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BIOTROPIA NO. 24, 2005 : 30 - 45

ANALYSIS OF THE TEMPERATURE DEPENDENCE OF CO2 ASSIMILATION
RATE (STUDY CASE: GLYCINE MAXL. MERR)

TANIA JUNE

BIOTROP-JCSEA, SEAMEO BIOTROP, BTIC Building,
Jl. Raya Tajur Km. 6 Bogor, Indonesia; email: taniajune@biotrop.org;
Laboratory o/Agrometeorology, Bogor Agricultural University, Bogor

ABSTRACT

The maximum rate of carboxylation (Kcmax) and maximum rate of regeneration of Ribulose bisphosphate (RuBP)
(controlled by the rate of electron transport, Jmax) arc two processes governing the photosynthetic capacity of plants. Both
processes are affected by temperature. This paper examines how the response of these two photosynthetic capacities to
temperature determines the temperature response curve of the CO2-assimilation rate for plants grown at different
temperatures, by using the concept of the Farquhar €3 photosynthesis model. The goal is to use photosynthetic parameters
from CO2 and light curves to predict the temperature dependence of the CO2-assimilation rate (A) of soybean and to estimate
the preferred growth temperature. Analysis shows that the optimum temperature of the assimilation rate changes with the
changing temperature dependence of carboxylation and regeneration of RuBP.

Key words : temperature dependence/soybean/modeling photosynthesis/preferred growth temperature.

INTRODUCTION

Photosynthesis is strongly affected by temperature. During gas exchange measurements,
the short-term temperature dependence of photosynthesis is strongly affected by other environmental
factors such as light intensity and intercellular COa concentration (Berry & Bjorkman 1980). Some
of these short-term effects can be modeled by C3 photosynthesis models of Farquhar et al.
(1980). However, the response varies not only among species but even within an individual
species subjected to changing growth temperature regimes during their developments (long-term
effects) (Berry & Bjorkman 1980). In many species, the optimum temperature at which maximum
short-term photosynthesis is obtained, shifts upwards when plants are grown at higher
temperatures (Lange et al. 1974; Slatyer 1977; Berry & Bjorkman 1980; Ferrar, Slatyer &
Vranjic 1989), which is commonly known as acclimation or adaptation. The long-term
temperature acclimation during growth may affect both the maximum photosynthetic rate per unit
leaf area and the shape of the photosynthetic temperature response curve. How this growth
temperature (long-term effect) affects the short-term temperature response of photosynthesis is
still unclear. It can be attributed at the enzyme level or at the gene action-DNA level. To understand
the mechanism of this change in temperature dependence, it is important to know the limiting factor
to photosynthesis at each measured temperature.

BIOTROPIA NO. 24, 2005

According to the Farquhar Cj photosynthesis model (Farquhar et al. 1980), carboxylation
and regeneration of RuBP are two processes governing photosynthesis. In the model, the
photosynthetic rate is limited either by the capacity of RuBP carboxylase (Rubisco) to consume
ribulose bisphosphate (RuBP), denoted as Fcmax, or by the capacity for RuBP regeneration,
denoted as Jmax/4. These capacities have different temperature dependencies, in the original
model and as confirmed, for example, by Kirschbaum & Farquhar (1984) and later by June (2002).

For a fixed temperature dependence of the electron transport rate (J), Farquhar & von
Caemmerer (1982) showed that increasing the ratio of the capacity of Rubisco to consume RuBP to
that of RuBP regeneration could change the optimum temperature (ro) by changing the relative
amounts of the two components, so that the optimum temperature would be higher when the ratio
is increased. June (2002) has shown that this ratio decreased with increasing temperature.
However, June (2002) also showed that temperature dependence of electron transport rate is not
fixed but changed, both at short-term and long-term time scales. The net effect is on the change in
the ratio Jmm/Vcmm with temperature. In the Farquhar & von Caemmerer (1982) paper, the ratio
of RuBP consumption to RuBP regeneration increased with increasing growth temperature. In
June (2002), the Jmm/Vcmax ratio decreased as the short-term temperature measurement
increased, for each of the growth condition.

This paper examines how the changes in these two photosynthetic capacities with
temperature affect the temperature response curve of the CO2-assimilation rate for plants grown at
different temperatures, using the concept of the Farquhar et al. (1980) C3 photosynthesis model.
The goal is to use parameters from CC>2 and light curves from June (2002) (Vcmm and Jmax
temperature dependences) to predict the temperature dependence of the CO2-assimilation rate (A)
and then to test the model with independent measurements of the temperature dependence of the
CC>2-assimilation rate. The plants used for testing the model were grown under the same
conditions as the plants used for the parametrisation of the model in June (2002).

MATERIALS AND METHODS

Seeds of indeterminate soybean (Glyclne max [L.] Merr. cv Stephen) were sown in 12 liter
plastic pots containing a mixture of sand and vermiculite (1:1, v/v) and plants were thinned to one
plant per pot after germination. Plants were grown in a controlled environment chamber with a 14-
hour photoperiod of around 700 umol quanta m"2 s"', 60/70 % relative humidity day/night and three
different temperature regimes: 20/15, 25/20, 32/27 day/night °C under ambient [CO2], 350 umol
mol'1. The lowest and highest temperature regimes were repeated with atmospheric [CCy
enrichment to 700 umol mol"1.

The source of light used in the growth chamber was a metalarc lamp (General Electric
Lighting), MVR 1000/U. Plants were well spaced (30 cm apart at sowing) to avoid mutual shading.
Rhizobial inoculation was not provided for the plants. Each

Analysis of the temperature dependence of CO2 assimilation rate - Tania June

pot was flushed every second day with full-strength Herridge's solution (0.50 mM MgSO4, 0.25
mM CaCl2, 0.25 mM KC1, 0.125 mM KH2PO4, 0.125 mM K2HPO4, 25 uM ferric monosodium salt
of EDTA, 12 uM H3BO3, 3.6 uM MnCl2, 77 uM ZnCl2, 76 nM CuCl2, 25 nM NaMoO4) (Herridge
1977) and watered twice daily on days when nutrients were not given. To obtain a range of nitrogen
levels in the plant leaves, three different concentrations of KNO3 were added to the nutrient
solution (2, 5 and 16 mM). The nutrient solutions were added to each pot until they drained at the
base (2.5 to 3.0 liters per pot).

For gas exchange measurement, several temperature response curves of assimilation rate were
measured at a light intensity of 1200 umol m~2 s"1 with CO2 concentrations of 350 umol mol"

1
using a photosynthetic gas exchange system developed in the Environmental Biology Group,
Research School of Biological Sciences, Australian National University. Two pots of plants were
used for replication. The vapour pressure difference was kept constant at around 12.5 mbar in most
cases and was less than 17 mbar in all cases. For each leaf, the CO2-assimilation rate was
measured at six temperatures from 15°C to 40°C, holding for 15 to 20 minutes at each temperature
measurement to reach a steady state condition. Data obtained from measurements are then
compared to simulation results where parameters are obtained from measurements by June (2002).

RESULTS AND DISCUSSION

Temperature dependence of CO2 assimilation rate

Figure 1 shows the temperature dependence of the absolute value of the CO2-assimilation rate
(A) measured at 350 umol mol"1 [CO2] and irradiance of 1200 umol m"

2 s"1, for plants grown under
350 umol mol'1 [CO2]. As expected, increasing the temperature from 15°C to 25°C increases the
assimilation rate: 18 % for plants grown at 20/15°C (day/night temperature), 88 % for plants grown
at 25/20°C and 98 % for plants grown at 32/27°C. Increasing the measurement temperature further
resulted in A reaching a maximum at the optimum temperature and then decreasing. After reaching
the optimum temperature, the photosynthesis rate dropped with further increasing temperature; by
40°C the drop in A was as much as 10 % for plants grown at 20/15°C, 24 % for plants grown at
25/20°C and 10 % for plants grown at 32/27°C. It is clear that the temperature dependence of the
CO2-assimilation rate is different depending on the growth temperature.

The photosynthetic processes in soybean exhibit a capacity for temperature acclimation. Plants
maintained at different day/night temperatures had different optimum photosynthetic temperatures (T0).
Plants grown at 32/27°C have an optimum temperature for the CO2‐assimilation rate of 32.7±0.2°C. When plants
were grown at 25/20°C, the optimum temperature was 30.1±0.8°C and when plants were grown at 20/15°C, the
optimum temperature was reduced to 28.5 ±0.9°C (Table 1).

Table 1. Optimum temperature for COz assimilation rate, 7"0, and assimilation rates, A, at optimum
temperature and at various other temperatures for plants growing at different temperatures,+
s.c. Plants were grown at the temperatures indicated in the table, CO2 concentration of 350
(imol mol"1 and nitrogen concentration of 16 mM. Gas exchange measurements were conducted
at [CO2]=350 (imol mol"' and light intensity, 7=1200 ̂ mol m"

2 s"'.

Analysis of the temperature dependence of CO2 assimilation rate - Tania June

In a similar study with Festuca arundinaceae grown at 10 and 25°C, Treharne & Nelson (1975) found
that at measurement temperatures above 15°C, net photosynthesis rates per unit area were higher in plants
grown at 25°C. The authors concluded that greater photorespiration rates were important in accounting for
the low net photosynthetic rates of the 10°C plants at higher temperature measurements. However, in the
photosynthesis model used in this manuscript, photorespiration is already taken into account in the form of F
* (CO2 compensation partial pressure in the absence of dark respiration) and c\ (CO2 concentration in the
intercellular air spaces). Treharne & Nelson (1975) further concluded that the decrease in photosynthesis
above 30°C seen in both groups of plants was due primarily to a decrease in stomatal conductance, and
hence c\, the decrease in c\ was not observed in my results (as seen in Figure. 2) with increasing temperature.

for net CC>2 uptake for plants grown at day/night temperature of 10/10°C was 12°C for Agave
americana and 15°C for A. deserti. When the growth temperature was raised to 30/30°C, the optimum
temperature shifted upward by 7°C for A. americana and 3°C for A. deserti. Shifting A. americana to the
higher growth temperature caused the maximum rate of net CC>2

BIOTROPIA NO. 24, 2005

uptake at the optimal temperature to increase, whereas the same shifting of A. deserti caused it to decrease.
The results showed that A(T0), i.e. the optimum temperature for net assimilation rate or rate of
photosynthesis, increase with increasing growth temperature.

Plants grown under 700 ^mol mol"' [CO2] exhibited a similar pattern as those grown under ambient [CO2], with
T0 = 28.0 ± 0.4 and 32.2 + 0.7°C and A(T0) = 20.7 + 2.0 and 21.8 ± 0.7 tamol m'

2 s'j for plants grown at 20/15 and
32/27°C, respectively.

It is important to note that a change in c\ (the intercellular CC>2 concentration) can cause a shift in the optimum
temperature of photosynthesis, with T0 increasing with Ci (Farquhar & von Caemmerer 1982; Kirschbaum & Farquhar
1984).

There is a linear correlation between growth temperature and the optimum temperature for CO2
assimilation rate (Figure 3). The linear regression from Table 1 can be solved to give a "preferred" temperature for
the CC>2 assimilation rate of 33°C. This concept of "preferred" temperature was initially suggested by Slatyer &
Ferrar (1977), and is the intersection of the linear regression line and the 45° line. The "preferred temperature" was
also used in June (2002) to descibe the acclimation of the electron transport rate (J) to growth temperature.

Analysis of the temperature dependence of CO2 assimilation rate ‐ Tania June

What controls the reduction in CO2assimilation rate after reaching optimum
temperature?

It has been reported that high temperature limits CO2 availability, because c the physiological
responses of leaves which result in increased resistance to the ga diffusion (Mukohata et al. 1971;
Monson et al. 1982). High temperature also alter the substrate specificity of Rubisco (Jordan &
Ogren 1984; Brooks & Farquha 1985) and its activity (Weis 1981; Santarius et al. 1991).
Working with Neriun oleander, Badger et al. (1982) showed that plants grown at low
temperature ha< higher activity of several photosynthetic enzymes at low temperatures but had
lowe heat stability relative to plants grown at high temperatures. Temperature acclimatioi in the
electron transport system could also be the reason for the change in the CO: assimilation rate at
high temperature. Several studies have shown that the temperature dependence of electron
transport capacity changes with growtr temperature (Armond et al. 1978; Badger et al. 1982;
Mitchell & Barber 1986) Such changes were also observed in June (2002), where plants
grown at highei temperature had a lower electron transport rate.

Modeling the temperature dependence of the CO2‐assiiniIation rate

The basic assumption underlying the modelling is that the rate of photosynthesis at any
temperature is controlled by the activity of enzyme RuBP carboxylase‐oxygenase (Rubisco),
denoted as Vcmm, and the potential rate of regeneration of RuBP, denoted as Jmax/4. Therefore,
at a given temperature, the net CO2‐assimilation rate, A, is taken as being either the Rubisco‐limited
rate, Av, or the estimated RuBP‐regeneration‐limited rate of photosynthesis, Aj, whichever is
smaller (units of umol m"2 s"1).

where c\ = partial pressure of CO2 in the leaf, F* = CO2 compensation partial pressure in the
absence of dark respiration, /?d

= dark respiration by the leaf which continues in the light, O =
ambient partial pressure of oxygen, and ATC and K0 are the Michaelis‐Menten constants for
carboxylation and oxygenation by Rubisco, respectively. Temperature dependence of c\ follows the
equations from Figure 2. R^ follows this equation:

BIOTROPIA NO. 24, 2005

Rd =A l +A 2 (T-25)+A,(T-25)2 (3)
where T i s leaf temperature (°C) and ,4], A2andAi are the fitted parameters of the Rf temperature
relationship (Table 2), which was obtained from June (2002). The temperature dependence of Kc
and K0 follows an Arrhenius function as

where R is the Universal gas constant, 8.3144 J mol"1 K"'. Ef and E0 are the apparent activation
energies with the 25 subscript representing the value at 25°C.

The effect of temperature on the CC>2 compensation point of photosynthesis in the
absence of mitochondrial (dark) respiration follows the equation of von Caemmerer et al.
(1994), assuming infinite wall conductance.

The temperature dependence ofJ and Fcmax is given by the following equations June (2002):

where J(T0), T0, Q, C\, C2 and C3 are the fitting parameters, specific for each set of growth
conditions (Table 2). The capacity of the electron transport rate can be inferred from

where the light dependence of electron transport, J, follows the equation by .Farquhar & Wong
(1984):

Analysis of the temperature dependence of CO2 assimilation rate - Tania June

•/max is the maximum (light-saturated) rate of electron transport capacity of the leaf, 0 is the
curvature factor of the light response curve of Eq. (10) and a-i is the quantum yield of electron
transport. / is the amount of light intensity incident on the leaf surface. /2 in Eq. (9) is equal to 021.
The temperature dependence of © follows the equation of June (2002):

where T\= 0.93, T2 = 0.0145, and T-> = -8.13 the W
4' These curvature factor parameters were

obtained from June (2002), where measurement of the light curves was done with light incident on
both the upper and lower surface of the leaf.

BIOTROPIA NO. 24,2005

Simulated CO2 assimilation rate

The simulation results, based on Table 2, at measurement temperatures of 15 to 40°C and / =
1200 umol m"2 s"1, are shown in Figure 4. Figure 5 shows the results for Jmax, converted from J
using Eqs. (9) to (11). Fcmax is constantly increasing with temperature, in relatively good agreement
with Wang et al. (1996) and other estimates (Wullschleger 1993). However, Ferrar et al.
(1989) who investigated several species of Eucalyptus grown at contrasting temperatures found that
in leaves grown at high temperature, F"cmax increased with short-term temperature measurement, but
in leaves grown at low temperature, Kcmax did not increase as measurement temperature increased.
They speculated that Rubisco may be inactivated or damaged at measurement temperatures
higher than the growth temperature. In my experiment, although Fcmax increases with short-term
temperature measurements for all growth conditions, plants grown at higher temperature have a
slightly lower Fcmax than plants grown at lower temperature.

June (2002) showed that there is an acclimation in the electron transport rate which favours
the lower growth temperature (20/15 °C). Hence, if there is no stomatal effect due to different
growth temperatures, then the CO2-assimilation rate of plants grown at 20/15 °C will be higher than
that of plants grown at 32/27 °C in the model (as seen in Figure 4).

The lower observed CO2-assimilation rate of plants grown at 20/15°C (Figure 1), and their
lower assimilation rate at T0, make these plants a poor representation of this simulation (compare
Figure 1 and Figure 4). The standard measurements of those particular leaves (standard
measurement was done at light intensity of 1200 umol irfV, vpd =12.5 mbar, [CCy = 350 umol
mol"', and temperature = 25°C), before starting each measurement were lower on the first day the
plants were taken out from the growth chamber (the day when those measurements were done).
They were increased by 19.5 % the next day. If the data (of the 20/15°C plants) were corrected
with this percentage, plus taking into account the reduced ci( then the CO2-assimilation rate at T0 of
plants grown at 20/15°C would be higher than the other two growth temperature of plants as shown
by the simulation result in Figure 4.

The simulation shows that differences in the temperature dependence of A are due to the
differences in the processes limiting^. For example, A for 20/15 °C plants is limited by RuBP
regeneration below 23°C and is limited by Rubisco activity at temperatures higher than 23°C,
while A for 32/27°C plants is limited by RuBP regeneration below 30°C and is limited by
Rubisco activity at temperature higher than 30°C. For plants grown at 25/20°C, A was limited by
RuBP regeneration below 28°C and limited by Rubisco activity at temperature higher than
28°C. A co-limitation of these two capacities occurs at the optimum temperature (where Av and AJ
lines cross in Figure 4) and only one of them would limit photosynthetic rate at other
temperatures, with the penalty of excess investment in the other capacity. Therefore, when
growth temperatures vary, changes in the organization of the photosynthetic apparatus are
necessary, and this can be shown by the changed optimal ratio of Jmaxs / Vmaxs (Farquhar &
Caemmerer 1982).

Analysis of the temperature dependence of CO2 assimilation rate - Tania June

The simulated ratio of Jmaxs / Vcmaxs

Figures 4 and 5 show that between 15 and 35°C, the relative slope of the increase in Jmax
is higher than it is in Fcmax; then the opposite happens with further increase in temperature. As the
slope of increase in Jmax with temperature was higher than that of Fcmax within the range of 15 - 30°C
(Figures 4 and 5), the simulation predicts that the ratio of Jmax/Vcmax would increase with
temperature within this range. Figure 5 indicates that plants change the allocation of their
photosynthetic resources between these two capacities as growth temperature changes. June (2002)
showed that ./max/Fcmax did have a lower value when plants were grown at 32/27°C compared to plants
grown at lower temperatures, which is supported here by the simulation.

BIOTROPIA NO. 24, 2005

Farquhar & von Caemmerer (1982) and recently Hikosaka (1997) predicted that the
photosynthetic rate should be co-limited by Fcmax and Jmax at the growth temperature for efficient
nitrogen utilization of photosynthesis. Figure 4 shows that the temperature where the two processes
co-limit photosynthesis in the simulation (i.e. where Av and Aj lines cross) was close to the growth
temperature. It was around 23°C for plants grown at 20/15°C, 27 °C for plants grown at 25/20°C
and 30°C for plants grown at 32/27°C. The slight differences are probably due to the different
light intensity used in the measurement (1200 iimol m"2 s"') compared to that in the growth chamber
(600-700 umol m~2 s"'). Under lower light, the electron transport rate would be lower and it might
co-limit at a lower temperature than the ones from Figure 4, which would improve the agreement
for plants grown at the lower two growth temperatures.

When J is converted to Jmax using Eq. (9), the value depends on which 0 value is used (as shown
in Figure 5). Using 0 = 0.7, the estimated Jmax was higher as tem-

Analysis of the temperature dependence of CO2 assimilation rate - Tania June

perature increased than the estimated Jmm calculated using a Θ that increased with temperature.
This difference affects the ratio of Jmm/ycmm, with a higher ratio obtained when Θ was held constant
at 0.7.

Now, the temperature where co-limitation occurs changes from that in Figure 4. For plants
grown at 20/15 and at 25/20°C, it is almost the same at 33 -35°C. Plants grown at 32/27°C, were
always limited by A-y Figure 6 also shows that for conditions in which electron transport
becomes limiting (that is, growth at high temperature), the electron transport rate will dominate
the behaviour of the CO2-assimilation rate, so the optimum temperature of A should shift towards the
optimum temperature of Jmm.

CONCLUSIONS

The temperature response characteristics of the photosynthetic process are not fixed but
depend on the prevailing conditions during growth. The present study shows how the
temperature dependence of the photosynthetic rate differs between plants grown at different
temperatures. The factors responsible for the difference include the change in temperature
dependences of the two processes controlling photosynthesis, carboxylation and regeneration
of RuBP. The change in the proportion of photosynthetic resources into these two capacities can be
shown by the change of the Jmax/ Vcmaxs ratio with growth temperature.

BIOTROPIA NO. 24, 2005

Acclimation to growth temperature occurred as shown by the changing optimum
temperature with growth temperature. This acclimation is important for plants in optimising their
photosynthesis rate in the environment they are exposed to in terms of the most economical way of
using photosynthetic resources.

For the soybean plants used in this experiment, the optimum temperature for electron
transport (J) was a few degrees higher than the preferred temperature for CO2-assimilation rate
(33°C). Hence an increase in temperature during the day to more than 33°C will still increase the
electron transport rate, although not the CO2-assimilation rate.

For the purpose of modelling plant growth or modelling the capacity of plants in absorbing
CO2 in relation to the changing environmental conditions (atmospheric CO2 concentration,
temperature, light intensity, nitrogen, and water availability effect on supply of CO2), the most
useful models will be those which incorporate acclimation processes at all levels of organization
within the plants. These models will be the most precise and the most responsive to changes in
the physical and biological factors which control photosynthesis. However, the knowledge of the
mechanisms of temperature dependence of photosynthesis is still limited and so the combination of
an empirical approach with the mechanical ones in these areas where the mechanism is already
established would be beneficial.

REFERENCES

Armond P. A., Schreibcr U. and O. Bjorkman. 1978. Photosynthetic acclimation to tempe-rature in the desert shrub,
Larrea diraricata. II. Light Harvesting Efficiency and electron transport. Plant Physiology, 61:411-415.

Badger, M. R. and G.J. Collate. 1977. Studies on the kinetic mechanism of ribulose-l,5-bisphosphate carboxylase and
oxygcnase reactions, with particular reference to the effect of temperature on kinetic parameters. Carnegie Institute
of Washington Yearbook, 76:355-361.

Badger, M.R., Bjorkman, O. and P.A. Armond. 1982. An analysis of photosynthetic response and adaptation to
temperature in higher plants: temperature acclimation in the desert evergreen Nerium oleander L. Plant, Cell and
Environment, 5: 85-99.

Berry, J. and O. Bjorkman. 1980. Photosynthetic response and adaptation to temperature in higher plants. Annual Review of
Plant Physiology, 31:491 -543.

Brooks, A. and G.D. Farquhar 1985. Effect of temperature on the COrO2 specificity of ribulose-1,5-bisphosphatc
carboxylasc/oxygenasc and the rate of respiration in the light. Estimates from gas exchange measurements on
spinach. Planta, 165: 397-406.

Farquhar, G. D. and S. von Caemmerer. 1982. Modelling of photosynthetic responses to environmental conditions.
Physiological plant ecology. II. Encyclopedia of Plant Physiology, New Series. O. L. Lange, P.S. Nobel, C.B.
Osmond and H. Ziegler. Berlin, Springer-Vcrlag.

Farquhar, G.D., von Caemmerer, S. And J.A. Berry. 1980. A biochemical model of photosynthetic CO2 assimilation in leaves
of C3 species. Planta, 149: 78-90.

Analysis of the temperature dependence of COZ assimilation rate - Tania June

Ferrar, P.J., Slatyer, R.O. and J.A. Vranjic. 1989. Photosynthetic temperature acclimation in Eucalyptus species from
diverse habitats and a comparison with Nerium oleander. Australian Journal of Plant Physiology, 16: 199-217.

Herridge, D.F. 1977. Carbon and nitrogen nutrition of two annual legumes. University of Western Australia.
Perth.

Hikosaka, K. 1997. Modelling optimal temperature acclimation of the photosynthetic apparatus in C3 plants with
respect to nitrogen use. Annals of Botany, 80: 721 -730.

Jordan, D. B. and W. L.Ogren 1984. The CO2/O2 specificity of ribulose, 1,5-bisphosphate carboxylase/oxygenase.
Dependence on ribulosebisphosphate concentration, pH and temperature. Planta, 161:308-313.

June, T. 2002. Environmental Effects on photosynthesis of C3 plants: scaling up from electron transport to the
canopy (Study case: Glycine max L. Merr). Environmental Biology, Research School of Biological Sciences.
Australian National University. Canberra.

Kirschbaum, M.U.F. and G.D. Farquhar. 1984. Temperature dependence of whole-leaf photosynthesis in Eucalyptus
pauciflora Sieb. ex Spreng. Australian Journal of Plant Physiology, 11: 519-538.

Lange, O.L., Schulze, E.D., Evenari, M., Kappen, L., and U. Buschbom. 1974. The temperature-related
photosynthetic capacity of plants under desert conditions. I. Seasonal changes of the photosynthetic response to
temperature. Oecologia, 17: 97-110.

Mitchell, R.A.C. and J. Barber. 1986. Adaptation of photosynthetic electron-transport rate to growth temperature
in pea. Planta, 169: 429-436.

Monson, R.K., Stidham, M.A., Williams, G.J. and G.E. Edwards. 1982. Temperature dependence of
phothosynthesis in Agropyron smithii Rydb. Plant Physiology, 69: 921-928.

Mukohata, Y., Mitsudo, M., Kakumoto, S., and M. Higashida. 1971. Biophysical studies on subcellular particles. V.
Effects of temperature on the fcrricyanide-Hill reaction, the light-induced pH shift and the light scattering
response of isolated spinach chloroplasts. Plant Cell Physiology, 12: 869-80.

Nobel, P.A and T.L. Hartsock. 1981. Shifts in the optimal temperature for nocturnal CO2 uptake caused by changes
in growth temperature for cacti and agaves. Physiologia Plantarum, 53: 523-527.

Santarius, K.A., Exner, M. and R. Thebud-Lassak. 1991. Effect of high temperature on the photosynthetic apparatus in
isolated mesophyll protoplasts of VaUrianella locusta (L.) Betcke. Photosynthetica, 25: 17-26.

Slatyer, R.O. 1977. Altitudinal variation in the photosynthetic characteristics of snow gum, Eucalyptus pauciflora
Sieb. Ex Spreng. IV. Temperature response of four populations grown at different temperatures. Australian
Journal of Plant Physiology, 4: 595-609.

Slatyer, R.O. and P.J. Ferrar. 1977. Altitudinal Variations in the photosynthetic characteristics of snow gum,
Eucalyptus pauciflora Sieb. Ex Spreng. V. Rate of acclimation to an altered growth environment.
Australian Journal of Plant Physiology, 4: 595-609.

Trehame & Nelson 1975 In: Plants and Temperature. (Eds. S.P. Long and F.I. Woodward). Symposium of the
Society of Experimental Biologists, vol. 42. Cambridge: Company of Biologists, p. 329-346.

von Caemmerer, S., Evans, J.R., Hudson, G.S. and T.J. Andrews. 1994. The kinetics of Rubisco inferred from
measurements of photosynthesis in leaves of transgenic tobaco with reduced Rubisco content. Planta, 195: 33-
47.

BIOTROPIA NO. 24, 2005

Wang, K. Y., Kellomaki, S. and K. Laitinen. 1996. Acclimation of photosynthetic parameters in Scots Pine after three
years exposure to elevated temperature and CO2. Agricultural and Forest Meteorology, 82: 195-217.

Weis, E. 1981. Reversible heat-inactivation of the calvin cycle: a possible mechanism of the temperature regulation of
photosynthesis. Planta, 151: 33-39.

Wullschleger, S.D. 1993. Biochemical limitation to carbon assimilation in €3 plants. A retrospective analysis of A/Ci
curves from 109 species. Journal of Experimental Botany, 44: 907-920.

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