Sensing of atmospheric CO2 by plants

Abstract. Despite recent interest in the effects of high CO₂ on plant growth and physiology, very little is known about the mechanisms by which plants sense changes in the concentration of this gas. Because atmospheric CO₂ concentration is relatively constant and because the conductance of the cuticle to CO₂ is low, sensory mechanisms are likely to exist only for intercellular CO₂ concentration. Therefore, responses of plants to changes in atmospheric CO₂ will depend on the effect of these changes on intercellular CO₂ concentration. Although a variety of plant responses to atmospheric CO₂ concentration have been reported, most of these can be attributed to the effects of intercellular CO₂ on photosynthesis or stomatal conductance. Short-term and long-term effects of CO₂ on photosynthesis and stomatal conductance are discussed as sensory mechanisms for responses of plants to atmospheric CO₂. Available data suggest that plants do not fully realize the potential increases in productivity associated with increased atmospheric CO₂. This may be because of genetic and environmental limitations to productivity or because plant responses to CO₂ have evolved to cope with variations in intercellular CO₂ caused by factors other than changes in atmospheric CO₂.     

Effects of source-sink relations on photosynthetic acclimation to elevated CO2

Abstract. While photosynthesis of C₃ plants is stimulated by an increase in the atmospheric CO₂ concentration, photosynthetic capacity is often reduced after long-term exposure to elevated CO₂. This reduction appears to be brought about by end product inhibition, resulting from an imbalance in the supply and demand of carbohydrates. A review of the literature revealed that the reduction of photosynthetic capacity in elevated CO₂ was most pronounced when the increased supply of carbohydrates was combined with small sink size. The volume of pots in which plants were grown affected the sink size by restricting root growth. While plants grown in small pots had a reduced photosynthetic capacity, plants grown in the field showed no reduction or an increase in this capacity. Pot volume also determined the effect of elevated CO₂ on the root/shoot ratio: the root/shoot ratio increased when root growth was not restricted and decreased in plants grown in small pots. The data presented in this paper suggest that plants growing in the field will maintain a high photosynthetic capacity as the atmospheric CO₂ level continues to rise.     

The effect of elevated CO2 on the chemical composition and construction costs of leaves of 27 C3 species

We determined the proximate chemical composition as well as the construction costs of leaves of 27 species, grown at ambient and at a twice-ambient partial pressure of atmospheric CO₂. These species comprised wild and agricultural herbaceous plants as well as tree seedlings. Both average responses across species and the range in response were considered. Expressed on a total dry weight basis, the main change in chemical composition due to CO₂ was the accumulation of total non-structural carbohydrates (TNC). To a lesser extent, decreases were found for organic N compounds and minerals. Hardly any change was observed for total structural carbohydrates (cellulose plus hemicellulose), lignin and lipids. When expressed on a TNC-free basis, decreases in organic N compounds and minerals were still present. On this basis, there was also an increase in the concentration of soluble phenolics. In terms of glucose required for biosynthesis, the increase in costs for one chemical compound – TNC – was balanced by a decrease in the costs for organic N compounds. Therefore, the construction costs, the total amount of glucose required to produce 1 g of leaf, were rather similar for the two CO₂ treatments; on average a small decrease of 3% was found. This decrease was attributable to a decrease of up to 30% in the growth respiration coefficient, the total CO₂ respired [mainly for N AD(P)H and ATP] in the process of constructing 1 g of biomass. The main reasons for this reduction were the decrease in organic N compounds and the increase in TNC.     

The effects of reduced and elevated CO2 and O2 on the seaweed Lomentaria articulata

We grew a non-bicarbonate using red seaweed, Lomentaria articulata (Huds.) Lyngb., in media aerated with four O₂ concentrations between 10 and 200% of current ambient [O₂] and four CO₂ concentrations between 67 and 500% of current ambient [CO₂], in a factorial design, to determine the effects of gas composition on growth and physiology. The relative growth rate of L. articulata increased with increasing [CO₂] up to 200% of current ambient [CO₂] but was unaffected by [O₂]. The relative growth enhancement, on a carbon basis, was 52% with a doubling of [CO₂] but fell to 23% under 5× ambient [CO₂]. Plants collected in winter responded more extremely to [CO₂] than did plants collected in the summer, although the overall pattern was the same. Discrimination between stable carbon isotopes (Δ¹³C) increased with increasing [CO₂] as would be expected for diffusive CO₂ acquisition. Tissue C and N were inversely related to [CO₂]. Growth in terms of biomass appeared to be limited by conversion of photosynthate to new biomass rather than simply by diffusion of CO₂, suggesting that non-bicarbonate-using macroalgae, such as L. articulata, may not be directly analogous to C3 higher plants in terms of their responses to changing gas composition.     

Interacting effects of elevated CO2, nutrient availability and plant species on a generalist invertebrate herbivore

By affecting plant growth and phytochemistry elevated CO₂ may have indirect effects on the performance of herbivores. These effects show considerable variability across studies and may depend on nutrient availability, the carbon/nutrient‐balance in plant tissues and the secondary metabolism of plants. We studied the responses to elevated CO₂ and different nutrient availability of 12 herbaceous plant species differing in their investment into secondary compounds. Caterpillars of the generalist herbivore Spodoptera littoralis were reared on the leaves produced and their consumption and growth rates analysed. Elevated CO₂ resulted in a similar increase of biomass in all plant species, whereas the positive effect of fertilization varied among plant species. Specific leaf weight was influenced by elevated CO₂, but the effect depended on nutrient level and identity of plant species. Elevated CO₂ increased the C/N ratio of the leaves of most species. Caterpillars consumed more leaf material when plants were grown under elevated CO₂ and low nutrients. This indicates compensatory feeding due to lower tissue quality. However, the effects of elevated CO₂, nutrient availability and plant species identity on leaf consumption interacted. Both the effects of CO₂ and nutrient availability on the relative growth rate of the herbivore depended on the plant species. The feeding rate of S. littoralis on plant species that do not produce nitrogen‐containing secondary compounds (NCSC) was higher under low nutrient availability. In contrast, in plants producing NCSC nutrient availability had no effect on the feeding rate. This suggests that compensatory feeding in response to low nutrient contents may not be possible if plants produce NCSC. We conclude that elevated CO₂ causes species‐specific changes in the quality of plant tissues and consequently in changes in the preferences of herbivores for plant species. This could result in changes in plant community composition.     

Interannual climatic variation mediates elevated CO2 and O3 effects on forest growth

We analyzed growth data from model aspen (Populus tremuloides Michx.) forest ecosystems grown in elevated atmospheric carbon dioxide ([CO₂]; 518 μL L^?1) and ozone concentrations ([O₃]; 1.5 × background of 30–40 nL L^?1 during daylight hours) for 7 years using free‐air CO₂ enrichment technology to determine how interannual variability in present‐day climate might affect growth responses to either gas. We also tested whether growth effects of those gasses were sustained over time. Elevated [CO₂] increased tree heights, diameters, and main stem volumes by 11%, 16%, and 20%, respectively, whereas elevated ozone [O₃] decreased them by 11%, 8%, and 29%, respectively. Responses similar to these were found for stand volume and basal area. There were no growth responses to the combination of elevated [CO₂+O₃]. The elevated [CO₂] growth stimulation was found to be decreasing, but relative growth rates varied considerably from year to year. Neither the variation in annual relative growth rates nor the apparent decline in CO₂ growth response could be explained in terms of nitrogen or water limitations. Instead, growth responses to elevated [CO₂] and [O₃] interacted strongly with present‐day interannual variability in climatic conditions. The amount of photosynthetically active radiation and temperature during specific times of the year coinciding with growth phenology explained 20–63% of the annual variation in growth response to elevated [CO₂] and [O₃]. Years with higher photosynthetic photon flux (PPF) during the month of July resulted in more positive growth responses to elevated [CO₂] and more negative growth responses to elevated [O₃]. Mean daily temperatures during the month of October affected growth in a similar fashion the following year. These results indicate that a several‐year trend of increasingly cloudy summers and cool autumns were responsible for the decrease in CO₂ growth response.     

Possible effects of rising C02 on climate

Abstract Two factors will determine the rate at which CO₂ levels in the atmosphere increase in the future: the rate of input to the atmosphere, primarily from fossil fuel burning, and the way in which this CO₂ is partitioned between atmosphere, ocean and biosphere. A brief review is given of the current state of knowledge of these aspects of the CO₂ issue prior to a discussion of the changes in climate that might be expected from increased levels of CO₂, whenever these might occur. The basis of climate modelling upon which our expectations rest is explained, indicating the nature of the uncertainty that currently exists in the model results. While some of the gross features of the likely climatic change seem reasonably well established qualitatively, considerable model development will be needed before reliable information on the likely regional effects is forthcoming. Observations have yet to confirm the occurrence of temperature change attributable to CO₂ increases. Nevertheless, the possibility exists of a change in climate during the coming century that may be substantial relative to past experience. Although direct measures to control CO₂ emissions would certainly be premature, long-term planning of infrastructures, closely tuned to present climatic conditions, should ensure their robustness in the face of the uncertain climatic changes that may lie ahead.     

Synergistic effects of climate change and local stressors: CO2 and nutrient-driven change in subtidal rocky habitats

Climate-driven change represents the cumulative effect of global through local-scale conditions, and understanding their manifestation at local scales can empower local management. Change in the dominance of habitats is often the product of local nutrient pollution that occurs at relatively local scales (i.e. catchment scale), a critical scale of management at which global impacts will manifest. We tested whether forecasted global-scale change [elevated carbon dioxide (CO₂) and subsequent ocean acidification] and local stressors (elevated nutrients) can combine to accelerate the expansion of filamentous turfs at the expense of calcifying algae (kelp understorey). Our results not only support this model of future change, but also highlight the synergistic effects of future CO₂ and nutrient concentrations on the abundance of turfs. These results suggest that global and local stressors need to be assessed in meaningful combinations so that the anticipated effects of climate change do not create the false impression that, however complex, climate change will produce smaller effects than reality. These findings empower local managers because they show that policies of reducing local stressors (e.g. nutrient pollution) can reduce the effects of global stressors not under their governance (e.g. ocean acidification). The connection between research and government policy provides an example whereby knowledge (and decision making) across local through global scales provides solutions to some of the most vexing challenges for attaining social goals of sustainability, biological conservation and economic development.     

Mathematical models of the photosynthetic response of tree stands to rising CO2 concentrations and temperatures

Two published models of canopy photosynthesis, MAESTRO and BIOMASS, are simulated to examine the response of tree stands to increasing ambient concentrations of carbon dioxide (C_a) and temperatures. The models employ the same equations to described leaf gas exchange, but differ considerably in the level of detail employed to represent canopy structure and radiation environment. Daily rates of canopy photosynthesis simulated by the two models agree to within 10% across a range of CO₂ concentrations and temperatures. A doubling of C_a leads to modest increases of simulated daily canopy photosynthesis at low temperatures (10% increase at 10°C), but larger increases at higher temperatures (60% increase at 30°C). The temperature and CO₂ dependencies of canopy photosynthesis are interpreted in terms of simulated contributions by quantum-saturated and non-saturated foliage. Simulations are presented for periods ranging from a diurnal cycle to several years. Annual canopy photosynthesis simulated by BIOMASS for trees experiencing no water stress is linearly related to simulated annual absorbed photosynthetically active radiation, with light utilization coefficients for carbon of ?= 1.66 and 2.07g MJ^?1 derived for C_a of 350 and 700 μmol mol^?1, respectively.     

Respiration of crop species under CO2 enrichment

Respiratory characteristics of wheat (Triticum aestivum L. cvs Gabo and WW15), mung bean (Vigna radiata L. Wilczek cv. Celera) and sunflower (Helianthus annuus L. cv. Sunfola) were studied in plants grown under a normal CO₂ concentration and in air containing an additional 340 (or 250) μl l^?1 CO₂. Such an increase in global atmospheric CO₂ concentration has been forecast for about the middle of the next century. The aim was to measure the effect of high CO₂ on respiration and its components. Polarographic and, with wheat, CO₂ exchange techniques were used. The capacity of the alternative pathway of respiration in roots was determined polarographically in the presence of 0.1 mM KCN. The actual rate of alternative pathway respiration was assessed by reduction in oxygen consumption caused by 10 mM salicylhydroxamic acid. Each species responded differently. In wheat, growth in high atmospheric CO₂ was associated with up to 45% reduction in respiration by both roots and whole plants. Use of respiratory inhibitors in polarographic measurements on wheat roots implicated reduction in the degree of engagement of the alternative pathway as a major contributor to this reduced respiratory activity of high-CO₂ plants. No change was found in the total sugar content per unit wheat root dry weight as a result of high CO₂. In none of the species was there an increase in the absolute, or relative, contribution by the alternative pathway to total respiration of the root systems. Thus the improved photosynthetic assimilate supply of plants grown in high CO₂ did not lead to increased diversion of carbon through the non-phosphorylating alternative pathway of respiration in the root. On the contrary, in wheat grown in high CO₂ the reduced loss of carbon through that route must have contributed to their larger dry weight.     

A mechanistic evaluation of photosynthetic acclimation at elevated CO2

Plants grown at elevated pCO₂ often fail to sustain the initial stimulation of net CO₂ uptake rate (A). This reduced, acclimated, stimulation of A often occurs concomitantly with a reduction in the maximum carboxylation velocity (V_c,max) of Rubisco. To investigate this relationship we used the Farquhar model of C₃ photosynthesis to predict the minimum V_c,max capable of supporting the acclimated stimulation in A observed at elevated pCO₂. For a wide range of species grown at elevated pCO₂ under contrasting conditions we found a strong correlation between observed and predicted values of V_c,max. This exercise mechanistically and quantitatively demonstrated that the observed acclimated stimulation of A and the simultaneous decrease in V_c,max observed at elevated pCO₂ is mechanistically consistent. With the exception of plants grown at a high elevated pCO₂ (> 90 Pa), which show evidence of an excess investment in Rubisco, the failure to maintain the initial stimulation of A is almost entirely attributable to the decrease in V_c,max and investment in Rubisco is coupled to requirements.     

Integration of photosynthetic acclimation to CO2 at the whole-plant level

Primary events in photosynthetic (PS) acclimation to elevated CO₂ concentration ([CO₂]) occur at the molecular level in leaf mesophyll cells, but final growth response to [CO₂] involves acclimation responses associated with photosynthate partitioning among plant organs in relation to resources limiting growth. Source–sink interactions, particularly with regard to carbon (C) and nitrogen (N), are key determinants of PS acclimation to elevated [CO₂] at the whole-plant level. In the long term, PS and growth response to [CO₂] are dependent on genotypic and environmental factors affecting the plant's ability to develop new sinks for C, and acquire adequate N and other resources to support an enhanced growth potential. Growth at elevated [CO₂] usually increases N use efficiency because PS rates can be maintained at levels comparable to those observed at ambient [CO₂] with less N investment in PS enzymes. A frequent acclimation response, particularly under N-limited conditions, is for the accumulation of leaf carbohydrates at elevated [CO₂] to lead to repression of genes associated with the production of PS enzymes. The hypothesis that this is an adaptive response, leading to a diversion of N to plant organs where it is of greatest benefit in terms of competitive ability and reproductive fitness, needs to be more rigorously tested. The biological control mechanisms which plants have evolved to acclimate to shifts in source–sink balance caused by elevated [CO₂] are complex, and will only be fully elucidated by probing at all scales along the hierarchy from molecular to ecosystem. Use of environmental manipulations and genotypic comparisons will facilitate the testing of specific hypotheses. Improving our ability to predict PS acclimation to [CO₂] will require the integration of results from laboratory studies using simple model systems with results from whole-plant studies that include measurements of processes operating at several scales. Abbreviations: CAM, crassulacean acid metabolism; FACE, Free-Air CO₂ Enrichment; Pi, inorganic phosphate; LAR, leaf area ratio (m² g^-1); LWR, leaf weight ratio (g g^-1); NAR, net assimilation rate (g m^-2 d^{- 1}); PS, photosynthetic; RGR, relative growth rate (g g^-1 d^-1); R:S, root/shoot ratio; rubisco, ribulose bisphosphate carboxylase/oxygenase; RuBP, ribulose bisphosphate; SLA, specific leaf area (m² g^-1); SPS, sucrose phosphate synthase; WUE, water use efficiency (g biomass g H₂O^-1).     

P uptake by arbuscular mycorrhizal hyphae: effect of soil temperature and atmospheric CO2 enrichment

Mycorrhizas are ubiquitous symbioses that may have an important role in the movement of C from air to soil. Studies on the effects of climate change factors on mycorrhizas have been concentrated on the effects of atmospheric [CO₂] whereas temperature effects have been neglected. Based on previous results showing no effect of varying atmospheric [CO₂] on the development and P uptake of the arbuscular mycorrhizal fungi (AMF) colonizing plants growing in controlled conditions, we hypothesized that soil temperature would have a higher impact on AMF development and nutrient uptake than the effects of [CO₂] on the host plant. Pea plants were grown in association with either a single isolate of Glomus caledonium or AMF from field soil in factorial combination with the corresponding current (10 °C) or elevated (15 °C) soil temperatures at current (350 p.p.m) or elevated (700 p.p.m) atmospheric [CO₂]. ³³P uptake by extraradical AMF hyphae was measured independently from root P uptake in a root exclusion compartment. Intraradical colonization developed well at both soil temperatures and almost duplicated from 10 to 15 °C. Extraradical mycelium developed only at 15 °C in the root exclusion compartment and hyphal P uptake could therefore be studied at 15 °C only. Hyphal P uptake differed markedly between inoculum types, but was not altered by growing the host plants at two atmospheric [CO₂] levels. No significant [CO₂] × soil temperature interactions were observed. The results suggested that, in the system tested, AMF development and function is likely more influenced by the temperature component of climate change than by its [CO₂] component. We suggest that much more attention should be paid to temperature effects in future studies.     

CO2 responsiveness of plants: a possible link to phloem loading

Of the many responses of plants to elevated CO₂, accumulation of total non-structural carbohydrates (TNC in % dry weight) in leaves is one of the most consistent. Insufficient sink activity or transport capacity may explain this obvious disparity between CO₂ assimilation and carbohydrate dissipation and structural investment. If transport capacity contributes to the problem, phloem loading may be the crucial step. It has been hypothesized that symplastic phloem loading is less efficient than apoplastic phloem loading, and hence plant species using the symplastic pathway and growing under high light and good water supply should accumulate more TNC at any given CO₂ level, but particularly under elevated CO₂. We tested this hypothesis by carrying out CO₂ enrichment experiments with 28 plant species known to belong to groups of contrasting phloem-loading type. Under current ambient CO₂ symplastic loaders were found to accumulate 36% TNC compared with only 19% in apoplastic loaders (P=0.0016). CO₂ enrichment to 600 μmol mol^?1 increased TNC in both groups by the same absolute amount, bringing the mean TNC level to 41% in symplastic loaders (compared to 25% in apoplastic loaders), which may be close to TNC saturation (coupled with chlornplast malfunction). Eight tree species, ranked as symplastic loaders by their minor vein companion cell configuration, showed TNC responses more similar to those of apoplastic herbaceous loaders. Similar results are obtained when TNC is expressed on a unit leaf area basis, since mean specific leaf areas of groups were not significantly different. We conclude that phloem loading has a surprisingly strong effect on leaf tissue composition, and thus may translate into alterations of food webs and ecosystem functioning, particularly under high CO₂.     

Effects of elevated CO2 on the protein concentration of food crops: a meta-analysis

Meta‐analysis techniques were used to examine the effect of elevated atmospheric carbon dioxide [CO₂] on the protein concentrations of major food crops, incorporating 228 experimental observations on barley, rice, wheat, soybean and potato. Each crop had lower protein concentrations when grown at elevated (540–958 μmol mol^?1) compared with ambient (315–400 μmol mol^?1) CO₂. For wheat, barley and rice, the reduction in grain protein concentration was ～10–15% of the value at ambient CO₂. For potato, the reduction in tuber protein concentration was 14%. For soybean, there was a much smaller, although statistically significant reduction of protein concentration of 1.4%. The magnitude of the CO₂ effect on wheat grains was smaller under high soil N conditions than under low soil N. Protein concentrations in potato tubers were reduced more for plants grown at high than at low concentrations of ozone. For soybean, the ozone effect was the reverse, as elevated CO₂ increased the protein concentration of soybean grown at high ozone concentrations. The magnitude of the CO₂ effect also varied depending on experimental methodology. For both wheat and soybean, studies performed in open‐top chambers produced a larger CO₂ effect than those performed using other types of experimental facilities. There was also indication of a possible pot artifact as, for both wheat and soybean, studies performed in open‐top chambers showed a significantly greater CO₂ effect when plants were rooted in pots rather than in the ground. Studies on wheat also showed a greater CO₂ effect when protein concentration was measured in whole grains rather than flour. While the magnitude of the effect of elevated CO₂ varied depending on the experimental procedures, a reduction in protein concentration was consistently found for most crops. These findings suggest that the increasing CO₂ concentrations of the 21st century are likely to decrease the protein concentration of many human plant foods.     

Interactions of tropospheric CO2 and O3 enrichments and moisture variations on microbial biomass and respiration in soil

Soil microbial biomass C (C_mic) is a sensitive indicator of trends in organic matter dynamics in terrestrial ecosystems. This study was conducted to determine the effects of tropospheric CO₂ or O₃ enrichments and moisture variations on total soil organic C (C_org), mineralizable C fraction (C_Min), C_mic, maintenance respiratory (qCO₂) or C_mic death (qD) quotients, and their relationship with basal respiration (BR) rates and field respiration (FR) fluxes in wheat‐soybean agroecosystems. Wheat (Triticum aestivum L.) and soybean (Glycine max. L. Merr) plants were grown to maturity in 3‐m dia open‐top field chambers and exposed to charcoal‐filtered (CF) air at 350 μL CO₂ L^?1; CF air + 150 μL CO₂ L^?1; nonfiltered (NF) air + 35 nL O₃ L^?1; and NF air + 35 nL O₃ L^?1 + 150 μL CO₂ L^?1 at optimum (? 0.05 MPa) and restricted soil moisture (? 1.0 ± 0.05 MPa) regimes. The + 150 μL CO₂ L^?1 additions were 18 h d^?1 and the + 35 nL O₃ L^?1 treatments were 7 h d^?1 from April until late October. While C_org did not vary consistently, C_Min, C_mic and C_mic fractions increased in soils under tropospheric CO₂ enrichment (500 μL CO₂ L^?1) and decreased under high O₃ exposures (55 ± 6 nL O₃ L^?1 for wheat; 60 ± 5 nL O₃ L^?1 for soybean) compared to the CF treatments (25 ± 5 nL O₃ L^?1). The qCO₂ or qD quotients of C_mic were also significantly decreased in soils under high CO₂ but increased under high O₃ exposures compared to the CF control. The BR rates did not vary consistently but they were higher in well‐watered soils. The FR fluxes were lower under high O₃ exposures compared to soils under the CF control. An increase in C_mic or C_mic fractions and decrease in qCO₂ or qD observed under high CO₂ treatment suggest that these soils were acting as C sinks whereas, reductions in C_mic or C_mic fractions and increase in qCO₂ or qD in soils under elevated tropospheric O₃ exposures suggest the soils were serving as a source of CO₂.