water potential gradient must be localized in the roots, and probably related to ion uptake. Symbols and abbreviations used in the text: Ψ: Plant water potential (thermocouple psychrometer); Ψx: Xylem water potential (pressure chamber); Ψs: Osmotic potential of xylem sap; Ψm: Matric potential of soil water; RWC: Relative water content.     

Xylem pressure potential and chlorophyll fluorescence as indicators of freezing survival in black locust and Western hemlock seedlings

Xylem pressure potential was determined using the Scholander pressure chamber on stems of cold hardened and non-hardened black locust (Robinia pseudoacacia L.) seedlings following freezing to various nonlethal and lethal temperatures and subsequent thawing. Correlation was found between immediate xylem pressure potential and long-term seedling survival. Chlorophyll fluorescence transients were monitored using needles of western hemlock (Tsuga heterophylla (Raf.) Sarg.) seedlings following freezing to various non-lethal and lethal temperatures and subsequent thawing. Immediate and repeatable differences in fluorescence transients correlated with long-term seedling survival. Methodology is described and correlations discussed relative to using either chlorophyll fluorescence or xylem pressure potential as an immediate indicator of long-term freezing survival in woody plant seedlings.     

Hydraulic efficiency and safety of branch xylem increases with height in Sequoia sempervirens (D. Don) crowns

The hydraulic limitation hypothesis of Ryan & Yoder (1997, Bioscience 47, 235-242) suggests that water supply to leaves becomes increasingly difficult with increasing tree height. Within the bounds of this hypothesis, we conjectured that the vertical hydrostatic gradient which gravity generates on the water column in tall trees would cause a progressive increase in xylem 'safety' (increased resistance to embolism and implosion) and a concomitant decrease in xylem 'efficiency' (decreased hydraulic conductivity). We based this idea on the historically recognized concept of a safety-efficiency trade-off in xylem function, and tested it by measuring xylem conductivity and vulnerability to embolism of Sequoia sempervirens branches collected at a range of heights. Measurements of resistance of branch xylem to embolism did indeed show an increase in 'safety' with height. However, the expected decrease in xylem 'efficiency' was not observed. Instead, sapwood-specific hydraulic conductivities (Ks) of branches increased slightly, while leaf-specific hydraulic conductivities increased dramatically, with height. The latter could be largely explained by strong vertical gradients in specific leaf area. The increase in Ks with height corresponded to a decrease in xylem wall fraction (a measure of wall thickness), an increase in percentage of earlywood and slight increases in conduit diameter. These changes are probably adaptive responses to the increased transport requirements of leaves growing in the upper canopy where evaporative demand is greater. The lack of a safety-efficiency tradeoff may be explained by opposing height trends in the pit aperture and conduit diameter of tracheids and the major and semi-independent roles these play in determining xylem safety and efficiency, respectively.     

Foliar water supply of tall trees: evidence for mucilage-facilitated moisture uptake from the atmosphere and the impact on pressure bomb measurements

The water supply to leaves of 25 to 60 m tall trees (including high-salinity-tolerant ones) was studied. The filling status of the xylem vessels was determined by xylem sap extraction (using jet-discharge, gravity-discharge, and centrifugation) and by (1)H nuclear magnetic resonance imaging of wood pieces. Simultaneously, pressure bomb experiments were performed along the entire trunk of the trees up to a height of 57 m. Clear-cut evidence was found that the balancing pressure (P(b)) values of leafy twigs were dictated by the ambient relative humidity rather than by height. Refilling of xylem vessels of apical leaves (branches) obviously mainly occurred via moisture uptake from the atmosphere. These findings could be traced back to the hydration and rehydration of mucilage layers on the leaf surfaces and/or of epistomatal mucilage plugs. Xylem vessels also contained mucilage. Mucilage formation was apparently enforced by water stress. The observed mucilage-based foliar water uptake and humidity dependency of the P(b) values are at variance with the cohesion-tension theory and with the hypothesis that P(b) measurements yield information about the relationships between xylem pressure gradients and height.     

Quantifying Apoplastic Flux through Red Pine Root Systems Using Trisodium, 3-hydroxy-5,8,10-pyrenetrisulfonate

The fluorescent compound trisodium, 3-hydroxy-5,8,10-pyrenetrisulfonate (PTS) was used to quantify the apoplastic flux through red pine (Pinus resinosa Ait.) root systems—that portion of the total water flux reaching the xylem without ever crossing a semipermeable membrane. Flow was induced by pressure through detopped root systems, and by transpiration through intact seedlings. Apoplastic flux was determined by multiplying total flux by the ratio of PTS concentration in the xylem exudate to PTS concentration in the bathing medium.

Under aeration, apoplastic flux was less than 1% of total flux. Under anaerobic conditions, up to 50% of total flux was apoplastic suggesting that anaerobic conditions change the pathway of water flow into root xylem. The change under anaerobic conditions was reversible. Detopped root systems under pressure and intact seedlings under transpiration gave similar results. In detopped root systems, the magnitude of the pressure gradient may alter the apoplastic contribution to total flux.

     

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

The cut ends of excised Zea mays roots were sealed to a pressure transducer and their root pressures recorded. These rose approximately hyperbolically to a maximum value of 4.21 ± 0.34 bar after 30 to 40 minutes. Xylem exudate could not be collected at this pressure since the flow rate was zero. Samples of exudate were collected at lower applied pressures (ΔP), however, and Δπ, the osmotic pressure difference between them and the solution bathing the root, was measured by freezing point depression. A plot of ΔP/Δπ against J_v/Δπ, where J_v is the volume flux, proved to be a straight line whose intercept, equal to σ, the reflection coefficient, was 0.853 ± 0.016. The maximum xylem concentrations of various chemical species were found by a similar extrapolative method and compared with those in the cell sap. This indicated that (a) Ca²⁺, Mg²⁺, NO₃²⁻, SO₄²⁻, and most amino acids move from the cells to the xylem down an electrochemical potential gradient; (b) relative to these ions H⁺, NH₄⁺, glutamine and asparagine are actively transported into the xylem; and (c) H₂PO₄⁻, and K⁺ are actively retained in the symplasm.