JXB Advance Access originally published online on December 19, 2005
Journal of Experimental Botany 2006 57(2):291-302; doi:10.1093/jxb/erj049
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
RESEARCH PAPER |
Temperature acclimation of photosynthesis: mechanisms involved in the changes in temperature dependence of photosynthetic rate
Graduate School of Life Sciences, Tohoku University, Sendai 980-8578, Japan
* To whom correspondence should be addressed. E-mail: hikosaka{at}mail.tains.tohoku.ac.jp
Received 19 June 2005; Accepted 10 November 2005
 |
Abstract |
|---|
Top
Abstract
IntroductionGrowth temperature alters temperature dependence of the photosynthetic rate (temperature acclimation). In many species, the optimal temperature that maximizes the photosynthetic rate increases with increasing growth temperature. In this minireview, mechanisms involved in changes in the photosynthesis–temperature curve are discussed. Based on the biochemical model of photosynthesis, change in the photosynthesis–temperature curve is attributable to four factors: intercellular CO2 concentration, activation energy of the maximum rate of RuBP (ribulose-1,5-bisphosphate) carboxylation (Vc max), activation energy of the rate of RuBP regeneration (Jmax), and the ratio of Jmax to Vc max. In the survey, every species increased the activation energy of Vc max with increasing growth temperature. Other factors changed with growth temperature, but their responses were different among species. Among these factors, activation energy of Vc max may be the most important for the shift of optimal temperature of photosynthesis at ambient CO2 concentrations. Physiological and biochemical causes for the change in these parameters are discussed.
Key words: Activation energy, gas exchange, limitation, limiting step, model, nitrogen use, optimal temperature, photosynthetic acclimation, temperature response
|
Introduction |
|---|
With the predicted increase in global air temperature induced by the greenhouse effect, plant responses to increasing temperature have become a major area of concern (Gunderson et al., 2000
; Rustad et al., 2001). For modelling of photosynthesis, many studies have used the biochemical model of Farquhar et al. (1980), which mechanistically and realistically describes photosynthetic responses to environmental variables. However, many modelling studies have ignored intra- and interspecific difference in photosynthetic responses to temperature. One of the reasons is insufficient information on the full parameterization of the temperature response of the model (Leuning, 2002; Medlyn et al., 2002a, b).
In most plants, as a direct response to temperature, the light-saturated rates of photosynthesis are low at extreme low and high temperatures and have an optimum at intermediate temperature. With changes in growth temperature many plants show considerable phenotypic plasticity in their photosynthetic characteristics. In general, plants grown at higher temperature have a higher optimal temperature of photosynthetic rate (Berry and Björkman, 1980). For example, Slatyer (1977) found a linear relationship between optimal and growth temperature with a slope of 0.34 °C °C–1 in Eucalyptus pauciflora, i.e. the optimal temperature increased by c. 1 °C with an increase in growth temperature by 3 °C. Similar slopes were observed in Oxyria digyna (Billings et al., 1971) and in Ledum groenlandicum (Smith and Hadley, 1974). Battaglia et al. (1996) reported 0.59 and 0.35 °C °C–1 for Eucalyptus globulus and E. nitens, respectively. Cunningham and Read (2002) studied four temperate and four tropical evergreen species and found an interspecific difference in the relationship. In one of the temperate species (Eucryphia lucida), the optimal temperature was independent of growth temperature. The other seven species showed significant dependence, but the slope differed among species from 0.10 °C to 0.48 °C °C–1.
Changes in the temperature dependence of photosynthesis may be ascribed to changes in the activity and amount of photosynthetic components and/or CO2 concentration in the carboxylation site. However, the response of each factor to temperature seems to differ among species (Berry and Björkman, 1980; Badger et al., 1982; Ferrar et al., 1989; Makino et al., 1994; Hikosaka et al., 1999; Yamasaki et al., 2002). In this minireview, mechanisms involved in the acclimational changes in the photosynthesis–temperature curve, based on the biochemical model of C3 photosynthesis (Farquhar et al., 1980; von Caemmerer, 2000) are discussed. Four parameters are raised in the model, which potentially cause the change in temperature dependence of photosynthetic rates. Using published and unpublished data, the contribution of each parameter to photosynthetic acclimation in actual plants was assessed. The biochemical background of the changes in the parameters is also discussed. This work focuses on the temperature range where plants can grow and reproduce and acclimation to stressful temperatures (i.e. freezing, chilling, and very high temperatures) is outside the scope.
|
Theory |
|---|
In the biochemical model of C3 photosynthesis, the photosynthetic rate is limited either by the RuBP (ribulose-1,5-bisphosphate) carboxylation or by the RuBP regeneration (Farquhar et al., 1980
). The limiting step is different depending on the CO2 concentration. At low CO2 concentrations, RuBP is saturated and carboxylation of RuBP is the limiting step of photosynthesis. The photosynthetic rate (Pc) is expressed as a function of intercellular CO2 concentration (Ci):
 | (1) |
* is the CO2 compensation point in the absence of day respiration.
Although Equation 1 is based on Rubisco kinetics, it involves other properties. First, Ci is not the same as the CO2 concentration at the carboxylation site (Cc). Cc can be determined with several methods, concurrent measurement of gas exchange and carbon isotope discrimination (von Caemmerer and Evans, 1991) or chlorophyll fluorescence (Harley et al., 1992a), although use of these methods for field-grown plants is not simple. Due to a significant resistance in CO2 diffusion from intercellular spaces to stroma, Cc is c. 70% of Ci (von Caemmerer and Evans, 1991; Evans and von Caemmerer, 1996). Kc and Ko in Equation 1 are adjusted to values including the effect of internal CO2 conductance and thus differ from their true values (von Caemmerer et al., 1994). Second, for catalysis, Rubisco needs to be activated with CO2 and Mg2+. The activation state of Rubisco changes in response to light, CO2 concentration, and other environmental factors (Perchorowicz et al., 1981; Sage et al., 1988; Kanechi et al., 1996; Feller et al., 1998). Regulation of activation is complex and involves the protein Rubisco activase (Salvucci and Crafts-Brandner, 2004a). Thus Pc is affected by Rubisco kinetics, Rubisco activation state, and CO2 diffusion within the leaf. In spite of the complexity, Equation 1 clearly demonstrates the CO2 dependence of photosynthetic rate at low Ci (von Caemmerer and Farquhar, 1981).
At high CO2 concentrations, RuBP is not saturated and the photosynthetic rate (Pr) is limited by RuBP regeneration. Under light-saturated conditions Pr is expressed as
 | (2) |
; Sage, 1990) is not included in the analyses, because of the difficulty in distinguishing TPU limitation from RuBP limitation in the CO2 response curve of photosynthesis (but it will be discussed later).
The rate of photosynthesis (P) that is realized is the minimum of the two,
 | (3) |
Temperature dependence of the parameters is fitted using the Arrhenius model if it increases exponentially:
 | (4) |
 | (5) |
S is an entropy term (Johnson et al., 1942; von Caemmerer, 2000; Medlyn et al., 2002b).
In the present study, the effect of dark respiration (day respiration) is ignored, although it sometimes has significant effects on the temperature dependence of net photosynthetic rates. Although the values of Kc, Ko, and * may be slightly different across species and growth conditions, the values have not been determined for each species. In the present study, as in many previous studies, it is assumed that Kc, Ko, and * are not affected by growth conditions or by species (but it will be discussed later). Changes in the temperature dependence of P are ascribed to changes in (i) Ci, (ii) Ea of Vc max, (iii) Ea of Jmax, and (iv) the ratio of Jmax to Vc max. In the following sections, how these factors change with growth temperature and their potential contribution to the photosynthesis–temperature curve will be discussed.
|
Intercellular CO2 concentration |
|---|
Temperature dependence of photosynthesis is sensitive to the CO2 concentration; the optimal temperature increases with CO2 concentration (Fig. 1a; Berry and Björkman, 1980
). Two factors are involved in this shift of optimal temperature (Kirschbaum and Farquhar, 1984). One is the shift of the limiting step. In many species, as discussed later, the optimal temperature of Pr is higher than that of Pc (Kirschbaum and Farquhar, 1984; Hikosaka et al., 1999). Since RuBP regeneration limits photosynthesis at higher CO2 concentrations, the optimal temperature is high at high CO2 concentrations. The other is related to the kinetics of Rubisco, which has a large effect on Pc. At low CO2 concentrations, the carboxylation rate is less sensitive to temperature because an increase in Kc partly cancels the increase in Vc max. Furthermore, the photorespiration rate increases with temperature because * increases (Brooks and Farquhar, 1985). These effects are smaller at higher CO2 concentrations, leading to an increase in the optimal temperature of Pc. Figure 1b shows the calculated CO2 dependence of the optimal temperature maximizing Pc. The optimal temperature increases by c. 0.05 °C per 1 µmol mol–1 CO2, although the increment decreases with increasing CO2 concentration.
|
Temperature dependence of Ci potentially affects the temperature dependence of photosynthesis. The optimal temperature is low if Ci decreases with increasing leaf temperature. Some studies showed that Ci decreases with increasing temperature in a leaf (Mooney et al., 1978
; Ferrar et al., 1989). However, it has been shown that stomatal conductance is more sensitive to vapour pressure deficit (VPD) than to temperature. Leuning (1995) suggested that stomatal conductance is regulated so as to maintain the ratio of Ci to Ca (air CO2 concentration) constant, irrespective of temperature if VPD is constant. If leaf temperature is increased with a constant water vapour pressure, then VPD increases with leaf temperature, which may decrease Ci.
Effects of growth temperature on Ci are different among species; in some studies Ci decreased with decreasing growth temperatures (Williams and Black, 1993; Hikosaka et al., 1999; Hikosaka, 2005) but not in others (Hendrickson et al., 2004). Ferrar et al. (1989) showed that two out of six Eucalyptus species had a low Ci when they were grown at low temperature, but four species did not show such tendencies. A large difference in Ci between leaves grown at different temperatures was found in Quercus myrsinaefolia; 230 and 300 µmol mol–1 in leaves grown at 15 °C and 30 °C, respectively (Hikosaka et al., 1999), which might cause a shift of optimal temperature by 3 °C.
|
Temperature dependence of RuBP carboxylation-limited photosynthesis |
|---|
In vitro Rubisco activity at saturating CO2 exponentially increases with temperature (Jordan and Ogren, 1984
). Similarly, in many species, Vc max determined at a leaf-level (‘apparent’ Vc max) exponentially increases from 15 °C to 30 °C, but the deactivation is often substantial at very high temperature (Harley and Tenhunen, 1991; Leuning, 2002; Medlyn et al., 2002b; Han et al., 2004). In Plantago asiatica, deactivation was not obvious until 40 °C so the Arrhenius model (Fig. 2a) was applied. The activation energy, EaV, is a measure of temperature dependence of Pc. EaV has been reported to increase with growth temperature (Fig. 2a; Hikosaka et al., 1999; Yamori et al., 2005). Figure 3a shows the relationship between EaV and growth temperature obtained from published and unpublished data. There was a large variation in EaV among species, but in each species, EaV consistently increased with growth temperature. It is notable that the slope is similar among species, suggesting that it is a general response to growth temperature.
|
|
As EaV increases, the optimal temperature of Pc at ambient CO2 increases with temperature (Fig. 2b). Figure 3b shows the calculated optimal temperature for Pc as a function of EaV. The optimal temperature increases by 0.54 °C per 1 kJ mol–1 EaV (of course, the optimal temperature is not a simple function of EaV if the deactivation is substantial). In this survey, the relationship between EaV and growth temperature implies that with a 10 °C increase in growth temperature the EaV increases by 10 kJ mol–1 (Fig. 3a). Combining Fig. 3a and b, the slope of the relationship between optimal and growth temperature is expected to be 0.54 °C °C–1. This is close to the values obtained in previous studies (see Introduction).
Several mechanisms may be involved in the change in EaV. The first one is the internal CO2 conductance. As mentioned above, Ci is not the same as CO2 concentration at the carboxylation site (Cc). The Cc to Ci ratio may vary among leaves (Terashima et al., 2005). If the Cc to Ci ratio is low, the optimal temperature for Pc decreases and the EaV will be calculated to be low. Makino et al. (1994) studied the relationship between gas exchange and Rubisco activity in rice (Oryza sativa) grown at different temperature. They found that the photosynthetic rate per unit Rubisco at a low Ci was low in leaves grown at low temperature. As Rubisco was not inactivated, they argued that Cc was lower in leaves grown at lower temperature. However, in Nerium oleander, a simultaneous measurement of gas exchange and chlorophyll fluorescence suggested that Cc was not different between leaves grown at 20 °C and 35°C (Hikosaka and Hirose, 2001). Bernacchi et al. (2002) determined the temperature dependence of internal CO2 conductance in tobacco (Nicotiana tabacum) leaves, which increased with increasing temperature with a temperature coefficient (Q10) of 2.2 and had a maximum at 35–37.5 °C. Therefore, the photosynthetic rate above a leaf temperature of 40 °C may be suppressed by a lowered Cc.
The second candidate is the activation state of Rubisco. It has been reported that the activation state of Rubisco decreases at high temperature (Weis, 1981; Kobza and Edwards, 1987). Crafts-Brandner and Salvucci (2000) showed that, when leaf temperature exceeded 35 °C, the photosynthetic rate in cotton was lower than that expected from Rubisco kinetics. The decrease in photosynthesis is ascribed to a decrease in Rubisco activation state (Law and Crafts-Brandner, 1999; Crafts-Brandner and Salvucci 2000; Salvucci and Crafts-Brandner, 2004a). Inactivation of Rubisco at high temperature may involve a decrease in activity of Rubisco activase (Crafts-Brandner and Salvucci, 2000; Salvucci and Crafts-Brandner, 2004a) and an increase in the synthesis of xylulose-1,5-bisphosphate, the catalytic misfire product, which inactivates Rubisco (Salvucci and Crafts-Brandner, 2004b).
In cotton grown at 28 °C, inactivation of Rubisco is obvious only at leaf temperatures higher than 35 °C (Crafts-Brandner and Salvucci, 2000; Salvucci and Crafts-Brandner, 2004a). The optimal temperature of Pc at ambient CO2 is lower than 35 °C in most of species, therefore Rubisco activation state may be less effective at the temperature that is lower than the optimum. However, for Antarctic hairgrass (Deschampsia antarctica), Salvucci and Crafts-Brandner (2004c) showed that inactivation occurred when leaf temperature exceeded 20 °C, which was responsible for the decrease in the optimal temperature. Thus the activation state may have a significant effect on temperature dependence of photosynthesis in some species. Change in the activity of Rubisco activase is possibly involved in the temperature acclimation of photosynthesis. Law et al. (2001) showed that heat stress induces the synthesis of a new form of Rubisco activase in cotton. The difference in the heat stability between the two isoforms of Rubisco activase can be responsible for the change in photosynthesis–temperature curves (Law and Crafts-Brander, 1999). However, experimental results suggest that activation state of Rubisco is not involved in temperature acclimation in Nerium oleander (Badger et al., 1982) and rice (Makino et al., 1994).
There may be several populations of Rubisco that respond differently to temperature (Yamori et al., 2005). The balance between the two populations changes with growth temperature that, in turn, changes the EaV. Higher plants have only a single copy per chloroplast genome of the large subunit gene, but the small subunit genes constitute a multigene family ranging from 2 to 12 members (Gutteridge and Gatenby, 1995). Different combinations of the large and small subunit may produce a different nature of Rubisco.
Kinetic parameters of Rubisco (Kc, Ko, *) have been evaluated for only a limited number of species, and therefore this limited data set of the kinetic parameters has been used for modelling of photosynthesis. However, recently it has been suggested that the kinetic parameters are different among speceis (Galmés et al., 2005). Bunce (1998) reported that * increased with decreasing growth temperature in wheat and barley. Its generality and contribution to temperature dependence are unclear.
|
Temperature dependence of RuBP regeneration-limited photosynthesis |
|---|
Jmax at a leaf level (‘apparent’ Jmax) can be assessed with several methods: gas exchange (Farquhar et al., 1980
), O2 evolution at saturating CO2 (Yamasaki et al., 2002), and chlorophyll fluorescence analysis at saturating CO2 (Niinemets et al., 1999). In many species, deactivation of Jmax occurs at high temperature (Fig. 4a; Harley and Tenhunen, 1991; Leuning, 2002; Medlyn et al., 2002b). The reduction of Jmax at high temperature affects the temperature dependence of Pr (Fig. 4b).
|
A shift in the optimal temperature for apparent Jmax with growth temperature was observed in some species (Fig. 4a; Badger et al., 1982
; Yamasaki et al., 2002), but not in others (Armond et al., 1978; Mitchell and Barber, 1986; Sage et al., 1995). Furthermore the slope of the curve below the optimal temperature increases with growth temperature in many studies (Armond et al., 1978; Badger et al., 1982; Mitchell and Barber, 1986; Sage et al., 1995; Hikosaka et al., 1999; Yamasaki et al., 2002). In Plantago asiatica, the Ha of the apparent Jmax in the peak model significantly increased with growth temperature (Fig. 4a). However, this pattern was not general in the data set of the survey (data not shown).
Changes in the heat tolerance in components of the RuBP regeneration process have been shown by many studies. Badger et al. (1982) showed that the thermal stability of various Calvin cycle enzymes changes with growth temperature in Nerium oleander. For example, exposure of leaves to 45 °C for 10 min decreased Ru5P (ribulose-5-phosphate) kinase activity in leaves grown at 20 °C by 50%, but did not affect leaves grown at 45 °C. Using chlorophyll fluorescence analysis, many studies have shown that the thermostability of photosystem II changes with growth temperature (Armond et al., 1978; Berry and Björkman, 1980; Yamasaki et al., 2002; Haldimann and Feller, 2005). However, it is unclear what components determine the temperature dependence of Jmax. Although it has been considered that electron transport limits the RuBP regeneration rate (Farquhar et al., 1980; Kirschbaum and Farquhar, 1984; von Caemmerer, 2000), temperature dependence of the electron transport rate in vitro (e.g. the Hill activity) is different from that of the apparent Jmax in several studies. For example, in pea (Pisum sativum) leaves, Ea of the O2 evolution rate increased with growth temperature, but the Hill activity was not affected by growth temperature (Mitchell and Barber, 1986). In Nerium oleander, the optimal temperature of photosynthetic rate at high CO2 increased with growth temperature, while the optimal temperature of the Hill activity did not change (Badger et al., 1982). Badger et al. (1982) suggested that stroma FBPase (fructose-1,6-bisphosphatase) was the limiting step in photosynthesis at high CO2 in Nerium oleander. In wheat (Triticum aestivum), on the other hand, temperature dependence of the Hill activity and photosystem II activity were similar to that of the O2 evolution rate (Yamasaki et al., 2002). These facts suggest that the limiting step for the RuBP regeneration process is different among species.
Triose-phosphate utilization (TPU) is the third potential limiting step for light-saturated photosynthesis (Sharkey, 1985; Sage, 1990). It has often been believed that TPU limits photosynthesis only at very high CO2 concentrations (Sage, 1994), but Labate and Leegood (1988) showed that TPU limits photosynthesis under normal CO2 concentrations at lower temperature in barley (Hordeum vulgare) leaves. When photosynthesis is limited by TPU, the photosynthetic rate does not depend on the CO2 concentration. Since Pr also becomes less sensitive to CO2 concentration at low temperatures, CO2 dependence of photosynthesis is not a good indicator to identify which of TPU or RuBP regeneration limits photosynthesis. O2 sensitivity is useful because of different O2 sensitivity between Pr and TPU-limited photosynthesis (Sharkey, 1985; Sage, 1990). Harley et al. (1992b) showed that the TPU-limited photosynthetic rate in cotton leaves had a temperature dependence that was similar to the temperature dependence of the apparent Jmax.
|
The balance between carboxylation and regeneration of RuBP |
|---|
Temperature dependences of Pc and Pr at normal CO2 concentration are generally different from each other (Kirschbaum and Farquhar, 1984
; Hikosaka et al., 1999). Therefore the temperature dependence of the photosynthetic rate changes depending on the limiting step. Furthermore, the balance between carboxylation and regeneration of RuBP potentially affects the temperature dependence of photosynthesis (Farquhar and von Caemmerer, 1982; Hikosaka, 1997; Onoda et al., 2005b). Figure 5 illustrates the effect of balance between the two processes on the temperature dependence of photosynthesis. At a normal CO2 concentration, as mentioned above, Pc is less temperature-dependent and has a lower optimal temperature than Pr (Figs 2b, 4b). When plants increase Pr relative to Pc (i.e. higher Jmax to Vc max ratio), the optimal temperature of photosynthesis decreases (Fig. 5a), and vice versa (Fig. 5b).
|
From a literature survey of 109 species Wullschleger (1993)
showed a strong correlation between Jmax and Vc max, suggesting that the balance between carboxylation and regeneration of RuBP is constant, irrespective of species and growth conditions. However, Hikosaka et al. (1999) showed that Quercus myrsinaefolia, an evergreen tree, alters the Jmax to Vc max ratio depending on the growth temperature. When the plants are grown at high temperature, the photosynthetic rate at 350 µmol mol–1 CO2 was limited by RuBP carboxylation above 22 °C and by RuBP regeneration below 22 °C, while it was limited by RuBP carboxylation at any temperature in plants grown at a low temperature (Fig. 6). Similar changes in the Jmax to Vc max ratio have been observed in Polygonum cuspidatum (Onoda et al., 2005a), spinach (Yamori et al., 2005), and Plantago asiatica (Hikosaka, 2005).
|
However, there are also many species that did not show growth temperature-dependent changes in the Jmax to Vc max ratio: eight annual species (Bunce, 2000
), Pinus pinaster (Medlyn et al., 2002a), Nerium oleander (Hikosaka and Hirose, 2001), Fagus crenata (Onoda et al., 2005b), and Quercus crispula (K Hikosaka, unpublished data). Why do some species alter the Jmax to Vc max ratio while others do not? If the temperature dependence of Pc and Pr are similar to each other, a change in the Jmax to Vc max ratio does not alter the temperature dependence of photosynthesis (Hikosaka, 1997). Whether or not Pc and Pr have a similar temperature dependence may be ascribed to the temperature response of Vc max and Jmax (Onoda et al., 2005b). Plants with a relatively low activation energy of Jmax (HaJ) have a temperature response of Pr similar to that of Pc. Onoda et al. (2005b) found that Fagus crenata with a relatively low HaJ did not alter the Jmax to Vc max ratio depending on growth temperature, while Polygonum cuspidatum with a relatively high HaJ altered the ratio. |
Which limits photosynthesis, Pc or Pr? |
|---|
At a normal CO2 concentration (c. 370 µmol mol–1), Pc and Pr are close to each other, but generally Pr is slightly higher than Pc (i.e. photosynthesis is limited by RuBP carboxylation) (Fig. 7a). In particular, photosynthesis at the optimal temperature is limited by Pc, irrespective of growth temperature (Figs 6, 7a; Hikosaka et al., 1999
). Therefore the changes in temperature dependence of photosynthesis may be explained mainly by Vc max. An increase in the optimal temperature of photosynthesis is ascribed to the increase in EaV. RuBP regeneration is not substantial and may be responsible only when Pr is lower than Pc, which is often observed when photosynthesis is determined at temperatures lower than the growth temperature (Fig. 6b).
|
At an elevated CO2 concentration (e.g. doubled CO2 concentrations), on the other hand, photosynthesis is generally limited by RuBP regeneration (Fig. 7b; Sage, 1990
, 1994). Thus temperature dependence of Jmax and the Jmax to Vc max ratio have a large effect on temperature dependence of photosynthesis. Onoda et al. (2005a) found that autumn leaves of Polygonum cuspidatum had a higher Jmax to Vc max ratio than summer leaves, irrespective of growth CO2 concentration. Therefore, when photosynthetic rates were compared at the growth CO2 concentration, the stimulation in photosynthetic rate by elevated CO2 was higher in autumn leaves. This result indicates that temperature acclimation affects the CO2 response of photosynthesis. |
Nitrogen partitioning in the photosynthetic apparatus under different growth temperatures |
|---|
As nitrogen is a limiting resource of plant growth in many ecosystems, efficient use of nitrogen is believed to contribute to plant fitness. Since about half of leaf nitrogen is allocated to the photosynthetic apparatus, photosynthetic acclimation has been analysed in terms of nitrogen partitioning among photosynthetic components (Evans, 1989
; Hikosaka and Terashima, 1995; Hikosaka, 2004). For example, shade leaves allocate more nitrogen to chlorophyll–protein complexes for light harvesting, while sun leaves have more nitrogen in Calvin cycle enzymes and electron carriers to achieve high photosynthetic capacity at high light (Boardman, 1977; Chow and Anderson, 1987; Evans, 1987; Terashima and Evans, 1988; Hikosaka, 1996; Hikosaka and Terashima, 1996; Makino et al., 1997; Muller et al., 2005a). Nitrogen reallocation from a non-limiting to a limiting process contributes to the efficient use of nitrogen in the photosynthetic apparatus (Evans, 1989; Hikosaka and Terashima, 1995; Hikosaka, 1997).
The temperature-dependent changes in the ratio of Jmax to Vc max may be explained with the change in nitrogen partitioning in the photosynthetic apparatus. In Polygonum cuspidatum, leaves grown at low temperature had a higher ratio of cytochrome f to Rubisco (Onoda et al., 2005a). A similar result was also obtained for spinach (Yamori et al., 2005). In Plantago asiatica, the relationship between Rubisco and leaf nitrogen content was not affected by growth irradiance and temperature, but low growth temperature increased the stroma FBPase level (Hikosaka, 2005). These results suggest that plants with a flexible Jmax to Vc max ratio invest more nitrogen in the RuBP regeneration process at lower growth temperature.
Using a model of nitrogen partitioning in the photosynthetic apparatus, Hikosaka (1997) predicted that the nitrogen use efficiency of photosynthesis is maximized when the photosynthetic rate is co-limited at the growth temperature (i.e. Pc=Pr). In Quercus myrsinaefolia (Hikosaka et al., 1999) and Plantago asiatica (Hikosaka, 2005), the Pr to Pc ratio at the growth temperature was 1.2–1.3, slightly higher than the optimum, but irrespective of growth temperatures. This suggests that plants regulate nitrogen partitioning to maintain a constant Pr to Pc ratio at growth temperature.
|
Photosynthetic rate at growth temperature |
|---|
Temperature acclimation involves changes in the absolute photosynthetic rate. When compared among plants grown at various temperatures, the highest photosynthetic rate at a leaf temperature tended to be found in the plant grown at the same temperature (Slatyer, 1977
; Mooney et al., 1978; Berry and Björkman, 1980; Badger et al., 1982; Hikosaka, 2005; Yamori et al., 2005). Plants may realize the best performance at their growth temperature. In Nerium oleander, two mechanisms were involved in the regulation of photosynthetic rates in temperature acclimation (Badger et al., 1982). First, to achieve higher photosynthetic rates at low temperature, low-temperature-grown leaves had a higher amount of photosynthetic proteins. Second, high-temperature-grown leaves had a higher heat tolerance of some Calvin cycle enzymes, which enabled higher photosynthetic rates at high temperatures.
Higher amounts of photosynthetic proteins in low-temperature-grown leaves have also been reported in many studies (Holaday et al., 1992; Huner et al., 1993, 1998; Steffen et al., 1995; Strand et al., 1999; Hikosaka, 2005). It may be a compensatory response to low temperature, which decreases enzyme activity. Interestingly, in some species, the photosynthetic rate at the growth temperature tends to be similar irrespective of growth temperature (Berry and Björkman, 1980). For example, Plantago asiatica had a photosynthetic rate of 19.0 and 19.4 µmol m–2 s–1 in leaves grown at 15 °C and 30 °C, respectively (Hikosaka, 2005). This suggests that temperature acclimation is a homeostatic response to maintain the photosynthetic rate at the growth condition.
Recently Muller et al. (2005b) discussed temperature response in absolute photosynthetic rates in relation to nitrogen use. The ecological and evolutionary significance of the environmental response in leaf nitrogen content per unit area have been analysed from the viewpoint of the optimization theory. Daily carbon gain as a function of leaf nitrogen content shows a saturating curve and there is a leaf nitrogen content that maximizes daily carbon gain per unit nitrogen (nitrogen use efficiency: Hirose, 1984; Hirose and Werger, 1987). The optimal leaf nitrogen content is higher at higher growth irradiance and there is a strong correlation among the optimal and actual nitrogen content (Hirose and Werger, 1987). Muller et al. (2005b) studied seasonal change in the photosynthesis–nitrogen relationship in Aucuba japonica, an understorey shrub. The optimal nitrogen content was higher in winter than in summer and was strongly correlated with the actual nitrogen content. It should be noted that the photosynthetic rate at the growth temperature was not constant in this study. Therefore, absolute photosynthetic rates may be regulated not to keep a certain value, but to maximize nitrogen use efficiency at the growth condition.
|
Conclusion |
|---|
The change in temperature dependence of photosynthesis is caused by several factors. In most cases in the survey, EaV increased with increasing growth temperature. Other factors, Ci, temperature dependence of Jmax, and Jmax to Vc max ratio, were also reported to change with growth temperature, but there are interspecific differences in their responses. Among these factors, EaV may be most important because photosynthesis at ambient CO2 concentrations is generally limited by RuBP carboxylation rather than by RuBP regeneration. In particular, the shift of optimal temperature of photosynthesis is mainly explained by the change in EaV. However, other factors may have substantial roles in temperature acclimation. Change in the Jmax to Vc max ratio may contribute to keeping a balance between the activities of the two processes, which may maximize nitrogen use efficiency in the photosynthetic apparatus. Jmax often determines the temperature dependence of photosynthesis at elevated CO2 concentrations. Incorporating changes in these parameters may contribute to better prediction of photosynthesis under a changing environment. Physiological or biochemical causes for the change in these parameters are important questions for future study.
|
Acknowledgements |
|---|
We thank W Yamori (Osaka University) for comments. This work was supported in part by grants-in-aid from the Japan Ministry of Education, Science, Sport, and Culture.
|
Footnotes |
|---|
Present address: Department of Plant Ecology, Utrecht University, PO Box 80084, 3508 TB Utrecht, The Netherlands. 
|
References |
|---|
Armond PA, Schreiber U, Björkman O. 1978. Photosynthetic acclimation to te