Stomatal and non-stomatal limitation to photosynthesis in two trembling aspen (Populus tremuloides Michx.) clones exposed to elevated CO2 and/or O3

Leaf gas exchange parameters and the content of ribulose‐1,5‐bisphosphate carboxylase/oxygenase (Rubisco) in the leaves of two 2‐year‐old aspen (Populus tremuloides Michx.) clones (no. 216, ozone tolerant and no. 259, ozone sensitive) were determined to estimate the relative stomatal and mesophyll limitations to photosynthesis and to determine how these limitations were altered by exposure to elevated CO₂ and/or O₃. The plants were exposed either to ambient air (control), elevated CO₂ (560 p.p.m.) elevated O₃ (55 p.p.b.) or a mixture of elevated CO₂ and O₃ in a free air CO₂ enrichment (FACE) facility located near Rhinelander, Wisconsin, USA. Light‐saturated photosynthesis and stomatal conductance were measured in all leaves of the current terminal and of two lateral branches (one from the upper and one from the lower canopy) to detect possible age‐related variation in relative stomatal limitation (leaf age is described as a function of leaf plastochron index). Photosynthesis was increased by elevated CO₂ and decreased by O₃ at both control and elevated CO₂. The relative stomatal limitation to photosynthesis (l_s) was in both clones about 10% under control and elevated O₃. Exposure to elevated CO₂ + O₃ in both clones and to elevated CO₂ in clone 259, decreased l_s even further – to about 5%. The corresponding changes in Rubisco content and the stability of C_i/C_a ratio suggest that the changes in photosynthesis in response to elevated CO₂ and O₃ were primarily triggered by altered mesophyll processes in the two aspen clones of contrasting O₃ tolerance. The changes in stomatal conductance seem to be a secondary response, maintaining stable C_i under the given treatment, that indicates close coupling between stomatal and mesophyll processes.     

Stomatal sensitivity to vapour pressure difference over a subambient to elevated CO2 gradient in a C3/C4 grassland

In the present study the response of stomatal conductance (g_s) to increasing leaf‐to‐air vapour pressure difference (D) in early season C₃ (Bromus japonicus) and late season C₄ (Bothriochloa ischaemum) grasses grown in the field across a range of CO₂ (200–550 µmol mol^?1) was examined. Stomatal sensitivity to D was calculated as the slope of the response of g_s to the natural log of externally manipulated D (dg_s/dlnD). Increasing D and CO₂ significantly reduced g_s in both species. Increasing CO₂ caused a significant decrease in stomatal sensitivity to D in Br. japonicus, but not in Bo. ischaemum. The decrease in stomatal sensitivity to D at high CO₂ for Br. japonicus fit theoretical expectations of a hydraulic model of stomatal regulation, in which g_s varies to maintain constant transpiration and leaf water potential. The weaker stomatal sensitivity to D in Bo. ischaemum suggested that stomatal regulation of leaf water potential was poor in this species, or that non‐hydraulic signals influenced guard cell behaviour. Photosynthesis (A) declined with increasing D in both species, but analyses of the ratio of intercellular to atmospheric CO₂ (C_i/C_a) suggested that stomatal limitation of A occurred only in Br. japonicus. Rising CO₂ had the greatest effect on g_s and A in Br. japonicus at low D. In contrast, the strength of stomatal and photosynthetic responses to CO₂ were not affected by D in Bo. ischaemum. Carbon and water dynamics in this grassland are dominated by a seasonal transition from C₃ to C₄ photosynthesis. Interspecific variation in the response of g_s to D therefore has implications for predicting seasonal ecosystem responses to CO₂.     

Asymmetric responses of adaxial and abaxial stomata to elevated CO2: impacts on the control of gas exchange by leaves

The response of adaxial and abaxial stomatal conductance in Rumex obtusifolius to growth at elevated atmospheric concentrations of CO₂ (250 μmol mol^?1 above ambient) was investigated over two growing seasons. The conductance of both the adaxial and abaxial leaf surfaces was found to be reduced by elevated concentrations of CO₂. Elevated CO₂ caused a much greater reduction in conductance for the adaxial surface than for the abaxial surface. The absence of effects upon stomatal density indicated that the reductions were probably the result of changes in stomatal aperture. Partitioning of gas exchange between the leaf surfaces revealed that increased concentrations of CO₂ caused increased rates of photosynthesis only via the abaxial surface. Additionally, leaf thickness was found to increase during growth at elevated concentrations of CO₂. The tendency for these amphistomatous leaves to develop a distribution of conductance approaching that of hypostomatous leaves clearly reduced their maximum photosynthetic potential. This conclusion was supported by measurements of stomatal limitation, which showed greater values for the adaxial surfaces, and greater values at elevated CO₂. This reduction in photosynthesis may in part be caused by higher diffusive limitations imposed because of increased leaf thickness. In an uncoupled canopy, asymmetrical stomatal responses of the kind identified here may appreciably reduce transpiration. Species which show symmetrical responses are less likely to show reduced transpirational rates, and a redistribution of water loss between species may occur. The implications of asymmetrical stomatal responses for photosynthesis and canopy transpiration are discussed.     

Elevated atmospheric CO2 alters stomatal responses to variable sunlight in a C4 grass

Native tallgrass prairie in NE Kansas was exposed to elevated (twice ambient) or ambient atmospheric CO₂ levels in open-top chambers. Within chambers or in adjacent unchambered plots, the dominant C₄ grass, Andropogon gerardii, was subjected to fluctuations in sunlight similar to that produced by clouds or within canopy shading (full sun > 1500 μmol m⁻² s⁻¹ versus 350 μmol m⁻² s⁻¹ shade) and responses in gas exchange were measured. These field experiments demonstrated that stomatal conductance in A. gerardii achieved new steady state levels more rapidly after abrupt changes in sunlight at elevated CO₂ when compared to plants at ambient CO₂. This was due primarily to the 50% reduction in stomatal conductance at elevated CO₂, but was also a result of more rapid stomatal responses. Time constants describing stomatal responses were significantly reduced (29–33%) at elevated CO₂. As a result, water loss was decreased by as much as 57% (6.5% due to more rapid stomatal responses). Concurrent increases in leaf xylem pressure potential during periods of sunlight variability provided additional evidence that more rapid stomatal responses at elevated CO₂ enhanced plant water status. CO₂-induced alterations in the kinetics of stomatal responses to variable sunlight will likely enhance direct effects of elevated CO₂ on plant water relations in all ecosystems.     

Effects of elevated O3 and CO2 concentrations on photosynthesis and stomatal conductance in Scots pine

Naturally regenerated Scots pines (Pinus sylvestris L.), aged 28–30 years old, were grown in open-top chambers and subjected in situ to three ozone (O₃) regimes, two concentrations of CO₂, and a combination of O₃ and CO₂ treatments From 15 April to 15 September for two growing seasons (1994 and 1995). The gas exchanges of current-year and 1-year-old shoots were measured, along with the nitrogen content of needles. In order to investigate the factors underlying modifications in photosynthesis, five parameters linked to photosynthetic performance and three to stomatal conductance were determined. Elevated O₃ concentrations led to a significant decline in the CO₂ compensation point (Г^*), maximum RuP₂-saturated rate of carboxylation (V_cmax), maximum rate of electron transport (J_max), maximum stomatal conductance (g_smax), and sensitivity of stomatal conductance to changes in leaf-to-air vapour pressure difference (?g_s/?D_v) in both shoot-age classes. However, the effect of elevated O₃ concentrations on the respiration rate in light (R_d) was dependent on shoot age. Elevated CO₂(700 μmol mol^?1) significantly decreased J_max and g_smax but increased R_d in 1-year-old shoots and the ?g_s/?D_v in both shoot-age classes. The interactive effects of O₃ and CO₂ on some key parameters (e.g. V_cmax and J_max) were significant. This may be closely related to regulation of the maximum stomatal conductance and stomatal sensitivity induced by elevated CO₂. As a consequence, the injury induced by O₃ was reduced through decreased ozone uptake in 1-year-old shoots, but not in the current-year shoots. Compared to ambient O₃ concentration, reduced O₃ concentrations (charcoal-filtered air) did not lead to significant changes in any of the measured parameters. Compared to the control treatment, calculations showed that elevated O₃ concentrations decreased the apparent quantum yield by 15% and by 18%, and the maximum rate of photosynthesis by 21% and by 29% in the current-year and 1-year-old shoots, respectively. Changes in the nitrogen content of needles resulting from the various treatments were associated with modifications in photosynthetic components.     

Elevated CO2 concentrations and stomatal density: observations from 17 plant species growing in a CO2 spring in central Italy

Stomatal density (SD) and stomatal conductance ( g _s) can be affected by an increase of atmospheric CO₂ concentration. This study was conducted on 17 species growing in a naturally enriched CO₂ spring and belonging to three plant communities. Stomatal conductance, stomatal density and stomatal index (SI) of plants from the spring, which were assumed to have been exposed for generations to elevated [CO₂], and of plants of the same species collected in a nearby control site, were compared. Stomatal conductance was significantly lower in most of the species collected in the CO₂ spring and this indicated that CO₂ effects on g _s are not of a transitory nature but persist in the long term and through plant generations. Such a decrease was, however, not associated with changes in the anatomy of leaves: SD was unaffected in the majority of species (the decrease was only significant in three out of the 17 species examined), and also SI values did not vary between the two sites with the exception of two species that showed increased SI in plants grown in the CO₂-enriched area. These results did not support the hypothesis that long-term exposure to elevated [CO₂] may cause adaptive modification in stomatal number and in their distribution.     

The cellular basis of guard cell sensing of rising CO2

Numerous studies conducted on both whole plants and isolated epidermes have documented stomatal sensitivity to CO₂. In general, CO₂ concentrations below ambient stimulate stomatal opening, or an inhibition of stomatal closure, while CO₂ concentrations above ambient have the opposite effect. The rise in atmospheric CO₂ concentrations which has occurred since the industrial revolution, and which is predicted to continue, will therefore alter rates of transpirational water loss and CO₂ uptake in terrestrial plants. An understanding of the cellular basis for guard cell CO₂ sensing could allow us to better predict, and perhaps ultimately to manipulate, such vegetation responses to climate change. However, the mechanisms by which guard cells sense and respond to the CO₂ signal remain unknown. It has been hypothesized that cytosolic pH and malate levels, cytosolic Ca²⁺ levels, chloroplastic zeaxanthin levels, or plasma-membrane anion channel regulation by apoplastic malate are involved in guard cell perception and response to CO₂. In this review, these hypotheses are discussed, and the evidence for guard cell acclimation to prevailing CO₂ concentrations is also considered.     

Stomatal acclimation over a subambient to elevated CO2 gradient in a C3/C4 grassland

An investigation to determine whether stomatal acclimation to [CO₂] occurred in C₃/C₄ grassland plants grown across a range of [CO₂] (200–550 µmol mol^?1) in the field was carried out. Acclimation was assessed by measuring the response of stomatal conductance (g_s) to a range of intercellular CO₂ (a g_s–C_i curve) at each growth [CO₂] in the third and fourth growing seasons of the treatment. The g_s–C_i response curves for Solanum dimidiatum (C₃ perennial forb) differed significantly across [CO₂] treatments, suggesting that stomatal acclimation had occurred. Evidence of non–linear stomatal acclimation to [CO₂] in this species was also found as maximum g_s (g_smax; g_s measured at the lowest C_i) increased with decreasing growth [CO₂] only below 400 µmol mol^?1. The substantial increase in g_s at subambient [CO₂] for S. dimidiatum was weakly correlated with the maximum velocity of carboxylation (V_cmax; r² = 0·27) and was not associated with CO₂ saturated photosynthesis (A_max). The response of g_s to C_i did not vary with growth [CO₂] in Bromus japonicus (C₃ annual grass) or Bothriochloa ischaemum (C₄ perennial grass), suggesting that stomatal acclimation had not occurred in these species. Stomatal density, which increased with rising [CO₂] in both C₃ species, was not correlated with g_s. Larger stomatal size at subambient [CO₂], however, may be associated with stomatal acclimation in S. dimidiatum. Incorporating stomatal acclimation into modelling studies could improve the ability to predict changes in ecosystem water fluxes and water availability with rising CO₂ and to understand their magnitudes relative to the past.     

Parameterization of the CO2 and H2O gas exchange of several temperate deciduous broad-leaved trees at the leaf scale considering seasonal changes

A combined model to simulate CO₂ and H₂O gas exchange at the leaf scale was parameterized using data obtained from in situ leaf‐scale observations of diurnal and seasonal changes in the CO₂ and H₂O gas exchange of four temperate deciduous broad‐leaved trees using a porometric method. The model consists of a Ball et al. type stomatal conductance submodel [Ball, Woodrow & Berry, pp. 221–224 in Progress in Photosynthesis Research (ed. I. Biggins), Martinus‐Nijhoff Publishers, Dordrecht, The Netherlands, 1987] and a Farquhar et al. type biochemical submodel of photosynthesis (Farquhar, von Caemmerer & Berry, Planta 149, 78–90, 1980). In these submodels, several parameters were optimized for each tree species as representative of the quantitative characteristics related to gas exchange. The results show that the seasonal physiological changes of V_cmax25 in the biochemical model of photosynthesis should be used to estimate the long‐term CO₂ gas exchange. For R_d25 in the biochemical model of photosynthesis and m in the Ball et al. type stomatal conductance model, the difference should be counted during the leaf expansion period.     

Photosynthesis and transpiration of tomato and CO2 fluxes in a greenhouse under changing environmental conditions in winter

Responses of tomato leaves in a greenhouse to light and CO₂ were examined at the transient stage at the end of winter, when both photoperiod and irradiance gradually increase. Additionally, CO₂ fluxes were calculated for a greenhouse without supplementary lighting and without CO₂ enrichment based on CO₂ sinks (plant photosynthesis) and CO₂ sources (plant and substrate respiration). In January, tomato leaves in the greenhouse showed low photosynthesis with a maximum assimilation of 6–8 μmol CO₂ m⁻² s⁻¹, a quantum yield of 0.06 μmol CO₂ μmol⁻¹ photosynthetic active radiation (PAR) and a low light compensation point of 26 μmol PAR m⁻² s⁻¹, a combination which classifies them as shade leaves. In February, tomato leaves increased their light compensation point to 39 μmol PAR m⁻² s⁻¹ and quantum yield to 0.08, the former indicating the adaptation to increased irradiance and photoperiod. These tomato leaves increased their transpiration from 0.4 to 0.9 in January to ∼2 mmol H₂O m⁻² s⁻¹ in February. Both photosynthesis and transpiration were primarily limited by light but neither by stomatal conductivity nor by CO₂. In January, light response of photosynthesis, dark respiration and transpiration were negligibly affected by increasing CO₂ concentrations from 600 to 900 ppm CO₂ under low light conditions, indicating no benefit of CO₂ enrichment unless light intensity increased. In February, tomato leaves were photoinhibited at inherent greenhouse CO₂ concentrations on the first sunny day; this photoinhibition was further enhanced by an increased CO₂ concentration of 1000 ppm. CO₂ fluxes in the greenhouse appeared strongly dependent on solar radiation. After exceeding the light compensation point in the morning, greenhouse CO₂ concentrations decreased by 58 or by 110 ppm CO₂ h⁻¹ on a sunny day in January or February and by 23 ppm on overcast days in both months. Calculated per overall tomato canopy, plant photosynthesis contributed 42–50% to the morning CO₂ depletion in the greenhouse. Dark respiration of tomato leaves was ∼2 μmol CO₂ m⁻² s⁻¹ in January and ∼3 μmol CO₂ m⁻² s⁻¹ in February. This dark respiration resulted in rises of 15 and 17 ppm CO₂ h⁻¹ at night in the greenhouse compartment and was identified as primary source of CO₂. Respiration of the substrate used to grow the plants, which produced 7.3 ppm CO₂ h⁻¹, was identified as secondary source of CO₂. The combined plant and substrate respiration resulted in peaks of up to 900 ppm CO₂ in the greenhouse before dawn.     

Interaction between CO2 enrichment and salinity stress in the C4 non-halophyte Andropogon glomeratus (Walter) BSP

Abstract Increasing atmospheric CO₂ may result in alleviation of salinity stress in salt-sensitive plants. In order to assess the effect of enriched CO₂ on salinity stress in Andropogon glomeratus, a C₄ non-halophyte found in the higher regions of salt marshes, plants were grown at 350, 500, and 650 cm³ m^?3 CO₂ with 0 or 100 mol m^?3 NaCl watering treatments. Increases in leaf area and biomass with increasing CO₂ were measured in salt-stressed plants, while decreases in these same parameters were measured in non-salt-stressed plants. Tillering increased substantially with increasing CO₂ in salt-stressed plants, resulting in the increased biomass. Six weeks following initiation of treatments, there was no difference in photosynthesis on a leaf area basis with increasing CO₂ in salt-stressed plants, although short-term increases probably occurred. Stomatal conductance decreased with increasing CO₂ in salt-stressed plants, resulting in higher water-use efficiency, and may have improved the diurnal water status of the plants. Concentrations of Na⁺ and Cl^? were higher in salt stressed-plants while the converse was found for K ⁺. There were no differences in leaf ion content between CO₂ treatments in the salt-stressed plants. Decreases in photosynthesis in salt-stressed plants occurred primarily as a result of decreased internal (non-stomatal) conductance.     

The interaction of rising CO2 and temperatures with water use efficiency

Abstract. Recent data concerning the impact of elevated atmospheric CO₂ upon water use efficiency (WUE) and the related measure, instantaneous transpiration efficiency (ITE), are reviewed. It is concluded from both short and long-term studies that, at the scale of the individual leaf or plant, an increase in WUE or ITE is generally observed in response to increased atmospheric CO₂ levels. However, the magnitude of this increase may decline with time. The opinion that elevated CO₂ may substantially decrease transpiration at the regional scale is discussed. The mechanisms by which elevated CO₂ may cause a change in these measures are discussed in terms of stomatal conductance, assimilation and respiration responses to elevated CO₂. Finally, recent experimental data and model outputs concerning the impact of the interaction of increased temperature with elevated CO₂ on WUE, ITE and yield are reviewed. It is concluded that substantially more data is required before reliable predictions about the regional scale response of WUE and catchment hydrology can be made.     

Leaf stomatal responses to vapour pressure deficit under current and CO2-enriched atmosphere explained by the economics of gas exchange

Using the economics of gas exchange, early studies derived an expression of stomatal conductance ( g ) assuming that water cost per unit carbon is constant as the daily loss of water in transpiration ( f _e) is minimized for a given gain in photosynthesis ( f _c). Other studies reached identical results, yet assumed different forms for the underlying functions and defined the daily cost parameter as carbon cost per unit water. We demonstrated that the solution can be recovered when optimization is formulated at time scales commensurate with the response time of g to environmental stimuli. The optimization theory produced three emergent gas exchange responses that are consistent with observed behaviour: (1) the sensitivity of g to vapour pressure deficit ( D ) is similar to that obtained from a previous synthesis of more than 40 species showing g to scale as 1 −  m  log( D ), where m   ∈  [0.5,0.6], (2) the theory is consistent with the onset of an apparent 'feed-forward' mechanism in g , and (3) the emergent non-linear relationship between the ratio of intercellular to atmospheric [CO₂] ( c _i/ c _a) and D agrees with the results available on this response. We extended the theory to diagnosing experimental results on the sensitivity of g to D under varying c _a.