Plant and Cell Physiology Advance Access originally published online on February 21, 2008
Plant and Cell Physiology 2008 49(4):583-591; doi:10.1093/pcp/pcn030
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The Role of Electron Transport in Determining the Temperature Dependence of the Photosynthetic Rate in Spinach Leaves Grown at Contrasting Temperatures
1Department of Biology, Graduate School of Science, Osaka University, 1-1 Machikaneyama-cho, Toyonaka, Osaka, 560-0043 Japan
2Department of Biological Sciences, Graduate School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, 113-0033 Japan
3Department of Life Science, University of Hyogo, 3-2-1 Kamigohri, Ako-Gun, Hyogo, 678-1297 Japan
*Corresponding author: E-mail, wataru.yamori{at}anu.edu.au; Fax, +61-2-6125-5075.
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Abstract |
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The temperature response of the uncoupled whole-chain electron transport rate (ETR) in thylakoid membranes differs depending on the growth temperature. However, the steps that limit whole-chain ETR are still unclear and the question of whether the temperature dependence of whole-chain ETR reflects that of the photosynthetic rate remains unresolved. Here, we determined the whole-chain, PSI and PSII ETR in thylakoid membranes isolated from spinach leaves grown at 30°C [high temperature (HT)] and 15°C [low temperature (LT)]. We measured temperature dependencies of the light-saturated photosynthetic rate at 360 µl l–1 CO2 (A360) in HT and LT leaves. Both of the temperature dependences of whole-chain ETR and of A360 were different depending on the growth temperature. Whole-chain ETR was less than the rates of PSI ETR and PSII ETR in the broad temperature range, indicating that the process was limited by diffusion processes between the PSI and PSII. However, at high temperatures, whole-chain ETR appeared to be limited by not only the diffusion processes but also PSII ETR. The C3 photosynthesis model was used to evaluate the limitations of A360 by whole-chain ETR (Pr) and ribulose bisphosphate carboxylation (Pc). In HT leaves, A360 was co-limited by Pc and Pr at low temperatures, whereas at high temperatures, A360 was limited by Pc. On the other hand, in LT leaves, A360 was solely limited by Pc over the entire temperature range. The optimum temperature for A360 was determined by Pc in both HT and LT leaves. Thus, this study showed that, at low temperatures, the limiting step of A360 was different depending on the growth temperature, but was limited by Pc at high temperatures regardless of the growth temperatures.
Keywords: Electron transport — Photosynthesis — RuBP carboxylation — RuBP regeneration — Temperature acclimation — Temperature dependence
Abbreviations: DBMIB, 5-dibromo-3-methyl-6-isopropyl-p-benzoquinone; DCIP, dichloroindophenol; ETR, electron transport rate; FBPase, fructose-1,6-bisphosphatase; HT, high temperature; LT, low temperature; RuBP, ribulose bisphosphate.
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Introduction |
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TopAbstractIntroductionResultsDiscussionMaterials and MethodsFundingAppendixAcknowledgmentsReferences |
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In many plants, the temperature response of photosynthesis depends on the growth temperature (Berry and Björkman 1980
, Yamori et al. 2005). The optimum temperature for photosynthesis increases with increasing growth temperature. According to the C3 photosynthesis model (Farquhar et al. 1980), the photosynthetic rate is limited either by the ribulose bisphosphate (RuBP) carboxylation rate (Pc) at ambient and low CO2, or by the RuBP regeneration rate (Pr) at high CO2. At temperatures below the optimum, photosynthetic rates are often limited by Pr, including the limitation by Pi regeneration (Sharkey 1985, Sage and Sharkey 1987, Labate and Leegood 1988, Cen and Sage 2005, Sage and Kubien 2007). On the other hand, the principal limitation of photosynthesis above the optimum temperature remains unclear. One proposed mechanism is that the photosynthetic rate is limited by Pc due to the heat-induced reductions in the activase activity which regulates the Rubisco activation state (Weis 1981, Kobza and Edwards 1987, Law and Crafts-Brandner 1999, Crafts-Brandner and Salvucci 2000, Salvucci and Crafts-Brandner 2004, Yamori et al. 2006a). Recently, Kurek et al. (2007) generated several mutants of Arabidopsis thaliana which varied in thermostability of Rubisco activase and showed that the principal limitation of photosynthesis at high temperature was Rubisco activation via Rubisco activase. Alternatively, Pr has been proposed as the limiting step (Schrader et al. 2004, Wise et al. 2004, Cen and Sage 2005, Makino and Sage 2007). They suggested that the decrease in Rubisco activation state at high temperatures is a regulated response resulting from other limitations including the electron transport rate (ETR). In all of the studies claiming that the Rubisco activation state limits the photosynthetic rate at high temperatures, however, analysis of Pr has been omitted. Therefore, we need to analyze the limitation of photosynthesis by Pr in plants for which the photosynthetic rate has been reported to be limited by the Rubisco activation state at high temperatures.
Pr is generally thought to be determined by the whole-chain ETR in thylakoid membranes, since Pr is dependent on the supply of ATP and NADPH (von Caemmerer 2000). The CO2-saturated photosynthetic rate at 25°C, which reflects Pr, correlated with the Cyt f content (Price et al. 1995, Price et al. 1998, Ruuska et al. 2000). The temperature response of the ETR in thylakoid membranes depends on the growth temperature, with considerable variation depending on the plant species (Tieszen and Helgager 1968, Armond et al. 1978, Badger et al. 1982, Mitchell and Barber 1986, Mawson et al. 1986, Mawson and Cummins 1989, Yamasaki et al. 2002). The temperature responses of the ETR in thylakoid membranes and the CO2-saturated photosynthetic rate were closely related in Saxifraga cernua (Mawson et al. 1986, Mawson and Cummins 1989) and Triticum aestivum (Yamasaki et al. 2002). These studies indicated that the temperature dependence of the whole-chain ETR was limited by that of the PSII ETR (Mawson and Cummins 1989, Yamasaki et al. 2002). However, it has not been quantitatively evaluated whether the temperature dependence of the photosynthetic rate is limited by that of the ETR.
On the other hand, it has also been reported that the temperature dependence of the CO2-saturated photosynthetic rate was not correlated with that of the ETR in Larrea divaricata (Armond et al. 1978, Mooney et al. 1978) or Nerium oleander (Badger et al. 1982). Therefore, it is possible that Pr may not necessarily be limited by the ETR. Thus, it is still unclear whether the temperature dependence of the ETR limits that of Pr.
Recently, we showed that the temperature dependences of the photosynthetic rate were different between the leaves of spinach grown at 15°C and those grown at 30°C (Yamori et al. 2005), and that the photosynthetic rate was limited by Pc across a broad temperature range, irrespective of the growth temperature (Yamori et al. 2006a, Yamori et al. 2006b). We showed that Pc was partly determined by the Rubisco activation state at high temperatures (Yamori et al. 2006a). The use of spinach grown at 15 and 30°C should therefore enable us to clarify the limiting step in photosynthesis across a range of temperatures, thereby revealing the comprehensive mechanisms of temperature acclimation of photosynthesis.
In the present study, we measured CO2 response curves of photosynthesis at saturating light intensity in spinach grown at 15°C [low temperature (LT)] and 30°C [high temperature (HT)], and determined the temperature response of the ETR (whole-chain and PSI and PSII partial reactions) in isolated thylakoid membranes. We compared the maximum ETRs measured in thylakoid membranes with those estimated from the CO2-saturated photosynthetic rates in HT and LT leaves. We quantitatively evaluated whether the photosynthetic rate measured at 360 µl l–1 CO2 was limited by the ETR in HT and LT leaves. The aims were to determine: (i) whether the temperature dependence of the whole-chain ETR differed depending on the growth temperature; (ii) what limited the temperature dependence of the whole-chain ETR; (iii) whether the temperature dependence of Pr was limited by that of the ETR; and (iv) which partial reaction of Pc and Pr limited the temperature dependence of the photosynthetic rate.
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Results |
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Temperature responses of photosynthetic rate
Temperature responses of the light-saturated photosynthetic rate at 360 µl l–1 CO2 (A360), the initial slope of the A–Ci curve (IS) and that of the photosynthetic rate at 1,500 µl l–1 CO2 (A1500) all depended on growth temperature (Fig. 1). The optimum temperatures for A360, IS and A1500 derived from the cubic curves were 30.5, 28.2 and 37.2°C, respectively, in HT leaves. In LT leaves, the optimum temperatures for A360, IS and A1500 were 23.5, 21.6 and 30.0°C, respectively. The dark respiration rate (Rd) of LT leaves was greater than that of HT leaves at any temperatue (data not shown).
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Temperature responses of electron transport rate
Temperature responses of whole-chain, PSI and PSII ETRs in thylakoid membranes isolated from HT and LT leaves (HT and LT thylakoids, respectively) are shown in Fig. 2. The temperature responses of the whole-chain ETR per unit of Chl differed depending on the growth temperature (Fig. 2a). The optimum temperature for the whole-chain ETR was 35 and 30°C in HT and LT thylakoids, respectively (Fig. 2a). At low temperatures, the whole-chain ETR in LT thylakoids was higher than that in HT thylakoids, whereas at high temperatures, the whole-chain ETR in LT thylakoids was lower than that in HT thylakoids. The PSII ETR showed a temperature dependence similar to that of the whole-chain ETR (Fig. 2b), and showed the optimum temperature at 35 and 30°C in HT and LT thylakoids, respectively. On the other hand, the PSI ETR showed steady increases up to 40°C (Fig. 2c). The PSI ETR at low temperatures was higher in LT thylakoids than in HT thylakoids, whereas at high temperatures, it was lower in LT thylakoids than in HT thylakoids.
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ETRs per unit of Chl were converted to a leaf area basis assuming four electrons per oxygen evolution in whole-chain and PSII electron transport, and two electrons per oxygen evolution in PSI electron transport (Fig. 2d, e, f). The whole-chain ETR per unit leaf area was greater in LT thylakoids than in HT thylakoids, except for at 40°C where it abruptly decreased (Fig. 2d). This temperature dependence corresponded to that of the PSII ETR per unit leaf area (Fig. 2e). The PSI ETR per unit leaf area was always greater in LT than in HT thylakoids (Fig. 2f). The whole-chain ETR was less than the PSI and PSII ETRs in both HT and LT thylakoids over the entire temperature range.
Temperature dependence of Jmax
The in vitro ETR per unit leaf area [Jmax (in vitro)] was estimated from the thylakoid whole-chain ETR (Fig. 2d). On the other hand, the in vivo ETR [Jmax (in vivo)] was estimated from A1500, using Equation 7 (see Appendix). At low temperatures, Jmax (in vitro) of HT leaves tended to be less than Jmax (in vivo). At high temperatures, Jmax (in vitro) exceeded Jmax (in vivo) for both HT and LT leaves (Fig. 3). However, the temperature dependences of Jmax (in vitro) were largely similar to that of Jmax (in vivo) in both HT and LT leaves (Fig. 3a, b). The optimum temperatures of 35 and 30°C in HT and LT leaves, respectively, were observed for both Jmax (in vitro) and Jmax (in vivo).
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We analyzed relationships between the temperature dependence of Jmax (in vivo) and that of Jmax (in vitro) in HT and LT leaves (Fig. 3c). We measured the CO2-saturated photosynthetic rate up to 38°C, whereas the ETR in the thylakoid membranes was measured up to 40°C. Therefore, we estimated the ETR at 38°C by fitting cubic curves. Jmax (in vivo) was correlated with Jmax (in vitro) in both HT (R2 = 0.96) and LT leaves (R2 = 0.95), although there were deviations between Jmax (in vivo) and Jmax (in vitro), especially at high temperatures.
Limiting step of A360
We estimated the photosynthetic rate limited by RuBP carboxylation (Pc) and RuBP regeneration rate (Pr) (Fig. 4). As described in the Appendix, Pc was calculated from Equation 2, using IS obtained in this study (Fig. 1b), the Rubisco activation state and Rubisco kinetic parameters (Yamori et al. 2006a), and internal conductance (Yamori et al. 2006b). Pr was calculated from Equation 6, using Jmax (in vitro) and Jmax (in vivo) (Fig. 3). Both Pc and Pr were estimated at the chloroplastic CO2 concentration. Then, we analyzed the limiting steps of the temperature dependence of A360 by Pc and Pr (Fig. 4).
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Pr (in vitro) showed a similar temperature dependence to Pr (in vivo) in both HT and LT leaves, although Pr (in vitro) was slightly greater than Pr (in vivo) at high temperatures (Fig. 4a, b). In HT leaves, both Pc and Pr generally matched with A360 at temperatures below 25–30°C, although Pr was slightly lower than Pc, except for the data at 10°C (Fig. 4a). At temperatures above 25–30°C, A360 reflected Pc rather than Pr. On the other hand, in LT leaves, A360 reflected Pc over the entire temperature range.
The optimum temperatures for A360, Pc, Pr (in vitro) and Pr (in vivo) derived from the cubic curves were 30.5, 30.8, 35.1 and 33.0°C, respectively in HT leaves (Fig. 4a). In LT leaves, the optimum temperatures for A360, Pc, Pr (in vitro) and Pr (in vivo) were 23.5, 25.5, 30.5 and 29.0°C. Growth temperature affected all of the optimum temperatures. For both HT and LT leaves, the optimum temperatures for A360 were very similar to those for Pc.
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Discussion |
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Temperature acclimation of the ETR
The temperature response of the whole-chain ETR in isolated thylakoid membranes depended on the growth temperature (Fig. 2a, d). When plants were grown at LT, the ETR per unit leaf area increased at low temperatures (Fig. 2d–f), as has been reported (e.g. Mitchell and Barber 1986
, Mawson and Cummins 1989, Yamasaki et al. 2002). The whole-chain ETR showed a temperature dependence similar to that of the PSII ETR (Fig. 2), as reported in S. cernua (Mawson and Cummins 1989) and T. aestivum (Yamasaki et al. 2002). However, the whole-chain ETR was much lower than the PSI and PSII ETRs in both HT and LT thylakoids (Fig. 2d–f). This indicates that the whole-chain ETR across a broad temperature range was mainly determined by diffusion processes between the PSI and PSII reaction centers. This result corresponded to those of previous studies which suggested that diffusion processes are one of the crucial factors that regulate the temperature dependence of the ETR (Barber et al. 1984, Mitchel and Barber 1986, Ott et al. 1999, Yamasaki et al. 2002). Plastoquinone and plastocyanin are thought to be the rate-limiting steps of electron transport between PSI and PSII, and are closely associated with the lipid layer of thylakoid membranes. Since the fluidity of the thylakoid membranes increases with increasing temperature, the ETR between PSI and PSII would also increase (Nolan and Smillie 1976, Pike and Berry 1980, Raison and Berry 1979, Quinn and Williams 1985, Wada and Murata 1990, Nishida and Murata 1996). However, the PSII ETR started to decrease at 30–35°C, in proportion to the decrease in the whole-chain ETR (Fig. 2). Therefore, it is thought that, at high temperatures, the whole-chain ETR would be determined by the balance of increases in the ETR in the diffusion processes and decreases in the ETR at PSII.
Limiting step of the RuBP regeneration rate
Jmax (in vivo) was similar to Jmax (in vitro) across a broad temperature range in both HT and LT leaves (Fig. 3). Pr (in vivo) and Pr (in vitro) showed similar temperature dependences, having the same optimum temperatures in HT and LT leaves, respectively (Fig. 4). Therefore, it is fair to say the assumption that the temperature dependence of Pr is determined by that of the whole-chain ETR is robust (Farquhar et al. 1980, Farquhar and von Caemmerer 1982, von Caemmerer 2000).
However, Jmax (in vitro) at low temperatures in HT leaves showed slightly lower values than Jmax (in vivo), whereas at high temperatures, Jmax (in vitro) showed higher values than Jmax (in vivo) in both HT and LT leaves (Fig. 3). In Nerium oleander, stromal fructose-1,6-bisphosphatase (FBPase) activity was suggested to be the limiting step of Pr, because the change in the temperature dependence of the CO2-saturated photosynthetic rate was highly correlated with that in stroma FBPase activity (Badger et al. 1982). By using antisense plants, it has been suggested that Pr would be limited by the capacities of some enzymes, such as FBPase (Koßmann et al. 1994, Muschak et al. 1999, Sahrawy et al. 2004), sedoheptulose 1,7-bisphosphatase (SBPase; Harrison et al. 2001, Ölçer et al. 2001, Lefebvre et al. 2005), glyceraldehyde 3-phosphate dehydrogenase (GAPDH; Price et al. 1995, Ruuska et al. 2000) and phosphoribulokinase (PRKase; Paul et al. 1995, Banks et al. 1999, Paul et al. 2000). Moreover, it is also possible that Pr would be limited by the capacity of ATPase synthase (Farquhar et al. 1980, von Caemmerer 2000). Therefore, the deviations at low and high temperatures would imply that the temperature dependence of Pr could be limited by processes other than the ETR.
Alternatively, it has been reported that alternative pathways, such as the water–water cycle and cyclic electron flow around PSI, are stimulated at low and high temperatures (for a review, see Arnon 1995, Asada 2000, Heber 2002, Öquist and Huner 2003, Sharkey 2005). It is also suggested that the cyclic electron transport would affect the PSII activity, and thus may limit Pr at high temperature (Sharkey 2005, Sage and Kubien 2007). Therefore, the possibility that alternative pathways affect Pr at low and high temperatures cannot be excluded.
Limiting step of the photosynthetic rate
We clearly showed that the temperature response of A360 depends on the growth temperature (Fig. 4). In LT leaves, A360 was solely limited by Pc over the entire temperature range (Fig. 4b). In contrast, in HT leaves, A360 was co-limited by Pc and Pr at low temperatures, whereas at high temperatures, A360 was limited exclusively by Pc (Fig. 4a). It has been reported that, at low temperatures, photosynthetic rates are often limited by Pr, including the Pi regeneration capacity (Sharkey 1985, Sage and Sharkey 1987, Labate and Leegood 1988, Cen and Sage 2005, Sage and Kubien 2007). This study showed that A360 was not necessarily limited by Pr at low temperatures, as this only occurred when plants were grown at high temperatures.
The limiting step of the photosynthetic rate at high temperatures has been debated recently. One proposed mechanism is the limitation of Pc caused by heat-induced deactivation of Rubisco (e.g. Law and Crafts-Brandner 1999, Crafts-Brandner and Salvucci 2000, Salvucci and Crafts-Brandner 2004, Kurek et al. 2007). The other proposed mechanism of decreases in photosynthetic rate at high temperatures is the limitation of Pr (e.g. Schrader et al. 2004, Wise et al. 2004, Cen and Sage 2005, Makino and Sage 2007). This study clearly shows that at high temperatures, A360 was limited by Pc rather than by Pr in both HT and LT leaves. In our previous study (Yamori et al. 2006a), we indicated that the Rubisco activation state decreased as the temperature increased above the optimum temperatures for A360 in HT and LT leaves grown under conditions identical to those of the present experiment. Therefore, in spinach, the decrease in A360 at moderately high temperatures would be partly attributed to the direct decrease in the Rubisco activation state. This is supported by the previous study where the optimum temperature of Rubisco activase in spinach leaves was around 25°C (Salvucci and Crafts-Brandner 2004) and close to the optimum temperature for A360 in the present study.
Conclusion
We conducted a series of experiments to clarify the limiting step of the temperature dependence of the photosynthetic rate and, thus, the comprehensive mechanisms of the temperature acclimation of photosynthesis in spinach leaves (Yamori et al. 2005, Yamori et al. 2006a, Yamori et al. 2006b). The present study showed that the temperature dependence of Pr was mainly determined by that of the ETR (Fig. 3). Our previous studies showed that the temperature dependence of Pc was determined by that of Rubisco kinetics (Yamori et al. 2006a), the Rubisco activation state (Yamori et al. 2006a) and internal conductance from the intercellular airspace to the chloroplast stroma in spinach (Yamori et al. 2006b). Overall, we clearly showed that, in LT leaves, A360 was solely limited by Pc over the entire temperature range, whereas in HT leaves, A360 was limited by Pc at high temperatures and co-limited by Pc and Pr at low temperatures (Fig. 4). The optimum temperature of A360 was determined by the temperature dependence of Pc in both HT and LT leaves. Thus, we clearly showed that the limiting step of A360 was different depending on the growth temperature.
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Materials and Methods |
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Plant growth conditions
Spinach (Spinacia oleracea L. cv. Torai) plants were grown in vermiculite, as described in Yamori et al. (2005
). The day/night lengths were 8 and 16 h. Photosynthetically active photon flux density (PPFD) in the daytime was 230 µmol photons m–2 s–1. The day/night air temperatures were either 30/25 or 15/10°C. These are referred to as the HT and the LT conditions, respectively. Similarly, the leaves grown at HT and LT are called HT and LT leaves.
Gas exchange measurements
The light-saturated photosynthetic rate and the dark respiration rate were measured using the most recently fully expanded leaves (LI-6400; Li-Cor Inc., Lincoln, NE, USA) as described previously (Yamori et al. 2005). The CO2 dependence of the photosynthetic rate was examined, based on measurements at CO2 concentrations in the ambient air (Ca) of 50, 100, 150, 200, 360 and 1,500 µl l–1. At each CO2 concentration, net photosynthetic rate (A) and intercellular CO2 concentration (Ci) were obtained.
Measurements of the electron transport rates in isolated thylakoid membranes
Chloroplasts were prepared according to the method of Terashima et al. (1989) with some modifications. Leaves were homogenized with a blender in a solution containing 0.3 M sorbitol, 40 mM HEPES-KOH (pH 7.0), 10 mM NaCl, 5 mM MgCl2 and 0.1% (w/v) bovine serum albumin (BSA). The homogenate was filtered through a layer of nylon mesh (26 µm) and the filtrate was centrifuged at 2,000 x g at 4°C for 1 min. Then, the chloroplasts were suspended in a solution containing 0.3 M sorbitol, 40 mM HEPES-KOH (pH 7.0), 10 mM NaCl and 5 mM MgCl2. Chl contents were determined by the procedure of Porra et al. (1989).
Immediately before the measurements of the ETR, the chloroplasts were subjected to osmotic shock in a solution containing 40 mM HEPES-KOH (pH 7.5), 10 mM NaCl and 5 mM MgCl2 in the cuvette of an oxygen electrode (Hansatech, King's Lynn, UK). The ETR in the thylakoid membranes (5–10 nmol Chl ml–1) was measured with an oxygen electrode, according to Yamasaki et al. (2002) with some modifications, at saturating light (3,000 µmol m–2 s–1). Saturating light was supplied from a slide projector (AF-250, Cabin, Japan) and passed through an OG 570 long-pass filter (Schott, Mainz, Germany), in order to prevent the quinone from absorbing the light of short wavelengths. For measurements of the whole-chain ETR (H2O
methyl viologen), 10 mM methylamine, 1 mM sodium azide and 1 mM methyl viologen were added to the suspension. For measurements of the PSI ETR [dichloroindophenol (DCIP) and ascorbatemethyl viologen], 10 mM methylamine, 1 mM sodium azide, 1 mM methyl viologen, 10 µM DCMU, 300 µM DCIP and 2 mM sodium ascorbate were added. For measurements of the PSII ETR (H2Ophenyl-p-benzoquinone), 10 mM methylamine, 1 mM phenyl-p-benzoquinone and 1.0 µM 2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone (DBMIB) were added. The PSII ETR at 40°C was much lower than the whole-chain ETR, when 10 mM methylamine, 1 mM phenyl-p-benzoquinone and 1.0 µM DBMIB were used for the assay. Therefore, only at 40°C, we measured the PSII ETRs in the buffer containing 1 mM methylamine, 0.1 mM phenyl-p-benzoquinone and 0.1 µM DBMIB.
Model analysis of the limiting step of the photosynthetic rate
Using the C3 photosynthesis model (Farquhar et al. 1980), the maximum rate of RuBP carboxylation (Vcmax) and the RuBP carboxylation rate (Pc) were estimated from the initial slope of the A vs. Ci curve (IS) obtained with the data measured at a Ca of 50, 100, 150 and 200 µl l–1 (see Appendix). Recently, we showed that the temperature dependence of Pc was limited by the Rubisco activation state and Rubisco kinetic parameters (Yamori et al. 2006a), and by internal conductance (Yamori et al. 2006b) in spinach leaves grown under conditions identical to those of the present study. Therefore, for calculations of Pc, we took account of the temperature dependences of the Rubisco activation state, Rubisco kinetic parameters and internal conductance in HT and LT leaves, respectively.
The Jmax (in vivo) and Pr (in vivo) were estimated from A at the highest Ca of 1,500 µl l–1 CO2 (see Appendix). Jmax (in vitro) and Pr (in vitro) were estimated from the measured whole-chain ETR in the isolated thylakoid membranes (see Appendix). Since the ETR from H2O to methyl viologen was measured as whole-chain electron transport, the maximum ETR was calculated for four electron flow per one oxygen evolution. Moreover, Pr was estimated at the chloroplastic CO2 concentration level as well as Pc, using the internal conductance (Yamori et al. 2006b).
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Funding |
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Japan Society for the Promotion of Science (to W.Y.).
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Appendix |
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A. C3 photosynthesis model
Based on the C3 photosynthesis model (Farquhar et al. 1980
), net leaf photosynthetic rate, A, can be expressed using the minimum rate of two partial reactions:
 | (1) |
):
 | (2) |
* (µl l–1) is the CO2 compensation point in the absence of day respiration, and R* is the Rubisco activation state. Beause the initial slope of the A vs. Cc curve [IS(Cc)] is identical to dPc(Cc)/dCc at Cc = *, Vcmax is expressed as:
 | (3) |
 | (4) |
). Then, using A, Ci and gi, Cc was calculated as:
 | (5) |
 | (6) |
 | (7) |
B. Limiting step of the photosynthetic rate
To analyze the limitation of the temperature dependence of the photosynthetic rate at 360 µl l–1 CO2 under saturating light intensities, we estimated the photosynthetic rate limited by Pc and Pr, respectively. The photosynthetic rate limited by Pc was evaluated according to Yamori et al. (2006a, 2006b). To estimate the temperature dependence of Pc from Equation 2, we assumed that day respiration rates (Rd) were half the dark respiration rates in HT and LT leaves. We first calculated the temperature dependence of Kc(1 + O/Ko) values, using Equation 3. Temperature dependences of the Rubisco activation state (R*), the maximum rate of RuBP carboxylation (Vcmax) and the CO2 compensation point in the absence of day respiration (*) were obtained from spinach leaves grown under conditions identical to those of the present experiment (Yamori et al. 2006a). IS(Cc) was determined from IS(Ci) measured in this study and gi obtained from spinach leaves grown under conditions identical to those of the present experiment (Yamori et al. 2006b), using Equation 4. Cc was determined from the photosynthetic rate at 360 µl l–1 CO2 and Ci measured in this study, and from gi (Yamori et al. 2006b), using Equation 5. The data for the temperature dependences of the parameters were obtained by fitting cubic curves to the actual data. Cc thus estimated at 25°C was 275.9 and 190.0 µl l–1 for HT and LT leaves, respectively.
Next, we calculated absolute values of Vcmax (µmol m–2 s–1) to match the Rubisco contents between the measured photosynthetic rates in this study and the estimated Pc. Vcmax values on a leaf area basis were estimated from Equation 2, at each temperature, using the photosynthetic rates obtained in this study. Then, Vcmax values estimated for each temperature were averaged for the HT and LT leaves, respectively. Vcmax values thus estimated at 25°C were 35.7 and 64.1 µmol m–2 s–1 for HT and LT leaves, respectively.
On the other hand, to estimate temperature dependence of Pr from Equation 6, we used the identical values of Rd, Cc and *, which were obtained in the estimation of Pc, in HT and LT leaves, respectively. The electron transport rate in the isolated thylakoid membranes was used for calculations of Pr (in vitro). Since the electron transport rate from H2O to methyl viologen was measured as whole-chain electron transport, the maximum electron transport rate was calculated for four electron flow per one oxygen evolution. Pr (in vivo) was estimated from estimated from A1500, using Equations 6 and 7.
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We are grateful to Dr. John Evans (Australian National University) for valuable comments on the manuscript.
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Footnotes |
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4Present address: Molecular Plant Physiology Group, Research School of Biological Sciences, Building 46, The Australian National University, Canberra, ACT, 2601 Australia.
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References |
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(Received December 31, 2007; Accepted February 18, 2008)
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