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1. Anatomical adjustments of the tree hydraulic pathway decrease canopy conductance under long-term elevated CO2

   https://doi.org/10.1093/plphys/kiac482  

   Gattmann, Marielle ; McAdam, Scott A ; Birami, Benjamin ; Link, Roman ; Nadal-Sala, Daniel ; Schuldt, Bernhard ; Yakir, Dan ; Ruehr, Nadine K ( October 2022 , Plant Physiology)

   The cause of reduced leaf-level transpiration under elevated CO2 remains largely elusive. Here, we assessed stomatal, hydraulic, and morphological adjustments in a long-term experiment on Aleppo pine (Pinus halepensis) seedlings germinated and grown for 22–40 months under elevated (eCO2; c. 860 ppm) or ambient (aCO2; c. 410 ppm) CO2. We assessed if eCO2-triggered reductions in canopy conductance (gc) alter the response to soil or atmospheric drought and are reversible or lasting due to anatomical adjustments by exposing eCO2 seedlings to decreasing [CO2]. To quantify underlying mechanisms, we analyzed leaf abscisic acid (ABA) level, stomatal and leaf morphology, xylem structure, hydraulic efficiency, and hydraulic safety. Effects of eCO2 manifested in a strong reduction in leaf-level gc (−55%) not caused by ABA and not reversible under low CO2 (c. 200 ppm). Stomatal development and size were unchanged, while stomatal density increased (+18%). An increased vein-to-epidermis distance (+65%) suggested a larger leaf resistance to water flow. This was supported by anatomical adjustments of branch xylem having smaller conduits (−8%) and lower conduit lumen fraction (−11%), which resulted in a lower specific conductivity (−19%) and leaf-specific conductivity (−34%). These adaptations to CO2 did not change stomatal sensitivity to soil or atmospheric drought, consistent with similar xylem safety thresholds. In summary, we found reductions of gc under elevated CO2 to be reflected in anatomical adjustments and decreases in hydraulic conductivity. As these water savings were largely annulled by increases in leaf biomass, we do not expect alleviation of drought stress in a high CO2 atmosphere.

    

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2. Altered cell wall hydroxycinnamate composition impacts leaf- and canopy-level CO2 uptake and water use in rice

   https://doi.org/10.1093/plphys/kiad428  

   Pathare, Varsha S. ; Panahabadi, Rahele ; Sonawane, Balasaheb V. ; Apalla, Anthony Jude ; Koteyeva, Nuria ; Bartley, Laura E. ; Cousins, Asaph B. ( July 2023 , Plant Physiology)

   Cell wall properties play a major role in determining photosynthetic carbon uptake and water use through their impact on mesophyll conductance (CO2 diffusion from substomatal cavities into photosynthetic mesophyll cells) and leaf hydraulic conductance (water movement from xylem, through leaf tissue, to stomata). Consequently, modification of cell wall (CW) properties might help improve photosynthesis and crop water use efficiency (WUE). We tested this using 2 independent transgenic rice (Oryza sativa) lines overexpressing the rice OsAT10 gene (encoding a “BAHD” CoA acyltransferase), which alters CW hydroxycinnamic acid content (more para-coumaric acid and less ferulic acid). Plants were grown under high and low water levels, and traits related to leaf anatomy, CW composition, gas exchange, hydraulics, plant biomass, and canopy-level water use were measured. Alteration of hydroxycinnamic acid content led to statistically significant decreases in mesophyll CW thickness (−14%) and increased mesophyll conductance (+120%) and photosynthesis (+22%). However, concomitant increases in stomatal conductance negated the increased photosynthesis, resulting in no change in intrinsic WUE (ratio of photosynthesis to stomatal conductance). Leaf hydraulic conductance was also unchanged; however, transgenic plants showed small but statistically significant increases in aboveground biomass (AGB) (+12.5%) and canopy-level WUE (+8.8%; ratio of AGB to water used) and performed better under low water levels than wild-type plants. Our results demonstrate that changes in CW composition, specifically hydroxycinnamic acid content, can increase mesophyll conductance and photosynthesis in C3 cereal crops such as rice. However, attempts to improve photosynthetic WUE will need to enhance mesophyll conductance and photosynthesis while maintaining or decreasing stomatal conductance.

    

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3. Stomatal behaviour and stem xylem traits are coordinated for woody plant species under exceptional drought conditions

   https://doi.org/10.1111/pce.13367  

   Pivovaroff, Alexandria L. ; Cook, Victoria M. W. ; Santiago, Louis S. ( August 2018 , Plant, Cell & Environment)

   Isohydry (maintenance of plant water potential at the cost of carbon gain) and anisohydry (gas exchange maintenance at the cost of declining plant water status) make up two ends of a stomatal drought response strategy continuum. However, few studies have merged measures of stomatal regulation with xylem hydraulic safety strategies based on in situ field measurements. The goal of this study was to characterize the stomatal and xylem hydraulic safety strategies of woody species in the biodiverse Mediterranean‐type ecosystem region of California. Measurements were conducted in situ when California was experiencing the most severe drought conditions in the past 1,200 years. We found coordination among stomatal, hydraulic, and standard leaf functional traits. For example, stem xylem vulnerability to cavitation (P₅₀) was correlated with the water potential at stomatal closure (P_close); more resistant species had a more negative water potential at stomatal closure. The degree of isohydry–anisohydry, defined at P_close–P₅₀, was correlated with the hydraulic safety margin across species; more isohydric species had a larger hydraulic safety margin. In addition, we report for the first time P_closevalues below −10 MPa. Measuring these traits in a biodiverse region under exceptional drought conditions contributes to our understanding of plant drought responses.

    

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4. Hydraulic traits that buffer deep‐rooted plants from changes in hydrology and climate

   https://doi.org/10.1002/hyp.13587  

   Hultine, Kevin R. ; Froend, Ray ; Blasini, Davis ; Bush, Susan E. ; Karlinski, Melissa ; Koepke, Dan F. ( November 2019 , Hydrological Processes)

   Groundwater‐dependent ecosystems are often defined by the presence of deeply rooted phreatophytic plants. When connected to groundwater, phreatophytes in arid regions decouple ecosystem net primary productivity from precipitation, underscoring a disproportionately high biodiversity and exchange of resources relative to surrounding areas. However, groundwater‐dependent ecosystems are widely threatened due to the effects of water diversions, groundwater abstraction, and higher frequencies of episodic drought and heat waves. The resilience of these ecosystems to shifting ecohydrological–climatological conditions will depend largely on the capacity of dominant, phreatophytic plants to cope with dramatic reductions in water availability and increases in atmospheric water demand. This paper disentangles the broad range of hydraulic traits expressed by phreatophytic vegetation to better understand their capacity to survive or even thrive under shifting ecohydrological conditions. We focus on three elements of plant water relations: (a) hydraulic architecture (including root area to leaf area ratios and rooting depth), (b) xylem structure and function, and (c) stomatal regulation. We place the expression of these traits across a continuum of phreatophytic habits from obligate to semi‐obligate to semi‐facultative to facultative. Although many species occupy multiple phreatophytic niches depending on access to groundwater, we anticipate that populations are largely locally adapted to a narrow range of ecohydrological conditions regardless of gene flow across ecohydrological gradients. Consequently, we hypothesize that reductions in available groundwater and increases in atmospheric water demand will result in either (a) stand replacement of obligate phreatophytic species with more facultative species as a function of widespread mortality in highly groundwater‐dependent populations or (b) directional selection in semi‐obligate and semi‐facultative phreatophytes towards the expression of traits associated with highly facultative phreatophytes in the absence of species replacement. Anticipated shifts in the expression of hydraulic traits may have profound impacts on water cycling processes, species assemblages, and habitat structure of groundwater‐dependent woodlands and riparian forests.

    

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5. Optimal stomatal drought response shaped by competition for water and hydraulic risk can explain plant trait covariation

   https://doi.org/10.1111/nph.16207  

   Lu, Yaojie ; Duursma, Remko A. ; Farrior, Caroline E. ; Medlyn, Belinda E. ; Feng, Xue ( October 2019 , New Phytologist)

   The classical theory of stomatal optimization stipulates that stomata should act to maximize photosynthesis while minimizing transpiration. This theory, despite its remarkable success in reproducing empirical patterns, does not account for the fact that the available water to plants is dynamically regulated by plants themselves, and that plants compete for water in most locations.

   Here, we develop an alternative theory in which plants maximize the expected carbon gain under stochastic rainfall in a competitive environment. We further incorporate xylem hydraulic limitation as an additional constraint to transpiration and evaluate its impacts on stomatal optimization by incorporating the direct carbon cost of xylem recovery and the opportunity cost of reduced future photosynthesis as a result of irrecoverable xylem damage.

   We predict stomatal behaviour to be more conservative with a higher cost induced by xylem damage. By varying the unit carbon cost and extent of xylem recovery, characterizing the direct and opportunity cost of xylem damage, respectively, our model can reproduce several key patterns of stomatal‐hydraulic trait covariations.

   By addressing the key elements of water limitation in plant gas exchange simultaneously, including plants’ self‐regulation of water availability, competition for water and hydraulic risk, our study provides a comprehensive theoretical basis for understanding stomatal behaviour.

    

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