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.     

Gas exchange parameters, water relations and carbohydrate partitioning in leaves of field-grown Prunus domestica following fruit removal

The effect of fruit removal on gas exchange, water relations, chlorophyll and non-structural carbohydrate content of leaves from mature, field-grown plum trees ( Prunus domestica L. cv. Stanley) was determined over 2 consecutive growing seasons. Removal of fruits during stage II of fruit development decreased CO₂ assimilation rate within 24 h from 12.6 to 8.5 μmol m^-2 s^-1 in 1986, and from 12.1 to 10.2 μmol m^-2 s^-1 in 1987. Depression of net photosynthesis persisted for at least 5 days and was greatest in the early afternoon. Recovery of the CO₂ assimilation rate to pretreatment levels coincided in defruited trees with vegetative growth that was more than 5-fold that of fruiting trees in the first 6 weeks after fruit removal in 1986. Estimated photorespiration was similar in both fruiting and defruited trees. The stomatal contribution to the decrease of CO₂ assimilation rate, calculated from assimilation/intercellular CO₂ curves, ranged from 31 to 46%. Defruiting did not affect leaf water potential, but decreased leaf osmotic potential. Leaf levels of chlorophyll, fructose, glucose, sorbitol and sucrose were not affected by defruiting, whereas starch content increased up to 51% in leaves of defruited trees within 24 h after fruit removal. However, because of the small starch pool present in plum leaves (<1.9% dry weight) it is unlikely that starch accumulation was responsible for the observed decline in CO₂ assimilation rate after fruit removal. The decrease of CO₂ assimilation rate is discussed in relation to the hypothesis of assimilate demand regulating photosynthesis through a feedback mechanism.     

Application of transgenic plants in understanding responses to atmospheric change

Acclimation of plants to an increase in atmospheric carbon dioxide concentration is a well described phenomenon. It is characterized by an increase in leaf carbohydrates and a degradation of ribulose 1, 5-bisphosphate carboxylase protein (Rubisco) leading in the long term to a lower rate of CO₂ assimilation than expected from the kinetic constants of Rubisco. This article summarizes studies with transgenic plants grown in elevated pCO₂ which are modified in their capacity of CO₂ fixation, of sucrose and starch synthesis, of triosephosphate and sucrose transport and of sink metabolism of sucrose. These studies show that a feedback accumulation of carbohydrates in leaves play only a minor role in acclimation, because leaf starch synthesis functions as an efficient buffer for photoassimilates. There is some evidence that in elevated pCO₂, plants grow faster and senescence is induced earlier.     

Adjustments of net photosynthesis in Solanum tuberosum in response to reciprocal changes in ambient and elevated growth CO2 partial pressures

Single leaf photosynthetic rates and various leaf components of potato ( Solanum tuberosum L.) were studied 1–3 days after reciprocally transferring plants between the ambient and elevated growth CO₂ treatments. Plants were raised from individual tuber sections in controlled environment chambers at either ambient (36 Pa) or elevated (72 Pa) CO₂. One half of the plants in each growth CO₂ treatment were transferred to the opposite CO₂ treatment 34 days after sowing (DAS). Net photosynthesis (P_n) rates and various leaf components were then measured 34, 35 and 37 DAS at both 36 and 72 Pa CO₂. Three-day means of single leaf P_n rates, leaf starch, glucose, initial and total Rubisco activity, Rubisco protein, chlorophyll ( a + b ), chlorophyll ( a/b ), α -amino N, and nitrate levels differed significantly in the continuous ambient and elevated CO₂ treatments. Acclimation of single leaf P_n rates was partially to completely reversed 3 days after elevated CO₂-grown plants were shifted to ambient CO₂, whereas there was little evidence of photosynthetic acclimation 3 days after ambient CO₂-grown plants were shifted to elevated CO₂. In a four-way comparison of the 36, 72, 36 to 72 (shifted up) and 72 to 36 (shifted down) Pa CO₂ treatments 37 DAS, leaf starch, soluble carbohydrates, Rubisco protein and nitrate were the only photosynthetic factors that differed significantly. Simple and multiple regression analyses suggested that negative changes of P_n in response to growth CO₂ treatment were most closely correlated with increased leaf starch levels.     

Comparative studies of sucrose and mannitol utilization in celery (Apium graveolens)

Utilization of sucrose and mannitol, the major forms of translocatable assimilate in celery ( Apium graveolens L. cv. Giant Pascal), was investigated in intact plants, excised leaves and leaf discs by estimating the soluble carbohydrate pools, starch levels and oxidation of [¹⁴C]-sucrose or mannitol in the light and after extended dark treatments. In detached mature fully-expanded leaves, mannitol pools remained constant, while sucrose decreased during a 48 h dark treatment. In attached leaves on plants trimmed to a single compound leaf, however, mannitol levels decreased after a dark treatment. In leaf discs floated on bathing solutions containing [¹⁴C]-sucrose or [¹⁴C]-mannitol, oxidation of mannitol was restricted to young leaf tissues, whereas sucrose was metabolized to CO₂ regardless of leaf age. Uptake of labelled mannitol, however, was greater than that of sucrose in the light in leaves of every age. Although both mannitol and sucrose are translocated out of leaf tissues, leaf age differences indicate that, unlike sucrose, mannitol utilization is restricted to active sink tissues. The results suggest different roles for mannitol and sucrose with mannitol representing a more rigorously sequestered transport carbohydrate.     

Effects of manganese toxicity on photosynthesis of white birch (Betula platyphylla var. japonica) seedlings

The effects of manganese (Mn) toxicity on photosynthesis in white birch ( Betula platyphylla var. japonica ) leaves were examined by the measurement of gas exchange and chlorophyll fluorescence in hydroponically cultured plants. The net photosynthetic rate at saturating light and ambient CO₂ (C_a) of 35 Pa decreased with increasing leaf Mn concentrations. The carboxylation efficiency, derived from the difference in CO₂ assimilation rate at intercellular CO₂ pressures attained at C_a of 13 Pa and O Pa, decreased with greater leaf Mn accumulation. Net photosynthetic rate at saturating light and saturating CO₂ (5%) also declined with leaf Mn accumulation while the maximum quantum yield of O₂ evolution at saturating CO₂ was not affected. The maximum efficiency of PSII photochemistry (F_v/F_m) was little affected by Mn accumulation in white birch leaves over a wide range of leaf Mn concentrations (2–17 mg g₋₁ dry weight). When measured in the steady state of photosynthesis under ambient air at 430 μmol quanta m₋₂ s₋₁, the levels of photochemical quenching (qP) and the excitation capture efficiency of open PSII (F'^v/F'^m) declined with Mn accumulation in leaves. The present results suggest that excess Mn in leaves affects the activities of the CO² reduction cycle rather than the potential efficiency of photochemistry, leading to increases in Q_A reduction state and thermal energy dissipation, and a decrease in quantum yield of PSII in the steady state.     

δ 13C of CO2 respired in the dark in relation to δ13C of leaf carbohydrates in Phaseolus vulgaris L. under progressive drought

The variations in δ ¹³C in both leaf carbohydrates (starch and sucrose) and CO₂ respired in the dark from the cotyledonary leaves of Phaseolus vulgaris L. were investigated during a progressive drought. As expected, sucrose and starch became heavier (enriched in ¹³C) with decreasing stomatal conductance and decreasing p _i/ p _a during the first half (15 d) of the dehydration cycle. Thereafter, when stomata remained closed and leaf net photosynthesis was near zero, the tendency was reversed: the carbohydrates became lighter (depleted in ¹³C). This may be explained by increased p _i/ p _a but other possible explanations are also discussed. Interestingly, the variations in δ ¹³C of CO₂ respired in the dark were correlated with those of sucrose for both well-watered and dehydrated plants. A linear relationship was obtained between δ ¹³C of CO₂ respired in the dark and sucrose, respired CO₂ always being enriched in ¹³C compared with sucrose by ≈ 6‰. The whole leaf organic matter was depleted in ¹³C compared with leaf carbohydrates by at least 1‰. These results suggest that: (i) a discrimination by ≈ 6‰ occurs during dark respiration processes releasing ¹³C-enriched CO₂; and that (ii) this leads to ¹³C depletion in the remaining leaf material.     

Effect of elevated CO2, temperature and drought on photosynthesis of nodulated alfalfa during a cutting regrowth cycle

Rising atmospheric CO₂ may increase potential net leaf photosynthesis under short-term exposure, but this response decreases under long-term exposure because plants acclimate to elevated CO₂ concentrations through a process known as downregulation. One of the main factors that may influence this phenomenon is the balance between sources and sinks in the plant. The usual method of managing a forage legume like alfalfa requires the cutting of shoots and subsequent regrowth, which alters the source/sink ratio and thus photosynthetic behaviour. The aim of this study was to determine the effect of CO₂ (ambient, around 350 vs. 700 µmol mol⁻¹), temperature (ambient vs. ambient + 4° C) and water availability (well-irrigated vs. partially irrigated) on photosynthetic behaviour in nodulated alfalfa before defoliation and after 1 month of regrowth. At the end of vegetative normal growth, plants grown under conditions of elevated CO₂ showed photosynthetic acclimation with lower photosynthetic rates, V_cmax and ribulose-1,5-bisphosphate carboxylase/oxygenase (rubisco) activity. This decay was probably a consequence of a specific rubisco protein reduction and/or inactivation. In contrast, high CO₂ during regrowth did not change net photosynthetic rates or yield differences in V_cmax or rubisco total activity. This absence of photosynthetic acclimation was directly associated with the new source-sink status of the plants during regrowth. After cutting, the higher root/shoot ratio in plants and remaining respiration can function as a strong sink for photosynthates, avoiding leaf sugar accumulation, the negative feed-back control of photosynthesis, and as a consequence, photosynthetic downregulation.     

Carbohydrate metabolism enzymes in CO2-enriched developing rice grains of cultivars varying in grain size

The increased supply of photosynthate from maternal tissue is known to promote grain growth in several crop species. However, the effect of increasing photosynthate supply on grain growth receives little attention in rice. This study was aimed at evaluating the effect of increasing photosynthate supply through CO₂ enrichment (650 μl I_-1) on grain growth in three rice cultivars differing in grain size. CO₂ enrichment was applied to the pot-grown plants between anthesis and final harvest. The results indicated that high CO₂ treatment enhanced the CO₂ exchange rate of leaf tissue, and subsequently increased the sucrose level of peduncle exudate, but it did not promote starch accumulation in the developing grains. This phenomenon was linked to the poor CO₂ responses for the grain activities of sucrose synthase, UDP-glucose pyrophosphorylase. ADP-glucose pyrophosphorylase, and starch synthases involved in the conversion of sucrose to starch. Significant cultivar differences also existed for the activities of sucrose to starch conversion enzymes with larger grain size cultivars tending to have higher enzymes activities (expressed on a grain basis), resulting in a greater carbohydrate accumulation.     

Assimilate relations in source and sink leaves during acclimation to a CO2-enriched atmosphere

Evidence from previous studies suggested that adjustments in assimilate formation and partitioning in leaves might occur over time when plants are exposed to enriched atmospheric CO₂. We examined assimilate relations of source (primary unifoliolate) and developing sink (second mainstem trifoliolate) leaves of soybean [ Glycine max (L.) Merr. cv. Lee] plants for 12 days after transfer from a control (350 μl l⁻¹) to a high (700 μ l⁻¹) CO₂ environment. Similar responses were evident in the two leaf types. Net CO₂ exchange rate (CER) immediately increased and remained elevated in high CO₂. Initially, the additional assimilate at high CO₂ levels in the light and was utilized in the subsequent dark period. After approximately 7 days, assimilate export in the light began to increase and by 12 days reached rates 3 to 5 times that of the control. In the developing sink leaf, high rates of export in the light occurred as the leaf approached full expansion. The results indicate that a specific acclimation process occurs in source leaves which increases the capacity for assimilate export in the light phase of the diurnal cycle as plants adjust to enriched CO₂ and a more rapid growth rate.     

Comparison of the effect of rapidly and gradually developing water-stress on carbohydrate metabolism in spinach leaves

Abstract. The effect of water-stress on photosynthetic carbon metabolism in spinach ( Spinacia oleracea L.) has been studied in experiments in which water-stress was induced rapidly by floating leaf discs on sorbitol solutions or wilting detached leaves, and in experiments in which water-stress was allowed to develop gradually in whole plants as the soil dried out. In both short- and long-term water stress, the rate of photosynthesis in saturating CO₂ did not decrease until leaf water potential decreased below -1.0 MPa. However, at smaller water deficits there was already an inhibition of starch synthesis, while sucrose synthesis remained constant or increased. This change in partitioning was accompanied by an increase in activation of sucrose-phosphate synthase (revealed as an increase in activity assayed in the presence of low hexose-phosphate and inorganic phosphate, while the activity assayed with saturating hexosephosphates remained unaltered). Water-stressed leaves had a two- to three-fold higher sucrose content at the end of the night, and contained less starch than non-stressed leaves. When leaves were held in the dark, sucrose was mobilized initially, while starch was not mobilized until the sucrose had decreased to a low level; in water-stressed leaves, starch mobilization commenced at a two-fold higher sucrose content. It is concluded that water-stressed leaves maintain higher sucrose and lower starch levels than non-stressed leaves. This response is found in rapid and long-term stress, and represents an inherent response to water deficits.     

Gas exchange measurements required to predict the newly fixed carbon pool size in a source leaf of corn (Zea mays L.)

Abstract. Steady-state photosynthesis (P_n), post-illumination CO₂ release rates (R), sucrose-phosphate synthase (SPS) activities, and levels of starch, sucrose and hexoses were measured in the source leaf of corn ( Zea mays L.) during a 16-h photoperiod at 800 μmol m ² s ¹. P_n and SPS activity remained constant. Carbohydrate pools increased at a linear rate, except the first and last hour of the photoperiod. Both the CO₂ evolution rate at the moment of light removal (R_max) and SPS activity decreased by one half after the onset of darkness (0 60 min). Sucrose diminished during this period by 40%, whereas the starch remained constant. Thereafter, starch mobilization began, followed by a gradual decline in leaf respiration. The average dark export rate was calculated to be 60% less than that during the day. Maintenance respiration (R_m) of an attached leaf after 48 h darkness was determined. Plants were illuminated for different intervals (e.g. 5, 10 or 20 min), each followed by dark periods sufficient for respiration to decline to R_m. The ratio of C assimilated in light to that released in dark was 6:1. After the 48-h dark period, the minimal period of illumination (T_min) required to restore P_n and R_max to the original level was determined. A mathematical analysis of the kinetics involved in the recovery of P_n and R_max provided an estimate of turnover time (0.22h) and pool size 9.15 mmol m ²) for the newly fixed carbon.     

Effects of cadmium on growth of Helianthus annuus seedlings: physiological aspects

Sunflower seedlings ( Helianthus annuus hybrid Select) were grown in a complete nutrient solution in the absence or presence of Cd²⁺ (10 and 20 μM). Analyses were performed to establish whether there was a differential effect of Cd²⁺ on mature and young leaves. After 7 d the growth parameters as well as the leaf area had decreased in both mature and young leaves. Accumulation of Cd²⁺ in the roots exceeded that in the shoots. Seedlings treated with Cd²⁺ exhibited reduced contents of chlorophyll and CO₂ assimilation rate, with a greater decrease in young leaves. The photochemical efficiency of photosystem II (PSII) was not altered by Cd²⁺ treatment in either mature or young leaves, although during steady-state photosynthesis in young leaves there was a significant alteration in the following parameters: quantum yield of electron transport by PSII (Φ_PSII), photochemical quenching ( q _P), non-photochemical quenching ( q _NP), and excitation capture efficiency of PSII (Φ_exc).     

Defoliation effects on mycorrhizal colonization, nitrogen fixation and photosynthesis in the Glycine-Glomus-Rhizobium symbiosis

Soybean [ Glycine max (L.) Merr. cv. Wells] plants grown in a greenhouse were inoculated with Rhizobium japonicum strain 61A118 and the vesicular-arbuscular mycorrhizal (VAM) fungus Glomus fasciculatum (Thaxt. sensu Gerd.) Gerd. & Trappe. Plants were defoliated (26, 48 and 66%) throughout the growth period and evaluated for VAM colonization, N₂, fixation and photosynthesis at harvest (six weeks). Photosynthate stress as a result of defoliation affected nodulation and nodule activity most severely. Colonization of the roots by the VAM fungus was little affected in comparison, and the intensity of colonization increased with increasing stress. The CO₂-exchange rate decreased less with defoliation than did leaf mass, and photosynthetic efficiency increased with the severity of defoliation. The increase in photosynthetic efficiency was significantly correlated with increases in leaf P (r = 0.91) and N (r = 0.97) concentrations. The results suggest that the VAM fungus should not be regarded as a simple P source and C sink in the tripartite legume association. Threeway source/sink relationships (VAM-P, Rhizobium-N, and host leaf-C) are discussed.     

How does the C4 grass Eragrostis pilosa respond to elevated carbon dioxide and infection with the parasitic angiosperm Striga hermonthica?

Eragrostis pilosa (Linn.) P Beauv., a C₄ grass native to east Africa, was grown at both ambient (350 μmol mol⁻¹ and elevated (700 μmol mol⁻¹) CO₂ in either the presence or absence of the obligate, root hemi-parasite Striga hermonthica (Del.) Benth. Biomass of infected grasses was only 50% that of uninfected grasses at both CO₂ concentrations, with stems and reproductive tissues of infected plants being most severely affected. By contrast, CO₂ concentration had no effect on growth of E. pilosa , although rates of photosynthesis were enhanced by 30–40% at elevated CO₂. Infection with S. hermonthica did not affect either rates of photosynthesis or leaf areas of E. pilosa , but did bring about an increase in root:shoot ratio, leaf nitrogen and phosphorus concentration and a decline in leaf starch concentration at both ambient and elevated CO₂. Striga hermonthica had higher rates of photosynthesis and shoot concentrations of soluble sugars at elevated CO₂, but there was no difference in biomass relative to ambient grown plants. Both infection and growth at elevated CO₂ resulted in an increase in the Δ¹³C value of leaf tissue of E. pilosa , with the CO₂ effect being greater. The proportion of host-derived carbon in parasite tissue, as determined from δ¹³C values, was 27% and 39% in ambient and elevated CO₂ grown plants, respectively. In conclusion, infection with S. hermonthica limited growth of E. pilosa , and this limitation was not removed or alleviated by growing the association at elevated CO₂.     

Photosynthate supply and utilization in alfalfa : a developmental shift from a source to a sink limitation of photosynthesis

Long-term carbon dioxide enrichment, ¹⁴CO₂ feeding, and partial defoliation were employed as probes to investigate source/sink limitations of photosynthesis during the development of symbiotically grown alfalfa. In the mature crop, long-term CO₂ enrichment does not affect the rates of net photosynthesis, relative growth, ¹⁴C export to nonphotosynthetic organs, or the rates of ¹⁴C label incorporation into leaf sucrose, starch, or malate. The rate of glycolate labeling is, however, substantially reduced under these conditions. When the mature crop was partially defoliated, a considerable increase in net photosynthesis occurred in the remaining leaves. In the seedling crop, long-term CO₂ enrichment increased dry matter accumulation, primarily as a result of increases in leaf starch content. Although the higher rates of starch synthesis are not maintained, the growth enhancement of the enriched plants persisted throughout the experimental period. These results imply a source limitation of seedling photosynthesis and a sink limitation of photosynthesis in more mature plants. Consequently, both the supply and the utilization of photosynthate may limit seasonal photosynthesis in alfalfa.     

Persistence of photosynthetic components and photochemical efficiency in ears of water-stressed wheat (Triticum aestivum)

Ear photosynthesis may be an important source of C for grain growth in water-stressed plants of cereals. The main objectives of this work were to determine the stability of the photosynthetic apparatus and the photochemical efficiency of ears in plants subjected to post-anthesis drought. Plants of wheat ( Triticum aestivum L. cv. Granero INTA) were grown in pots under a rain shelter and subjected to water stress (soil water potential around −0.6 to −0.8 MPa) starting 4  days after anthesis. Post-anthesis drought substantially accelerated the loss of chlorophyll, Rubisco and the light-harvesting complex of photosystem II (LHCII) in the flag leaf, but the degradation of these photosynthetic components was much less affected by water deficit in awns and ear bracts. Quantum yield of PSII (Φ_PSII) decreased in leaves of water-stressed plants. In contrast, ear bracts had a higher Φ_PSII than leaves, and Φ_PSII of ear bracts did not decrease at all in response to drought. Removing the grains immediately before fluorescence measurements (less than 30 min) slightly reduced Φ_PSII, indicating that CO₂ supplied by grain respiration may contribute to the high photochemical efficiency of ears in droughted plants. However, other factors may be involved in maintaining high Φ_PSII, since even in the absence of grains Φ_PSII remained much higher in ear bracts than in the flag leaf. The relative stability of ear photosynthetic components and their relatively high photochemical efficiency may help to maintain ear photosynthesis during the grain filling period in droughted plants.     

Photochemical response to drought acclimation in two sunflower genotypes

The effects of drought acclimation on CO₂ assimilation and light utilization were investigated in two sunflower genotypes ( Helianthus annuus L., T32 and Viki) in relation to water deficit and/or high light conditions. Drought interaction with PSII efficiency was observed in the genotype T32 with a sustained decrease in the potential photochemical efficiency of PSII, F_n/F_m. In response to drought acclimation, T32 displayed some tendency to accumulate closed PSII traps (higher value of 1-qp) without an enhancement of thermal deactivation (Stem-Volmer non-photochemical quenching, NPQ). Irrespective of the growth conditions (growth chamber or greenhouse), only Viki was responsive to drought acclimation, with (1) increased net photosynthesis in well-watered plants, (2) higher maintenance of photochemical electron transfer under water deficit and/or high light, (3) limited PSII inactivation (lower value of 1-qp) through increased non-photochemical energy dissipation (Stern-Volmer NPQ) which was readily reversible even at low leaf water potentials, and (4) higher F_v/F_m recovery after high light treatment. Additionally, drought acclimation delayed turgor loss during subsequent water stress in Viki. Thus, the response to drought acclimation, with an adjustment of water relations and of energy utilization by PSII, was observed under both growth conditions and was mainly genotype dependent.