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American Journal of Botany 95(2): 165–176. 2008.

Effects of elevated CO2 on the tolerance of
photosynthesis to acute heat stress in C3, C4, and
CAM species1
Dan Wang,2,4 Scott A. Heckathorn,2 Deepak Barua,2 Puneet Joshi,2
E. William Hamilton,3 and Jacob J. LaCroix2

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

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 (Pn), stomatal conductance (gst), leaf internal [CO2], and photosystem II (PSII) and
post-PSII electron transport during AHS. Thermotolerance of Pn 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 gst in five of nine species, but stomatal limitations to Pn increased during AHS in only two coolseason 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, 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
1 Manuscript

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, 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

received 17 April 2007; revision accepted 14 December 2007.

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:, phone:


15) 1.30) 2. and SOD activity.. growth CO2 level was 370 ppm.33) 0. 95 American Journal of Botany Overview of past studies examining effects of elevated CO2 on tolerance to acute heat stress. N = 3–5..10) 2.44) 3. carboxylation efficiency Positive effects on recovery Hamerlynck et al.13) 1. duration CO2 effects Betula populifolia. C3 Eucalyptus rossii. all species were grown under identical thermal regimes. 2004).85 (0. gst.45 (0. depending on species and variable Huxman et al. Fv/Fm.24 (0. qn. Roden and Ball 1996a. Whole-plant fresh mass (g) Species C3. 1998 Eucalyptus macrorhyncha. 1994. Fv′/Fm′. Plants were 2. C3 Yucca schidigera. leaf damage Negative effects. variable-to-maximum fluorescence of PSII in dark & light-adapted leaves.. especially the most shade-tolerant species 32–40°C. 2000). 2000 Yucca whipplei.. C3 28°C 45°C.02 (0. CAM 45°C 53°C. stomatal conductance to H2O. In addition.20) 0. HS.08 (0.14) 2. C3 25°C 45°C. C3 45°C 53°C. Similar temperature effects were observed for shoot dry mass after 6 wk of growth in separate experiments (not shown).61 (0.80 (0. Huxman et al. CAT. SOD. 2000 PSIIb Biomass. Temperatures are daytime growth temperatures.27) 1. C3 20°C 45°C. catalase activity.01 (0.02) 3. 1998 Larrea tridentata. 9 d Anet. cool-season Pisum sativum Chenopodium album Triticum aestivum C3. Response factorsa Species and photosynthetic pathway GT HS. ΦPSII. 1998. gst. Fv/Fm Positive effects Amax. organisms and photosynthesis to acute heat stress (e.30) 2. Amax. C3 Acer pennsylvanicum. 4 h Biomass. A . day growth temperature.99 (0.59 (0.53 (0. Fv/Fm. C3 Sinapis alba. warm-season Glycine max Helianthus annus Lycopersicon esculentum C4 Zea mays Solanum bicolor Amaranthus retroflexus 20°C 25°C 30°C 2.24 (0.83 (0. Barua and Heckathorn. Fv/Fm. C3 Amaranthus retroflexus. Given that growth temperature is known to strongly influence the response and tolerance of Table 2.30 (0. qn. Fv/Fm. heat-stress temperature.72 (0.31) 0. 1991. NPQ.14 (0.. comparisons of the heat-stress responses of species not grown at their respective optimal (or sub. heat stress treatments in the previous studies varied Effects of growth temperature on whole-plant fresh mass.06 (0. ΦPSII Negative effects Roden and Ball.57 (0..27) 0. [N] No effects on biomass.34 (0. b.31) 1.. 8 d Amax.. but supraor suboptimal for others. 3 h Anet.13 (0. 1996b Cucumis sativus. Taub et al.78 (0. 3 h Fv/Fm... 1 d Abutilon theophrasti.00 (0. which were likely closer to optimal for some of the species examined.5 wk old postplanting (5 wks for C. C3 Eucalyptus rossii.28) 2.22) 0. ΦPSII Positive and negative effects. Amax.166 Table 1. bOther C species were included. 4 h Anet. C3 20°C 45°C. retroflexus).04) 0. negative on CAT Faria et al. Fv′/Fm′.05) 1. Fv′/Fm′. 1994 Coleman et al. quantum yield of PSII. 1988.61 (0.23) 35°C Note: Results are means (+1 SE). mixed effects on Taub et al.. . 4 h Amax. SOD. 3 (Coleman et al.29 (0.52 (0. 1996a Eucalyptus macrorhyncha.22) 0. 9 d Anet. gs Positive effects on Amax and recovery from water deficit and heat stress Ferris et al. net and maximum CO2 assimilation.. [Vol.41) 3. superoxide dismutase activity. C3 Yucca brevifolia. 4 h Amax. C3 Betula alleganiensis. C4 20°C Quercus suber.06) 1. gst. C3b 28°C 40°C. Weis and Berry. Fv/Fm. C3 25°C 45°C.09) 3. 1996 Fv/Fm Quercus suber.23) 3. NPQ Negative effects on Fv/Fm Roden and Ball. leaf N concentration. Bassow et al. gst.11) 2. CAT Positive effects on Amax. 1991 Notes: GT. 1999 Glycine max. gst. rubisco activity Positive effects on C assimilation and Faria et al.67 (0. gst. two different calculations of nonphotochemical quenching. C3 17°C 30°C.08) 2. A net max.g. but on which only basal PSII fluorescence was measured.or supra-optimal) growth temperatures may obscure response patterns that otherwise may be evident.08) 3.22) 2. a [N]..49 (0.26 (0. album and A. negative on [N] Source Bassow et al.

with a day length of 14 h and a light level of 1000 µmoles⋅m-2⋅s-1 PAR (photosynthetically active radiation) at the canopy level of plants. Plants were grown in 5-L pots in a 1:1:1 mixture of top-soil. to the 6th leaf stage in corn.. but negative in the C4. 25/17°C.g. Chenopodium album L. In a preliminary study with Pisim sativum (pea. Each data point represents the mean (±SD) of 4–6 independent replicates. Perry. and CAM species and both cool.wheat). 1999). species (Joshi. Plants were rotated at least once per week to avoid position effects in the chambers. In this study. cool-season C3) and Zea mays (corn. We also determined if CO2 effects on photosynthetic thermotolerance were associated with changes in stomatal or biochemical (especially electron transport) limitations to photosynthesis (e. lambs quarters. Sorghum bicolor L. Further. we grew and heat-stressed 11 species. and two CAM species (Agave americana L. 6 wk) in ambient or elevated CO2 until the early vegetative stage (e. effects of elevated CO2 on photosynthetic thermotolerance were positive in the C3. before and during a 4-h heat stress. 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. as well as at temperatures that reflect the natural conditions that each species will more typically encounter in the field. a subset (15–18) of uniformly Fig. All the species were grown under four temperature regimes (20/12°C. The agave and cactus species used are perennials. USA) equipped with light. and CO2 control. C4. sand. decreases in net photo- 167 synthesis during heat stress caused by stomatal closure at high CO2). corn or maize. All C3 and C4 species used are annuals and were germinated and grown (ca. Triticum aestivum L. from which photosynthetic data were collected... pigweed]... Iowa. making it difficult to directly compare across studies.. to help clarify the influence of elevated CO2 on the tolerance of photosynthesis to acute heat stress. Prior to treatment. at current or elevated CO2. 2006). 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. including C3. and for the cactus species to increase in diameter by ca. Ferocactus wislizenii Britt. 1..g. 25°C in C3 cool-season. century plant.. Plants were grown at both species-specific optimal preheat-stress growth temperatures and at 30°C (if optimal was different from 30°C). thereby allowing us to determine if any observed differences were related to photosynthetic pathway or to organismal heat tolerance. Table 2). and young (ca. & Rose. the species with the largest plants in this study). fish-hook cactus]. . 30/22°C and 35/27°C for day/night respectively.. 2 cm). 30°C in all other species). and only one study included CAM species (1 species in Huxman et al.. three warmseason C3 species [Glycine max L. Plants were grown at either ambient (370 ± 15 ppm) or enriched (700 ± 15 ppm) CO2.and warm-season C3 species. 1991). pea. Lycopersicon esculentum L. 1998). and perlite and placed in growth chambers (E-36HO.. However.. The dotted lines for the C3 cool-season species are for plants grown at 30°C .February 2008] Wang et al. warm-season C4). but photosynthesis was not measured in this study.. including three cool-season C3 species (Pisum sativum L.—Effects of elevated CO2 on thermotolerance widely in both intensity and duration (Table 1). exposed to 370 (dark circles) or 700 ppm CO2 (light circles). sorghum. Helianthus annuus L. soybean. (Moench). Percival Scientific. to permit comparisons at both a common temperature regime. CAM species were also grown at 38/30°C) to determine species-specific optimal (or near-optimal) temperatures (based on biomass. sunflower. three C4 species (Zea mays L. tomato). temperature. only one previous study included C4 species (1 species in Coleman et al. MATERIALS AND METHODS Plant material and growing conditions—Eleven species were examined in this study. Amaranthus retroflexus L. Time course of net photosynthesis (Pn) in nine species grown at species-specific optimal daytime prestress temperatures (solid lines.

Ci. and qp as dependent variables (*significance at α = 0.8** 0.8 11.4 1. album. Walz. Ci.1** 24. Cary. and then measured to determine pH. USA) was used to test for significant effects of CO2. 2004). Fv′/Fm′ and qp for C3 and C4 species.0 Time CO2 Time × CO2 Fv′/Fm′ Time CO2 Time × CO2 qp Time CO2 Time × CO2 20.6* 4.3 31.7* 2.8** 14.. Prior to this stress.1** 26.8** 391.5** 14. warm-season C3.8** 160.1** 3. Basal fluorescence (Fs) under steady-state illumination (900 µmol·m-2⋅s-1 PAR) was measured initially.9 0. mays S.5* 0.1** 11. as described in Heckathorn et al. and functional types (cool-season C3.5 5. All results were collected from recently expanded. Plants were measured before and during heat stress. CAM species photosynthetically fix CO2 at night into malic acid. a light level of 1000 µmol⋅m-2⋅s-1 PAR (ca.4** 1.6** 3.9** 29. Fv′/Fm′. all plants were at similar stages of development (e.4** 0.1. (1996). Effeltrich.2 13.3** 11. net CO2 exchange) of leaves was measured with a portable photosynthesis–transpiration system with an infra-red gas analyzer (model 6400.5 13. retroflexus 2.0 11.8** 12. aestivum at 30°C (not shown).9** 252.4 5. Table 3. Unless indicated otherwise.1** 3.2** 39.3** 5. aestivum G. Pocasset. USA). the near-optimal growth temperature for the cool-season C3 species was ca.2** 1. fully lit leaves of intact plants. heat stress duration (control. and their interactions as independent factors.2 0.9** 7. LiCOR.g.2** 5.6* 1. Posthoc Tukey honestly significant difference (HSD) tests were run on specific contrasts to examine significant treatment effects among groups (JMP software).1** 2. Photosynthesis measurements—Steady-state net photosynthesis (Pn.6* 17.1* 0. and qp as dependent factors and CO2.0** 7.0-s pulse of saturating white light (>5000 µmol⋅m-2⋅s-1 PAR).8** 9.5 4.1 15.3** 0. 4 h of heat stress).6** 5.6** 94.0** 48. and they decarboxylate this CO2 during the day and use it and ATP and NADPH from the light reactions to produce sugars.3** 45.5** 1571. heat-stress duration. these results were compared to results with logtransformed data and results of partial-correlation analysis. which yielded similar conclusions. Chlorophyll fluorescence was measured in unstressed control plants and on HS plants during heat stress at 1000 and 1300 hours. SAS Institute. USA) between Pn and gst. and their interaction on Pn.6** 99. For the CAM species.2** 0. respectively. and at species-specific growth temperatures. North Carolina. Subsamples of tissue were later ground completely with a mortar and pestle. equipped with a 250-mm3 leaf chamber.05.7* 0.2** 99.9 20. Pn was measured twice at 1000 and 1300 hours.4** 2.8** 5.4 124. and C4) as independent factors. and Pn.4** 1.8** 2.1 software.3* 0. To examine heat effects on PSII and post-PSII electron transport.4** Time CO2 Time × CO2 6. Fv′/Fm′ and qp were then calculated as in Genty et al.2 95.4** 15.9** 9. esculentum Z. gst. Heat-stress treatments—Heat-stress treatments were applied during vegetative growth. North Carolina. C.4** 28.4 24.168 [Vol. Ci.5 39. Absolute data were used in correlation analyses (SAS version 9. If heat stress affected net CO2 fixation in the CAM species. Cary. 1 h of heat stress. gst.1** 58.5 0. with 5–6 plants in each group. 95 American Journal of Botany sized plants of each species was selected within each chamber for further use.6* 2. 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).3 0.3** 2. followed by maximum fluorescence (Fm′) after a 1.9 16. at the same CO2 levels at which the plants were growing (either 370 or 700 ppm CO2). CO2.5* 2.5 10. 30°C for the warm-season C3 and the C4 species. and again after stabilization of CO2 and H2O flux to ensure that photosynthetic responses reflected those within the growth chambers. (1989). similar number of leaves).2** 10. F values Variable P.0 0. Chamber temperatures in all treatments were monitored using Hobo Dataloggers and probes (Onset Corp.1* 100.9 15.3 6.8** 20. RESULTS On the basis of the seedling biomass for species grown at different temperatures (Table 2). Minimum fluorescence (Fo′) was then measured after turning off both actinic and flash light-sources.0** 38.4** 3. Ci. equal to that at the tops of the plants).1** 13.7** 5.9** 4. annus Time CO2 Time × CO2 38.3** 38.01).1 1. The controls were not heat stressed.1** 45.8** 269.2 2. Three-way ANOVAs were also conducted among C3 and C4 species to determine whether CO2 effects differed as a function of different photosynthetic groups.7** 8. album T.5** 2. Germany). and T. Lincoln.9* 32.9 17.2** L.9** 0. so that plants were not water or nutrient limited. diluted with 10 mL of deionized water. 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.6 93. sativum C.4** 6. lowering tissue pH throughout the night in the absence of other large pools of acid. Fv′/Fm′.7 91.0** 906.1 22.1 0.9** 77.1 101. and within each species. Nebraska.6 2.7 0. plants in each chamber were randomly assigned to one of two groups (control = C and heatstress = HS). During heat stress. **significance at α = 0.9 172. Results from analysis of variance (F values) for treatment effects in each species at their species-specific optimal growth temperature. and qp through the time course of the high-temperature period. gst. with time (duration of heat stress). and qp = (Fm′ − Fs)/(Fm′ − Fo′). max H. Measurements were made within 1–2 min of insertion of leaves into the cuvette. Massachusetts. thereby increasing cell pH throughout the day (Taiz and Zeiger. SAS Institute.7 8.7** 14. PSII efficiency (Fv′/Fm′) and photochemical quenching (qp) in light-adapted leaves were monitored by analysis of chlorophyll fluorescence using a pulse-amplitude modulated (PAM) fluorometer (model PAM 101/103.1** 11.0 0.5* 13. . and HS plants were heat stressed at 15°C higher than daytime growth temperatures from 9:00 am to 1:00 pm.1* 65.2** 488.0** 28.0** 2.2** 16.0 Pn gst Ci Note: Similar results were obtained for P.1 0. where Fv′/Fm′ = (Fm′ − Fo′)/Fm′.6* 143. Analyses were conducted within each species to determine whether the physiological variables differed as a function of different treatments. All the pots were watered as needed and fertilized regularly (every other week with a commercial complete nutrient mix). 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.3 3.2** 185. Therefore.2** 7.2** 10.8 1.3** 16.1** 4.0 2. See Table 2 for full names of species. Fv′/Fm′. Plants were harvested at the end of the heat-stress treatment and immediately frozen and stored at −70°C.6 3. 25°C and was ca.. bicolor A.7** 118.6** 229. sativum.8** 5. USA). a split-plot two-way ANOVA (JMP 5. with Pn.9** 4.

2. As expected. soybean. while C4 species had little stimulation of Pn in elevated CO2 (Fig. 4). heat stress significantly decreased Fv′/Fm′ in all species. exposed to 370 (dark circles) or 700 ppm CO2 (light circles). the decreases in Pn caused by AHS were more pronounced in plants grown at elevated CO2 than in those grown at ambient CO2. Pn decreased significantly in all species (Table 3). rather than increases in stomatal limitations. the positive effects of elevated CO2 on Pn during AHS were evident both for plants grown at optimal daytime growth temperatures before AHS and for plants grown at 30°C before AHS. prior to initiation of acute heat stress (AHS). Heat stress significantly decreased qp in five of nine species. plants grown at elevated CO2 had a lower gst than plants at ambient CO2. 1). and biologically significant decreases were observed only in chenopodium and in pea at 25°C in high CO2. C3 species (except for wheat at 25°C and chenopodium at 30°C) grown at elevated CO2 had a significant stimulation of Pn compared to ambient CO2. Elevated CO2 had a negative effect on qp for nearly all species (except chenopodium at 25°C). For the cool-season C3 species. and sunflower at both 25° and 30°C). except in wheat at 25°C and tomato (Fig. 2. before and during a 4-h heat stress. with additional decreases in Pn with continuing heat stress. The dotted lines for the C3 cool-season species are for plants grown at 30°C. (i. pigweed). And for all species (except for sorghum).e. the stimulatory effects of high CO2 were not as great at the higher growth temperature. Fig. ambient CO2. wherein heat stress both increased relative stomatal limitations to photosynthesis and damaged photosynthetic metabolism (discussed later). the quantum efficiency of PSII (Fv′/Fm′) was not significantly different in plants grown at elevated vs.February 2008] Wang et al. Ci was increased by AHS in seven of nine species (Fig. During heat stress. . except soybean (note that decreases were small and transient in wheat at 30°C and in tomato) (Table 3). such that after 4 h of AHS. As with Pn. 5. which means that the capacity of these species to keep PSII reaction centers in an open configuration was decreased by heat stress. plants grown at elevated CO2 had a higher Ci than plants at ambient CO2. before the initiation of AHS. elevated CO2 had a negative effect on Fv′/Fm′ in the C4 species. Table 3). respectively. Each data point represents the mean (±SD) of 4–6 independent replicates. negative effects on chenopodium and pea at 30°C. Similar to 169 gst. Table 3). Time course of stomatal conductance to water vapor (gst) in nine species grown at species-specific optimal daytime prestress temperatures (solid lines. Table 3). decreases in Pn during AHS were caused by negative effects on photosynthetic metabolism. In contrast to Pn. Hence.—Effects of elevated CO2 on thermotolerance in subsequent experiments. and no effects on wheat at 30°C. For the C4 species. decreases in Pn were observed for most species. in all species except for chenopodium. but had no consistent effects on C3 species. For all species but pigweed. 25°C in C3 cool-season.. however. Stomatal conductance increased or remained essentially unchanged by AHS for all species except for small decreases (absolute and relative to Pn) in chenopodium (25° and 30°C) and wheat (30°C) (Fig. Patterns similar to Fv′/Fm′ were found for qp (Fig. 3. 30°C in all other species). Within 1 h of AHS. though the CO2 effects were biologically insignificant for some species (soybean. pea at 25°C. positive effects on tomato and wheat at 25°C. indicating heat-stress effects on postPSII electron transport. 25°C and 30°C were used as the optimal daytime growth temperatures for cool-season C3 and warm-season C3 & C4 species. indicating that the decreases in Pn during heat stress were not caused by stomatal closure (as confirmed later). sunflower.

Pn was positively correlated with gst. Pn was positively correlated with Fv′/Fm′ before and during heat stress and with qp only during heat stress. but was again positively correlated with gst. 3. In contrast. Each data point represents the mean (±SD) of 4–6 independent replicates. Importantly. exposed to 370 (dark circles) or 700 ppm CO2 (light circles). and (especially) qp after 4 h of heat stress (and weakly negatively correlated with Ci). Fv′/Fm′. a positive effect on Fv′/Fm′ and qp at 30/23°C. Elevated CO2 effects on the tolerance of Fv′/Fm′. only pH was decreased by AHS. not to organismal thermotolerance (confirmed by three-way ANOVA. though the effect on Fv′/Fm′ and qp were transient for cactus. Small but significant negative effects of high CO2 were also observed on chlorenchyma pH in heatstressed plants of the CAM species (high growth temperature only). and pH for both agave and cactus. Φet = Fv′/Fm′⋅qp. 95 American Journal of Botany Fig. qp. For both agave and cactus. and because the quantum yield of PSII electron transport (Φet) is the product of the efficiency of PSII and the fraction of open PSII (i.. but decreased thermotolerance of Pn in C4 species. CO2 effects were related to photosynthetic pathway. suggesting that net photosynthesis was negatively impacted by high CO2 during heat stress for CAM plants. and qp before heat stress (especially Fv′/Fm′). and pH during AHS at 25/18°C and 30/23°C. Time course of leaf internal CO2 concentration (Ci) in nine species grown at species-specific optimal daytime prestress temperatures (solid lines. qp. and chlorenchyma pH for CAM species were assayed at three temperatures because of the lack of biomass data to determine optimal growth temperatures (Fig. For agave. and qp) was conducted (for C3 and C4 data only) to determine which variables were correlated with Pn and whether the relationships changed with heat stress (Fig. was not correlated with any of the other variables after 1 h of heat stress. before and during a 4-h heat stress. but pH was significantly decreased for agave and cactus (Fig. elevated CO2 decreased Φet during AHS in all species but tomato. hence. 7). 8). CO2 had no effect on Fv′/Fm′. qp. Ci. For cactus. Fv′/Fm′.. AHS did not decrease Fv′/Fm′ or qp for either agave and cactus (Fig. Genty et al. such that high CO2 decreased pH relative to either low CO2 in heat-stressed plants (agave) or relative to high-CO2 controls (cactus).01 for .170 [Vol. and pH were decreased by AHS for agave after 4 h. For C3 species. 25°C in C3 cool-season. At 30/23°C. AHS decreased Fv′/Fm′. and pH at 25/18°C. Fv′/Fm′. 1989). Fv′/Fm′. At 25/18°C (day/night). The dotted lines for the C3 cool-season species are for plants grown at 30°C. where P < 0.and warm-season species. Correlation analysis between Pn and the other photosynthetic variables (gst. elevated CO2 had negative effects on either Fv′/Fm′ or qp during AHS in all species. 6). At 35/28°C. but had a negative effect on qp at 35°C and a positive effect on pH (in controls). CO2 had no significant effect on Fv′/Fm′. 30°C in all other species). there was a significant interaction between CO2 and heat stress at 35°C. but for cactus. for the C4 species. DISCUSSION Elevated CO2 increased the tolerance of net photosynthesis (Pn) to acute heat stress in C3 species. Table 4). but a negative effect on Fv′/Fm′ and qp for plants grown at 35/28°C. 6–7.e. but was negatively correlated with Ci before and during heat stress and with gst before heat stress. qp. qp. Increases in Pn thermotolerance with high CO2 in C3 species were observed in both cool.

. both before heat stress and after 4 h of heat stress. 4. and electron transport became an important limitation later in the heat-stress treatment. but was likely limited (or colimited) by damage to electron transport at some point in the heat stress period. stomatal limitations to Pn increased during heat stress in only two species examined.and cool. the interactive effect of functional types and CO2. in the cool-season C3 species grown at optimal + 5°C = 30°C). 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).season species). but with both PSII and post-PSII efficiency during heat stress. Interestingly. the relative benefits of elevated CO2 on Pn thermotolerance were significantly reduced in the C3 species grown at supra-optimal prestress growth temperatures (i. the strength of the correlation between Pn and electron transport decreased with duration of heat stress (i.g. Notably. no such correlation was observed after 1 h of heat stress. yet.February 2008] Wang et al. as might be expected. suggesting the possibility that the relative importance of electron transport in limiting Pn during heat stress decreased with the duration of heat stress. such that PSII quantum yield (ΦPSII) decreased with high CO2 in all species (including the two CAM species) but one (tomato. across species. 1996a). Pn was only correlated with PSII efficiency before heat stress. during heat stress. C3). before and during a 4-h hea stress. In agreement with this. However. hence. Time course of photosystem II efficiency (Fv′/Fm′) in nine species grown at species-specific optimal daytime prestress temperatures (solid lines. The correlation analyses also indicated that. Pn was not limited by gst or Ci during heat stress in either C3 or C4 species.e. Together. In contrast. the effects of elevated CO2 on Pn thermotolerance were caused by negative effects of high CO2 on photosynthetic metabolism in the majority of species. rubisco activity via rubisco activase) limited Pn early in the heat stress. either by decreasing the efficiency of PSII (Fv′/Fm′) and/or by decreasing the performance of post-PSII electron transport relative to PSII (qp). Pn was strongly correlated with electron transport (both PSII and post-PSII). of heat stress).—Effects of elevated CO2 on thermotolerance 171 Fig. and then 4 h. Also. 30°C in all other species). Pn was strongly correlated with electron transport before and during heat stress in both C3 and C4 species. rather than by CO2-induced decreases in stomatal conductance. Although elevated CO2 decreased stomatal conductance in most species. not significant when comparing C3 warm. exposed to 370 (dark circles) or 700 ppm CO2 (light circles). from time 0. Although Pn was positively correlated with gst prior to heat stress in C3 species. these results suggest that the benefit of elevated CO2 to Pn 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. Given that photorespiration increases with temperature and that C3 species have high levels of photorespiration . 25°C in C3 cool-season..e. in C3 species. Each data point represents the mean (±SD) of 4–6 independent replicates. in C4 species. in C4 species. In contrast. to 1 h.. elevated CO2 decreased the thermotolerance of electron transport. but gst and Ci did not generally decrease). indicating that some aspect of photosynthesis other than electron transport (e. The dotted lines for the C3 cool-season species are for plants grown at 30°C. Pn was mostly not (or even negatively) correlated with gst and Ci during heat stress in both C3 and C4 species (because Pn decreased in all species during heat stress.

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. . 5. Heat stress effects on Fv′/Fm′ and qp of CAM species (agave and cactus) grown at 25. Taiz and Zeiger. 30°C in all other species). 95 Fig. before and during a 4-h heat stress. Time course of photochemical quenching (qp) in nine species grown at species-specific optimal daytime prestress temperatures (solid lines. 6. exposed to 370 (dark circles) or 700 ppm CO2 (light circles). compared to C4 and CAM species (Sage and Monson. exposed to 370 (dark circles) or 700 ppm CO2 (light circles). 1999. 25°C in C3 cool-season. and 35°C daytime prestress temperatures. This prediction is supported by the relative decrease in the benefits of elevated CO2 to Pn in the cool-season C3 species grown at supraoptimal prestress growth temperatures (30°C) Fig. before and during a 4-h heat stress. 2004). Each data point represents the mean (±SD) of 4–6 independent replicates. The dotted lines for the C3 cool-season species are for plants grown at 30°C. 30. Each data point represents the mean (±SD) of 4–6 independent replicates.172 American Journal of Botany [Vol.

.. Williams et al. in a future warmer world with increases in both mean and extreme temperatures.0 556. as in this study.3 1. hh: 700 ppm CO2..2** 4.3* Time × CO2 0. 30.6** 0. 1998).5** 0. the carotenoids (especially zeaxanthin) (Havaux. 7. Huxman et al.4 0. so negative effects of elevated CO2 on photosynthetic electron transport in C3 species should begin to limit Pn during acute heat stress at temperatures over ca. 1999.8 6.4 0..1 4. 1998). including cellular adaptations conferring plant tolerance to acute heat stress. qp. The positive effect of elevated CO2 on net photosynthetic (Pn) thermotolerance in C3 species have also been observed in other studies (Faria et al. lh: 370 ppm CO2.7** 1. with heat stress.8** 53. positive. 2000. 1. with time (for Fv′/Fm′.. 1996a. heat = heat treatments (control. and their interactions as independent factors. and in only one CAM species was the effect studied (neutral effect.2* 392... 1998. 2002). Results from analysis of variance (F values) for treatment effects in CAM species at three growth temperatures. 1998). Taub et al.4 1. negative. without heat stress.9** 0.. and negative effects of high CO2 during heat stress on biomass were observed for three C3 tree species (Bassow et al. Agave americana Variable 25°C 30°C Fv′/Fm′ 0.8 7. Hamerlynck et al.5** CO2 0. Huxman et al. As in this study.4 43. Feller et al.9 7.9** 0. Growth at elevated CO2 profoundly alters cellular and subcellular concentrations of many soluble compounds (Poorter et al.0 0.. Wang and Heckathorn.5* qp Time 8. 1998.5* 0. whereas Huxman et al. and Fv′/Fm′. Crafts-Brandner and Salvucci.1* pH Heat 397. 1998). according to Tukey HSD test). Each bar represents the mean (±SD) of 3–4 independent replicates. heat-shock proteins (Heckathorn et al. 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. 1998.0 0.2** CO2 0.8** synthetic thermotolerance in C4 species was not previously studied. wherein high CO2 decreased Fv /Fm during heat stress (Huxman et al.2 0. protective solutes.3 0.0 Time × CO2 0. and pH as dependent variables. CO2. negative effects of high CO2 on photosynthetic heat tolerance were also observed for C3 species (Roden and Ball. b. hc: 700 ppm CO2. suggesting that negative effects of elevated CO2 on heat tolerance of electron transport may be generalized to heat stress of various durations. Hamerlynck et al. And. 1996a. Thus. For example. 4-h heat stress) harvested at the same time at end of the treatment period (*significance at α = 0.. Further experiments are needed to supply direct evidence of an association between.6** 42. Heat stress effects on chlorenchyma pH of CAM species (agave and cactus) grown at 25. only one CAM species had been examined. in the two previous studies to measure quantum yield of electron transport (ΦPSII). and CO2-related changes in these heat-stress adaptations will likely impact photosynthetic thermotolerance.2 0..1** 17.9 6. Different letters above the bars indicate a significant difference among treatments at the same temperature (P < 0.2* CO2 Time × CO2 1. Tognetti et al..4** 11. and neutral effects of elevated CO2 on heat tolerance of Fv /Fm have been observed in C3 species (no C4 species examined) (Faria et al. 1994). 2000). 2000. 1998. qp) or heat (for pH). or 4 h). 35–40°C. for example.4 7. (1998) found that growth at elevated CO2 increased saturation of some classes of thylakoid lipids. heat shock protein content is decreased at low N and at high CO2 in leaves (Heckathorn et al. Both increases and decreases in isoprene emission have been reported for plants grown under elevated CO2 (Sharkey et al. 1997. 2005) are known to confer photosynthetic thermotolerance. 1998).0 6.8** Time 0.1 0.1 7.7 5. 1996.8** 0.4** 44..and warm-season species (Eckardt and Portis. (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. Roden and Ball.0 9. 2004).3 0.February 2008] Wang et al. Previously. Huxman et al.. 2000). 1998. 1997). to determine if high-CO2-related . Also.. protective compatible solutes (Williams et al. 35–40°C in representative cool.0 Ferocactus wislizzenii 35°C 25°C 30°C 35°C 81. Taub et al.05. lipid saturation level (Larkindale and Huang. the negative effects of elevated CO2 on electron transport may commonly limit Pn in C3. without heat stress. compared to those grown at optimal temperatures (25°C). 1996. and thermotolerance at elevated CO2. 1991. elevated CO2 decreased thermotolerance of ΦPSII in all species (four C3.0 0. heat shock proteins.. one CAM) (Roden and Ball. there are other aspects of metabolism that are affected by growth under elevated CO2. 1996. 2000). Huxman et al. isoprene.. The CO2 effects on photo- Table 4. with heat stress). as well as in C4 and CAM species. **significance at α = 0. subjected plants to a maximum daily temperature of 55°C for 9 d). 1999.9** 0. and isoprene production (Velikova and Loreto. similar to this study. A notable difference between the current study and Huxman et al.6 3.. In previous studies. lipid changes.8 4.2 22. depending on species. Ferris et al.6 34. In addition to photorespiration. in one of two species.. unpublished manuscript)..6** 0. Time = duration of heat stress (0. and 35°C daytime prestress temperatures after a 4-h heat stress (lc: 370 ppm CO2.01). 1996a). yet the two studies obtained similar results.—Effects of elevated CO2 on thermotolerance 173 Fig.05. 1992).

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