A mechanistic analysis of light and carbon use efficiencies

We explore the extent to which a simple mechanistic model of short-term plant carbon (C) dynamics can account for a number of generally observed plant phenomena. For an individual, fully expanded leaf, the model predicts that the fast-turnover labile C, starch and protein pools are driven into an approximate or moving steady state that is proportional to the average leaf absorbed irradiance on a time-scale of days to weeks, even under realistic variable light conditions, in qualitative agreement with general patterns of leaf acclimation to light observed both temporally within the growing season and spatially within plant canopies. When the fast-turnover pools throughout the whole plant (including stems and roots) also follow this moving steady state, the model predicts that the time-averaged whole-plant net primary productivity is proportional to the time-averaged canopy absorbed irradiance and to gross canopy photosynthesis, and thus suggests a mechanistic explanation of the observed approximate constancy of plant light-use efficiency (LUE) and carbon-use efficiency. Under variable light conditions, the fast-turnover pool sizes and the LUE are predicted to depend negatively on the coefficient of variation of irradiance. We also show that the LUE has a maximum with respect to the fraction of leaf labile C allocated to leaf protein synthesis ( a_lp ), reflecting a trade-off between leaf photosynthesis and leaf respiration. The optimal value of a_lp is predicted to decrease at elevated [CO₂] _a , suggesting an adaptive interpretation of leaf acclimation to CO₂. The model therefore brings together a number of empirical observations within a common mechanistic framework.     

The acquisition and accumulation of inorganic carbon by the unicellular green alga Chlorella ellipsoidea

Abstract. The uptake and accumulation of inorganic carbon has been investigated in Chlorella ellipsoidea cells grown at acid or alkaline pH. Carbonic anhydrase (CA) was detected in ceil extracts but not in intact cells and CA activity in acid-grown cells was considerably less than that in alkali-grown cells. Both cell types demonstrates low K_1/2 (CO₂) values in the range pH 7.0–8.0 and these were unaffected by O₂ concentration. The CO₂ compensation concentrations of acid- and alkali-grown cells suspended in aqueous media were not significantly different in the range of pH 6.0–8.0, but at pH 5.0, the CO₂ compensation concentrations of acid-grown cells (57.4cm³ m⁻³) were lower than those of alkali-grown cells (79.2cm³ m⁻³). The rate of photo-synthetic O₂ evolution in the range pH 7.5–8.0 exceeded the calculated rate of CO₂ supply two- to three-fold, in both acid- and alkali-grown cells, indicating that HCO₃⁻ was taken up by the cells. Accumulation of inorganic carbon was measured at pH 7.5 by silicone-oil centri-fugation, and the concentration of unfixed inorganic carbon was found to be 5.1 mol m⁻³ in acid-grown and 6.4mol m⁻³ in alkali-grown cells. These concentrations were 4.6- and 5.9-fold greater than in the external medium. These results indicate that photorespiration is suppressed in both acid- and alkali-grown cells by an intracellular accumulation of inorganic carbon due, in part, to an active uptake of bicarbonate.     

Photosynthetic inorganic carbon uptake and accumulation in two marine diatoms

Some physiological characteristics of photosynthetic inorganic carbon uptake have been examined in the marine diatoms Phaeodactylum tricornutum and Cyclotella sp. Both species demonstrated a high affinity for inorganic carbon in photosynthesis at pH7.5, having K_1/2(CO₂) in the range 1.0 to 4.0mmol m^?3 and O_2? and temperature-insensitive CO₂ compensation concentrations in the range 10.8 to 17.6 cm³ m^?3. Intracellular accumulation of inorganic carbon was found to occur in the light; at an external pH of 7.5 the concentration in P. tricornutum was twice, and that in Cyclotella 3.5 times, the concentration in the suspending medium. Carbonic anhydrase (CA) was detected in intact Cyclotella cells but not in P. tricornutum, although internal CA was detected in both species. The rates of photosynthesis at pH 8.0 of P. tricornutum cells and Cyclotella cells treated with 0.1 mol m^?3 acetazolamide, a CA inhibitor, were 1.5- to 5-fold the rate of CO₂ supply, indicating that both species have the capacity to take up HCO₃^? as a source of substrate for photosynthesis. No Na⁺ dependence for HCO₃^? could be detected in either species. These results indicate that these two marine diatoms have the capacity to accumulate inorganic carbon in the light as a consequence, in part, of the active uptake of bicarbonate.     

Interdependence of CO2 and inorganic nitrogen on crassulacean acid metabolism and efficiency of nitrogen use by Littorella uniflora (L.) Aschers

The hypothesis is tested that crassulacean acid metabolism (CAM) in isoetids is a mechanism which not only conserves inorganic carbon but also plays a role in nitrogen economy of the plants. This hypothesis was tested in an outdoor experiment, where Littorella uniflora (L.) Aschers. were grown at two CO₂ and five inorganic nitrogen concentrations in a crossed factorial design. The growth of Littorella responded positively to enhanced nitrogen availability at high but not at low CO₂ indicating that growth was limited by nitrogen at high CO₂ only. For the nitrogen-limited plants, the capacity for CAM (CAM_cap) increased with the degree of nitrogen limitation of growth and an inverse coupling between CAM and tissue-N was found. Although this might indicate a role of CAM in economizing on nitrogen in Littorella , the hypothesis was rejected for the following reasons: (1) although CAM_cap was related to tissue-N no relationship between tissue-N and ambient CAM activity (CAM_ambient) was found whereas a close relationship would be expected if CAM was regulated by nitrogen availability; (2) the photosynthetic nitrogen use efficiency for high CO₂-grown plants declined with increased CAM_ambient and with CAM_cap; and (3) growth per unit tissue-N per unit time declined with increased CAM_ambient and CAM_cap.     

Photosynthetic inorganic carbon utilization and growth of Porphyra linearis (Rhodophyta)

Photosynthetic (oxygen evolution) and growth (biomass increase) responses to ambient pH and inorganic carbon (Ci) supply were determined for Porphyralinearis grown in 0.5 L glass cylinders in the laboratory, or in 40 L fibreglass outdoor tanks with running seawater. While net photosynthetic rates were uniform at pH 6.0–8.0, dropping only at pH 8.7, growth rates were significantly affected by pH levels other than that of seawater (c. pH 8.3). In glass cylinders, weekly growth rates averaged 76% at external pH 8.0, 13% at pH 8.7 and 26% at pH 7.0. Photosynthetic O₂ evolution on a daily basis(i.e. total O₂ evolved during day time less total O₂ consumed during night time) was similar to the growth responses at all experimental pH levels, apparently due to high dark respiration rates measured at acidic pH. Weekly growth rates averaged 53% in algae grown in fibreglass tanks aerated with regular air (360 mg L_-1 CO₂) and 28% in algae grown in tanks aerated with CO₂-enriched air (750 mg L^-1 CO₂). The pH of the seawater medium in which P. linear is was grown increased slightly during the day and only rarely reached 9.0. The pH at the boundary layer of algae submerged in seawater increased in response to light reaching, about pH 8.9 within minutes, or remained unchanged for algae submerged in a CO₂-free artificial sea water medium. Photosynthesis of P. linearissaturated at Ci concentrations of seawater (K_0.5560 μM at pH 8.2) and showed low photosynthetic affinity for CO₂(K_0.5 61 μM) at pH 6.0. It is therefore concluded that P. linearisuses primarily CO₂ with HCO₃ ^- being an alternative source of Ci for photosynthesis. Its fast growth could be related to the enzyme carbonic anhydrase whose activity was detected intra- and extracellularly. This revised version was published online in August 2006 with corrections to the Cover Date.     

Interactions of blue light and inorganic carbon supply in the control of light-saturated photosynthesis in brown algae

Photosynthetic capacities of five species of brown algae in red light were found to be strongly limited by the inorganic carbon supply of natural sea water. Under these conditions, pH 8·2 and dissolved inorganic carbon concentration (DIG) of 2·1 mol m^?3, a short pulse of blue light was found to increase the subsequent rate of photosynthesis in saturating red light. The degree of blue light stimulation varied between species, ranging from an increase of over 200% of the original rate in Colpomenia peregrins to only 10% in Dictyota dichotoma. Increasing the DIG concentration of sea water by bicarbonate addition resulted in carbon saturation of photosynthesis in all five species. Blue light stimulation was greatly reduced at these higher DIG concentrations. The response in Laminaria digitata was examined in more detail by manipulation of pH and DIG to produce solutions with different concentrations of dissolved CO₂. At a CO₂ concentration typical of normal sea water (12·4 mmol m^?3), blue light treatment increased photosynthetic rate by approximately 50%. Blue light stimulation was increased to over 150% at CO₂ concentrations below that of sea water, whereas at concentrations above that of sea water, the effect was diminished. Therefore, the effect of blue light on photosynthetic capacity appears to involve an increase in the rate of supply of carbon dioxide to the plant.     

Pelagic and benthic net production of dissolved inorganic carbon in an unproductive subarctic lake

1. Both the pelagic and benthic net dissolved inorganic carbon (DIC) productions were measured in situ on four occasions from June to September 2004, in the unproductive Lake Diktar-Erik in subarctic Sweden. The stable isotopic signal ( δ ¹³C) of respired organic material was estimated from hypolimnion water data and data from a laboratory incubation using epilimnion water.
2. Both pelagic and benthic habitats were net heterotrophic during the study period, with a total net DIC production of 416 mg C m⁻² day⁻¹, of which the pelagic habitat contributed approximately 85%. The net DIC production decreased with depth both in the pelagic water and in the sediments, and most of the net DIC production occurred in the upper water column.
3. Temporal variations in both pelagic and benthic DIC production were small, although we observed a significant decrease in pelagic net DIC production after the autumn turnover. Water temperature was the single most important factor explaining temporal and vertical variations in pelagic DIC production. No single factor explained more than 10% of the benthic net DIC production, which probably was regulated by several interacting factors.
4. Pelagic DIC production, and thus most of the whole-lake net production of DIC, was mainly due to the respiration of allochthonous organic carbon. Stable isotope data inferred that nearly 100% of accumulated DIC in the hypolimnion water had an allochthonous carbon source. Similarly, in the laboratory incubation using epilimnion water, c. 85% of accumulated DIC was indicated to have an allochthonous organic carbon source.     

Respiration as a percentage of daily photosynthesis in whole plants is homeostatic at moderate, but not high, growth temperatures

Here, we investigated the impact of temperature on the carbon economy of two Plantago species from contrasting habitats. The lowland Plantago major and the alpine Plantago euryphylla were grown hydroponically at three constant temperatures: 13, 20 and 27 degrees C. Rates of photosynthetic CO(2) uptake (P) and respiratory CO(2) release (R) in shoots and R in roots were measured at the growth temperature using intact plants. At each growth temperature, air temperatures were changed to establish short-term temperature effects on the ratio of R to P (R/P). In both species, R/P was essentially constant in plants grown at 13 and 20 degrees C. However, R/P was substantially greater in 27 degrees C-grown plants, particularly in P. euryphylla. The increase in R/P at 27 degrees C would have been even greater had biomass allocation to roots not decreased with increasing growth temperature. Short-term increases in air temperature increased R/P in both species, with the effects of air temperature being most pronounced in 13 degrees C-grown plants. We conclude that temperature-mediated changes in biomass allocation play an important role in determining whole-plant R/P values, and, while homeostasis of R/P is achieved across moderate growth temperatures, homeostasis is not maintained when plants are exposed to growth temperatures higher than usually experienced in the natural habitat.     

The effects of increased atmospheric carbon dioxide and temperature on carbon partitioning, source-sink relations and respiration

Abstract. Herbaceous C₃ plants grown in elevated CO₂ show increases in carbon assimilation and carbohydrate accumulation (particularly starch) within source leaves. Although changes in the partitioning of biomass between root and shoot occur, the proportion of this extra assimilate made available for sink growth is not known. Root:shoot ratios tend to increase for CO₂-enriched herbaceous plants and decrease for CO₂-enriched trees. Root:shoot ratios for cereals tend to remain constant. In contrast, elevated temperatures decrease carbohydrate accumulation within source and sink regions of a plant and decrease root:shoot ratios. Allometric analysis of at least two species showing changes in root: shoot ratios due to elevated CO₂ show no alteration in the whole-plant partitioning of biomass. Little information is available for interactions between temperature and CO₂. Cold-adapted plants show little response to elevated levels of CO₂, with some species showing a decline in biomass accumulation. In general though, increasing temperature will increase sucrose synthesis, transport and utilization for CO₂-enriched plants and decrease carbohydrate accumulation within the leaf. Literature reports are discussed in relation to the hypothesis that sucrose is a major factor in the control of plant carbon partitioning. A model is presented in support.     

A stable carbon isotope study of dissolved inorganic carbon cycling in a softwater lake

The dissolved inorganic carbon (DIC) cycle in a softwater lake was studied using natural variations of the stable isotopes of carbon,¹²C and¹³C. During summer stratification there was a progressive decrease in epilimnion DIC concentration with a concomitant increase in ¹³C_DIC), due to preferential uptake of¹²C by phytoplankton and a change in the dominant CO₂ source from inflow andin situ oxidation to invasion from the atmosphere. There was an increase in hypolimnion DIC concentration throughout summer with a concomitant general decrease in ¹³C_DIC from oxidation of the isotopically light particulate organic carbon that sank down through the thermocline from the epilimnion.Mass balance calculations of DI¹²C and DI¹³C in the epilimnion for the summer (June 23–September 25) yield a mean rate of net conversion of DIC to organic carbon (C_org) of 430 ± 150 moles d^-1 (6.5 ± 1.8 m moles m^-2 d^-1. Net CO₂ invasion from the atmosphere was 420 ± 120 moles d^-1 (6.2 ± 1.8 m moles m^-2 d^-1) with an exchange coefficient of 0.6 ± 0.3m d^-1. These results imply that at least for the summer months the phytoplankton obtained about 90% of their carbon from atmosphere CO₂. About 50% of CO₂ invasion and conversion to C_org for the summer occurred during a two week interval in mid-summer.DIC concentration increased in the hypolimnion at a rate of 350 ± 70 moles DIC d^-1 during summer stratification. The amount of DIC added to the hypolimnion was equivalent to 75 ± 20% of net conversion of DIC to C_org in the euphotic zone over spring and summer implying rapid degradation of POC in the hypolimnion. The ¹³C of DIC added to the deep water (-22.) was too heavy to have been derived from oxidation of particulate organic carbon alone. About 20% of the added DIC must have diffused from hypolimnetic sediments where relatively heavy CO₂ (-7) was produced by a combination of POC oxidation and as a by-product of methanogenesis.     

The effect of different growth conditions on dark and light carbon assimilation in Littorella uniflora

The effect of long-term exposure to different inorganic carbon, nutrient and light regimes on CAM activity and photosynthetic performance in the submerged aquatic plant, Littorella uniflora (L.) Aschers was investigated. The potential CAM activity of Littorella was highly plastic and was reduced upon exposure to low light intensities (43 μmol m⁻² s⁻¹), high CO₂ concentrations (5.5 mM, pH 6.0) or low levels of inorganic nutrients, which caused a 25–80% decline in the potential maximum CAM activity relative to the activity in the control experiments (light: 450 μmol m⁻² s⁻¹; free CO₂: 1.5 mM). The CAM activity was regulated more by light than by CO₂, while nutrient levels only affected the activity to a minor extent. The minor effect of low nutrient regimes may be due to a general adaptation of isoetid species to low nutrient levels.
The photosynthetic capacity and CO₂ affinity was unaffected or increased by exposure to low CO₂, irrespective of nutrient levels. High CO₂, low nutrient and low light, however, reduced the capacity by 22–40% and the CO₂ affinity by 35-45%, relative to control.
The parallel effect of growth conditions on CAM activity and photosynthetic performance of Littorella suggest that light and dark carbon assimilation are interrelated and constitute an integrated part of the carbon assimilation physiology of the plant. The results are consistent with the hypothesis that CAM is a carbon-conserving mechanism in certain aquatic plants. The investment in the CAM enzyme system is beneficial to the plants during growth at high light and low CO₂ conditions.     

Photosynthesis and carbon balance of a Sahelian fallow savanna

Eddy-covariance measurements of CO₂ exchange above a Sahelian savanna consisting of small shrubs over a near-continuous herb layer were made during the HAPEX-Sahel experiment in Niger, West Africa. The measurements were made near-continuously during an 8-week period, covering the main part of the rainy season and three weeks at the beginning of the dry season. The measurements were corrected for in-canopy storage of CO₂ and the night-time measurements used to derive respiration functions for the soil, roots and above-ground plant material. Photosynthetic CO₂ uptake was estimated and compared to simulations using a biochemical photosynthesis model in a simple, ‘big-leaf’, implementation. The model satisfactorily reproduced the measurements (coefficient of determination 0.80) using parameters defined from the literature and based on soil nutrient concentrations. When the quantum yield (α) and rubisco capacity (V_mr) were fitted to the data with allowance for physiological changes through the season, an excellent agreement between model and measurements was obtained (coefficient of determination 0.93, RMS error 1.46 μmol m^–2 s^–1). The fitted photosynthesis and respiration model was used to estimate the carbon balance of the savanna site during the growing season of 1992 and for the complete calendar year. Harvest estimates of net plant biomass accumulation during the growing season and annual wood accumulation agreed well with modelled net photosynthesis and annual net carbon accumulation, respectively. Peak instantaneous ecosystem CO₂ uptake was comparable to peak values observed in other biomes, but annual photosynthesis and carbon sequestration were considerably lower than observed elsewhere.     

Photosynthetic use of light and inorganic carbon in air and water by the intertidal alga Petalonia fascia (Scytosiphonales, Phaeophyta)

The photosynthetic performance of the intertidal alga Petalonia fascia (0. F. Muller) Kuntze (Scytosiphona-ceae, Phaeophyta) has been investigated, both in air and water, by analyzing the relationship between apparent photosynthesis rate and photon irradiance and inorganic carbon. In relation to the use of photon irradiance, it was found that the net photosynthetic capacity in water was 5.7 times that in air (fully hydrated thallus). The light compensation point was achieved at 5.9 and 3.0 μmol photons m^?2 s^?1 in air and water, respectively. The light onset-saturation parameter and the photosynthetic efficiency were 77% and 25% greater in water than in air, respectively. The dark respiration rate was one-third greater when emersed in comparison to submersion conditions. These data suggest that the photosynthetic response to irradiance in P. fascia is similar to that in infralittoral species rather than the intertidal species. This assessment can be explained by the winter seasonality of the bladed stage of growth, when storms and waves permit a permanent hydrated status of P. fascia that in the intertidal zone. Moreover, the minimum tissue water content that permitted active photosynthesis in the alga was around 20%. The net photosynthetic capacity as a function of inorganic carbon (C) concentration in water was 1.5 times that in air. Photosynthesis was saturated in both media with respect to the availability of inorganic C in natural conditions. The affinity to inorganic C, and the carbon conductance, were two orders of magnitude higher in air than in water. However, the higher photosynthetic capacity when submerged in comparison to emersion conditions suggests that P. fascia can assimilate the external HCO₃,– or the occurrence of a CO₂ concentrating mechanism in this species.     

Interactive effects of elevated carbon dioxide and growth temperature on photosynthesis in cotton leaves

Cotton (Gossypium hirsutum L., cv DPL 5415) plants were grown in naturally lit environment chambers at day/night temperature regimes of 26/18 (T-26/18), 31/23 (T-31/23) and 36/28 °C (T-36/28) and CO2 concentrations of 350 (C-350), 450 (C-450) and 700 L L-1 (C-700). Net photosynthesis rates, stomatal conductance, transpiration, RuBP carboxylase activity and the foliar contents of starch and sucrose were measured during different growth stages. Net CO2 assimilation rates increased with increasing CO2 and temperature regimes. The enhancement of photosynthesis was from 24 mol CO2 m-2 s-1 (with C-350 and T-26/18) to 41 mol m-2 s-1 (with C-700 and T-36/28). Stomatal conductance decreased with increasing CO2 while it increased up to T-31/23 and then declined. The interactive effects of CO2 and temperature resulted in a 30% decrease in transpiration. Although the leaves grown in elevated CO2 had high starch and sucrose concentrations, their content decreased with increasing temperature. Increasing temperature from T-26/18 to 36/28 increased RuBP carboxylase activity in the order of 121, 172 and 190 mol mg-1 chl h-1 at C-350, C-450 and C-700 respectively. Our data suggest that leaf photosynthesis in cotton benefited more from CO_2 enrichment at warm temperatures than at low growth temperature regimes.