CO₂ elevation improves photosynthetic performance in progressive warming environment in white birch seedlings

Introduction

Global climate warming and increases in atmospheric CO₂ concentration are currently key topics for scientists, politicians and the general public alike¹. Such changes have been observed in the past 150 years and supported by modeling results for the longer term, e.g., warming ocean water, shrinking mountain glaciers, retreating snow cover, and CO₂ concentration dynamics in Arctic/Antarctic ice cores^2–6. It is projected that the global temperatures will increase by an average of 3°C with a range of 2 to 4.5°C under the scenario of doubling atmospheric CO₂ concentration by the end of the century². Global climate warming will likely have profound and diverse impacts on biological systems^2,4–13.

Increases in CO₂ and temperature to a certain extent should have positive impact on photosynthesis and growth, as the current atmospheric CO₂ concentration is below the saturation point for RuBisCO (Ribulose-1,5-bisphosphate carboxylase oxygenase)¹⁴. Furthermore, higher CO₂ concentrations suppress photorespiration and increase the partitioning of photosynthetic electron transport to carboxylation¹⁴. However, the situation will become complicated if the temperature goes beyond plants’ ability to acclimate, or when the rate of temperature increase exceeds the pace of acclimation. In such cases, temperature and CO₂ will have opposite effects on photosynthesis, i.e., the higher temperature induced increase in photorespiration may exceed the beneficial effect of CO₂ elevation, resulting in a decline in net photosynthesis. Consequently, the direction and magnitude of change in net photosynthesis will be determined by the relative magnitudes of the two opposite effects¹⁵. Kirschbaum¹⁶ has conducted a theoretical analysis on the dependence of photosynthesis on temperature and CO₂ concentration for C3 plants and found that at 35°C, photosynthesis at the ambient CO₂ concentration reaches only 50% of the rate at saturating CO₂ concentration, whereas the corresponding value at 5°C is 77%. Therefore, there is greater potential photosynthetic enhancement by CO₂ elevations at higher temperatures. This theory has been supported by the results of a number of studies^15,17–19. Long²⁰ has suggested that the increase in atmospheric CO₂ will not only increase photosynthetic rate, but also alter the photosynthetic response to temperature. Mooney et al.²¹ indicate that the photosynthetic acclimation to elevated temperature and CO₂ mainly involves changes in the heat stability of the thylakoids and RuBisCO activity. Hence, high temperature and CO₂ elevations may have synergistic effect on photosynthesis and CO₂ elevations may lead to improved acclimation to high temperatures. However, such interactions may vary with plant species^22,23 and other environmental conditions. Variations in acclimation ability can change the interactions within and between species and the composition and functioning of plant communities under future climatic conditions. Furthermore, in most past studies, high temperature treatments are achieved in one step, which is in contrast with the gradual, progressive increases in temperature occurring in global climate changes.

The boreal forest is an important terrestrial ecosystem with a high carbon sequestration potential²⁴. As the global climate change accelerates, the boreal forest has been experiencing progressive increases in temperatures and CO₂. The response of the boreal forests could have great impact on the global carbon balance²⁵. White birch is one of the most widely distributed tree species in the boreal forest. The growth conditions of white birch in northwest Ontario are characterized by a long cold winter and short summer. For example, the annual mean temperature in Thunder Bay region is 2.4°C while the January and July average temperatures are -14.9°C and 17.6°C (based on Environment Canada’s online weather records for the time period of January 1943 to December 2003). Nevertheless, based on our past experience in growing white birch seedlings in greenhouses, it appears that the species is capable of acclimating to continuous warming to more than 40°C in the early afternoon on sunny summer days (see Figure 1). In this current study, we test the hypothesis that CO₂ elevation will enhance the photosynthetic performance of white birch seedlings growing in a progressively warming environment.

Figure 1. Time course of temperatures in the greenhouses during the experimental period (March 1 through August 15).

(A) Postmeridian (hour) pattern between 13:00 and 16:00; (B) Diel (hour) pattern between 0:00 and 24:00.

Materials and methods

Results

In situ photosynthetic gas exchange

There was a significant (P<0.01) interactive effect of temperature and CO₂ on Pn (Figure 2). Pn was higher (P<0.01) at 37°C than at 26°C under elevated CO₂(Figure 2), but there was no significant (P>0.05) temperature effect on Pn under ambient CO₂. CO₂ elevation significantly increased Pn at both temperatures (P<0.05, P<0.001 at 26°C and 37°C, respectively). g_s significantly (P<0.05) decreased at 37°C under both ambient and elevated CO₂(Figure 2), and there was no significant (P>0.05) CO₂ effect on g_s. Meanwhile high temperature significantly (P<0.05) stimulated E under both ambient and elevated CO₂(Figure 2). Water-use efficiency (WUE) was significantly (P<0.05) higher at 26°C than that at 37°C under both CO₂ regimes. CO₂ elevation greatly (P<0.001) increased WUE at both temperatures.

Figure 2. Pn, g_s, E and WUE (mean ± SD, n=3–4) for current year white birch seedlings after they were exposed to continuous warming under ambient CO₂ and elevated CO₂ concentrations for 5 months.

The in situ measurements were taken at 26°C and 37°C under ambient CO₂ and elevated CO₂. The significance levels (*** = P<0.001, ** = P<0.01, * = P<0.05). If the interaction between measurement temperature and CO₂ was significant for a given parameter, Scheffe’s F test for post hoc pairwise comparisons was conducted. Means sharing the same letter or letters are not significantly different.

High temperature significantly reduced C_i under both ambient and elevated CO₂ (P<0.05, P<0.01, respectively) and, also, elevated CO₂ significantly (P<0.001) increased C_i at both temperatures.

In vivo RuBisCO activity

V_cmax, J_max and TPU at 37°C were significantly (P<0.001) higher than those at 26°C (Figure 3). The temperature dependencies of V_cmax and J_max were changed by CO₂, and those values at 37°C enhanced much more (P<0.05) under elevated CO₂ than under ambient CO₂.

Figure 3. V_cmax, J_max, TPU and C_i in current year white birch seedlings.

V_cmax, J_max and TPU were derived from A-C_i curves, which were measured at 26°C and 37°C under ambient CO₂ and elevated CO₂. See Figure 2 for other explanations.

Photosystem II efficiency and electron transport partitioning to carboxylation and oxygenation

There was a significant (P<0.001) interactive effect of CO₂ and temperature on (F_m’-F)/F_m’ and J_T(Figure 4). (F_m’-F)/F_m’ and J_T greatly increased at 37°C as compared to at 26°C under elevated CO₂, and there was no significant temperature effect on (F_m’-F)/F_m’ and J_T under ambient CO₂.

The pattern of CO₂ and temperature effects on J_c was almost the same as (F_m’-F)/F_m’ and J_T(Figure 4), and J_c was greater (P<0.001) at 37°C than that at 26°C under elevated CO₂, and there was no significant temperature effect on J_c under ambient CO₂. Elevated CO₂ greatly suppressed J_o/J_T, and there was no significant (P > 0.05) effect of temperature on J_o/J_T(Figure 4).

Figure 4. (F_m’-F)/F_m’, J_T, J_c and J_o/J_T in the current year white birch seedlings (F_m’-F)/F_m’ and J_T were derived from chlorophyll fluorescence measurements, and J_c and J_o were derived from both chlorophyll fluorescence and gas exchange measurements.

See Figure 2 for other explanations.

Discussion

Our results suggest that the photosynthetic mechanisms of white birch seedlings have high capacity to acclimate to a progressively warming environment, particularly under elevated CO₂. This result is in contrast to the results of most studies with a single step warming treatment. Larcher³⁶ has suggested that plants’ optimal temperature is closely related to the climate in which they grow. The measurement temperatures of 26°C and 37°C used in this study are believed to be the normal (or optimal) and stressful temperature, respectively, for most boreal forest tree species growing at their natural environments. Zhang et al.³⁷ have found that the Pn of mature oak even in warm-temperate zones decline greatly at temperatures over 30°C, as compared to measurements at temperatures of 20–30°C, which occurs naturally north of temperate zones or even warm-temperate zones. However, in this experiment the Pn of white birch didn’t decline at 37°C under ambient CO₂, as compared to that at 26°C; furthermore, Pn increased substantially at 37°C under elevated CO₂. These results indicate that the photosynthetic mechanisms of white birch acclimated to the progressive warming environment, and this high temperature acclimation was greatly strengthened by elevated CO₂. Long²⁰ argued that CO₂ elevation could change the photosynthesis dependence of temperature.

The activity of RuBisCO is highly temperature-dependent. According to Jordan and Ogren³⁸, the Rubisco’s specificity for CO₂/O₂ decreases as increasing temperatures over the optimal range, but the increase in RuBisCO oxygenation will exceed that of carboxylation because the solubility of CO₂ declines faster than that of O₂ at even higher temperatures, resulting in a decline in net photosynthetic rate. White birch’s acclimation to warming was also evidenced by V_cmax measured at the two different temperatures and two CO₂ regimes. V_cmax at 37°C was much higher than at 26°C under both ambient and elevated CO₂, indicating a shift in the temperature dependency of RuBisCO. Furthermore, the partitioning of total electron transport to oxygenation was not significantly different between the two temperatures under either ambient CO₂ or elevated CO₂, suggesting that the higher temperature did not change the RUBisCO specificity for CO₂/O₂ which could be a contributing factor for the enhanced acclimation of photosynthesis to the progressive warming. Overdieck et al.¹⁵ have also found that both the temperature treatment alone and the combination of elevated CO₂ and temperature depressed V_cmax in Scots pine at temperatures below the optimum range, but increased V_cmax when the temperature was above the optimum. Additionally, the magnitude of the change in V_cmax increased as temperature increased.

The decrease in C_i at the high temperature could be attributable to either enhanced RuBisCO activity or declines in stomatal conductance or both. Not only V_cmax, but J_max and TPU were also higher at 37°C than at 26°C, suggesting that the CO₂ assimilation process, including carboxylation, electron transport for RuBP regeneration, ATP supply and the translocation of the primary photosynthates, all maintained at high levels in the warm environment. In this study, there was no down-regulation of RuBisCO activity in association with the CO₂ elevation, to the contrary, CO₂ elevation greatly increased V_cmax and J_max at 37°C, as well as Pn at both 26°C and 37°C.

While high temperature enhanced V_cmax under both ambient and elevated CO₂, the increases in actual PSII efficiency (ΔF’/F_m’) and J_c associated with the high temperature only occurred under elevated CO₂, suggesting that the high temperature did not significantly affect the total electron transport, and its partitioning to carboxylation, t under the ambient CO₂. Conversely, the partitioning of total electron flow to oxygenation increased more than 40% in response to the high temperature under elevated CO₂. The reduced electron transport partitioning to carboxylation and low C_i might explain why Pn was relatively low at 37°C under the ambient CO₂, even though the corresponding V_cmax was quite high, implying that the slow electron transport to carboxylation and CO₂ supply at high temperature under ambient CO₂ didn’t match the high activity of RuBisCO. This again confirms Kirschbaum’s theoretical analysis that photosynthesis has a higher potential to be stimulated by CO₂ elevation at high temperatures than at low temperatures¹⁶.