Temperature as a control over ecosystem CO2 fluxes in a high-elevation, subalpine forest.

We evaluated the hypothesis that CO(2) uptake by a subalpine, coniferous forest is limited by cool temperature during the growing season. Using the eddy covariance approach we conducted observations of net ecosystem CO(2) exchange (NEE) across two growing seasons. When pooled for the entire growing season during both years, light-saturated net ecosystem CO(2) exchange (NEE(sat)) exhibited a temperature optimum within the range 7-12 degrees C. Ecosystem respiration rate ( R(e)), calculated as the y-intercept of the NEE versus photosynthetic photon flux density (PPFD) relationship, increased with increasing temperature, causing a 15% reduction in net CO(2) uptake capacity for this ecosystem as temperatures increased from typical early season temperatures of 7 degrees C to typical mid-season temperatures of 18 degrees C. The ecosystem quantum yield and the ecosystem PPFD compensation point, which are measures of light-utilization efficiency, were highest during the cool temperatures of the early season, and decreased later in the season at higher temperatures. Branch-level measurements revealed that net photosynthesis in all three of the dominant conifer tree species exhibited a temperature optimum near 10 degrees C early in the season and 15 degrees C later in the season. Using path analysis, we statistically isolated temperature as a seasonal variable, and identified the dynamic role that temperature exhibits in controlling ecosystem fluxes early and late in the season. During the spring, an increase in temperature has a positive effect on NEE, because daytime temperatures progress from near freezing to near the photosynthetic temperature optimum, and R(e )values remain low. During the middle of the summer an increase in temperature has a negative effect on NEE, because inhibition of net photosynthesis and increases in R(e). When taken together, the results demonstrate that in this high-elevation forest ecosystem CO(2) uptake is not limited by cool-temperature constraints on photosynthetic processes during the growing-season, as suggested by some previous ecophysiological studies at the branch and needle levels. Rather, it is warm temperatures in the mid-summer, and their effect on ecosystem respiration, that cause the greatest reduction in the potential for forest carbon sequestration.

Isoprene Emission from Velvet Bean Leaves (Interactions among Nitrogen Availability, Growth Photon Flux Density, and Leaf Development).

Although isoprene synthesis is closely coupled to photosynthesis, both via ATP requirements and carbon substrate availability, control of isoprene emission is not always closely linked to photosynthetic processes. In this study we grew velvet bean (Mucuna sp.) under different levels of photon flux density (PFD) and nitrogen availability in an effort to understand better the degree to which these two processes are linked. As has been observed in past studies, we found that during early leaf ontogeny the onset of positive rates of net photosynthesis precedes that of isoprene emission by 3 to 4 d. Other studies have shown that this lag is correlated with the induction of isoprene synthase activity, indicating that overall control of the process is under control of that enzyme. During leaf senescence, photosynthesis rate and isoprene emission rate declined in parallel, suggesting similar controls over the two processes. This coordinated decline was accelerated when plants were grown with high PFD and high nitrogen availability. The latter effect included declines in the photon yield of photosynthesis, suggesting that an unexplained stress arose during growth under these conditions, triggering a premature decline in photosynthesis and isoprene emission rate. In mature leaves, growth PFD and nitrogen nutrition affected photosynthesis and isoprene emission in qualitatively similar, but quantitatively different, ways. This resulted in a significant shift in the percentage of fixed carbon that was re-emitted as isoprene. In the case of increasing growth PFD, isoprene emission rate was more strongly affected than photosynthesis rate, and more carbon was lost as isoprene. In the case of increasing nitrogen, photosynthesis rate increased more than isoprene emission rate, and leaves containing high amounts of nitrogen lost a lower percentage of their assimilated carbon as isoprene. Taken together, our results demonstrate that, although the general correlation between isoprene emission rate and photosynthesis rate is consistently expressed, there is evidence that both processes are capable of independent responses to plant growth environment.

Environmental and developmental controls over the seasonal pattern of isoprene emission from aspen leaves.

Isoprene emission from plants represents one of the principal biospheric controls over the oxidative capacity of the continental troposphere. In the study reported here, the seasonal pattern of isoprene emission, and its underlying determinants, were studied for aspen trees growing in the Rocky Mountains of Colorado. The springtime onset of isoprene emission was delayed for up to 4 weeks following leaf emergence, despite the presence of positive net photosynthesis rates. Maximum isoprene emission rates were reached approximately 6 weeks following leaf emergence. During this initial developmental phase, isoprene emission rates were negatively correlated with leaf nitrogen concentrations. During the autumnal decline in isoprene emission, rates were positively correlated with leaf nitrogen concentration. Given past studies that demonstrate a correlation between leaf nitrogen concentration and isoprene emission rate, we conclude that factors other than the amount of leaf nitrogen determine the early-season initiation of isoprene emission. The late-season decline in isoprene emission rate is interpreted as due to the autumnal breakdown of metabolic machinery and loss of leaf nitrogen. In potted aspen trees, leaves that emerged in February and developed under cool, springtime temperatures did not emit isoprene until 23 days after leaf emergence. Leaves that emrged in July and developed in hot, midsummer temperatures emitted isoprene within 6 days. Leaves that had emerged during the cool spring, and had grown for several weeks without emitting isoprene, could be induced to emit isoprene within 2 h of exposure to 32°C. Continued exposure to warm temperatures resulted in a progressive increase in the isoprene emission rate. Thus, temperature appears to be an important determinant of the early season induction of isoprene emission. The seasonal pattern of isoprene emission was examined in trees growing along an elevational gradient in the Colorado Front Range (1829-2896 m). Trees at different elevations exhibited staggered patterns of bud-break and initiation of photosynthesis and isoprene emission in concert with the staggered onset of warm, springtime temperatures. The springtime induction of isoprene emission could be predicted at each of the three sites as the time after bud break required for cumulative temperatures above 0°C to reach approximately 400 degree days. Seasonal temperature acclimation of isoprene emission rate and photosynthesis rate was not observed. The temperature dependence of isoprene emission rate between 20 and 35°C could be accurately predicted during spring and summer using a single algorithm that describes the Arrhenius relationship of enzyme activity. From these results, it is concluded that the early season pattern of isoprene emission is controlled by prevailing temperature and its interaction with developmental processes. The late-season pattern is determined by controls over leaf nitrogen concentration, especially the depletion of leaf nitrogen during senescence. Following early-season induction, isoprene emission rates correlate with photosynthesis rates. During the season there is little acclimation to temperature, so that seasonal modeling simplifies to a single temperature-response algorithm.

Theoretical Considerations when Estimating the Mesophyll Conductance to CO(2) Flux by Analysis of the Response of Photosynthesis to CO(2).

The conductance for CO(2) diffusion in the mesophyll of leaves can limit photosynthesis. We have studied two methods for determining the mesophyll conductance to CO(2) diffusion in leaves. We generated an ideal set of photosynthesis rates over a range of partial pressures of CO(2) in the stroma and studied the effect of altering the mesophyll diffusion conductance on the measured response of photosynthesis to intercellular CO(2) partial pressure. We used the ideal data set to test the sensitivity of the two methods to small errors in the parameters used to determine mesophyll conductance. The two methods were also used to determine mesophyll conductance of several leaves using measured rather than ideal data sets. It is concluded that both methods can be used to determine mesophyll conductance and each method has particular strengths. We believe both methods will prove useful in the future.

Estimation of Mesophyll Conductance to CO(2) Flux by Three Different Methods.

The resistance to diffusion of CO(2) from the intercellular airspaces within the leaf through the mesophyll to the sites of carboxylation during photosynthesis was measured using three different techniques. The three techniques include a method based on discrimination against the heavy stable isotope of carbon, (13)C, and two modeling methods. The methods rely upon different assumptions, but the estimates of mesophyll conductance were similar with all three methods. The mesophyll conductance of leaves from a number of species was about 1.4 times the stomatal conductance for CO(2) diffusion determined in unstressed plants at high light. The relatively low CO(2) partial pressure inside chloroplasts of plants with a low mesophyll conductance did not lead to enhanced O(2) sensitivity of photosynthesis because the low conductance caused a significant drop in the chloroplast CO(2) partial pressure upon switching to low O(2). We found no correlation between mesophyll conductance and the ratio of internal leaf area to leaf surface area and only a weak correlation between mesophyll conductance and the proportion of leaf volume occupied by air. Mesophyll conductance was independent of CO(2) and O(2) partial pressure during the measurement, indicating that a true physical parameter, independent of biochemical effects, was being measured. No evidence for CO(2)-accumulating mechanisms was found. Some plants, notably Citrus aurantium and Simmondsia chinensis, had very low conductances that limit the rate of photosynthesis these plants can attain at atmospheric CO(2) level.

An improved model of C3 photosynthesis at high CO2: Reversed O 2 sensitivity explained by lack of glycerate reentry into the chloroplast.

Current models of C3 photosynthesis incorporate a phosphate limitation to carboxylation which arises when the capacity for starch and sucrose synthesis fails to match the capacity for the production of triose phosphates in the Calvin cycle. As a result, the release of inorganic phosphate in the chloroplast stroma fails to keep pace with its rate of sequestration into triose phosphate, and phosphate becomes limiting to photosynthesis. Such a model predicts that when phosphate is limiting, assimilation becomes insensitive to both CO2 and O2, and is thus incapable of explaining the experimental observation that assimilation, under phosphate-limited conditions, frequently exhibits reversed sensitivity to both CO2 and O2, i.e., increasing O2 stimulates assimilation and increasing CO2 inhibits assimilation. We propose a model which explains reversed sensitivity to CO2 and O2 by invoking the net release of phosphate in the photorespiratory oxidation cycle. In order for this to occur, some fraction of the glycollate carbon which leaves the stroma and which is recycled to the chloroplast by the photorespiratory pathway as glycerate must remain in the cytosol, perhaps in the form of amino acids. In that case, phosphate normally used in the stromal glycerate kinase reaction to generate PGA from glycerate is made available for photophosphorylation, stimulating RuBP regeneration and assimilation. The model is parameterized for data obtained on soybean and cotton, and model behavior in response to CO2, O2, and light is demonstrated.

Factors influencing carbon fixation and water use by mediterranean sclerophyll shrubs during summer drought.

Mediterranean sclerophyll shrubs respond to seasonal drought by adjusting the amount of leaf area exposed and by reducing gas exchange via stomatal closure mechanisms. The degree to which each of these modifications can influence plant carbon and water balances under typical mediterranean-type climate conditions is examined. Leaf area changes are assessed in the context of a canopy structure and light microclimate model. Shifts in physiological response are examined with a mechanistically-based model of C3 leaf gas exchange that simulates progressive reduction of maximum photosynthesis and transpiration rates and increasingly strong midday stomatal closure over the course of drought. The results demonstrate that midday stomatal closure may effectively contribute to drought avoidance, increase water use efficiency, and strongly alter physiological efficiency in the conversion of intercepted light energy to photoproducts. Physiological adjustments lead to larger reductions in water use than occur when comparing leaf area index 3.5 to 1.5, extremes found for natural stands of sclerophyll shrubs in the California chaparral. Reductions in leaf area have the strongest effect on resource capture and use during non-water-stressed periods and the least effect under extreme drought conditions, while shifts in physiological response lead to large savings of water and efficient water use under extreme stress. An important model parameter termed GFAC (proportionality factor expressing the relation of conductance [g] to net photosynthesis rate) is utilized, which changes in response to the integrated water stress experimence of shrubs and alters the degree to which stomata may open for a given rate of carbon fixation. We attempt to interpret this parameter in terms of physiological mechanisms known to modify control of leaf gas exchange during drought. The analysis helps visualize means by which canopy gas exchange behavior may be coupled to physiological changes occurring in the root environment during soil drying.

Water content effects on photosynthetic response of Sphagnum mosses from the foothills of the Philip Smith Mountains, Alaska.

In tussock tundra areas of the foothills north of the Brooks Range, Alaska, up to two-thirds of annual precipitation may occur during intermittent summer thunderstorms. The seasonal pattern in capitulum water content of Sphagnum spp. depends on the frequency and duration of these precipitation events, on the microtopography of the habitat including depth of thaw, and on morphological characteristics of the individual species. The response of net photosynthesis to varying water content in Sphagnum squarrosum and S. angustifolium growing under willow canopies in a tussock tundra area near the Dalton Highway on the North Slope of Alaska was examined in the field. After a period in June required to develop photosynthetic capability, capitula water content was essentially optimal for photosynthesis in the range from 6 to 10 g H2O/g DW. Above this range, the rate of CO2 uptake was reduced, presumably due to limitations on CO2 diffusion to the photosynthetically active sites. At water contents below the optimum, net photosynthesis fell rapidly until reaching compensation at approximately 1 g H2O/g DW. Dependent on changes in weather conditions, average water content of Sphagnum samples collected in the field occasionally fell below 5 g H2O/g DW. During a particularly dry period, water content of individual Sphagnum hummocks fell below 1 g H2O/g DW, indicating that water stress does limit Sphagnum photosynthetic production in this habitat.

Irradiance and temperature effects on photosynthesis of tussock tundra Sphagnum mosses from the foothills of the Philip Smith Mountains, Alaska.

Photosynthetic characteristics of three species of Sphagnum common in the foothills of the Brooks Range on the North Slope of Alaska were investigated. Generally, light-saturated rates of net photosynthesis decreased in the order S. squarrosum, S. angustifolium, and S. warnstorfii when plants were grown under common growth chamber conditions. For field-grown S. angustifolium, average light compensation point at 10°C was 37 µmol m-2s-1 photosynthetic photon flux density (PPFD), and light saturation occurred between 250 and 500 µmol m-2 s-1. At 20°C, compensation point increased to 127 µmol m-2s-1 and the PPFD required for light saturation increased to approximately 500 µmol m-2s-1, while maximum rates of CO2 uptake increased only slightly. Light response curves of chamber-grown plants exhibited substantially lower compensation points and higher light-saturated rates of CO2 assimilation than field-grown material, due perhaps to a higher percentage of green, photosynthetically competent tissue. All three species exhibited broad responses to temperature, with optima near 20°C, and maintained at least 75% of maximum assimilation between approx. 13° and 30°C. Rates at 5°C were approx. 50% of maximum. Studies of the microclimate of Sphagnum at the field research site suggest that CO2 uptake should occur at near light-saturated rates during the day in open tussock tundra but that PPFD may often be limiting under Salix and Betula canopies in a water track drainage. Simulations using a simple model provided a seasonal estimate of 0.78 g dry weight (DW) of S. angustifolium produced from each initial g of photosynthetic tissue under willow canopies, assuming no water limitations. Although the simulation model suggests that production would be 66% higher in open tussock tundra, S. angustifolium is rarely found in this potentially more stressful habitat. To explain the relative abundance of Sphagnum in shaded water track areas as compared to open tussock tundra, we postulate that the vascular plant canopies provide protection from adverse effects of high temperatures, excess irradiance and reduced water availability. Under conditions of normal water availability, removal of the vascular plant cover did not affect the tissue water content of S. squarrosum, but resulted in a strong decrease in photosynthetic capacity, accompanied by chlorophyll bleaching. These results suggest that photoinhibition may limit production under certain conditions.

Seasonal changes in net photosynthesis rates and photosynthetic capacity in leaves of Cistus salvifolius, a European mediterranean semi-deciduous shrub.

During five different periods between Nov. 1982 and Aug. 1983, the diurnal patterns exhibited in photosynthetic CO2 uptake and stomatal conductance were observed under natural conditions on twigs of Cistus salvifolius, a Mediterranean semi-deciduous shrub which retains a significant proportion of its leaves through the summer drought. During the same periods, net photosynthesis at saturating CO2 partial pressure was measured on the same twigs as a function of irradiance at different temperatures. From these data, photosynthetic capacity, defined here as the CO2- and light-saturated net photosynthesis rate, was obtained as a function of leaf temperature. C. salvifolius is a winter growing species, shoot growth being initiated in Nov. and continuing through May. Photosynthetic capacity was quite high in Nov., March and June, exceeding 40 µmol m-2 s-1 at optimum temperature. In Dec., photosynthetic capacity was somewhat reduced, perhaps due to low night-time temperatures (<5°C) during the measurement period. In Aug., capacity in oversummering shoots at optimum temperature fell to less than 8 µmol m-2 s-1, due to water trees and perhaps leaf aging. Seasonal changes in maximal photosynthetic rates under ambient conditions were similar, and like those found in co-occurring evergreen sclerophylls. Like the evergreens, Cistus demonstrated considerable stomatal control of transpirational water loss, particularly in oversummering leaves. During each measurement period except Aug. when capacity was quite low, the maximum rates of net photosynthesis measured under ambient conditions were less than half the measured photosynthetic capacities at comparable temperatures, suggesting an apparent excess nitrogen investment in the photosynthetic apparatus.

Formation of false stems in Cymopterus longiopes: an uplifting example of growth form change.

The leaves of Cymopterus longipes form prostrate rosettes early in the spring. As the weather warms, these leaves are elevated on a pseudoscape (false stem) which develops below the rosette through the elongation of the caudex (in the region between root and shoot). The effect of this growth form change on the water relations and photosynthesis in C. longipes was investigated. Pseudoscape height was not linked to phenology or plant size. Leaf conductance, leaf temperature, and leaf water potential were notably similar between plants with different pseudoscape height growing in different microsites. Experimental manipulation of the microclimate around plants growing naturally allowed us to demonstrate that increased temperature led to an increase in the rate of pseudoscape elongation. By changing the distance above the ground surface of the rosettes of some plants we determined that leaf temperature, leaf to air vapour concentration deficits, leaf conductances, and leaf water potentials were all influenced by pseudoscape height. Leaf conductance in C. longipes had a strong negative relationship with ΔW. Since the temperature response of net photosynthesis was extremely flat it was concluded that pseudoscape elongation may be an important morphological means of increasing water use efficiency.

Use of an analytical model to study limitations on net photosynthesis in Arbutus unedo under field conditions.

From field gas-exchange measurements on Arbutus unedo growing in Portugal, parameter values necessary to apply an analytical, physiologicallybased model of C 3 photosynthesis were obtained. The model successfully simulated measured diurnal photosynthetic responses in Arbutus during periods without water stress, under both natural and CO2-saturating conditions. The model was used to analyze those factors limiting primary productivity during each of the experimental days. Due to a large investment in ribulose bisphosphate (RuBP) regeneration capacity, irradiance was rarely limiting, even during cloudy periods, but the limitation imposed by stomatal conductance was quite large, averaging over 30%. The fact that experimental leaves were maintained in a horizontal position is at least partially responsible for these results. Possible other reasons for this apparent excess of RuBP regeneration capacity visa-vis RuBP carboxylase-oxygenase concentration are discussed.

Interactive effects of light, leaf temperature, CO2 and O 2 on photosynthesis in soybean.

A biochemical model of C 3photosynthesis has been developed by G.D. Farquhar et al. (1980, Planta 149, 78-90) based on Michaelis-Menten kinetics of ribulose-1,5-bisphosphate (RuBP) carboxylase-oxygenase, with a potential RuBP limitation imposed via the Calvin cycle and rates of electron transport. The model presented here is slightly modified so that parameters may be estimated from whole-leaf gas-exchange measurements. Carbon-dioxide response curves of net photosynthesis obtained using soybean plants (Glycine max (L.) Merr.) at four partial pressures of oxygen and five leaf temperatures are presented, and a method for estimating the kinetic parameters of RuBP carboxylase-oxygenase, as manifested in vivo, is discussed. The kinetic parameters so obtained compare well with kinetic parameters obtained in vitro, and the model fits to the measured data give r (2)values ranging from 0.87 to 0.98. In addition, equations developed by J.D. Tenhunen et al. (1976, Oecologia 26, 89-100, 101-109) to describe the light and temperature responses of measured CO2-saturated photosynthetic rates are applied to data collected on soybean. Combining these equations with those describing the kinetics of RuBP carboxylase-oxygenase allows one to model successfully the interactive effects of incident irradiance, leaf temperature, CO2 and O2 on whole-leaf photosynthesis. This analytical model may become a useful tool for plant ecologists interested in comparing photosynthetic responses of different C3 plants or of a single species grown in contrasting environments.

Limitations due to water stress on leaf net photosynthesis of Quercus coccifera in the Portuguese evergreen scrub.

Gas exchange characteristics in leaves of the sclerophyll shrub Quercus coccifera were studied in the natural habitat in Portugal during spring and during the summer dry period. Compared to other sclerophyll species growing at the same site, photosynthesis in leaves of Quercus coccifera was less affected by water stress. Moderate water stress after six weeks of drought led to large decreases in stomatal conductance but no change in mesophyll photosynthetic capacity as compared to late spring. Leaf internal CO2 pressure remained near 220 µbar during diurnal courses in the spring. On midsummer days, leaf internal CO2 decreased from a late morning value of 200 µbar to a late afternoon value of approximately 150 µbar. In contrast to Quercus suber (Tenhunen et al. 1984), restriction of CO2 supply due to stomatal closure reduced net CO2 uptake at midday and in the afternoon during midsummer. A decrease in leaf carboxylation efficiency and an increase in CO2 compensation point at midday also played an important role in determining the diurnal course of net photosynthesis. During the late stages of drought in September, severe water stress led to reduction in mesophyll photosynthetic capacity and further reduction in leaf conductance. The observed decrease in mesophyll photosynthetic capacity was correlated with decrease in the daily minimum leaf water potential to greater negative values than-30 bar. At this time, CO2 saturated photosynthetic rates decreased as much as 50% over the course of a day when measured at constant saturating light, 32° C leaf temperature, and a water vapor mole fraction difference between leaf and air of 30 mbar bar-1.

The diurnal time course of net photosynthesis of soybean leaves: Analysis with a physiologically based steady-state photosynthesis model.

A physiologically based steady-state model of whole leaf photosynthesis (WHOLEPHOT) is used to analyze observed net photosynthesis daily time courses of soybean, Glycine max (L.) Merr., leaves. Observations during two time periods of the 1978 growing season are analyzed and compared. After adjustment of the model for soybean, net photosynthesis rates are calculated with the model in response to measured incident light intensity, leaf temperature, air carbon dioxide concentration, and leaf diffusion resistance. The steady-state calculations closely approximate observed net photosynthesis. Results of the comparison reveal a decrease in photosynthetic capacity in leaves sampled during the second time period, which is associated with decreasing ability of leaves to respond to light intensity and internal air space carbon dioxide concentration, increasing mesophyll resistance, and increasing stomatal resistance.