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First published online June 12, 2003; 10.1104/pp.103.021246 Plant Physiology 132:1577-1585 (2003) © 2003 American Society of Plant Biologists C4 Photosynthesis at Low Temperature. A Study Using Transgenic Plants with Reduced Amounts of Rubisco1Department of Botany, University of Toronto, 25 Willcocks Street, Toronto, Ontario, Canada M5S 3B2 (D.S.K., R.F.S.); Research School of Biological Sciences, Australian National University, G.P.O. 475, Canberra 2601, Australia (S.v.C.); and Commonwealth Scientific and Industrial Research Organisation, Division of Plant Industry, G.P.O. 1600, Canberra 2601, Australia (R.T.F.)
C4 plants are rare in the cool climates characteristic of high latitudes and elevations, but the reasons for this are unclear. We tested the hypothesis that CO2 fixation by Rubisco is the rate-limiting step during C4 photosynthesis at cool temperatures. We measured photosynthesis and chlorophyll fluorescence from 6°C to 40°C, and in vitro Rubisco and phosphoenolpyruvate carboxylase activity from 0°C to 42°C, in Flaveria bidentis modified by an antisense construct (targeted to the nuclear-encoded small subunit of Rubisco, anti-RbcS) to have 49% and 32% of the wild-type Rubisco content. Photosynthesis was reduced at all temperatures in the anti-Rbcs plants, but the thermal optimum for photosynthesis (35°C) did not differ. The in vitro turnover rate (kcat) of fully carbamylated Rubisco was 3.8 mol mol–1 s–1 at 24°C, regardless of genotype. The in vitro kcat (Rubisco Vcmax per catalytic site) and in vivo kcat (gross photosynthesis per Rubisco catalytic site) were the same below 20°C, but at warmer temperatures, the in vitro capacity of the enzyme exceeded the realized rate of photosynthesis. The quantum requirement of CO2 assimilation increased below 25°C in all genotypes, suggesting greater leakage of CO2 from the bundle sheath. The Rubisco flux control coefficient was 0.68 at the thermal optimum and increased to 0.99 at 6°C. Our results thus demonstrate that Rubisco capacity is a principle control over the rate of C4 photosynthesis at low temperatures. On the basis of these results, we propose that the lack of C4 success in cool climates reflects a constraint imposed by having less Rubisco than their C3 competitors.
C4 plants often dominate the warm climate regions of the earth when they have access to at least moderate light intensities (Sage et al., 1999  ).
Conversely, C4 species are relatively rare in the cool climates
characteristic of high latitudes or high elevations
(Teeri and Stowe, 1976;
Tieszen et al., 1979;
Rundel, 1980;
Long, 1983;
Sage et al., 1999). In North
America, temperature is the best predictor of the success of C4
grasses, which rarely occur when the minimal temperature of the warmest month
of the growing season is below 8°C
(Teeri and Stowe, 1976).
Globally, C4 plants are rare at latitudes and elevations where the
average growing season temperatures are less than approximately 16°C
(Sage et al., 1999). The
transition from C4- to C3-dominated landscapes generally
occurs between 30°N and 40°N and between 1,500 and 3,000 m elevation
(Sage et al., 1999).
The reason for the relative lack of C4 plants in cool regions
remains unclear. The lower quantum yield of photosynthesis
(
The possibility that the bundle sheath reactions may limit C4
photosynthesis at suboptimal temperatures has received less attention.
Björkman and Pearcy (1971
A Rubisco limitation can be quantified if the amount of the enzyme is
changed without affecting the activities of other enzymes
(Stitt and Schulze, 1994
In the C4 dicot Flaveria bidentis L. Kuntze, Rubisco
content has been reduced with antisense-RNA constructs targeting the
nuclear-encoded small-subunit of Rubisco (RbcS;
Chitty et al., 1994 In the present study, we tested the hypothesis that Rubisco is the primary rate-limiting step during C4 photosynthesis at low temperatures. We used three F. bidentis genotypes with a 3-fold difference in Rubisco content. To examine the nature of the rate limitation during the temperature response of C4 photosynthesis, we measured gas exchange and chlorophyll a fluorescence across a range of temperatures from 6°C to 40°C and the in vitro activities of Rubisco and PEPCase from 0°C to 42°C. To quantify the control of CO2 assimilation by Rubisco and whether this control is affected by temperature, we determined the Cra at temperatures ranging from 6°C to 40°C.
The antisense constructs led to significant reductions in the amount of Rubisco present in F. bidentis leaves (Table I). The 136-13 and 141-1 anti-RbcS lines had 49% and 32% of the wild-type Rubisco content, respectively. The Rubisco turnover rate (kcat) did not differ between any of the lines, indicating that the antisense constructs had no effect on the kinetics of the enzyme. There was no difference in the activity of PEPCase between the genotypes (Table I). In each genotype, the Arrhenius plots for Rubisco and PEPCase indicated enzyme dissociation at low temperatures in vitro (Table I). The Ea of Rubisco increased from approximately 57 to 100 kJ mol–1 between 12°C and 18°C, whereas the Ea of PEPCase increased from 71 to 180 kJ mol–1 at similar temperatures. The wild-type plants had higher chlorophyll content than the anti-RbcS lines, but there were no changes in the ratio of chlorophyll a/b (Table I).
Reducing the amount of Rubisco by antisense led to a large reduction in the net CO2 assimilation rate (A) relative to the wild type at all measurement temperatures (Fig. 1a). Furthermore, the ratio of wild type to antisense photosynthesis increased as leaf temperature was reduced. F. bidentis had a photosynthetic thermal optimum of about 35°C when grown under these conditions, regardless of genotype (Fig. 1a). Dark respiration (Rd) did not vary with genotype (P = 0.67, ANOVA; Fig. 1a). The Ea of net photosynthesis was about 20% higher in the anti-RbcS lines (Table I). The antisense lines had lower stomatal conductance than the wild type below 20°C (Fig. 1b) but maintained a higher intercellular CO2 (Ci) across the range of temperatures measured, due to their greatly reduced photosynthetic rates (Fig. 1c). The Ci corresponding to an ambient CO2 of 370 µbar was sufficient to saturate photosynthesis at each measurement temperature in all genotypes (data not shown). Stomatal conductance was relatively stable in each genotype below 20°C, and Ci rose markedly as temperature declined below this point.
At 30°C, the ratios of variable to maximal fluroescence
(Fv/Fm) were 0.80 ± 0.01 and
0.82 ± 0.01 (+ SE; n = 8) for the wild type and
141-1 lines, respectively. At a light intensity of 1,500 µmol
m–2 s–1, the wild-type
leaves had a higher quantum yield of photosystem II (PSII;
The instantaneous quantum requirement of PSII per CO2
(
The in vitro kcat increased with increasing assay temperature, but there were no differences between the genotypes (Fig. 4a). Dividing the gross CO2 assimilation rate by the concentration of Rubisco catalytic sites yielded the in vivo kcat (Fig. 4b). At 15°C or lower, in vitro and in vivo kcat were the same in each genotype. Above 20°C, in vitro kcat exceeded the in vivo value in each genotype. The in vivo kcat in the anti-RbcS lines was greater than the wild-type value above 30°C (Fig. 4b).
The Rubisco control coefficient (Cra) was determined from the relationship between gross photosynthesis and the concentration of Rubisco catalytic sites (Fig. 5a). At low-measurement temperatures, this relationship is linear, and a higher amount of Rubisco increased photosynthesis. At warmer temperatures, the relationship between photosynthesis and Rubisco content reached a plateau as other limitations became important. The control coefficient was inversely related to temperature, being about 0.68 at the thermal optimum and rising to 0.99 at the lowest measurement temperature; at 6°C, Cra was statistically equivalent to one (Fig. 5b).
C4 plants are largely excluded from cool climates, probably because of poor photosynthetic performance at low temperatures relative to C3 species (Osmond et al., 1982 ). This poor performance may reflect an inherent biochemical
limitation, and different steps of C4 photosynthesis have been
suggested to be the rate-limiting factor at low temperatures. Using F.
bidentis modified with antisense constructs to reduce Rubisco content, we
determined the pattern of control exerted by Rubisco on C4
photosynthesis over the 6°C to 40°C temperature range. Although
control is shared near the thermal optimum, Rubisco becomes a principle
control over C4 photosynthesis at low temperatures. Several lines
of evidence support this assertion. The in vitro activity of Rubisco matches
the in vivo rate of gross photosynthesis at low temperatures, which indicates
that the enzyme is the rate-limiting step. The apparent leakage of
CO2 from the bundle sheath increases at low temperature in the wild
type to an extent similar to the increase accompanying the reduction of
Rubisco by antisense. Finally, the Rubisco Cra
increases to near unity at low temperatures, which indicates almost complete
control of C4 photosynthesis by Rubisco.
Between 6°C and 15°C, the kcat of Rubisco in vitro and the
rate of gross photosynthesis in vivo are equivalent in wild-type F.
bidentis. This indicates a strong Rubisco limitation of C4
photosynthesis at low temperatures. Reducing Rubisco content extends its
control of C4 photosynthesis to higher temperatures, as shown by
the wider thermal range across which the in vivo and the in vitro
kcat values are equivalent in the anti-RbcS lines. The in
vivo kcat was less than the in vitro kcat of Rubisco above
15°C in wild-type plants, and above 25°C in the anti-RbcS
lines. A similar finding has been previously reported in the C4
grass B. gracilis (Pittermann and
Sage, 2000
At temperatures where Rubisco exerts high control, the activation energy
(Ea) of gross assimilation (A*) should reflect the Ea of the enzyme.
In F. bidentis, the situation is complicated by the increase in the
Ea of Rubisco observed below 15°C. The Ea of A* between 5°C
and 30°C was between the values for Rubisco above and below the break in
the thermal response of the enzyme, as would be expected if the thermal
response of the enzyme controls the thermal response of CO2
assimilation. The Ea of Rubisco from F. bidentis determined between
18°C to 42°C is similar to the 50 to 60 kJ
mol–1 reported for a range of C4
species (Sage, 2002
Reducing Rubisco capacity by antisense results in greater CO2
leakage (
The quantum requirement of CO2 assimilation is constant above
15°C in a range of C4 dicots and monocots, indicating that the
stoichiometry of the C4 and C3 cycles is unaltered at
intermediate and warm temperatures
(Oberhuber and Edwards, 1993
The Cra defines the control exerted by Rubisco
over the flow of carbon through the entire C4 photosynthetic
pathway (Stitt, 1995
A limitation by Rubisco capacity on C4 photosynthesis at low
temperature represents a mechanism to explain the relative rarity of the
C4 syndrome in cool climate habitats. The carboxylation efficiency
of Rubisco improves at low temperatures, because both the relative
availability of CO2 versus O2 and the specificity of
Rubisco for CO2 increase as temperature declines
(Badger and Collatz, 1977
The minimal amount of Rubisco theoretically required for C4
plants to match C3 photosynthetic rates increases at lower
temperatures (Long, 1999
The Rubisco content of C4 species may be limited by the
compartmentalization of the enzyme, because it is restricted to a reduced
fraction of the leaf volume relative to C3 species
(Dengler and Nelson, 1999
In summary, we propose that C4 plants cannot contain sufficient
Rubisco to match the photosynthetic rates of ecologically similar
C3 species at low temperatures. A reduction in the amount of
Rubisco by C4 species is possible because of the high
CO2 concentration in the bundle sheath and is one of the
fundamental advantages C4 plants have over their C3
competitors (Osmond et al.,
1982
Plant Growth
Wild-type and anti-RbcS transgenic Flaveria bidentis were
germinated in sand in a naturally lit greenhouse. The transgenic plants were
T2 progeny of the 141-1 (one insert) and 136-13 (four inserts)
primary transformants (Furbank et al.,
1996
The photosynthetic responses to temperature and CO2 were
measured with an open type leaf gas-exchange system using an infrared gas
analyzer (Li-6262, Li-Cor, Lincoln, NE) to detect both CO2 and
water vapor. In this system, mass flow controllers (model 840, Sierra
Instruments, Monterey, CA) were used to supply N2, O2,
and CO2 at the desired levels. All temperature and CO2
responses were measured at 200 ± 5 mbar O2. The air stream
was humidified by passing the mixture through a water-filled flask which was
set to a specific temperature in a water bath. For measurements at lower
temperatures, the flask was placed on ice and filled with either water or a
70% (w/v) Suc solution. After humidification, CO2 was injected, and
the flow of air was measured by a mass-flow transducer (831, Edwards,
Wilmington, MA) before being passed through the temperature-controlled leaf
cuvette and an infrared gas analyzer. Leaf temperature was measured by placing
three fine wire (36-gauge) thermocouples in contact with the abaxial surface
of the leaf. Illumination was provided by a cool-light source (KL-2500,
Schott, Mainz, Germany). All gas exchange measurements were made on the
youngest fully expanded leaf and were calculated according to von Caemmerer
and Farquhar (1981 Photosynthetic temperature responses were measured either at a constant PPFD of 1,500 µmol m–2 s–1 or at a temperature-dependent PPFD that was sufficient to saturate photosynthesis. These points were determined by evaluating the photosynthetic responses to light at 12°C, 22°C, and 32°C, using a portable photosynthesis system (Li-6400, Li-Cor). The y intercept of light response curve was taken as an estimate of Rd at each temperature. This approach was used to mitigate the potential for photoinhibition, particularly at the lower temperatures. Light intensity in the cuvette was measured using a photodiode (G1738, Hamamatsu, Bridgewater, NJ) calibrated against a quantum sensor (Li-190s, Li-Cor). The temperature responses were measured at an ambient CO2 of 370 ± 2 µbar. The leaf to air vapor pressure deficit was maintained at 12 ± 2 mbar at temperatures greater than 10°C; at cooler temperatures, vapor pressure deficit was reduced. All temperature response measurements were initiated at 30°C; leaf temperature was subsequently increased in 5°C intervals to 40°C and then decreased to the lower temperatures. At each temperature, the leaf was allowed to equilibrate for a minimum of 15 min before measurement. After the last measurement was completed, the leaf was warmed to about 15°C, and two leaf discs (1.55 cm2 each) were rapidly removed and frozen in liquid N2. Leaf samples were stored at –80°C until enzymes were assayed.
Chlorophyll a fluorescence was determined simultaneously with gas
exchange during the temperature response measurements of the wild-type and
141-1 lines. We used a PAM-101 (Walz, Effeltrich, Germany) equipped with an
emitter-detector unit (ED-101BL, Walz) that provides excitation light at 470
nm and detection in the 660- to 710-nm waveband. This enabled us to isolate
the fluorescence signal originating from PSII
(Pfündel, 1998
The in vitro activities of Rubisco and PEPCase were assayed from 0°C to
42°C using leaf discs harvested from the leaves used for gas exchange
analysis. Leaf samples (3.1 cm2) were rapidly ground (<90 s) at
0°C using a ten-broek glass-in-glass homogenizer containing 7 mL of
extraction buffer (100 mM HEPES, pH 7.6, 2 mM Na-EDTA, 5
mM MgCl2, 5 mM dithiothreitol [DTT], 9 mg
mL–1 polyvinyl polypyrrolidone, 2 mg
mL–1 bovine serum albumin, 2 mg
mL–1 polyethylene glycol, 2.8% (v/v) Tween-80, 2
mM NaH2PO4, 11 mM
amino-n-caproic acid, and 2.2 mM benzamide). Chlorophyll
content was determined spectrophotometrically in
N,N-dimethylformamide, using two aliquots of the crude
extract (Porra et al.,
1989
Rubisco was quantified in aliquots of the crude extract, using a
[14C]carboxy-arabinitol bisphosphate (CABP)-binding assay and
assuming 6.5 binding sites per Rubisco
(Butz and Sharkey, 1989
A 3.33-mL aliquot of the crude leaf extract was added to 370 µL of a
Rubisco activating solution (100 mM Bicine, pH 8.2) containing 280
mM MgCl2 and 200 mM NaHCO3, giving
final concentrations of 28 mM MgCl2 and 20 mM
NaHCO3, respectively (Sage and
Seemann, 1993
Rubisco activity was assayed in a buffer containing 100 mM
Bicine (pH 8.2), 1 mM Na-EDTA, 20 mM MgCl2, 5
mM DTT, 1 unit mL–1 ribulose-5-P
kinase, 1.7 unit mL–1 phospho-ribulo-isomerase, 2
mM ATP, 2 mM Rib-5-P, and 12 mM
NaH14CO3 (specific activity, 27 Bq
nmol–1, ICN Pharmaceuticals, Costa Mesa, CA;
Pittermann and Sage, 2000
PEPCase activity was assayed in a buffer containing 50 mM Bicine
(pH 8.2), 1 mM Na-EDTA, 5 mM MgCl2, 5
mM DTT, 4.6 mM PEP, and 4.6 mM G-6-P, 0.2 mM
NADH, 0.3 unit mL–1 MDH, and 5.4 mM
NaH14CO3 (Pittermann
and Sage, 2000
A flux control coefficient (Cra) was calculated to
determine the extent to which Rubisco controls C4 photosynthesis
across the range of measurement temperatures
(Kacser and Burns, 1973
 A*/[E] between
6°C and 40°C. A second-order polynomial was fit to the respiration
rates, determined during the light response measurements, to provide an
estimate of respiration at each temperature.
We thank George Espie (University of Toronto) for the use of the PAM-101. Katharina Siebke and Oula Ghannoum (Australian National University) and Prof. Steve Tonsor (University of Pittsburgh) provided helpful comments and interesting discussion. Received January 29, 2003; returned for revision February 19, 2003; accepted March 24, 2003.
Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.103.021246.
1 This work was supported by the Natural Sciences and Engineering Research
Council of Canada (grant no. OGP0154273 to R.F.S.).
2 Present address: Institute of Molecular BioSciences, Massey University,
Private Bag 11 222, Palmerston North, New Zealand. * Corresponding author; e-mail d.kubien{at}massey.ac.hz; fax 64–6–350–5688.
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TOP
ABSTRACT
RESULTS
CO2, the initial slope of the light-response curve) in
C4 versus C3 species at low temperatures has been
proposed to account for the differences in the biogeography of the two
pathways (Ehleringer and Björkman,
1977
) and anti-RbcS (
and 
). Photosynthesis was measured at a temperature- and
genotype-dependent PPFD that was just sufficient to saturate photosynthesis at
370 µbar CO2 and 200 mbar O2. Each point represents
the mean (± SE) of measurements on five different leaves. Rd
was determined as the y intercept of the light response of
photosynthesis in the wild-type and 141-1 lines. Respiration did not differ
between genotypes, and pooled values are shown here. The relationship between
Rd and temperature is described by Rd =
3.76e–3 T2 +
5.74e–4 T +
8.56e–9 (where T is leaf
temperature [°C], R2 = 0.927). This was used to
correct the net assimilation for respiration in all ensuing calculations.
PSII) than the anti-RbcS leaves at temperatures below
the thermal optimum (
) and anti-RbcS (
,
) F. bidentis. Note the different scales on the two
panels. The in vitro data reflect the activity of the fully carbamylated
enzyme; in vivo kcat is estimated as gross photosynthesis divided by
the number of Rubisco catalytic sites. Each value represents the mean
(± SE) of four measurements.
