Thermal acclimation of foliar respiration and photosynthesis is critical for projection of changes in carbon exchange of terrestrial ecosystems under global warming.
A field manipulative experiment was conducted to elevate foliar temperature (Tleaf) by 2.07°C in a temperate steppe in northern China. Rd/Tleaf curves (responses of dark respiration to Tleaf), An/Tleaf curves (responses of light-saturated net CO2 assimilation rates to Tleaf), responses of biochemical limitations and diffusion limitations in gross CO2 assimilation rates (Ag) to Tleaf, and foliar nitrogen (N) concentration in Stipa krylovii Roshev. were measured in 2010 (a dry year) and 2011 (a wet year). Significant thermal acclimation of Rd to 6-year experimental warming was found. However, An had a limited ability to acclimate to a warmer climate regime. Thermal acclimation of Rd was associated with not only the direct effects of warming, but also the changes in foliar N concentration induced by warming.
Warming decreased the temperature sensitivity (Q10) of the response of Rd/Ag ratio to Tleaf. Our findings may have important implications for improving ecosystem models in simulating carbon cycles and advancing understanding on the interactions between climate change and ecosystem functions.
Citation: Chi Y, Xu M, Shen R, Yang Q, Huang B, Wan S (2013) Acclimation of Foliar Respiration and Photosynthesis in Response to Experimental Warming in a Temperate Steppe in Northern China. PLoS ONE 8(2): e56482. https://doi.org/10.1371/journal.pone.0056482
Editor: Gil Bohrer, The Ohio State University, United States of America
Received: July 26, 2012; Accepted: January 14, 2013; Published: February 15, 2013
Copyright: © 2013 Chi et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: Financial support came from the National Key Research and Development Program of China (2010CB833500, http://www.973.gov.cn), the 100 Talents Program of the Chinese Academy of Sciences supported M. Xu’s work (http://www.cas.cn) and National Natural Science Foundation (30925009, http://www.nsfc.gov.cn). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
The balance between respiration and photosynthesis is critical to the exchange of carbon between the atmosphere and the terrestrial biosphere –. Instantaneous increases in foliar temperature (Tleaf) typically result in an increase in respiration/photosynthesis (R/A) ratio because the response of respiration to Tleaf normally follows an approximate exponential-type curve (at moderate temperatures) while the response of photosynthesis to Tleaf often bears a bell-shaped curve [i.e. the thermal optimum (Topt) of respiration is higher than that of photosynthesis] , . In contrast, long-term warming experiments have suggested that R/A ratio is often conservative to changes in growth temperature (Tgrowth) through acclimation, the metabolic adjustment for compensating changes in Tgrowth –. Acclimation could occur via suppression of respiration in response to changes in foliar carbohydrate supplies , . The thermal acclimation of respiration and photosynthesis is associated with multitudes of signal cascades and networks, which involves the reallocation of resources to achieve and maintain not only optimal R/A ratio but also protective strategies under sustained warming as projected by global climate models –. However, the mechanisms of thermal acclimation of respiration and photosynthesis to climate warming are far from clear, especially in natural ecosystems.
The acclimation of foliar respiration to warmer Tgrowth has been found in numerous studies , –, which may also be associated with plant developmental stage and other abiotic factors, such as drought and nutrient availability –. Thermal acclimation of respiration might occur via changes in the temperature sensitivity, Q10, or the basal respiration, R10 (respiration at a reference temperature, such as 10°C) . Altered Q10 partially reflects temperature-mediated changes in energy demand and/or available substrates , ,  whereas changes in R10 may be associated with temperature-mediated changes in respiratory capacity, reflecting changes in mitochondrial abundance, structure and/or protein composition –. As a result, thermal acclimation of respiration may enhance plant net carbon assimilation by reducing carbon loss under warmer Tgrowth while maintaining basal rates of respiration in colder Tgrowth for subsequent recovery , , , .
The thermal acclimation of the foliar net CO2 assimilation rate (An) may involve three primary sets of processes that control the An/Tleaf curves (response of An versus Tleaf), namely respiratory, biochemical and stomatal processes . First, An is the difference between gross CO2 assimilation rate (Ag) and foliar dark respiration (Rd), An = Ag – Rd, which requires the decoupling of the two processes because Ag and Rd feature different thermal dynamic properties and thus involve different thermal acclimation processes . This could result in a shift in Topt and a change in the shape of the An/Tleaf curve. Therefore, Rd must be evaluated separately and factored out to understand the acclimation mechanisms of Ag in response to global warming , , . Second, the acclimation of Ag to warmer Tgrowth deals with the changes in Rubisco activity – and electronic transport processes  where Tgrowth affects the thermal dependence of various enzymes in the dark and light reactions , . Therefore, the temperature sensitivity of the maximum rate of Rubisco carboxylation (Vcmax) and the maximum rate of photosynthetic electron transport (Jmax) are associated with the acclimation of Ag , . In addition, the change in the balance between carboxylation and regeneration of RuBP, indicated by Jmax/Vcmax ratio, may also result in the shift of Topt of Ag due to nitrogen (N) partitioning in the photosynthetic apparatus , , , . Finally, the temperature-dependent diffusion processes of CO2 to chloroplasts, such as stomatal conductance (gs) and mesophyll conductance (gm), can also affect the thermal acclimation of photosynthesis , . Kirschbaum and Farquhar  showed that higher conductance could cause an increase of CO2 concentrations in the carboxylation site (Cc) and then resulted in a shift in limitation of Ag from Rubisco to electron transport capacity. Since Topt of electron transport-limited Ag is higher than that of Rubisco-limited Ag, Topt of Ag was increased (0.05°C per 1 µmol mol−1 CO2) .
Stipa krylovii Roshev. is a keystone species in the temperate steppe in northern China , . Climate models predict this region will be 4°C warmer by 2100, which may have severe impacts on Stipa krylovii Roshev. . Examining the respiration and photosynthesis of this species is critical to the steppe productivity and the carbon cycle of the ecosystem. The objectives of the current study are to examine: (1) the acclimation capacity of respiration and photosynthesis to experimental warming under field conditions, and (2) the homeostasis of respiration/photosynthesis ratio in response to experimental warming in the steppe ecosystem.
Materials and Methods
The research site (42°02′ N, 116°17′ E, 1324 m a.s.l.) is a typical temperate steppe located in Duolun County, Inner Mongolia Autonomous Region, China. The experiment has received the permits for the field study from the land owner, Institution of Botany, Chinese Academy of Sciences. The mean annual temperature (MAT) is 2.1°C, with monthly mean temperature ranging from −17.5°C in January to 18.9°C in July. The mean annual precipitation (MAP) is approximately 385 mm with approximately 85% falling from May to September. The soils are chestnut (Chinese classification system) or Haplic Calcisols (FAO classification system), with 62.8% sand, 20.3% silt, and 17.0% clay respectively. The soils are characterized as sandy, slightly alkaline and nutrient poor with pH values around 7.7 and bulk density of 1.3 g cm−3 and soil total organic C and N concentrations of 16.1 and 1.5 g kg−1 respectively. The plant communities in the temperate steppe are dominated by Stipa krylovii Roshev., Artemisia frigid Willd., Potentilla acaulis L., Cleistogenes squarrosa (Trin.) Keng., Allium bidentatum Fisch. ex Prokh., and Agropyroncristatum (L.) Gaertn.
The warming experiment was initiated in April 2006 with infrared heaters (MSR-2420, Kalglo Electronics Inc., USA; radiation output is approximately 1600 W) as the heating source (Fig. 1). Briefly, an infrared heater of 1.65 m in length was suspended at 2.25 m above the ground in each warming plot which features a dimension of 3×4 m. A reflector associated with the heater can be adjusted so as to generate an evenly distributed radiant input to the plant canopy. In the control plots, a ‘dummy’ heater with the same shape and size was suspended at the same height to simulate shading effects of the infrared radiator. The effects of warming on Tleaf were measured using a portable infrared thermometer (FLUKE 574, Fluke Inc., USA). The mean daytime Tleaf in the warming plots was increased by 2.07°C compared to the control plots. The warming experiment was designed for long-term simulation of global change and it featured a complete random block design with multiple treatments (day warming, night warming, diel warming, and N addition) and six replicates. We took advantage of this multi-factor experiment by selecting the diel warming and control plots with all the other factors kept at control levels. The details of the experiment can be found in Wan et al.  and Xia et al. .
Gas Exchange Measurements
We measured foliar gas exchange using a portable photosynthesis system (LI-6400, LI-COR Inc., USA) in the middle of the growing seasons (late July to early August) in 2010 and 2011 (Fig. 2) to remove the effect of seasonal changes in photosynthetic and respiratory acclimation in Stipa krylovii Roshev. . Four individuals (one individual per plot) were measured in each treatment. Eight days were required to complete all field measurements each year. Light, Tleaf, humidity, and CO2 concentration were independently controlled in a 2×3 cm cuvette. Given the Tleaf control capacity is limited (within ±6°C) with the factory setup of the LI-6400 system, we modified the Tleaf control system by adding metal blocks with water channels to heat or cool the peltiers, thermoelectric cooling elements. The water channels were connected to a heating/cooling water bath whose temperature was controlled by adding hot water or ice. This modification allows holding Tleaf at any level between 10 and 40°C during the summer growing season in the steppe.
The filled rectangles on the top of figure indicate the growing season (May to October) and the open rectangles for the non-growing season (November to April). The arrows mark the timing of field campaigns when the gas exchange measurements were initiated.
The photosynthetically active photon flux density (PPFD) was provided by the red/blue LED light source built in the foliar cuvette calibrated against an internal photodiode (LI-6400-02B, LI-COR Inc.). The vapor pressure deficit (VPD) in the foliar cuvette was controlled by passing the air entering the cuvette through either anhydrous calcium sulfate for the lower Tleaf when humidity was high or bubbling air via water at higher Tleaf when the air was dry. CO2 concentrations in the cuvette were controlled using an injector system (LI-6400-01, LI-COR Inc.) which functions with a CO2 mixer and compressed CO2 cartridges. Cuvette was sealed with plasticine to prevent leakage. Potential leakage of CO2 out and into the empty cuvette was determined for each concentration and used to correct the measured foliar fluxes with the equations provided by von Caemmerer and Farquhar  and Galmés et al. . The gas exchange system was zeroed using H2O and CO2 free air every day.
Typical An/Ci curves (An versus calculated intercellular CO2 concentrations, Ci) were measured at Tleaf changing from 10 to 40°C with 5°C increments each. We started with the An/Ci curves at low Tleaf (10°C) in the morning around 7∶00 am finished at high Tleaf around noon. As to the problem of co-variance between the daily cycle and temperature, Luo et al.  and Way and Sage  suggested that the observed responses in the biochemical parameters resulted mainly from changes in temperature rather than changes in time of day. It usually took c. 5 min for Tleaf to reach stability at each step change in temperature. Photosynthesis was induced for 10 min in saturating PPFD (1500 µmol photons m−2 s−1) and at ambient CO2 concentration (Ca) of 380 ppmv. Measurements were made at saturating light (1500 µmol photons m−2 s−1), and a leaf VPD between 0.5 and 2.0 kPa, except for 40°C where the VPD was 4.5±0.05 kPa. An was measured at cuvette CO2 partial pressures between 50 and 1200 ppmv CO2. The Ca was lowered stepwise from 380 to 50 ppmv and then increased again from 380 to 1200 ppmv with the total of 9 points. In total, 112 An/Ci curves were measured and used for the analysis of physiological parameters in this study. An/Tleaf curves (response of light-saturated An at 380 ppmv versus Tleaf) were obtained based on the An/Ci curves measured from 10 to 40°C.
Rd was measured by turning off the LED light source for at least 5 minutes in the cuvette after each An/Ci curve was accomplished . All other conditions were the same as An/Ci curve measurements. Measurements of Rd on previously illuminated leaves were performed after a period of darkness in order to avoid light-enhanced dark respiration (LEDR) , . Five data points of Rd were logged at a 30 s interval and averaged for Rd at a given Tleaf. Ag was calculated by adding Rd to An at each Tleaf.
Estimation of Vcmax, Jmax, TPU and gm
An/Cc curves (An versus chloroplastic CO2 concentration) were fitted to estimate Vcmax, Jmax, TPU (triose-phosphate utilization) and gm. The spreadsheet-based software of Sharkey et al.  was modified (Appendix S1) to fit the An/Cc curve by fixing the Rd value which was measured following the An/Ci curve. This modification will improve the model performance by reducing the number of estimated parameters and thus decreasing the degree of freedom in fitting the model. As in the original software the optimum of Vcmax, Jmax, TPU and gm was obtained by minimizing the root mean square error (RMSE) of each curve , .
Estimation of Dependence of Reaction Rates on Temperature
The responses of Rd and Vcmax to Tleaf were fitted to a non-peaked model, following Harley et al. , due to the fact that the deactivation of Rd and Vcmax was not observed in our study:(1)where c is a scaling constant, ΔHa is the activation energy, R is the molar gas constant (0.008314 kJ K−1 mol−1) and Tk is the absolute Tleaf (K) . Q10 of Rd and Vcmax were modeled using the following general function:(2)where ref10 is the estimated basal rate at the reference temperature of 10°C, and Tleaf is the leaf temperature (°C). The responses of An, Ag and Jmax to Tleaf were fitted using a peak model in view that the deactivation at high Tleaf was substantial:(3)where ΔHd is a term for deactivation and ΔS is an entropy term , . The second derivative of Eqn 3 shows that Topt can be calculated  as follows if the parameter includes a peak:(4)
Estimation of Biochemical Limitations to Photosynthesis
Temperature dependence of Ag limited by RuBP carboxylation (Ac), RuBP regeneration (Aj) and TPU (Ap) were reconstructed as follows:(5)(6)(7)where Vcmax, Jmax and TPU were derived from fitted kinetic parameters (c, ΔHa, ΔHd and ΔS) in our study, Kc, Ko and ? ? were derived from a general set of kinetic parameters in Sharkey et al. . Cc was set at 250.8 ppmv in view that the mean Cc/Ca ratio was 0.66 at ambient CO2 concentration (380 ppmv) for all the An/Ci curves measured in the current study, O was the partial pressure of oxygen at Rubisco.
Foliar N concentration on an area basis was determined using the foliage covered in the cuvette during the gas exchange measurements. The foliage samples were first used to measure the leaf area with an area meter (Li-3100, Li-Cor Inc.) and then biomass where the samples were dried at 65°C for 48 h. Then the dry samples were ground to powder for measuring the total C and N concentrations with a CN analyzer (NA Series 2, CE Inc., Germany).
The raw data from the gas exchange measurements were cleaned and processed in Excel spreadsheets where the non-linear An/Cc curve fitting was performed as in Sharkey et al. . The fitting was improved by fixing Rd with the measured value (Appendix S1). Further statistical analyses were conducted using SPSS (version 17.0, SPSS Inc., USA). One-way ANOVA was used to analyze the effects of warming on (1) the foliar chemical properties (C, N, and C/N ratio) and (2) the thermal dynamic properties (c, ΔHa, ΔHd, ΔS, Q10, Topt and ref10) of foliar gas exchange (An, Rd and Ag) and photosynthetic metabolism (Vcmax and Jmax ). Differences were considered statistically significant at P<0.05. Linear regression was employed to examine relationships between foliar properties and climate (i.e. Tgrowth). Tgrowth in the control plots was an average for daytime Tair during the 5 d prior to gas exchange measurements in each plot. This choice was based on: (1) our observation that the bulk of individual foliar development by Stipa krylovii Roshev. species typically required 4–6 d; and (2) published results indicating that adjustments of foliar metabolism to climate change can occur rapidly (e.g. in a span of 1–5 d following a shift in Tgrowth , , –); (3) Gunderson et al.  found that Topt for photosynthesis was strongly correlated with mean daytime Tair. In addition, Tgrowth in the warming plots were approximatively calculated by adding warming effects (2.07°C) to the mean daytime Tair during the 5 d prior to gas exchange measurements in each plot.
Microclimate and Experimental Warming
The meteorological data collected at the experimental site showed that the growing season of 2010 was dry while the growing season of 2011 was wet (Fig. 2). The daily mean Tair between 1 May, the onset of plant growth, and the time of the field measurements (27 July in 2010 and 2011) was 17.2°C in 2010 and 15.6°C in 2011 with the long-term average (1953–2011) of 15.5°C during the same period. Meanwhile, the precipitation during the same period was only 115 mm in 2010 and 183 mm in 2011 with the long-term average of 177 mm. The growing season precipitation in 2010 was only about 65% of that in a normal year, confirming 2010 was a dry year (Fig. 2).
The experimental warming significantly increased daytime Tleaf by 2.07°C (P<0.001), on average (Fig. 3). Warming increased daytime Tgrowth in the warming plots reaching 28.59 and 23.14°C in 2010 and 2011, respectively. Meanwhile, the daytime Tgrowth in the control plots was only 25.72 and 21.31°C in 2010 and 2011, respectively. The details of the warming effects on microclimate at the study site can be found in Wan et al.  and Xia et al. .
Warming significantly decreased respiratory temperature sensitivity, Q10, in both years (both P<0.05) (Fig. 4, Table 1). Q10 of Rd on a foliar area basis decreased from 1.83 in the control plots to 1.66 in the warming plots in 2010 (P = 0.049) (Table 2) and from 2.19 to 1.81 in 2011 (P = 0.042) (Table 3). Meanwhile, Q10 of Rd on a foliar N basis marginally decreased from 1.81 to 1.66 in 2010 (P = 0.094) and significantly decreased from 2.25 to 1.76 in 2011 (P = 0.011) (Table 2, 3). Warming marginally reduced base respiration rate at 10°C (R10) on a foliar area basis from 1.70 to 1.35 µmol m−2 s−1 in 2010 (P = 0.090) but increased that from 0.58 to 0.92 µmol m−2 s−1 in 2011 (P = 0.050) (Table 2, 3). Warming effects on the R10 on a foliar N basis were similar to the area-based Rd (Fig. 4).
The filled circles indicate the warming plots and the open circles for the control plots. (A) to (F) foliar area based: (A) and (B) net CO2 assimilation (An); (C) and (D) dark respiration (Rd); (E) and (F) gross CO2 assimilation (Ag); (G) to (L) foliar nitrogen based: (G) and (H) An ; (I) and (J) Rd; (K) and (L) Ag. Each data point is the average of 4 replicates.
The An/Tleaf curves were typically bell-shaped in both warming and control plots (Fig. 4). Warming had little effect on Topt of An in both years (both P>0.05) (Table 1). Topt of An on a foliar area basis was 22.49 and 23.99°C for the control and the warming plots respectively in 2010, and 24.89 and 26.48°C respectively in 2011 (Fig. 4). Topt of Ag on a foliar area basis was 22.53 and 24.30°C for the control and the warming plots respectively in 2010 (P = 0.328), and 25.65 and 27.34°C respectively in 2011 (P = 0.637) (Fig. 4). Warming also had little effects on Topt of An and Ag on a foliar N basis in either 2010 or 2011 (all P>0.05) (Table 1).
Biochemical Limitations to Photosynthesis
The effects of warming on Q10 of Vcmax were not statistically significant between the warming and the control plots in both years (both P>0.05) (Table 1), but we found a general decreasing trend from the control to warming plots (Fig. 5). Q10 of Vcmax on a foliar area basis was 1.91 and 1.74 for the control and the warming plots respectively in 2010 (P = 0.062), and 1.87 and 1.83 respectively in 2011 (P = 0.779) (Fig. 5, Table 2, 3). Q10 of Vcmax on a foliar N basis was 1.87 and 1.72 for the control and the warming plots respectively in 2010 (P = 0.174), and 1.90 and 1.78 respectively in 2011 (P = 0.668) (Fig. 5, Table 2, 3). The warming effects on Q10 of Jmax were not be detected in 2010 or 2011 (both P>0.05) (Table 1). In addition, the warming effects on the slope and y-intercept of the temperature-response curves for Jmax/Vcmax ratio were not statistically significant (all P>0.05), though the ratio decreased linearly with the Tleaf (Fig. 5).
The filled circles indicate the warming plots and the open circles for the control plots. (A) and (B) area-based Vcmax; (C) and (D) area-based Jmax; (E) and (F) N-based Vcmax; (G) and (H) N-based Jmax; (I) and (J) the Jmax/Vcmax ratio. Each data point is the average of 4 replicates.
Diffusion Limitations to Photosynthesis
In 2010, a dry year, gs in the warming plots was marginally greater than that in the control plots (P = 0.137), and Topt for gs was about 17.42°C in the warming plots and less than 10°C in the control plots (Fig. 6). The gm in the warming plots was significantly greater than that in the control plots (P<0.001), and Topt for gm appeared at 37.09°C in the warming plots and 27.86°C in the control plots (Fig. 6). Cc in the warming plots was approximately 35 ppmv greater than that in the control plots (P<0.001), but Cc was independent of Tleaf in both the warming and the control plots (both P>0.05) (Fig. 6). Similarly, Cc/Ca ratio was constant and independent of Tleaf in the warming and the control plots (both P>0.05) (Fig. 6). However, experimental warming significantly increased Cc/Ca ratio in 2010 (P = 0.001) with an average value of 0.70 in the warming plots and 0.61 in the control plots (Fig. 6).
The filled circles indicate the warming plots and the open circles for the control plots. Each data point is the average of 4 replicates. Note: gm is constrained to be 30 (µmol m−2 s−1 Pa−1) or less.
In 2011, a wet year, Warming had little effect on gs and gm (both P>0.05), which resulted in no difference in Cc between the warming and the control plots (P = 0.860) (Fig. 6). Experimental warming also had little effect on Cc/Ca ratio in 2011 (P = 0.447) with an average value of 0.67 in the warming plots and 0.65 in the control plots (Fig. 6).
Warming marginally decreased foliar N concentration in 2010 (P = 0.063), but significantly increased that in 2011 (P = 0.002) (Table 4). Warming had little effect on foliar carbon concentration in both years (both P>0.05). Foliar C/N ratio was significantly higher in the warming plots than in the control plots in 2010 (P<0.001) and the opposite was true in 2011 (Table 4).
Acclimation of Respiration
Rd was sensitive to Tleaf with the Rd/Tleaf relationship following a typical exponential curve, but warming reduced the magnitude (Fig. 4, Table S1). Our results are consistent with previous studies , ,  that the temperature sensitivity of Rd is negatively related to the Tgrowth (Fig. 7). According to the respiratory acclimation mechanisms proposed by Atkin and Tjoelker , the temperature-mediated change in Q10 is determined by the maximum enzyme activity and/or substrate availability , , . Earlier results from the same warming experiment confirmed that day warming significantly reduced foliar starch concentrations (–6.1%, P = 0.009), suggesting the reduction in Q10 in the current study might be attributed to the lower substrate concentrations.
Foliar N concentrations induced by experimental warming in our study may also affect the temperature sensitivity of Rd, Q10 (Fig. 7). To date, few studies have examined the role of N in the change in Q10. Turnbull et al.  found that Q10 of Rd for the trees in a temperate rainforest increased with increasing N availability along a soil chronosequence in New Zealand. However, Ow et al.  have reported that N had little or no impact on Q10 of Rd when saplings grown at high and low N availabilities were transferred to a different Tgrowth regime. Here, we found a negative correlation between Q10 of Rd and foliar N concentrations (Fig. 7). The detailed mechanisms are not clear, but the confounding effect of foliar N concentrations with other factors, such as temperature and precipitation, may have played an important role in the “apparent” Q10 , , .
In the current study we found that experimental warming marginally reduced base respiration rate at 10°C (R10) in 2010 but increased that in 2011 (Table 2, 3). This could have been attributed to the differential responses of foliar N concentration to warming in the two hydrologically contrasting growing seasons. Warming marginally decreased foliar N concentration in the dry growing season (2010), but increased that in the wet growing season (2011) (Table 4). A growing number of studies , , , including our current study, have found that foliar N concentration was strongly related to R10 (Fig. 7). Therefore, we believed that foliar N concentration played an important role in the diverging responses of R10 to warming in both years.
Acclimation of Photosynthesis
Photosynthesis has long been known to acclimate to prevailing Tgrowth by shifting the Topt . For example, Gunderson et al.  have reported that a 3-year warming of 2–4°C has resulted in a higher Topt of An for five species of deciduous trees. In the current study we found that a 6-year warming of 2.07°C did not resulted in changes in Topt of An (Fig. 4, Table S1). We also found that there were not statistically significant differences between the shift in Topt of An and Ag in 2010 (P = 0.896) or 2011 (P = 0.984). This suggests that the instantaneous response of photosynthesis was independent of changes in Rd.
It has been proposed that the increase in the temperature sensitivity of Vcmax, indicated by ΔHa of Vcmax, contributed to the thermal acclimation of photosynthesis to experimental warming , , . However, in the current study we found that warming slightly decreased ΔHa of Vcmax (Fig. 5, Table 1). Biochemically, the change in ΔHa of Vcmax is closely related to the temperature dependence of Rubisco activity , Rubisco activation status , , dimorphism of Rubisco , and the amount of Rubisco . The lower ΔHa of Vcmax obtained from the warming plots indicated that warming slightly decreased the temperature sensitivity of those processes.
Previous studies found that RuBP regeneration processes may play an important role in the thermal acclimation of photosynthesis , , . The increase in the thermal stability of photosystem II, indicated by ΔHa of Jmax, has been shown to be related to the thermal acclimation of Ag to warming –, . However, in the current study we found only minor response of ΔHa of Jmax to warming (Fig. 5, Table 1). This is also confirmed by our results that the RuBP regeneration seldom limited Ag (Fig. 8).
The top panels indicate the control plots and the lower panels for the warming plots. Cc was set at 250.8 ppmv considering that the mean Cc/Ca ratio was 0.66 at ambient CO2 concentration (380 ppmv) for all the An/Ci curves measured. The response of Ag is delineated by the minimum value of either Rubisco-limited (solid curve), ribulose bisphosphate (RuBP) regeneration-limited (dashed curve) and Pi regeneration-limited (dotted curve). Circle indicates co-limited point, moving from the Rubisco-limited state to RuBP regeneration-limited state.
A number of studies have reported that the balance between the carboxylation and the regeneration of RuBP, indicated by Jmax/Vcmax ratio, can also affect the thermal acclimation of photosynthesis , . In our study, the experimental warming had little effect on the linear trend of Jmax/Vcmax ratio to Tleaf (Fig. 5). Nevertheless, in this study we found that Jmax/Vcmax ratio declined sharply and linearly with the instantaneous increase in Tleaf (Fig. 5). Many ecosystem models, such as Biome-BGC , have set Jmax/Vcmax ratio as a constant (2.1) which is independent of Tleaf. Wullschleger  analyzed 164 An/Ci curves for 109 C3 plant species which were measured under Tleaf ranging from 13 to 35°C and found the average Jmax/Vcmax ratio was 2.1. Others found that Jmax/Vcmax ratio was not a constant instead varying with Tleaf through a linear , – or nonlinear relationship . Our current results show that the relationship (between Jmax and Vcmax) itself is highly temperature dependent, suggesting that photosynthesis models have to consider the temperature dependence of Jmax/Vcmax ratio.
In addition to biochemical limitations, the thermal acclimation of photosynthesis may also relate to CO2 diffusion processes in leaves and chloroplasts, such as gs and gm, because changes in Tgrowth may affect CO2 diffusivity, solubility, membrane permeability and stomatal movement –. Previous studies have found that increasing gs and/or gm can cause the increase of Topt of An , , , , . In the current study we found that warming increased gm (Fig. 6) in 2010 which might contribute to the modest variation in Topt of Ag in 2010. However, we found smaller increases in gs and gm (Fig. 6) in 2011, which may explain the weaker acclimation in 2011 (Fig. 4). The differential responses of CO2 diffusion process to warming in the two hydrologically contrasting growing seasons could have been attributed to changes in soil moisture and N availability induced by warming . It is noted that, so far, no consistent conclusions have been achieved on the warming effect on gs and gm. Some researchers found that warming increased gs , – and gm , and others found warming decreased gs  and gm , or no effect on gs  and gm . Those various studies suggest that other factors, such as warming-induced water depletion and change in N availability, may have interacting effects on responses of CO2 diffusion process to warming. These results call for multi-factor experiments, such as the combination of warming with water manipulation and fertilization , for understanding the mechanisms of thermal acclimation of photosynthesis under future global change.
Balance between Respiration and Photosynthesis
The acclimation of foliar respiration and photosynthesis is also reflected in R/A ratio which indicates the balance between carbon gain, loss and accumulation , . Our results show that the instantaneous (<5 h) warming at foliage level has non-linearly increased Rd/Ag ratio, indicating proportionally more carbon loss through Rd as Tleaf goes up (Fig. 9). However, the 6-year experimental warming has resulted in thermal acclimation of the grasses as evidenced by the decrease of the curvature of the response curve of Rd/Ag ratio to Tleaf (Fig. 9). It is important to note that though the balance between Rd and Ag was re-established through the thermal acclimation , , , , Rd/Ag ratio was still increasing with Tgrowth in a wet year (Fig. 9). This means that, at foliage level, acclimation can only partially compensate the negative impact from the global warming.
The filled circles indicate the warming plots and the open circles for the control plots. The blue and red circles indicate Rd/Ag ratio at growth temperature (Tgrowth), computed using the thermal dynamic properties (individual ΔHa and c values for each plot) and the Tgrowth.
Results (P-values) of two-way ANOVA on the effects of warming, year, and both interactions on the responses of An (the net CO2 assimilation rate), Rd (dark respiration), Ag (the gross CO2 assimilation rate), Vcmax (the maximum rate of Rubisco carboxylation) and Jmax (the maximum rate of photosynthetic electron transport) expressed per unit foliar area and nitrogen to instantaneous change (10–40°C within a 5 h period) in Tleaf (foliar temperature). c is a scaling constant, ΔHa is the activation energy, ΔHd is a term for deactivation, ΔS is an entropy term, Topt is the thermal optimum, Q10 is the temperature sensitivity and ref10 is the estimated basal rate at the reference temperature of 10°C. Significant values (P<0.05) are shown bold.
User’s guide for the A/Cc curve fitting model with measured respiration, modified based on Sharkey et al.’s  Microsoft Excel spreadsheet-based software to reduce the number of fitting parameters (Rd is fixed in the model), version 1.2 (Last updated 25 July, 2012).
Conceived and designed the experiments: YC MX SW. Performed the experiments: YC RS QY. Analyzed the data: YC MX QY. Contributed reagents/materials/analysis tools: BH SW. Wrote the paper: YC MX RS QY BH SW.
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