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Effects of elevated CO₂ on the tolerance of photosynthesis to acute heat stress in C₃, C₄, and CAM species¹

² Department of Environmental Sciences, University of Toledo, Toledo, Ohio 43606 USA ³ Department of Biology, Washington & Lee University, Lexington, Virginia 24450 USA

Received for publication 17 April 2007. Accepted for publication 14 December 2007.

ABSTRACT

Determining the effect of elevated CO₂ on the tolerance of photosynthesis to acute heat stress (AHS) is necessary for predicting plant responses to global warming because photosynthesis is heat sensitive and AHS and atmospheric CO₂ will increase in the future. Few studies have examined this effect, and past results were variable, which may be related to methodological variation among studies. In this study, we grew 11 species that included cool and warm season and C₃, C₄, and CAM species at current or elevated (370 or 700 ppm) CO₂ and at species-specific optimal growth temperatures and at 30°C (if optimal 30°C). We then assessed thermotolerance of net photosynthesis (P_n), stomatal conductance (g_st), leaf internal [CO₂], and photosystem II (PSII) and post-PSII electron transport during AHS. Thermotolerance of P_n in elevated (vs. ambient) CO₂ increased in C₃, but decreased in C₄ (especially) and CAM (high growth temperature only), species. In contrast, elevated CO₂ decreased electron transport in 10 of 11 species. High CO₂ decreased g_st in five of nine species, but stomatal limitations to P_n increased during AHS in only two cool-season C₃ species. Thus, benefits of elevated CO₂ to photosynthesis at normal temperatures may be partly offset by negative effects during AHS, especially for C₄ species, so effects of elevated CO₂ on acute heat tolerance may contribute to future changes in plant productivity, distribution, and diversity.

Key Words: C₃ • C₄ • CAM • carbon dioxide • global climate change • photosystem II • thermotolerance

Anthropogenic contributions to atmospheric CO₂ likely are largely responsible for recent increases in global mean surface temperatures, which rose by 0.6°C from 1990 to 2000 and are projected to increase by another 1.4 to more than 5°C by 2100 (Houghton et al., 2001; IPCC, 2001). In addition to mean increases in annual temperatures, there will also be increases in the frequency, duration, and severity of periods with exceptionally high temperatures (i.e., heat waves) (Wagner, 1996; Haldimann and Feller, 2004). Thus, in the future, plants will likely undergo increases in acute heat stress, which can impact plant growth and development, decreasing crop and ecosystem productivity (Ciais et al., 2005) and biodiversity (Davis, 1986; Thomas et al., 2004).

Negative effects of heat stress on plants are caused to a large extent by negative effects on photosynthesis, which is among the most thermosensitive aspects of plant function (e.g., Berry and Björkman, 1980; Weis and Berry, 1988; Wise et al., 2004; Kim and Portis, 2005). Both the light (electron transport) and dark (Calvin cycle) reactions of photosynthesis have thermolabile components, especially photosystem II (PSII) in the light reactions (Santarius, 1975; Berry and Björkman, 1980; Weis and Berry, 1988; Heckathorn et al., 1998, Heckathorn et al., 2002) and rubisco (ribulose 1,5-bisphosphate carboxylase/oxygenase) activase in the Calvin (CO₂ fixation) cycle (Eckardt and Portis, 1997; Crafts-Brandner and Salvucci, 2000). However, increases in atmospheric levels of CO₂ above current levels can increase photosynthesis by decreasing photorespiration (fixation of O₂ rather than CO₂ by rubisco, the first step of the Calvin cycle), which increases with temperature and is higher in plants with C₃-type photosynthesis (the majority of plants) vs. plants with the other two types of photosynthesis, C₄ and CAM plants (Sage and Monson, 1999; Taiz and Zeiger, 2004); thus, elevated CO₂ might benefit C₃ plants more than C₄ plants during heat stress. Additionally, elevated CO₂ can also increase water-use efficiency, in part by decreasing stomatal conductance and transpiration (Ainsworth et al., 2002), which may increase tolerance to acute heat by increasing plant water status. On the other hand, stomatal conductance (opening) in both C₃ and C₄ plants is reduced with increasing CO₂ (e.g., 20% for C₃ and 50% for C₄ species with a doubling of CO₂) (Sage, 1994; Wand et al., 1999; Reich et al., 2001; Maherali et al., 2002), so the lower average stomatal conductance of C₄ plants at any given CO₂ level means lower average transpiration (water loss) and thus higher leaf temperatures in C₄ plants, which may increase heat-related damage in C₄ plants compared to C₃ plants in the same habitat.

Because increases in temperature and CO₂ may have interactive effects on photosynthesis, many studies have examined the effects of elevated CO₂ and increased growth temperature (typically 3–5°C) on photosynthesis (reviewed by Morison and Lawlor, 1999). In contrast, the effects of elevated CO₂ and the interactions between elevated CO₂ and higher mean growth temperature on plant responses to acute heat stress have been examined in only a few studies, and the results have been variable (Table 1). For example, elevated CO₂ has yielded positive (Faria et al., 1996, Faria et al., 1999; Ferris et al., 1998; Huxman et al., 1998; Hamerlynck et al., 2000; Taub et al., 2000), negative (Bassow et al., 1994; Roden and Ball, 1996a, b; Huxman et al., 1998; Taub et al., 2000), and no effects (Coleman et al., 1991) on photosynthetic and plant tolerance to acute heat stress. In the previous studies that compared elevated-CO₂ effects on tolerance to acute heat stress in relatively heat-sensitive vs. -tolerant species or in species with different photosynthetic pathways (Coleman et al., 1991; Bassow et al., 1994; Roden and Ball 1996a, b; Huxman et al., 1998; Taub et al., 2000), all species were grown under identical thermal regimes, which were likely closer to optimal for some of the species examined, but supra- or suboptimal for others. Given that growth temperature is known to strongly influence the response and tolerance of organisms and photosynthesis to acute heat stress (e.g., Weis and Berry, 1988; Barua and Heckathorn, 2004), comparisons of the heat-stress responses of species not grown at their respective optimal (or sub- or supra-optimal) growth temperatures may obscure response patterns that otherwise may be evident. In addition, heat stress treatments in the previous studies varied widely in both intensity and duration (Table 1), making it difficult to directly compare across studies. Further, only one previous study included C₄ species (1 species in Coleman et al., 1991), but photosynthesis was not measured in this study, and only one study included CAM species (1 species in Huxman et al., 1998). In a preliminary study with Pisim sativum (pea, cool-season C₃) and Zea mays (corn, warm-season C₄), effects of elevated CO₂ on photosynthetic thermotolerance were positive in the C₃, but negative in the C₄, species (Joshi, 2006). However, it remains to be determined if this difference can be generalized and is related to photosynthetic pathway or organismal thermotolerance because C₄ species are also warm-season species originating from tropical/subtropical climates (Sage and Monson, 1999).

MATERIALS AND METHODS

Plant material and growing conditions
Eleven species were examined in this study, including three cool-season C₃ species (Pisum sativum L., pea; Chenopodium album L., lambs quarters; Triticum aestivum L.,wheat), three warm-season C₃ species [Glycine max L., soybean; Helianthus annuus L., sunflower; Lycopersicon esculentum L., tomato), three C₄ species (Zea mays L., corn or maize; Sorghum bicolor L. (Moench), sorghum; Amaranthus retroflexus L., pigweed], and two CAM species (Agave americana L., century plant; Ferocactus wislizenii Britt. & Rose, fish-hook cactus]. All C₃ and C₄ species used are annuals and were germinated and grown (ca. 6 wk) in ambient or elevated CO₂ until the early vegetative stage (e.g., to the 6th leaf stage in corn, the species with the largest plants in this study). The agave and cactus species used are perennials, and young (ca. 3 yr old) plants (initially raised under ambient CO₂) were raised under controlled ambient or elevated CO₂ levels for three months prior to use to ensure acclimation to CO₂ treatments (Note: This was sufficient time for the agave species to produce two new fully expanded leaves, from which photosynthetic data were collected, and for the cactus species to increase in diameter by ca. 2 cm). Plants were grown in 5-L pots in a 1:1:1 mixture of top-soil, sand, and perlite and placed in growth chambers (E-36HO, Percival Scientific, Perry, Iowa, USA) equipped with light, temperature, and CO₂ control. All the species were grown under four temperature regimes (20/12°C, 25/17°C, 30/22°C and 35/27°C for day/night respectively; CAM species were also grown at 38/30°C) to determine species-specific optimal (or near-optimal) temperatures (based on biomass, Table 2). Plants were grown at either ambient (370 ± 15 ppm) or enriched (700 ± 15 ppm) CO₂, with a day length of 14 h and a light level of 1000 µmoles µm^–2·S^–1 PAR (photosynthetically active radiation) at the canopy level of plants. Plants were rotated at least once per week to avoid position effects in the chambers. Prior to treatment, a subset (15–18) of uniformly sized plants of each species was selected within each chamber for further use. All the pots were watered as needed and fertilized regularly (every other week with a commercial complete nutrient mix), so that plants were not water or nutrient limited.

Photosynthesis measurements
Steady-state net photosynthesis (P_n; net CO₂ exchange) of leaves was measured with a portable photosynthesis–transpiration system with an infra-red gas analyzer (model 6400, LiCOR, Lincoln, Nebraska, USA), equipped with a 250-mm³ leaf chamber. Measurements were made within 1–2 min of insertion of leaves into the cuvette, and again after stabilization of CO₂ and H₂O flux to ensure that photosynthetic responses reflected those within the growth chambers. Plants were measured before and during heat stress, as described in Heckathorn et al. (1996), at the same CO₂ levels at which the plants were growing (either 370 or 700 ppm CO₂), a light level of 1000 µmol·m^–2·S^–1 PAR (ca. equal to that at the tops of the plants), and at species-specific growth temperatures. During heat stress, P_n was measured twice at 1000 and 1300 hours. All results were collected from recently expanded, fully lit leaves of intact plants.

For the CAM species, we monitored treatment effects on net CO₂ fixation by determining the pH of chlorenchyma (green) tissue at the end of the heat treatment in both heat-stressed and unstressed control plants. CAM species photosynthetically fix CO₂ at night into malic acid, lowering tissue pH throughout the night in the absence of other large pools of acid, and they decarboxylate this CO₂ during the day and use it and ATP and NADPH from the light reactions to produce sugars, thereby increasing cell pH throughout the day (Taiz and Zeiger, 2004). If heat stress affected net CO₂ fixation in the CAM species, then the pH of the photosynthetic tissue should be lower in heat-treated plants compared to controls because utilization of the CO₂ fixed at night would be hindered and the normal daytime increase in pH would be slowed. Plants were harvested at the end of the heat-stress treatment and immediately frozen and stored at –70°C. Subsamples of tissue were later ground completely with a mortar and pestle, diluted with 10 mL of deionized water, and then measured to determine pH.

To examine heat effects on PSII and post-PSII electron transport, PSII efficiency (F_v'/F_m') and photochemical quenching (q_p) in light-adapted leaves were monitored by analysis of chlorophyll fluorescence using a pulse-amplitude modulated (PAM) fluorometer (model PAM 101/103, Walz, Effeltrich, Germany). Chlorophyll fluorescence was measured in unstressed control plants and on HS plants during heat stress at 1000 and 1300 hours. Basal fluorescence (F_s) under steady-state illumination (900 µmol·m^–2·S^–1 PAR) was measured initially, followed by maximum fluorescence (F_m') after a 1.0-s pulse of saturating white light (>5000 µmol·m^–2·S^–1 PAR). Minimum fluorescence (F_o') was then measured after turning off both actinic and flash light-sources. F_v'/F_m' and q_p were then calculated as in Genty et al. (1989), where F_v'/F_m' = (F_m' – F_o')/F_m', and q_p = (F_m' – F_s)/(F_m' – F_o').

Statistical analysis
All photosynthesis and fluorescence results are means derived from independent replicate plants (separate sets of plants were used for controls and each heat-stress time point). Analyses were conducted within each species to determine whether the physiological variables differed as a function of different treatments. Unless indicated otherwise, a split-plot two-way ANOVA (JMP 5.1 software, SAS Institute, Cary, North Carolina, USA) was used to test for significant effects of CO₂, heat stress duration (control, 1 h of heat stress, 4 h of heat stress), and their interaction on P_n, g_st, C_i, F_v'/F_m', and q_p through the time course of the high-temperature period. Three-way ANOVAs were also conducted among C₃ and C₄ species to determine whether CO₂ effects differed as a function of different photosynthetic groups, with P_n, g_st, C_i, F_v'/F_m', and q_p as dependent factors and CO₂, heat-stress duration, and functional types (cool-season C₃, warm-season C₃, and C₄) as independent factors. Posthoc Tukey honestly significant difference (HSD) tests were run on specific contrasts to examine significant treatment effects among groups (JMP software). Absolute data were used in correlation analyses (SAS version 9.1, SAS Institute, Cary, North Carolina, USA) between P_n and g_st, C_i, F_v'/F_m' and q_p for C₃ and C₄ species, respectively; these results were compared to results with log-transformed data and results of partial-correlation analysis, which yielded similar conclusions.

RESULTS

On the basis of the seedling biomass for species grown at different temperatures (Table 2), the near-optimal growth temperature for the cool-season C₃ species was ca. 25°C and was ca. 30°C for the warm-season C₃ and the C₄ species. Therefore, in subsequent experiments, 25°C and 30°C were used as the optimal daytime growth temperatures for cool-season C₃ and warm-season C₃ & C₄ species, respectively.

As expected, prior to initiation of acute heat stress (AHS), C₃ species (except for wheat at 25°C and chenopodium at 30°C) grown at elevated CO₂ had a significant stimulation of P_n compared to ambient CO₂, while C₄ species had little stimulation of P_n in elevated CO₂ (Fig. 1). Within 1 h of AHS, decreases in P_n were observed for most species, with additional decreases in P_n with continuing heat stress, such that after 4 h of AHS, P_n decreased significantly in all species (Table 3). For the C₄ species, the decreases in P_n caused by AHS were more pronounced in plants grown at elevated CO₂ than in those grown at ambient CO₂. For the cool-season C₃ species, the positive effects of elevated CO₂ on P_n during AHS were evident both for plants grown at optimal daytime growth temperatures before AHS and for plants grown at 30°C before AHS; however, the stimulatory effects of high CO₂ were not as great at the higher growth temperature.

View larger version (18K): [in this window] [in a new window]   Fig. 1. Time course of net photosynthesis (Pn) in nine species grown at species-specific optimal daytime prestress temperatures (solid lines, 25°C in C3 cool-season, 30°C in all other species), exposed to 370 (dark circles) or 700 ppm CO2(light circles), before and during a 4-h heat stress. The dotted lines for the C3 cool-season species are for plants grown at 30°C . Each data point represents the mean (±SD) of 4–6 independent replicates.

View this table: [in this window] [in a new window]   Table 3. Results from analysis of variance (F values) for treatment effects in each species at their species-specific optimal growth temperature, with time (duration of heat stress), CO2, and their interactions as independent factors, and Pn, gst, Ci, Fv'/Fm', and qp as dependent variables (*significance at = 0.05; **significance at = 0.01).

View larger version (18K): [in this window] [in a new window]   Fig. 2. Time course of stomatal conductance to water vapor (gst) in nine species grown at species-specific optimal daytime prestress temperatures (solid lines, 25°C in C3 cool-season, 30°C in all other species), exposed to 370 (dark circles) or 700 ppm CO2(light circles), before and during a 4-h heat stress. The dotted lines for the C3 cool-season species are for plants grown at 30°C. Each data point represents the mean (±SD) of 4–6 independent replicates.

View larger version (16K): [in this window] [in a new window]   Fig. 3. Time course of leaf internal CO2 concentration (Ci) in nine species grown at species-specific optimal daytime prestress temperatures (solid lines, 25°C in C3 cool-season, 30°C in all other species), exposed to 370 (dark circles) or 700 ppm CO2(light circles), before and during a 4-h heat stress. The dotted lines for the C3 cool-season species are for plants grown at 30°C. Each data point represents the mean (±SD) of 4–6 independent replicates.

View larger version (17K): [in this window] [in a new window]   Fig. 4. Time course of photosystem II efficiency (Fv'/Fm') in nine species grown at species-specific optimal daytime prestress temperatures (solid lines, 25°C in C3 cool-season, 30°C in all other species), exposed to 370 (dark circles) or 700 ppm CO2(light circles), before and during a 4-h hea stress. The dotted lines for the C3 cool-season species are for plants grown at 30°C. Each data point represents the mean (±SD) of 4–6 independent replicates.

View larger version (17K): [in this window] [in a new window]   Fig. 5. Time course of photochemical quenching (qp) in nine species grown at species-specific optimal daytime prestress temperatures (solid lines, 25°C in C3 cool-season, 30°C in all other species), exposed to 370 (dark circles) or 700 ppm CO2(light circles), before and during a 4-h heat stress. The dotted lines for the C3 cool-season species are for plants grown at 30°C. Each data point represents the mean (±SD) of 4–6 independent replicates.

View larger version (14K): [in this window] [in a new window]   Fig. 6. Heat stress effects on Fv'/Fm' and qp of CAM species (agave and cactus) grown at 25, 30, and 35°C daytime prestress temperatures, exposed to 370 (dark circles) or 700 ppm CO2(light circles), before and during a 4-h heat stress. Each data point represents the mean (±SD) of 4–6 independent replicates.

View larger version (21K): [in this window] [in a new window]   Fig. 7. Heat stress effects on chlorenchyma pH of CAM species (agave and cactus) grown at 25, 30, and 35°C daytime prestress temperatures after a 4-h heat stress (lc: 370 ppm CO2, without heat stress; lh: 370 ppm CO2, with heat stress; hc: 700 ppm CO2, without heat stress; hh: 700 ppm CO2, with heat stress). Each bar represents the mean (±SD) of 3–4 independent replicates. Different letters above the bars indicate a significant difference among treatments at the same temperature (P < 0.05, according to Tukey HSD test).

View this table: [in this window] [in a new window]   Table 4. Results from analysis of variance (F values) for treatment effects in CAM species at three growth temperatures, with time (for Fv'/Fm', qp) or heat (for pH), CO2, and their interactions as independent factors, and Fv'/Fm', qp, and pH as dependent variables. Time = duration of heat stress (0, 1, or 4 h); heat = heat treatments (control, 4-h heat stress) harvested at the same time at end of the treatment period (*significance at = 0.05; **significance at = 0.01).

View larger version (26K): [in this window] [in a new window]   Fig. 8. Correlation analysis between Pn and the other photosynthetic variables for C3 and C4 species separately (within each panel, data for all C3 and C4 species combined and not separated by CO2 level). (A) Pn vs. gst, (B) Ci, (C) Fv'/Fm', and (D) qp; panel –0 = results from controls, –1 = results after 1 h of heat stress, and –2 = results after 4 h of heat stress. C3 species, closed circles; C4 species, open circles.

Elevated CO₂ increased the tolerance of net photosynthesis (P_n) to acute heat stress in C₃ species, but decreased thermotolerance of P_n in C₄ species. Small but significant negative effects of high CO₂ were also observed on chlorenchyma pH in heat-stressed plants of the CAM species (high growth temperature only), suggesting that net photosynthesis was negatively impacted by high CO₂ during heat stress for CAM plants. Increases in P_n thermotolerance with high CO₂ in C₃ species were observed in both cool- and warm-season species; hence, CO₂ effects were related to photosynthetic pathway, not to organismal thermotolerance (confirmed by three-way ANOVA, where P < 0.01 for the interactive effect of functional types and CO₂, not significant when comparing C₃ warm- and cool- season species). Also, the pattern of CO₂ effects observed here was evident whether comparing plants grown at their respective optimal prestress growth temperatures or when comparing plants raised at a common growth temperature (30°C). Notably, the relative benefits of elevated CO₂ on P_n thermotolerance were significantly reduced in the C₃ species grown at supra-optimal prestress growth temperatures (i.e., in the cool-season C₃ species grown at optimal + 5°C = 30°C). Although elevated CO₂ decreased stomatal conductance in most species, stomatal limitations to P_n increased during heat stress in only two species examined; hence, the effects of elevated CO₂ on P_n thermotolerance were caused by negative effects of high CO₂ on photosynthetic metabolism in the majority of species, rather than by CO₂-induced decreases in stomatal conductance. In agreement with this, elevated CO₂ decreased the thermotolerance of electron transport, either by decreasing the efficiency of PSII (F_v'/F_m') and/or by decreasing the performance of post-PSII electron transport relative to PSII (q_p), such that PSII quantum yield (_PSII) decreased with high CO₂ in all species (including the two CAM species) but one (tomato, C₃).

The correlation analyses also indicated that, across species, P_n was not limited by g_st or C_i during heat stress in either C₃ or C₄ species, but was likely limited (or colimited) by damage to electron transport at some point in the heat stress period. Although P_n was positively correlated with g_st prior to heat stress in C₃ species, as might be expected, during heat stress, P_n was mostly not (or even negatively) correlated with g_st and C_i during heat stress in both C₃ and C₄ species (because P_n decreased in all species during heat stress, but g_st and C_i did not generally decrease). In contrast, P_n was strongly correlated with electron transport before and during heat stress in both C₃ and C₄ species. Interestingly, in C₄ species, P_n was only correlated with PSII efficiency before heat stress, but with both PSII and post-PSII efficiency during heat stress. However, in C₄ species, the strength of the correlation between P_n and electron transport decreased with duration of heat stress (i.e., from time 0, to 1 h, and then 4 h, of heat stress), suggesting the possibility that the relative importance of electron transport in limiting P_n during heat stress decreased with the duration of heat stress. In contrast, in C₃ species, P_n was strongly correlated with electron transport (both PSII and post-PSII), both before heat stress and after 4 h of heat stress; yet, no such correlation was observed after 1 h of heat stress, indicating that some aspect of photosynthesis other than electron transport (e.g., rubisco activity via rubisco activase) limited P_n early in the heat stress, and electron transport became an important limitation later in the heat-stress treatment.

Together, these results suggest that the benefit of elevated CO₂ to P_n thermotolerance in C₃ plants is related to decreased photorespiration during heat stress and that the negative impact of elevated CO₂ on photosynthetic light reactions was offset by decreases in photorespiration (as also indicated in Roden and Ball, 1996a). Given that photorespiration increases with temperature and that C₃ species have high levels of photorespiration compared to C₄ and CAM species (Sage and Monson, 1999; Taiz and Zeiger, 2004), then the photorespiratory benefits of elevated CO₂ to C₃ plants during heat stress should outweigh negative effects until such a point that rubisco is damaged or that damage to electron transport becomes limiting to net photosynthesis. This prediction is supported by the relative decrease in the benefits of elevated CO₂ to P_n in the cool-season C₃ species grown at supraoptimal prestress growth temperatures (30°C) compared to those grown at optimal temperatures (25°C). Studies of the thermal sensitivity of rubisco or rubisco activase activity indicates that rubisco function (primarily via damage to rubisco activase) begins to decrease significantly by ca. 35–40°C in representative cool- and warm-season species (Eckardt and Portis, 1997; Feller et al., 1998; Crafts-Brandner and Salvucci, 2000), so negative effects of elevated CO₂ on photosynthetic electron transport in C₃ species should begin to limit P_n during acute heat stress at temperatures over ca. 35–40°C. Thus, in a future warmer world with increases in both mean and extreme temperatures, the negative effects of elevated CO₂ on electron transport may commonly limit P_n in C₃, as well as in C₄ and CAM species.

The positive effect of elevated CO₂ on net photosynthetic (P_n) thermotolerance in C₃ species have also been observed in other studies (Faria et al., 1996, Faria et al., 1999; Ferris et al., 1998; Huxman et al., 1998, in one of two species; Hamerlynck et al., 2000; Taub et al., 2000). In previous studies, negative effects of high CO₂ on photosynthetic heat tolerance were also observed for C₃ species (Roden and Ball, 1996a), and negative effects of high CO₂ during heat stress on biomass were observed for three C₃ tree species (Bassow et al., 1994). The CO₂ effects on photosynthetic thermotolerance in C₄ species was not previously studied, and in only one CAM species was the effect studied (neutral effect; Huxman et al., 1998).

As in this study, negative, positive, and neutral effects of elevated CO₂ on heat tolerance of F_v /F_m have been observed in C₃ species (no C₄ species examined) (Faria et al., 1996, Faria et al., 1999; Roden and Ball, 1996a, b; Huxman et al., 1998; Hamerlynck et al., 2000; Taub et al., 2000). Previously, only one CAM species had been examined, wherein high CO₂ decreased F_v /F_m during heat stress (Huxman et al., 1998), as in this study. Also, similar to this study, in the two previous studies to measure quantum yield of electron transport (_PSII), elevated CO₂ decreased thermotolerance of _PSII in all species (four C₃, one CAM) (Roden and Ball, 1996a; Huxman et al., 1998). A notable difference between the current study and Huxman et al. (1998) is the magnitude and duration of the temperature stress imposed upon the plants (we subjected plants to a 4-h treatment at 40–50°C, depending on species, whereas Huxman et al. subjected plants to a maximum daily temperature of 55°C for 9 d), yet the two studies obtained similar results, suggesting that negative effects of elevated CO₂ on heat tolerance of electron transport may be generalized to heat stress of various durations.

In addition to photorespiration, there are other aspects of metabolism that are affected by growth under elevated CO₂, including cellular adaptations conferring plant tolerance to acute heat stress, and CO₂-related changes in these heat-stress adaptations will likely impact photosynthetic thermotolerance. For example, heat-shock proteins (Heckathorn et al., 1998, Heckathorn et al., 2002), lipid saturation level (Larkindale and Huang, 2004), the carotenoids (especially zeaxanthin) (Havaux, 1998), protective compatible solutes (Williams et al., 1992), and isoprene production (Velikova and Loreto, 2005) are known to confer photosynthetic thermotolerance. Williams et al. (1998) found that growth at elevated CO₂ increased saturation of some classes of thylakoid lipids. Both increases and decreases in isoprene emission have been reported for plants grown under elevated CO₂ (Sharkey et al., 1991; Tognetti et al., 1998). Growth at elevated CO₂ profoundly alters cellular and subcellular concentrations of many soluble compounds (Poorter et al., 1997). And, heat shock protein content is decreased at low N and at high CO₂ in leaves (Heckathorn et al., 1996; Wang and Heckathorn, unpublished manuscript). Further experiments are needed to supply direct evidence of an association between, for example, lipid changes, protective solutes, isoprene, heat shock proteins, and thermotolerance at elevated CO₂, to determine if high-CO₂-related decreases in heat-stress adaptations are linked to decreased thermotolerance of electron transport observed in this study.

Regardless of the underlying mechanisms, the results of this study indicate that increases in atmospheric CO₂ will alter plant photosynthetic responses to acute heat stress (or heat waves) and that the effect of CO₂ will likely vary with the photosynthetic pathway (C₃, C₄, CAM). Given that the frequency, duration, and severity of heat stress will increase for plants in the coming decades (Wagner, 1996; Haldimann and Feller, 2004) and that photosynthesis is relatively heat sensitive (Weis and Berry, 1988), these results indicate that interactions between elevated CO₂ and plant thermotolerance may contribute to future changes in plant (including crop) productivity, distribution, and diversity associated with global environmental change. Specifically, our results indicate that increases in atmospheric CO₂ and acute heat stress in combination may further tip the balance toward C₃ species, beyond what high CO₂ alone might do, which may contribute to increases in C₃ vegetation, both globally and in communities containing a mix of C₃ and C₄ species (e.g., midcontinental grasslands in the United States). However, the negative effects of elevated CO₂ to C₄ species during heat stress may be alleviated by higher water-use efficiency of C₄ species at both the leaf and whole-plant levels, especially in years with water stress (Owensby, 1993; Hamerlynck et al., 1997; Owensby et al., 1999), and the benefits of elevated CO₂ to C₃ species at near-optimal growth temperatures may be offset by expected increases in mean growth temperatures or by likely changes in other environmental factors that influence thermotolerance differentially (e.g., increases or decreases in precipitation that might increase or decrease tolerance, respectively, and increasing ozone which might decrease tolerance).

FOOTNOTES

¹ The authors thank the two anonymous reviewers and J. Frantz for helpful comments on the manuscript. This research was supported by grants from the National Science Foundation to S.A.H. and E.W.H.

⁴ Author for correspondence (e-mail: dan.wang{at}utoledo.edu), phone: 1-419-530-2925

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