The correlations and sequence of plant stomatal, hydraulic, and wilting responses to drought

Abstract

Climate change is expected to exacerbate drought for many plants, making drought tolerance a key driver of species and ecosystem responses. Plant drought tolerance is determined by multiple traits, but the relationships among traits, either within individual plants or across species, have not been evaluated for general patterns across plant diversity. We synthesized the published data for stomatal closure, wilting, declines in hydraulic conductivity in the leaves, stems, and roots, and plant mortality for 262 woody angiosperm and 48 gymnosperm species. We evaluated the correlations among the drought tolerance traits across species, and the general sequence of water potential thresholds for these traits within individual plants. The trait correlations across species provide a framework for predicting plant responses to a wide range of water stress from one or two sampled traits, increasing the ability to rapidly characterize drought tolerance across diverse species. Analyzing these correlations also identified correlations among the leaf and stem hydraulic traits and the wilting point, or turgor loss point, beyond those expected from shared ancestry or independent associations with water stress alone. Further, on average, the angiosperm species generally exhibited a sequence of drought tolerance traits that is expected to limit severe tissue damage during drought, such as wilting and substantial stem embolism. This synthesis of the relationships among the drought tolerance traits provides crucial, empirically supported insight into representing variation in multiple traits in models of plant and ecosystem responses to drought.

Keywords: drought tolerance; leaf hydraulics; stem hydraulics; stomatal closure; turgor loss point.

Fig. 1.

Correlations among drought tolerance traits across species. Symbols follow Table 1. Blue points represent angiosperms, and black points represent gymnosperms. Solid black lines are standard major axis relationships that are significant across all species. Dashed lines are correlations that are significantly different between the gymnosperms (black lines) and angiosperms (blue lines). All significant correlations remained significant after correcting for multiple tests (46). The r values are shown on each graph, and P values and sample sizes are in SI Appendix, Table S2. All of the traits were significantly correlated (A–F and I–L), except for K_leaf Ψ₅₀ and g_S Ψ₅₀ (G) and g_S Ψ₉₅ (H). For graphical clarity, correlations with K_stem Ψ₁₂ and Ψ₈₈ are not shown. All of the stem hydraulic traits showed the same correlations, except that K_stem Ψ₁₂ was not significantly correlated with g_S Ψ₅₀ and K_leaf Ψ₅₀ was not significantly correlated with K_stem Ψ₈₈ (SI Appendix, Table S2). K_stem Ψ₁₂ was significantly correlated with K_leaf Ψ₅₀ in the gymnosperms but not the angiosperms, whereas the two functional types showed significantly different slopes for the correlations of K_stem Ψ₅₀ with π_tlp (D) and with K_stem Ψ₁₂ (SI Appendix, Table S4). We did not compile variation in plant Ψ_lethal from the literature, because most published studies use different definitions for plant death, but instead show this correlation from the largest study of these traits (11) for comparison with the other correlations with π_tlp (F).

Fig. 2.

Testing hypotheses for the drivers of the correlations among the drought tolerance traits. Most of the trait correlations are predicted to be driven by concerted convergence, wherein the selective pressure of water stress (Ψ_{min, MD} or Ψ_{min, PD}) acts independently on each trait to optimize overall plant function during drought (10, 17, 28). These hypotheses are indicated with dashed lines. Additionally, π_tlp was hypothesized to influence K_leaf Ψ₅₀ mechanistically (20). K_leaf Ψ₅₀, in turn, would influence g_S Ψ₅₀ and Ψ₉₅ and the threshold Ψ_leaf for leaf death (leaf Ψ_lethal) (30, 31), and the stem and root hydraulic traits would influence the plant mortality threshold (plant Ψ_lethal) (19). These hypotheses are indicated with solid lines. As predicted, π_tlp and K_leaf Ψ₅₀ were more correlated than expected from water stress and relatedness alone. Functionally coordinated traits are indicated with blue lines. Other correlations were best explained by the independent relationship of each trait with water stress. Concerted convergence is indicated with black lines. Conversely, K_stem Ψ₅₀ was also more strongly correlated with K_leaf Ψ₅₀ and, when characterizing water stress with Ψ_{min, MD,} with π_tlp than expected from concerted convergence, consistent with strong functional coordination within the hydraulic system across organs (SI Appendix, Tables S5 and S6). The remaining hypotheses had insufficient data to test (indicated with gray lines).

Fig. 3.

The hypothesized (A) and observed (B) sequence of water potential values for the drought tolerance traits within individual plants. A shows the relationship between organ water potential (Ψ_W) and the percent decline in stomatal conductance (g_S, blue), hydraulic conductivity in the leaves, roots and stems (K_leaf and K_root, purple; K_stem, red), and turgor pressure (Ψ_P, yellow). The numbered circles show the order in which given declines in function will occur if plants generally follow a trait sequence that is expected to limit tissue damage during drought. In this sequence, 50% declines in stomatal conductance (g_S Ψ₅₀, #1) are expected to occur at the least negative water potentials to slow transpiration (37), followed by moderate (50%) declines in K_leaf and K_root (K_leaf and K_root Ψ₅₀) and minor (12%) declines in K_stem (K_stem Ψ₁₂), if leaf and root dysfunction protects the stem from embolism, as predicted by vulnerability segmentation (17). (These traits are labeled #2–4 but shown in the same position, because their order is not hypothesized). Stomatal closure, or g_S Ψ₉₅ (#5), would occur before potentially major damage, including loss of turgor pressure in the leaf cells, or wilting (π_tlp, #6), and 50% declines in K_stem (K_stem Ψ₅₀, #7) (6, 10). K_stem Ψ₅₀ is hypothesized to limit the water stress that plants tolerate, and thus, we expected the most negative Ψ_leaf values plants reach under natural growing conditions (Ψ_{min, MD}, #8) to be near K_stem Ψ₅₀ (4). Eighty-eight percent declines in K_stem (K_stem Ψ₈₈, #9) have been hypothesized to induce irreversible xylem damage and, thus, to occur somewhat before plant death (plant Ψ_lethal, #10) (19), which we estimated as the Ψ_leaf at which all leaves showed tissue damage (11). The sequence is determined from pairwise comparisons between all of the traits (SI Appendix, Table S7), but, for clarity, B shows the mean of each trait from its pairwise comparison with the trait immediately after (i.e., more negative than) it in the sequence. The traits generally followed this sequence, with the order of K_stem Ψ₁₂ > K_leaf Ψ₅₀ & Ψ_{min, MD} > π_tlp > K_stem Ψ₅₀ > K_stem Ψ₈₈ supporting the hypothesized sequence, with the exception that K_leaf Ψ₅₀ and Ψ_{min, MD} were not significantly different. π_tlp occurred after g_S Ψ₅₀, as hypothesized, but before g_S Ψ₉₅, contrary to prediction. There were insufficient data to test K_root Ψ₅₀, or to compare the stomatal traits to any other trait. For each trait, the number to the left is the number of other traits it was significantly different from, and the number to the right is the total number of trait comparisons with sufficient data to test. Notably, the sequence is shown with respect to organ-specific water potentials; in the transpiring plant, the high resistance of the hydraulic pathway produces a gradient of increasingly negative water potentials from the root to the leaf. Thus, the stem may undergo less embolism than suggested by this sequence.