Temperature acclimation of photosynthesis: mechanisms involved in the changes in temperature dependence of photosynthetic rate (2024)

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Abstract

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

Although Equation 1 is based on Rubisco kinetics, it involves other properties. First, C_i is not the same as the CO₂ concentration at the carboxylation site (C_c). C_c 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, C_c is c. 70% of C_i (von Caemmerer and Evans, 1991; Evans and von Caemmerer, 1996). K_c and K_o 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 P_c 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 C_i (von Caemmerer and Farquhar, 1981).

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 K_c, K_o, and Γ* 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 K_c, K_o, and Γ* 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) C_i, (ii) E_a of V_c max, (iii) E_a of J_max, and (iv) the ratio of J_max to V_c 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 P_r is higher than that of P_c (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 P_c. At low CO₂ concentrations, the carboxylation rate is less sensitive to temperature because an increase in K_c partly cancels the increase in V_c max. Furthermore, the photorespiration rate increases with temperature because Γ* increases (Brooks and Farquhar, 1985). These effects are smaller at higher CO₂ concentrations, leading to an increase in the optimal temperature of P_c. Figure 1b shows the calculated CO₂ dependence of the optimal temperature maximizing P_c. 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 C_i potentially affects the temperature dependence of photosynthesis. The optimal temperature is low if C_i decreases with increasing leaf temperature. Some studies showed that C_i 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 C_i to C_a (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 C_i.

Effects of growth temperature on C_i are different among species; in some studies C_i 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 C_i when they were grown at low temperature, but four species did not show such tendencies. A large difference in C_i 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, V_c max determined at a leaf-level (‘apparent’ V_c 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, E_aV, is a measure of temperature dependence of P_c. E_aV has been reported to increase with growth temperature (Fig. 2a; Hikosaka et al., 1999; Yamori et al., 2005). Figure 3a shows the relationship between E_aV and growth temperature obtained from published and unpublished data. There was a large variation in E_aV among species, but in each species, E_aV 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 E_aV increases, the optimal temperature of P_c at ambient CO₂ increases with temperature (Fig. 2b). Figure 3b shows the calculated optimal temperature for P_c as a function of E_aV. The optimal temperature increases by 0.54 °C per 1 kJ mol⁻¹E_aV (of course, the optimal temperature is not a simple function of E_aV if the deactivation is substantial). In this survey, the relationship between E_aV and growth temperature implies that with a 10 °C increase in growth temperature the E_aV 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 E_aV. The first one is the internal CO₂ conductance. As mentioned above, C_i is not the same as CO₂ concentration at the carboxylation site (C_c). The C_c to C_i ratio may vary among leaves (Terashima et al., 2005). If the C_c to C_i ratio is low, the optimal temperature for P_c decreases and the E_aV 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 C_i was low in leaves grown at low temperature. As Rubisco was not inactivated, they argued that C_c was lower in leaves grown at lower temperature. However, in Nerium oleander, a simultaneous measurement of gas exchange and chlorophyll fluorescence suggested that C_c 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 C_c.

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 P_c 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 E_aV. 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 (K_c, K_o, Γ*) 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 Γ* 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

J_max at a leaf level (‘apparent’ J_max) 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 J_max occurs at high temperature (Fig. 4a; Harley and Tenhunen, 1991; Leuning, 2002; Medlyn et al., 2002b). The reduction of J_max at high temperature affects the temperature dependence of P_r (Fig. 4b).

A shift in the optimal temperature for apparent J_max 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 H_a of the apparent J_max 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 J_max. 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 J_max in several studies. For example, in pea (Pisum sativum) leaves, E_a 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 P_r 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 P_r 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 J_max.

The balance between carboxylation and regeneration of RuBP

Temperature dependences of P_c and P_r 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, P_c is less temperature-dependent and has a lower optimal temperature than P_r (Figs 2b, 4b). When plants increase P_r relative to P_c (i.e. higher J_max to V_c 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 J_max and V_c 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 J_max to V_c 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 J_max to V_c 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 J_max to V_c max ratio: eight annual species (Bunce, 2000), Pinus pinaster (Medlyn et al., 2002a), Nerium oleander (Hikosaka and Hirose, 2001), fa*gus crenata (Onoda et al., 2005b), and Quercus crispula (K Hikosaka, unpublished data). Why do some species alter the J_max to V_c max ratio while others do not? If the temperature dependence of P_c and P_r are similar to each other, a change in the J_max to V_c max ratio does not alter the temperature dependence of photosynthesis (Hikosaka, 1997). Whether or not P_c and P_r have a similar temperature dependence may be ascribed to the temperature response of V_c max and J_max (Onoda et al., 2005b). Plants with a relatively low activation energy of J_max (H_aJ) have a temperature response of P_r similar to that of P_c. Onoda et al. (2005b) found that fa*gus crenata with a relatively low H_aJ did not alter the J_max to V_c max ratio depending on growth temperature, while Polygonum cuspidatum with a relatively high H_aJ altered the ratio.

Which limits photosynthesis, P_c or P_r?

At a normal CO₂ concentration (c. 370 μmol mol⁻¹), P_c and P_r are close to each other, but generally P_r is slightly higher than P_c (i.e. photosynthesis is limited by RuBP carboxylation) (Fig. 7a). In particular, photosynthesis at the optimal temperature is limited by P_c, irrespective of growth temperature (Figs 6, 7a; Hikosaka et al., 1999). Therefore the changes in temperature dependence of photosynthesis may be explained mainly by V_c max. An increase in the optimal temperature of photosynthesis is ascribed to the increase in E_aV. RuBP regeneration is not substantial and may be responsible only when P_r is lower than P_c, 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 J_max and the J_max to V_c 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 J_max to V_c 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 J_max to V_c 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 J_max to V_c 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. P_c=P_r). In Quercus myrsinaefolia (Hikosaka et al., 1999) and Plantago asiatica (Hikosaka, 2005), the P_r to P_c 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 P_r to P_c 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, E_aV increased with increasing growth temperature. Other factors, C_i, temperature dependence of J_max, and J_max to V_c max ratio, were also reported to change with growth temperature, but there are interspecific differences in their responses. Among these factors, E_aV 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 E_aV. However, other factors may have substantial roles in temperature acclimation. Change in the J_max to V_c 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. J_max 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.

†

Present address: Department of Plant Ecology, Utrecht University, PO Box 80084, 3508 TB Utrecht, The Netherlands.

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.

References

© The Author [2005]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved. For Permissions, please e-mail: journals.permissions@oxfordjournals.org

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