Limited plasticity of anatomical and hydraulic traits in aspen trees under elevated CO2 and seasonal drought

Abstract

The timing of abiotic stress elicitors on wood formation largely affects xylem traits that determine xylem efficiency and vulnerability. Nonetheless, seasonal variability of elevated CO2 (eCO2) effects on tree functioning under drought remains largely unknown. To address this knowledge gap, 1-year-old aspen (Populus tremula L.) trees were grown under ambient (±445 ppm) and elevated (±700 ppm) CO2 and exposed to an early (spring/summer 2019) or late (summer/autumn 2018) season drought event. Stomatal conductance and stem shrinkage were monitored in vivo as xylem water potential decreased. Additional trees were harvested for characterization of wood anatomical traits and to determine vulnerability and desorption curves via bench dehydration. The abundance of narrow vessels decreased under eCO2 only during the early season. At this time, xylem vulnerability to embolism formation and hydraulic capacitance during severe drought increased under eCO2. Contrastingly, stomatal closure was delayed during the late season, while hydraulic vulnerability and capacitance remained unaffected under eCO2. Independently of the CO2 treatment, elastic, and inelastic water pools depleted simultaneously after 50% of complete stomatal closure. Our results suggest that the effect of eCO2 on drought physiology and wood traits are small and variable during the growing season and question a sequential capacitive water release from elastic and inelastic pools as drought proceeds.

Figure 1

Effect of CO₂ enrichment and seasonal drought on wood anatomical traits. A, Transverse stem sections of studied aspen trees and (B) relative (bar plot) and cumulative (line plot) abundancy of vessels classified by four size classes (N_{v_class}, upper panels) and their relative contribution to overall hydraulic conductance (k_{h_class}, lower panels) during the early (ESE—2019) and the late (LSE—2018) season experiment. Trees were subjected to different levels of atmospheric [CO₂] (ambient [aCO₂] and elevated [eCO₂]). Scale bars correspond with 1 mm. Lignified and non-lignified cell walls are colored red and blue, respectively, with distinction of cambium (Ca), periderm (Pe), phloem (Ph), pith (Pi), and xylem (Xy) from the first year (Y1) and the second year (Y2). Bar plot and error bars indicate the mean and standard error, respectively. Letters indicate differences in N_{v_class} and k_{h_class} contributions within each [CO₂] treatment and seasonal experiment (Wilcoxon test, P < 0.05). Difference between aCO₂ and eCO₂ (n = 4 for ESE and LSE) within each diameter class are also indicated (linear model, •P < 0.1).

Figure 2

Effect of CO₂ enrichment on hydraulic vulnerability and capacitance during the early and late season. Acoustic vulnerability curves (VC_AE, upper panels) and DCs (lower panels) during early (ESE—2019) and late (LSE—2018) season bench dehydration experiments. Trees were subjected to different levels of atmospheric [CO₂] (ambient [aCO₂] and elevated [eCO₂]). Xylem water potential (Ψ_xylem) at which 12%, 50%, and 88% of the embolism-related AE occur (AE₁₂ [●], AE₅₀ [▲], AE₈₈ [∎], respectively) are shown (upper panels; n = 4 for ESE and LSE). Blue and red lines on the DCs display the Ψ_xylem range of elastic and inelastic water release, respectively. Corresponding hydraulic capacitances (elastic and inelastic) are calculated as the slope of the linear relationship between VWC and Ψ_xylem (n = 3 and 4 for ESE and LSE, respectively, under aCO₂, and n = 4 for ESE and LSE under eCO₂). Shaded areas indicate the standard error of each curve.

Figure 3

Effect of CO₂ enrichment and seasonal drought on stomatal conductance. Stomatal conductance (g_s) over time (left-hand side panels) and relative g_s loss with decreasing xylem water potential (Ψ_Xylem; right-hand side panels) during the early (ESE—2019) and late (LSE—2019) season in vivo drought experiment. Trees were subjected to combined treatments of atmospheric [CO₂] (ambient [a] and elevated [e]) and drought stress (well-watered [W] and drought-stressed [D]). Points and shaded areas denote average and standard error in left-hand side panels. Thin red lines show the sigmoidal relation between relative g_s loss and Ψ_xylem for individual trees. Dashed and solid lines illustrate aCO₂ and eCO₂, respectively. Bold lines and shaded areas indicate model fit applying average ± SE parameter for aCO₂ and eCO₂ (n = 4 and 5 for ESE and LSE, respectively). With DOY day of year.

Figure 4

Effect of CO₂ enrichment and seasonal drought on stem diameter variations. Stem diameter (D) over time (left-hand side panels) and relative increase of TWD with decreasing xylem water potential (Ψ_xylem; right-hand side panels) during the early (ESE—2019) and the late (LSE—2018) season in vivo drought experiment. Trees were subjected to combined treatments of atmospheric CO₂ (ambient [a] and elevated [e]) and drought stress (well-watered [W] and drought-stressed [D]). Discrete Ψ_xylem measurements were linearly regressed over time to match temporal resolution (on a daily basis) of TWD and Ψ_xylem (average R² = 0.71 ± 0.04). Error bars indicate the standard error of the mean stem diameter size per [CO₂] treatment at the onset of the drought event and the shaded areas the standard error in the variation of stem diameter. Black lines show the preceding maximum stem diameter of the drought-stressed trees as reference to estimate TWD. Thin red lines show sigmoidal relation between TWD and Ψ_xylem for individual drought-stressed trees. Dashed and solid lines illustrate aCO₂ and eCO₂, respectively. Bold lines and shaded areas indicate model fit applying average and standard error parameter values for aCO₂ (n = 3 for ESE and LSE) and eCO₂ (n = 4 and 5 for ESE and LSE, respectively). With DOY day of year.

Figure 5

Relative variation of the stomatal conductance (g_s, n = 4 and 5 for ESE and LSE, respectively), TWD (n = 3 for ESE and LSE, respectively, under aCO₂, and n = 4 and 5 for ESE and LSE, respectively, under eCO₂) and embolism-related AEs (n = 4 for ESE and LSE) with decreasing xylem water potential (Ψ_xylem) during the early (ESE—2019) and the late (LSE—2018) season drought experiment (upper panels) and pairwise comparison of their corresponding hydraulic thresholds (lower panels). Trees were subjected to different levels of atmospheric [CO₂] (aCO₂ and eCO₂ for ambient and elevated [CO₂], respectively). Lines and shades areas show model fit applying average and standard error parameter values under aCO₂ (dashed lines) and eCO₂ (solid lines). Boxplots show hydraulic thresholds corresponding with 12%, 50%, and 88% loss of each of the variables for aCO₂ (light colored) and eCO₂ (dark colored). Center line, box limits, whiskers, and points in the boxplot denote median, upper and lower quartiles, 1.5 × interquartile range, and outliers, respectively. Letters indicate difference between variables (linear mixed effect model, P < 0.05, pooling aCO₂ and eCO₂ data). Differences between [CO₂] treatments for each threshold are also indicated (linear model, •P < 0.1, *P < 0.05).