Journal of Experimental Botany, Vol. 53, No. 369, pp. 609-620,
April 1, 2002
© 2002 Oxford University Press
Review Article |
Variation in the kcat of Rubisco in C3 and C4 plants and some implications for photosynthetic performance at high and low temperature
Department of Botany, University of Toronto, 25 Willcocks Street, Toronto, ON M5S3B2 Canada
Received 5 November 2001; Accepted 21 December 2001
 |
Abstract |
|---|
 Top Abstract IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
The capacity of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) to consume RuBP is a major limitation on the rate of net CO2 assimilation (A) in C3 and C4 plants. The pattern of Rubisco limitation differs between the two photosynthetic types, as shown by comparisons of temperature and CO2 responses of A and Rubisco activity from C3 and C4 species. In C3 species, Rubisco capacity is the primary limitation on A at light saturation and CO2 concentrations below the current atmospheric value of 37 Pa, particularly near the temperature optimum. Below 20 °C, C3 photosynthesis at 37 and 68 Pa is often limited by the capacity to regenerate phosphate for photophosphorylation. In C4 plants, the Rubisco capacity is equivalent to A below 18 °C, but exceeds the photosynthetic capacity above 25 °C, indicating that Rubisco is an important limitation at cool but not warm temperatures. A comparison of the catalytic efficiency of Rubisco (kcat in mol CO2 mol-1 Rubisco active sites s-1) from 17 C3 and C4 plants showed that Rubisco from C4 species, and C3 species originating in cool environments, had higher kcat than Rubisco from C3 species originating in warm environments. This indicates that Rubisco evolved to improve performance in the environment that plants normally experience. In C4 plants, and C3 species from cool environments, Rubisco often operates near CO2 saturation, so that increases in kcat would enhance A. In warm-habitat C4 species, Rubisco often operates at CO2 concentrations below the Km for CO2. Because kcat and Km vary proportionally, the low kcat indicates that Rubisco has been modified in a manner that reduces Km and thus increases the affinity for CO2 in C3 species from warm climates.
Key words: Amaranthus, Chenopodium, CO2 response, C3 and C4 photosynthesis, Rubisco, temperature response.
|
Introduction |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
The evolution of C4 photosynthesis resulted in the localization of Rubisco into the bundle-sheath compartment where CO2 concentration is higher than the surrounding atmosphere (Edwards et al., 1985
). At moderate temperatures of 20–30 °C, Rubisco in C4 plants encounters CO2 concentrations close to saturation, and the potential for photorespiration is low (von Caemmerer and Furbank, 1999). By contrast, CO2 concentrations in C3 plants at 20–30 °C are near the Km for CO2 of Rubisco, and photorespiration can be high (Jordan and Ogren, 1984; Sharkey, 1988). As a result of the high CO2 environment that allows Rubisco to function near CO2 saturation, C4 species at 20–30 °C require one-third to one-quarter as much Rubisco as C3 species to maintain a given CO2 assimilation rate (Brown, 1978; Sage et al., 1987; Long, 1999). This reduced requirement explains the 60–80% lower Rubisco content of C4 plants relative to C3 species of similar life form (Long, 1999). In many C4 species, the kinetic properties of Rubisco are also modified from the ancestral C3 isozyme to yield a type with kinetics similar to CO2-concentrating algae. For example, the kcat and Km of Rubisco from C4 grasses can be twice that of C3 grasses and dicots, indicating that C4 plants evolved a type of Rubisco that more efficiently utilizes high CO2 (Yeoh et al., 1980, 1981; Seemann et al., 1984; Sage and Seemann, 1993).
At moderate temperatures, the control of Rubisco and other limitations over photosynthetic capacity are well understood, and robust theoretical models of C3 and C4 photosynthesis are now available (Harley and Sharkey, 1991; von Caemmerer and Furbank, 1999; von Caemmerer, 2000). Below moderate temperatures, the understanding of photosynthetic limitations is less certain In early work, Rubisco was suggested to limit C4 photosynthesis below 20 °C (Björkman and Pearcy, 1971; Caldwell et al., 1977; Pearcy, 1977). Subsequent research emphasized chilling sensitivity and limitations arising from cold-lability of light-harvesting and C4-cycle enzymes (reviewed in Leegood and Edwards, 1996). Recent work using C4 plants from cooler climates has shown that deficiencies in light-harvesting and PPDK do not appear following chilling, indicating that C4 photosynthesis is not inherently limited by these processes (Simon and Hatch, 1994; Leegood and Edwards, 1996; Matsuba et al., 1997; Long, 1999). Instead, as indicated by early work, Rubisco appears to exert high control over net CO2 assimilation (A) at low temperature in chilling-tolerant C4 species (Pittermann and Sage, 2000, 2001). In chilling-tolerant C3 species, the capacity of starch and sucrose synthesis to regenerate Pi for photophosphorylation commonly limits A at low temperatures (8–15 °C), but primarily when plants were grown at moderate conditions (Sage and Sharkey, 1987; Labate and Leegood, 1988; Labate et al., 1990). When plants are grown in cool conditions, the capacity for Pi regeneration apparently increases as indicated by the recovery of O2 and CO2 sensitivity of A (Cornic and Louason, 1980; Huner et al., 1986, 1993; Mawson et al., 1986; Holaday et al., 1992, 1993; Paul et al., 1990), and the control over A can shift to either Rubisco capacity or electron transport capacity (Mawson and Cummins, 1989; Holaday et al., 1992; Leegood and Edwards, 1996).
Similarly, at temperatures above 30 °C, the controlling role of Rubisco over C3 and C4 photosynthesis is uncertain. From gas exchange analyses, C3 leaves exposed to high temperature often maintain intercellular CO2 levels that fall on the initial slope of the photosynthetic CO2 response curve (Sage and Sharkey, 1987; Sage et al., 1990a, 1995). This is a region commonly thought to reflect a limitation in Rubisco capacity (von Caemmerer, 2000). Alternatively, in the C3 weed Chenopodium album, whole-chain electron transport exhibits an identical temperature optimum as photosynthesis, indicating RuBP regeneration capacity above the temperature optimum may be a principal limitation on A (Sage et al., 1995). Rubisco also deactivates at high temperature in C3 species (Weis, 1981; Kobza and Edwards, 1987; Sage et al., 1990a; Vu et al., 1997). This could be a regulatory response to a limitation in RuBP regeneration, as proposed for C. album (Sage et al., 1995). Alternatively, as shown for wheat, cotton and tobacco, it may be a direct effect of high temperature on the carbamylation state, in which case Rubisco capacity declines, lowering A in the process (Feller et al., 1998; Law and Crafts-Brandner, 1999; Sharkey et al., 2001). In C4 plants, Rubisco does not appear to limit A at elevated temperature because its in vitro capacity is well in excess of the net photosynthetic rate (Pittermann and Sage, 2000, 2001).
To understand plant performance in the field, it is necessary to have a comprehensive picture of Rubisco performance across a range of temperatures. In addition, because the modern flora evolved in atmospheres that were substantially different from those of today, consideration of Rubisco use and photosynthetic temperature responses across a range of CO2 concentrations is necessary. This report reviews the current understanding of Rubisco control over C3 and C4 photosynthesis at different temperature and CO2 conditions. New data on photosynthetic and Rubisco temperature responses are presented, including results that show the kcat of Rubisco varies between C3 plants originating in cool versus warm habitats.
|
Materials and methods |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Plant material and culture
Plants were grown in four locations, (1) the greenhouse of the University of Georgia, Athens (UGA); (2) in fields in the vicinity of Athens, Georgia USA (Athens); (3) outdoors in 20 l pots of soil at the roof-top garden of the Botany Department, University of Toronto (UTB) or (4) unmanaged fields near the campus of the University of Toronto (UT). Samples for Rubisco assay were collected during summer months at 25–35 °C by removing 2–4 cm2 of leaf material and freezing it immediately in liquid nitrogen. Samples were stored in liquid nitrogen or in a -70 °C freezer until assay. Leaves were sampled at light intensities above 1000 µmol m-2 s-1. All cultivated plants were well fertilized, using standard greenhouse fertilizer mixes. All plants sampled in field locations were selected to have a vigorous appearance and deep green colour.
Plants sampled for Rubisco assay were Amaranthus retroflexus (seed from Prague, Czech Republic; C4; UTB, sampled at 30 °C); Arachis hypogea (escaped peanut, C3, Athens, 30 °C); Capsicum chinense (Habanero chile pepper, C3, Athens, 30 °C); Chenopodium album (C3; Prague seed, UTB, 28 °C); Cynodon dactylon (Bermuda grass, C4, Athens, 35 °C), Digitaria sanguinalis (crabgrass, C4, Athens, 35 °C); Flaveria trinervia (Harold Brown collection No. 84-1, C4, UGA, 33 °C); Flaveria pringlei (Harold Brown collection No. 85-207; C3, UGA, 33 °C; Gossypium hirsutum (cotton, cv. Coker 201, C3; 30 °C); Oryza sativa (rice, cv. IR42, C3, UGA 30 °C); Muhlenbergia montanum (mountain muhly, grown from culms collected at Kenosha Pass, Colorado; C4, UTB, 30 °C); Portulaca oleracea (C4, Athens, 35 °C); Poa arctica (Hoosier Pass Colorado source; C3, UTB, 25 °C); Poa pratensis (bluegrass, C3, UT, 25 °C); Pueraria lobata (kudzu, C3, Athens, 30 °C); Solanum tuberosum (potato cv. Eigen, UGA, 25 °C); Zoysia japonica (C4, Athens, 35 °C).
Gas exchange analysis
The temperature and CO2 response of photosynthesis was determined for Amaranthus retroflexus and Chenopdium album plants grown outdoors in 20 l pots at the roof-top garden at UTB. The plant material originated from seed collected at the north-eastern outskirts of Prague, Czech Republic, 50° N latitude. All gas exchange responses were measured using a temperature-regulated, null-balance gas exchange system (Pittermann and Sage, 2000). To determine the temperature response of the net rate of CO2 assimilation (A), leaves were first equilibrated at the measurement CO2 level and 25–30 °C. Leaf temperature was then raised to the maximum measurement temperature near 40 °C, and lowered in 4–5 °C steps to 5–10 °C. Gas exchange parameters were determined at each step after a 15–30 min equilibration period. The rate of net CO2 assimilation was determined at approximately 27 °C before and after the elevation in temperature to the maximum measurement value. If the two measurements did not correspond, the measurement was discontinued. The CO2 response of photosynthesis was determined by first equilibrating leaves in air at the measurement temperature, after which CO2 was reduced to the minimum measurement level. Gas exchange parameters were determined as CO2 was increased in a series of steps to maximum measurement values. Measurements were conducted just above the light saturation point for A. At temperatures above 20 °C, the light saturation point was greater than 1500 µmol m-2 s-1. Below 20 °C, the light saturation point declined with reductions in temperature and the measurement light intensity was reduced by an equivalent amount as described earlier (Pittermann and Sage, 2000).
Rubisco assay
To determine the temperature response of the activity of fully activated Rubisco, leaves were rapidly ground in a pH 8.0 extraction buffer (Pittermann and Sage, 2000). The extract was then centrifuged at 5000 g for 60 s, and the Rubisco in the supernatant was allowed 5 min to reach full activation. Rubisco activity was determined by assaying the rate at which 14CO2 was incorporated into acid-stable products during a 30 or 60 s incubation period (Sage and Seemann, 1993; Sage et al., 1993). The assay buffer was 100 mM Bicine (pH 8.2) with 1 mM Na-EDTA, 5 mM dithiothreitol, 28 mM MgCl2, 15 mM [14C]NaHCO3 (20 Bq nmol-1), 2 mM ATP, 1.5 mM ribose 5-phosphate, 1 unit ml-1 ribose-5-phosphate isomerase, and 0.1–0.3 units ml-1 ribulose-5-phosphate kinase. RuBP (1.5 mM) was generated in vitro by isomerization and phosphorylation of ribose 5-phosphate. The drift in pH with temperature was less than ±1.5 pH units between 4 °C and 40 °C, which did not significantly affect measured activity values. Assays were conducted at a range of temperatures between 0 °C and 45 °C using water baths to control leaf temperature. Four to five baths were used to minimize the time between grinding and assaying of Rubisco. At most, 30 min elapsed between a grind and the final assay from a given extraction. No loss of Rubisco activity was observed over this period if the extract was left on ice prior to assay.
To minimize problems associated with incubation time after extraction and exchange of 14C between the assay buffer and the atmosphere, the assay buffer remained covered at 0 °C except during a 120 s period to equilibrate with the water bath temperature. To minimize variation between assay days, which can be a problem due to differences in the 14C source material, pairs of species giving the more interesting comparisons were assayed at the same time using the same extraction and assay buffer. For example, samples of the C3 and C4 Flaveria species were assayed on the same day in an alternating sequence. This ensured that any differences observed were due to differences in the species rather than the assay conditions.
Rubisco content was determined by measuring the binding of [14C]-carboxyarabinitol bisphosphate (CABP) to the Rubisco catalytic sites, with rabbit anti-Rubisco antibodies being used to precipitate the CABP-Rubisco complexes (Sage and Seemann, 1993). The amount of [14C]CABP bound to Rubisco was estimated using scintillation spectroscopy after filtration through a supor-450 filter (Gelman Science, Ann Arbor, MI 48106). The binding stoichiometry of CABP to Rubisco was assumed to be 6.5 CABP molecules per molecule of Rubisco (Butz and Sharkey, 1989). The kcat of Rubisco (mol CO2 mol-1 Rubisco catalytic sites s-1) was determined by dividing the activity of Rubisco by the content determined for a given leaf sample. To ensure the assay was consistent over the experimental period, the kcat of bean (Phaseolus vulgaris) was routinely determined. If the bean kcat shifted from previously determined values (Sage et al., 1993), the assay was halted until the problem was rectified.
|
Results |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Temperature and CO2 responses in Chenopodium album and Amaranthus retroflexus
In the C3 species Chenopodium album exposed to Pleistocene levels of CO2 (18.5 Pa), the net CO2 assimilation rate (A) was moderately affected by temperature below 20 °C, and it exhibited a broad temperature optimum between 20 °C and 30 °C (Fig. 1
). At higher CO2 levels, the temperature response of A below 25 °C was more pronounced, exhibiting a Q10 near 2. Below 18 °C, A was stimulated by rising CO2 concentration between 18 and 38 Pa, but not above 38 Pa. Above 20 °C, the relative stimulation of A by rising CO2 was increased below 38 Pa, and became pronounced above 38 Pa. In the C4 plant Amaranthus retroflexus, the temperature sensitivity of A was similarly enhanced by rising CO2 above 20 °C as observed in the C3 species (Fig. 1B). Below 18 °C, CO2 increase had little effect on the temperature response of A in contrast to the marked response observed above 20 °C.
|
In C. album, the Vmax of Rubisco measured in vitro was well in excess of the CO2 assimilation rate observed at the same temperature, with the discrepancy rising as temperature increased (Fig. 1A
). Using an estimate of Rubisco activity at 25 °C and the activation energy determined for C. album (Table 1), A was modelled assuming Rubisco capacity was the only limitation. At 38 Pa, modelled A corresponded to observed A at optimal temperatures, but was greater than observed A at sub-optimal temperatures. At 18.5 Pa, the modelled temperature response of A exhibited a similar response as measured A above 10 °C. At 68 Pa, by contrast, modelled A was greater than the measured A at all temperatures. In A. retroflexus, in vitro activities of Rubisco correspond to the observed rates of A at temperatures below 15–20 °C at all measurement CO2 levels, but are well in excess of A above 20 °C (Fig. 1B).
|
In C. album and A. retroflexus, the response of A to variation in intercellular CO2 (Ci) was similarly affected by temperature (Fig. 2
). Temperature had a relatively small effect on the initial slope of the A/Ci response in both species, but rising temperature markedly stimulated the CO2-saturated rate of A (Figs 2, 3). As a result, the CO2 saturation point of A increased with temperature in both photosynthetic types (Fig. 2). The operating Ci (the intercellular CO2 partial pressure corresponding to a given ambient CO2 partial pressure) increased slightly with declining temperature in both species, as indicated by the arrows for C. album or circled data points for A. retroflexus in Fig. 2.
|
|
Temperature responses of Rubisco in a variety of C3 and C4 species
The kcat of Rubisco at 16, 28 and 40 °C was consistently larger in C4 relative to C3 species (Table 1). C3 species originating from cool habitats exhibited Rubisco kcat values that were approximately 24% below that of C4 species, but 40–70% above the kcat values observed in C3 species from warm habitats. Activation energies ranged between 50 and 70 kJ mol-1 in the 17 species. No statistical differences in activation energy were observed between species differing in photosynthetic pathway or temperature environment although the majority of C3 species from warm habits exhibited activation energies greater than 60 kJ mol-1, while most cool-temperate C3 species, and C4 species, had Rubisco with activation energies below 60 kJ mol-1. The Q10 for all species ranged between 2.2 and 2.9 except for rice at temperatures below a breakpoint, where the Q10 was 4.1 (Fig. 4).
|
In all 17 species, the kcat of Rubisco increased exponentially with rising temperature between 5 °C and 40 °C (see Fig. 4
for four examples). Rubisco from C4 species commonly exhibited a higher kcat at a given temperature than C3 species. There was little evidence of a thermal break in the corresponding Arrhenius plots with the exception of rice, which exhibited a sharp break at 22 °C (Fig. 5). The Arrhenius responses slopes of the species were similar, except for the rice response below 20 °C. The important difference between the Arrhenius response was the y-axis intercept was lower in warm-habitat C3 species. Thus, the difference in Rubisco between warm-habitat C3 and the other two groups is not in the activation energy, but in the turnover capacity of the enzyme at a given temperature.
|
The difference between Rubisco from C3 plants of warm and cool habitats is well demonstrated by a comparison of the temperature response of Capsicum chinense and potato, Solanum tuberosum (Fig. 6
). Capsicum chinense, the Habanero chile pepper, originated in the lowland tropics of South America and grows best above 30 °C (RF Sage, personal observation). Potatoes originated in the high montane environments of South America and grow exclusively in cool climates or seasons where daytime temperatures rarely rise above 30 °C (Evans, 1993). Both are in the Solanaceae. In Habanero peppers, the kcat of Rubisco is lower than potato at all temperatures (Fig. 6A). Arrhenius plots also show the downward shift in the response of Rubisco in Habanero pepper compared to potato; however, the slopes of the responses were similar, as were the estimated activation energies (Table 1; Fig. 6B).
|
|
Discussion |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Photosynthetic limitation as a function of temperature in C3 and C4 plants
In the current atmosphere, the net rate of CO2 assimilation is often equivalent between ecologically similar C3 and C4 species at 25–30 °C. Photosynthesis is typically greater in C3 species below this temperature, but greater above it in C4 species (Pearcy et al., 1981
; Edwards et al., 1985; Sage and Pearcy, 1987, 2000). Increases in atmospheric CO2 are commonly thought to stimulate A in C3 species, but have a minimal effect in C4 species (Cure and Acock, 1986; Wand et al., 1999, 2001). This impression is biased, however, because research has emphasized CO2 responses above recent atmospheric CO2 levels of 33–37 Pa (Morison and Lawlor, 1999). When temperature responses at low CO2 are considered, C4 photosynthesis exhibits a similar response to rising CO2 as C3 species, in that the CO2 stimulation of A is minor at cool temperature while it is substantial at high temperature (Fig. 1). This interaction between low CO2 and temperature is important when considering the responses of C3 and C4 vegetation to CO2 variation in prehistoric times. During the past 2 million years, CO2 levels have varied between 18 and 28 Pa during glacial to interglacial cycles (Sage and Pearcy, 2000). Because C4 species largely occur in warmer habitats where greater CO2 sensitivity of A is expected, substantial reduction of C4 photosynthesis per unit area likely followed a decline in CO2 to 18 Pa during past glacial episodes.
The response of A to intercellular CO2 (Ci) is widely used to evaluate mechanisms controlling photosynthetic responses to environmental variation (Sharkey, 1985). In both C3 and C4 species, analysis of A/Ci responses show the CO2-saturated rate of A is markedly enhanced by rising temperature, while the initial slope has a small temperature response (Fig. 3; Kirschbaum and Farquhar, 1984; Sage and Sharkey, 1987; Sage et al., 1990a). Consequently, the CO2 saturation point increases with rising temperature such that at ambient CO2 levels below 40–50 Pa, the operating Ci corresponds to the initial slope region of the A/Ci response where CO2 sensitivity is high. Below 20 °C, the CO2 saturation point of both C3 and C4 photosynthesis declines to values that are below current air levels of CO2, such that the operating Ci falls on or near the CO2-saturated plateau. Hence, A has little response to rising CO2 at lower temperatures.
The biochemical limitations controlling A have been well described at moderate temperatures and robust theoretical models are available to interpret A/Ci responses in terms of the biochemical controls (von Caemmerer, 2000; see also the Wimovac photosynthesis program of Humphries and Long, 1995). At saturating light levels, the initial slope region of the A/Ci response is thought to reflect Rubisco limitations on A in C3 plants, and PEP carboxylase limitations in C4 plants (von Caemmerer and Furbank, 1999; von Caemmerer, 2000). The CO2-saturated rate of A reflects RuBP regeneration limitations in C3 plants, and either Rubisco, RuBP regeneration, and PEP regeneration limitations in C4 plants (Furbank et al., 1997; von Caemmerer and Furbank, 1999; von Caemmerer, 2000). The interpretation of the biochemical controls over the A/T response is less clear than the A/Ci response, although analysis of Rubisco activity and A/Ci responses at a range of temperatures allows for enough interpretation to contrast differences in the mechanisms controlling C3 and C4 temperature responses. In C. album, Rubisco activity in vitro is markedly greater than A at all but the lowest measurement temperatures (Fig. 1). This must be the case in C3 plants because in vivo, Rubisco activity in air is depressed below the Rubisco activity measured in vitro by the deficiency of substrate CO2, the presence of 21% O2, and possible depressions in the activation state of Rubisco (von Caemmerer and Farquhar, 1981; Sage et al., 1987, 1990b). CO2 levels in the chloroplast are reduced about 50% with respect to air levels of CO2 by diffusion restrictions in the boundary layer, stomata and mesophyll tissue (Evans and Loreto, 2000). Thus, in the current atmosphere, the CO2 concentration in the C3 chloroplast is near the Km of Rubisco at 25 °C, and below it above 30 °C. When enzyme kinetics, diffusion restrictions, O2 concentration, and CO2 supply are accounted for, predicted A calculated from the Rubisco capacity measured in vitro is often equal to measured A (von Caemmerer and Farquhar 1981, 1984; von Caemmerer and Quick, 2000). In C. album at 38 Pa CO2, modelled A, assuming Rubisco activity was limiting, was similar to measured A at the temperature optimum (Fig. 1). In accordance, the A/Ci response shows the operating Ci occurs in the initial slope region at the temperature optimum (about 31 °C) in C. album, indicating high Rubisco control over A.
Below the temperature optimum of C. album at 38 Pa, modelled A is greater than measured A, and A is minimally affected by CO2 enrichment above 38 Pa below 18 °C. This possibly reflects a ceiling on A established by a limitation in the capacity of starch and sucrose synthesis to regenerate Pi for photophosphorylation (Sage and Sharkey, 1987). A Pi-regeneration limitation is generally indicated by a lack of stimulation of A by rising CO2 at CO2 levels below 100 Pa where photorespiration occurs (Sharkey, 1985; Harley and Sharkey, 1991). If Rubisco or RuBP regeneration capacity were limiting, A would respond positively to increases in CO2, because a higher CO2 concentration inhibits photorespiration (Sharkey, 1988). The appearance of a strong CO2 response at the temperature optimum indicates the limitation on A at high CO2 shifts from Pi regeneration to Rubisco capacity or one of the components limiting the capacity for RuBP regeneration (Sage and Sharkey, 1987). Results presented here and in other studies indicate Rubisco is not limiting A at elevated CO2 because modelled Rubisco-limited A is in excess of observed A, and the operational Ci occurs on the plateau of the A/Ci response at all temperatures (von Caemmerer and Farquhar, 1981, 1984; Kirschbaum and Farquhar, 1984; Sage and Sharkey, 1987; Sage et al., 1990a). In addition, the capacity for electron transport in C. album has a similar temperature optimum as A at high CO2, indicating the capacity of RuBP regeneration is limiting A at warmer temperatures and high CO2 (Sage et al., 1995).
At 18 Pa CO2, modelled A in C. album has a similar response to temperature as measured A, except below 10 °C. A Rubisco limitation is generally assumed to predominate in C3 plants at low CO2 (von Caemmerer, 2000) and this is consistent with results presented here. The operating Ci corresponds to the initial slope of the A/Ci response at 23 °C and 31 °C, indicating a Rubisco limitation is present at warmer temperatures. The relatively flat temperature response of A at low CO2 is consistent with a Rubisco limitation, as is the low temperature effect on the initial slope of the A/Ci response (Kirschbaum and Farquhar, 1984; Sage et al., 1995). The reason for the flat temperature response of Rubisco-limited A, and hence the initial slope of the A/Ci response, is that the Km for CO2 and Vmax of Rubisco both have a similar Q10 (Berry and Raison, 1981). When this occurs, Rubisco activity at CO2 levels below the Km has a Q10 near 1.
In C4 plants, the ability of the leaf to concentrate CO2 around Rubisco allows Rubisco in vivo to function close to its CO2-saturated rate, as it does in vitro during the assay (Edwards et al., 1985; von Caemmerer and Furbank, 1999). Hence, when Rubisco capacity is limiting, its in vivo activity should correspond to the observed rate of A. This was the case at cooler temperatures, but not at temperatures above 20 °C. Notably, A at all CO2 levels exhibited a similar value below 16 °C, which corresponded to the measured Rubisco activity. These observations indicate that Rubisco capacity is a common limitation on A in A. retroflexus at lower temperatures. By contrast, at temperatures approaching and exceeding the temperature optimum, Rubisco capacity is well in excess of observed A, indicating Rubisco is non-limiting. Instead, the capacity for RuBP or PEP regeneration is a more likely limitation in cases where A is CO2 saturated (von Caemmerer and Furbank, 1999). If the temperature rise is high enough to cause the operational Ci to drop below the CO2 saturation point, PEP carboxylase activity could also become an important limitation on A at warmer temperature.
Two montane C4 grasses from the Rocky mountains, USA (Bouteloua gracilis and Muhlenbergia montanum) exhibited similar responses of A and Rubisco activity below 18 °C as observed in A. retroflexus (Pittermann and Sage, 2000, 2001). All three species have some degree of cold tolerance that is associated with occurrence at high altitude or northern latitude (Pittermann and Sage, 2000, 2001). Together, the results from these species indicate that Rubisco is a widespread limitation on A in cold-tolerant C4 plants in low temperature, but not at elevated temperature. If so, then photosynthetic acclimation and adaptation to low temperature in C4 species could involve an enhancement in Rubisco content to remove this limitation. Pittermann and Sage examined this possibility in B. gracilis and M. montana, but saw no evidence that ecotypes from higher altitude, nor plants grown in chilling conditions, enhanced Rubisco capacity (Pittermann and Sage, 2000, 2001). By contrast, Osmond et al. noted that C4 Atriplex species from cold climates have proportionally greater Rubisco contents than C4 species from warm climates, indicating there may be some compensation for limiting Rubisco capacity at low temperature (Osmond et al., 1982).
In the experiments presented here, the vapour pressure difference between leaf and air was maintained below 1.5 kP except at high temperature. Under these conditions, A. retroflexus and C. album operate at high Ci/Ca ratios for their respective photosynthesis types, and stomata show little response to temperature. In natural environments, VPD usually increases with rising temperature (Schulze and Hall, 1982). This will usually reduce stomatal conductance and Ci/Ca such that the operating Ci is more likely to correspond to the initial slope region of the A/Ci response (Sage and Sharkey, 1987). At the biochemical level, this will increase the temperature at which Rubisco controls A in C3 plants and PEP carboxyase controls A in C4 plants, and will result in higher CO2 responsiveness of A than may be otherwise expected.
The significance of differences in the kcat of Rubisco
Previous work has shown that Rubisco from most C4 plants has a higher catalytic turnover rate at 25–30 °C than most C3 plants (expressed either as molar activity or kcat; Seemann et al., 1984; Sage and Seemann, 1993). Associated with this is a tendency for C4 Rubisco to have a lower specificity for CO2 relative to O2 than Rubisco from C3 species (Badger, 1987; von Caemmerer and Quick, 2000). These results demonstrate that Rubisco in most C4 plants has evolved into a type that is better adapted to exploit the high-CO2 conditions in the bundle sheath compartment (Seemann et al., 1984; Badger, 1987). Unlike the trends between C3 and C4 Rubisco, however, no trend in catalytic performance has previously been identified between Rubisco from C3 species of different habitats, although it is recognized that the kcat of Rubisco can vary substantially between C3 species (Seemann et al., 1984; Evans and Austin, 1986). Here, enough species have been characterized to identify a pattern where warm-habitat C3 plants have a lower kcat for Rubisco than cool-habitat C3 species. Consistently, Rubisco kcat was 24–39% lower in the C3 species from warm habits (cotton, Phaseolus bean and soybean) than cool habit species (spinach and wheat) (Seemann et al., 1984).
A higher kcat of Rubisco from C4 species is advantageous because less enzyme is required for a given photosynthesis rate if CO2 levels around Rubisco are near saturation (Seemann et al., 1984). Increased catalytic turnover is associated with a reduced affinity (increased Km) for CO2, so the cost of the higher kcat in C4 plants is lower affinity and specificity for CO2 (Badger, 1987; von Caemmerer and Quick, 2000). Because Rubisco in C4 plants operates in a very high CO2 environment, the cost of reduced affinity for CO2 is negligible and the advantages of the higher kcat are substantial. In C3 plants, by contrast, Rubisco operates in a low CO2 environment, and thus there is greater advantage in having a higher relative specificity, but this comes at the cost of reduced turnover capacity (Badger, 1987). Although appropriate for moderate temperature, this interpretation is limited because it does not consider the differences in Rubisco kinetics at high and low temperature, which often are the conditions in which species function. By considering temperature effects on kcat, the advantage of higher kcat in C3 species from cool habitats can be identified.
As temperature falls, the CO2 concentration required to saturate Rubisco declines (Fig. 7), such that below 10 °C, enough CO2 is present in plants to allow the enzyme to function near the CO2 saturation point (Fig. 8). As the CO2 saturation point approaches the operating Ci, the Vmax of Rubisco become an important determinant of in vivo activity. For species in cool conditions, increasing the kcat of Rubisco will therefore increase photosynthesis and nitrogen use efficiency (Pittermann and Sage, 2000). Photorespiratory costs associated with decreased affinity are offset because cooler temperatures directly increase CO2 specificity of Rubisco and the solubility of CO2 relative to O2 (Jordan and Ogren, 1984). At high temperature (>30 °C), by contrast, the Km for CO2 (kc) and the CO2 saturation point rise substantially such that the operating Ci corresponds to CO2 levels below the kc, even at atmospheric CO2 levels greater than that of today (Figs 7, 8). In addition, the low atmospheric CO2 content of recent evolutionary time enhances the potential for photorespiration at elevated temperature (Sharkey, 1988; Sage, 1999). Thus, selection pressure for greater CO2 affinity by Rubisco may have been high for species that grow in warm to hot environments.
|
|
Prior surveys have generally assessed only one component of Rubisco kinetics, for example, kc (Yeoh et al., 1980
, 1981), kcat (Seemann et al., 1984; Sage et al., 1993); or relative specificity (Parry et al., 1989; Kane et al., 1994; Kent and Tomany, 1995). Because of variation in these parameters reported for the same species used in the different studies, it is difficult to obtain a clear picture of possible trade-offs between kcat and affinity in C3 plants. One of the best comparisons of Rubisco is the literature review by von Caemmerer and Quick (von Caemmerer and Quick, 2000). This shows that plants of cool habitat (Atriplex glabriuscula, Lolium perenne, spinach, and wheat) have kc of 33–62 Pa (11–21 µM), and apparent Michaelis constants in the presence of O2, kc(1+O/ko), of 49.5–110 Pa. Plants of warm habits (rice, soybean and tobacco) have Km of 23–34.4 Pa and Michaelis constants of 41.8–71.3 Pa. Relative specificity exhibited no clear trend. In addition, a recent report shows the CO2 compensation point in the absence of mitochondrial respiration (
*) decreases in Taraxacum officinale plants grown in warm environments, indicating there is some adjustment in Rubisco properties to maintain catalytic efficiency as growth temperature changes (Bunce, 2000). In summary, the results presented here indicate there is microevolutionary adjustments of Rubisco properties to enhance performance in the temperature environment to which a plant is adapted. For C3 plants in cool environments, this may be the expression of a type of Rubisco similar to C4 plants in terms of kcat and activation energy. In C3 plants from warm to hot habitats, the Rubisco may be a form with slower turnover capacity at CO2 saturation, but a greater affinity for CO2 at the CO2 and temperature conditions in which the plant grows. To validate these possibilities, careful biochemical measurements are required on a range of species, particularly those from markedly contrasting climates.
|
Acknowledgments |
|---|
I thank the following individuals for technical assistance on this project: Paul Alloway, Professor Harold Brown, and Jarmila Pittermann. This research was supported by grant No. OGP0154273 from the National Science and Engineering Council of Canada.
|
Notes |
|---|
1 Fax: +14169785878. E-mail: rsage{at}botany.utoronto.ca
|
References |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Badger MR. 1987. Coevolution of Rubisco and CO2 concentrating mechanisms. In: Biggens J, ed. Progress in photosynthesis research, Vol. III. Dordrecht, The Netherlands: Martinus Niijhoff, 601–609.
Björkman O, Pearcy RW. 1971. Effect of growth temperature on the temperature dependence of photosynthesis in vivo and on CO2 fixation by carboxydismutase in vitro in C3 and C4 species. Carnegie Institute of Washington Yearbook 70, 511–520.
Bernacchi CJ, Singsaas EL, Pimental C, Portis Jr AR, Long SP. 2001. Improved temperature response functions for models of Rubisco-limited photosynthesis. Plant, Cell and Environment 24, 253–259.
Berry JA, Raison JK. 1981. Responses of macrophytes to temperature. In: Lange OL, Nobel PS, Osmond CB, Ziegler H, eds. Encyclopedia of plant physiology, New series, Vol. 12A. Berlin: Springer-Verlag, 277–388.
Brown RH. 1978. A difference in the N use efficiency in C3 and C4 plants and its implications in adaptation and evolution. Crop Science 18, 93–98.
Bunce JA. 2000. Acclimation to temperature of the response of photosynthesis to increased carbon dioxide in Taraxacum officinale. Photosynthesis Research 64, 89–94.
Butz ND, Sharkey TD. 1989. Activity ratios of ribulose-1, 5-bisphosphate carboxylase accurately reflect carbamylation ratios. Plant Physiology 89, 735–739.
Caldwell MM, Osmond CB, Nott DL. 1977. C4 pathway photosynthesis at low temperature in cold-tolerant Atriplex species. Plant Physiology 60, 157–164.
Cornic G, Louason G. 1980. The effects of O2 on net photosynthesis at low temperatures (5 °C). Plant, Cell and Environment 3, 149–157.
Cure JD, Acock B. 1986. Crop responses to carbon dioxide doubling: a literature survey. Agriculture and Forest Meteorology 38, 127–145.
Edwards GE, Ku MSB, Monson RK. 1985. C4 photosynthesis and its regulation. In: Barber J, Baker NR, eds.Photosynthetic mechanisms and the environment. The Netherlands: Elsevier Science, 287–327.
Evans JR, Austin RB. 1986. The specific activity of ribulose-1, 5-bisphosphate carboxylase in relation to genotype in wheat. Planta 167, 344–350.
Evans JR, Loreto F. 2000. Acquisition and diffusion of CO2 in higher plant leaves. In: Leegood RC, Sharkey TD, von Caemmerer S, eds. Photosynthesis: physiology and metabolism. Dordrecht, The Netherlands: Kluwer Academic Press, 321–351.
Evans L. 1993. Crop evolution, domestication and yield. Cambridge, Cambridge University Press.
Feller U, Crafts-Bradner SJ, Salvucci ME. 1998. Moderately high temperatures inhibit ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) activase-mediated activation of Rubisco. Plant Physiology 116, 539–546.
Furbank RT, Chitty JA, Jenkins CLD, Taylor WC, Trevanion SJ, von Caemmerer S, Ashton AR. 1997. Genetic manipulation of key photosynthetic enzymes in the C4 plant Flaveria bidentis. Australian Journal of Plant Physiology 24, 477–485.
Harley PC, Sharkey TD. 1991. An improved model of C3 photosynthesis at high CO2: reversed CO2 sensitivity explained by lack of glycerate re-entry into the chloroplast. Photosynthesis Research 27, 169–178.
Holaday AS, Martindale W, Alred R, Brooks AL, Leegood RC. 1992. Changes in activities of enzymes of carbon metabolism in leaves during exposure of plants to low temperature. Plant Physiology 98, 1105–1114.
Humphries SW, Long SP. 1995. WIMOVAC: a software package for modeling the dynamics of plant leaf and canopy photosynthesis. CABIOS 11, 361–371 (see http://www.life.uiuc.edu/plantbio/wimovac for the software).
Huner NPA, Migus W, Tollenaar M. 1986. Leaf CO2 exchange rates in winter rye grown at cold-hardening and non-hardening temperatures. Canadian Journal of Plant Sciences 66, 443–452.
Huner NPA, Oquist G, Hurry VM, Krol M, Falk S, Griffith M. 1993. Photosynthesis, photoinhibition and low temperature acclimation in cold-tolerant plants. Photosynthesis Research 37, 19–39.
Jordan DB, Ogren WL. 1984. The CO2/O2 specificity of ribulose-1,5-bisphosphate carboxylase/oxygenase. Planta 161, 308–313.[Web of Science]
Kane HJ, Viil J, Entsch B, Paul K, Morell MK, Andrews TJ. 1994. An improved method for measuring the CO2/O2 specificity of ribulose bisphosphate carboxylase-oxygenase. Australian Journal of Plant Physiology 21, 449–461.
Kent SS, Tomany MJ. 1995. The differential of the ribulose 1,5-bisphosphate carboxylase/oxygenase specificity factor among higher plants and the potential for biomass enhancement. Plant Physiology and Biochemistry 33, 71–80.
Kirschbaum MUF, Farquhar GD. 1984. Temperature dependence of whole-leaf photosynthesis in Eucalyptus pauciflora Sieb. ex Spreng. Australian Journal of Plant Physiology 11, 519–538.
Kobza J, Edwards GE. 1987. Influences of leaf temperature on photosynthetic carbon metabolism in wheat. Plant Physiology 83, 69–74.
Labate CA, Adcock MD, Leegood RC. 1990. Effects of temperature on the regulation of photosynthetic carbon assimilation in leaves of maize and barley. Planta 181, 547–554.
Labate C, Leegood RC. 1988. Limitation of photosynthesis by changes in temperature. Planta 173, 519–527.
Law RD, Crafts-Bradner SJ. 1999. Inhibition and acclimation of photosynthesis to heat stress is closely correlated with activation of ribulose-1,5-bisphosphate carboxylase/oxygenase. Plant Physiology 120, 173–181.
Leegood RC, Edwards GE. 1996. Carbon metabolism and photorespiration: temperature dependence in relation to other environmental factors. In: Baker NR, ed. Photosynthesis and the environment. Dordrecht, The Netherlands: Kluwer Academic Publishers, 191–221.
Long SP. 1999. Environmental responses. In: Sage RF, Monson RK, eds. C4 plant biology. San Diego: Academic Press, 215–249.
Matsuba K, Imaizumi N, Kaneko S, Samejima M, Ohsugi R. 1997. Photosynthetic responses to temperature of phosphoenolpyruvate carboxykinase type C4 species differing in cold sensitivity. Plant, Cell and Environment 20, 268–274.
Mawson BT, Cummins WR. 1989. Thermal acclimation of photosynthetic electron transport activity by thylakoids of Saxifraga cernua. Plant Physiology 89, 325–332.
Mawson BT, Svoboda J, Cummins RW. 1986. Thermal acclimation of photosynthesis by the arctic plant Saxifraga cernua. Canadian Journal of Botany 64, 71–76.
Morison JIL, Lawlor DL. 1999. Interactions between increasing CO2 concentration and temperature during growth. Plant, Cell and Environment 22, 659–682.
Osmond CB, Winter K, Ziegler H. 1982. Functional significance of different pathways of CO2 fixation in photosynthesis. In: Lange OL, Nobel PS, Osmond CB, Ziegler H, eds. Encylcopaedia of plant physiology, New series, Vol. 12B. Physiological plant ecology. II. Water relations and carbon assimilation. Berlin: Springer-Verlag, 479–547.
Parry MAJ, Keys AJ, Gutteridge S. 1989. Variation in the specificity factor of C3 higher plant Rubiscos determined by the total consumption of ribulose-P2. Journal of Experimental Botany 40, 317–320.
Paul MJ, Lawlor DW, Driscoll SP. 1990. The effect of temperature on photosynthesis and carbon fluxes in sunflower and rape. Journal of Experimental Botany 41, 547–555.
Pearcy RW. 1977. Acclimation of photosynthetic and respiratory carbon dioxide exchange to growth temperature in Atriplex lentiformis (Torr.) Wats. Plant Physiology 59, 795–799.
Pearcy RW, Tumosa N, Williams K. 1981. Relationships between growth, photosynthesis and competitive interactions for a C3 and a C4 plant. Oecologia 48, 371–376.
Pitterman J, Sage RF. 2000. Photosynthetic performance at low temperature of Bouteloua gracilis Lag., a high altitude C4 grass from the Rocky Mountains, USA. Plant, Cell and Environment 23, 811–823.
Pittermann J, Sage RF. 2001. The response of the high altitude C4 grass Muhlenbergia montanum (Nutt.) A.S. Hitchc. to long- and short-term chilling. Journal of Experimental Botany 52, 829–838.
Sage RF. 1999. Why C4 plants? In: Sage RF, Monson RK, eds. C4 plant biology. San Diego: Academic Press, 3–16.
Sage RF, Pearcy RW. 1987. The nitrogen use efficiency of C3 and C4 plants. II. Leaf nitrogen effects on the gas exchange characteristics of Chenopodium album L. and Amaranthus retroflexus L. Plant Physiology 84, 959–963.
Sage RF, Pearcy RW. 2000. The physiological ecology of C4 photosynthesis. In: Leegood RC, Sharkey TD, von Caemmerer S, eds. Photosynthesis: physiology and metabolism. Dordrecht, The Netherlands: Kluwer Academic, 497–532.
Sage RF, Pearcy RW, Seemann JR. 1987. The nitrogen use efficiency of C3 and C4 plants. III. Leaf nitrogen effects on the activity of carboxylating enzymes in Chenopodium album L. and Amaranthus retroflexus L. Plant Physiology 85, 355–359.
Sage RF, Reid CD, Moore Bd, Seemann JR. 1993. Long-term kinetics of the light-dependent regulation of ribulose-1,5-bisphosphate carboxylase/oxygenase activity in plants with and without 2-carboxyarabinitol 1-phosphate. Planta 191, 222–230.[Web of Science]
Sage RF, Santrucek J, Grise DJ. 1995. Temperature effects on the photosynthetic response of C3 plants to long-term CO2 enrichment. Vegetatio 121, 67–77.
Sage RF, Seemann JR. 1993. Regulation of ribulose-1,5-bisphosphate carboxylase/oxygenase activity in response to reduced light intensity in C4 plants. Plant Physiology 102, 21–28.[Abstract]
Sage RF, Sharkey TD. 1987. The effect of temperature on the occurrence of O2 and CO2 insensitive photosynthesis in field-grown plants. Plant Physiolology 84, 658–664.
Sage RF, Sharkey TD, Pearcy RW. 1990a. The effect of leaf nitrogen and temperature on the CO2 response of photosynthesis in Chenopodium album L., a C3 dicot. Australian Journal of Plant Physiology 17, 135–148.
Sage RF, Sharkey TD, Seemann JR. 1990b. The regulation of ribulose-1,5-bisphosphate carboxylase activity in response to light and CO2 in the C3 annuals Chenopodium album L. and Phaseolus vulgaris L. Plant Physiology 94, 1735–1742.
Schulze ED, Hall AE. 1982. Stomatal responses, water loss and CO2 assimilation rates of plants in contrasting environments. In: Lange OL, Nobel PS, Osmond CB, Ziegler H, eds. Encyclopedia of plant physiology, New series, Vol. 12B. Berlin: Springer-Verlag, 181–230.
Seemann JR, Badger MR, Berry JA. 1984. Variations in the specific activity of ribulose-1,5-bisphosphate carboxylase between species utilizing differing photosynthetic pathways. Plant Physiology 74, 791–794.
Sharkey TD. 1985. Photosynthesis in intact leaves of C3 plants. Its occurrence and a possible explanation. Botanical Review 51, 53–105.
Sharkey TD. 1988. Estimating the rate of photorespiration in leaves. Physiologia Plantarum 73, 147–152.
Sharkey TD, Badger MR, von Caemmerer S, Andrews TJ. 2001. Increased heat sensitivity of photosynthesis in tobacco plants with reduced Rubisco activase. Photosynthesis Research 67, 147–156.[Web of Science][Medline]
Simon JP, Hatch MD. 1994. Temperature effects on the activation and inactivation of pyruvate PI-dikinase in two populations of the C4 weed Echinochloa crus-galli (Barnyard grass) from sites of contrasting climates. Australian Journal of Plant Physiology 21, 463–473.
von Caemmerer S. 2000. Biochemical models of leaf photosynthesis. Canberra: CSIRO.
von Caemmerer S, Farquhar GD. 1981. Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153, 376–387.[Web of Science]
von Caemmerer S, Farquhar GD. 1984. Effects of partial defoliation, changes of irradiance during growth, short-term water stress and growth at enhanced p(CO2) on the photosynthetic capacity of Phaseolus vulgaris L. Planta 160, 320–329.
von Caemmerer S, Furbank RT. 1999. Modeling C4 photosynthesis. In: Sage RF, Monson RK, eds. C4 plant biology. San Diego: Academic Press, 173–211.
von Caemmerer S, Quick WP. 2000. Rubisco: physiology in vivo. In: Leegood RC, Sharkey TD, von Caemmerer S, eds, Photosynthesis: physiology and metabolism. Dordrecht, The Netherlands: Kluwer Academic Press, 85–113.
Vu JCV, Allen Jr LH, Boote KJ, Bowes G. 1997. Effects of elevated CO2 and temperature on photosynthesis and Rubisco in rice and soybean. Plant, Cell and Environment 20, 68–76.
Wand SJE, Midgley GF, Jones MH, Curtis PS. 1999. Responses of wild C4 and C3 grass (Poaceae) species to elevated atmospheric CO2 concentrations: a meta-analytic test of current theories and perceptions. Global Change Biology 5, 723–741.
Wand SE, Midgley GF, Stock WD. 2001. Growth responses to elevated CO2 in NADP-ME, NAD-ME and PCK C4 grasses and a C3 grass from South Africa. Australian Journal of Plant Physiology 28, 13–25.[Web of Science]
Weis E. 1981. The temperature sensitivity of dark-inactivation and light-activation of the ribulose-1,5-bisphosphate carboxylase in spinach chloroplasts. FEBS Letters 129, 197–200.
Yeoh H-H, Badger MR, Watson L. 1980. Variations in Km(CO2) of ribulose-1,5-bisphosphate carboxylase among grasses. Plant Physiology 66, 1110–1112.
Yeoh H-H, Badger MR, Watson L. 1981. Variations in kinetic properties of ribulose-1,5-bisphosphate carboxylase among plants. Plant Physiology 67, 1151–1155.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  A. D.B. Leakey Rising atmospheric carbon dioxide concentration and the future of C4 crops for food and fuel Proc R Soc B, July 7, 2009; 276(1666): 2333 - 2343. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. Nagai and A. Makino Differences Between Rice and Wheat in Temperature Responses of Photosynthesis and Plant Growth Plant Cell Physiol., April 1, 2009; 50(4): 744 - 755. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
W. Yamori, K. Noguchi, K. Hikosaka, and I. Terashima Cold-Tolerant Crop Species Have Greater Temperature Homeostasis of Leaf Respiration and Photosynthesis Than Cold-Sensitive Species Plant Cell Physiol., February 1, 2009; 50(2): 203 - 215. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P.-A. Christin, N. Salamin, A. M. Muasya, E. H. Roalson, F. Russier, and G. Besnard Evolutionary Switch and Genetic Convergence on rbcL following the Evolution of C4 Photosynthesis Mol. Biol. Evol., November 1, 2008; 25(11): 2361 - 2368. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. Wang, A. R. Portis Jr., S. P. Moose, and S. P. Long Cool C4 Photosynthesis: Pyruvate Pi Dikinase Expression and Activity Corresponds to the Exceptional Cold Tolerance of Carbon Assimilation in Miscanthus x giganteus Plant Physiology, September 1, 2008; 148(1): 557 - 567. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. S. Kubien, S. M. Whitney, P. V. Moore, and L. K. Jesson The biochemistry of Rubisco in Flaveria J. Exp. Bot., May 1, 2008; 59(7): 1767 - 1777. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. F. Sage, D. A. Way, and D. S. Kubien Rubisco, Rubisco activase, and global climate change J. Exp. Bot., May 1, 2008; 59(7): 1581 - 1595. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Wang, S. L. Naidu, A. R. Portis Jr, S. P. Moose, and S. P. Long Can the cold tolerance of C4 photosynthesis in Miscanthusxgiganteus relative to Zea mays be explained by differences in activities and thermal properties of Rubisco? J. Exp. Bot., May 1, 2008; 59(7): 1779 - 1787. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Makino and R. F. Sage Temperature Response of Photosynthesis in Transgenic Rice Transformed with 'Sense' or 'Antisense' rbcS Plant Cell Physiol., October 1, 2007; 48(10): 1472 - 1483. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Suzuki, M. Ohkubo, H. Hatakeyama, K. Ohashi, R. Yoshizawa, S. Kojima, T. Hayakawa, T. Yamaya, T. Mae, and A. Makino Increased Rubisco Content in Transgenic Rice Transformed with the 'Sense' rbcS Gene Plant Cell Physiol., April 1, 2007; 48(4): 626 - 637. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G. G. B. Tcherkez, G. D. Farquhar, and T. J. Andrews From the Cover: Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized PNAS, May 9, 2006; 103(19): 7246 - 7251. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. M. Morgan-Kiss, J. C. Priscu, T. Pocock, L. Gudynaite-Savitch, and N. P. A. Huner Adaptation and Acclimation of Photosynthetic Microorganisms to Permanently Cold Environments Microbiol. Mol. Biol. Rev., March 1, 2006; 70(1): 222 - 252. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. F. Sage and A. D. McKown Is C4 photosynthesis less phenotypically plastic than C3 photosynthesis? J. Exp. Bot., January 1, 2006; 57(2): 303 - 317. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. von Caemmerer, L. Hendrickson, V. Quinn, N. Vella, A.G. Millgate, and R.T. Furbank Reductions of Rubisco Activase by Antisense RNA in the C4 Plant Flaveria bidentis Reduces Rubisco Carbamylation and Leaf Photosynthesis Plant Physiology, February 1, 2005; 137(2): 747 - 755. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
O. Ghannoum, J. R. Evans, W. S. Chow, T. J. Andrews, J. P. Conroy, and S. von Caemmerer Faster Rubisco Is the Key to Superior Nitrogen-Use Efficiency in NADP-Malic Enzyme Relative to NAD-Malic Enzyme C4 Grasses Plant Physiology, February 1, 2005; 137(2): 638 - 650. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 F. EWERT Modelling Plant Responses to Elevated CO2: How Important is Leaf Area Index? Ann. Bot., June 1, 2004; 93(6): 619 - 627. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. E. Salvucci and S. J. Crafts-Brandner Relationship between the Heat Tolerance of Photosynthesis and the Thermal Stability of Rubisco Activase in Plants from Contrasting Thermal Environments Plant Physiology, April 1, 2004; 134(4): 1460 - 1470. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Makino, H. Sakuma, E. Sudo, and T. Mae Differences between Maize and Rice in N-use Efficiency for Photosynthesis and Protein Allocation Plant Cell Physiol., September 15, 2003; 44(9): 952 - 956. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. S. Kubien, S. von Caemmerer, R. T. Furbank, and R. F. Sage C4 Photosynthesis at Low Temperature. A Study Using Transgenic Plants with Reduced Amounts of Rubisco Plant Physiology, July 1, 2003; 132(3): 1577 - 1585. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. L. Naidu, S. P. Moose, A. K. AL-Shoaibi, C. A. Raines, and S. P. Long Cold Tolerance of C4 photosynthesis in Miscanthus x giganteus: Adaptation in Amounts and Sequence of C4 Photosynthetic Enzymes Plant Physiology, July 1, 2003; 132(3): 1688 - 1697. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. A. J. Parry, P. J. Andralojc, R. A. C. Mitchell, P. J. Madgwick, and A. J. Keys Manipulation of Rubisco: the amount, activity, function and regulation J. Exp. Bot., May 1, 2003; 54(386): 1321 - 1333. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. J. Crafts-Brandner and M. E. Salvucci Sensitivity of Photosynthesis in a C4 Plant, Maize, to Heat Stress Plant Physiology, August 1, 2002; 129(4): 1773 - 1780. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||