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Review

Physiological Responses of Plants to Combined Drought and Heat under Elevated CO2

by
Lamis Osama Anwar Abdelhakim
*,
Rong Zhou
and
Carl-Otto Ottosen
Department of Food Science—Plant, Food & Climate, Aarhus University, Agro Food Park 48, DK-8200 Aarhus N, Denmark
*
Author to whom correspondence should be addressed.
Agronomy 2022, 12(10), 2526; https://doi.org/10.3390/agronomy12102526
Submission received: 31 August 2022 / Revised: 8 October 2022 / Accepted: 12 October 2022 / Published: 16 October 2022
(This article belongs to the Collection Abiotic Stress Tolerance in Plants: Towards a Sustainable Agriculture)
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Abstract

:
Anthropogenic activities over the last century have caused rapid changes in environmental conditions through increasing CO2 emissions in the atmosphere that contribute to global warming. Moreover, the increased global average temperature is linked with changes in the precipitation rate and distribution, resulting in a negative impact on crop health and productivity. Plants in nature often experience combined stresses; therefore, they have developed adaptive mechanisms to cope with fluctuating environmental conditions. Thus, investigating plant responses under unfavorable environmental conditions will provide a better understanding of how crops can adapt and thereby assist in selecting climate-resilient crops that can withstand climate variability. This review highlights the main adaptive physiological and biochemical responses of crops grown under elevated CO2 (eCO2) and exposed to combined abiotic stresses (drought and heat). Moreover, the mitigation and limitation impact of elevated CO2 on plants under the combination of stress is discussed.

1. Introduction

The continued rise of atmospheric CO2 levels and other greenhouse gas emissions contribute to global warming where not less than 1.5–2 °C has been extended since the last century to the average surface temperature [1]. The current global average CO2 concentration is 418 ppm, according to the USA National Oceanic and Atmospheric Administration [2]. The atmospheric CO2 level is expected to exceed 450 ppm by 2030 and it will reach levels above 720 ppm by the end of this century, according to the Intergovernmental Panel on Climate Change [3,4]. Furthermore, the increased frequency, intensity, and duration of heat waves and drought events are threatening agricultural productivity and food security [4]. The development of climate and crop growth models has an essential role in clarifying the upcoming trends of climate variability and the influence of climate change on crop productivity [5,6]. Long-term climate studies showed the negative impact of warmer temperatures and changes in precipitation where the soil C content was reduced, but it was alleviated under higher CO2 levels [7]. Moreover, many studies have focused on the impacts of environmental stresses on the development and productivity of different crops [8]. The application of agronomic management practices and genomic selection approaches, and the development of crop varieties with high productivity are needed to alleviate the detrimental effects of heat and drought [9]. To mitigate climate change’s impact on crop yield, finding high-yielding and stress-resistant varieties that can withstand extreme climate events is necessary [10]. Therefore, understanding the underlying mechanisms and responses of crops, particularly among different varieties and genotypes, is essential for developing robust crop varieties for the future [11,12].
The incidence of long-term multiple stresses under field conditions results in extensive yield losses. To cope with unfavorable environmental conditions such as drought and heatwaves, plants in nature have developed various morpho-physiological and biochemical adaptive strategies, as they are frequently exposed to combined stresses. However, these agronomic traits have not been the focus of breeding in crop plants [13,14]. Plant phenotypic plasticity enables acclimation to the fluctuation of environmental conditions through stress tolerance and/or avoidance mechanisms [15]. Complex metabolic networks are involved in regulating the different physiological and biochemical functions, including plant growth, photosynthesis, osmotic adjustment, and carbohydrate homeostasis as acclimation responses to stress [16]. Identifying crop tolerance mechanisms at different organizational levels, including whole plant phenotyping, metabolomics, proteomics, and genomics under combined drought and heat stress, is essential for developing tolerant crops [17]. Both elevated CO2 (eCO2) and the combination of stresses add complexity to the response of plants, and to understand their underlying mechanisms, further investigations are required [18,19,20]. In this review, we are discussing the physiological responses of plants grown under eCO2 and exposed to combined stress (i.e., drought and heat stress as major abiotic stress combinations). Moreover, we are highlighting the eCO2 mitigation impacts and limitations under combined stress in wheat as the model crop. Knowledge of the adaptive mechanisms of plants under combined stress and high CO2 levels can be utilized for the development and selection of climate-resilient crops.

2. Elevated CO2 Improves Plant Photosynthesis and WUE under Moderate Drought Stress

The effect of eCO2 in regulating the plant-water relations depends on drought severity and susceptibility of plants, where drought-stressed plants can benefit from eCO2 as observed in higher biomass accumulation and yield, compared to well-watered conditions [18,21]. Elevated CO2 is claimed to alleviate moderate drought stress effect by enhancing the water use efficiency (WUE) through lowering stomatal conductance (gs) and maintaining the photosynthetic rate, as the intercellular CO2 (Ci) level is high and thereby protects the photosynthetic apparatus from water stress-induced damage [22,23,24]. In addition, the increase in abscisic acid concentration to regulate stomatal aperture under drought stress, together with enhanced WUE and high carbon assimilation by eCO2, have improved drought tolerance in plants [25]. Such regulations have an alleviation impact on maintaining the growth rate when plants are exposed to moderate short-term stress [26]. Moreover, a reduction in water consumption due to lower gs and evapotranspiration rate can conserve soil moisture content for a longer time, particularly in later developmental stages. Consequently, plants will be less susceptible to water deficit and utilize eCO2 efficiently [27]. Higher photosynthetic acclimation with improved WUE and nitrogen use efficiency (NUE) and upregulation of the antioxidant defense metabolism reflect the amelioration effect of eCO2 that is pronounced under moderate drought stress levels [28]. In wheat, plants grown under combined drought and eCO2 enhanced photosynthesis and regulated the antioxidants and carbohydrate metabolic enzyme activities to maintain the grain yield [29]. However, the drought stress did lower the CO2 fertilization effect on photosynthesis, due to the reduction in gs and transpiration rate that may lead to a reduction in the uptake of N, which is needed for Ribulose-1,5-bisphosphate carboxylase—oxygenase (Rubisco) activity [30]. Furthermore, different studies on soybean showed that eCO2 increased the photosynthesis and WUE in drought-stressed cultivars during the vegetative stage but not the final yield, whereas other cultivars with high-yielding traits showed enhanced biomass and grain yield [31,32]. Thus, the mitigation effect of eCO2 on the final yield under drought depends on the potential of the cultivar.

3. Elevated CO2 Reduces Plant Photorespiration and Enhances Photosynthesis under Heat Stress

Photosynthetic rate is dependent on Rubisco enzyme that has the potential to respond to high CO2 levels where the higher Rubisco carboxylation efficiency over oxygenation enhances assimilation CO2 as higher Ci increases the CO2:O2 ratio in the chloroplast and thereby decreases photorespiration [33]. The reduced photorespiration at eCO2 lowered the hydrogen peroxide (H2O2) production and thus protected the chloroplasts from oxidative stress [34]. The occurrence of heat stress can cause irreversible effects on plant growth and development as photosynthesis is sensitive to high temperatures [35]. However, eCO2 enhances heat stress-tolerance of photosynthesis and photosystem II (PSII) thermotolerance without the occurrence of other limiting factors [36]. Despite the acclimation of photosynthesis to increasing temperatures being enhanced by eCO2, the response may change depending on short or long-term growth under eCO2 [37]. For example, the changes in photosynthesis and Rubisco activity in response to combined eCO2 and temperature in the long term are influenced by other limiting factors, such as nitrogen (N) availability [38,39].
Under high temperatures, the increased transpiration rate is an important trait in heat-tolerant genotypes to cool the leaves and maintain photosynthesis [40]. By combining eCO2 and heat stress at 40 °C for 3 days, high photosynthetic rate and maximum quantum efficiency of PSII (Fv/Fm) were maintained in the heat-tolerant wheat cultivar at booting and anthesis stages, compared with ambient CO2 (aCO2) [41]. The occurrence of stress at the late developmental stage inhibits plant development and causes a dramatic reduction in final yield regardless of CO2 level. Even though eCO2 mitigated the negative effect of heat stress on photosynthesis and biomass during anthesis, the grain yield was reduced due to grain abortion [42]. Moreover, the occurrence of heat stress during post-anthesis has diminished the positive effects of eCO2 on photosynthesis and yield-related traits [43]. Thus, limitations in eCO2 utilizations in the final yield still require further investigations to find high-yielding varieties that maintain the yield or show less reduction in yield under combined stresses.

4. Complex Physiological Responses of Plants to Drought and Heat Stress under eCO2

Opposing signaling under drought and heat stress is involved in different stomatal regulations where stomata close to prevent excess water loss under drought stress and stomatal opening increases under heat stress to avoid overheating of leaves [44]. Moreover, the limitation of photosynthetic activity differs when plants are exposed to drought or heat stress. The stomatal limitation under moderate drought stress causes a reduction in the photosynthetic rate without damaging the photosynthetic apparatus, due to the increase in photorespiration, which acts as a protective mechanism [45]. Thus, such protection enables plants to maintain electron transport rates and lower the consumption of NADPH and ATP for CO2 assimilation [46]. However, if the rate of photosynthesis is reduced, whereas the Ci is maintained at a high level, that indicates the metabolic limitation (non-stomatal limitation) is dominant [47]. Since the Rubisco activity and synthesis of RuBP have a vital role in regulating photosynthetic carbon assimilation, any reduction in Rubisco activation and electron transport rate under drought stress will thus limit the photosynthetic rate [48]. With increasing drought severity, the utilization rate of NADPH and ATP in the photosynthetic metabolism decreases and will not be compensated by the photorespiration and Mehler-peroxidase reaction or other electron sinks in the chloroplasts, leading to a reduction in the PSII operating efficiency and damage to PSII [46]. Moreover, the imbalance between the input from the electron transport chain in the thylakoid membrane and the output from the Calvin–Benson cycle in the chloroplast affects the efficiency of PSII [46].
When CO2 fixation is limited under stress conditions, alternative protective mechanisms exist, such as non-photochemical quenching (NPQ) for the dissipation of excess photons and electrons from the photosynthetic apparatus [49]. The thylakoid membranes (where NADPH and ATP are produced by the light-dependent reactions of the photosystems) are sensitive to high temperatures and act as the main reaction sites for photochemical reactions [50,51]. The Rubisco deactivation correlates with the reduction in photosynthesis at high temperatures [52]. The rate of photosynthesis decreases due to the impairment of thylakoid membranes in wheat exposed to high temperatures at 35–36 °C for 16 days of stress [53,54]. Thus, under moderate heat stress, the reduction in Rubisco activation and electron transport rate limit the photosynthesis [51]. When heat is combined with drought, the role of Rubisco amount and activities in regulating photosynthesis will depend on the species and the dominant stress [55]. Moreover, the combination of drought and heat stress have more detrimental impacts on plant growth and productivity compared to individual stress, as different signaling pathways might interact and inhibit each other in response to combined stress [56]. Thus, the response of plants to individual abiotic stress is different when stresses are combined (Figure 1), and so current and future research focuses more on investigating the potential tolerance of different plants to natural environmental conditions where combined stress occurs [57]. Consequently, investigating the effect of stress combinations on the underlying mechanisms of plants is necessary to find climate-resilient crops that can maintain the yield under future climate conditions [58,59].
The alleviating responses by eCO2 under combined stress vary in wheat and other crops, as summarized in Table 1. Large sink capacity for the utilization of photosynthate under eCO2 is vital in the selection of determinate cultivars [60]. The photosynthetic rate and the acclimation of carboxylation capacity under eCO2 are regulated by the adjustment of the nitrogen supply and sink capacity [61]. Since the source–sink balance varies between the different growth stages, it affects photosynthetic acclimation [62]. A down-regulation in photosynthetic rate and an increase in starch accumulation and C: N ratio were observed in grapevine leaves under long-term eCO2, reflecting acclimation responses regardless of heat and drought treatments [62]. Such acclimation is essential to balance the source–sink relationship that will probably mitigate the sink limitation under eCO2 [63]. However, it has been questioned whether increased photosynthesis under eCO2 leads to a higher yield [64]. Higher biomass due to eCO2 would accelerate water consumption and plants would be more susceptible to drought. Consequently, a reduction in the final yield was observed in wheat where more tillers did not produce heads and grains [63]. Under abiotic stress, the eCO2 will not have a fertilizing impact as the carbon sink activity (carbon demand by growth) constrains the carbon source activity (carbon fixation by photosynthesis) [64]. Thus, plants with low sink strength are not able to utilize the additional assimilates developed under eCO2 [63]. Furthermore, phenotyping photosynthesis and connecting it with the harvest yield requires further investigation. The natural variation between wheat cultivars affected the response between the photosynthetic capacity of the flag leaf and grain yield where no correlation was found in one year, but a clear correlation was observed in the following year [65,66]. Thus, the limiting factor for the growth and harvest yield of crops seems to be dependent on both the environmental conditions and the balance between the source and sink capacity. Therefore, finding tolerable traits that can sustain productivity under combined stresses and utilize the eCO2 effect is necessary.

5. The Mitigation of eCO2 on Plants under Combined Drought and Heat Stress

Generally, eCO2 can alleviate the negative effects of drought and/or heat on plants as shown in Figure 2, depending on the tolerance level of the specific genotypes to the induced stress and their transpiration efficiency that is more pronounced in heat-tolerant varieties [79]. Furthermore, the intensity of stress affects eCO2 mitigation on the yield under stress where an increase in the biomass and grain yield was reported at 2 °C above the ambient temperature under eCO2 in wheat and showed less reduction when combined with terminal drought, compared with 4–6 °C higher temperatures [80]. In addition, a long-term experiment in the UK used a crop simulation model to analyze the impact of high temperature and eCO2 on winter wheat yield in the 20th century where the increment in simulated yield with high CO2 was dependent on the water availability during anthesis and grain filling stages [81]. Even though eCO2 alleviated the negative effect of moderate heat stress by improving photosynthesis, total dry weight, and seed productivity compared to ambient temperature, such pronounced impact on morpho-physiological traits is dependent on the severity of other limiting factors, such as water and nutrients [82].
Antioxidant defense systems in plants include both enzymatic and non-enzymatic antioxidants that are activated to reduce oxidative stress and to maintain the cellular redox balance when plants are exposed to extreme abiotic stressed conditions [83]. Thus, plants alleviate the damaging effects of reactive oxygen species (ROS) through these enzymatic and non-enzymatic antioxidants that work together and thereby enhance tolerance against stressed conditions [84]. To avoid ROS accumulation due to the impairment of photosynthetic function under stress, eCO2 increases NPQ to compensate for energy sink reduction and thereby enhance PSII photoprotection and prevent photooxidative stress [85]. Moreover, under moderate stress conditions, the enzymatic antioxidant system is maintained, which reflects less stressed plants grown under eCO2 due to protected PSII [85,86]. The intensity of stress influences the antioxidant defense capacity in plants grown under eCO2 where the antioxidant concentration decreases at eCO2 by increasing the stress severity [86]. Thus, the reduction in oxidation damage and higher ROS scavenging capacity reflects the mitigation impact under eCO2 [87]. In addition, the synthesis of metabolites as compatible solutes with antioxidant properties such as proline and cadaverine are pronounced under combined drought and heat stress and have been involved in osmotic adjustment and improved WUE, and thereby maintained photosynthesis when combined with eCO2 [70]. Thus, enhancing plant stress tolerance through the accumulation of phenolic compounds and compatible solutes has an important role in maintaining the water balance of the plant and reducing the oxidative damage of ROS as an antioxidant defense mechanism [83,88].

6. The Limitations of eCO2 on Plants under Combined Drought and Heat Stress

Improved plant responses under eCO2 could be diminished with increasing high- temperature and the negative impact is even exacerbated when combined with drought [89]. Prominent changes in plant responses and yield losses occur when plants are exposed to combined drought and heat stress under eCO2, as summarized in Figure 2. The combination of drought and heat stress intensifies the negative effect on the growth, development, and yield of crops, compared with individual stress [90]. The predominant effect of a stressor, such as drought, often overruled the heat stress when combined and thereby negatively affected the physiological responses [91]. Enhanced photosynthesis and biomass were reported under combined eCO2 and heat stress, whereas the occurrence of the drought was dominant and intensified the stress, regardless of eCO2 [92]. One of the major constraints on grain yield improvement at eCO2 of spring wheat under Scandinavian climatic conditions is sink limitation [93]. Winter wheat grown under Mediterranean conditions showed that the early flowering cultivars have a higher yield compared with early sowing cultivars due to the fulfillment of the vernalization and adequate phenological development [94]. Thus, crop varieties adapted to the current European climate are at risk for grain abortion and a lower yield, due to the occurrence of frequent warmer and drier weather patterns during the reproductive stage [95]. Plants grown under eCO2 in Free Air CO2 Enrichment (FACE) showed higher N uptake over time, but the reduction in N content in wheat grains was not mitigated by additional N application [96]. With long-term exposure to eCO2, photosynthesis was down-regulated due to limitation in nutrient supply [97]. Moreover, considering the fluctuating eCO2 levels in FACE influenced photosynthesis, stomatal regulation, and biomass accumulation that could have a negative effect compared to constant eCO2 levels [98]. The response under eCO2 changes depending on the developmental stages in wheat grown in the dryland cropping system where higher net CO2 assimilation rates and less reduction in grain N concentrations were observed when plants were exposed to a heatwave during pre-anthesis but not during post-anthesis [99]. Although the stem water-soluble carbohydrates reserve was enhanced in plants grown under eCO2, it did not improve the C translocation to the grains and led to a reduction in the final yield [99]. With proper agricultural practices, the effect of heat and water deficit can be mitigated to some extent depending on the region, but, due to the effect of eCO2, it is a challenge to maintain yield quality [100]. In addition, the response to eCO2 varies depending on the photosynthetic response of different cultivars and N availability [101]. For instance, a reduction in the photosynthetic rate was observed under a low N supply in wheat, regardless of eCO2 [102]. Even though eCO2 increased the biomass and NUE in tobacco, the leaf N concentration was reduced [103]. Thus, an additional application of N might be required to avoid the negative impact on grain protein content under eCO2 [103,104]. Moreover, the effect of eCO2 on grain yield and protein content is influenced by the balance between shoot and root nitrate assimilation [105]. The increase in atmospheric CO2 concentration by 19% with other environmental factors in field studies between 1985–2019 showed a reduction in wheat grain yield and protein yield by 13%, with no significant change in the protein content of grain [106]. Consequently, new tolerant cultivars need to maintain grain protein and yield under yield-limiting environmental conditions [107].

7. Conclusions

Various adaptive mechanisms are developed in plants in response to the interaction of multiple environmental factors. The combined effects of heat and drought stress under eCO2 are crucial to investigate because of the opposing signals. For instance, a higher transpiration rate is vital for lowering leaf temperatures of plants under heat stress, whereas improved WUE under drought stress is essential to avoid excess water loss and to maintain the photosynthetic apparatus. The severity level of combined stress is determined when one stress overrules the effect of the other stress. Drought stress tends to be more dominant than heat stress, clearly depending on the stress intensity and duration. Despite eCO2 having a mitigation effect on plant development under drought or heat stress, the frequent occurrence of the stress will diminish such positive effects of eCO2. The fact that the enhanced response of the photosynthesis and plant–water relation by eCO2 is not reflected in the final yield can be related to several reasons, such as source–sink limitation, nutrient deficiency, or cultivar dependence. In addition, the occurrence of warming and drought trends during the flowering and grain-filling stage has a negative impact on grain quantityand quality. It will be important to determine whether the relevant phenological and agronomic traits and whether heat-tolerant or drought-tolerant cultivars will cope better with the combination of heat and drought and thus benefit more from the eCO2 mitigation. Phenotyping of plants under combined stress tolerance is still challenging, due to the interactions of genotype, growth environment, and agronomic management (G × E × M) in determining the yield. Further investigations and applications of applied phenomics approaches will be crucial to improve our understanding of combined stress responses in target environments and find climate-resilient crops.

Author Contributions

Conceptualization, L.O.A.A. and C.-O.O.; writing—original draft preparation, L.O.A.A.; writing—review and editing, R.Z. and C.-O.O. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Independent Research Foundation of Denmark (0217-00084B) as part of the SUSWHEAT (green transition) and in part supported by iClimate (Interdisciplinary Centre for Climate Change) at Aarhus University.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

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Agronomy 12 02526 g001 550
Figure 1. The effect of elevated CO2, drought, and heat stress individually and in combination on the main physiological responses of plants without the occurrence of other limiting factors.
Figure 1. The effect of elevated CO2, drought, and heat stress individually and in combination on the main physiological responses of plants without the occurrence of other limiting factors.
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Figure 2. The mitigation and limitation effect under combined elevated CO2, drought, and heat stress on the main physiological and biochemical responses in plants.
Figure 2. The mitigation and limitation effect under combined elevated CO2, drought, and heat stress on the main physiological and biochemical responses in plants.
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Table
Table 1. Overview of studies investigating the responses under the combination of drought and heat stresses and elevated CO2.
Table 1. Overview of studies investigating the responses under the combination of drought and heat stresses and elevated CO2.
CropseCO2, ppmCombination of StressFocus/ResponsesMitigation Effect of eCO2 under Combined StressReferences
Wheat800eCO2, heat, and droughtPhysiological level and yieldeCO2 increased the grain yield by 20.8% in wheat.[67]
Wheat550 FACESemi-arid environmentsMorpho-physiological levels and yieldMitigation was reflected in increased final yield.[68]
Wheat800eCO2, heat, and droughtPhysiological leveleCO2 increased photosynthesis and maintained higher Fv/Fm in some genotypes under combined stress compared to aCO2.[69]
Wheat800eCO2, heat, and droughtPhysiological, biochemical levels and yieldNo eCO2 mitigation effect on the final yield despite enhanced WUE.[70]
Tomato800eCO2, heat, and droughtPhysiological levelNo eCO2 mitigation due to increased severity of water deficit.[71]
Arabidopsis730eCO2, heat, and droughtPhysiological, biochemical, and genome-wide transcriptional levelsMitigation is associated with reduced photorespiration and increased content of different antioxidant mechanisms.[72]
Arabidopsis700eCO2, heat, and droughtPhysiological and molecular levelseCO2 increased stress tolerance under combined drought and heat by mitigating oxidative stress and improving the water status of plants.[73]
Arabidopsis700eCO2, heat, and droughtPhysiological and molecular levelseCO2 partially mitigated the adverse effect of stresses on some traits in the selected genotypes.[74]
Brassica napus800eCO2, heat, and droughtMorpho-physiological levelsMitigation is associated with improving plant water relations, but not during the recovery.[75]
Cotton640eCO2, heat, and droughtMorpho-physiological levelseCO2 enhanced biomass and WUE, but not under high temperatures and rapid water deficit, due to the stomatal limitation.[76]
Plants/treesMeta-analysiseCO2, eO3, heat, and droughtPhysiological levelImproved WUE by eCO2 mitigated the negative stress impacts on photosynthesis to some extent.[77]
Two types of grass;
Lolium perenne,
Poa pratensis.
Two legumes;
Medicago lupulina,
Lotus corniculatus.		615eCO2, heat, and droughtPhysiological and biochemical levelsEnhanced physiological responses by eCO2 under stress in the grass, whereas mitigation through regulating lipid peroxidation and H2O2 levels were more pronounced in legumes.[78]
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Abdelhakim, L.O.A.; Zhou, R.; Ottosen, C.-O. Physiological Responses of Plants to Combined Drought and Heat under Elevated CO2. Agronomy 2022, 12, 2526. https://doi.org/10.3390/agronomy12102526

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Abdelhakim LOA, Zhou R, Ottosen C-O. Physiological Responses of Plants to Combined Drought and Heat under Elevated CO2. Agronomy. 2022; 12(10):2526. https://doi.org/10.3390/agronomy12102526

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Abdelhakim, Lamis Osama Anwar, Rong Zhou, and Carl-Otto Ottosen. 2022. "Physiological Responses of Plants to Combined Drought and Heat under Elevated CO2" Agronomy 12, no. 10: 2526. https://doi.org/10.3390/agronomy12102526

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