Tree Physiology 23, 937–947
© 2003 Heron Publishing—Victoria, Canada
Midday depression of net photosynthesis in the tropical rainforest tree
Eperua grandiflora: contributions of stomatal and internal
conductances, respiration and Rubisco functioning†
THIJS L. PONS1,2 and ROB A. M. WELSCHEN1
1
Department of Plant Ecophysiology, Utrecht University, P.O. Box 80084, 3508 TB Utrecht, The Netherlands
2
Author to whom correspondence should be addressed ([email protected])
Received February 6, 2003; accepted March 29, 2003; published online September 1, 2003
Summary High midday temperatures can depress net photosynthesis. We investigated possible mechanisms underlying
this phenomenon in leaves of Eperua grandiflora (Aubl.)
Benth. saplings. This tropical tree establishes in small gaps in
the rainforest canopy where direct sunlight can raise midday
temperatures markedly. We simulated this microclimate in a
growth chamber by varying air temperature between 28 and
38 °C at constant vapor pressure. A decrease in stomatal conductance in response to an increase in leaf-to-air vapor pressure
difference (∆W ) caused by an increase in leaf temperature
(Tleaf ) was the principal reason for the decrease in net photosynthesis between 28 and 33 °C. Net photosynthesis decreased
further between 33 and 38 °C. Direct effects on mesophyll
functioning and indirect effects through ∆W were of similar
magnitude in this temperature range. Mitochondrial respiration during photosynthesis was insensitive to Tleaf over the
investigated temperature range; it thus did not contribute to
midday depression of net photosynthesis. Internal conductance
for CO2 diffusion in the leaf, estimated by combined gas
exchange and chlorophyll fluorescence measurements, decreased slightly with increasing Tleaf. However, the decrease in
photosynthetic rate with increasing Tleaf was larger and thus the
difference in CO2 partial pressure between the substomatal
cavity and chloroplast was smaller, leading to the conclusion
that this factor was not causally involved in midday depression.
Carboxylation capacity inferred from the CO2 response of photosynthesis increased between 28 and 33 °C, but remained
unchanged between 33 and 38 °C. Increased oxygenation of
ribulose-1,5-bisphosphate relative to its carboxylation and the
concomitant increase in photorespiration with increasing Tleaf
were thus not compensated by an increase in carboxylation capacity over the higher temperature range. This was the principal reason for the negative effect of high midday temperatures
on mesophyll functioning.
Keywords: canopy gap, chlorophyll fluorescence, CO2 response, microclimate, photorespiration, temperature response, vapor pressure difference.
†
Introduction
Photosynthetic rates are often reduced during warm midday
hours relative to the cooler morning. This midday depression
of transpiration and CO2 assimilation rates has been well documented for trees in arid environments (Schulze et al. 1972) and
hot and dry summer conditions in Mediterranean and subtropical climates (Tenhunen et al. 1984, Küppers et al. 1986, Pathre
et al. 1998). The same phenomenon also occurs in tropical
rainforest trees, as indicated by a marked decrease in photosynthetic rate and stomatal conductance during midday and afternoon, particularly in the dry season (Huc et al. 1994, Zotz et
al. 1995, Ishida et al. 1999). Canopy conductance calculated
from xylem sap flow measurements has provided independent
evidence for the stomatal component (Granier et al. 1996,
Bonal et al. 2000).
Midday depression of net CO2 assimilation (A n) can be partitioned between stomatal and non-stomatal effects. An increase in leaf temperature (Tleaf) causes an increase in vapor
pressure difference between the intercellular spaces in the leaf
and the atmosphere (∆W ). This causes a decrease in stomatal
conductance (gs ) in most plant species, including tropical trees
(Schulze and Hall 1982, Franks and Farquhar 1999). High
midday Tleaf can also have direct negative effects on functioning of mesophyll cells. When in direct sunlight, temperatures
of tropical rainforest canopy leaves rise to between 35 and
40 °C (Huc et al. 1994, Zotz et al. 1995, Ishida et al. 1999) and
may be even higher in sapling leaves growing in canopy gaps
(Mulkey and Pearcy 1992). Temperatures in this range can be
supraoptimal for A n in C3 plants except those adapted to hot
climates (Berry and Björkman 1980). In this study, we analyzed the factors contributing to midday depression of photosynthesis in a tropical rainforest tree.
Stomatal closure in response to increasing ∆W is well documented and is often considered a major factor contributing to
midday depression of net photosynthesis (Schulze et al. 1974,
Raschke and Resemann 1986). At a constant demand for CO2
by chloroplasts, low gs causes a low intercellular CO2 partial
pressure (Ci ), which limits the carboxylation reaction of
Rubisco. However, a decrease in gs is not always associated
The first term on the right-hand side of Equation 3 should be Jc /12, not Jc /3 as originally published. The error has been corrected in this revision,
published November 12, 2003. A notice of the correction will appear in a forthcoming issue of the print journal.
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PONS AND WELSCHEN
with decreases in apparent Ci, particularly under drought conditions (Tenhunen et al. 1984, Küppers et al. 1986, Ort et al.
1994), indicating that mesophyll factors may also be involved
in photosynthetic limitations.
An important limitation for CO2 assimilation is the conductance for CO2 diffusion from the substomatal cavity to the site
of carboxylation in the chloroplast (gi ) (Evans and Loreto
2000), which causes chloroplast CO2 partial pressure (Cc) to
be substantially lower than Ci estimated from gas exchange
measurements. In non-stressed tree leaves at light-saturated
photosynthetic rates, the gradient in CO2 from the stomata to
the chloroplast can be of similar magnitude to the CO2 gradient across the stomata (Lloyd et al. 1992, Epron et al. 1995,
Hanba et al. 1999). A decrease in gi with increasing temperature could increase the magnitude of this limitation, but recent
data suggest an opposite effect (Bernacchi et al. 2002).
Mitochondrial respiration typically increases with temperature. However, the temperature effect is reduced or eliminated
after a period of acclimation (Körner and Larcher 1988). Furthermore, mitochondrial respiration that continues in the light
during photosynthesis (RL) may be much less than respiration
in the dark (RD) (Krömer 1995). The increase in RL with temperature may also be much less compared with RD (Atkin et al.
2000a). Hence, using RD from short-term measurements at different temperatures may substantially overestimate the negative effect of mitochondrial respiration on net carbon gain.
The activity of Rubisco, limited by the supply of its substrates, CO2 or ribulose-1,5-bisphosphate (RuBP), is another
potential limiting factor for A n at high temperatures. The temperature dependence of Rubisco kinetics and its consequence
for in vivo functioning has been extensively investigated
(Badger and Collatz 1977, Farquhar and von Caemmerer
1982, Kirschbaum and Farquhar 1984). The affinity of
Rubisco for CO2, and thus its carboxylating activity at ambient
CO2 partial pressure, decreases with increasing temperature
unless compensated by an increase in its maximum velocity.
The oxygenation reaction of Rubisco, and consequently photorespiration, is enhanced relative to carboxylation at high
temperatures, further adding to a negative effect on A n (Berry
and Björkman 1980). The latter factor can be quantitatively
important during midday depression, particularly when CO2
supply is low because of stomatal closure, which further enhances the oxygenation reaction relative to carboxylation.
The partitioning of the limitation of An during warm midday
hours was investigated in saplings of Eperua grandiflora
(Aubl.) Benth., a common canopy tree on well-drained sandy
soils in northern South America. Direct effects of high temperature on mesophyll functioning and indirect effects mediated
through stomatal conductance were experimentally separated.
Mesophyll functioning was further analyzed by gas exchange
and chlorophyll fluorescence techniques. Temperature effects
on mitochondrial respiration and conductance for diffusion of
CO2 in the mesophyll were examined. The CO2 responses of
An at different temperatures were used to evaluate the effects of
temperature and stomatal and internal conductances on
Rubisco functioning.
Materials and methods
Plant material and growth conditions
Eperua grandiflora (Ceasalpiniaceae) can grow up to 30 m
tall. The species occurs on nutrient-poor, bleached, sandy soils
(“white sands”) of the Guyana shield in South America. Together with congenerics, it often dominates the forest. Seeds
were collected in the forest in Central Guyana. Plants were
grown in a greenhouse at about 25 °C in 20-l pots containing a
2:1 (v/v) mixture of perlite and sand, and supplied yearly with
10 g per pot of slow-release fertilizer (Osmocote plus, release
time 12 months). Regular pruning kept plant height at about
1 m. At least 2 months before the experiments, plants were
transferred to a growth chamber (Weiss Klimatechnik, Reiskirchen-Lindenstruth, Germany) equipped with high-pressure
metal-halide lamps (HPI-T, 400 Watt, Philips, Eindhoven, The
Netherlands) positioned about 1 m above the top of the plants.
Conditions at the height of the measured leaves were: photon
flux density (PFD) of 300 µmol m –2 s –1, day/night temperature
of 33/24 °C and day/night relative humidity (RH) of 60/80%.
Plants were watered with a complete nutrient solution containing 5 mM N as ammonium nitrate plus other nutrients in proportion. Pots were flushed with tap water twice a month. Only
leaves that had developed in these conditions were used for the
measurements.
Simulation of a gap microclimate
Mean air temperature in Central Guyana is 26 °C with a mean
daily maximum of around 30 °C and a mean daily minimum
RH of 70% (Jetten 1994). Daily maxima may reach 38 °C on
clear days in gaps in the forest canopy (van Dam 2001) and
leaf temperature (Tleaf) can rise even higher (N.C. Houter,
Utrecht University, unpublished results). A representative leaf
microclimate was used to study the responses of gas exchange
to daily changes in Tleaf and air humidity.
The first experiment was performed in a growth chamber.
Measurements were started at an air temperature (Tair) of
28 °C, which was the same as Tleaf, and an RH of 80% (vapor
pressure 3.0 kPa), representative of the diffuse light conditions
early in the day. Leaf temperature was increased by increasing
Tair to 33 °C and then to 38 °C at constant water vapor pressure.
This caused corresponding decreases in RH to 60 and 46% and
an increase in ∆W from 0.8 to 2.0 and then to 3.6 kPa. The Tair
was increased and kept constant for 1 h at each step and was
then brought back to the initial conditions to simulate daily
variations in Tleaf and ∆W in a gap environment. Direct and indirect effects of high midday Tleaf were separated by changing
Tair at constant RH and by decreasing RH at constant Tair . Relative humidity rather then ∆W was kept constant across temperature treatments because the ∆W of 3.6 kPa at 38 °C and 46%
RH exceeds the vapor pressure at 28 °C. It was thus not possible to change ∆W at constant Tleaf over the whole range; furthermore, humidity in the growth chamber could not be made
high enough at 38 °C to achieve a constant ∆W of 0.8 kPa
across the whole temperature range. Measurements of gas exchange were performed at the end of each hour at a particular
Tair and RH. The CO2 in our exhalation was trapped in soda
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MIDDAY DEPRESSION IN NET PHOTOSYNTHESIS
lime, thereby preventing a rise in CO2 concentration in the
growth chamber during the measurements.
In a second experiment, we measured gas exchange responses of single leaves to Tleaf and ∆W at a PFD of 500 instead
of 300 µmol m –2 s –1. The room where the measurements were
carried out was kept at the measurement Tleaf, but vapor pressure and PFD were low for the plant parts outside the leaf
chambers (about 1 kPa and 10 µmol m–2 s –1, respectively).
Steady-state responses were recorded, which required the
maintenance of constant conditions for up to 2 h. Three replications were started with measurements made at 28 °C and a
∆W of 0.8 kPa and three others at high Tleaf or high ∆W or both.
In the treatment where only Tleaf was varied, vapor pressure
was manipulated such that ∆W remained constant between 0.8
and 1.0 kPa.
Gas exchange and chlorophyll fluorescence
In the growth chamber experiment, gas exchange was measured with a portable system (LI-6400, Li-Cor, Lincoln, NE),
at a PFD of 300 µmol m –2 s –1 using the red LED source and a
CO2 partial pressure of 37 Pa. Leaf temperature was kept at Tair
and the humidity of the inlet air was somewhat below that prevailing in the growth chamber. The data obtained with the
short incubation times used (1 min) were considered representative for the growth chamber conditions.
Measurement of steady-state gas exchange responses to Tleaf
and ∆W were carried out in a system where differences in CO2
and H2O partial pressures between air entering and leaving the
leaf chambers were measured with a Li-Cor LI-6262. Three
leaf chambers with a 69 × 67 mm2 window were used for this
experiment (see Poot et al. 1996 and Pons and Welschen 2002
for more details). Water vapor and CO2 are expressed in partial
pressures; mean air pressure was 101.5 kPa. Measurements of
the CO2 response of photosynthesis and RD were also performed with this system.
Combined measurements of gas exchange and chlorophyll
fluorescence were used to estimate Cc and gi. The system previously described was used, except that Parkinson leaf chambers (PP systems, Hitchin, U.K.) were employed. The chamber had a holder that keeps a PAM-2000 fiber optic probe at
60°. The chamber window angled at 20° to the light beam of a
slide projector that prevented the probe from shading the leaf.
The greater part of the enclosed area of this small circular leaf
chamber (diameter 18 mm) was covered by the beam of the fiber optic probe. Net photosynthetic rates and respiration rates
were corrected for respiratory CO2 that diffuses into the chamber from under the gasket (Pons and Welschen 2002).
CO2 compensation point and respiration
Respiration in the light and the CO2 compensation point in the
absence of RL (Γ*) were determined according to Brooks and
Farquhar (1985). The CO2 response of An at low CO2 partial
pressures (Ci between 3 and 10 Pa) was measured at PFDs of
500, 70 and 30 µmol m –2 s –1. These PFDs were chosen to produce different slopes of the An –Ci relationship. The linear regressions produced a common intercept that represents RL at
Γ*. Measurements at 28, 33 and 38 °C were made on the same
939
leaf, but on different days. Dark respiration was measured after a 20-min incubation in the dark.
Chloroplast CO2 concentration and internal conductance
The CO2 partial pressure in the chloroplast and gi were calculated from the gas exchange and chlorophyll fluorescence
measurements. The approach was similar to the variable J
method described by Harley et al. (1992), but measurements
were carried out at ambient CO2 partial pressure only. Temperature dependence of gi was determined from measurements at
28, 33 and 38 °C with an RH between 80 and 70% (∆W <
1.6 kPa). The response was measured on each replicate leaf on
the same day. Measurements were made in ambient air, in a
mixture of N2 and 10% ambient air (1% O2) immediately afterward, and then again in ambient air. A low O2 concentration
was used to suppress oxygenation so that the ratio of electron
transport derived from fluorescence (JF) and from gas exchange (JC) could be estimated for each leaf at each temperature. The JF /JC ratio was used as a calibration factor for the JF
measurements at 21% O2. Measurements were carried out at a
near saturating PFD of 300 µmol m –2 s –1.
Calculations
The gas exchange parameters A n, gs and Ci were calculated according to von Caemmerer and Farquhar (1981). For further
calculations of carboxylation capacity (VCmax), electron transport (J), Cc and gi, a biochemically based model of leaf photosynthesis was employed (Farquhar and von Caemmerer 1982,
von Caemmerer 2000).
From the measurements of the CO2 response of A n at light
saturation (500 µmol m –2 s –1), VCmax (µmol CO2 m –2 s –1) was
calculated from the initial RuBP-saturated part of the response
curve. In the case of known VCmax, A n was calculated by the
same formula as used for modeling.
A n + RL =
VCmax (Cc – Γ* )
Cc + K C ( 1 + O / K O )
(1)
where KC and KO are the catalytic constants of Rubisco for
carboxylation and oxygenation, respectively, and O is oxygen
concentration.
Electron transport rate (JC; µmol e– m –2 s –1) used for the
carboxylation (VC) and oxygenation (VO) reactions of Rubsico
was calculated from the RuBP-limited part of the A n –CO2 relationship at high CO2 partial pressure. The formula was also
used to calculate Cc from known JC and An + RL.
A n + RL =
( JC / 4 )(Cc – Γ* )
Cc + 2 Γ*
(2)
The partitioning of JC among VC, VO and photorespiration
(RP) was calculated as:
VC = JC / 12 + 2 / 3 ( A n + RL )
(3)
VO = JC / 6 – 2 / 3 ( A n + RL )
(4)
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PONS AND WELSCHEN
A n + RL = VC – R P
(5)
RP = 0.5VO
(6)
Electron transport rate derived from fluorescence measurements (JF; µmol e– m –2 s –1) was calculated as (Genty et al.
1989):
JF = 0.5 (( Fm′ – F )/ Fm′ )PFD abs
(7)
A value of 0.84 was assumed for leaf absorptance (abs).
Based on the assumption that the efficiency of photochemistry remains constant between 1 and 21% O2, JC at 21% O2
(JC(21)) was calculated as:
JC(21) = JF(21) ( JC (1) / JF (1) )
(8)
We then calculated Cc (Pa) at 21% O2 from JC(21) with Equation 2, and gi was calculated from Cc and A n:
gi =
An
P
(C i – Cc )
(9)
where P is air pressure and Ci is intercellular CO2 partial pressure calculated from the gas exchange measurements. In
Equations 1 and 2, Cc was either assumed to be equal to Ci, or
was calculated as:
Cc = Ci – A n / g i
(10)
When performing calculations that include the Ci – Cc gradient, Γ*( g i ) was calculated from measured Γ*:
Γ*( g i ) = Γ* + R L / g i
(11)
We used the values of KC and KO determined by von
Caemmerer et al. (1994) for Nicotiana tabacum L. These were
26.0 Pa for K C(C c ) , 40.4 Pa for K C(C i ), 17.9 kPa for K O(C c ) and
24.8 kPa for K O(C i ), where subscripts Cc and Ci denote the scenarios where gi is taken into account and where Cc is assumed
to be equal to Ci , respectively. The temperature dependencies
of these parameter values were calculated according to Farquhar and von Caemmerer (1982). The Γ* values determined in
this study were used in the calculations and adjusted to low O2
concentration where relevant.
complete when conditions were returned to initial values. The
reduction in A n was accompanied by strong decreases in gs and
Ci and thus by an increase in the CO2 gradient from the atmosphere to the substomatal cavity in the leaf (Ca – Ci ). This suggests a dominant role for stomatal control of the decrease in
gas exchange. The same decrease in RH but at constant Tair had
a smaller effect on gs, and a much smaller effect on A n (Figure 1b). A change in Tair at constant RH also caused a midday
depression in A n, particularly when Tair increased to 38 °C
(Figure 1d). Although gs decreased as well, the Ca –Ci gradient
was unaffected, indicating that stomatal limitation was similar
across the range of temperatures. Both A n and gs decreased
slightly over time at 28 °C and 80% RH (Figure 1c). These results indicate that there is a clear stomatal component in the
midday depression of photosynthesis. However, the decrease
in A n at high Tleaf independent of Ci indicates that there is also a
negative effect of high midday temperature on mesophyll
functioning.
In the leaf chamber experiment, the reduction in gs in response to a decrease in humidity resulted in only a small increase in transpiration, and ∆W irrespective of temperature
determined stomatal regulation of transpiration (results not
shown). Increasing Tleaf to 33 and 38 °C at a constant ∆W of
about 1 kPa caused a decrease in A n at constant Ci (Figure 2).
Hence, stomatal limitation remained similar across temperatures. Increasing ∆W at a constant Tleaf of 28 °C caused a decrease in both A n and Ci along a line that is similar to the CO2
response curve at 28 °C (see below). This indicates that stomatal closure in response to ∆W caused the reduction in A n.
When Tleaf and ∆W were changed simultaneously, as normally
occurs during the first half of a sunny day, A n and Ci also decreased during warming from 28 to 33 °C. However, A n decreased further without a substantial decrease in Ci when Tleaf
was increased from 33 to 38 °C at a constant vapor pressure of
3 kPa and thus an increasing ∆W from 2.1 to 3.7 kPa (Figure 3). This suggests that limitation of An in the final Tleaf and
∆W step was partitioned equally between stomatal and mesophyll factors.
Possible involvement of photoinhibition in this experiment
was investigated by measuring Fv /Fm before and after exposure of a leaf to a PFD of 500 µmol m –2 s –1 for 4 h. A small decrease in Fv /Fm from 8.1 to 7.4 was found at 38 °C and to 7.6 at
28 and 33 °C. The Fv /Fm values fully recovered overnight, indicating that no chronic photoinhibition occurred and that
transient down-regulation of PSII was of minor significance.
Respiration
Results
Temperature and humidity effects in a simulated gap
microclimate
Plants were subjected to a simulated canopy gap microclimate
with respect to Tair and RH. A PFD of 300 µmol m –2 s –1 was
near the saturation point of the Eperua grandiflora leaves
(light-response curves not shown). An increase in Tair at constant vapor pressure, which caused a decrease in RH, decreased A n substantially (Figure 1a). Recovery was almost
An increase in Tleaf caused a sharp increase in Γ* (Figure 3a).
The Γ* values and their temperature dependence were similar
to earlier findings (Brooks and Farquhar 1985, Atkin et al.
2000a, Bernacchi et al. 2001). The data were derived from the
same measurements that were used to determine RL (Figure 3b). On average, RL was 47% lower than RD over the measured temperature range (28 to 38 °C; Figure 3b). Neither RL
nor RD increased significantly with increasing Tleaf up to 38 °C
(Figure 3b). These RD measurements were made after the
leaves had been at the measurement Tleaf for about 6 h. How-
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MIDDAY DEPRESSION IN NET PHOTOSYNTHESIS
941
Figure 1. Changes in gas exchange parameters in a growth
chamber under simulated microclimate conditions representative of a forest canopy
gap. Air temperature (Tair ) and
relative humidity (RH) were
manipulated in combination or
independently. Parameter values are expressed relative to
the initial value. (a) In 1-h
steps, Tair was increased from
28 to 33 to 38 °C, and then decreased to 33 °C and then to
28 °C again. Vapor pressure
was kept constant; consequently, RH decreased from
80 to 60 and then 46%, and
then increased again. (b) The
Tair was kept constant at 28 °C
and RH was decreased from
80 to 46% and then returned to
80%. (c) Both Tair and RH
were kept constant, at 28 °C
and 80%, respectively. (d) The
Tair was varied as in (a), and
RH was held constant at 80%.
The PFD was 300 µmol m –2
s–1 and CO2 partial pressure was about 37 Pa. Parameters and their initial values were: net photosynthesis (A n; 4.9 ± 0.4 µmol m –2 s –1; 䊉),
stomatal conductance (gs; 97 ± 17 mmol m –2 s –1; 䉭), and the difference between atmospheric and intercellular CO2 partial pressures (Ca – Ci;
11.1 ± 0.9 Pa; 䊐). Means ± SE are presented; n = 4.
Internal conductance for CO2 in the mesophyll
Cc to be 15.6 Pa at 33 °C, as a result of a high demand for CO2
and the low leaf conductance at that temperature, but the Ci –
Cc gradient had decreased to 6.5 Pa. The Ci – Cc gradient was
reduced to 3.7 Pa by the substantially lower photosynthetic activity at 38 °C and a ∆W of 3.6 kPa.
A possible temperature effect on gi was investigated by a combination of gas exchange and chlorophyll fluorescence measurements at ambient CO2 partial pressure, high RH and at 21
and 1% O2. As a result of suppression of oxygenation of RuBP
at ambient CO2 partial pressure, An increased but JF decreased
after switching from 21 to 1% O2 (Figures 4a and 4b). The ratio JC /JF at 1% O2, which was used to calculate JC at 21% O2,
decreased from 0.97 to 0.84 with increasing Tleaf (Figure 4b),
suggesting that alternative electron sinks were engaged at high
Tleaf.
Mean gi was low and decreased somewhat with increasing
Tleaf (Figure 4d). Values of Cc were 6.8 and 7.6 Pa lower than Ci
at 28 and 33 °C, respectively. This was somewhat less than the
10 Pa CO2 gradient from the atmosphere to the substomatal
cavity (Figure 4c). However, the Ci – Cc gradient decreased to
5.0 Pa at 38 °C because of stronger decreases in photosynthetic
activity than in gi.
Based on gi calculated from the measurements at high RH,
Cc was determined for the combined increases in Tleaf and ∆W
that occur during midday. Values of A n, gs and Ci from the experiment shown in Figure 3 were used for this purpose. The
low gs at high Tleaf dominated the effect of total leaf conductance on Cc under these conditions (Figure 4c). We estimated
Figure 2. Effects of leaf temperature (Tleaf; 䉭) and vapor pressure difference between leaf and air (∆W; 䊊) independently and in combination (䊉) on net photosynthesis (A n) versus intercellular CO2 partial
pressure (Ci ). Leaves were measured at a saturating photon flux density of 500 µmol m –2 s –1. Measurements were carried out at three Tleaf
(28, 33 and 38 °C) and three ∆W (0.8, 2.0 and 3.6 kPa) values. Means
± SE are presented; n = 6.
ever, when RD was measured at 20-min intervals, a sharp decrease in RD with decreasing Tleaf was apparent (Q10 = 2.5;
Figure 3c).
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PONS AND WELSCHEN
Figure 3. Temperature dependence of CO2 compensation point and
respiration rates. (a) The CO2 compensation point in the absence of
respiration in the light (Γ*). (b) Respiration rates in the light (RL; 䊊)
and in darkness (RD; 䊏); RD was measured after RL. (c) Response of
RD to a decrease in leaf temperature (Tleaf), measured after 20 min at
each Tleaf. Means ± SE are presented; n = 6. Results of ANOVA are
shown; ns = not significant; * = P < 0.05; ** = P < 0.01; and *** = P <
0.001.
CO2 response of photosynthesis and partitioning of electron
transport
Electron transport capacity (Jmax) and carboxylation capacity
(VCmax ) were derived from the RuBP-limited rates of photosynthesis at high CO2 partial pressure and the RuBP-saturated
initial part of the CO2 response curve, respectively. Calculations were carried out for scenarios where Cc was assumed to
equal Ci and where Cc was calculated from Ci, An and gi (Equation 10). Values of Jmax and VCmax were similar for the two scenarios (Figure 5): they increased between 28 and 33 °C but no
further increases were observed as Tair increased from 33 to
38 °C (Figure 5).
Figure 4. Measurements associated with the calculation of the temperature dependence of conductance for CO2 diffusion in the mesophyll
(gi). (a) Net photosynthetic rates (A n) in air with normal (21%; 䊊) and
low (1%; 䊉) O2 concentrations. (b) Electron transport rate based on
chlorophyll fluorescence (JF) at 1% (䊉) and 21% (䊊) O2, and the ratio
of JF to JC (䉬), where JC is the electron transport rate calculated from
gas exchange at 1% O2. (c) Intercellular (Ci; 䊉, 䊊) and chloroplastic
(Cc; 䉱, 䉭) CO2 partial pressures. (d) Internal (gi; 䊉) and stomatal (gs;
䊏, 䊐) conductances for CO2 diffusion. Closed symbols in (c) and (d)
represent measurements made at high humidity (RH 70–80%), and
open symbols represent values calculated from measurements made
at increasing ∆W with increasing Tleaf (data from the experiment
shown in Figures 2 and 3). Values are means ± SE; n = 6. Results of
the statistical analysis (GLM repeated measures) on temperature effects are also shown: ns = not significant; * = P < 0.05; ** = P < 0.01;
and *** = P < 0.001.
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High CO2 partial pressures were required to saturate photosynthesis at its RuBP-limited rate at 33 and 38 °C (Figure 6).
When Cc is assumed to be equal to Ci, the transition between
RuBP-saturated and RuBP-limited photosynthesis occurred at
Cc values of 44, 78 and 89 Pa at 28, 33 and 38 °C, respectively.
These values are well above those found at ambient CO2 partial pressures. When gi was included in the calculation of Cc
(Equation 10), co-limitation of photosynthesis by Jmax and
VCmax occurred at substantially lower Cc (Figure 6). However,
that does not change the conclusion that photosynthesis at
light saturation and ambient CO2 partial pressure in the temperature range studied was limited by Rubisco activity. The
lower A n at 38 °C and ambient CO2 partial pressure was apparently not only the result of a higher CO2 compensation point
(Figure 3) but also the result of a somewhat lower carboxylation efficiency, as indicated by the lower initial slope at a Tleaf
of 38 °C (Figure 6).
Further analysis of the depression of A n with increasing Tleaf
was based on partitioning of electron transport (JC) among its
components VO, RP, RL and A n, where the latter three components make up VC. Measured values of Ci, RL, Γ*, gi and VCmax,
presented in Figures 2–5, respectively, were used for the calculations. The RL fraction was a few percent of JC at all temperatures. However, RL increased from 5% at 28 °C to 12% at
38 °C when expressed as a percentage of A n, largely a result of
the decrease in A n with increasing Tleaf. Oxygenation and photorespiration (VO and RP) were substantial fractions of JC at the
high test temperatures. Their combined share of JC increased
from 47 to 60% between 28 and 33 °C, and then to 65% at
38 °C. This resulted in only 32% of JC remaining for A n at
38 °C. Because JC was constant between 28 and 33 °C, the de-
943
Figure 6. Response of net photosynthesis (A n ) to intercellular CO2
partial pressure (Ci ) at 28 (䊉), 33 (䉫) and 38 °C (䉭). Data are for one
representative leaf out of the six replications used for the calculation
of Jmax and VCmax (Figure 5).
crease in A n could be attributed to the increase in VO and
consequently RP at the higher Tleaf and lower Cc. The further
decrease in A n at 38 °C was caused by a proportional increase
in VO and RP arising from the negative effect of high temperature on Rubisco specificity, but there was no change in Cc (Figure 4). However, the absolute value of JC decreased at 38 °C,
which was the main reason for the additional decrease in A n
(Figure 7).
Discussion
Mitochondrial respiration
Increasing respiration with increasing Tleaf is a potential factor
Figure 5. Effects of temperature on carboxylation capacity (VCmax; 䊊,
䊉) and electron transport capacity (Jmax; 䉭, 䉱) derived from the CO2
response curve of photosynthesis. Values of Jmax and VCmax were calculated based on the assumption that chloroplast CO2 partial pressure
(Cc ) is equal to the intercellular CO2 partial pressure (Ci ) (closed symbols) or that internal conductance (gi ) causes Cc to be lower than Ci
(open symbols). Values are means ± SE; n = 6. Results of the statistical analysis (GLM repeated measures procedure) are also shown: * =
P < 0.05 and *** = P < 0.001.
Figure 7. Partitioning of electron transport (JC) associated with the oxygenation (VO) and carboxylation (VC) activity of Rubisco. Shown are
VO, photorespiration (RP = 0.5VO), respiration in the light (RL) and net
CO2 assimilation (A n ). The latter three components make up VC. Calculations were based on Γ*, RL, gi and VCmax values presented in Figures 3–5. The Ci values were from the treatment where Tleaf was
varied at constant vapor pressure (thus increasing ∆W), presented in
Figure 2.
TREE PHYSIOLOGY ONLINE at http://heronpublishing.com
944
PONS AND WELSCHEN
contributing to the reduction in A n at high Tleaf. However, RL
and RD measured after several hours at a constant Tleaf were
largely independent of Tleaf (Figure 4b). Most reports on the effect of Tleaf on RD show a clear temperature effect with a Q10 of
around 2 (Kirschbaum and Farquhar 1984, Hikosaka et al.
1999, Bernacchi et al. 2001), as we found for our short-term
measurements (Figure 3c). Reported temperature responses
are mostly short-term, although time steps used for the temperature steps are not always specifically mentioned. Homeostasis of RD is known from measurements made on plants grown
at different temperatures (Pearcy 1977, Körner and Larcher
1988, Collier 1996). For instance, Eucalyptus pauciflora
Sieber ex. A. Spreng. had similar RD in winter and summer
when measured in situ (Atkin et al. 2000b). There are few
studies on the time course of adjustment of respiration rate to
Tleaf. Atkin et al. (2000b) found that a majority of the change
occurs within a day. Apparently, RD adjusts within 6 h to a new
Tleaf in Eperua grandiflora (Figure 3), but the details of the
time course of the adjustment were not investigated. We derived RL from measurements made after 2 to 5 h at the measurement Tleaf. In Eucalyptus pauciflora, RL was largely
independent of Tleaf when PFD was 200 µmol m –2 s –1 and
higher (Atkin et al. 2000a), which was similar to our findings
for Eperua grandiflora. An RL value lower than RD is also
commonly found (Brooks and Farquhar 1985, Krömer 1995,
Atkin et al. 1997). Our results, supported by data from other
studies, indicate that RL during photosynthesis is small and
largely independent of temperature. Hence, respiration rate
did not seem to contribute to the decrease in net photosynthesis
during hot midday hours, particularly when periods of high
temperature were long enough for adjustment of RL to occur.
Internal conductance
Combined gas exchange and fluorescence measurements were
used to estimate gi, a method considered suitable when conductances are low (Loreto et al. 1992, Evans and Loreto 2000).
Conductance was low in Eperua grandiflora, as it is in many
other trees (Lloyd et al. 1992). However, photosynthetic rates
were also low, as has been reported for the related tree Eperua
falcata Aubl. in its natural habitat (Raaimakers et al. 1995).
The Ci – Cc gradient was thus not particularly large. The 6.8 Pa
difference at 28 °C was below the mean of 8.5 Pa calculated by
Evans and Loreto (2000). Hence, the rather thick (about
300 µm) hypostomatous leaves, which have been predicted to
have an important gas phase resistance (Evans and Loreto
2000), do not constitute an important limitation for diffusion
of CO2 relative to other species. Bernacchi et al. (2002) observed an increase in gi in Nicotiana until 35 °C and a decrease
at 40 °C, and concluded that gi is an important limiting factor
for photosynthesis at 40 °C. In Eperua grandiflora, we found a
small decrease in gi between 28 and 38 °C (Figure 5d), but A n
decreased proportionally more over the same temperature
range. Consequently, the limitation of CO2 assimilation by gi
was smaller at high Tleaf, even at the relatively high gs prevailing as a result of the low ∆W we applied. The Ci – Cc gradient
of 3.5 Pa, calculated for the low gs associated with the high Tleaf
and ∆W normally occurring during midday hours (Figure 4c),
was even smaller. Hence, we conclude that the temperature dependence of gi is not an important factor depressing photosynthesis of Eperua grandiflora during hot midday hours, at least
not for the range of temperatures that we investigated.
Stomatal conductance
The results of the experiments where temperature and humidity were varied in combination and independently (Figures 1
and 2) indicated that the effects of ∆W on stomatal opening
dominated the decrease in photosynthetic activity when Tleaf
increased from 28 to 33 °C at constant vapor pressure. When
∆W was increased from 0.8 to 2.0 kPa at 28 °C only, A n decreased by 24% (Figure 1) and 33% (Figure 2). Calculations
based on parameters derived from the CO2 response curve indicated that stomatal effects at 33 and 38 °C were of similar
magnitude. A negative effect of increasing ∆W on gs is commonly found (Schulze and Hall 1982), and tropical trees are no
exception (Pearcy 1987, Tinoco-Ojanguren and Pearcy 1993,
Franks and Farquhar 1999). A similar negative response of increasing ∆W on gs has also been described for the related tree
Eperua falcata (Bonal and Guehl 2001), which grows in the
same forest type.
A constant Ci with decreasing gs, as observed when Tleaf was
increased with a concomitant increase in ∆W (Figure 2), is
similar to that observed in Mediterranean trees and shrubs during midday depression of A n (Tenhunen et al. 1984, Raschke
and Resemann 1986). This is generally interpreted as a coordinated decrease in gs and demand for CO2 in the mesophyll.
However, the correct estimate of Ci has been questioned in
such cases, because Ci could be overestimated as a result of
patchy stomatal closure (Beyschlag et al. 1992, Mott and
Buckley 1998). An increase in ∆W resulted in oscillations in gs
in our experiment on the effect of Tleaf and ∆W on gas exchange
(Figure 2). Such oscillations are probably associated with
patchy stomatal closure (Mott and Buckley 1998). However,
the oscillations gradually faded out during the 2-h period at
each Tleaf and ∆W, and only data recorded at the end of the period were used. Patchy stomatal closure, and thus an overestimation of Ci, is not thought to play an important role under
such conditions. The direct negative effect of 38 °C on A n at
low ∆W is thus likely to be the outcome of simultaneous decreases in gs and mesophyll demand for CO2 (Figure 2).
When the gap microclimate was simulated in the growth
chamber (Figure 1), the period between measurements was
1 h. Plants were thus exposed to the changed climatic conditions for no more than 45 min. Hence, oscillations and patchy
stomatal closure are more likely to play a role in this experiment than in the leaf chamber experiment. However, these effects may also occur in the field as a result of the rapid increase
in Tleaf and ∆W when saplings in a canopy gap are suddenly exposed to direct sunlight during a clear day, as found in Mediterranean trees (Beyschlag et al. 1992).
Direct effect of high temperature on the photosynthetic
apparatus
The direct effect of Tleaf was measured at high RH, when stomatal patchiness is unlikely to play a role. Values of A n at light
TREE PHYSIOLOGY VOLUME 23, 2003
MIDDAY DEPRESSION IN NET PHOTOSYNTHESIS
saturation were slightly lower at 33 than at 28 °C, but substantially lower at 38 °C (Figures 1 and 2). This direct negative effect of high Tleaf varied between experiments (41 and 18% in
Figures 1 and 2, respectively). Hence, across experiments, the
effect of Tleaf was of similar magnitude as the indirect stomatal
effect at 38 °C. The optimum Tleaf for A n is probably around
30 °C, which is not particularly high when compared with the
optimum temperature for C3 plants from hot climates such as
Larrea divaricata Cav. and Nerium oleander L., which have
optima of 35 to 40 °C (Berry and Björkman 1980). Apparently,
the shade-tolerant tree Eperua grandiflora, which establishes
in small gaps in the rainforest canopy, is not well adapted to
high temperatures, a phenomenon also observed in Australian
tropical rainforest trees in the field (Pearcy 1987). It remains to
be determined whether pioneer tree species, which establish in
large canopy gaps where high temperatures occur more frequently, have higher temperature optima.
The CO2 response of photosynthesis showed that, at a Ci of
20 to 28 Pa, An was limited by the activity of Rubisco over the
investigated temperature range (Figure 6). Hence, the temperature dependence of Jmax is less relevant for understanding the
limitations on A n. At ambient Ci, A n at 38 °C was consistently
below the rates at 28 and 33 °C as a result of increases in Γ*
with increasing Tleaf (Figure 3) and, to a lesser extent, to a decrease in the initial slope (Figure 6). A relative constancy of
the initial slope of the CO2 response curve over a broad range
of temperatures was also found in other C3 species (Kirschbaum and Farquhar 1984, Sage 2002). The reduction in A n at
38 °C and high RH, leading to a constantly high Ci (Figures 1,
2 and 4), is thus a result of high rates of oxygenation and photorespiration relative to carboxylation. Furthermore, VCmax increased little between 33 and 38 °C (Figure 6). The increase in
KC of Rubisco (Badger and Collatz 1977) was thus not compensated by higher activity. An increase in enzyme activity
would be expected over this temperature range. However,
Crafts-Brandner and Salvucci (2000) found that Rubisco deactivation increased with increasing Tleaf, and this deactivation
was not completely compensated by increased activase activity above 35 °C. This phenomenon may explain the observed
lack of an increase in VCmax at 38 °C. Inefficiency of Rubisco
functioning at high Tleaf during midday depression is enhanced
by the low gs that causes a low Cc, leading to a high percentage
of electron transport used for VO and RP (Figure 7). Similar
large percentages were also found for savannah trees in Brazil
measured in their natural habitat (Franco and Lüttge 2002).
Photoinhibition is another possible reason for decreased
chloroplastic demand for CO2. The saturating irradiance used
in our experiments (500 µmol m –2 s –1) was high compared
with the growth irradiance of 300 µmol m –2 s –1. Only a small
decrease in Fv /Fm occurred at 38 °C. This factor was thus of little importance for net photosynthesis. Daily irradiance under
the experimental growth conditions (13 mol m –2 day –1) was of
similar magnitude to that in a fairly large gap in the forest canopy (about 2500 m2, unpublished results). However, peak irradiances in gaps and sun flecks can be much higher and can,
in combination with the prevailing high temperature, cause
945
photoinhibition (Chazdon et al. 1996). This is most pronounced when plants growing in the forest understory are suddenly exposed to a gap as a result of a tree fall (Lovelock et al.
1994). It is also an important factor in shade-adapted plants
such as Coffea arabica L. (Ramalho et al. 1997) and Camellia
sinensis (L.) Kuntze (Mohotti and Lawlor 2002). However, after a period of acclimation, predawn Fv /Fm is typically high for
plants that naturally occur in canopy gaps (Lovelock et al.
1994, Krause et al. 2001) and also in canopy trees (Ishida et al.
1999). Although transient midday reductions in Fv /Fm are
found, these probably lead to only small reductions in midday
carbon gain (Long et al. 1994, Yu et al. 2001).
Conclusion
Direct and indirect negative effects of high midday leaf temperatures contributed similarly to the midday depression of net
photosynthesis of Eperua grandiflora in a simulated canopy
gap microclimate. The indirect negative effect of high temperature, through its effect on vapor pressure difference, decreased stomatal conductance and thus decreased CO2 availability in the chloroplast. Mitochondrial respiration during
photosynthesis was not temperature sensitive over the investigated temperature range of 28 to 38 °C, and hence is unlikely
to contribute to midday depression of net photosynthesis. Internal conductance for CO2 diffusion inside the leaf decreased
slightly with increasing temperature. However, the decrease in
photosynthetic rate was larger, leading to the conclusion that
internal conductance was not causally involved in the midday
depression of photosynthesis. The direct negative effect of
high temperature on photosynthesis, evident at 38 °C, must
have been associated with its effect on Rubisco activity. The
decrease in the carboxylation activity of Rubisco relative to
oxygenation and the decrease in affinity for CO2 with increasing temperature were incompletely compensated by the increase in carboxylation capacity.
Acknowledgments
Nico Houter’s assistance with the measurements was much appreciated. His experience with similar measurements in the forest in Guyana was a valuable guideline for the design of the experiments.
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