Hydraulic failure defines the recovery and point of death in water-stressed conifers

Abstract

This study combines existing hydraulic principles with recently developed methods for probing leaf hydraulic function to determine whether xylem physiology can explain the dynamic response of gas exchange both during drought and in the recovery phase after rewatering. Four conifer species from wet and dry forests were exposed to a range of water stresses by withholding water and then rewatering to observe the recovery process. During both phases midday transpiration and leaf water potential (Psileaf) were monitored. Stomatal responses to Psileaf were established for each species and these relationships used to evaluate whether the recovery of gas exchange after drought was limited by postembolism hydraulic repair in leaves. Furthermore, the timing of gas-exchange recovery was used to determine the maximum survivable water stress for each species and this index compared with data for both leaf and stem vulnerability to water-stress-induced dysfunction measured for each species. Recovery of gas exchange after water stress took between 1 and >100 d and during this period all species showed strong 1:1 conformity to a combined hydraulic-stomatal limitation model (r2 = 0.70 across all plants). Gas-exchange recovery time showed two distinct phases, a rapid overnight recovery in plants stressed to <50% loss of leaf hydraulic conductance (Kleaf) and a highly Psileaf-dependent phase in plants stressed to >50% loss of Kleaf. Maximum recoverable water stress (Psimin) corresponded to a 95% loss of Kleaf. Thus, we conclude that xylem hydraulics represents a direct limit to the drought tolerance of these conifer species.

Figure 1.

Examples of diurnal patterns of whole-plant transpiration in a single individual of A. arenarius during several weeks of withholding water. The three plots show data while unstressed (Ψ_leaf = −1.15 MPa; black circles), moderately stressed (Ψ_leaf = −1.65 MPa; triangles), and stressed to >80% stomatal closure (Ψ_leaf = −2.85 MPa; white circles). E_md was measured during the shaded time interval.

Figure 2.

Pooled data (n = 5) showing the response of transpiration (proportional to stomatal conductance under the controlled vapor pressure growth regime) to increasingly negative Ψ_leaf as soil dried during the drought treatment. Regressions are sigmoidal functions in each case, and these regression functions were used to define the stomatal dependence upon Ψ_leaf to evaluate the degree of hydraulic limitation during drought recovery (see Fig. 5A).

Figure 3.

Simultaneous plots of declining K_leaf and increasing percentage loss of K_stem in response to increasingly negative water potential. Leaf data are pooled from three plants exposed to gradually increasing water stress while stem data are means (n = 4) from excised branches exposed to a range of hydraulic tensions induced by centrifuge. Sigmoid functions are fitted to both stem and leaf data and were used to predict 50% and 95% loss of function in stems and leaves.

Figure 4.

An example of recovery from mild (black circles) and severe (white circles) water stress in rewatered plants of L. franklinii. The mildly stressed plant shows a minimal reduction of K_plant and is able to rapidly recover leaf hydration and gas exchange. By contrast the severely stressed plant experiences profound depression of K_plant that recovers slowly, thus limiting gas-exchange recovery, which has a t_1/2 of 6.5 d. Although Ψ_leaf recovers relatively quickly in both plants, it remains limiting during recovery of the severely stressed plant, thus preventing stomatal reopening.

Figure 5.

Modeled and measured recovery data for a C. rhomboidea plant subject to a stress sufficient to reduce K_leaf by approximately 90%. A, According to the hydraulic-stomatal limitation model, in fully hydrated soils E will be equal to the intersection of a hydraulic supply function (defined by K_plant) and the stomatal control function (determined empirically from the regression equations in Fig. 2). B, The observed recovery of whole-plant hydraulic conductivity after rewatering. C, The predicted (white circles, dotted line) recovery of midday E closely matches the observed (black circles, unbroken line) dynamic as the rewatered plant initially rehydrates rapidly to the edge of the stomatal control window (shown as the gray region, representing the Ψ_leaf range responsible for a 20% to 80% reduction in stomatal aperture) then slowly thereafter, thus limiting stomatal conductance and gas exchange. Predicted %E is calculated from entering the measured Ψ_leaf (triangles) into the stomatal control function equation %E = ƒ(Ψ_leaf) shown in A.

Figure 6.

Predicted and observed recovery of E_md (white circles) in all plants after rewatering from all levels of drought. Predicted and observed %E_md are shown simultaneously (black circles) for plants during the droughting phase as well to provide a comparative data set showing stomatal control of gas exchange under limiting soil water content. All plants showed good correlation between observed and predicted %E_md during drought recovery. Only in L. franklinii was there any significant difference in the slopes between recovery and droughting datasets.

Figure 7.

A, The relationship between recovery time (plotted as t_1/2⁻¹) and final Ψ_leaf prior to rewatering in all individuals of A. arenarius (white circles), C. rhomboidea (black circles), D. dacrydioides (black triangles), and L. franklinii (white triangles). Recovery time showed two phases, the first phase was insensitive to Ψ_leaf (1/t_1/2 = 1) and the second highly dependent. Linear regressions fitted through this second phase as t_1/2 fell from 1 (overnight recovery of t_1/2) to 0 (plant death). The x intercept of these regressions was defined as the minimum recoverable water potential (Ψ_min). B, Shows the very highly significant 1:1 relationships between Ψ_min derived from A and 50% loss of K_stem (r²= 0.98) and 95% loss of K_leaf (r²=0.94), symbols as in A. Correlation coefficients are for regression lines forced through the origin.

Figure 8.

Examples of measured (white circles) and modeled (lines) recovery trajectory of transpiration in a L. franklinii plants over 20 d following rewatering from drought (−3.5 MPa). Three curves depict three models of stomatal-hydraulic behavior: the hydraulic-stomatal limitation model with a fixed E = f(Ψ_leaf) (bold line); a hydraulic-stomatal limitation model with osmotic adjustment to promote stomatal opening at lower Ψ_leaf (dotted line); and a nonhydraulic limited recovery where stomatal sensitivity to Ψ_leaf is enhanced or nonexistent postdrought, e.g. as might occur if ABA was limiting stomatal aperture (dashed line). The measured recovery response for this individual and all individuals (Fig. 6) was best described by the constant E = f(Ψ_leaf) function.