A hydromechanical and biochemical model of stomatal conductance

A mathematical model of stomatal conductance is presented. It is based on whole‐plant and epidermal hydromechanics, and on two hypotheses: (1) the osmotic gradient across guard cell membranes is proportional to the concentration of ATP in the guard cells; and (2) the osmotic gradient that can be sustained per unit of ATP is proportional to the turgor pressure of adjacent epidermal cells. In the present study, guard cell [ATP] is calculated using a previously published model that is based on a widely used biochemical model of C₃ mesophyll photosynthesis. The conductance model for Vicia faba L. is parameterized and tested As with most other stomatal models, the present model correctly predicts the stomatal responses to variations in transpiration rate, irradiance and intercellular CO₂. Unlike most other models, however, this model can predict the transient stomatal opening often observed before conductance declines in response to decreases in humidity, soil water potential, or xylem conductance. The model also explicitly accommodates the mechanical advantage of the epidermis and correctly predicts that stomata are relatively insensitive to the ambient partial pressure of oxygen, as a result of the assumed dependence on ATP concentration.     

Endogenous circadian regulation of carbon dioxide exchange in terrestrial ecosystems

It is often assumed that daytime patterns of ecosystem carbon assimilation are mostly driven by direct physiological responses to exogenous environmental cues. Under limited environmental variability, little variation in carbon assimilation should thus be expected unless endogenous plant controls on carbon assimilation, which regulate photosynthesis in time, are active. We evaluated this assumption with eddy flux data, and we selected periods when net ecosystem exchange (NEE) was decoupled from environmental variability in seven sites from highly contrasting biomes across a 74° latitudinal gradient over a total of 36 site‐years. Under relatively constant conditions of light, temperature, and other environmental factors, significant diurnal NEE oscillations were observed at six sites, where daily NEE variation was between 20% and 90% of that under variable environmental conditions. These results are consistent with fluctuations driven by the circadian clock and other endogenous processes. Our results open a promising avenue of research for a more complete understanding of ecosystem fluxes that integrates from cellular to ecosystem processes.     

Qualitative effects of patchy stomatal conductance distribution features on gas-exchange calculations

The qualitative influence of patchy stomatal conductance distributions on the values of photosynthesis (A) and intercellular CO₂ concentration (c_i) as determined by gas-exchange measurements were investigated using computer modelling. Gas-exchange measurements were simulated for different conductance distributions by modelling photosynthesis explicitly for each patch, summing these rates, and inferring c_i from a diffusion equation. Qualitative relationships are presented between conductance distribution features and the difference between assimilation rates measured for patchy and homogeneous leaves at the same c_i (A_p and A_h, respectively). These data show that, although most conductance distributions have little effect on the value of A measured for a given c_i, some distribution features (which we have termed ‘bimodality’, ‘position’, ‘skewness’ and ‘range’) play a key role in controlling the magnitude of these effects. Distributions that are more nearly bimodal, span regions of lower conductance, are right-skewed, or have broader conductance ranges are associated with larger effects on the A(c_i) relationship. To clarify our mathematical analysis and illustrate some of the trends it predicts, we present conductance distributions and gas-exchange data from leaves of Malus dolgo var. Spring Snow Dial were treated with ABA. The results are discussed in the light of recent controversy over the effect of patchy stomatal conductance on gas-exchange data.     

Differences between the flag leaf and the ear of a spring wheat cultivar (Triticum aestivum cv. Arkas) with respect to the CO2 response of assimilation, respiration and stomatal conductance

The CO₂- and H₂O-exchanges in the flag leaf and the ear of a spring wheat cultivar (Triticum aestivum L. cv. Arkas) were measured at CO₂ partial pressures, p_i(CO₂), between 8 and 400 Pa under high photosynthetic photon flux densities (2000 μmol m^?2 s^?1). The experiments were carried out on each organ separately while attached to the intact plant, from the time of ear emergence through senescence. To study the contribution of the kernels to the gas exchange of ears, experiments were also carried out on sterilized ears (treatment A), and on ears from which the kernels were removed (treatment B). Flag leaves and ears differed considerably with regard to CO₂-dependence of assimilation, response of stomata to varying p_a(CO₂), CO₂ compensation point (and its temperature dependence), dark respiration, and dissimilation in the light (i.e. CO₂ production which is not due to oxygenation of ribulose 1,5-bisphosphate). The higher dark respiration of the ear originated mainly from the kernels and continued to some extent in the light. Thus, the CO₂ compensation point was attained at higher CO₂ partial pressures for the ear than for the flag leaf. The CO₂ uptake of the ear was not saturated at intercellular CO₂ partial pressures below 180 Pa CO₂, while that of the flag leaf reached saturation at about 80 Pa CO₂. CO₂-saturated rates of CO₂ uptake were 2.5 and 1.5 times the rates at natural CO₂ partial pressure for ear and flag leaf, respectively. The stomatal conductance decreased with rising CO₂ partial pressure above 35 Pa, in a more pronounced manner for the flag leaf than for the ear.     

Relationships between nitrogen uptake and carbon assimilation in whole plants of tall fescue

Abstract. The present study investigates the relationships between nitrogen uptake, transpiration, and carbon assimilation. Plants growing on nutrient solution were enclosed for 10–16 d in a growth chamber, where temperature, photon flux density, vapour saturation deficit and CO₂ concentration were controlled. One of these factors was modified every 4 to 5 d. Shoot photosynthesis and root and shoot respiration were recorded every half-hour. Nitrogen uptake from the root medium and plant transpiration were measured daily. In most cases, an increase in photon flux density led to increases in transpiration, net daily carbon assimilation, and nitrogen uptake. By modifying transpiration rate without changing photosynthesis (varying vapour saturation deficit), or by modifying transpiration and carbon assimilation in opposite ways (varying CO₂ air concentration), it was shown that nitrogen uptake does not follow transpiration, but is linked to the carbon uptake of the plant. When light was increased from low to intermediate levels, the N uptake/C assimilation ratio remained constant. At higher photon flux density, this ratio declined markedly. It is proposed that in the first case, growth is limited by carbohydrate availability, thus any increase in carbon assimilation leads to a proportional increase in nitrogen uptake, in contrast to the second situation where carbohydrates may accumulate in the plant without further nitrogen requirement.     

Mesophyll conductance in land surface models: effects on photosynthesis and transpiration

The CO₂ transfer conductance within plant leaves (mesophyll conductance, g_m) is currently not considered explicitly in most land surface models (LSMs), but instead treated implicitly as an intrinsic property of the photosynthetic machinery. Here, we review approaches to overcome this model deficiency by explicitly accounting for g_m, which comprises the re‐adjustment of photosynthetic parameters and a model describing the variation of g_m in dependence of environmental conditions. An explicit representation of g_m causes changes in the response of photosynthesis to environmental factors, foremost leaf temperature, and ambient CO₂ concentration, which are most pronounced when g_m is small. These changes in leaf‐level photosynthesis translate into a stronger climate and CO₂ response of gross primary productivity (GPP) and transpiration at the global scale. The results from two independent studies show consistent latitudinal patterns of these effects with biggest differences in GPP in the boreal zone (up to ~15%). Transpiration and evapotranspiration show spatially similar, but attenuated, changes compared with GPP. These changes are indirect effects of g_m caused by the assumed strong coupling between stomatal conductance and photosynthesis in current LSMs. Key uncertainties in these simulations are the variation of g_m with light and the robustness of its temperature response across plant types and growth conditions. Future research activities focusing on the response of g_m to environmental factors and its relation to other plant traits have the potential to improve the representation of photosynthesis in LSMs and to better understand its present and future role in the Earth system.     

Herbivore perception decreases photosynthetic carbon assimilation and reduces stomatal conductance by engaging 12‐oxo‐phytodienoic acid,mitogen‐activated protein kinase 4 and cytokinin perception

Herbivory‐induced changes in photosynthesis have been documented in many plant species; however, the complexity of photosynthetic regulation and analysis has thwarted progress in understanding the mechanism involved, particularly those elicited by herbivore‐specific elicitors. Here, we analysed the early photosynthetic gas exchange responses in Nicotiana attenuata plants after wounding and elicitation with Manduca sexta oral secretions and the pathways regulating these responses. Elicitation with M. sexta oral secretions rapidly decreased photosynthetic carbon assimilation (A_C) in treated and systemic (untreated, vascularly connected) leaves, which were associated with changes in stomatal conductance, rather than with changes in Rubisco activity and 1‐5 ribulose‐1,5‐bisphosphate turnover. Phytohormone profiling and gas exchange analysis of oral secretion‐elicited transgenic plants altered in phytohormone regulation, biosynthesis and perception, combined with micrografting techniques, revealed that the local photosynthetic responses were mediated by 12‐oxo‐phytodienoic acid, while the systemic responses involved interactions among jasmonates, cytokinins and abscisic acid signalling mediated by mitogen‐activated protein kinase 4. The analysis also revealed a role for cytokinins interacting with mitogen‐activated protein kinase 4 in CO₂‐mediated stomatal regulation. Hence, oral secretions, while eliciting jasmonic acid‐mediated defence responses, also elicit 12‐oxo‐phytodienoic acid‐mediated changes in stomatal conductance and A_C, an observation illustrating the complexity and economy of the signalling that regulates defence and carbon assimilation pathways in response to herbivore attack.     

Effects of carbon dioxide concentration on the interactive effects of temperature and water vapour on stomatal conductance in soybean

Soybeans were grown at three CO₂ concentrations in outdoor growth chambers and at two concentrations in controlled-environment growth chambers to investigate the interactive effects of CO₂, temperature and leaf-to-air vapour pressure difference (LAVPD) on stomatal conductance. The decline in stomatal conductance with CO₂ was a function of both leaf temperature and LAVPD. In the field measurements, stomatal conductance was more sensitive to LAVPD at low CO₂ at 30 °C but not at 35 °C. There was also a direct increase in conductance with temperature, which was greater at the two elevated carbon dioxide concentrations. Environmental growth chamber results showed that the relative stomatal sensitivity to LAVPD decreased with both leaf temperature and CO₂. Measurements in the environmental growth chamber were also performed at the opposing CO₂, and these experiments indicate that the stomatal sensitivity to LAVPD was determined more by growth CO₂ than by measurement CO₂. Two models that describe stomatal responses to LAVPD were compared with the outdoor data to evaluate whether these models described adequately the interactive effects of CO₂, LAVPD and temperature.     

The kinetics of stomatal responses to VPD in Vicia faba: electrophysiological and water relations models

Abstract. An Ohm's law analogy is frequently employed to calculate parameters of leaf gas exchange. For example, resistance to water vapour loss is calculated as the quotient of vapour pressure difference (VPD) and vapour loss by transpiration. In the present research, this electrical analogy was extended. Steady-state transpiration as a function of VPD, assayed in leaflets of Vicia faba using gas exchange techniques, was compared with steady-state K⁺ current magnitude as a function of voltage in isolated guard cell protoplasts of Vicia faba, assayed using the patch clamping technique in the whole cell configuration. An electrophysiological model originally developed to explain the kinetics of current changes following step changes in voltage across a cell membrane was used to fit the kinetics of transpiration changes following step changes in VPD applied to leaflets of Vicia faba. Following step increases in VPD, transpiration exhibited an initial increase, reflecting the increased driving force for water loss and, for large step increases in VPD, a transient decrease in stomatal resistance. Transpiration subsequently declined, reflecting stomatal closure. By analogy to electrophysiological responses, it is hypothesized that the humidity parameter that is sensed by guard cells is VPD. Two models based on epidermal water relations were also applied to transpiration kinetics. In the first model, the transient increase in transpiration following a step increase in VPD was attributed partially to an increase in the Physical driving force (VPD) and partially to a transient decrease in stomatal resistance resulting from reduced epidermal backpressure. In the second model, the transient decrease in stomatal resistance was attributed to a direct response of the guard cells to VPD. Both models based on water relations gave good fits of the data, emphasizing the need for further study regarding the metabolic nature of the guard cell response to humidity.     

Distribution profile of stomatal conductance and its interrelations to transpiration rate and water dynamics in young maize laminas under sulfate deprivation

Seven-day-old maize (Zea mays) plants were grown hydroponically for 10 days in S-deprived nutrient solution. The distribution profiles according to the position on the stem of the S-deprived laminas’ stomatal conductance, transpiration rate, photosynthetic rate, dry mass, water content, and specific surface area were monitored relative to control among others. Photochemical efficiency of photosystem II remained unaffected by the deprivation, as well as the specific surface area of all but the embryonic laminas after d2. In S-deficient plants, the embryonic (L0) and the uppermost lamina or the one below it presented mostly significant changes. The response ratios (Rr) of the L0 stomatal conductance oscillated; the oscillation started with an increase at d2. The corresponding Rr values of L0 transpiration and photosynthetic rates started oscillating at d4 in the same fashion. At d8, an increasing gradient appeared in water-content Rr values from L1 to the uppermost lamina. At d10, all but the embryonic laminas presented significantly reduced Rr values in water content. Changes in dry mass and surface area of laminas were synchronized. In control, the transpiration rate expressed per DM unit remained constant during the examined period, while under the deprivation it followed a power function of surface area.     

A field study of the effects of elevated CO2 on carbon assimilation, stomatal conductance and leaf and branch growth of Pinus taeda trees

A study was conducted in 21-year-old loblolly pine (Pinus taeda L.) trees growing in plantation in north central Georgia, USA. The experiment used branch chambers to impose treatments of ambient, ambient +165 and ambient + 330 μmol mol^?1 CO₂. After one growing season there was no indication of acclimation to elevated CO₂. In August and September, carbon assimilation, measured by two different methods, was twice as high at ambient +330 μmol mol^?1 CO₂ than at ambient. Dark respiration was suppressed by 6% at ambient +165 and by 14% at ambient + 330 μmol mol^?1 CO₂. This suppression was immediate, and not an effect of exposure to elevated CO₂ during growth, since respiration was reduced by the same amount in all treatments when measured at a high CO₂ concentration. Elevated CO₂ increased the growth of foliage and woody tissue. It also increased instantaneous transpiration efficiency, but it had no effect on stomatal conductance. Since the soil at the study site had low to moderate fertility, these results suggest that the growth potential of forests on many sites may be enhanced by global increases in atmospheric CO₂, concentration.     

The effect of elevated CO2 on diel leaf growth cycle, leaf carbohydrate content and canopy growth performance of Populus deltoides

Image sequence processing methods were applied to study the effect of elevated CO₂ on the diel leaf growth cycle for the first time in a dicot plant. Growing leaves of Populus deltoides, in stands maintained under ambient and elevated CO₂ for up to 4 years, showed a high degree of heterogeneity and pronounced diel variations of their relative growth rate (RGR) with maxima at dusk. At the beginning of the season, leaf growth did not differ between treatments. At the end of the season, final individual leaf area and total leaf biomass of the canopy was increased in elevated CO₂. Increased final leaf area at elevated CO₂ was achieved via a prolonged phase of leaf expansion activity and not via larger leaf size upon emergence. The fraction of leaves growing at 30–40% day^?1 was increased by a factor of two in the elevated CO₂ treatment. A transient minimum of leaf expansion developed during the late afternoon in leaves grown under elevated CO₂ as the growing season progressed. During this minimum, leaves grown under elevated CO₂ decreased their RGR to 50% of the ambient value. The transient growth minimum in the afternoon was correlated with a transient depletion of glucose (less than 50%) in the growing leaf in elevated CO₂, suggesting diversion of glucose to starch or other carbohydrates, making this substrate temporarily unavailable for growth. Increased leaf growth was observed at the end of the night in elevated CO₂. Net CO₂ exchange and starch concentration of growing leaves was higher in elevated CO₂. The extent to which the transient reduction in diel leaf growth might dampen the overall growth response of these trees to elevated CO₂ is discussed.     

The boundary layer and the apparent responses of stomatal conductance to wind speed and to the mole fractions of CO2 and water vapour in the air

The experiments and simulations reported in this paper show that, for stomata sensitive to both CO₂ and water vapour concentrations, responses of stomatal conductance (g^w_s) to boundary layer thickness have two components, one resulting from changes in intercellular CO₂ concentration (χ^c_i) and another from changes in leaf surface water vapour saturation deficit (D^w_s). The experiments and simulations also show that the boundary layer conductance (g^w_b) can significantly alter the apparent response of g^w_s to ambient air CO₂ mole fraction (χ^c_a) and water vapour mole fraction (χ^w_a). Because of the feedback loop involved the responses of g^w_s for χ^c_a and χ^w_a each include responses to both χ^c_i and D^w_s. The boundary layer alters the state of the variables sensed by the guard cells—i.e. χ^c_i and D^w_s—and so it is a source of feedback. Thus, when scaling up from responses of stomata to the response of g^w_s for a whole leaf, the effect of the boundary layer must be considered. The results indicate that, for given responses of g^w_s to χ^c_i and D^w_s, the apparent responses of g^w_s to D^w_a and χ^c_a depend on the size of the leaf and wind speed, showing that this effect of the boundary layer should be considered when comparing data measured under different conditions, or with different methods.     

Variability of photosynthetic gas exchange parameters, dark respiration, and stomatal numbers in species of Polygonum

Within the genus Polygonum a large variation was found between species with regard to stomatal number, gas phase resistance, intracellular resistance and dark respiration. Interspecific variation in CO₂ compensation concentration and intercellular CO₂ concentration at constant external concentration were comparatively small. Correlations were found between stomatal number and gas phase resistance, stomatal number and Γ, and Γ and the product of dark respiration rate and intracellular resistance. The influence of dark respiration and stomatal number on photosynthetic gas exchange is discussed. It was concluded that dark respiration in light was enhanced by 22% as a mean value in 9 Polygonum species and by 62% in Polygonum lapathifolium .     

Seasonal trends of light-saturated net photosynthesis and stomatal conductance of loblolly pine trees grown in contrasting environments of nutrition, water and carbon dioxide

Repeated measures analysis was used to evaluate the effect of long-term CO₂ enhancement on seasonal trends of light-saturated rates of net photosynthesis (A_sat) and stomatal conductance to water vapour (g_sat) of 9-year-old loblolly pine (Pinus taeda L.) trees grown in a 2 × 2 factorial experimental design of nutrition and water. A significant interaction effect of CO₂ and nutrition on mean A_sat was observed for juvenile foliage. Also, juvenile foliage exposed to +350 μmol mol^?1 CO₂ had a higher rate of increase of A_sat between late summer and early autumn. This would lead to a greater potential for recharging carbohydrate reserves for winter. Mature foliage was affected by CO_sat, water and nutrient treatments in two ways. First, A_sat was significantly increased as a result of elevated CO₂ in January, a period when stomatal conductance was only 47% of the maximum observed rate. Secondly, the rate of increase of A_sat from winter to early spring was accelerated as a result of both nutrient + water and + 350 μmol mol^?1 CO₂ treatments. This accelerated response resulted in a greater potential for photosynthate production during the period when growth initiation occurred. Nutrient, water or carbon dioxide treatments did not significantly alter trends in g_sat for mature or juvenile foliage. A significant nutrition × CO₂ interaction was observed for the mature foliage, suggesting that g_sat increased with increasing CO₂ and nutrition. These results may have important consequences for the determination of the water use efficiency of loblolly pine. In spite of low g_sat in the winter to early spring period, there was a substantial gain in A_sat attributable to elevated CO₂ concentrations.     

Functional diversity of photosynthesis during drought in a model tropical rainforest – the contributions of leaf area, photosynthetic electron transport and stomatal conductance to reduction in net ecosystem carbon exchange

The tropical rainforest mesocosm within the Biosphere 2 Laboratory, a model system of some 110 species developed over 12 years under controlled environmental conditions, has been subjected to a series of comparable drought experiments during 2000–2002. In each study, the mesocosm was subjected to a 4–6 week drought, with well‐defined rainfall events before and after the treatment. Ecosystem CO₂ uptake rate (A_eco) declined 32% in response to the drought, with changes occurring within days and being reversible within weeks, even though the deeper soil layers did not become significantly drier and leaf‐level water status of most large trees was not greatly affected. The reduced A_eco during the drought reflected both morphological and physiological responses. It is estimated that the drought‐induced 32% reduction of A_eco has three principal components: (1) leaf fall increased two‐fold whereas leaf expansion growth of some canopy dominants declined to 60%, leading to a 10% decrease in foliage coverage of the canopy. This might be the main reason for the persistent reduction of A_eco after rewatering. (2) The maximum photosynthetic electron transport rate at high light intensities in remaining leaves was reduced to 71% for three of the four species measured, even though no chronic photo‐inhibition occurred. (3) Stomata closed, leading to a reduced ecosystem water conductance to water vapour (33% of pre‐drought values), which not only reduced ecosystem carbon uptake rate, but may also have implications for water and energy budgets of tropical ecosystems. Additionally, individual rainforest trees responded differently, expressing different levels of stress and stress avoiding mechanisms. This functional diversity renders the individual response heterogeneous and has fundamental implications to scale leaf level responses to ecosystem dynamics.     

Drivers of radial growth and carbon isotope discrimination of bur oak (Quercus macrocarpa Michx.) across continental gradients in precipitation,vapour pressure deficit and irradiance

Tree‐ring characteristics are commonly used to reconstruct climate variables, but divergence from the assumption of a single biophysical control may reduce the accuracy of these reconstructions. Here, we present data from bur oaks (Quercus macrocarpa Michx.) sampled within and beyond the current species bioclimatic envelope to identify the primary environmental controls on ring‐width indices (RWIs) and carbon stable isotope discrimination (Δ¹³C) in tree‐ring cellulose. Variation in Δ¹³C and RWI was more strongly related to leaf‐to‐air vapour pressure deficit (VPD) at the centre and western edge of the range compared with the northern and wettest regions. Among regions, Δ¹³C of tree‐ring cellulose was closely predicted by VPD and light responses of canopy‐level Δ¹³C estimated using a model driven by eddy flux and meteorological measurements (R² = 0.96, P = 0.003). RWI and Δ¹³C were positively correlated in the drier regions, while they were negatively correlated in the wettest region. The strength and direction of the correlations scaled with regional VPD or the ratio of precipitation to evapotranspiration. Therefore, the correlation strength between RWI and Δ¹³C may be used to infer past wetness or aridity from paleo wood by determining the degree to which carbon gain and growth have been more limited by moisture or light.