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. 2021 Oct 8;27(10):2345–2355. doi: 10.1007/s12298-021-01080-5

Elevated carbon dioxide offers promise for wheat adaptation to heat stress by adjusting carbohydrate metabolism

Aneela Ulfat 1,2, Ansar Mehmood 2,✉, Khawaja Shafique Ahmad 2, Sami Ul-Allah 3
PMCID: PMC8526630  PMID: 34744370

Abstract

Carbohydrate metabolism in plants is influenced by thermodynamics. The amount of carbon dioxide (CO2) in the atmosphere is expected to rise in the future. As a result, understanding the effects of higher CO2 on carbohydrate metabolism and heat stress tolerance is necessary for anticipating plant responses to global warming and elevated CO2. In this study, five wheat cultivars were exposed to heat stress (40 °C) at the onset of anthesis for three continuous days. These cultivars were grown at two levels of CO2 i.e. ambient CO2 level (a[CO2], 380 mmol L−1) and elevated CO2 level (e[CO2], 780 mmol L−1), to determine the interactive effect of elevated CO2 and heat stress on carbohydrate metabolism and antioxidant enzyme activity in wheat. Heat stress reduced the photosynthetic rate (Pn) and grain yield in all five cultivars, but cultivars grown in e[CO2] sustained Pn and grain yield in contrast to cultivars grown in a[CO2]. Heat stress reduced the activity of ADP-glucose pyrophosphorylase, UDP-glucose pyrophosphorylase, invertases, Glutathione reductase (GR), Peroxidase (POX), and Superoxide dismutase (SOD) at a[CO2] but increased at e[CO2]. The concentration of sucrose, glucose, and fructose mainly increased in tolerant cultivars under heat stress at e[CO2]. This study confirms the interaction between the heat stress and e[CO2] to mitigate the effect of heat stress on wheat and suggests to have in-depth knowledge and precise understanding of carbohydrate metabolism in heat stressed plants in order to prevent the negative effects of high temperatures on productivity and other physiological attributes.

Supplementary Information

The online version contains supplementary material available at 10.1007/s12298-021-01080-5.

Keywords: e[co2], a[co2], Heat stress, Wheat, Carbohydrates, Invertases

Introduction

Rapid global climate change has increased atmospheric carbon dioxide (CO2) in the last two centuries (Xu et al. 2013), and it is expected to become more frequent and intense in the future. CO2 levels, for example, are expected to rise to 550 ppm by 2050 (Barriopedro et al. 2011). Being a substrate for photosynthesis, elevated CO2 (e[CO2] increases the photosynthesis and enhances the plant biomass and grain yield of many field crops (Amthor 2001; Yang et al. 2007; Hogy et al. 2009; Madan et al. 2012). In addition to photosynthesis, e[CO2] also improves water use efficiency by lowering stomatal conductance at one end and reducing transpiration at the other end (Ainsworth and Rogers 2007). The e[CO2] is broadly beneficial for plants, but it is also a major contributor to the global temperature rise as an anthropogenic greenhouse gas (Erice et al. 2006). Heat stress affects crop development, productivity, and food security, resulting in a billion dollar loss in agriculture globally (Źróbek-Sokolnik 2012; Fahad et al. 2017).

Climate models anticipate high heat stress events as a result of global warming, which will have a substantial impact on crop growth and productivity around the world (Semenov and Shewry 2011). The rate of photosynthesis, PSII photochemical efficiency, and biomass production are all directly related to temperature (Ogweno et al. 2009; Ding et al. 2010; Williams et al. 2013). In addition to inhibiting photosynthetic rate, heat stress reduces the availability of carbohydrates for energy and carbon skeletons to sustain plant growth (Wardlaw et al. 2002). Heat stress also affects protein stability, causing misfolding and breakdown of protein structures, resulting in a reduction in the efficiency of enzymatic activity and an unbalanced metabolism in plants (Saidi et al. 2011; Mittler et al. 2012; Merewitz et al. 2012). Variations in temperature also cause membrane damage (Larkindale & Knight, 2002), and programmed cell deaths (Distéfano et al. 2017), resulting in reduced plant productivity.

Studies reported that e[CO2] can mitigate the effects of abiotic stress particularly heat stress in plants (Hamilton et al. 2008; Prasad et al. 2009). Under e[CO2], temperature tolerance of photosynthesis increases because of an increase in the maximum rate of carboxylation due to change in rubisco protein at higher temperatures (Alonso et al. 2008; Wang et al. 2008a, b). Chavan et al. (2019) found that e[CO2] mitigated the effect of heat stress on photosynthesis and biomass of wheat. Similarly, e[CO2] reduced the negative impact of high temperature in Kentucky bluegrass by maintaining the carbon balance and accumulating of carbohydrates (Song et al. 2014). Shanmugam et al. (2013) reported that e[CO2] significantly mitigate the effect of heat stress on photosynthetic rate and carbohydrate contents in wheat cultivars. Likewise, a mitigation effect of e[CO2] against drought and heat stress was found on grain yield of wheat (Li et al. 2019). However, some studies reported a non-mitigation effect of e[CO2]. For example, Zhang et al. (2018) found a decrease in photosynthetic rate, antioxidant enzyme activities, and grain yield in wheat under e[CO2] and heat stress in combination. Additionally, e[CO2] was found unable to fully compensate the negative effects of heat stress on biomass and yield in rice and wheat, rather yield was decreased in e[CO2] under heat stress (Cai et al. 2016). However, other studies have found that while e[CO2] improves photosynthesis and shoot development, it suppresses dark respiration and photorespiration (Leakey et al. 2006; Reddy et al. 2010). These findings suggest that plant responses to e[CO2] and heat stress interactions are not simply predictable, and the mitigation effect of e[CO2] on heat stress could depend on concentration of CO2, severity of stress, and plant species and cultivars specific (Ewert, et al. 2002; Suzuki et al. 2014).

Wheat is one of the most used staple foods in the world. It is extremely sensitive to high temperature, particularly in terms of carbohydrate and antioxidant metabolism, which ultimately affect the grain yield (Liu et al. 2016; Weichert et al. 2017). Therefore, it is critical to look at how different wheat cultivars respond to climatic change, such as e[CO2] and high temperature. In this study, we studied five wheat cultivars (AAR-11, Chakwal-50, Shahkar, Pakistan-13, and FSD-08) subjected to e[CO2] and heat stress at the onset of anthesis and investigated the carbohydrate and antioxidant metabolism and grain yield. The primary aim was to evaluate the response of wheat to heat stress under both ambient CO2 (a[CO2]) and e[CO2]. Secondly, to observe whether e[CO2] can mitigate the damaging effect of heat stress by adjusting carbohydrate and antioxidant metabolism.

Materials and methods

Experimental setup

A pot experiment was performed in the CO2-controlled greenhouse of the University of Copenhagen. Each pot was 10 cm in diameter and 40 cm in depth. The pot was filled with peat material (0–20 mm, Pindstrup 2, Pindstrup Mosenurg A/S, Ryomgaard), composed of sphagnum, 32% organic matter, 5.6–6.4 pH and 0.45 ms cm−1 electric conductivity. Five wheat cultivars, viz. AARI-11, Chakwal-50, Shahkar, Pakistan-13, and FSD-08, were obtained from NARC Islamabad, Pakistan. Four of the selected genotypes (Chakwal-50, Shahkar, Pakistan-13, and FSD-08) were stress tolerant and one of them was sensitive cultivar (AARI-11). Five seeds of each cultivar were sown per pot with five replicates under greenhouse conditions with (380 mmol L−1) ambient, (780 mmol L−1) elevated CO2 level, relative humidity ranged from 50 to 60%, 16 h day length, and day/night temperature of 15/10 °C. In addition to natural light, supplemental light was provided when natural light intensity was dropped below 30 µmol m−2 s−1. Supplemental light was turned off when the natural light level came back to 90 µmol m−2 s−1. The pot was irrigated through automated irrigation available in the greenhouse. From sowing, half of the plants were exposed to ambient CO2 (a[CO2]) concentration (AC, 380 mmol L−1), and elevated CO2 (e[CO2]) concentration (EC, 780 mmol L−1). Pure CO2 was released from a bottling tank to get enriched CO2 concentration and distributed through channels in the whole greenhouse. When the plants reached the anthesis stage Zadoks- code 61, half of the plants from a[CO2] and half of the plants from e[CO2] were transferred to the high-temperature chamber for 3-day heat stress conditions of 40 ºC during both day and night (Zadoks et al. 1974). During the heat stress, relative humidity was 70% and photosynthetic photon flux density (PPFD) was maintained at 200 µmol m−2 s−1. A total of four treatments were established as a[CO2] (AC), e[CO2] (EC), a[CO2] + heat stress (AC + H), and e[CO2] + heat stress (EC + H). The sampling was done after the three days of onset of anthesis Zadoks-code 61.

Carbohydrate metabolic and antioxidant enzymes activity

To determine the mobilization of carbohydrates and antioxidant enzyme activity, top and fully expended flag leaf was taken at Zadoks code 61 (Zadoks et al. 1974) because flag leaf contributes 80% in photosynthesis. Sampling was done from both controlled and heat stressed samples. Sampled leaves were harvested in liquid nitrogen. All extraction steps were performed in the ice at 4 °C following a standard procedure proposed by Bisswanger (2004). Ice-covered samples were ground in liquid nitrogen with 0.1% polyvinylpolypyrrolidone (PVPP). For extraction, 500 mg material was used with extracted buffer 1 mm, 1 mM EDTA, 3 mM MgCl2, 40 mM TRIS–HCl, 24 μM Nicotinamide adenine dinucleotide phosphate (NADP), 1 mM benzamidine, 0.1 mM phenylmethylsulfonyl fluoride (PMSF), and diluted β-mercapto-ethanol 14 mM. The homogenate was centrifuged at 8000 rpm to obtain pellet at 4 °C for 5–20 min. The supernatant was centrifuged at 8000 rpm for 20 min at 4 °C to remove all impurities. Distilled water was used to wash pellets and then sodium chloride buffer 1 mL was added and stored overnight at 4 °C. Both supernatant and pellet (after washing) were dialyzed overnight against 20 mM potassium phosphate buffer (pH 7.4) at 4 °C. These extracts were used for different enzymatic assays.

Enzymatic assays

All the enzymatic assays were performed in a 96-well microtiter plate reader (Ascent Multiskan; Thermo Fisher Scientific, Waltham, MA, USA) in a UV-transmissive single-use microcuvettes (Plastibrand®; Brand, Wertheim, Germany) with different volume concentrations of extracts (up to 25 μL) and a total reaction volume of 160 μL in a spectrophotometer (U-3000; Hitachi, Tokyo, Japan). Assays were subsequently adapted to a 96-well microtitre plate format. For all measurements, aliquots (up to 25 μl) of the different extracts were incubated in a plate reader (Ascent Multiskan; Thermo Fisher Scientific) at 30 °C for 40 min in UV-transmissive flat bottom 96-well plates (UV-Star;Greiner Bio One, Kremsmünster, Austria) in a total reaction volume of 160 μL with a mixture of buffer components, substrate(s), auxiliary substance(s), and auxiliary enzymes and absorbance at 340 nm was monitored throughout the entire period of incubation. All assays were carried out in triplicate. For control reactions, substrate was neglected. The change in absorbance per second during the linear phase of substrate conversion was used as the basis for the calculation of specific enzyme activity in nkat g–1 FW.

Activities of enzymes ADP-glucose pyrophosphorylase (ADGPase), UDP-glucose pyrophosphorylase (UDGPase), cell wall invertase (CwInv), vacuolar (vacInv), cytoplasmic (cytInv), Glutathione reductase (GR), Peroxidase (POX) and Superoxide dismutase (SOD) were determined. For ADGPase activity, in each well, the extract was mixed with 100 mM Tris–HCl (pH. 8.0), 1 mM NADP, 0.44 mM EDTA, 5 mM MgCl2, 1.28 U of G6PDH, 0.1% BSA, 2 mM ADPGlc, 1.5 mM PPi, 2 mM 3-PG and 0.432 U of PGM (Pelleschi et al. 1997), incubated in plate reader at 30 °C for 40 min and absorbance was measured 340 nm. The specific activity is expressed as nkat g–1 FW. For UGPase activity, the dialyzed extract was mixed with 100 mM Tris–HCl at pH 8.0, 0.44 mM EDTA, 5 mM MgCl2, 0.1% BSA, 2 mM UDPGlc, 1.5 mM PPi, 1 mM NADP, 0.432 U of PGM, 2 mM 3-PG and 1.28 U of G6PDH (Pelleschi et al. 1997; Appeldoorn et al. 1999) and incubated at 30 °C for 40 min in a plate reader. In control samples, UDPGlc was not used. The absorbance was measured at 340 nm and results are presented as nkat g–1 FW.

Invertase activity was assayed with the help of the standard procedure of Sung et al. (1989). For cell wall invertase (CwInv) , vacuolar invertases (VacInv) and cytoplasmic invertases (CytInv) dialyzed extract was used. Flat bottom 96-well plates with 5 μL of 100 mM sucrose and 5 μL of reaction buffer pH 4.5 and 6.8 were used and the final volume of 50 μL was made by adding distilled water and incubated at 37 ºC. 200 μL of GOD-POD reagent (10 U mL–1 GOD, 0.8 U mL–1 POD, and 0.8 mg mL–1 ABTS in 0.1 M potassium phosphate buffer, pH 7.0) was added after 30 min of incubation. The absorbance of each sample was measured at 405 nm in a plate reader (Ascent Multiskan; Thermo Fisher Scientific, Waltham, MA, USA) and specific activity was expressed as nkat g–1 FW.

For the determination of GR activity, a method adopted by (Edwards et al. 1990) was used. Dialyzed extract was mixed with 100 mM Tris HCl pH 7.8, 0.2 mM NADPH, and 0.6 mM glutathione oxidized (GSSG) and incubated at 30 °C for 40 min. In the control, GSSG was omitted. Absorbance was recorded at 340 nm, and the slope of the curve representing the disappearance of NADPH was recorded. The specific activity was expressed in nkat g–1 FW. For POX activity, a method proposed by Rang et al. (2011) was used. Dialyzed extract was mixed with 100 mM buffer pH 7, guaiacol 20 mM, and 10 mM H2O2. For the control reaction, H2O2 was omitted. The samples were inubated at 30 °C for 40 min and absorbance was recorded at 450 nm. The slope of the curve representing the formation of tetraguaiacol was recorded. The specific activity was expressed in nkat g–1 FW. SOD activity was measured by a standard method (McCord & Fridovich, 1969). Dialyzed extract was mixed with buffer (50 mM KPO4 PH 7.8 and 0.1 mM EDTA) along with 0.05 cytochrome c and 10 mM xanthine and incubated at 30 °C for 40 min. For control xanthine was omitted. The specific activity was expressed in nkat g–1 FW.

Carbohydrate contents

The leaf samples for carbohydrate analysis were taken from plants before and after the 3 days heat stress treatment. A small leaf disc was cut 15 cm from the tip of the leaf and immediately frozen in liquid nitrogen and stored at −80 °C until further analysis. Extraction was made from frozen leaf discs, weighed and ground in a mixer mill (MM200, Retsch Inc., Haan, Germany). The soluble carbohydrates such as fructose, glucose, and sucrose were extracted with 80% ethanol and 5 mM HEPES solution. The extraction was further analysed for soluble carbohydrates by ion chromatography using a pulsed amperometic detector (PAD) with a gold electrode (Dionex, ICS 3000, Sunnywale, Canada), using 200 mM NaOH as eluent ((Dvorackova et al. 2014)).

Photosynthetic rate (Pn) and Grain yield

Photosynthesis rate (Pn) was measured with an Infrared Gas Analyzer (IRGA, Model: LI6400) at noon for each treatment with and without the heat stress. The fully expanded leaf from the top of the plant pot was taken. Leaf was adjusted in the leaf cuvette of the gas analyzer and data was recorded (Shanmugam et al. 2013). At the physiological maturity of the crop, grain yield in terms of grain weight per plant (g/plant) was measured.

Statistical analysis

All the data were subjected to Analysis of Variance (ANOVA) with 5 replicates using the software Statistica 8.1. The means were compared by the least significant difference to access the effect of different treatments. The p-values less than 0.05 were considered as significant. Regression analysis was used to establish the relationship between photosynthetic rate and grain yield (Li et al. 2019).

Results and discussion

In this study, we investigated the carbohydrate metabolism, antioxidant enzyme activity, carbohydrate contents, photosynthetic rate, and grain yield in five wheat cultivars such as AAR-11, Chakwal-50, Shahkar, Pakistan-13, and FSD-08 to understand the interactive effect of e[CO2] and heat stress. In general, we observed that acute heat stress of 40 ºC had negative effects on wheat cultivars when there was a[CO2]. Whereas, under e[CO2] treatment, wheat cultivars tolerated the heat stress and increased the carbohydrate or antioxidant activities. The possible mechanism through which wheat plants tolerated heat stress under e[CO2] is demonstrated in Fig. 1. The output of ANOVA for all the parameters is provided in supplementary Table 1.

Fig. 1.

Fig. 1

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Flowchart depicting a possible mechanism of heat tolerance under e[CO2] by wheat plants (Ainsworth et al. 2002)

Carbohydrate and antioxidant enzyme activity

Carbohydrate metabolism is one of the best parameters to study the effect of heat stress because carbohydrates are very sensitive to environmental cues, such as environmental CO2 and temperature changes. In support of this fact, several studies confirm the changes in carbohydrate metabolism during heat stress (Farooq et al. 2009; Wardlaw et al. 2002) and e[CO2] (McGuire et al. 1997; Poorter et al. 1997), and these are interlinked with each other (Chaturvedi et al. 2017; Córdoba et al. 2017). For carbohydrate metabolism, we studied different enzyme activities such as UDGPase, ADGPase, VacInv, CytInv, and CwInv under the heat stress for both a[CO2] and e[CO2]. Heat stress and e[CO2] significantly affect UDPase and ADPase activities in all the test wheat cultivars (Fig. 2). Under a[CO2], heat stress significantly reduced the UDPase activity in all the cultivars except AARI-11, where it was increased in heat stressed plants, compared to heat stress. However, under e[CO2], the UDPase activity was significantly increased in heat stress plants, as compared to non-stressed plants. Without the heat stress, a significantly higher UDPase activity was found in plants grown under e[CO2], compared with plants grown under a[CO2]. The ADPase activity was significantly decreased during the heat stress in all the cultivars exposed to a[CO2] as compared to control except in Chakwal-50; where it was significantly increased. We found that e[CO2] mitigated the effect of heat stress and increased the activity of ADPase under heat stress. Without the heat stress, ADPase activity was higher under e[CO2] as compared to a[CO2] in AARI-11, Chahkar, Pakistan-13, and FSD-08; however, it remained the same in Chakwal-50 both at a[CO2] and e[CO2]. The increased activity of UDPase and ADPase under e[CO2] during the heat stress may be due to a feedback inhibition of synthesis or recycling of sucrose that accumulates phosphorylated metabolites, stimulates ADGPase by an increased 3PGA: phosphate ratio, and increases expression of ADGPase as a result of sugar-mediated signaling (Nielsen et al. 1998). The activity of other enzymes such as VacInv, CytInv, and CwInv, was also tended to change with CO2 and temperature (Fig. 3). For example, a significant reduction was found in VacInv activity in heat-stressed plants under a[CO2], in comparison with non-stressed plants, while the changes in VacInv activity was non-significant in heat-stressed plant under e[CO2] with that of non-stressed plants. When a[CO2] and e[CO2] treatments were compared, a significant increase in VacInv activity was found in e[CO2] treatment. In all cultivars, the activity of CytInv was significantly reduced in heat-stressed plants under a[CO2] than that of non-stressed plants. Similarly, e[CO2] significantly increased the CytInv activity in all cultivars, in comparison with a[CO2]. Exposed to combined treatment of heat stress and e[CO2], all five cultivars showed differential responses with relation to e[CO2] treatment. For example, AARI-11, Chakwal-50, and FSD-08 had lower CytInv activity, Pakistan-13 had higher CytInv activity, and Shahkar had same CytInv activity. The CwInv activity responded differently to treatments in all cultivars. The CwInv activity was significantly decreased in heat-stressed plants exposed to a[CO2], in comparison with non-stressed plants in Chakwal-50, Pakistan-13, and FSD-08, while in AARI-11 and Shahkar, it remained the same in both stressed and non-stressed plants under a[CO2]. Under e[CO2], heat-stressed plants maintained the CwInv activity with that of non-stressed plants in all cultivars except in AARI-11, where CwInv activity was reduced in stressed plants as compared to non-stressed plants. As compared to a[CO2], the plants under e[CO2] had higher CwInv activity.

Fig. 2.

Fig. 2

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ADP-glucose pyrophosphorylase (ADGPase) and UDP-glucose pyrophosphorylase (UDGPase) activity affected by ambient CO2 (AC) concentration (380 mmol L−1), elevated CO2 (EC) concentration (780 mmol L−1), ambient CO2 + heat stress (AC + H), and elevated CO2 + heat stress (EC + H). The temperature of heat stress was 40 ºC. Error bar represents the standard error of means (n = 5). Different letters in the same sub-group of columns indicate significant difference at p < 0.05 level

Fig. 3.

Fig. 3

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Cell wall invertase (CwInv), vacuolar invertase (VacInv), and cytoplasmic inverstase (cytInv) activity affected by ambient CO2 (AC) concentration (380 mmol L−1), elevated CO2 (EC) concentration (780 mmol L−1), ambient CO2 + heat stress (AC + H), and elevated CO2 + heat stress (EC + H). The temperature of heat stress was 40 ºC. Error bar represents the standard error of means (n = 5). Different letters in the same sub-group of columns indicate significant difference at p < 0.05 level

For antioxidant enzyme activity, the activities of GR, POX, and SOD were determined both at a[CO2] and e[CO2] during heat-stressed and non-heat-stressed conditions (Fig. 4). Before exposure to heat stress, e[CO2] had a positive effect on GR activity in AARI-11, Chakwal-50, and FSD-08, while in Shahkar and Pakistan-13, the GR activity was reduced under e[CO2], compared to a[CO2]. When the plants were exposed to heat stress, a significant increase in GR activity was found in most of the cultivars at a[CO2] and e[CO2], compared to not-stressed plants. Nevertheless, a noteworthy increase was found in the plants grown under e[CO2]. A significant difference was found in POX activity in all cultivars when grown under a[CO2] and e[CO2] before the heat treatment. The cultivars AARI-11, Shahkar, and FSD-08 had higher POX activity under e[CO2], whereas Chakwal-50 and Pakistan-13 had lower POX activity, as compared to a[CO2]. After the heat stress, three cultivars AARI-11, Pakistan-13, and FSD-08 showed increased POX activity under e[CO2] and two cultivars Chakwal-50 and Shahkar showed reduced POX activity, as compared to relative non-stressed plants. However, heat stress significantly reduced the POX activity in all cultivars under a[CO2], as compared to control. Results of ANOVA indicated a significant difference in SOD activity under different treatments. Under e[CO2], Pakistan-13 and FSD-08 had increased SOD activity, Chakwal-50 and Shahkar had decreased SOD activity, and AARI-11 had no difference in SOD activity, in comparison with a[CO2]. When the heat treatment was applied, the SOD activity was significantly reduced under a[CO2] in all cultivars. But under e[CO2], heat stress posed either a positive effect on SOD activity in some cultivars or remained unchanged both in heat-stressed and non-stressed plants. The activities of these enzymes either increased or maintained in tolerant wheat cultivars grown under e[CO2] during heat stress, consistent with the common conclusion about e[CO2]-increased enzyme activities during heat stress (Powell et al. 2012; Geissler et al. 2010; Zinta et al. 2014).

Fig. 4.

Fig. 4

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Glutathione reductase (GR), Peroxidase (POX), and Superoxide dismutase (SOD) activity affected by ambient CO2 (AC) concentration (380 mmol L−1), elevated CO2 (EC) concentration (780 mmol L−1), ambient CO2 + heat stress (AC + H), and elevated CO2 + heat stress (EC + H). The temperature of heat stress was 40 ºC. Error bar represents the standard error of means (n = 5). Different letters in the same sub-group of columns indicate significant difference at p < 0.05 level

Carbohydrate contents

The ANOVA results indicated a significant effect of e[CO2] and heat stress on the concentration of soluble sugars such as fructose, glucose, and sucrose, in all five wheat cultivars (Fig. 5). Under e[CO2], the concentration of fructose was significantly higher in Pakistan-13 and FSD-08, lower in Shahkar, while it remained non-significant in AARI-11 and Chakwal-50 in comparison with a[CO2]. The concentration of glucose and sucrose was found higher in e[CO2] treatment than a[CO2]. After the heat treatment, the concentration of fructose, glucose, and sucrose was significantly increased in the plants grown under e[CO2] than those exposed to e[CO2] with heat stress. However, under a[CO2], heat stress caused different effects on carbohydrate contents in distinct cultivars. It was observed that heat stress at anthesis significantly affects the accumulation of soluble sugars in the leaves of wheat cultivars. This accumulation of soluble carbohydrates during heat stress possible occurs because photosynthesis was largely increased at the e[CO2], whereas carbohydrate partitioning to other plant parts was restricted by high temperature. These results are in agreement with the previous studies that carbohydrate portioning particularly is inhibited in heat stress (Geissler et al. 2010). Furthermore, increased soluble sugar levels have been linked to increased osmotic adjustment in heat stressed plants (Zou et al. 2016), suggesting that higher soluble sugar concentrations in cultivars grown at e[CO2] could be linked to better heat tolerance in these cultivars under the alleviating effect of e[CO2]. Another example is the soybean leaves, where an increased level of hexoses has been found under e[CO2], resulting in augmented tolerance against heat stress (Vu et al. 2001). The accumulation of soluble carbohydrates can also be linked to the ratio of photosynthesis and respiration rate. In general, high temperature increases the respiration rate and decreases the Pn, resulting in higher carbohydrate consumption than production, leading to a decline in soluble sugars. However, e[CO2] could play an alleviating role and increase Pn during high temperature, resulting in high carbohydrate content as observed in this study.

Fig. 5.

Fig. 5

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Leaf carbohydrate contents such as fructose, glucose, and fructose affected by ambient CO2 (AC) concentration (380 mmol L−1), elevated CO2 (EC) concentration (780 mmol L−1), ambient CO2 + heat stress (AC + H), and elevated CO2 + heat stress (EC + H). The temperature of heat stress was 40 ºC. Error bar represents the standard error of means (n = 5). Different letters in the same sub-group of columns indicate significant difference at p < 0.05 level

Photosynthetic rate (Pn) and grain yield

The statistical data revealed significant effects of e[CO2] and heat stress on Pn, in all the wheat cultivars (Fig. 6). Heat stress significantly reduced the Pn in plants that were grown in a[CO2], compare to non-stressed plants. However, plants grown in e[CO2] under heat stress nearly maintained photosynthetic rate with that in e[CO2] under non-stress control. In all five wheat cultivars, e[CO2] significantly increased the Pn in control plants, compared with a[CO2]. This indicated that wheat cultivars still increase the Pn when e[CO2] was provided under heat stress, showing that these wheat cultivars possessed higher adaptation ability to heat stress. Other plant species have also shown the increased Pn under e[CO2], in contrast to a[CO2]. For example, an increased level of Pn was found under e[CO2] in Glycine max (Li et al. 2020), Sorghum bicolor (Zheng et al. 2017), Lolium perenne (Casella and Soussana 1997), and Deschampsia flexuosa (Albert et al. 2011). Many associated factors are the reason for enhancing Pn under e[CO2] such as increased Rubisco activity, decreased stomatal opening, ribulose-1,5-bisphosphate (RuBP) regeneration capacity, and photorespiration suppression (Bowes 1991; Faria et al. 1996; Cannell and Thornley 1998; Qaderi et al. 2006; Wang et al. 2008a, b). The increased Pn by e[CO2] in wheat cultivars could be related to changes in above mentioned metabolic activities, although these were not investigated in this study, but are worth further investigation in future studies.

Fig. 6.

Fig. 6

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Net photosynthetic rate (Pn) and grain yield affected by ambient CO2 (AC) concentration (380 mmol L−1), elevated CO2 (EC) concentration (780 mmol L−1), ambient CO2 + heat stress (AC + H), and elevated CO2 + heat stress (EC + H). The temperature of heat stress was 40 ºC. Error bar represents the standard error of means (n = 5). Different letters in the same sub-group of columns indicate significant difference at p < 0.05 level

Grain yield was also significantly increased by e[CO2] relative to their a[CO2] in all five cultivars (Fig. 6). Under heat stress, a significant reduction was found in grain yield in the plants grown under a[CO2]. However, under e[CO2], the grain yield was also significantly lower than control but much higher than that of plants exposed to a[CO2] during heat stressed treatment. Moreover, a positive linear correlation was found between Pn and grain yield across all the treatments in five wheat cultivars (Fig. 7). It has been reported that grain yield was significantly influenced by e[CO2] in Triticum aestivum (Varga et al. 2017). Generally, high temperature decreases the photosynthetic efficiency, resulting in weak leaf development and tiller formation and ultimately low crop yield (Mathur and Jajoo 2014; Modarresi et al. 2015). Higher temperature also causes early flowering and maturity, results in lower yield due to availably of small duration for grain filling. Other effects of higher temperature are poor germination, low photosynthesis, decreased pollen viability, leaf senescence, and less and small-sized grains (Ugarte et al. 2007; Asseng et al. 2011). However, e[CO2] alleviated the effect of heat stress and maintained the crop yield (Ferris et al. 1999; Hamerlynck et al. 2000; Taub et al. 2000). Based on these facts, some authors consider climatic change as a positive one, because an increase in temperature increases the amount of CO2 on earth that may increase wheat yield by 37–101% by 2050 (Pimentel et al. 2005). Inclusively, we have observed different effects of CO2 concentrations and heat stress in test wheat cultivars, owing to the cultivar-dependent effects. For example, Pakistan-13 and FSD-08 were found to more tolerant cultivars to heat stress under e[CO2]. It has already been shown that the concentration of CO2, timing, gravity of heat stress, and crops cultivars all play a role in determining the effects of e[CO2] and heat stress in plants (Bauweraerts et al. 2013).

Fig. 7.

Fig. 7

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Correlation between photosynthetic rate (Pn) and grain yield in wheat cultivars under various treatments (n = 5)

Conclusion

According to the findings, e[CO2] reduced the effects of high temperatures, and wheat cultivars that were cultivated under e[CO2] fared better with heat stress. In compared to plants cultivated at a[CO2], the plants cultivated at e[CO2] maintained high metabolic activity, Pn and grain production after heat stress. We found that the plant's response to climatic changes, such as heat stress, was affected by the concentration of CO2 in the atmosphere. This study suggests that through altering carbohydrate metabolism, e[CO2] might improve the tolerance of certain wheat cultivars to heat stress.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 16 kb) (16.9KB, docx)

Acknowledgements

We acknowledge the National Agricultural Research Center (NARC) for providing seeds of wheat varieties. Author would like to thank Higher Education Commission of Pakistan for providing opportunity for research visit.

Abbreviations

Pn

Photosynthetic rate

e[CO2]

Elevated carbon

NARC

National agricultural research center

EC

Electrical conductivity

PVPP

Polyvinylpolypyrrolidone

NADP

Nicotinamide adenine dinucleotide phosphate

PMSF

Phenylmethylsulfonyl fluoride

AGPase

ADP-glucose pyrophosphorylase

UGPase

UDP-glucose pyrophosphorylase

CwInv

Cell wall invertase

VacInv

Vacuolar

CytInv

Cytoplasmic

GR

Glutathione reductase

POX

Peroxidase

SOD

Superoxide dismutase

PAD

Pulsed amperometric detector

Authors' contributions

AU: Investigation, Data curation, Writing—original draft. AM: Methodology, Conceptualization, Writing—review & editing, Supervision. KS A Writing—review & editing. SU-A: Writing—review & editing.

Funding

The authors did not receive support from any organization for the submitted work.

Data availability

The datasets used and/or analysed during the current study available from the corresponding author on reasonable request.

Declarations

Conflict of interest

The authors have no relevant financial or non-financial interests to disclose.

Consent for publication

All authors have approved the final version for submission.

Footnotes

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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Supplementary Materials

Supplementary file1 (DOCX 16 kb) (16.9KB, docx)

Data Availability Statement

The datasets used and/or analysed during the current study available from the corresponding author on reasonable request.

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