Journal of Experimental Botany, Vol. 51, No. 90001, pp. 391-397,
February 2000
© 2000 Oxford University Press
Is there scope for improving balance between RuBP-regeneration and carboxylation capacities in wheat at elevated CO2?
Biochemistry and Physiology Department, IACR-Rothamsted, Harpenden, Herts. AL5 2JQ, UK
Received 19 April 1999; Accepted 29 September 1999
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Abstract |
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Carboxylation and RuBP-regeneration capacities, which determine light-saturated photosynthetic rate, were analysed in leaves of spring wheat )Triticum aestivum L. cv. Minaret( grown under different atmospheric CO2 partial pressure )pCa( and N supply regimes. Capacities were estimated from a large number of gas exchange, Rubisco and ATP-synthase content measurements, and from these, the pCa at which the two capacities are equal was derived, to allow direct comparison with growth pCa. Acclimation of the balance between the two capacities to growth at elevated pCa in wheat was only partial and appears to occur mostly in older flag leaves and at low N. However, in contrast to conclusions drawn from previous analyses of these data, there was evidence of a specific effect of growth at 70 Pa pCa, where carboxylation capacity is reduced more than RuBP-regeneration capacity for a given leaf N content. A model was used to estimate the effects of fluctuations in PPFD and temperature in the growth environment on the optimal balance between these capacities. This showed that the observed balance between carboxylation and RuBP-regeneration capacities in young wheat leaves could be consistent with adaptation to the current, or even the preindustrial pCa.
Key words: Triticum aestivum, carboxylation, RuBP regeneration, carbon dioxide, nitrogen, photosynthesis
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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The current atmospheric CO2 partial pressure )pCa( is already the highest experienced by plants at any time over at least the last 160 000 years )Barnola et al., 1987(, possibly for several million years, and is rapidly increasing. There may therefore be opportunities to improve the adaptation of photosynthesis of C3 crops, since their recent ancestors evolved under lower pCa. Furthermore, there is evidence that breeding has increased stomatal conductance in wheat )Fischer et al., 1998(, thereby further increasing the CO2 at the site of carboxylation ) pCc( compared to that experienced by wheat ancestors.
One consequence of increasing pCa is that carboxylation by Rubisco becomes more efficient compared with RuBP-regeneration and other processes. For maximum photosynthesis )A( per unit leaf N )N-use efficiency(, a decrease in Rubisco relative to RuBP-regeneration components is therefore theoretically required at high pCa )Medlyn, 1996; Sage, 1994(. This theory is supported by observations in plants where the amount of Rubisco has been decreased by genetic manipulation. In tobacco, the amount of Rubisco in leaves of plants grown at ambient pCa largely determines light-saturated photosynthetic rate, but does not limit photosynthesis at elevated pCa )Quick et al., 1992( and the pCa at which RuBP-regeneration begins to limit photosynthesis is much higher in plants with decreased Rubisco content )Masle et al., 1993; von Caemmerer et al., 1994(. In a comparison of rice lines grown at ambient pCa, those with decreased Rubisco content had a greater N-use efficiency measured at high pCa )Makino et al., 1997(. However, there remains the question of whether there are acclimatory responses to long-term growth at elevated CO2 such that any excess investment in Rubisco is decreased or removed. Reviews of gas exchange studies )Medlyn, 1996; Sage, 1994( have concluded that there is evidence of some rebalancing occurring under certain conditions )particularly nutrient deficiency(, but usually it is less than the predicted optimum and often there is none. A large )60%( decrease in Rubisco content relative to wild type in transgenic tobacco plants had a smaller relative effect on growth at elevated compared to ambient pCa )Masle et al., 1993(. Had perfect acclimation occurred, Rubisco would be equally limiting at both pCa and the relative effect of the reduction in content would be about the same. Furthermore, sample A–pCi responses again showed only a small shift in favour of RuBP-regeneration over carboxylation capacity in wild-type leaves )Masle et al., 1993(.
In recent work )Theobald et al., 1998(, gas-exchange and leaf composition measurements were used to estimate the amount of excess Rubisco at elevated pCa in flag-2, flag-1 and flag leaves of wheat grown at different pCa and N supply regimes. Most of the excess Rubisco at high pCa persisted even in plants grown at high pCa. It was also concluded that what decrease in excess there was in these plants occurred probably as a consequence of elevated growth pCa inducing a reduction in leaf N content, which was strongly associated with a decrease in the fraction of Rubisco that was in excess. Here, the gas-exchange measurements are re-examined specifically to estimate the value of RuBP regeneration capacity and the effects of growth pCa and N on the balance between RuBP-regeneration and carboxylation capacities in wheat. This new analysis has somewhat modified one of the original conclusions.
In order to interpret how these results compare with theoretical optima, it is necessary to remember that photosynthetic components are often not optimized such as to maximize photosynthesis for )unnatural( constant conditions, but rather appear to invest such that they can exploit changes that would be expected in a natural environment )Stitt and Schulze, 1994(. In the case of the balance between carboxylation and RuBP-regeneration capacities, the optimum is affected by temperature and PPFD, which fluctuate too rapidly to be acclimated to in a natural environment. A model was therefore developed which describes the balance of carboxylation and RuBP-regeneration capacities as a function of pCa, temperature and PPFD. This model allows the investigation of how the optimal balance of capacities under the measuring conditions of light-saturation and 20 °C will differ from the optimal balance for a natural environment.
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Materials and methods |
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Experimental
The experimental methods have been described in detail )Theobald et al., 1998(, but a brief summary is given here. Spring wheat stands were grown from emergence to maturity at 600 µmol m-2 s-1 PPFD, day/night temperature 20/12 °C, and vapour-pressure deficit 0.8/0.4 kPa VPD. They were grown either under ambient )36 Pa( or elevated )70 Pa( CO2 partial pressures and with low or high N supply. Response of light-saturated photosynthesis to internal CO2 partial pressure ) pCi( was measured at intervals in flag-2, flag-1 and flag leaves. The same leaves were sampled to determine leaf N, Rubisco and ATP-synthase contents, and Rubisco activation state.
Carboxylation capacity )Vcmax( was estimated from fitting points below a critical pCi )as detailed in Theobald et al., 1998(. RuBP-regeneration capacity )Jmax( was estimated from fitting points above critical pCi to the equation )Farquhar and Sharkey, 1994(:
 | (1) |
* is photorespiratory compensation point and
 | (2) |
A further parameter was derived from estimates of Jmax and Vcmax. The pCc at which the two capacities are equal ) pCc,bal( is given by:
 | (3) |
Modelling
The same parameter values used in the fitting procedure were used in the model )Table 1
(. Additional parameters assumed were necessary to treat the temperature dependence of these parameters, and to investigate the effect of variable PPFD. This latter effect was treated by using the solution to the equation )Farquhar and Sharkey, 1994(:
 | (4) |
is the curvature of the response, 
is the fraction of incident light usefully absorbed by PSII and I is the PPFD of incident light. For model runs shown here, a light distribution was chosen with a range of 100–1500 mol m-2 s-1 with the duration of each being the same for 100–600 µmol m-2 s-1, and then decreasing linearly to 10% of this at 1500 µmol m-2 s-1.
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For modelling of optimal balance it is also necessary to assume a relative N cost for Jmax compared to that for Vcmax )NRC(. If Jmax can only be increased by increasing the number of photosynthetic cells and chloroplasts per unit leaf area then NRC
2 )Table 1(.
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Results |
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Figure 1
shows the relationship between Jmax estimated from gas exchange and the ATP-synthase content of the same leaf section, estimated by Western blots )Theobald et al., 1998(. The data are reasonably well correlated )R2=0.65(, although not as tightly as Rubisco content and Vcmax )Theobald et al., 1998(.
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( Low N, 36 Pa CO2; )•( low N, 70 Pa CO2; )
( high N, 36Pa CO2; 
high N, 70 Pa CO2.Changes of Jmax in flag leaves through time )Fig. 2
( showed that low N supply generally decreased Jmax, and that elevated growth pCa never significantly increased Jmax and sometimes induced a decrease. Also shown in Fig. 2 is the balance of carboxylation and RuBP-regeneration capacities, expressed as the pCa at which they would be equal ) pCa,bal calculated from Vcmax and Jmax values using equation 3(. Optimal use of resources for the measurement conditions is therefore given by pCa,bal=growth pCa )i.e. 36 or 70 Pa(. In plants grown with pCa=36 Pa, the value of pCa,bal is initially above 36 Pa and tends to decrease with time )especially with high N supply(, indicating increased limitation by RuBP-regeneration. Growth at 70 Pa pCa had no significant effect on pCa,bal values in flag leaves at full emergence )first point(, and there was no consistent effect for any point for high N plants. However, growth at 70 Pa pCa did significantly increase pCa,bal values to 55–60 Pa for low N plants in the period 9–16 d after anthesis.
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This rebalancing could be explained as a reduction in leaf N content, which is generally associated with a decrease in carboxylation capacity relative to RuBP-regeneration capacity in our data )Theobald et al., 1998(. Figure 3
shows the data from the first four occasions in Fig. 2 replotted against leaf N content for individual leaf segments. Jmax is significantly, but not very tightly, correlated with leaf N content )R2=0.38(, and there are no significant differences between growth environments in the relationship. However, the relationship between pCa,bal and leaf N was significantly improved by assuming separate intercepts and slopes for plants grown in the two pCa environments )R2=0.53(. These lines suggest that growth at elevated pCa induces a rebalancing in favour of RuBP-regeneration capacity for leaves with low N content )<1.5 g m-2( in addition to any effect on leaf N content.
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The results of running the model to find the optimal value of relative investment in components responsible for RuBP-regeneration and carboxylation for variable environments are shown in Figs 4
and 5, and are expressed as the pCa,bal that would be observed at 20 °C and saturating light. The more curved the light-response of photosynthesis )i.e. the lower the value of (, the greater the value of pCa,bal )Fig. 4(. As approaches 1, where there is no co-limitation, the optimal value approaches the growth pCa. It is interesting to note that the observed values of pCa,bal from this study are consistent with optimization to the pre-industrial pCa for reasonable values of )
0.85(. Figure 5 shows the effect of a difference in leaf temperature between growth and measurement conditions. The measured pCa,bal will tend to exceed the growth pCa if it is optimized to a lower temperature than the measurement temperature, and vice versa.
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Discussion |
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Assuming ATP-synthase is substrate-saturated and fully activated under conditions where RuBP-regeneration limits photosynthesis, it is possible to estimate a kcat from the regression line through the origin in Fig. 1. A value of 260 mol ATP mol-1 ATP-synthase s-1, is given by assuming 1 ATP : 3 protons : 1 electron. However, these assumptions give a higher value than the ATP-requirement for the observed photosynthetic rates in the range where RuBP-regeneration is assumed limiting, i.e. the points used to estimate Jmax )data not shown(. This is because equation 1, used to estimate Jmax, assumes limitation of photosynthesis by production of reductant rather than ATP. The two estimates match closely if 1 ATP : 4 protons and 3 protons : 1 electron are assumed )Noctor and Foyer, 2000(, giving a kcat of 200 mol ATP mol-1 ATP-synthase s-1.
The reanalysis of the gas-exchange data )396 A–pCi responses( from previously reported experiments )Theobald et al., 1998( is consistent with the main conclusions arrived at there: that there is a tendency to over-invest in Rubisco for optimization of photosynthesis to growth at 70 Pa pCa )shown by pCa,bal<70 Pa in Fig. 2(, and that this tendency is much greater in leaves with high N contents )Fig. 3(. When elevated pCa does induce an apparent rebalancing, it is by a reduction in Rubisco content, rather than a stimulation of RuBP-regeneration components, since Jmax was never increased by growth at elevated pCa )Fig. 2(, and it appears to occur only in older leaves with low N supply. However, while it was concluded )Theobald et al., 1998( that this rebalancing was entirely explicable as a consequence of elevated pCa reducing leaf N content, specific analysis of the relationship between RuBP-regeneration and carboxylation capacities suggests that RuBP-regeneration: carboxylation is increased by growth at elevated pCa for a given leaf N content )Fig. 3(.
Recent studies on response of photosynthetic capacities to elevated pCa have confirmed the conclusions from a review of earlier studies )Sage, 1994(, that the response is variable and more likely to occur when N is deficient. In field experiments on wheat, it was found that Rubisco decreased more in response to elevated pCa in plants grown with limiting N supply than with free access to N )Rogers et al., 1996( and no evidence was found of a decrease in photosynthetic capacity of young, fully-expanded leaves until grain-fill in a well-fertilized crop )Garcia et al., 1998(, although there was some evidence for a decrease in Rubisco in leaves lower in the canopy )Osborne et al., 1998(. This latter study also found increased amounts of light-harvesting complex in these leaves, but this is consistent with acclimation to low incident radiation and would not be expected to increase Jmax. In a controlled-environment experiment on wheat, it has been shown that changes in photosynthetic capacity at elevated pCa were completely eliminated by supplying N in proportion to growth, thus removing the indirect effect of pCa in increasing the limitation of N on growth )Farage et al., 1998(. In a study which looked specifically at the ratio of RuBP-regeneration capacity : carboxylation capacity in soybean )Sims et al., 1998a(, growth at elevated pCa increased the ratio more in plants grown at low N than at high N. However, they found that low N supply alone did not affect, or even increased this ratio. This contrasts with the results of the present study for wheat, where low N supply increased pCa,bal )Fig. 2(, equivalent to a decrease in the ratio, a finding which is consistent with the observation that the ratio of Rubisco : ATP-synthase contents increases in wheat leaves with high N contents )Theobald et al., 1998(.
It is interesting to speculate on the mechanism behind the shift in balance between RuBP-regeneration and carboxylation capacities that sometimes occurs in response to elevated pCa. It now seems clear that it is not a direct response to pCa, but rather a consequence of the change in the balance of limitations for plant growth which occurs at elevated pCa )Farage et al., 1998; Sage, 1994; Sims et al., 1998b(. It is often suggested that sugar accumulation in the leaf, which suppresses expression of photosynthetic genes, may be the cause )van Oosten and Besford, 1996(, but this also decreases expression of genes encoding components of RuBP-regeneration )Krapp and Stitt, 1995(. It may be that the amount of active Rubisco responds more quickly than other components, but this has not been established. In the later leaves of wheat, this mechanism seems less likely as fructan synthesis in the internodes represent a very large sink for sugar export. Leaf carbohydrate content was not increased at elevated pCa in the experiments )JC Theobald, unpublished data( and was not correlated with changes in message levels for photosynthetic components in a field experiment on wheat )Nie et al., 1995(. The timing of the effect seems more consistent with an increased demand for N from an increased number of grain at elevated pCa, an interpretation that also applied to a number of open-topped chamber experiments carried out in Europe )Mitchell et al., 1999(.
In this paper, the balance of RuBP-regeneration : carboxylation capacities has been presented as pCa,bal, which allows comparison with the growth environment pCa. However, pCa=pCa,bal does not correspond to optimal use of resources for the growth environment where incident radiation fluctuates, because Jmax is believed to have an influence on photosynthesis at sub-saturating light intensities )Farquhar et al., 1980(. It has been shown that this increases the optimal ratio of Jmax : Vcmax, depending on the curvature in equation 4 and the light distribution that is assumed )Medlyn, 1996(. An arbitrary light distribution was chosen in this work, which has the necessary property that the duration of intensities approaching full sunlight are shorter than those for lower intensities; other distributions with this property gave similar results. In this case, the curvature )( reflects genuine co-limitation between Jmax and PPFD, rather than any heterogeneity within the leaf. The model shows )Fig. 4( that the observation that pCa,bal usually exceeds the current ambient pCa )in young leaves pCa,bal40 Pa in these data, Fig. 2(, in agreement with results elsewhere )Makino et al., 1988; Masle et al., 1993; von Caemmerer et al., 1994(, could be consistent with optimization. Indeed, it could even be consistent with adaptation to the pre-industrial pCa )Fig. 4(.
The model was also used to examine the effect of temperature on the optimal balance of capacities. The specific temperature dependencies in Table 1 are open to some doubt, since published data are sparse, and for Kc and Ko a temperature dependency for spinach was used to correct the published wheat value determined at 25 °C. Nevertheless, it seems certain that Jmax is less increased by temperature than Vcmax, for example, in cotton )Harley et al., 1992(. This has the consequence that if leaves optimize their resources to a lower average temperature than they are measured at, the observed pCa,bal will be greater than the growth pCa )Fig. 5(.
For an optimal resource allocation between RuBP-regeneration and carboxylation capacities at a growth pCa of 70 Pa, the pCa,bal should exceed this value, as shown in Fig. 4. This was not observed in these data )Fig. 3(. The only occasions on which partial rebalancing did occur in response to elevated growth pCa, were between 6 d and 15 d after anthesis in the low N treatment )Fig. 3(, possibly corresponding to large N demand from the developing grain. It therefore appears that there is a tendency for wheat to over-invest in Rubisco at elevated pCa, so genetic manipulation to reduce Rubisco relative to RuBP-regeneration capacity could benefit N-use efficiency of photosynthesis under these conditions.
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Acknowledgements |
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Gift of antibodies against CF1 sub-units from Professor JC Gray, University of Cambridge, UK is gratefully acknowledged. We thank Dr PJ Andralojc for assistance and advice with the ATP-synthase work, and SP Driscoll and VJ Mitchell for technical assistance. We thank Professors CB Osmond and SP Long for useful comments on the manuscript. JCT was supported by a grant from the European Union as part of the ESPACE-Wheat project, contract number EV5V-C793–0301. RACM receives support from UK Ministry of Agriculture, Fisheries and Food contract CSA4532. IACR-Rothamsted receives grant-aided support from the Biotechnology and Biological Sciences Research Council of the United Kingdom.
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Footnotes |
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1 To whom correspondence should be addressed. Fax: +44 1582 763010. E-mail:rowan.mitchell{at}bbsrc.ac.uk
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Abbreviations |
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, fraction of incident light usefully absorbed by photosystems;; ß, pCi/pCa ratio; *, photorespiratory compensation point; , curvature of photosynthetic light response; 
, Rubisco specificity factor; A, light-saturated net CO2 assimilation rate; Ag, light-saturated CO2 assimilation rate gross of non-photorespiratory respiration; gW, conductance for diffusion of CO2 from intercellular space to site of carboxylation; Jmax, maximum rate of non-cyclic photosynthetic electron transport; Kc, Rubisco Michaelis constant for CO2; Ko, Rubisco Michaelis constant for O2; NRC, relative N cost of investing in RuBP-regeneration capacity compared to carboxylation capacity; pCa, atmospheric CO2 partial pressure; pCa,bal, pCa at which carboxylation and RuBP-regeneration capacities are equal; pCc, CO2 partial pressure at site of carboxylation; pCc,bal, pCc at which carboxylation and RuBP-regeneration capacities are equal; pCi, CO2 partial pressure in intercellular space; PPFD, photosynthetically-active photon flux density; RuBP, ribulose-1,5-bisphosphate; Rubisco, RuBP carboxylase/oxygenase; Vcmax, maximum rate of carboxylation. |
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