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Plant Physiol. (1998) 117: 1037-1045
Does Leaf Position within a Canopy Affect Acclimation of
Photosynthesis to Elevated CO2?1
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ABSTRACT |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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Previous studies of photosynthetic acclimation to elevated CO2 have focused on the most recently expanded, sunlit leaves in the canopy. We examined acclimation in a vertical profile of leaves through a canopy of wheat (Triticum aestivum L.). The crop was grown at an elevated CO2 partial pressure of 55 Pa within a replicated field experiment using free-air CO2 enrichment. Gas exchange was used to estimate in vivo carboxylation capacity and the maximum rate of ribulose-1,5-bisphosphate-limited photosynthesis. Net photosynthetic CO2 uptake was measured for leaves in situ within the canopy. Leaf contents of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco), light-harvesting-complex (LHC) proteins, and total N were determined. Elevated CO2 did not affect carboxylation capacity in the most recently expanded leaves but led to a decrease in lower, shaded leaves during grain development. Despite this acclimation, in situ photosynthetic CO2 uptake remained higher under elevated CO2. Acclimation at elevated CO2 was accompanied by decreases in both Rubisco and total leaf N contents and an increase in LHC content. Elevated CO2 led to a larger increase in LHC/Rubisco in lower canopy leaves than in the uppermost leaf. Acclimation of leaf photosynthesis to elevated CO2 therefore depended on both vertical position within the canopy and the developmental stage.
The pCO2 is expected to increase
from the current 36 to 55 Pa by the late 21st century (Schimel et al.,
1996 During the growth of cereal crops, leaves of the main stem and major
tillers emerge into full sunlight at the top of the canopy but then
become progressively more shaded as newer canopy elements form in
sequence above them. Leaves shaded within crop canopies show changes in
the photosynthetic system that are typical of shade-acclimated leaves
(Evans, 1993 FACE allows direct study of the effects of elevated
pCO2 on crops under field conditions
without any direct modification of microclimate (Hendrey et al., 1993 FACE System and Wheat Crop
INTRODUCTION
Top
Abstract
Introduction
Methods
Results
Discussion
References
). Instantaneous increases in pCO2
lead to a stimulation in C3 photosynthesis
through higher carboxylation efficiency and substrate concentration at the primary carboxylating enzyme, Rubisco (Drake et al., 1997). Acclimation of C3 photosynthesis, especially in
the form of decreased activity and amount of Rubisco, has often been
observed in crops grown at elevated
pCO2 but is rarely sufficient to
completely offset the increase in photosynthetic
CO2 uptake (Gunderson and Wullschleger, 1994;
Sage, 1994; Drake et al., 1997). However, decreased Rubisco content is
associated with a decline in N content, since the enzyme accounts for
10% to 25% of leaf N (Field and Mooney, 1986; Evans, 1989; Long and
Drake, 1992). Stimulation of photosynthetic CO2
uptake and a decline in N content therefore tend to result in increased
photosynthetic N-use efficiency at elevated
pCO2 (Drake et al., 1997). As a
consequence, photosynthetic acclimation to elevated
pCO2 has important implications for
crop N use.
). LHC proteins may increase, but Rubisco content and the
RuBP-regeneration capacity tend to decline (Björkman, 1981;
Anderson, 1986; Baker and McKiernan, 1988; Evans, 1993). Shaded leaves
in a cereal canopy are therefore older and likely have a modified
photosynthetic system compared with sunlit leaves at the top of the
canopy. Previous studies of photosynthetic acclimation to elevated
pCO2 have focused on the most
recently expanded and sunlit leaves in the canopy (Hakala and Mela,
1995; Ziska et al., 1996; Vu et al., 1997). However, acclimation
could differ between sunlit leaves and older, more shaded leaves deeper
within the canopy. If ignored, any differences could lead to important
errors in determining the acclimation response of whole crop canopies.
Acclimation could occur at the canopy level without being detected in
the most recently expanded leaf. An understanding of acclimation in
crop canopies will be critical for predicting the effects of increasing
pCO2 on crop photosynthesis and N use
in the future.
).
Large areas of undisturbed canopy are available in which edge and wall
effects and other disturbances typical of the small canopies enclosed
within controlled-environment and open-top chambers can be avoided. The
FACE wheat (Triticum aestivum L.) project therefore provided
an unrivaled opportunity to examine the null hypothesis that
photosynthetic acclimation to elevated
pCO2 in the form of loss of
carboxylation capacity and Rubisco content is identical in a vertical
profile of leaves through the canopy. Relationships between acclimation
or lack of acclimation and photosynthetic CO2
uptake in situ and leaf N-use efficiency were determined.
Photosynthetic acclimation of lower canopy leaves was examined at three
stages of crop development under elevated
pCO2: inflorescence emergence, when
whole-plant sink demand for C and N is low, and two stages of grain
development, when C and N are being rapidly exported to the ear
(Simpson, 1992).
MATERIALS AND METHODS
Top
Abstract
Introduction
Methods
Results
Discussion
References
). The
FACE apparatus consisted of 25-m-diameter toroidal plenums that were
placed on the soil surface immediately after sowing. Vertical-vent
pipes were connected to the plenum at 2-m intervals.
). The enrichment was maintained continuously
from emergence (January 1) until harvest (mid-May). Control plots were
prepared in the same way but without any airflow and had a daytime
ambient pCO2 of 36 Pa. The
experimental design consisted of four replicate blocks, each containing
one elevated pCO2 (approximately 55 Pa) FACE ring and one control (approximately 36 Pa) ring. The plots
were 22 m in diameter, and blocks were separated by at least
90 m. One-half of each plot was subjected to a drought treatment
(Pinter et al., 1996). In this paper we report only the plants grown
with adequate water. These well-watered plants were irrigated with
underground drip tubes whenever the available water in the root zone
decreased below 30%. The amounts of water added in each irrigation
were calculated to replace the evapotranspiration that had occurred since the preceding irrigation, after adjustment for any precipitation. The crop received 277 kg N ha
1 and 44 kg P
ha1 in 1992/1993 and 277 kg N
ha1 and 29 kg P ha1 in
1993/1994. Other nutrients were adjusted to avoid any potential deficiencies.
and Pinter et al. (1996). This study
concerns photosynthesis of the three uppermost leaves of the flowering
stems of wheat, which form most of the active canopy, the lower leaves
having commenced or completed senescence. By convention, leaves of
cereal stems are numbered from the base upward. The 7th leaf is the
lowest and oldest, the 8th leaf is above and in about the middle of the
canopy, and the 9th leaf, the flag leaf, is the youngest and forms the
top of the leaf canopy.
Light Penetration in the Canopy
was determined at the mean height of the flag, at the 8th and
7th leaves, and at the soil surface. It was estimated by one of two
methods, in parallel with leaf gas-exchange measurements: (a) from the
hemispherical distribution of light within the canopy under diffuse
sky-lighting conditions, using a canopy analyzer (LAI-2000, Li-Cor,
Lincoln, NE) following the procedure of Welles and Norman (1991); and
(b) at approximately solar noon it was estimated under a cloudless sky
(Sunfleck Ceptometer, Decagon Devices, Pullman, WA).
Carboxylation Capacity and RuBP-Limited Photosynthesis
Leaf CO2 and water vapor fluxes were measured in fully controlled microenvironment cuvettes incorporated into two identical, open gas-exchange systems (MPH-1000, Campbell Scientific, Logan, UT) and used to determine the response of light-saturated photosynthesis to variations in the ci. Each of these laboratory systems incorporated an IR gas analyzer (LI-6262, Li-Cor) calibrated for CO2 using a gravimetrically prepared calibration mixture of CO2 in air (±1%, Primary Standard, Matheson Gas Products, Cucamonga, CA), and for water vapor with a dew point generator (LI-610, Li-Cor). Set point pCO2 was provided around the leaf by feedback control of the flows of compressed gases.2 s1. A and
ci were determined in real time using the
equations of von Caemmerer and Farquhar (1981). The initial, linear
slope of the A/ci response was
used to estimate Vc, max after the method of Wullschleger (1993), incorporating the temperature correction of
Harley et al. (1992). Amax was measured at
a pCO2 of 85 Pa in 1 kPa
pO2 to ensure that photorespiration
was eliminated, and photosynthesis was limited by the maximum rate of
RuBP regeneration (von Caemmerer and Farquhar, 1981).
Rubisco and N Contents
A subsample of the leaves used for gas-exchange determination of Vc, max and Amax was rapidly frozen in liquid N2 and then stored at
80°C until subsequent
analysis. Total proteins were extracted by grinding leaf tissue (1 or 2 cm2) in 5% SDS and 60 mM Tris, pH
8.0, directly in a microcentrifuge tube containing 0.1 g of glass
beads. After an aliquot for protein measurement was removed, DTT and
Glc were added to a final concentration of 50 mM and 7.5%,
respectively. Total proteins extracted from the same leaf surface area
for each treatment and from each leaf position combination were
separated by SDS-PAGE. Gels were analyzed by western blot to identify
LHC and the large subunit of Rubisco and quantified as described
previously (Nie et al., 1995b). A second subsample of leaves was dried
at 80°C for at least 48 h and then ground to a powder.
N was measured as described previously (Osborne et al.,
1997).
Photosynthesis under in Situ Conditions
The diurnal course of leaf CO2 uptake for each leaf category and treatment was established using spot measurements on randomly selected stems with two closed gas-exchange systems (LI-6200, Li-Cor). Each IR gas analyzer was calibrated against a gravimetrically prepared calibration mixture of CO2 in air (Primary Standard, Matheson Gas Products) and chamber humidity sensors were calibrated with a dew point generator (LI-610, Li-Cor) immediately prior to use. Measurements of A were started at a leaf chamber pCO2 of 55 ± 2.7 Pa for leaves grown at elevated pCO2 and at 36 ± 1.8 Pa for control leaves. The equations of von Caemmerer and Farquhar (1981) were used to calculate A. Measurements were
made from dawn until dusk at mid-grain development (on DAE 101 in 1993)
using parts of the canopy that were previously undisturbed. The central portion of most of the leaves was approximately horizontal, and the
leaf cuvette was clamped onto this portion of the leaf and maintained
in the horizontal aspect. This portion was chosen to minimize both
within-leaf variation in photosynthetic capacity and the effect of leaf
angle on incident Q.
Statistical Analysis
The null hypothesis that leaf position in the canopy had no effect on photosynthetic acclimation to elevated pCO2 was examined using two-way ANOVA for each of Vc, max, Amax, Rubisco, LHC, LHC/Rubisco, and N, where sources of variation tested were CO2 treatment, leaf position on the stem, and the interaction between the two. Three-way or repeated-measures ANOVA were not considered appropriate because two samples were taken in 1 year and one in another. The null hypothesis that the profile of was
identical throughout control and elevated
pCO2 canopies was also tested using
two-way ANOVA, examining the effects of the same sources of variation.
In each case the individual FACE and control plots were treated as
the sample (n = 4).
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RESULTS |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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Light Penetration in the Canopy
Two-way ANOVA showed no difference in the profile of through
the canopy (Table I; inflorescence
emergence, F1, 18 = 0.35, not
significant at P = 0.05; early grain development,
F1, 18 = 0.66, not significant at P = 0.05; and mid-grain development, F1, 3 = 1.20, not significant at P = 0.05).
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Acclimation of Photosynthesis
Growth at elevated pCO2 had no effect on Vc, max or Amax prior to anthesis but led to a significant reduction in both during grain development (Fig. 1). An independent and highly significant reduction in Vc, max and Amax occurred with leaf position down the stem at all growth stages examined (Fig. 1). Interaction between elevated pCO2 and leaf position on Vc, max was absent prior to anthesis but was highly significant at mid-grain development (Fig. 1). At mid-grain development, growth in elevated pCO2 had produced a significant decline in the Vc, max of the 7th and 8th leaves relative to controls but not in the flag leaf (Fig. 1). Rubisco contents similarly decreased with leaf position, showing a decline of 50% from the flag to the 7th leaf during early grain development (Figs. 2 and 3). Rubisco contents were significantly lower in the leaves grown in elevated pCO2 (Figs. 2 and 3). LHC showed no significant change with leaf position (Figs. 2 and 3). There was a highly significant effect of CO2 treatment on LHC content (Figs. 2 and 3). The ratio of LHC to Rubisco showed a significantly greater increase with leaf position in elevated pCO2 (Figs. 2 and 3).
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Photosynthesis under in Situ Conditions
Acclimation of Photosynthesis
View larger version (26K):
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Figure 4.
Scatter plots of Vc,
max and Amax and Rubisco content
against N. There was always a highly significant
regression relationship (P = 0.01) between Vc,
max, Amax, or Rubisco with
N when leaf positions were pooled within
pCO2 treatment and crop developmental stage.
One-way ANOVA was used to investigate changes in the slope of the
regression attributable to growth pCO2 and
the stage of crop development. ANOVA showed no change in the slope of
regressions between Vc, max and
N (F3, 42 = 2.44; not
significant at P = 0.05) or Rubisco and N
(F1, 22 = 0.11; not significant at P = 0.05). CO2 treatments were therefore pooled for the plotted
regression lines. Elevated pCO2 had no
effect on the slope of regressions between
Amax and N, but a decrease in
slope occurred during grain development compared with inflorescence
emergence (F3, 42 = 3.43; P = 0.05).
CO2 treatments were therefore pooled, but crop
developmental stages were separated for regression lines. 
,
Inflorescence emergence at 36 Pa; 
, inflorescence emergence at 55 Pa; 
, grain development at 36 Pa; 
, grain development
at 55 Pa.
View larger version (22K):
[in a new window]
Figure 5.
Left, Diurnal course of A measured
for the flag ( 
), 8th (), and 7th () leaves of wheat in control
(36 Pa) conditions in the field. Middle, Diurnal course of
A measured for the flag (
), 8th (), and 7th ()
leaves of wheat in elevated pCO2 (55 Pa) conditions in the field. Measurements were made on DAE 101, at mid-grain development (1993). Each point is the mean (±1
SD) for six measurements made within a 90-min period in two
replicate blocks. MST, U.S. Mountain Standard Time. Right,
Meteorological data for the daylight period of DAE 101 (1993) based on
hourly average readings from the Arizona Meteorological Network station at Maricopa. Photosynthetically active photon flux density (Q), air
temperature (Tair), and vapor pressure
deficit (D) show patterns typical of the spring climate
in the region (Kimball et al., 1995).
View this table:
Table II.
Am and A 
(integrated from the curves
in Fig. 5) for the flag, 8th, and 7th leaves in wheat grown in control
conditions (36 Pa) and in elevated pCO2 (55 Pa)
Means (±SD) for Am are for
measurements made 1 h on either side of solar noon of the diurnal time
course at mid-grain development (Fig. 5). Each value is the mean net
CO2 uptake for a given leaf integrated between 5 AM and 8 PM (±SD), corrected for
night-time respiration. The integral of night-time respiration was
estimated by linear interpolation between measurements made at the
beginning and end of the night.
DISCUSSION
Top
Abstract
Introduction
Methods
Results
Discussion
References
for this stage of the crop. The larger relative
decreases in Rubisco observed in the lower leaves with elevated
pCO2 were paralleled by decreases in Vc, max.
), acclimation of
Vc, max and
Amax to elevated pCO2 in shaded leaves could not be
explained by the difference in leaf age between
CO2 treatments. The 35% reduction in
Vc, max in lower leaves at elevated
pCO2 compared with the control was greater than the reduction in Vc, max
that occurred in any control leaf position between inflorescence
emergence and early grain development, a period of 20 d (Fig. 1).
;
Wardlaw, 1990). However, light penetration to each leaf position was
not affected by growth pCO2 in the
wheat canopy at any of the three developmental stages investigated. Destructive analysis at these stages of development similarly showed no
increase in leaf-area index with growth at elevated pCO2 (Pinter et al., 1996).
Measurements at different growth stages were made in different years.
However, the experimental treatment was the same in both years, and
crop responses to pCO2 were apparently similar (Pinter et al., 1996). A similar pattern of acclimation, occurring only after anthesis in the leaves of the lower canopy, was
observed in both years.
Photosynthesis under in Situ Conditions
In situ CO2 uptake increased at elevated pCO2 in all leaves, despite the more rapid decline in Vc, max with depth into the canopy (Figs. 1 and 5). Acclimation here may therefore be interpreted as increased efficiency of resource use rather than an adverse reaction to elevated pCO2. The decreases in Vc, max and Amax in the lower leaves with elevated pCO2 will decrease light-saturated CO2 uptake. The actual increase in lower canopy photosynthesis in situ can therefore be attributed to the stimulation of light-limited photosynthesis under elevated pCO2. Increased C gain at elevated pCO2 compared with controls under light limitation was also partly due to a lower light compensation point for leaves, allowing positive net C gain for a longer period in the day (Fig. 5; Long and Drake, 1991; Osborne et al., 1997).
Stimulation of light-limited C3 photosynthesis is
expected at elevated pCO2, despite
reductions in Vc, max or Amax. An increase in the ratio of
pCO2 to
pO2 suppresses the oxygenation reaction of Rubisco, allowing carboxylation of a greater proportion of
the available RuBP pool irrespective of carboxylation or
RuBP-regeneration capacities.
;
Wechsung et al., 1995; Pinter et al., 1996). The areas of the flag,
8th, and 7th leaves were very similar at the stage of development that
we examined. Therefore, the measured rates of photosynthesis would be
directly proportional to their absolute contribution to canopy
photosynthesis. Considering these three leaves together, which formed
the bulk of the canopy, the combined increase in photosynthetic
CO2 uptake over 1 d at elevated
pCO2 was 280 mmol
CO2 m2. The two lower and
shaded leaves accounted for 39% of this increase, emphasizing their
importance to the absolute increase in canopy C gain at elevated
pCO2 (Table II).
N
Stimulation of photosynthesis occurred despite decreases in N at elevated pCO2, resulting in an increased efficiency of leaf photosynthetic N use (Figs. 3 and 5). N, calculated as Am/N, declined with leaf position. However, the increase with elevated pCO2 relative to controls increased with leaf position. Compared with controls, leaf photosynthetic N use efficiency was 58%, 94%, and 353% higher in flag, 8th, and 7th leaves, respectively, grown at elevated pCO2.). Photosynthetic
acclimation to elevated pCO2 is
commonly associated with a decrease in N (for review, see
Drake et al., 1997), and lower N may be a consequence of
reduced investment of N resources in the photosynthetic apparatus (Woodrow, 1994) or of a dilution by increased biomass at elevated pCO2 (Coleman et al., 1993; Sage,
1994). Specific leaf area was unchanged by elevated
pCO2 in the present study, removing
dilution as a possible explanation.
; Simpson
et al., 1983; Simpson, 1992). Although there was a slight decrease in
the N per unit mass of grain (3%), the absolute quantity of N in the
grain at harvest was 5% higher because of the 8% increase in grain
yield at elevated pCO2 (A. Giuntoli,
unpublished data; Kimball et al., 1995; Pinter et al., 1996). Total
plant N content was unchanged at elevated
pCO2 (G. Wechsung, personal
communication); therefore, increased mobilization from other plant
parts had to occur to support the increased amount of N allocated to
grain. The grain-filling period was shorter in elevated
pCO2 compared with controls,
suggesting significant increases in the rate of N mobilization. This
would explain acclimatory reductions in leaf N under elevated
pCO2. The loss of Rubisco, but not
LHC, that accompanied this decrease in N may have functional
significance, since at elevated pCO2
less Rubisco but not LHC would be required to support a given
CO2-assimilation rate (Woodrow, 1994).
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CONCLUSIONS |
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Most previous studies of the acclimation of leaf photosynthesis to elevated pCO2 have concerned the most recently emerged, upper canopy leaves. This study shows that, even at stages of development at which no marked acclimation to elevated pCO2 is apparent in the upper leaves, acclimation in carboxylation capacity and RuBP-limited photosynthesis occurs in the lower, shaded leaves. Acclimation was accompanied by a decline in Rubisco and an increase in LHC/Rubisco. Loss of photosynthetic capacity was not sufficient to remove an enhancement of photosynthetic activity under elevated pCO2 and resulted in an increased photosynthetic N-use efficiency. Our results could be explained by photosynthetic acclimation to elevated pCO2 in response to increased internal demand for N by the increased mass of developing grain.
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FOOTNOTES |
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Received December 1, 1997;
accepted March 24, 1998.
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ABBREVIATIONS |
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Abbreviations:
A, net rate of CO2
uptake per unit leaf area.
Am, A at midday in situ.
Amax, CO2- and light-saturated value of A.
A, daily integral of A.
ANOVA, analysis
of variance.
ci, pCO2 in the substomatal cavity.
DAE, days
after emergence.
FACE, free-air CO2 enrichment.
LHC, light-harvesting complex.
N, total leaf N content.
pCO2, partial pressure of CO2 in
the atmosphere.
pO2, partial pressure of
O2 in the atmosphere.
Q, photosynthetically
active photon flux density.
RuBP, ribulose-1,5-bisphosphate.
, canopy transmittance, i.e. the proportion of light at the canopy
surface penetrating to a given level .
Vc, max, maximum RuBP-saturated rate of carboxylation in vivo.
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ACKNOWLEDGMENTS |
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We thank Roy Rauschkolb and his staff (Maricopa Agricultural Center, University of Arizona) for help and support and also Martin Parry for the antibodies to Rubisco.
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LITERATURE CITED |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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Y. Onoda, K. Hikosaka, and T. Hirose Seasonal change in the balance between capacities of RuBP carboxylation and RuBP regeneration affects CO2 response of photosynthesis in Polygonum cuspidatum J. Exp. Bot., February 1, 2005; 56(412): 755 - 763. [Abstract] [Full Text] [PDF]
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 C. P. Osborne and D. J. Beerling The Penalty of a Long, Hot Summer. Photosynthetic Acclimation to High CO2 and Continuous Light in "Living Fossil" Conifers Plant Physiology, October 1, 2003; 133(2): 803 - 812. [Abstract] [Full Text] [PDF]
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 D. J. BEERLING and C. P. OSBORNE Physiological Ecology of Mesozoic Polar Forests in a High CO2 Environment Ann. Bot., March 1, 2002; 89(3): 329 - 339. [Abstract] [Full Text] [PDF]
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A. Makino, H. Nakano, T. Mae, T. Shimada, and N. Yamamoto Photosynthesis, plant growth and N allocation in transgenic rice plants with decreased Rubisco under CO2 enrichment J. Exp. Bot., February 1, 2000; 51(90001): 383 - 389. [Abstract] [Full Text]
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R.A.C. Mitchell, J.C. Theobald, M.A.J. Parry, and D.W. Lawlor Is there scope for improving balance between RuBP-regeneration and carboxylation capacities in wheat at elevated CO2? J. Exp. Bot., February 1, 2000; 51(90001): 391 - 397. [Abstract] [Full Text]
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