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Plant Physiol. (1998) 118: 683-689
Acclimation of Photosynthesis to Elevated CO2
under
Low-Nitrogen Nutrition Is Affected by the Capacity for
Assimilate Utilization. Perennial Ryegrass under
Free-Air
CO2 Enrichment1
Alistair Rogers,
Bernt U. Fischer,
Jonathan Bryant,
Marco Frehner,
Herbert Blum,
Christine A. Raines, and
Stephen P. Long*
Department of Biological Sciences, John Tabor
Laboratories, University of Essex, Wivenhoe Park, Colchester CO4 3SQ,
United Kingdom (A.R., J.B., C.A.R., S.P.L.); Institute of Plant
Sciences, Swiss Federal Institute of Technology,
Universitätstrasse 2, 8092 Zurich, Switzerland (B.U.F., M.F.,
H.B.); and Environmental Biology and Instrumentation Division, Building
318, Brookhaven National Laboratory, Upton, New York 11973 (S.P.L.)
 |
ABSTRACT |
Acclimation of photosynthesis to
elevated CO2 has previously been shown to be more
pronounced when N supply is poor. Is this a direct effect of N or an
indirect effect of N by limiting the development of sinks for
photoassimilate? This question was tested by growing a perennial
ryegrass (Lolium perenne) in the field under elevated
(60 Pa) and current (36 Pa) partial pressures of CO2
(pCO2) at low and high levels of N fertilization.
Cutting of this herbage crop at 4- to 8-week intervals removed about
80% of the canopy, therefore decreasing the ratio of photosynthetic area to sinks for photoassimilate. Leaf photosynthesis, in vivo carboxylation capacity, carbohydrate, N, ribulose-1,5-bisphosphate carboxylase/oxygenase, sedoheptulose-1,7-bisphosphatase, and
chloroplastic fructose-1,6-bisphosphatase levels were determined for
mature lamina during two consecutive summers. Just before the cut, when the canopy was relatively large, growth at elevated
pCO2 and low N resulted in significant
decreases in carboxylation capacity and the amount of
ribulose-1,5-bisphosphate carboxylase/oxygenase protein. In high N
there were no significant decreases in carboxylation capacity or
proteins, but chloroplastic fructose-1,6-bisphosphatase protein levels
increased significantly. Elevated pCO2
resulted in a marked and significant increase in leaf carbohydrate
content at low N, but had no effect at high N. This acclimation at low N was absent after the harvest, when the canopy size was small. These
results suggest that acclimation under low N is caused by limitation of
sink development rather than being a direct effect of N supply on
photosynthesis.
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INTRODUCTION |
Acclimation of photosynthesis to growth in elevated
pCO2 has frequently been shown to be
more marked under suboptimal N supply (Drake et al., 1997 ). Growth in
low N limits the development of the shoot and root, and therefore the
capacity for utilization of the additional photoassimilate formed under
elevated pCO2. Low N may therefore
exacerbate the accumulation of carbohydrate observed under elevated
pCO2 (Webber et al., 1994; Drake et
al., 1997). Alternatively, nitrate accumulation within the plant can alter gene expression (Paul and Driscoll, 1997; Scheible et al., 1997),
and could lead to different patterns of acclimation to elevated
pCO2 depending on the N supply. Wheat
grown under limiting N supply showed a greater loss of Rubisco in
response to elevated pCO2 than plants
grown with free access to N (Rogers et al., 1996). This appeared to
result from an accumulation of soluble carbohydrates in leaves,
resulting in sugar repression of the expression of the genes encoding
the LSU and the small subunit of Rubisco (rbcL and
rbcS, respectively) (Stitt, 1991; Sheen, 1994; Krapp and
Stitt, 1995; Koch, 1996).
Most studies of acclimation to elevated
pCO2 under different levels of N
nutrition have been conducted in containers in the laboratory. However,
Arp (1991) demonstrated that such restriction of rooting volume might
accentuate acclimation to elevated
pCO2. In addition to the physical
constraint imposed by container walls, the initially enhanced growth
under elevated pCO2 will lead to a
more rapid exhaustion of the N within the pot (Pettersson and MacDonald, 1994). In the field there is no restriction on rooting volume, and increased exploration of the soil with accelerated growth
under elevated pCO2 would allow the
plant to utilize additional sources of N. Enclosures, including
open-top chambers, allow the effects of elevated
pCO2 to be investigated in the field
but impose significant changes in microclimate, which adds other
uncertainties as to whether the same effects would be observed in the
open air (Lewin et al., 1994). FACE overcomes the limitations imposed
by open-top chambers and other field enclosures (Lewin et al.,
1994).
We have taken the unique opportunity provided by the FACE experiment on
farmland at Eschikon, Switzerland (Zanetti et al., 1996) to examine in
open-field conditions the hypotheses that acclimation to elevated
pCO2 is accentuated in low N, and that this in turn is an indirect effect resulting from N limitation of the
development of sinks for photoassimilate. In this FACE experiment the
perennial ryegrass Lolium perenne L. has been managed as a
frequently cut herbage crop at low- and high-N supplies and at elevated
and current pCO2. L. perenne is a major C3 pasture grass of
Western Europe that has evolved under grazing conditions and is
therefore adapted to survive periodic partial defoliation. Cutting will
abruptly decrease the ratio of source, i.e. photosynthetic tissues, to
sinks for photoassimilates, and in addition will lead to an increased
demand for carbohydrate in shoot regrowth. Therefore, if increased
acclimation of photosynthesis to elevated
pCO2 under low N results because sink
development is limited by N supply, then in L. perenne
cutting should alleviate acclimation. This study is the first, to our
knowledge, to test the effects of manipulating the source-sink balance
on photosynthetic acclimation to elevated pCO2 in open-field conditions.
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MATERIALS AND METHODS |
Plants, Growth Conditions, and Experimental Design
Swards of the perennial ryegrass Lolium perenne L. (cv
Bastion) were planted according to a split plot, randomized design in
three blocks, with each block including an elevated
pCO2 ring and an equivalent ring in
the current ambient pCO2 of
approximately 36 Pa. FACE elevated
pCO2 to 60 Pa in each treatment ring.
Fumigation began in 1993 and pCO2 was
maintained at 60 ± 6 Pa for 92% of the total fumigation time
(Zanetti et al., 1996). Within each ring, L. perenne was
grown in monoculture at both low and high levels of N application as
NH4HO3; 140 and 560 kg
N/hectare, respectively. The swards were cut eight times between April
and November each year (Hebeisen et al., 1997). L. perenne
was cut to a height of 4 cm above ground level. In June, 1994, laminae
were sampled the day before the sward was cut and again 7 d later
for carbohydrate, N, and protein analysis. Gas-exchange measurements
were made in parallel with sampling. In 1995, the sampling procedure
was changed to rule out any possibility of a confounding effect of
separation of the before- and after-harvest samples in time. One-half
of the plot was cut and the other was left uncut. Samples for protein, N, and carbohydrate analysis, and measurements of gas exchange were
then made on cut and uncut halves of the plots on the same days. To
ensure a similar developmental age, all samples were taken from
vegetative tillers and measurements were made on the laminae at about 5 cm from the point of emergence from the pseudostem. Samples for
carbohydrate and protein analysis were frozen immediately in liquid
N2 and stored at  80°C.
Photosynthetic Gas Exchange
Leaf gas-exchange measurements were made using an open
gas-exchange system incorporating a CO2/water
vapor IR gas analyzer (version 1.4., CIRAS 1, PP Systems, Hitchin, UK,
or version LCA4, ADC, Ltd., Hoddesdon, UK) and a leaf cuvette (PLC
version, PP Systems). These systems were calibrated with known water
vapor concentrations provided by a water vapor generator (type WG-600, Analytical Development Co., Hoddesden, UK) and with
CO2 calibration gas at 60.5 Pa
pCO2 (27548-type 30L, Carbagas, Swiss
Calibration, Zurich, Switzerland). The derived gas-exchange parameters
A and ci were calculated
according to the method of von Caemmerer and Farquhar (1981). Projected
leaf area was estimated by measuring leaf width and then calculating
the area from the chamber diameter. Leaf CO2
uptake in situ was measured for 2 h on either side of solar noon.
Within each plot of each pCO2 × N
combination, measurements were made of five leaves starting at 11 AM, and the cycle was repeated three times until 3 PM. Mean rates of CO2 uptake were therefore based on 45 measurements for each
pCO2 × N treatment.
The response of A to variation in
ci was determined for two to four leaves
per treatment per ring. A stabilized quartz-iodide light source was
clipped over the leaf chamber to provide uniform, near-saturating PPFDs
(750 µmol m 2 s1). A
stabilized 12-V direct current power supply ensured a constant photon flux for up to 8 h. Measurements were taken before 1 PM and/or were limited to overcast days to minimize the
possibility of feedback inhibition of photosynthesis due to
carbohydrate accumulation and cytosolic Pi limitation.
Vc,max and
Jmax (light-saturated potential rate
of electron transport [µmol m2 s1])
were the key variables determining in vivo Rubisco activity and maximum
capacity for RuBP regeneration, respectively. These were calculated by
fitting the equations of Farquhar et al. (1980) and Evans and Farquhar
(1991), following the procedure of Wullschleger (1993). Because
temperature varied significantly between measurements, all estimates of
Vc,max and Jmax
were corrected to 25°C, following the equations of McMurtrie and Wang
(1993).
Carbohydrate Analysis
WSCs were extracted as described in Fischer et al. (1997). The
1994 samples were analyzed using an anthrone/sulfuric acid method
modified from Deriaz (1961) and optimized for the simultaneous determination of Glc and Fru. The 1995 samples were analyzed by the
similar phenol-sulfuric acid technique as described by Dubois et al.
(1956).
Protein Isolation, Western Blotting, Immunodetection,
and Quantification
Frozen leaf segments were powdered in liquid
N2 with a mortar and pestle. Total protein was
extracted with 10% (w/v) TCA in acetone with 0.07% (v/v)
 -mercaptoethanol as described by Damerval et al. (1986), followed by
three washes in acetone with 0.07% (v/v) -mercaptoethanol. The
resulting dried protein pellet was solubilized in 62 mM
Tris, 2% (w/v) SDS, 65 mM DTT, and 10% (v/v) glycerol, pH
6.8. To avoid interference from this solubilization buffer, the protein
in a subsample was precipitated with 5% (w/v) TCA, washed in acetone,
and resuspended in 0.1 M NaOH prior to determination
of the protein content (detergent-compatible microplate protein assay,
Bio-Rad). Samples were loaded on an equal-protein basis and resolved on
15% SDS-polyacrylamide gels and electroblotted onto a PVDF membrane
(Immobilon-P, Millipore; Trans-Blot, Bio-Rad). The western blots were
blocked with 30 g L1 fat-free, dried milk
prior to probing with antibodies raised against Rubisco holoenzyme,
FBPase, and SBPase, all from wheat. After washing in PBS in the
presence of a mild detergent (0.0005% [v/v] Tween 20), blots were
probed with the secondary antibody, a sheep anti-rabbit IgG,
horseradish peroxidase conjugate (Serotec Ltd., Oxford, UK). Specific
proteins were detected with enhanced chemiluminesence immunodetection
(Amersham). Quantification of the individual enhanced chemiluminescence
signals was performed from two-dimensional densitometric scanning of
the film using a computer-controlled laser-scanning densitometer (model
300A, Molecular Dynamics, Sunnyvale, CA). Because of the
nonproportional solubilization step in the preparation of protein
samples for SDS-PAGE, determination of protein content per unit leaf
area required a separate protein assay. A subsample of the
lyophilized TCA protein precipitate was dissolved in 0.1 M
NaOH prior to determination of protein content (detergent-compatible
microplate protein assay, Bio-Rad).
Leaf N Content
On completion of gas-exchange measurements, leaf segments were cut
and dried to constant weight at 80°C. Each individual leaf sample was
ground to a fine powder, and total leaf N was determined by combustion
and then thermal conductivity separation in an elemental analyzer (PE
2400 series II CHNS/O Analyzer, Perkin-Elmer). The analyzer was
previously calibrated with acetanilide standards (Perkin-Elmer).
Statistical Analyses
Differences in Vc,max, WSC, and N were
examined by analysis of variance (version 5.04, Systat, Inc., Evanston,
IL) using P = 0.05 as the level of significance. The data were
analyzed as a split-split block design with
pCO2 and block as the main effects and
N and cut as split-block factors (Mead et al., 1993). A post hoc
Tukey's test was used to examine significant pairwise comparisons. In
1995 no data were collected for the high-N-defoliated treatment. These
data were therefore analyzed as two separate analysis of variances:
first, analyzing pCO2 × N in the
uncut subplots and second, analyzing
pCO2 × cutting in the low-N plots.
Data were treated as a split-block design, as for the 1994 data. Where
significant effects were detected, pairwise comparison of means was by
MSD based on Student's t-distribution (Mead et al., 1993).
For pCO2 comparisons of WSC levels and
Vc,max, critical values of Student's t-distribution for a 1-tailed test were used, since our
hypothesis predicts an increase in WSC content and a decrease in
Vc,max. All other comparisons used a
two-tailed test, since the direction of change was not hypothesized.
Comparisons of the absolute levels of Calvin cycle proteins are only
possible within a blot, and not between, because of variation in
exposure time, chemiluminescence, and the reaction of an individual
protein with its antibody. The resulting ratio of a protein at elevated
pCO2 to current
pCO2 was determined within each
block. Data were tested for heteroscedasticity, which, when found, was
removed by log transformation (Zar, 1984). The means of the blocks,
transformed where necessary, were then compared by Student's
t test.
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RESULTS |
Average midday leaf photosynthetic rates were about 35% higher in
leaves growing under elevated pCO2,
irrespective of N supply or cutting (Fig.
1). A similar increase was observed in
1995 (Hymus, 1995). In 1994 growth at elevated
pCO2 resulted in a significantly higher WSC content (F1,2 = 50.7, P < 0.05;
Fig. 2A). There was a strong interaction
between pCO2 and N
(F1,4 = 39.75, P < 0.05); at low
N the soluble carbohydrate content of lamina grown at elevated pCO2 was almost double that of leaves
grown at current pCO2 (P < 0.01 post hoc Tukey's test). Conversely, at high N there was no significant
difference between the carbohydrate contents in leaves grown at current
and elevated pCO2 (Fig. 2). Following cutting, carbohydrate concentration showed a highly significant decline
(F1,8 = 299.8, P < 0.01), correlating to the large
decrease in the source-to-sink ratio. The difference in WSC between
elevated and current pCO2-grown leaves
before the cut at low N was absent after the cut (Fig. 2A). A similar
pattern was observed when the measurements were repeated in 1995;
growth at elevated pCO2 and low N
resulted in a significantly higher WSC content (MSD, P < 0.05;
Fig. 2B).
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| Figure 1.
A measurements made for 2 h
on either side of solar noon on days with clear skies in June, 1994. Measurements were taken on mature lamina of L. perenne.
Plants were grown and measured at current (C; 36 Pa) and at elevated
(E; 60 Pa) pCO2. There were two levels of N
application; low N (LN; 140 kg hectare1) and high N (HN;
520 kg hectare1). Measurements were made before a harvest
(UNCUT) and again 7 d after the canopy was partially defoliated
(CUT); n = 3 blocks.
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| Figure 2.
WSC content measured in mature lamina of L. perenne in 1994 (A) and 1995 (B). Treatments and their
abbreviations are as in the legend for Figure 1. For 1994, means with a
common letter are not significantly different; n = 3 (post hoc Tukey's test; P < 0.05). There was no defoliation
experiment at high N in the 1995 season requiring a different method of
comparing means. A common letter indicates no significant difference.
Statistical comparisons between uncut high-N and cut low-N treatment
combinations were not possible for 1995. n = 3 (MSD, P < 0.05). n.d., No data.
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The A/ci response of
photosynthesis implied acclimation to elevated
pCO2. Before the cut, leaves grown at
high pCO2 and low N showed a
Vc,max that was 30% below that of controls
(P < 0.05, post hoc Tukey's test; Fig.
3A), implying a marked decrease in the
amount of active Rubisco. In contrast,
Vc,max in leaves grown in high N was
unaffected by pCO2 treatment, whereas
pCO2 treatment had no effect on
Vc,max in leaves grown in either N
treatment after the cut (Fig. 3A). In 1995 (Fig. 3B), the pattern was
repeated, although the decrease in Vc,max
at elevated pCO2 and low N was smaller
(MSD, P < 0.05).
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| Figure 3.
Vc,max
measurements determined in parallel with the measurements as described
in Figure 2, for 1994 (A) and 1995 (B). Treatments and their
abbreviations are as in the legend for Figure 1. Letters above bars are
described in the legend for Figure 2. n.d., No data.
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Leaf N content (Fig. 4) and total
leaf-protein content (F1,2 = 0.58, P > 0.05) were not significantly decreased by growth at elevated
pCO2. In 1994, leaf N contents rose
significantly both on a unit leaf-area basis (F1,4 = 7.72, P < 0.05) and a dry-mass basis (F1,4 = 49.17, P < 0.01) after the cut in both N treatments; this may have reflected
the application of the fertilizer immediately after the cut. This was
confirmed in 1995, when N-fertilizer application was withheld until
completion of the measurements and there was no significant rise in
leaf N content following cutting of plants grown at elevated
pCO2 (Fig. 4, C and D). There was no
significant effect of N treatment (F1,8 = 3.21, P > 0.05) or the cut (F1,2 = 5.35, P > 0.05) on total leaf-protein content. Rubisco large subunit showed a
significant (Student's t test, P < 0.05) decrease in
leaves grown at elevated pCO2 and low
N prior to the cut (Figs. 5 and 6A) and
corresponding to the significant increase in WSC. This appeared to be a
selective effect upon Rubisco content, as there were no significant
decreases in the amounts of two other Calvin cycle enzymes, FBPase and
SBPase (Fig. 5). In high N before the cut and at high and low N
after the cut, there were no significant decreases in Rubisco due to
elevated pCO2 (Figs. 5 and 6, A and B). However, at high N before the cut there was a significant increase
in the FBPase protein levels (Student's t test, P < 0.05) (Fig. 5 and 6A), a pattern repeated in 1995 (Fig. 5 and 6D).
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| Figure 4.
Leaf N content of the plants described in the
legend for Figure 2 for 1994 (A and B) and 1995 (C and D) expressed on
a dry-mass basis (A and C) and a leaf-area basis (B and D). Treatments
and their abbreviations are as in the legend for Figure 1. Letters
above bars are as described in the legend for Figure 2. n.d., No
data.
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| Figure 5.
Western blots showing levels of LSU, FBPase, and
SBPase. Leaves sampled are as described in the legend for Figure 2. For
each N and cutting treatment, proteins extracted from each
pCO2 treatment and for each replicate block
were separated by SDS-PAGE and blotted. Because of variation in
exposure time, chemiluminescence, and the reaction of a given protein
with its antibody, comparisons are only possible within a blot. This
allows for a comparison between pCO2
treatments and any N or cutting treatment, but does not allow for a
comparison between N and cutting treatments, except when standardized
as a proportion of the control, as in Figure
6.
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| Figure 6.
Levels of LSU, FBPase, and SBPase as a proportion
of the quantity at current pCO2 controls
(n = 3). The value for each replicate was the
average of three to five repeated western blots. The broken line
indicates no difference between elevated/current
pCO2. 1994 (A and B) and 1995 (C and D) at
low N ( ) and high N ( ). There was no defoliation experiment at
high N in the 1995 season. *, Statistically significant at the 0.05 level (t, P < 0.05); **, statistically significant at the 0.01 level (t, P < 0.01) two-tailed t test.
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| |
DISCUSSION |
Our results showed clearly that significant acclimation in
L. perenne grown in open-field conditions at elevated
pCO2 was absent when N supply was high
and when plants grown with a low-N supply were partially defoliated to
lower the source-to-sink ratio. In addition, our results lend further
support to the hypothesis that acclimation of photosynthesis to growth
at elevated pCO2 at low N is an
indirect effect resulting from N limitation of the development of sinks
for photoassimilate.
Although acclimation decreased Rubisco content by about 25% (Figs. 5
and 6) and Vc,max by 30% (Fig. 2) in the
low-N treatment prior to cutting, the stimulation of leaf
photosynthesis by elevated pCO2 was
similar to that of controls (Fig. 1). This may be explained by the
shift in metabolic control away from Rubisco limitation as
pCO2 is increased. For leaves grown at
the current ambient pCO2 the
A/ci response showed that the
inflection between Rubisco and RuBP limitation occurred at a
pCO2 of about 30 Pa, just above the
ci obtained in the current atmosphere (data
not shown). This suggests that the amount of Rubisco was just
sufficient to support the observed rate of light-saturated
photosynthesis in the current atmosphere. Following the calculations of
Woodrow (1994) these leaves growing under elevated
pCO2 at the mean measurement
temperature of 27°C (Bryant, 1994; Hymus, 1995) would have about a
40% excess of Rubisco. This would mean that under elevated
pCO2 these leaves could lose 40% of
their Rubisco, yet still maintain a photosynthetic rate at elevated
pCO2 equal to that of the leaves grown
and measured at current pCO2. In this
study leaves lost about 25% of their Rubisco when grown at elevated
pCO2 and low N, yet still showed a
stimulation of A in the field. These lower Rubisco levels
may simply reflect a reallocation of resources away from Rubisco, which
is in excess under the current growth conditions. In shifting control
away from Rubisco, the rate of photosynthesis becomes limited by the
regeneration of RuBP (Woodrow, 1994). FBPase and SBPase are considered
to be two potential control points for the regeneration of RuBP
(Bassham and Krause, 1969; Woodrow and Berry, 1988; Harrison et al.,
1998). Neither of these proteins was decreased by growth at elevated
pCO2, even under low-N supply. Optimum
use of resources would require a system that would allow a decrease in
Rubisco but without loss of capacity for RuBP regeneration (Drake et
al., 1997).
Under high N no acclimatory loss of Vc,max
or Rubisco was observed in elevated
pCO2, but FBPase protein increased by
about 30%. Although this might imply an increase in capacity for RuBP regeneration, this was not evident in any significant increase in
the CO2-saturated rate of photosynthesis in these
leaves at elevated pCO2 (data not
shown). However, other studies have shown an increase in the maximum
CO2-saturated rate of photosynthesis that would
result from an increased capacity for regeneration of RuBP (Wong 1979;
Sage et al., 1989; Ziska et al., 1991), which in turn implies increased
FBPase activity, together with the other activity increases that would
be necessary.
Acclimatory loss of Rubisco and carboxylation capacity with growth in
elevated CO2 have been phenomenologically linked
to an increase in carbohydrate content (Webber et al., 1994; Drake et
al., 1997). Our results are consistent with the idea that either an
increase in carbohydrate content underlies acclimation or that acclimation and an increase in carbohydrate content at elevated CO2 share a common cause. The absence of
acclimation in plants grown at high N and elevated
pCO2, and in plants grown at low N and
elevated pCO2 when the source-to-sink
ratio is low, show that acclimation is neither a direct effect of
elevated pCO2 nor directly modified by
N supply. The results do show that under conditions that would
exacerbate carbohydrate accumulation in the leaf, i.e. a high
source-to-sink ratio and low N limiting the development of additional
sink capacity, acclimation occurs. Carbohydrate repression of gene
expression has been suggested as a cause of this pattern (Sheen, 1994).
However, this simple model would not explain a loss of Rubisco without
the loss of FBPase or SBPase, two other Calvin cycle enzymes whose
expression is affected by carbohydrates (Jones et al., 1996). This
might be explained if the threshold levels of carbohydrates required to
affect expression differ or if amounts are affected
posttranslationally. The relation of bulk carbohydrate content to
acclimation is further complicated by compartmentalization, i.e. the
fact that only a portion of the leaf carbohydrate could be in a
compartment that could influence either gene expression or
posttranslational processes (Moore et al., 1997). Nevertheless, and
consistent with our hypothesis, acclimation is correlated closely with
conditions that induce accumulation of nonstructural carbohydrates in
the leaf. In conclusion, this study has shown for the first time to our
knowledge that in field conditions acclimation of photosynthesis to
growth in elevated CO2 conditions is an indirect
effect of N and is dependent on the sink-source balance of the plant.
| |
FOOTNOTES |
1
This work was supported by a studentship to A.R.
from the Natural Environment Research Council (UK), by the Swiss
Federal Institute of Technology, and by grants from the Swiss National Energy Foundation and the Carbon Dioxide Research Program of the Office
of Health and Environmental Research of the U.S. Department of Energy.
*
Corresponding author; e-mail stevel{at}essex.ac.uk; fax
44-206-873416.
Received March 13, 1998;
accepted July 20, 1998.
| |
ABBREVIATIONS |
Abbreviations:
A, net rate of CO2
uptake per unit leaf area (µmol m2 s1).
ci, pCO2 in the
substomatal cavity.
FACE, free-air CO2 enrichment.
FBPase, chloroplastic Fru-1,6-bisphosphatase.
LSU, large subunit of Rubisco.
MSD, minimum significant difference.
pCO2, partial pressure of CO2 in the atmosphere (Pa).
RuBP, ribulose-1,5-bisphosphate.
SBPase, sedoheptulose-1,7-bisphosphataseVc,.
max, maximum RuBP-saturated rate of
carboxylation in vivo (µmol m2 s1).
WSC, water-soluble carbohydrate.
| |
ACKNOWLEDGMENTS |
We thank Martin Parry (IACR Rothamsted Experimental, Harpenden,
UK) for the antibodies against Rubisco holoenzyme and Tristan A. Dyer
(JIC Norwich, UK) for antibodies against FBPase and SBPase.
| |
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Top
Abstract
Introduction