Does Enhanced Photosynthesis Enhance Growth? Lessons Learned from CO2 Enrichment Studies

Plants typically convert only 2% to 4% of the available energy in radiation into new plant growth. This low efficiency has provided an impetus for trying to genetically manipulate plants in order to achieve greater efficiencies. But to what extent can increased photosynthesis be expected to increase plant growth? This question is addressed by treating plant responses to elevated CO2 as an analog to increasing photosynthesis through plant breeding or genetic manipulations. For plants grown under optimal growth conditions and elevated CO2, photosynthetic rates can be more than 50% higher than for plants grown under normal CO2 concentrations. This reduces to 40% higher for plants grown under the average of optimal and suboptimal conditions, and over the course of a full day, average photosynthetic enhancements under elevated CO2 are estimated to be about 30%. The 30% enhancement in photosynthesis is reported to increase relative growth rate by only about 10%. This discrepancy is probably due to enhanced carbohydrate availability exceeding many plants’ ability to fully utilize it due to nutrient or inherent internal growth limitations. Consequently, growth responses to elevated CO2 increase with a plant’s sink capacity and nutrient status. However, even a 10% enhancement in relative growth rate can translate into absolute growth enhancements of up to 50% during the exponential growth phase of plants. When space constraints and self-shading force an end to exponential growth, ongoing growth enhancements are likely to be closer to the enhancement of relative growth rate. The growth response to elevated CO2 suggests that increases in photosynthesis almost invariably increase growth, but that the growth response is numerically much smaller than the initial photosynthetic enhancement. This lends partial support to the usefulness of breeding plants with greater photosynthetic capacity, but dramatic growth stimulation should not be expected. The usefulness of increasing photosynthetic capacity can be maximized through changes in management practices and manipulation of other genetic traits to optimize the conditions under which increased photosynthesis can lead to maximal growth increases. Photosynthesis is a relatively inefficient process, with only a maximum of 8% to 10% of the energy in sunlight being converted to the chemical energy in reduced sugars (Long et al., 2006; Zhu et al. 2010). Further considering carbon losses from autotrophic respiration and limitations by other factors such as water and nutrient limitations, realized conversion efficiencies are typically just 2% to 4% of the energy received in sunlight (Long et al., 2006; Zhu et al. 2010). Therefore, it has been a long-standing aim to increase the photosynthesis of plants to achieve greater conversion efficiencies of available sunlight (Reynolds et al., 2000; Sinclair et al., 2004; Long et al., 2006; Zhu et al., 2010). But to what extent can increased photosynthesis increase ultimate plant growth? Is growth controlled by photosynthesis, or are other plant or environmental factors more important in controlling growth? Is the rate of photosynthesis simply scaled up or down to provide an amount of carbon that is controlled by other growth-limiting processes? If photosynthesis controls growth, it can provide an impetus and rationale for enhancing photosynthesis, but if other factors are more important in controlling growth, then any emphasis on improving photosynthesis might lead to little ultimate growth increase. There is a very useful analog for addressing this question. For C3 plants, increasing CO2 concentration enhances photosynthesis in much the same way as any engineering approaches might (Drake et al., 1997). Increasing CO2 concentrations, however, also modify stomatal conductance, which can become important under water-limited conditions. This constitutes an important difference between CO2- and plant breeding-mediated enhancements of photosynthesis. The following discussion, therefore, is restricted to conditions where CO2 responses are due to direct photosynthetic responses rather than involving changes in plant water balance. Leaf photosynthesis is readily observed to increase with increasing CO2 concentration (Drake et al., 1997), and these responses have been formalized through models of leaf photosynthesis (Farquhar et al., 1980; Farquhar and von Caemmerer, 1982; Medlyn et al., 2002). Using these models, coupled with assumptions about changes in stomatal conductance with changing CO2 concentration (Ball et al., 1987), it is possible to calculate the response of photosynthesis to increasing CO2 concentration (Fig. 1; Kirschbaum, 2004). Internal (air space and “wall”) resistances are ignored in these calculations, although they can substantially reduce chloroplast CO2 concentrations below average intercellular concentrations (Evans and von Caemmerer, 1996). Photosynthetic response to CO2 concentration, shown at four temperatures, based on calculations for RuBP regeneration-limited photosynthesis. All rates are expressed relative to the rates at 350 mmol mol–1. Calculations are based on the model of Farquhar et al. (1980) and Farquhar and von Caemmerer (1982) as described by Medlyn et al. (2002). It is important to distinguish between the responses of Rubisco-limited photosynthetic rates, which respond more strongly to CO2, and ribulose 1,5-bisphosphate (RuBP) regeneration-limited rates, which respond less strongly (Fig. 2). The relative responsiveness to increases in CO2 concentration also gradually diminishes with increasing atmospheric CO2 (Fig. 2). Photosynthesis shifts from limitation by Rubisco kinetics at lower intercellular CO2 concentrations to RuBP regeneration-limited rates at higher concentration. At lower radiation levels, photosynthesis is also generally RuBP regeneration limited. Zhu et al. (2010) also argued that most plants still have amounts and kinetic properties of Rubisco that are better suited to preindustrial CO2 concentrations, so that even under current conditions, plants generally have excess Rubisco and are more likely to be RuBP regeneration limited. In the context of responses to elevated CO2, and over most conditions experienced by leaves, the RuBP regeneration-limited responsiveness to CO2 concentration, therefore, is likely to be the relevant response function. Photosynthetic response to increasing atmospheric CO2 concentration shown as a function of temperature and separately for photosynthesis limited by Rubisco or RuBP regeneration. This was calculated for base CO2 concentrations of 350 and 400 mmol mol–1 as shown. Data are expressed as percentage increase in net assimilation rate (%A) for a percentage increase in CO2 concentration (%pa). Based on the calculations of Medlyn et al. (2002). These enhancements of photosynthesis are broadly consistent with experimental observations (Table I). Ellsworth et al. (2004) and Ainsworth and Long (2005) in their respective reviews of the literature found 40% and 29% enhancements of photosynthesis in free-air CO2 enrichment (FACE) experiments (Table I) at elevated CO2 concentrations of 500 to 600 mmol mol–1. Drake et al. (1997), in a review of potted plant experiments, found that photosynthesis was increased by 23% to 58% when plants were grown in elevated CO2 of about 700 mmol mol–1, depending on their nitrogen status and the size of pots they were grown in. Plants grown with inadequate nutrients or in small pots were likely to be affected by feedback inhibition, an issue that is further discussed below. For the plants that were least affected by these extra limitations, a 58% enhancement in photosynthesis was observed, which lies between the theoretical enhancements for RuBP regeneration-limited and Rubisco-limited rates at 25°C (Table I). The enhancement of rates between 700 and 350 mmol mol–1, based on simulations with the Farquhar photosynthesis model as described by Medlyn et al. (2002), using RuBP regeneration-limited or Rubisco-limited responsiveness as indicated. Drake et al. (1997) summarized the results of pot experiments, and Ellsworth et al. (2004) and Ainsworth and Long (2005) summarized the results of FACE experiments. The elevated CO2 concentration in pot experiments was usually around 700 mmol mol–1, whereas in FACE experiments, increased CO2 concentrations were usually only 500 to 600 mmol mol–1. Large pots were defined as having a root volume greater than 10 L, and small pots had root volumes less than that. Acclimation is defined as the rate of photosynthesis measured at a common CO2 concentration. The enhancement of rates between 700 and 350 mmol mol–1, based on simulations with the Farquhar photosynthesis model as described by Medlyn et al. (2002), using RuBP regeneration-limited or Rubisco-limited responsiveness as indicated. Drake et al. (1997) summarized the results of pot experiments, and Ellsworth et al. (2004) and Ainsworth and Long (2005) summarized the results of FACE experiments. The elevated CO2 concentration in pot experiments was usually around 700 mmol mol–1, whereas in FACE experiments, increased CO2 concentrations were usually only 500 to 600 mmol mol–1. Large pots were defined as having a root volume greater than 10 L, and small pots had root volumes less than that. Acclimation is defined as the rate of photosynthesis measured at a common CO2 concentration. However, photosynthetic measurements are usually taken under saturating radiation levels and avoid measurements at cold temperatures. These are the conditions that most likely lead to Rubisco limitation and where the CO2 enhancement of photosynthesis is maximized (Fig. 2; Table I). For parts of the day with lower temperature or lower radiation, or for canopies where a proportion of leaves experience reduced light levels through self-shading, the enhancement of photosynthesis is likely to be less. Conversely, for plants experiencing times of high temperatures, the photosynthetic stimulation could be even greater than that measured under moderate temperatures. For most experimental growing conditions, however, it seems likely that the actual enhancement of photosynthesis will be less than that measured under high irradiation and warm temperatures; therefore, it is likely to be less than the enhancements reported by Drake et al. (1997). The simple average of photosynthetic enhancements reported with large and small pots and high and low nitrogen reported by Drake et al. (1997) was 42%. If one assumes the average enhancement in photosynthesis over the day to be only about three-quarters of that measured under high radiation, the actual realized average enhancement of photosynthesis would be about 30%. Does a 30% photosynthetic enhancement lead to a 30% increase in growth? Poorter (1993) showed in an experiment with 10 species with contrasting growth rates, and Poorter and Navas (2003) showed for 179 experimental observations obtained from the literature, that the change in relative growth rate (ƊRGR) by elevated CO2 was a strong linear function of the relative growth rate of the same plants at 350 mmol mol–1 (Fig. 3). This meant that the relative growth enhancement (ƊRGR/RGR) was the same for different species with different inherent relative growth rates. This relative enhancement also constituted a relative increase of relative growth rate by only about 10%. Increase in relative growth rate (RGR) for plants grown in elevated CO2 expressed against the plant’s relative growth rate under normal atmospheric CO2. Data are shown for woody and herbaceous species. A linear relationship was fitted to the observations and forced through the origin. The slope of the relationship is 0.099 and implies an average 9.9% stimulation of relative growth rate by exposure to elevated CO2. Without forcing the line through the origin, the slope of the relationship would be 0.095. Data are redrawn from Poorter and Navas (2003). This leads to the question of why a 30% increase in photosynthesis results in an increase in relative growth rate of only about 10%. Poorter (1993) analyzed the growth response to elevated CO2 of 10 species in greater detail and found that photosynthesis expressed on a leaf area basis was enhanced by 20%, but the enhancement was only 6.5% on a weight basis because leaves also tended to be heavier per unit leaf area. It appeared that the increased amounts of carbohydrates could not be fully utilized by plants. Much of the extra carbohydrate remained in the leaf as sugars or starch (Table I) and made leaves heavier per unit area (Poorter, 1993). This contributed to an ineffective transformation of photosynthetic carbon gain into new growth. The reason for the much lower growth-rate enhancement than the enhancement of photosynthesis may be understood with reference to Figure 4. Extra carbon can only lead to extra growth if plants have a use for it, which may be for the growth of new foliage, roots, or other sinks such as developing seeds. If a plant’s capacity to utilize carbon is limited (sink limited), any increase in photosynthesis cannot be sustained and will be curtailed through feedback processes. Hence, the rate of photosynthesis measured under standard conditions, or the concentration of photosynthetic enzymes, is usually lower in plants grown under elevated CO2, here referred to as “downward acclimation.” Conceptual diagram of the interaction between foliage, roots, and potential carbon (C) and nitrogen (N) sources, sinks, and fluxes in the plant. Dashed lines show feedback control processes, which are only shown here for carbon fluxes. The feedback arrow from roots is designated by a question mark to indicate that this feedback process will operate in small pots but not in large pots or in the field. Additional carbon can also only be converted into useful plant tissue if nutrients are available as well. This is illustrated here with respect to nitrogen, as that is commonly the most limiting nutrient in nature, but the same consideration applies with respect to any other plant nutrient. If plant nutrition is limited, then any additional carbon cannot be used productively, and a growth stimulation cannot be sustained despite an initial enhancement of photosynthetic carbon gain. It has been argued that it is common in nature for plants to have excess carbon (Körner, 2003; Millard et al., 2007). Others (Long et al., 2006), on the other hand, have reasoned that this is contradicted by the fact that nearly all species show growth responses to elevated CO2 (Fig. 3). Therefore, it is probably better to consider growth not as being categorically limited by carbon or by specific other factors but as a continuum where the greater availability of one resource (carbon) shifts the plant toward greater limitation by other growth-limiting resources (Reynolds et al., 2000). For instance, Thomas and Strain (1991) showed experimentally, and Arp (1991) showed from a literature review, that the frequently observed downward acclimation of photosynthesis for plants grown in elevated CO2 was strongly related to the size of the pots that plants were grown in. Downward acclimation was generally confined to that used pots with a volume of less than 10 L, whereas consistent downward acclimation was reported from that used pot volumes and only downward acclimation was typically observed in FACE experiments (Table Ellsworth et al., 2004; Ainsworth and This was also in the summarized by Drake et al. (1997). summarized for plants grown in large pots showed a 58% photosynthetic enhancement at growth CO2 concentration and a of in photosynthetic rate measured at a common CO2 concentration (Table I). In plants grown in small pots showed a photosynthetic enhancement of only and downward acclimation of respect to pot the feedback is likely to operate through the availability of carbon growth can be curtailed by volumes in small to strong downward acclimation (Fig. but root growth in large pots or in the to downward The of the on CO2 responsiveness was shown more by et al. (2002), with found a strong stimulation of photosynthesis during the initial growth phase but a much reduced stimulation during the plant’s when plants were to have been sink limited. The CO2 stimulation was during the when developing constituted a large potential sink to utilize any enhanced carbon Ainsworth et al. (2004) used a FACE to that had been genetically to between and growth In one of the the showed a more sustained growth response to elevated CO2 than the For the other the sustained responsiveness to elevated CO2. This was to indicate that for even the had sink capacity to fully utilize increased amounts of whereas for the to an growth substantially increased ability to utilize an increased carbohydrate In further and (2003) that of photosynthesis in plants was related to the radiation of the day and a direct to the plant’s carbohydrate balance. a direct to photosynthesis was also by et al. showed for grown in the that leaves that had experienced high radiation levels for a day their photosynthetic carbon gain in the with leaves that had received less radiation and had less A was for the CO2 responsiveness of plants grown with different nitrogen rates, with reported downward acclimation of for plants and for grown with low nitrogen (Table I). The of carbohydrate is further by the reported increases in starch and in plants (Table I). These support the that are generally between and plants, because even plants grown in small pots or with limited nitrogen still showed enhanced photosynthesis with elevated CO2, but the responsiveness to CO2 when other factors more limiting as the availability of nutrients or root The discussed that the feedback from a plant’s carbohydrate status is a common of under current and CO2 concentrations, but also that it not generally lead to sink to lower the responsiveness of plant growth to CO2 enrichment but not growth even under conditions when plants have high sink their growth response still not to the potential enhancement that might be based on a consideration of their photosynthetic responses A large of have summarized enhancement due to growing plants in elevated CO2 (Table enhancement are numerically to initial photosynthetic are generally less for than for plants, less for than for plants, less for plants grown at low temperatures, but for herbaceous and woody species. CO2 responses reported for generally showed much greater responses than where plants were grown in (Table enhancement for plants were numerically also much greater than the enhancement in relative growth rates with Table 3). on the in CO2 responses between and that invariably showed the from are shown on the in CO2 responses between and that invariably showed the from are shown These between plant and growing conditions can be understood through consideration of the exponential growth of plants that can even moderate changes in relative growth rate into more enhancements in at growth and that an plant with a relative growth rate to the of the reported by Poorter and Navas as shown in Figure one can a growth as in Figure A and increases at but as plants increase in self-shading and the initial exponential growth changes into linear growth during the of a (Fig. response to CO2 concentration based on exponential growth rate for the initial growth phase and for a growth and the enhancement calculated as the of the shown in The in A and to growth at 350 and 700 mmol mol–1, of the model are in Leaf area enhancement in response to CO2 concentration for experiments or the of experiments on herbaceous and woody plant (Poorter, 1993). of the model are in Based on the enhancement in relative growth rate from Figure it is that the relative growth rate is increased by 10% through elevated CO2, which results in the in Figure A and Plants at the same initial leaf area at the of the but the of plants under the contrasting growth conditions plants in high and low CO2 are by the same ultimate space limitations. the simple assumptions used here for and of carbohydrate to other plant plants a size and growth even at the size of their If one the of the of the plants in elevated and normal CO2, it at the same at the of the but then the with the size the assumptions used found (Fig. The difference between and plants then diminishes the relative growth rate is enhanced by only that can lead to a 50% enhancement at growth but only a greater than 10% enhancement when the is for a of an experiment and for the same relative enhancement of relative growth the observed enhancement increase with increasing relative growth rate to a for a relative growth rate of about (Fig. This why plants have higher enhancement than growing plants (Table despite having the same relative increase in relative growth rate from 3). It might also the lower enhancement in plants grown with lower nutrients (Table although has been of the relative increase in relative growth rate for plants under different conditions. But why woody plants show the same enhancement as herbaceous plants despite typically having lower inherent relative growth rates (Fig. This is due to experiments on herbaceous plants typically being for only to whereas experiments on woody plants are for an average of over (Poorter, which then lead to observed enhancement for herbaceous and woody plants (Fig. This simple model can and the from different and different experimental Photosynthesis may be enhanced by 50% under optimal conditions (Drake et al., 1997), 40% over the average of optimal and suboptimal conditions the calculations and 30% over the this 30% increase in photosynthesis, relative growth rate to be enhanced by only 10% and the exponential growth however, a 10% enhancement in relative growth rate can lead to an absolute growth enhancements of 50% at growth as in most such as by Poorter and Navas (2003). from exponential growth to and to with the enhancement of initial carbon gain in the summarized by Ainsworth and et al., et al., Table enhancement are a of the responsiveness of plants to elevated CO2, as the same relative enhancements of relative growth rate in and used for the simulations can lead to very different enhancement by simply the of an experiment and It simply the of over which the during the exponential growth phase can to the actual response to CO2. Additional through showed that the growth response of was less than the response of Hence, even if one can and the that modify responses to elevated CO2, further are in trying to to plants growing under The that in species however, not the of results in such as for where a manipulation of photosynthetic capacity might be Increasing carbon is likely to also modify plant which will have their important A direct is the generally observed in concentrations in grown under elevated CO2 et al., A and more interaction the of plant nutrient concentrations on and and a of and found that plants grown under elevated CO2 usually had lower nutrient concentrations, which reduced the growth rate of on that plant The to for their reduced nutrient by greater amounts of foliage, but even with that less when on plants grown in elevated CO2. would have to that the same could be expected for plants with increased photosynthetic capacity if that can be greater nitrogen in have here to the current from CO2 enrichment that can the extent to which increasing photosynthesis is likely to translate into increased growth. experiments provide a of observations that can be useful in the potential that could from enhancing photosynthesis. Increasing photosynthesis increases carbon availability for plants. or to what that into increased growth on the nature of nutrient increase in carbon availability will nutrient limitations. This interaction may from a of any growth response to increasing photosynthesis in very conditions to a strong enhancement under very conditions. are likely to between these A more additional limitation lies in the limited growth capacity or of growing in a plant. Plants may have all the resources available but be to into new growth because of a limitation of tissue because of a growth If a plant’s growth is limited by genetic plant growth will respond to an increase in resource availability only up to the by these genetic Extra carbon will then be to be utilized by plants. the many experiments, growth enhancements are generally only with an average 10% enhancement of relative growth rate. the other hand, even a 10% enhancement in relative growth rate can translate into much more absolute growth enhancements during the exponential growth phase of plants. The experience from experiments that enhancing photosynthesis generally increases growth. This would support to the usefulness of increasing plant photosynthesis. experiments also show however, that growth responses are numerically only a of the potential enhancement of photosynthesis, which reduces the from plant to increase photosynthetic rates. This also that the with which photosynthetic can be into growth is affected by other plant and environmental responses to be greater under conditions where plants have to nutrition and for plants with greater sink capacity, be that due to growth or genetic such as having an rather than growth manipulation of photosynthesis should consider or for other plant to the of any increase in photosynthetic The following are available in the of this of a simple model to the exponential growth Poorter for to the for Figure and for useful of the of plant responses to elevated CO2 as as von Caemmerer, and for useful on the