Plant Physiol. (1999) 120: 173-182

Inhibition and Acclimation of Photosynthesis to Heat Stress Is Closely Correlated with Activation of Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase

R. David Law and Steven J. Crafts-Brandner^*

United States Department of Agriculture-Agricultural Research Service, Western Cotton Research Laboratory, 4135 East Broadway Road, Phoenix, Arizona 85040-8803

	ABSTRACT

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Increasing the leaf temperature of intact cotton (Gossypium hirsutum L.) and wheat (Triticum aestivum L.) plants caused a progressive decline in the light-saturated CO₂-exchange rate (CER). CER was more sensitive to increased leaf temperature in wheat than in cotton, and both species demonstrated photosynthetic acclimation when leaf temperature was increased gradually. Inhibition of CER was not a consequence of stomatal closure, as indicated by a positive relationship between leaf temperature and transpiration. The activation state of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco), which is regulated by Rubisco activase, was closely correlated with temperature-induced changes in CER. Nonphotochemical chlorophyll fluorescence quenching increased with leaf temperature in a manner consistent with inhibited CER and Rubisco activation. Both nonphotochemical fluorescence quenching and Rubisco activation were more sensitive to heat stress than the maximum quantum yield of photochemistry of photosystem II. Heat stress led to decreased 3-phosphoglyceric acid content and increased ribulose-1,5-bisphosphate content, which is indicative of inhibited metabolite flow through Rubisco. We conclude that heat stress inhibited CER primarily by decreasing the activation state of Rubisco via inhibition of Rubisco activase. Although Rubisco activation was more closely correlated with CER than the maximum quantum yield of photochemistry of photosystem II, both processes could be acclimated to heat stress by gradually increasing the leaf temperature.

	INTRODUCTION

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Inhibition of photosynthetic CO₂ fixation by high temperature has been documented in many plant species (for review, see Berry and Björkman, 1980). Several components of the photosynthetic apparatus and associated metabolic processes are heat labile. For example, PSII is thermally labile (Havaux, 1993; Havaux and Tardy, 1996) but can be acclimated to heat stress (Havaux, 1993). Recent evidence indicates that a chloroplast-localized heat-shock protein protects PSII from damage at high temperature (Heckathorn et al., 1998). Export of photoassimilate is another metabolic process that is sensitive to inhibition by high temperature. Jiao and Grodzinski (1996) reported that heat stress inhibited assimilate export to a greater degree than net photosynthesis. Inhibition was especially apparent at a high atmospheric CO₂ concentration at which assimilate export, but not net photosynthesis, was inhibited by heat stress. However, in a similar study using a different plant species (Leonardos et al., 1996), heat stress under a high atmospheric CO₂ concentration inhibited net photosynthesis but not assimilate export. Thus, the sensitivity of assimilate export to inhibition by heat stress may differ among plant species and/or associated environmental conditions.

Based on Chl fluorescence analysis, Bilger et al. (1987) reported that Calvin cycle activity was sensitive to rapid heat-stress treatments. Previous reports have documented that Rubisco activation is a primary site of inhibition (Weis, 1981a, 1981b; Kobza and Edwards, 1987; Feller et al., 1998). For example, Weis (1981a, 1981b) reported that rapid heat stress led to reversible inhibition of the light-dependent activation of Rubisco in spinach chloroplasts and leaves. Similar findings were reported for wheat (Triticum aestivum L.) leaves (Kobza and Edwards, 1987).

The close relationship between the activation state of Rubisco and photosynthesis in response to varying light intensity (Seemann et al., 1990) or altered activase content (Andrews et al., 1995; Eckardt et al., 1997) indicates the pivotal role of activase in the regulation of photosynthetic CO₂ fixation. The activity of Rubisco assayed immediately after extraction from leaves exposed to light levels that are saturating for photosynthesis is directly related to the ability of Rubisco activase to activate Rubisco. At optimal temperatures in air, it has been shown that this "initial activity" of Rubisco is similar to the activity after incubation of the enzyme with saturating levels of CO₂ and Mg²⁺ (von Caemmerer and Edmondson, 1986; Seemann et al., 1988; Feller et al., 1998). Fully activated Rubisco activity, both in leaf extracts from heat-stressed leaves and using isolated Rubisco, has been shown to be very stable at high temperatures (Kobza and Edwards, 1987; Eckardt and Portis, 1997; Feller et al., 1998). Therefore, the altered initial activity of Rubisco from light-saturated, heat-stressed leaves is directly related to changes in the activity of Rubisco activase. The lack of any effect of heat stress on extractable Rubisco activity after incubation with CO₂ and Mg²⁺ (Kobza and Edwards, 1987; Feller et al., 1998) precludes the possibility that decreases in initial Rubisco activity are associated with the formation of inhibitors of Rubisco.

Feller et al. (1998) proposed that heat stress rapidly and reversibly inhibited the light-dependent activation of Rubisco by inhibiting Rubisco activase activity. Evidence was presented that heat stress perturbed the structural properties of activase. In support of this hypothesis, the activity of isolated activase has been shown to be extremely sensitive to high temperature (Robinson and Portis, 1989; Holbrook et al., 1991; Crafts-Brandner et al., 1997; Eckardt and Portis, 1997). Crafts-Brandner et al. (1997) presented evidence that high temperature inhibited activase by disrupting subunit interactions.

In the present study, we have extended our previous work (Crafts-Brandner et al., 1997; Feller et al., 1998) to the level of the whole plant. We found the following: (a) Rubisco activation acclimates to heat stress in both cotton (Gossypium hirsutum L.) and wheat; (b) CER in wheat is more sensitive to inhibition by heat stress than CER in cotton under both acclimating and nonacclimating conditions; and (c) Rubisco activation and CER are remarkably well correlated during both rapid and gradual heat stress. For both plant species, Rubisco activation was more sensitive to heat stress than was F_v/F_m under both rapid and gradual heat stress.

	MATERIALS AND METHODS

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Plant Material

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CER Measurements

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For rapid heat-stress treatments, steady-state CER was determined first at the control temperature, after which the leaf temperature was increased to the desired level at a rate of approximately 1°C min¹. One hour after the leaf temperature was increased, steady-state CER was again determined. A different leaf from a nonstressed plant was used for each measurement, and at least three measurements were made at each temperature. Two independent experiments were conducted. For gradual heat-stress experiments, CER was measured for an individual leaf over the entire range of temperatures. After steady-state CER was determined at the control temperature, the leaf temperature was increased in 2.5°C increments (at a rate of approximately 1°C min¹) and measurements were made after 1 h at each temperature. Three leaves, each from a different plant, were sampled in each of two independent experiments.

The effect of leaf temperature on dark respiration was determined as described above, except that the measurements were made in darkness. Temperature effects on photorespiration were determined by measuring CER as described above, except that CO₂ was scrubbed from the sample-chamber inlet air. T₅₀ values for the effect of temperature on CER were calculated using a nonlinear least-squares regression kinetics computer program (Brooks, 1992).

Determination of Light-Dependent Activation of Rubisco

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Leaf tissue (20 mg fresh weight) was extracted using a glass homogenizer in 1.5 mL of CO₂-free buffer containing 100 mM Tricine, pH 8.0, 5 mM MgCl₂, 0.1 mM EDTA, 5 mM DTT, 1% (w/v) PVP, 1% (w/v) casein, 0.05% (v/v) Triton X-100, 1 mM PMSF, and 20 µM leupeptin. Within 30 s, an aliquot (25 µL) of extract was assayed at 30°C for 30 s to determine the Rubisco activation state (initial Rubisco activity). Rubisco assays were conducted as described by Salvucci and Anderson (1987), except that Triton X-100 and casein were not included in the assay medium. Activity was based on incorporation of ¹⁴CO₂ into acid-stable products. T₅₀ values for the effect of temperature on initial Rubisco activity were calculated as described for CER.

Determination of Chl Fluorescence

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For selected heat-stress treatments, relaxation kinetics of qN were analyzed immediately after the fluorescence-quenching analysis. Relaxation kinetics were measured using a preprogrammed protocol (Standard Run 5) of the PAM 2000 fluorometer. After the quenching analysis, illumination with actinic light (125 µmol photons m² s¹ emitted at 665 nm) was continued for 1 min, after which the actinic light was turned off and 1.2-s pulses of strong white light (>4000 µmol photons m² s¹) were applied at exponentially increasing intervals for a 16-min period.

Determination of Metabolites

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	RESULTS

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CER was inhibited at leaf temperatures greater than 35°C and 30°C for cotton and wheat, respectively (Fig. 1). Complete inhibition occurred when the leaf temperature was increased at a rate of 1°C min¹ to more than 42.5°C for cotton or 40°C for wheat. Acclimation to heat stress occurred for both plant species if the leaf temperature was increased gradually by 2.5°C every hour (Fig. 1). Acclimation was most pronounced at the higher leaf temperatures. For example, wheat leaf CER at 40°C was 43% or 14% of the 25°C controls when temperature was increased gradually or rapidly, respectively. When cotton leaf temperature was gradually increased to 45°C, the leaves maintained a CER that was 20% of the controls.

View larger version (22K): [in this window] [in a new window]   Figure 1. The effect of rapid and gradual increases in leaf temperature on CER of cotton and wheat leaves. Values are reported relative to the CER of the control, which was set at 100%. Each point is the mean ± SE of two independent experiments in which three measurements were made for each temperature treatment. CER for the controls averaged 32.3 ± 1.8 and 26.2 ± 1.9 µmol CO2 m2 s1 for cotton and wheat, respectively.

Dark respiration rates of both species were approximately 2.5 ± 1.0 µmol m² s¹ at the control leaf temperature. Increasing the leaf temperature to 37.5°C and 40°C for wheat and cotton, respectively, caused a nearly 2-fold increase in the dark respiration rate (data not shown). At higher leaf temperatures, the dark respiration rate declined to the level of the control. The rate of photorespiration, as estimated by CO₂ evolution into CO₂-free air in the light, was approximately 3.0 ± 1.0 µmol m² s¹ at the control temperature for both species. Photorespiration decreased approximately 3-fold as leaf temperature was increased gradually to 42.5°C and 45°C for wheat and cotton, respectively (data not shown). Thus, although dark respiration and photorespiration were significantly altered by heat stress, the magnitude of the effect was small relative to the large changes in CER (Fig. 1).

For well-watered plants, high leaf temperatures could be attained only under conditions of high (>75%) RH. Under these conditions, there was no evidence that stomatal closure had any influence on the heat-stress-induced inhibition of CER. Leaf transpiration increased progressively as leaf temperature was increased (Fig. 2). In addition, both leaf conductance to CO₂ and internal CO₂ concentration were increased as leaf temperature was increased (data not shown). Leonardos et al. (1996) reported a similar relationship between leaf temperature and transpiration for leaves of Alstroemeria.

View larger version (18K): [in this window] [in a new window]   Figure 2. The effect of gradual increases in leaf temperature on the transpiration rate of cotton and wheat leaves. Each point is the mean ± SE of two independent experiments in which three measurements were made for each temperature treatment.

At leaf temperatures greater than 35°C and 30°C for cotton and wheat, respectively, the initial activity of Rubisco (Fig. 3) was inhibited to an extent that was very similar to the inhibition of CER (Fig. 1). Acclimation to high temperature was apparent based on the differences between the rapid and the gradual heat-stress treatments at the higher leaf temperatures. The T₅₀ values for initial Rubisco activity (Fig. 3) were nearly identical to those calculated for CER (Fig. 1). Analysis of the entire data set, including both rapid and gradual heat-stress treatments, indicated a close correlation between CER and initial Rubisco activity, with correlation coefficients > 0.98 for both cotton and wheat (Fig. 4).

View larger version (24K): [in this window] [in a new window]   Figure 3. The effect of rapid and gradual increases in leaf temperature on initial Rubisco activity. Values are reported relative to the initial Rubisco activity of the control, which was set at 100%. Each point is the mean ± SE of two independent experiments in which three measurements were made for each temperature treatment. Initial Rubisco activity of the controls averaged 0.452 ± 0.016 and 0.433 ± 0.018 µmol CO2 g1 fresh weight s1 for cotton and wheat, respectively.

View larger version (18K): [in this window] [in a new window]   Figure 4. Correlation between initial Rubisco activity and CER of cotton and wheat leaves. Data points are from Figures 1 and 3. , Rapid heat stress; , gradual heat stress.

Differences in Chl fluorescence quenching were apparent when leaf temperature was gradually increased compared with rapidly increased. Steady-state qN increased at leaf temperatures greater than 35°C and 30°C for cotton and wheat, respectively (Fig. 5). Compared with rapid heat stress, gradual heat stress markedly decreased the magnitude of the increase in qN, especially for wheat. However, for both types of heat-stress treatments, this trait reflected inhibition of CER (Fig. 5, insets).

View larger version (27K): [in this window] [in a new window]   Figure 5. The effect of rapid and gradual increases in leaf temperature on steady-state qN of cotton and wheat leaves. Values are reported relative to the qN of the control, which was set at 100%. Each point is the mean ± SE of two independent experiments in which three measurements were made for each temperature treatment. Steady-state qN values for control cotton and wheat leaves averaged 0.330 ± 0.028 and 0.322 ± 0.030, respectively. The insets represent the correlation between CER (from data in Fig. 1) and steady-state qN. , Rapid heat stress; , gradual heat stress.

High-temperature stress also inhibited F_v/F_m (Fig. 6), but the inhibition occurred at higher temperatures than the corresponding perturbations in qN (Fig. 5). The T₅₀ values for F_v/F_m were higher than those for CER and initial Rubisco activity (Fig. 6). For cotton, F_v/F_m was relatively stable until leaf temperature exceeded 40°C. The small decrease in F_v/F_m between 35°C and 40°C for the rapid heat-stress treatment was caused by a gradual increase in the initial Chl fluorescence (data not shown). As leaf temperature exceeded 35°C for wheat, there was an abrupt decrease in F_v/F_m for the rapid heat-stress treatment. For the gradual heat-stress treatment, however, F_v/F_m at 40°C was 80% of the control F_v/F_m. As in cotton, the decrease in F_v/F_m between 32.5°C and 40°C for the gradual heat-stress treatment was associated with a gradual increase in the initial Chl fluorescence (data not shown).

View larger version (22K): [in this window] [in a new window]   Figure 6. The effect of rapid and gradual increases in leaf temperature on Fv/Fm of cotton and wheat leaves. Values are reported relative to the Fv/Fm of the control, which was set at 100%. Each point is the mean ± SE of two independent experiments in which three measurements were made for each temperature treatment. Fv/Fm for control cotton and wheat leaves averaged 0.769 ± 0.073 and 0.766 ± 0.063, respectively.

Figure 7 shows the effect of heat stress on the time course of the relaxation kinetics of steady-state qN developed during 5 min in the light. For controls of both species, qN relaxed to levels comparable to those of dark-adapted leaves during the 15-min time course. When leaf temperature was rapidly increased to 40°C and 35°C for cotton and wheat, respectively, relaxation of qN occurred but not nearly to the extent seen in the controls.

View larger version (20K): [in this window] [in a new window]   Figure 7. The effect of rapid increases in leaf temperature on the relaxation kinetics of qN of a cotton and a wheat leaf. Relaxation kinetics were analyzed immediately after quenching analysis, during which steady-state qN had developed in the light. Experiments were conducted first at the control temperatures of 28°C and 25°C for cotton and wheat, respectively, and then again after the leaf temperature was rapidly increased to 40°C and 35°C for cotton and wheat, respectively. The data reported were obtained from one representative leaf.

Heat stress altered the pools of PGA and RuBP in a manner consistent with a decrease in the activation state of Rubisco (Fig. 8). The level of PGA was very sensitive to increases in leaf temperature for both cotton and wheat, with significant decreases occurring before heat-stress-induced inhibition of CER (Fig. 1). At leaf temperatures of 45°C and 40°C for cotton and wheat, respectively, the level of PGA was barely detectable. The content of RuBP was relatively stable until leaf temperature exceeded 35°C for both plant species. Significant increases in RuBP content were observed at leaf temperatures greater than 35°C.

View larger version (21K): [in this window] [in a new window]   Figure 8. The effect of rapid increases in leaf temperature on the levels of PGA and RuBP in leaves of cotton and wheat. Each point is the mean ± SE of two independent experiments in which three leaves were analyzed for each experiment.

	DISCUSSION

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Isolated activase is extremely heat labile (Robinson and Portis, 1989; Holbrook et al., 1991; Crafts-Brandner et al., 1997; Eckardt and Portis, 1997), and the different polypeptide forms of activase differ in their sensitivity to inactivation by high temperature (Crafts-Brandner et al., 1997). The basis of thermal sensitivity appears to be disruption of subunit interactions that are necessary for activity (Crafts-Brandner et al., 1997). Feller et al. (1998) confirmed and extended the earlier reports of Weis (1981a, 1981b, 1982) and Kobza and Edwards (1987) by showing that Rubisco activation in intact leaf tissue was sensitive to rapid increases in leaf temperature. This inhibition was attributed to activase, which was shown to be denatured at temperatures greater than 40°C (Feller et al., 1998). Here we demonstrate that the activation state of Rubisco can acclimate to high-temperature stress in intact cotton and wheat plants and that the degree of acclimation is directly related to photosynthetic CO₂ fixation. CER and Rubisco activation were closely correlated for both plant species analyzed in all of the temperature treatments (Fig. 4). Based on previous data (Crafts-Brandner et al., 1997; Feller et al., 1998), we attribute heat-stress-induced inhibition and acclimation of CER and Rubisco activation state to inhibition of activase and specifically to disrupted activase subunit interactions. Direct measurement of activase activity in leaf extracts of heat-stressed leaves is not feasible because the in situ stromal environment that promotes or disrupts subunit interactions would not be preserved upon tissue homogenization.

Under both acclimating and nonacclimating heat-stress conditions, wheat was more sensitive to heat stress than cotton. For example, rapidly increasing the leaf temperature to 40°C caused a much more severe inhibition of CER for wheat than for cotton (Fig. 1). Both species, however, were able to acclimate to heat stress if the leaf temperature was increased gradually. Under acclimating conditions, the T₅₀ values of both CER and Rubisco activation were increased approximately 1.5°C to 2.0°C (Figs. 1 and 3). This degree of acclimation to heat stress was similar to that observed for kudzu when photosynthesis was determined in the presence of isoprene added to the air supplied to the leaves (Singsaas et al., 1997). It would be interesting to determine if isoprene influences Rubisco activation during heat stress of isoprene-emitting species.

Although the correlation between CER and initial Rubisco activity was very strong (Fig. 4), close inspection of the data indicated that there was a tendency for CER to be inhibited more than initial Rubisco activity at the higher leaf temperatures. Based on results using antisense activase plants, He et al. (1997) proposed that activase promotes the catalytic turnover of carbamylated Rubisco in addition to facilitating Rubisco carbamylation. It is possible that increasing leaf temperature has a differential effect on activase-mediated carbamylation, compared with activase-mediated catalytic turnover, of Rubisco. In addition, the specificity of Rubisco for O₂ increases with temperature (Jordan and Ogren, 1984), which would influence the relationship between CER and Rubisco activation at higher leaf temperatures.

It is known that the sensitivity of the photosynthetic apparatus to heat stress is altered by light intensity. Based on Chl fluorescence analysis, Schreiber and Berry (1977) reported that light protects PSII from heat damage, whereas Weis (1982) found little effect of light on PSII activity. Weis (1982) also reported that photosynthesis and Rubisco activation were more sensitive if rapid heat treatments were imposed under dark versus light conditions. In our experiments, measurements of Chl fluorescence were made using leaves that were heat stressed under conditions of saturating light and subsequently dark adapted for a minimal amount of time. This protocol was used to best approximate the conditions used for CER and Rubisco activation experiments and to best approximate the environmental conditions in which heat stress would likely occur. Chl fluorescence analysis (Figs. 5 and 6) proved to be a sensitive indicator of heat-stress-induced inhibition of CER (Fig. 1) and initial Rubisco activity (Fig. 3). Heat stress was associated with increased qN, an indicator of Calvin cycle activity, and decreased F_v/F_m. Thus, heat stress inhibited both Calvin cycle and electron-transport processes. Under both rapid and gradual heat-stress treatments, however, significant perturbations in qN were detected at lower leaf temperatures than were required to alter F_v/F_m. Furthermore, relaxation of steady-state qN was delayed at temperatures that did not significantly alter F_v/F_m (Fig. 7), suggesting that the dissipation of the transthylakoid energy gradient was inhibited by heat stress. Heat-stress-related effects on xanthophyll metabolism could also be associated with the decreased relaxation of qN (Havaux and Tardy, 1996). Overall, Chl fluorescence analysis corroborated Rubisco activation assays and indicated that Calvin cycle activity was more sensitive to high temperature than F_v/F_m for both plant species under acclimating and nonacclimating conditions.

Using Chl fluorescence techniques, Havaux (1993) demonstrated that PSII activity in potato leaves could be acclimated to heat stress. Our Chl fluorescence experiments for cotton and wheat confirmed that PSII activity, as well as Calvin cycle activity, could acclimate to heat stress. Furthermore, comparison of the two species indicated that heat tolerance of PSII was greater in cotton than in wheat (Fig. 6). Because Calvin cycle activity (based on qN measurements; Fig. 5) and, more specifically, activase-dependent activation of Rubisco (Fig. 3) acclimated to heat stress in a species-specific manner similar to that seen in PSII, it appeared that sensitivity/tolerance to heat stress was manifested throughout the photosynthetic apparatus.

Perturbations in the levels of the substrate and product of Rubisco (Fig. 8) provided support for our conclusion that heat stress inhibited the flow of carbon through Rubisco. For both plant species, PGA content declined markedly in response to rapid increases in leaf temperature, such that PGA was barely detectable at the highest temperature. PGA levels were decreased (Fig. 8) before any detectable change was seen in CER or initial Rubisco activity (Figs. 1 and 3). PGA is a substrate in numerous metabolic reactions, and its content and allocation to the Calvin cycle could be influenced according to the temperature dependence of several enzymes. On the other hand, RuBP content is directly indicative of Rubisco activity, and inhibition of any other Calvin cycle enzyme would lead to depletion of RuBP. There was no evidence of heat-related depletion of RuBP for either species. At temperatures greater than 35°C, RuBP levels were increased significantly, which is indicative of inhibited carbon flow through Rubisco. Gradual increases in leaf temperature had a similar effect on PGA and RuBP levels, as observed for rapid temperature increases (data not shown). Kobza and Edwards (1987) reported similar effects of rapid heat stress on PGA and RuBP levels in wheat. Additionally, PGA content was more sensitive than RuBP content when the flow of carbon through Rubisco was restricted in antisense Rubisco plants (Quick et al., 1991) or antisense activase plants grown under ambient CO₂ (He et al., 1997).

We conclude that the light-dependent activation of Rubisco, which is mediated by Rubisco activase, is one of the most thermally labile reactions associated with the photosynthetic apparatus. Inhibition of this reaction is directly related to inhibition of CER and, as such, could have a significant effect on plant growth and development. Our results indicate that activase sensitivity to high temperature varies among plant species and that activase activity can acclimate during a relatively short period when the leaf temperature is increased in gradual increments. It will be important to determine the mechanism associated with activase acclimation and why cotton activase is more heat tolerant than wheat activase. Differences in heat tolerance between the two forms of activase from spinach (Crafts-Brandner et al., 1997) indicate that the inherent thermal properties of the subunits of the enzyme may differ both within and among species. Heat-stress-induced changes in the pools of ATP and ADP, which are substrates known to stabilize activase (Robinson and Portis, 1989; Wang et al., 1993), could influence the acclimation of activase as leaf temperature is gradually increased. Acclimation to high temperature may be associated with altered biosynthesis of the molecular forms of activase.

	FOOTNOTES

   Received October 19, 1998; accepted January 19, 1999.
¹   Mention of a trade name does not constitute a guarantee or warranty of the product by the U.S. Department of Agriculture and does not imply its approval over other products that may also be suitable.

	ABBREVIATIONS

Abbreviations: CER, CO₂-exchange rate. Chl, chlorophyll. F_v/F_m, maximum quantum yield of photochemistry of PSII. PGA, 3-phosphoglyceric acid. qN, nonphotochemical Chl fluorescence quenching. RuBP, ribulose-1,5-bisphosphate. T₅₀, temperature that causes 50% inhibition.

	ACKNOWLEDGMENTS

We acknowledge the excellent technical assistance provided by Donald L. Brummett. We also thank M.E. Salvucci for many insightful discussions and H.C. Huppe for helpful suggestions concerning the metabolite analysis.

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