JXB Advance Access originally published online on September 22, 2006
Journal of Experimental Botany 2006 57(14):3793-3799; doi:10.1093/jxb/erl140
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© 2006 The Author(s).
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.This paper is available online free of all access charges (see http://jxb.oxfordjournals.org/open_access.html for further details)
RESEARCH PAPER |
Effect of activase level and isoform on the thermotolerance of photosynthesis in Arabidopsis
1USDA-ARS, Arid-Land Agricultural Research Center, Maricopa, AZ 85239, USA
2USDA-ARS, Photosynthesis Research Unit, Urbana, IL 61801, USA
* To whom correspondence should be addressed. E-mail: msalvucci{at}wcrl.ars.usda.gov
Received 30 May 2006; Accepted 26 July 2006
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Abstract |
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Ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco) activation decreases under moderate heat stress. This decrease is caused by an impairment of activase function, which is exacerbated by faster rates of Rubisco deactivation at elevated temperatures. To determine if stromal oxidation causes inhibition of activase, transgenic Arabidopsis plants expressing suboptimal amounts of either the redox-regulated 46 kDa
- or non-redox regulated 43 kDa ß-isoform of activase were examined. Photosynthesis, as measured by gas exchange and chlorophyll fluorescence, and Rubisco activation were inhibited to a much greater extent by moderately high temperatures in the two transgenic lines expressing suboptimal levels of the individual isoforms of activase compared with wild-type plants or transgenic plants expressing levels of the ß-isoform sufficient for wild-type rates of photosynthesis. Net photosynthesis and Rubisco activation in transgenic plants expressing suboptimal amounts of the ß-isoform of activase from the Antarctic hairgrass were even more sensitive to inhibition by moderate heat stress than in the transgenic plants containing Arabidopsis activase. The results demonstrate that photosynthesis exhibits a similar sensitivity to inhibition by moderately high temperature in plants expressing either of the two different isoforms of activase. Thus, impairment of activase function under heat stress is not caused by oxidation of the redox-sensitive sulphydryls of the -isoform of activase. Instead, the results are consistent with thermal denaturation of activase under moderate heat stress, the effects of which on Rubisco activation would be enhanced when activase levels are suboptimal for photosynthesis. Key words: Carbon metabolism, heat stress, photosynthesis, Rubisco, temperature stress
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionSupplementary materialReferences |
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Photosynthesis is extremely susceptible to inhibition by moderate heat stress (Berry and Björkman, 1980). Of the components of photosynthesis that are impaired as temperature increases, ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco) activation has long been recognized as one of the most sensitive (Weis, 1981a, b; Kobza and Edwards, 1987). At permissive temperatures, Rubisco is maintained in an active state by the continued action of activase, a molecular chaperone that converts Rubisco from an inactive closed conformation to an active open conformation (Andrews, 1996; Spreitzer and Salvucci, 2002; Portis, 2003). Processes that inactivate Rubisco, including the synthesis of catalytic misfire products (Edmondson et al., 1990; Kane et al., 1998), increase with temperature to at least 50 °C (Salvucci and Crafts-Brandner, 2004b), whereas the ability of activase to reverse inactivation exhibits a relatively low temperature optimum (Eckhardt and Portis, 1997; Crafts-Brandner and Salvucci, 2002; Salvucci and Crafts-Brandner, 2004a, c). Consequently, Rubisco deactivates at elevated temperatures because increased rates of Rubisco deactivation are not offset by faster rates of reactivation by activase (Crafts-Brandner and Salvucci, 2002).
Activase catalyses ATP hydrolysis (Robinson and Portis, 1989), an activity that is required for it to act as chaperone towards Rubisco (Shen et al., 1991; Salvucci and Klein, 1994). Since ATP hydrolysis is inhibited by ADP, Rubisco activation by activase is responsive to changes in the ATP/ADP ratio (Robinson and Portis, 1989; Zhang and Portis, 1999). In many plant species, the relative sensitivity of activase to inhibition by ADP depends on the redox status of the longer, -form of activase. This form of activase, which is not present in some plant species (Salvucci et al., 1987), contains two cysteine residues near the C-terminus that can be oxidized to form a disulphide (Zhang and Portis, 1999). Reduction of this disulphide by thioredoxin-f decreases the sensitivity of the activase holoenzyme to inhibition by ADP, making activase responsive to changes in irradiance via its sensitivity to the redox status of the chloroplast (Zhang et al., 2002).
Estimates of the redox state of chloroplasts in heat-stressed leaves, determined from changes in the activation state of malate dehydrogenase, indicated that the chloroplast stroma becomes more oxidized under moderate heat stress (Schrader et al., 2004). This finding led to the suggestion of a cause and effect relationship between stromal oxidation and Rubisco inactivation. Studies by Kim and Portis (2005) with transgenic Arabidopsis plants appeared to lend support to this idea by showing that photosynthesis in plants expressing only the redox-regulated -isoform of activase was more sensitive to inhibition by moderate heat stress than photosynthesis in the wild type or in plants expressing only the non-redox regulated ß-isoform. However, the steady-state levels of activase were limiting for photosynthesis in the plants that expressed only the -isoform, but not in the plants that only expressed the ß-isoform. As the authors indicated, differences in the amount rather than the form of activase might explain the difference in thermotolerance between transgenic lines that expressed the different forms of activase.
To determine the role of stromal oxidation and activase amount in the inactivation of Rubisco, a transgenic Arabidopsis line, 
43, was produced that expresses lower amounts of the non-redox-regulated ß-isoform of activase. For additional comparison, transgenic plants were also produced that expressed the ß-isoform of activase from the Antarctic hairgrass, Deschampsia antarctica. Activase from D. antarctica was previously shown to have an exceptionally low temperature optimum for activity (Salvucci and Crafts-Brandner, 2004c). The temperature response of photosynthesis and Rubisco activation was determined in plants from these two lines and compared with the responses of wild-type plants and the transgenic plants described previously by Kim and Portis (2005). The results are inconsistent with an involvement of stromal oxidation in the loss of Rubisco activation under moderate heat stress.
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Materials and methods |
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Plant material
Transgenic Arabidopsis thaliana plants expressing near wild-type levels of the ß-isoform and suboptimal levels of the
-isoform have been described previously (Zhang et al., 2002; Kim and Portis, 2005). Arabidopsis plants expressing suboptimal levels of the Arabidopsis and D. antarctica ß-isoform of activase were produced by Agrobacterium-mediated transformation of the activase-deficient rca mutant. A full-length cDNA for the coding region of the ß-isoform of activase from these species (Salvucci et al., 2004c) containing the Arabidopsis activase transit peptide was constructed using polymerase chain reaction (PCR). The Arabidopsis cDNA was engineered to include nucleotides that encoded an eight amino acid S-tag (Skerra and Schmidt, 2000) attached to the C-terminus via a serine–alanine linker. The resulting cDNAs were cloned into the binary expression vector pMDC32 (Curtis and Grossniklaus, 2003) via the pENTR/D-TOPO vector using Gateway clonase technology, which is based on bacteriophage 
site-specific recombination (Invitrogen, Carlsbad, CA, USA). After confirmation by nucleotide sequencing, expression cassettes were transferred into Agrobacterium strain GV3850. Arabidopsis plants were transformed using a floral dip method (Clough and Bent, 1998). Positive transformants were identified by selecting kanamycin-resistant seedlings. T3 lines homozygous for a single active T-DNA insert were used for further experiments. Wild-type and transgenic plants were grown in air at 23 °C under an irradiance of 250 µmol photons m–2 s–1 with a 10 h light/14 h dark photoperiod.
Gas exchange and fluorescence measurements
The gas exchange of attached leaves was measured at air levels of CO2 (internal CO2 
280 µbar) and either 202 or 9.6 mbar O2 on 4–8-week-old plants (see text) using a Li-Cor 6400 as described previously (Salvucci and Crafts-Brandner, 2004c). Control plants were measured after at least 1 h at 23 °C. Heat stress was imposed by increasing the temperature of the growth chamber and the leaf cuvette from 23 °C to 37.5 °C over a 15 min period and then measuring gas exchange after 1 h at the higher temperature. This temperature was sufficient to cause moderate (<50%) inhibition of net photosynthesis in wild-type plants (see below). The relative humidity in the chamber was maintained at 80% during the treatment to ensure that leaf temperatures were similar to air temperatures. Chlorophyll fluorescence of attached leaves was measured at 250 µmol photons m–2 s–1 as described previously (Salvucci and Crafts-Brandner, 2004c). For fluorescence measurements, the temperature of the growth chamber was increased in increments of 2–5 °C. Fluorescence measurements were made after 20 min at each temperature. The results presented are the means ±SEM of individual measurements on 6–10 separate plants.
Rubisco activation
Initial and total Rubisco assays were conducted at 25 °C as described previously (Salvucci et al., 1986; Salvucci and Crafts-Brandner, 2004c), except that 1 mM phenylmethylsulphonyl fluoride (PMSF) and 10 µM leupeptin were included in the extraction buffer. Leaf discs were excised from intact plants and immediately frozen in liquid N2. Heat stress was imposed as described above for the gas exchange measurements and plants were sampled after 1 h of exposure to control or high temperature. Duplicate assays were conducted on each sample, each sample consisting of two discs each from a separate plant. The results presented are the means ±SEM of 3–5 samples.
Protein determination and analysis
Soluble protein was determined by a dye binding assay (Bradford, 1976). Methods for SDS–PAGE and immunoblots have been described previously (Salvucci et al., 2001). The levels of activase in leaf extracts of 43 plants were determined by image analysis of immunoblots using serial dilutions of purified recombinant Arabidopsis and D. antarctica activase as standards. Recombinant activase was purified from Escherichia coli cells as described previously (Salvucci and Crafts-Brandner, 2004c). For immunoblots, leaf discs were collected on the same day that gas exchange and Rubisco activation measurements were conducted and from the same cohort of plants. Discs were extracted in the same extraction buffer used for the activity measurements.
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Results |
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Activase levels and plant growth
Wild-type Arabidopsis plants express approximately equal amounts of the 46 kDa redox-regulated
- and 43 kDa non-redox-regulated ß-isoforms of activase (Fig. 1; Salvucci et al., 1997). The transgenic lines rwt46 and rwt43 described previously (Kim and Portis, 2005) expressed reduced amounts of the - and ß-isoforms of Arabidopsis activase, respectively. The amount of activase in the rwt46 plants, 51% of the total amount in wild type, was insufficient to support wild-type rates of photosynthesis, whereas the amount in rwt43, 71% of the total amount in wild type, was adequate for wild-type rates of net photosynthesis (Zhang et al., 2002; also see below).
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The transgenic line,
43, constructed for this study expressed reduced amounts of the ß-isoform of Arabidopsis activase relative to the level of ß-isoform in the wild type. The amount of activase in the leaves of 43 plants was 12% of the total (i.e. - plus ß-isoform) amount in wild-type leaves based on immunoblots (Fig. 1). The transgenic line, Da, also expressed reduced amounts of just the ß-isoform of activase, but the activase was from the Antarctic hairgrass, D. antarctica (Salvucci et al., 2004c). The amount of D. antarctica activase in Da plants was 10% of the total amount of activase in wild-type Arabidopsis based on immunoblots.
The 43 plants grew well in air, although their growth was slower than the wild type under the short day growth conditions used in this study. Above-ground biomass for 1-month-old plants was 1.56±0.14 and 0.67±0.03 g–1 FW plant or 0.112 and 0.031 g–1 DW plant for wild-type and 43 plants, respectively. At this stage of development, the difference in biomass between wild type and the 43 plants represented <1 week of growth. The Da plants that expressed activase from D. antarctica looked normal and reached a similar size to the wild type, but grew much more slowly than the wild type. Consequently, these plants required 8 weeks to accumulate the equivalent amount of biomass to 4-week-old wild-type plants.
Response of photosynthesis to moderate heat stress
Net photosynthesis in air at 23 °C was similar in the wild type and the transgenic line, rwt43, but reduced in the transgenic line rwt46 (Table 1). The 43 plants exhibited photosynthetic rates that were only 53% of the wild type, while the Da plants had even lower photosynthetic rates. Thus, at the control temperature of 23 °C, net photosynthesis was limited by the amount of activase in 43 and rwt46 plants, the two transgenic lines with reduced amounts of Arabidopsis activase, and in Da transgenic Arabidopsis plants that expressed reduced amounts of the D. antarctica activase.
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When Arabidopsis plants were exposed to a moderate heat stress of 37.5 °C, net photosynthesis in air was inhibited to a similar extent in wild-type and rwt43 plants, but inhibition was much greater for the rwt46 plants (Table 1). These results were similar to those reported previously by Kim and Portis (2005). Net photosynthesis in the two new lines with reduced levels of activase,
43 and Da, was also much more sensitive to inhibition by moderate heat stress than plants expressing wild-type levels of activase. The Da plants were the most sensitive to moderate heat stress, exhibiting net CO2 evolution in the light in air at 37.5 °C. For all transgenic lines, transpiration rates increased at the higher temperature, indicating that stomatal conductance was not reduced under moderate heat stress (data not shown).
The effect of moderate heat stress on photosynthesis was also examined at 9.6 mbar O2 to minimize interference from photorespiration and to eliminate the possibility that ribulose 1,5-bisphosphate (RuBP) regeneration was limiting for photosynthesis under moderate heat stress (Wise et al., 2004). Net photosynthesis was inhibited at 37.5 °C under low O2, although the extent of inhibition was less than at air levels of O2. Net photosynthesis in transgenic lines that expressed reduced levels of either isoform of activase exhibited greater sensitivity to inhibition by moderate heat stress than in wild-type plants with normal amounts of activase. As in air, net photosynthesis of the Da plants was the most sensitive to inhibition by moderate heat stress.
The temperature response of the operating efficiency of photosystem II (
PSII) was determined in the wild type and the transgenic lines as an additional and independent measure of the relative sensitivity of photosynthesis to inhibition by elevated temperatures. For both wild-type and rwt43 plants, gradual temperature increases up to 45 °C had little effect on PSII (Fig. 2). By contrast, PSII decreased precipitously as the temperature increased above 35 °C in transgenic lines rwt46 and 43 with reduced levels of activase. At 23 °C, the PSII was already at the low value of 0.45 in the Da plants, making it difficult to measure further decreases in PSII with temperature.
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Response of Rubisco activation to moderate heat stress
To determine if the inhibition of photosynthesis by moderate heat stress is accompanied by changes in Rubisco activation, the initial extractable activity and fully carbamylated activities of Rubisco were measured in wild-type Arabidopsis and the transgenic lines. At 23 °C, initial Rubisco activity was markedly reduced in the three transgenic lines with reduced rates of net photosynthesis and lower levels of activase protein compared with the wild type, but not in the rwt43 line that had sufficient activase for wild-type rates of net photosynthesis (Table 2). The
Da plants had the lowest initial activity, whereas the rwt46 and 43 plants had similar activities equivalent to 60% of the wild-type.
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At 23 °C, the activation state (initial/total activities) of Rubisco was <100% in the rwt46,
43 and especially the Da transgenic plants. By contrast, the initial activities of wild-type and rwt43 plants were slightly greater than the ‘total’ activities measured after incubation for 5 min or 10 min with high CO2 and Mg2+ to carbamylate the enzyme ‘fully’. Various control experiments including extract dilution experiments, time-course experiments, inclusion and omission of protease inhibitors, and experiments involving pre-incubation of RuBP with components of the extraction media failed to resolve the question of how Rubisco activation in wild-type and rwt43 plants could be >100% (data not shown). However, findings somewhat related to these were reported by He et al. (1997). These investigators presented evidence for an influence of activase in promoting the activity of carbamylated Rubisco. The data presented here also suggest the possibility that Rubisco might assume a ‘hyperactive’ conformation in vivo that is slowly lost upon extraction and dilution of Rubisco. If so, very rapid extraction and assay of initial activity might ‘capture’ a form of the enzyme that is subsequently lost upon incubation.
The initial activity of wild-type Arabidopsis and the four transgenic lines was considerably lower after a 1 h exposure to moderate heat stress compared with the control temperature. As shown previously for cotton, wheat, and oak (Feller et al., 1998; Haldimann and Feller, 2004), total activities were largely unaffected by exposure to 37.5 °C (Table 2). Thus, changes in initial activity mirrored changes in the activation state. At both 23 °C and 37.5 °C, the activation state of the Da plants was lowest among the transgenic lines, while rwt43 exhibited the highest activation state, even higher than the wild type. Rubisco activation in rwt46 and 43 plants was similar at 23 °C, but was reduced to a greater extent by moderate heat stress in the rwt46 plant than in the 43 plants.
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionSupplementary materialReferences |
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The essential role of activase in maintaining Rubisco in an active conformation was initially established in studies of an Arabidopisis mutant deficient in activase protein (Salvucci et al., 1985, 1986). The results were later verified using antisense technology to reduce the level of activase in transgenic Arabidopsis, tobacco, rice, and Flaveria plants (Mate et al., 1993; Jiang et al., 1994; Eckardt et al., 1997; Jin et al., 2004; von Caemmerer et al., 2005). In every case, transgenic plants with drastically reduced amounts of activase had lower rates of net photosynthesis, even in atmospheres containing elevated CO2. Since the central function of activase is to keep Rubisco active sites free of tight-binding inhibitors, these results indicate that when the amount of activase is reduced below a critical threshold amount, the remaining activase is insufficient to service the available Rubisco molecules.
Direct measurements of xylulose bisphosphate synthesis have shown that the rate of catalytic misfire by Rubisco increases with increasing temperature to at least 50 °C, exhibiting the same Q10 as the increase in catalytic activity (Salvucci and Crafts-Brandner, 2004b). This epimer of RuBP, which is produced directly at the active site by misprotonation of the enediol reaction intermediate (Edmonson et al., 1990), inactivates Rubisco by trapping sites in a closed, dead-end complex. This complex is slow to open without the intervention of activase. It is proposed that Rubisco deactivates at elevated temperatures because the increased rates of synthesis of xylulose bisphosphate and possibly other (Kane et al., 1998; Pearce and Andrews, 2003) catalytic misfire products are not offset by faster rates of reactivation by activase. Recently, Kim and Portis (2006) showed that the rate but not the final extent of Rubisco deactivation increases with temperature, but the differences were less significant at physiological concentrations of Mg2+. These investigators suggested a role for increased decarbamylation in the deactivation of Rubisco with temperature, particularly at physiological concentrations of Mg2+ (Kim and Portis, 2006).
Based on the relationship between activase amount and photosynthesis described above, it would be expected that photosynthesis in plants with reduced amounts of activase should exhibit greater sensitivity to inhibition by moderate heat stress than in plants with wild-type amounts of activase. With less activase to service the available Rubisco, even slight increases in misfire product production with temperature would cause Rubisco to deactivate and photosynthesis to decline more precipitously in plants with reduced amounts of activase. Exacerbating the decrease in Rubisco activation is the relatively low temperature optimum of activase. A lower activase activity at elevated temperatures would reduce the rate of reactivation, further increasing the rate of Rubisco deactivation (Salvucci and Crafts-Brandner, 2004a, b). Thus, the greater sensitivity of photosynthesis to inhibition by moderate heat stress observed with the rwt46, 43, and Da plants is entirely consistent with a proposed mechanism for photosynthetic inhibition based on relative rates of deactivation and reactivation. That photosynthesis is more thermotolerant in transgenic tobacco plants with reduced amounts of Rubisco (SJ Crafts-Brandner and ME Salvucci, unpublished data) provides further support for this mechanism. Compared with the wild type, the higher ratio of activase: Rubisco in these plants should be capable of offsetting the faster rates of Rubisco deactivation at higher temperatures.
Stromal oxidation accompanies moderate heat stress and is thought to be a consequence of thylakoid leakiness (Schrader et al., 2004). Based on this observation, Schrader et al. (2004) suggested that a more oxidized stroma inhibits photosynthesis, possibly by inhibiting activase. However, Kim and Portis (2005) showed that photosynthesis in transgenic Arabidopsis plants with thylakoid membranes that are less permeable to ion leakage due to alterations in the fatty acid composition showed no improvement in thermotolerance. Measurements of the activation state of malate dehydrogenase indicated that stromal oxidation initially increased in wild-type Arabidopsis plants when the temperature was increased from 25 °C to 30 °C, but remained constant with additional increases in temperature (Kim and Portis, 2005). Thus, direct evidence for membrane leakiness during moderate heat stress is lacking, and the response of stromal oxidation to temperature does not always correlate with inhibition of photosynthesis.
The data presented here and in previous studies also argue against the proposed involvement of stromal oxidation as a causative agent in the temperature inhibition of activase (Schrader et al., 2004). While the redox-sensitive disulphide of the -isoform of activase could be adversely affected by increased stromal oxidation, the results with transgenic Arabidopsis lines expressing suboptimal levels of either the 43 (43) or 46 kDa (rwt46) activase isoform showed that photosynthesis in both lines was sensitive to inhibition by moderate heat stress. Similarly, Rubisco activation decreases under moderate heat stress in plant species such as tobacco and maize that express only the non-redox-regulated isoform of activase (Crafts-Brandner and Salvucci, 2000, 2002). Thus, plants that expressed the form of activase that is insensitive to changes in redox state were affected by moderate heat stress in a similar manner to plants that expressed just the redox-sensitive form or both forms of activase. Photosynthesis and Rubisco activation in the 43 and rwt46 lines were much more sensitive to moderate heat stress than in the wild type, indicating that the amount rather than the isoform was the important factor for determining heat sensitivity. It should be noted that Rubisco activation was slightly more sensitive to moderate heat stress in the rwt46 compared with the 43 plants, and net photosynthesis was more sensitive to inhibition by moderate heat stress under low O2 conditions. This result is consistent with the finding that the -isoform is the more heavily regulated of the two activase isofoms (Zhang and Portis, 1999; Zhang et al., 2002) and could reflect a slightly greater sensitivity of this form of activase to changes in redox, ATP/ADP ratio or other conditions in the chloroplasts.
The lowest photosynthetic rates and Rubisco activation state were observed with the Da plants that expressed activase from the Antarctic hairgrass. Even though the amount of activase in these plants was similar to the amount in the 43 plants, their growth and photosynthesis rates were significantly slower under control temperatures. In addition, photosynthesis and Rubisco activation in the Da plants exhibited greater sensitivity to inhibition by moderate temperature than in either of the transgenic lines expressing reduced amounts of Arabidopsis activase. While it is tempting to speculate that the greater sensitivity of the Da plants was caused by the more thermolabile activase in these plants (Salvucci et al., 2004c), direct measurement of the ability of purified D. antarctica activase to activate Arabidopsis Rubisco showed that the interaction with Rubisco was somewhat compromised (see supplementary material at JXB online). Reduced interaction with Rubisco would be tantamount to reducing the amount of activase, which the present results show would lead to greater heat sensitivity and would explain the poor performance of the Da plants under control temperatures. Thus, future attempts to improve the thermotolerance of activase will require alterations in activase structure that improve its temperature response without adversely affecting its interaction with Rubisco.
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Supplementary material |
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Data showing that purified activase from D. antarctica was less effective than purified activase from Arabidopsis in activating Arabidopsis Rubisco is available as supplementary material at JXB online. Recombinant versions of the same forms of the enzymes that were expressed in the
Da and 43 transgenic plants, i.e. the ß-isoform of D. antarctica activase and the ß-isoform of Arabidopsis activase containing an S-Tag, respectively, were used for the comparison.
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Acknowledgements |
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The authors wish to acknowledge the technical assistance of Nancy Parks.
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Abbreviations |
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RuBP, ribulose 1,5-bisphosphate; Rubisco, ribulose 1,5-bisphosphate carboxylase/oxygenase.
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