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

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.

Efflux and assimilation of xylem-transported CO2 in stems and leaves of tree species with different wood anatomy.

Determining the fate of CO2 respired in woody tissues is necessary to understand plant respiratory physiology and to evaluate CO2 recycling mechanisms. An aqueous 13 C-enriched CO2 solution was infused into the stem of 3-4 m tall trees to estimate efflux and assimilation of xylem-transported CO2 via cavity ring-down laser spectroscopy and isotope ratio mass spectrometry, respectively. Different tree locations (lower stem, upper stem and leafy shoots) and tissues (xylem, bark and leaves) were monitored in species with tracheid, diffuse- and ring-porous wood anatomy (cedar, maple and oak, respectively). Radial xylem CO2 diffusivity and xylem [CO2 ] were lower in cedar relative to maple and oak trees, thereby limiting label diffusion. Part of the labeled 13 CO2 was assimilated in cedar (8.7%) and oak (20.6%) trees, mostly in xylem and bark tissues of the stem, while limited solution uptake in maple trees hindered the detection of label assimilation. Little label reached foliar tissues, suggesting substantial label loss along the stem-branch transition following reductions in the radial diffusive pathway. Differences in respiration rates and radial xylem CO2 diffusivity (lower in conifer relative to angiosperm species) might reconcile discrepancies in efflux and assimilation of xylem-transported CO2 so far observed between taxonomic clades.

Leaf and tree responses of young European aspen trees to elevated atmospheric CO2 concentration vary over the season.

Elevated atmospheric CO2 concentration (eCO2) commonly stimulates net leaf assimilation, decreases stomatal conductance and has no clear effect on leaf respiration. However, effects of eCO2 on whole-tree functioning and its seasonal dynamics remain far more uncertain. To evaluate temporal and spatial variability in eCO2 effects, 1-year-old European aspen trees were grown in two treatment chambers under ambient (aCO2, 400 p.p.m.) and elevated (eCO2, 700 p.p.m.) CO2 concentrations during an early (spring 2019) and late (autumn 2018) seasonal experiment. Leaf (net carbon assimilation, stomatal conductance and leaf respiration) and whole-tree (stem growth, sap flow and stem CO2 efflux) responses to eCO2 were measured. Under eCO2, carbon assimilation was stimulated during the early (1.63-fold) and late (1.26-fold) seasonal experiments. Stimulation of carbon assimilation changed over time with largest increases observed in spring when stem volumetric growth was highest, followed by late season down-regulation, when stem volumetric growth ceased. The neutral eCO2 effect on stomatal conductance and leaf respiration measured at leaf level paralleled the unresponsive canopy conductance (derived from sap flow measurements) and stem CO2 efflux measured at tree level. Our results highlight that seasonality in carbon demand for tree growth substantially affects the magnitude of the response to eCO2 at both leaf and whole-tree level.

Temporal variability in tree responses to elevated atmospheric CO2.

At leaf level, elevated atmospheric CO2 concentration (eCO2 ) results in stimulation of carbon net assimilation and reduction of stomatal conductance. However, a comprehensive understanding of the impact of eCO2 at larger temporal (seasonal and annual) and spatial (from leaf to whole-tree) scales is still lacking. Here, we review overall trends, magnitude and drivers of dynamic tree responses to eCO2 , including carbon and water relations at the leaf and the whole-tree level. Spring and early season leaf responses are most susceptible to eCO2 and are followed by a down-regulation towards the onset of autumn. At the whole-tree level, CO2 fertilization causes consistent biomass increments in young seedlings only, whereas mature trees show a variable response. Elevated CO2 -induced reductions in leaf stomatal conductance do not systematically translate into limitation of whole-tree transpiration due to the unpredictable response of canopy area. Reduction in the end-of-season carbon sink demand and water-limiting strategies are considered the main drivers of seasonal tree responses to eCO2 . These large temporal and spatial variabilities in tree responses to eCO2 highlight the risk of predicting tree behavior to eCO2 based on single leaf-level point measurements as they only reveal snapshots of the dynamic responses to eCO2 .

Woody tissue photosynthesis increases radial stem growth of young poplar trees under ambient atmospheric CO2 but its contribution ceases under elevated CO2.

Woody tissue photosynthesis (Pwt) contributes to the tree carbon (C) budget and generally stimulates radial stem growth under ambient atmospheric CO2 concentration (aCO2). Moreover, Pwt has potential to enhance tree survival under changing climates by delaying negative effects of drought stress on tree hydraulic functioning. However, the relevance of Pwt on tree performance under elevated atmospheric CO2 concentration (eCO2) remains unexplored. To fill this knowledge gap, 1-year-old Populus tremula L. seedlings were grown in two treatment chambers at aCO2 and eCO2 (400 and 660 ppm, respectively), and woody tissues of half of the seedlings in each treatment chamber were light-excluded to prevent Pwt. Radial stem growth, sap flow, leaf photosynthesis and stomatal and canopy conductance were measured throughout the growing season, and the concentration of non-structural carbohydrates (NSC) in stem tissues was determined at the end of the experiment. Fuelled by eCO2, an increase in stem growth of 18 and 50% was observed in control and light-excluded trees, respectively. Woody tissue photosynthesis increased radial stem growth by 39% under aCO2, while, surprisingly, no impact of Pwt on stem growth was observed under eCO2. By the end of the growing season, eCO2 and Pwt had little effect on stem growth, leaf photosynthesis acclimated to eCO2, but stomatal conductance did not, and homeostatic stem NSC pools were observed among combined treatments. Our results highlight that eCO2 potentially fulfils plant C requirements, limiting the contribution of Pwt to stem growth as atmospheric [CO2] rises, and that radial stem growth in young developing trees was C (source) limited during early phenological stages but transitioned towards sink-driven control at the end of the growing season.

Woody tissue photosynthesis delays drought stress in Populus tremula trees and maintains starch reserves in branch xylem tissues.

Photosynthesis in woody tissues (Pwt ) is less sensitive to water shortage than in leaves, hence, Pwt might be a crucial carbon source to alleviate drought stress. To evaluate the impact of Pwt on tree drought tolerance, woody tissues of 4-m-tall drought-stressed Populus tremula trees were subjected to a light-exclusion treatment across the entire plant to inhibit Pwt . Xylem water potential (Ψxylem ), sap flow ( FH2O ), leaf net photosynthesis (Pn,l ), stem diameter variations (ΔD), in vivo acoustic emissions in stems (AEs) and nonstructural carbohydrate concentrations ([NSC]) were monitored to comprehensively assess water and carbon relations at whole-tree level. Under well-watered conditions, Pwt kept Ψxylem at a higher level, lowered FH2O and had no effect on [NSC]. Under drought, Ψxylem , FH2O and Pn,l in light-excluded trees rapidly decreased in concert with reductions in branch xylem starch concentration. Moreover, sub-daily patterns of ΔD, FH2O and AEs were strongly related, suggesting that in vivo AEs may inform not only about embolism events, but also about capacitive release and replenishment of stem water pools. Results highlight the importance of Pwt in maintaining xylem hydraulic integrity under drought conditions and in sustaining NSC pools to potentially limit increases in xylem tension.

Woody tissue photosynthesis reduces stem CO2 efflux by half and remains unaffected by drought stress in young Populus tremula trees.

A substantial portion of locally respired CO2 in stems can be assimilated by chloroplast-containing tissues. Woody tissue photosynthesis (Pwt ) therefore plays a major role in the stem carbon balance. To study the impact of Pwt on stem carbon cycling along a gradient of water availability, stem CO2 efflux (EA ), xylem CO2 concentration ([CO2 ]), and xylem water potential (Ψxylem ) were measured in 4-year-old Populus tremula L. trees exposed to drought stress and different regimes of light exclusion of woody tissues. Under well-watered conditions, local Pwt decreased EA up to 30%. Axial CO2 diffusion (Dax ) induced by distant Pwt caused an additional decrease in EA of up to 25% and limited xylem [CO2 ] build-up. Under drought stress, absolute decreases in EA driven by Pwt remained stable, denoting that Pwt was not affected by drought. At the end of the dry period, when transpiration was low, local Pwt and Dax offset 20% and 10% of stem respiration on a daily basis, respectively. These results highlight (a) the importance of Pwt for an adequate interpretation of EA measurements and (b) homeostatic Pwt along a drought stress gradient, which might play a crucial role to fuel stem metabolism when leaf carbon uptake and phloem transport are limited.

Sugars from woody tissue photosynthesis reduce xylem vulnerability to cavitation.

Reassimilation of internal CO2 via woody tissue photosynthesis has a substantial effect on tree carbon income and wood production. However, little is known about its role in xylem vulnerability to cavitation and its implications in drought-driven tree mortality. Young trees of Populus nigra were subjected to light exclusion at the branch and stem levels. After 40 d, measurements of xylem water potential, diameter variation and acoustic emission (AE) were performed in detached branches to obtain acoustic vulnerability curves to cavitation following bench-top dehydration. Acoustic vulnerability curves and derived AE50 values (i.e. water potential at which 50% of cavitation-related acoustic emissions occur) differed significantly between light-excluded and control branches (AE50,light-excluded  = -1.00 ± 0.13 MPa; AE50,control  = -1.45 ± 0.09 MPa; P = 0.007) denoting higher vulnerability to cavitation in light-excluded trees. Woody tissue photosynthesis represents an alternative and immediate source of nonstructural carbohydrates (NSC) that confers lower xylem vulnerability to cavitation via sugar-mediated mechanisms. Embolism repair and xylem structural changes could not explain this observation as the amount of cumulative AE and basic wood density did not differ between treatments. We suggest that woody tissue assimilates might play a role in the synthesis of xylem surfactants for nanobubble stabilization under tension.