Journal of Experimental Botany

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Journal of Experimental Botany, Vol. 52, No. 362, pp. 1779-1784, September 1, 2001
© 2001 Oxford University Press

Original Papers

Small decreases in SBPase cause a linear decline in the apparent RuBP regeneration rate, but do not affect Rubisco carboxylation capacity

Elizabeth P. Harrison¹, Hulya Olcer², Julie C. Lloyd, Stephen P. Long³ and Christine A. Raines⁴

Department of Biological Sciences, John Tabor Laboratories, University of Essex, Colchester CO4 3SQ, UK

Received 1 February 2001; Accepted 10 May 2001

	Abstract

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The response of net photosynthetic CO₂ uptake (A) to increasing leaf intercellular CO₂ concentration (c_i) was determined in antisense Nicotiana tabacum plants, derived from six independent transformation lines, displaying a range of sedoheptulose-1, 7-bisphosphatase (SBPase) activities. The maximum in vivo ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) carboxylation (V_c,max) and RuBP regeneration (J_max) rates were calculated from the steady-state measurements of the A to c_i response curves. In plants with reductions in SBPase activity of between 9% and 60%, maximum RuBP regeneration capacity declined linearly (r²=0.79) and no significant change in apparent in vivo Rubisco activity (V_c,max) was observed in these plants. No correlation between V_c,max and a decrease in capacity for RuBP regeneration was observed (r²=0.14) in the SBPase antisense plants. These data demonstrate that small decreases in SBPase activity limit photosynthetic carbon assimilation by reducing the capacity for RuBP regeneration.

Key words: Antisense, photosynthesis, Rubisco, SBPase.

	Introduction

Top Abstract Introduction Materials and methods Results Discussion References

 
A model of CO₂ uptake (Farquhar et al., 1980) has provided a widely used method that allows the limitation of photosynthesis, under saturating light conditions, to be partitioned between Rubisco activity and the capacity for RuBP regeneration. By determining the response of net leaf CO₂ uptake (A) to intercellular CO₂ concentration (c_i), the model may be used to partition limitation of the rate of carbon assimilation (A) between Rubisco activity (V_c,max) and maximum rate of RuBP regeneration, which is assumed proportional to the maximum rate of whole chain electron transport (J_max). When c_i is low, Rubisco activity normally controls A. However, at higher c_i, control shifts to the regeneration of RuBP. This means that the formation of RuBP is limited by the maximum rate of whole chain electron transport, or co-limited by the rate of whole chain electron transport and enzymes in the regenerative phase of the Calvin cycle (Farquhar et al., 1980; von Caemmerer, 2000).

A practical value of the model of Farquhar et al. lies in the assumption that the variables V_c,max and J_max are independent (Farquhar et al., 1980). However, a survey of data obtained from 109 species revealed a linear relationship between J_max and V_c,max (Wullschleger, 1993). Leuning re-analysed these data by adjusting the estimates to a common temperature, using equations for the temperature dependence of these parameters (Leuning, 1997). This increased the correlation coefficient (r²) of J_max with V_c,max to 0.87. Evans showed that within a species V_c,max/J_max remained more or less constant over a wide range of leaf nitrogen contents, from optimal to deficient levels (Evans, 1986). These correlations may simply be chance but may also reflect co-ordinated synthesis or/and activation of the photosynthetic components by parallel factors conserved across species. As such it may not be possible to have a decrease in J_max without a decrease in V_c,max. The possibility of genetically modifying J_max, independently from V_c,max and vice versa, has assumed added significance in considering the adaptation of C₃ crops to elevated [CO₂]. Here optimization of investment within the photosynthetic apparatus for elevated [CO₂], would require increased investment into capacity for the regeneration of RuBP and decreased investment into Rubisco (Long and Drake, 1992). Transgenic plants with altered levels of individual Calvin cycle enzymes have provided a means to test whether J_max may be varied independently of V_c,max.

Several studies with transgenic antisense plants have shown that an imbalance between V_c,max and J_max, relative to wild-type plants, may be induced either by a reduction of Rubisco content or by a decrease of a component affecting RuBP regeneration. However, whilst the correlation apparent in the survey by Wullschleger is broken (Wullschleger, 1993), a decrease in J_max has rarely been achieved without some decrease in V_c,max and vice versa. Price et al. found that a decrease in the Calvin cycle enzyme GAPDH of more than 65% was necessary to effect any decrease in CO₂ assimilation (Price et al., 1995). In their comparison of A/c_i responses of wild-type and antisense plants it was shown that with a 90% decrease in GAPDH, J_max is decreased by 57%, however, V_c,max was also decreased by 43%. A decrease in V_c,max was also indicated by a linear decline in the number of Rubisco binding sites per unit leaf area when GAPDH activity was reduced below 50% of wild-type activity. However, a more recent analysis of the same GAPDH transformant lines, suggested that in vivo Rubisco activity during transient RuBP saturation, was unaffected by comparison to wild-type plants (Ruuska et al., 1998). This showed clearly that potential V_c,max was unaltered by large decreases in J_max, however, the possibility still exits for steady-state V_c,max to be altered via feedback control. Is it possible to show the separation of J_max from variation in V_c,max, indicated by Ruuska et al. (Ruuska et al., 1998), under steady-state conditions?

An ideal antisense approach to test whether a decrease in J_max effects a change in steady-state V_c,max would target an enzyme where even a small decrease will cause a significant decrease in J_max. Previous analysis of transgenic plants with small reductions in SBPase activity revealed a loss of photosynthetic capacity (Harrison et al., 1998; Raines et al., 2000). In this paper, transgenic lines have been used with a wide range of SBPase activities to test the hypothesis that steady-state RuBP regeneration (J_max) may be decreased without affecting Rubisco activity in vivo (V_c,max).

	Materials and methods

Top Abstract Introduction Materials and methods Results Discussion References

 
Plant material
The transgenic tobacco (Nicotiana tabacum L. cv. Samsun) used in this study were the T1 progeny resulting from the self-fertilization of six independent antisense SBPase parents (T0) generated as described previously (Harrison et al., 1998). Seeds were germinated on sterile MS media supplemented with 3% (w/v) sucrose (Murashige and Skoog, 1962) and kanamycin (100 µg ml^-1) in a 14 h photoperiod at 20 °C. Four-week-old seedlings were transferred to soil (Levington F2, Fisons) and placed in a controlled-environment greenhouse under the same light/dark regime at c. 26 °C during the light period and 18 °C during the dark period. The plants were illuminated with natural light supplemented with high pressure sodium lamps giving 1000–1400 µmol m^-2 s^-1 at leaf level (measured at midday), and a minimum of 500 µmol m^-2 s^-1 throughout the photoperiod. Plants were grown individually in 18 cm pots positioned at random, relocated at regular intervals, and watered daily with Hoagland's solution (Hoagland and Arnon, 1950). Gas exchange measurements were made on each side of the mid-rib midway on the long axis of the leaf. Leaves 7 and 8, each on completion of expansion, were used for these measurements. Immediately on completion of photosynthetic measurement, discs (1.5 cm diameter) were cut from the same areas of the leaf, snap frozen into liquid N₂ and stored at -80 °C.

Photosynthesis measurements
Gas-exchange measurements were conducted at saturating PPFD (1000 µmol m^-2 s^-1) with a leaf temperature of 25± 1.5 °C and vapour pressure deficit of c. 1 kPa. Rates of CO₂ uptake and water vapour efflux were measured in an open gas-exchange system, incorporating infrared CO₂ and H₂O analysers and a leaf cuvette (CIRAS-1 and PLC, PP Systems, Hitchin, UK). The analyser was calibrated against a known CO₂ standard (Linde Gas, Stoke-on-Trent, UK) and water vapour concentrations provided by a water vapour generator (WG 600, ADC Ltd., Hoddesdon, Herts., UK). PPFD was measured with a quantum sensor (Skye Instruments Ltd., Wales). A and c_i were determined using the equations of von Caemmerer and Farquhar (von Caemmerer and Farquhar, 1981). To determine the response of A to c_i, A was first measured at the ambient CO₂ concentration (c_a) in which the plants had grown. To determine the initial slope of the A/c_i response, c_awas decreased in several steps to c. 50 µmol mol^-1. The c_a was then returned to the growth concentration to check that the original rate could be regained and was then finally increased stepwise to 2000 µmol mol^-1 to complete the response curve.

The maximum Rubisco activity in vivo (V_c,max) was estimated from the initial slope of the response of A to c_i as described earlier (Wullschleger, 1993) and using the Rubisco kinetic parameters of von Caemmerer et al. (von Caemmerer et al., 1994). V_c,max, estimated in this way, provided a measure of the activity of Rubisco within the leaves analysed. The points above the inflection of the response curve of A to c_i were used to estimate J_max.

SBPase activity, Western blot analysis and photosynthetic pigments
Frozen leaf discs were ground to a powder at liquid N₂ temperature and then used for enzyme activity, protein and pigment assays. SBPase activity was determined by the phosphate release method as described previously (Harrison et al., 1998). SBPase and Rubisco SSU protein levels were determined by separation on 12% SDS-PAGE followed by Western blotting using a horseradish peroxidase conjugated second antibody and ECL kit (Amersham International PLC) (Harrison et al., 1998). Rubsico LSU and SSU were determined using a laser densitometric scanner (Molecular Dynamics, Sevenoaks, Kent). Chlorophylls were determined by the method of Hill et al. (Hill et al., 1985).

	Results

Top Abstract Introduction Materials and methods Results Discussion References

 
Plant phenotypes
Fifteen T1 progeny, from six independent transgenic lines containing a tobacco antisense SBPase transgene, were found to have levels of SBPase activity decreased between 9% and 82%, relative to wild-type levels. SBPase protein levels were closely and positively correlated with SBPase activity (r²=0.97). Western blot analysis of samples from seven of these SBPase antisense plants is shown in Fig. 1. These data indicated that there was no detectable change in either Rubisco SSU or LSU in the SBPase antisense plants relative to wild-type plants, except where SBPase activity was decreased by more than 60%. The antisense plants with reductions of 60% or less of wild-type SBPase activity had the same leaf appearance and chlorophyll content as the wild-type plants (examples shown in Table 1). However, plants with greater reductions in SBPase activity showed an obvious reduction in chlorophyll content.

View larger version (57K): [in this window] [in a new window]   Fig. 1. SBPase and Rubisco protein levels in SBPase antisense tobacco plants. Soluble leaf proteins, loaded on an equal leaf area basis, were separated using SDS-PAGE. SBPase, Rubisco SSU and LSU were detected using ECL after Western blotting and sequential probing with polyclonal antiserum against SBPase and Rubisco holoenzyme. These data are examples taken from the analysis of five different wild-type plants and, for the transgenic plants, samples were taken from each plant from two separate leaves.

 

View this table: [in this window] [in a new window]   Table 1. SBPase activities, light-saturated photosynthetic rates (Amax), chlorophyll and carotenoid content in the same two fully expanded leaves (7, 8) of seven antisense SBPase plants with reductions in activity of between 9–82% of wild type Data are means ±SE. Samples were for five different plants for the wild type. For the individual transgenes samples were taken from two separate leaves.

 

A/c_i response analysis
The response of net CO₂ uptake (A) to increasing intercellular CO₂ (c_i), the A/c_i response curve, showed clear differences between antisense and wild-type plants. All of the SBPase antisense plants analysed in this study had a lower A at the highest c_i, (A_max) (examples shown in Table 1). In contrast, the initial slopes of the response appeared identical to the wild-type plants, except in the transgenic plants where SBPase activity was decreased by more than 60%. Three typical A/c_i response curves obtained from the SBPase antisense plants are shown in Fig. 2. From these data it can be seen that reductions in SBPase activity to 38% and 57% of wild-type plants decreased RuBP-limited photosynthesis (J_max), but not Rubisco-limited (V_c,max) photosynthesis. In contrast, in plants with more severe reductions in SBPase activity, both J_max and V_c,max were reduced (Fig. 2). This is in keeping with the Western blot analysis of Rubisco LSU and SSU that showed that the amount of Rubisco protein was reduced in plants with SBPase activities decreased by 60% or more relative to wild-type plants (Fig. 1). In four of the antisense plants SBPase activity was reduce by more than 60% which clearly caused pleiotropic effects on Rubisco and photosynthetic pigments; for this reason these plants were eliminated from the analysis of dependence of J_max on V_c,max.

View larger version (24K): [in this window] [in a new window]   Fig. 2. Response of CO2 assimilation rates to intercellular CO2 concentration (ci) at saturating PPFD (1000–1400 µmol m-2 s-1) in SBPase antisense tobacco plants. Measurements were made on single transformants and on five wild-type plants. Each datum point represents the mean of measurements on five individual wild-type plants and for the transgenes two separate leaves were measured at full expansion on each plant.

 

Analysis of dependence of J_max on V_c,max
Using the model of Farqhuar et al., values for in vivo Rubisco activity (V_c,max) and RubP regeneration (J_max) were calculated from the A/c_i response curves of 11 antisense plants with reductions in SBPase activity of between 9% to 60% (Farqhuar et al., 1980). In these plants V_c,max was unchanged, while J_maxdeclined linearly with SBPase activity (Fig. 3). A strong linear and significant relationship between J_max and SBPase activity was found with a slope of 0.69 (r²=0.79, p<0.01; Fig. 3). In contrast, there was no significant correlation of SBPase activity with V_c,max (r²=0.25, ns) in these plants (Fig. 3). Additionally, in the transgenic plants with reductions in SBPase acitivity between 9% and 60%, there was no correlation of V_c,max with J_max (r²=0.14, ns).

View larger version (27K): [in this window] [in a new window]   Fig. 3. The relationship of percentage reduction in Vc,max and in Jmax to percentage reduction in SBPase activity. Vc,max and Jmax were determined from the A/ci relationships of 11 antisense plants with SBPase activities reduced to between 9–60% (examples plotted in Fig. 2). Each point represents the mean data for an individual transformant (two separate leaves were measured at full expansion for each transformant); the value for 0% reduction in SBPase activity represents the mean of five wild-type plants. The broken lines indicate the 95% confidence limits. The control co-efficient for SBPase activity over Jmax was derived from the gradient of line obtained by plotting the % decrease in Jmax against the % decrease in SBPase activity.

 

	Discussion

Top Abstract Introduction Materials and methods Results Discussion References

 
These data confirm the hypothesis that a decrease in the steady-state in vivo maximum regeneration rate of RuBP, as reflected in the maximum rate of whole chain electron transport calculated from gas exchange (J_max), can be engineered without altering the steady-state, apparent in vivo maximum Rubisco activity (V_c,max). An imbalance between V_c,max and J_max has also been inferred from a number of previous studies of antisense plants in which photosynthetic properties have been altered (Quick et al., 1992; Hudson et al., 1992; Price et al., 1995, 1998; Ruuska et al., 1998). In these studies (with the exception of Ruuska et al., 1998), an engineered decrease in J_max was accompanied by a decrease in Rubisco activity or vice versa. The plants used in these previous studies have all involved large reductions in the target protein, typically >60%. Here a complete independence of steady-state V_c,max from J_max has been shown determined from steady-state A/c_i responses (Fig. 3). Even the small decreases in V_c,max indicated (Fig. 3) are likely to be over-estimates of the true decrease in in vivo Rubisco activity, because diffusive conductance of CO₂ within the mesophyll has been shown to decline with photosynthetic capacity in tobacco with decreased photosynthetic capacity (Evans et al., 1994). The present results show that steady-state J_max can be decreased by up to 50% without having a significant effect on, or correlation with apparent steady-state V_c,max.

Many gas exchange studies have found that there is a remarkably strong correlation between J_max and V_c,max (reviewed by Wullschleger, 1993; Leuning, 1997). Manipulation of photosynthetic capacity using either shade conditions or nitrogen deficiency appears to result in the co-ordinate reduction of V_c,max and J_max such that control remains shared equally between Rubisco activity and RuBP regeneration (Evans, 1986; Evans and Farquhar, 1991). This could imply that either there are feedback control mechanisms or that synthesis of Rubisco and components of the photosynthetic apparatus determining RuBP regeneration are so tightly linked, that one can not be varied without affecting the other. This present study, together with that of Ruuska et al. (Ruuska et al., 1998), has demonstrated that RuBP regeneration can be varied substantially using genetic engineering without affecting Rubisco activity. This potential flexibility in the relationship between Rubisco activity and the rate of RuBP regeneration could be of benefit under conditions of rising atmospheric CO₂ concentration where the limitation on carbon assimilation shifts from Rubisco to RuBP regeneration (Stitt, 1991; Drake et al., 1997). Plants may be able to optimize investment in the photosynthetic apparatus such that Rubisco levels would decrease and/or investment in the enzymes involved in regeneration would increase.

Interestingly, the data here also showed that J_max is very sensitive to small decreases in SBPase activity, with an apparent linear dependence, indicating a control coefficient for SBPase activity over J_max of 0.69. It has been assumed that RuBP regeneration at light saturation is controlled by the potential whole chain electron transport rate, rather than by the enzymes of the Calvin cycle downstream of Rubisco (Farquhar et al., 1980; von Caemmerer, 2000). This assumption has been supported by the results obtained from the analysis of plants with antisense decreases in other individual enzymes of the Calvin cycle. Large decreases (>60%) in GAPDH (Price et al., 1995), FBPase (Kossmann et al., 1994), PRKase (Paul et al., 1995, 2000) were necessary to decrease photosynthesis and regeneration of RuBP. In contrast, only a small decrease in SBPase (9%) was needed to effect a decrease in the apparent in vivo maximum rate of RuBP regeneration ( J_max). The assumption that the limitation to J_max is within the electron transport pathway could only be consistent with these findings if SBPase activity is just slightly in excess of the activity needed to support the observed wild-type J_max. The cytochrome b/f complex is commonly regarded as a limiting step in whole chain electron transport, but analysis of antisense plants with reduced levels of this complex have not resolved this issue. A decrease in electron transport rate was not apparent in the data given for these plants by Price et al. (Price et al., 1998) until cytochrome f content was decreased by more than 50%. The results of the present study suggest that wild-type SBPase activities may be close to controlling J_max and that any de-activation of this thioredoxin-regulated enzyme would decrease, or at least co-limit, J_max calculated from the A/c_i response.

In conclusion, this study has shown from the steady-state A/c_i response, that J_max may be varied substantially without affecting V_c,max. The data presented here also indicated that SBPase may be unusual among the Calvin cycle enzymes downstream of Rubisco, including the closely related FBPase, in being just sufficient in activity to support observed rates of RuBP regeneration in vivo.

	Acknowledgments

 
This work was supported by grant number P01723 from the Biotechnology and Biological Sciences Research Council (EPH). We are grateful to Dr Martin Parry for the kind gift of Rubisco antibodies and to Dr Susanne von Caemmerer for discussion of this work.

	Notes

 
¹ Present address: Horticulture Research International, Wellesbourne, Warwick CV35 9EF, UK.

² Present address: Dumlupinar Üniversitesi, Fen Edebiyat Fakültesi, Biyoloji Bolümü, Kütahya, Turkey.

³ Present address: Departments of Crop Science and Plant Biology, ERML190, University of Illinois, Urbana, Illinois 61801, USA.

⁴ To whom correspondence should be addressed. Fax: +44 1206 873416. rainc{at}essex.ac.uk

	Abbreviations

 
A, leaf CO₂ uptake (µmol m^-2 s^-1); c_a, ambient CO₂ concentration (µmol mol^-1); c_i, intercellular CO₂ concentration (µmol mol^-1); FBPase, fructose-1,6-bisphosphatase; J_max, maximum capacity for whole chain electron transport (µmol m^-2 s^-1); MS, Murashige and Skoog; PPFD, photosynthetically active photon flux density (µmol m^-2 s^-1); PRKase, phosphoribulokinase; Rubisco, ribulose-1,5-bisphosphate carboxylase/oxygenase (LSU large subunit, SSU small subunit); RuBP, ribulose-1,5-bisphosphate; V_c,max, apparent maximum Rubisco activity (µmol m^-2 s^-1); SBPase, sedoheptulose-1,7-bisphosphatase; T1, first generation of primary transformants..

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