Next Article in Journal
Understanding and Comprehensive Evaluation of Cold Resistance in the Seedlings of Multiple Maize Genotypes
Next Article in Special Issue
High Atmospheric CO2 Concentration Mitigates Drought Effects on Acanthostyles buniifolius an Important Grassland Weed in South America
Previous Article in Journal
Identification of Putative Candidate Genes from Galphimia spp. Encoding Enzymes of the Galphimines Triterpenoids Synthesis Pathway with Anxiolytic and Sedative Effects
Previous Article in Special Issue
Rising Carbon Dioxide and Global Nutrition: Evidence and Action Needed
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:

Physiological and Molecular Responses of Woody Plants Exposed to Future Atmospheric CO2 Levels under Abiotic Stresses

Department of Biodiversity, Institute of Biosciences, São Paulo State University, UNESP, Rio Claro 13506-900, Brazil
Institute of Environmental Research, São Paulo 04301-002, Brazil
Centre for Natural and Human Sciences, Federal University of ABC, São Bernardo do Campo 09606-045, Brazil
Authors to whom correspondence should be addressed.
Plants 2022, 11(14), 1880;
Received: 6 June 2022 / Revised: 1 July 2022 / Accepted: 5 July 2022 / Published: 20 July 2022
(This article belongs to the Special Issue The Effect of Carbon Dioxide Concentration on Plant Physiology)


Climate change is mainly driven by the accumulation of carbon dioxide (CO2) in the atmosphere in the last century. Plant growth is constantly challenged by environmental fluctuations including heat waves, severe drought and salinity, along with ozone accumulation in the atmosphere. Food security is at risk in an increasing world population, and it is necessary to face the current and the expected effects of global warming. The effects of the predicted environment scenario of elevated CO2 concentration (e[CO2]) and more severe abiotic stresses have been scarcely investigated in woody plants, and an integrated view involving physiological, biochemical and molecular data is missing. This review highlights the effects of elevated CO2 in the metabolism of woody plants and the main findings of its interaction with abiotic stresses, including a molecular point of view, aiming to improve the understanding of how woody plants will face the predicted environmental conditions. Overall, e[CO2] stimulates photosynthesis and growth and attenuates mild to moderate abiotic stress in woody plants if root growth and nutrients are not limited. Moreover, e[CO2] does not induce acclimation in most tree species. Some high-throughput analyses involving omics techniques were conducted to better understand how these processes are regulated. Finally, knowledge gaps in the understanding of how the predicted climate condition will affect woody plant metabolism were identified, with the aim of improving the growth and production of this plant species.

1. Introduction

The concentration of greenhouse gases in the atmosphere has changed in the last millennium, mostly as a consequence of anthropogenic activities since the Industrial Revolution. The global warming effect observed from the middle 20th century is mainly driven by the high accumulation in the concentration of carbon dioxide (CO2) and other gases, such as methane (CH4), nitrous oxide (N2O) and ozone (O3), in the atmosphere [1]. Fossil-fuel burning and land-use change have contributed to the atmospheric CO2 rise over the years, from 283 ppm in the 1800s to the current global average level of ~418 ppm in 2022 [2,3,4]. As the emission rate of CO2 continues around the world, an increase of ~140 ppm is expected in the mid-century, which will probably reach ~1000 ppm by 2100 [5]. Additionally, climate changes involving higher temperatures (up to 4.8 °C) and extreme environmental conditions, such as severe drought, flooding, cold and heatwave events, are predicted to negatively impact all living species on the planet [6,7,8,9].
In this scenario, plant growth, phenological phases and development will be frequently challenged by climatic fluctuations, leading food security and food quality to be at risk in an increasing world population [10,11,12]. A range of studies over the years has been developed in an attempt to understand how plants will cope with elevated CO2 (e[CO2]), isolated or combined with other abiotic stresses, to identify new approaches to increase global sustainability and crop yield [13,14,15,16,17,18]. However, most of these are focused on photosynthesis and the growth rate of annual crops, leaving a gap in knowledge involving woody plants, especially in integrating physiological and molecular data. Besides their role in the ecosystem, many tree species have particular importance for worldwide agriculture production, and little is known about the effects of e[CO2] and other environmental stresses on their metabolism [19,20].
In the literature, the experiments involving woody plants exposed to e[CO2] are fragmented and controversial. The main reasons for these controversial results could be related to the short-term experiments considering the perennial characteristics of woody plants, the limitations to carrying out long-term experiments (e.g., pots and chambers size) and the high costs of field experiments. Nevertheless, in general, the responses include physiological, biochemical, molecular and morphological modifications which, in many cases, increase photosynthesis and water use efficiency and trigger stress defense mechanisms such as ROS (reactive oxygen species) scavenging [21,22,23,24,25,26]. Whether these responses activated by e[CO2] make woody plants more resistant to abiotic stresses and how the whole plant metabolism is regulated under these conditions are under investigation. We hypothesized that finding markers induced by e[CO2] is promising to improve the growth of woody plants exposed to adverse environmental conditions. Therefore, we outline here an integrative view of the effects of e[CO2] and other abiotic stresses on the growth and development of woody plants, specially selecting studies using large-scale “omics” technologies to depict molecular responses to e[CO2] to better understand how woody plants will cope with climate change (Table S1).

2. Woody Plant Growth and Development under Elevated CO2

2.1. Effect on Leaf Photosynthesis

Atmospheric e[CO2] usually stimulates the source activity of woody plants, but the response varies with species and exposure time. Initially, photosynthesis can be enhanced by the higher CO2 availability surrounding ribulose-1,5-bisphosphate (RuBP) carboxylase/oxygenase (Rubisco). Under these conditions, the carboxylation role of Rubisco is favored to the detriment of its oxygenation activity, increasing photosynthetic efficiency and the production of sugars. However, in some species, after an acclimation period, these reactions slow down or decrease when compared to the initial levels, mostly as a consequence of stomatal closure and/or soluble sugar accumulation in the mesophyll cells [27,28]. According to the FvCB model, photosynthesis can be limited biochemically by Rubisco activity, RuBP regeneration or triose phosphate utilization (TPU) [29,30,31]. Hence, as Rubisco’s substrate CO2 increases, a gradual decrease in photosynthesis by RuBP regeneration or TPU restrictions is expected [32]. Afterwards, the rise of internal CO2 partial pressure (Ci) and the accumulation of specific metabolites can culminate in a series of negative feedback regulations, such as a decrease in stomatal conductance (gS) and stomatal density and the inhibition of photosynthesis-related proteins [33,34].
However, many studies over the decades have shown that the behavior of gS on e[CO2] is contradictory and species-specific. Ainsworth and Rogers (2007) reported in a meta-analysis study from FACE (free-air concentration enrichment) experiments that e[CO2] decreased gS in all plant groups, but to less extent in trees compared to grasses and herbaceous crops [27]. In a previous meta-analysis work, specific to woody plants, Medlyn et al. (2001) found no reduction in gS after a short-term e[CO2] exposure (less than 1 year), while under long-term exposure (more than 1 year), gS decreased 23% [35]. Additionally, they reported that conifers are less sensitive to e[CO2] than deciduous and evergreen broadleaf species. Notably, some studies reported that particular coniferous trees (Pinus taeda and Pinus densiflora) have guard cells insensitive to e[CO2] [36,37]. This response corroborates the finding that gS-[CO2] sensitivity increased as tree species evolved (gymnosperms < deciduous angiosperms < evergreen angiosperms) due to atmospheric CO2 level changes over the years [20]. Purcell et al. (2018), using in situ measurements of 51 woody plants, demonstrate that gS can be increased in response to e[CO2] in specific weather conditions (high temperature and low humidity) depending on water availability [38]. Therefore, the downregulation of gS under e[CO2] in some studies might be more related to methodological artefacts involving differences in the climatic and/or measurements conditions, water status and/or nutrients and signal-to-noise ratio of gS [39] than an increase of Ci itself in the mesophyll and guard cells.
Stomatal size and density are other traits that could interfere with photosynthetic activity, but there is no clear evidence of this in woody plants in response to CO2 enrichment [27,40]. In Coffea exposed to long-term e[CO2], stomatal density and size showed dichotomous behavior, decreasing and increasing, respectively, without significant negative impacts on gS and CO2 assimilation [40]. An increase in leaf area index (LAI) is observed in growing season trees, which can offset any downregulation of gS on CO2 assimilation [41]. Nevertheless, after archive maturity, LAI tends to decrease in the upper layer of the canopy, reducing the shade effect and favoring light capture and photosynthesis in the whole shoot [25,41]. The coordination between gS and the photosynthetic rate was described in many plant species grown in several environmental conditions [42]. It is clear that the stomatal aperture should maximize CO2 uptake while minimizing water loss to increase photosynthesis and water use efficiency. However, the connection between gS and CO2 assimilation is diverse in woody plants, and while stomatal conductance does not seem to acclimate, photosynthesis does under e[CO2] [35].

2.2. Effect on Source–Sink Relationship and Nitrogen Metabolism

Photosynthetic downregulation after a long period of e[CO2] exposure has been termed CO2 acclimation, which was demonstrated in some species [43,44]. This response might be associated with the negative regulation of photosynthesis-related proteins, especially Rubisco, as in many cases reductions in Vcmax (in vivo Rubisco maximum carboxylation rate) are observed [44]. One hypothesis for this photosynthesis acclimation is the unbalance between source and sink activity. The accumulation of carbohydrates in source leaves (photosynthetic active) by the low utilization in sink tissues (non-photosynthetic) downregulates photosynthesis owing to negative feedback, decreasing the amount and activity of photosynthetic proteins [28,45,46]. The stimulation of photosynthesis by higher sink activity (root biomass) was observed in cassava (Manihot esculenta Crantz.) after e[CO2] acclimation [47]. Indeed, the export of photosynthates might increase to sink tissues by e[CO2] as plant growth increase and the expression/activity of sugar metabolism-related enzymes change [47,48,49].
A second hypothesis is related to nutrient dilution/acquisition, mainly nitrogen (N) and phosphorus (P), as a consequence of the rapid growth and/or allocation in sink tissues [50,51,52]. Rubisco is the most abundant protein in plants; then, a strong N-sink and reductions in its amount can be a common symptom of N deficiency and/or remobilization to other pathways, directly decreasing CO2 assimilation. Feng et al. (2015) reported a negative correlation between e[CO2] and plant N concentration in different ecosystems, including croplands, grasslands and forests. In this study, N limitation was more associated with the negative effects of e[CO2] on plant N uptake by unknown mechanisms rather than growth dilution [53]. The C/N unbalanced ratio seems to be related to the inhibition of photorespiration in plants exposed to e[CO2], as it was observed in a metabolic model that the levels of glycine and serine are correlated with de novo N assimilation [54]. However, the mechanisms underlying how e[CO2] limits N acquisition and if it is a cause or a consequence of photosynthesis acclimation are still open questions.
Actually, photosynthesis acclimation after e[CO2] exposure can be found in many plant species, especially in non-woody crops [46,55]. Nevertheless, it is a rare event in woody plants growing in normal conditions with no limitations of root growth space, water and nutrients [20,41]. For instance, tree species from northeast Asia grown under FACE conditions in infertile and immature volcanic ash (VA) and fertile brown forest (BF) soils for 2 years had different photosynthetic responses [56]. The photosynthesis of Betula platyphylla was downregulated in both soils, while in Betula maximowicziana, this response happened only in VA soil, probably due to the reduced N and Rubisco content. In contrast, a negative regulation in Alnus hirsute was observed only in BF soil, which might be related to higher amounts of starch in the leaves [56]. In many other studies, the photosynthetic rate in woody plants does not seem to acclimate, neither presenting any down-regulation nor even up-regulation [22,24,57,58].
High CO2 enhanced overall photosynthesis and Rubisco-specific activity, even with decreases in Rubisco content and photochemical parameters in Betula pendula [59,60]. A study with aspen tree (Populus tremuloides) exposed to e[CO2] revealed an increase in photosynthesis, despite the downregulation of many transcripts involved with chloroplast biosynthesis and function, including the photosynthetic protein genes Rubisco and Rubisco activase, proteins from photosystem I and II, light harvest complex and chlorophyll biosynthesis [61,62]. This transcriptional level pattern might be related to negative feedback triggered by the accumulation of sugars in leaves [62].
The carbohydrate level in source tissues is controlled by sink pathways (growth rate, respiration and storage/compartmentalization in certain organs), which tend to increase in high CO2-acclimated trees to keep a metabolic balance between synthesis and consumption. Respiration rate also responds in different ways according to the species and environmental conditions, and there is no immediate effect of high CO2 on mitochondrial respiration rate [63,64]. This process has been strongly increased in Eucalyptus saligna, while in Coffea spp. it has not been affected under e[CO2] [40,65]. Additionally, it has been demonstrated that leaf mitochondrial respiration could be unaffected by e[CO2], especially at night-time under mild temperatures, but the overall rate might be higher considering the whole plant leaf area, which usually increases in those conditions [65,66]. Some studies noticed a stimulation of gene expression and metabolite alterations of the TCA (tricarboxylic acid) cycle, such as citric, succinic, fumaric and malate acid in e[CO2]-enriched leaves [67,68].
In fact, the respiratory process in leaves should be slightly affected considering the photosynthetic stimulation in elevated CO2-exposed plants, as these are opposite reactions and strictly regulated. It is hypothesized that leaf respiration might be stimulated due to the higher concentration of non-structural carbohydrates (respiratory substrate), whereas the N dilution induced by elevated CO2 might reduce protein turnover and the demand for respiratory energy [65,69]. However, what has been reported to e[CO2] acclimated forest is an increase in fine root growth and rhizosphere respiration, indicating the export of photosynthates and utilization of heterotrophic respiration [7,70].
Therefore, the increase of belowground biomass and soil respiration might be a reason to support higher CO2 assimilation in trees fertilized with e[CO2] under non-stressful conditions, allowing a narrow connection between photosynthesis and ecosystem respiration [7,70]. The up-regulation expression of respiratory genes triggered by e[CO2] has been reported in leaves of non-woody plants [69,71]. However, the effect of e[CO2] focused on the respiration process at the transcriptional level of tree species is poorly investigated, particularly in roots.
Certainly, the behavior of source activity will depend on sink strength and how the whole plant metabolism will be adjusted to grow with the available resources. It is clear in the literature that woody plants will cope with e[CO2] by remodeling their metabolism to decrease the expression of key photosynthetic proteins, adjust nutrient distribution between the tissues and increase CO2 assimilatory capacity.

2.3. Growth and Developmental Stage-Dependent Regulation

The pattern of growth and establishment of woody plants exposed to e[CO2] will also depend on a wide range of factors—ultimately on species, genotype, developmental stage and environment. Studies linking physiological and molecular data are better documented in Populus genera, which is considered a model tree genus, than in other species [61,62,72,73,74,75,76]. In general, these works report photosynthesis and above-ground biomass stimulation with increases in stem wood density in high CO2-fertilized Populus, except for the triploid white poplar, which had lower photosynthesis but a higher stem diameter. The enhancement of shoot growth by e[CO2] was also observed in Pinus radiata [77], Pinus sylvestris [78], Acacia karroo and Acacia nilotica [22] and Aulonemia aristulata [58]. Along with this physiological response, the expression of genes from different categories in leaves and stems was strongly changed in P. deltoides [74]. In this work, stems showed more CO2-responsive transcripts than leaves (2.5-fold upregulated and 6.5-fold down-regulated in stems compared to leaves), and most of them were related to metabolism. The main enhanced genes in leaves were those involved with storage proteins and wall expansion, whereas in stems, they were more related to lignin biosynthesis (enzymes responsible for lignin formation and polymerisation and ethylene response factors), cell wall formation and cell growth, corroborating the growth stimulation response.
The effects of e[CO2] in plant metabolism also rely on the developmental stage of each species [61,79,80]. The gene expression pattern was dependent on leaf age in elevated CO2-acclimated Populus [61]. While in young leaves, the most differentially expressed genes were upregulated, in semimature leaves, were downregulated under e[CO2]. This environmental condition upregulated 16-photosynthetic gene transcripts, including Rubisco small subunit, in young leaves compared to older leaves [61]. Certainly, the predicted elevated CO2 atmosphere concentration will change the carbon (C) status in plants. Some studies have suggested that the leaf development pattern is likely to be accelerated by e[CO2], as gene expression related to photosynthesis, cell-wall loss and synthesis (xyloglucan endotransglycosylase) and calcium-signaling (CPK2) were up-regulated in young leaves [61,81]. These findings support the hypothesis of growth promotion and sucrose-cleaving and synthesizing enzyme activity modifications by CPKs under e[CO2] [82,83]. Moreover, in mature leaves, the C flux can be redirected to the glycolysis pathway once the transcripts for adenylate kinase are upregulated [61].
A commonly raised question would be whether leaf senescence is intensified in woody CO2-fertilized plants, once growth and LAI are generally increased. Different groups demonstrated that senescence-related gene (β-amylase and metallothioneins) expression and proteins were lower and, consequently, leaf longevity was augmented in e[CO2]-acclimated plants [61,62,73,80]. Moreover, a transcriptome study in Populus demonstrated that delayed senescence was correlated with the up-regulation of glycolysis and secondary metabolism genes, including anthocyanin biosynthesis-related genes (leucoanthocyanidin dioxygenase–LDOX, and dihydroflavonol reductase–DFR) [75].
Therefore, despite the limited studies, the findings obtained so far with woody species suggest that e[CO2] will increase plant growth through modifications in C allocation to different pathways (secondary metabolism) and organs (stem) and will also affect the ecosystem of soil microorganisms by enhancing respiratory substrates (fine roots turnover) [61,73,74,75]. Besides this, lignin accumulation in stems could contribute to pathogen resistance but may negatively impact the wood quality for both timber and paper production [74]. Hence, CO2-fertilized trees may not act directly to C sequestration, and the metabolic pathway changes may not be desired by agriculture. To better understand how e[CO2] will affect woody plant metabolism, more studies are needed, especially under the projected climate change scenarios.

3. Integrative Responses of Woody Plants under Elevated CO2 and Other Abiotic Stresses

Taking the main impact of e[CO2] on woody plant metabolism, photosynthesis and growth will tend to increase, as mentioned before. However, in addition to the accumulation of atmospheric [CO2], warm days and nights and an increased frequency of heat waves and drought, which contribute to land salinization and decrease in soil fertility, are expected worldwide [6,84]. These abiotic stresses, in addition to O3 tropospheric accumulation (secondary pollutant), are considered the primary causes of crop loss around the globe, reducing average yields and quality [18,85,86]. To grow and develop in such adverse conditions, plant metabolism must be completely rearranged, including changes at morphological, physiological, biochemical and molecular levels. The main findings obtained so far with woody plants exposed to the predicted climate changes are detailed in this work, aiming to answer the following questions: Will e[CO2] mitigate the negative effects of abiotic stresses? How will woody plants face multiple environmental adverse conditions?

3.1. Effects of Elevated CO2 and Heat Stress

The exponential accumulation of CO2 concentration in the atmosphere is considered the main driver of global warming. Since the pre-industrial era, along with the 129 ppm CO2 increase, the temperature has increased by 0.85 °C. According to the Intergovernmental Panel on Climate Change [6,87], it is expected that atmospheric CO2 levels will increase from the current 412 ppm to 936 ppm along with warmer weather, with temperatures rising between 0.3–1.7 °C in a mild scenario or even 2.6–4.8 °C in a severe scenario. Plant growth and development are directly dependent on air temperature, which determines the distribution of species around the planet [88]. However, supra-optimal temperatures lead to heat stress, which restricts plant growth and productivity by affecting water relations, membrane fluidity and stability (with negative impacts on the chloroplast and mitochondria reactions) and the whole metabolism [89,90]. In order to control water status under high temperatures, plants often reduce stomatal aperture, which further decreases CO2 flux and photosynthesis [91]. Moreover, in that condition, gas solubility increases, affecting the availability of O2/CO2 next to Rubisco active sites, which stimulate photorespiration and respiration, modifying plant energetic metabolism [27].
Therefore, it can be hypothesized that the negative impact of high temperature could be mitigated or plant growth could even be improved under the simultaneous increase of CO2, since e[CO2] increases photosynthesis and water use efficiency. In fact, many studies with different plant species reported that e[CO2] positively influenced photosynthesis and biomass yield under high-temperature conditions [15,92,93,94,95,96]. Despite the investigation of this, environmental studies involving trees are scarce and focused on physiological and biochemical approaches, although they clearly suggest that these species could take advantage of e[CO2] under higher temperatures if water and nutrient supplies and root growth space were sufficient. A study with two Eucalyptus species (E. saligna and E. sideroxylon) seedlings exposed to elevated CO2 (650 ppm) and temperature (ambient +4 °C) showed that each isolated condition stimulated photosynthesis and growth by increasing light-saturated photosynthesis, light and CO2-saturated photosynthesis and a maximal electron transport rate with no interaction between e[CO2] and high-temperature treatments [93,97]. Despite the lack of interaction, these results indicate that, in the future, plants such as eucalyptus could take advantage of e[CO2] under high temperatures by enhancing growth and potentially performing C sequestration if water and nutrients were sufficiently supplied.
It was demonstrated that e[CO2] ameliorated the negative impacts of high temperature in two Coffea species: C. arabica and C. canephora [96,98,99]. In these works, the combination of e[CO2] and high temperature (from 25 °C to 42 °C) improved photochemical efficiency, energy use and biochemical functioning in both species, particularly in the warmer condition, when compared to plants grown at ambient [CO2]. The better performance of coffee plants at higher temperatures and e[CO2] was related to the induction of protective molecules, such as antioxidants and molecular chaperones, which favored the maintenance of ROS at controlled levels and metabolism function [98]. Furthermore, Rodrigues et al. (2016) and Martins et al. (2016) reported that C. arabica and C. canephora are heat tolerant up to 37 °C, and irreversible effects of the extreme temperature threshold (42 °C) were strongly attenuated by e[CO2] [96,98]. The transcriptomic analysis in these Coffea genotypes exposed to the combination of heat and e[CO2] revealed a genotype-dependent gene expression [99].
This environmental condition resulted in differential expressed genes (DEGs) related to photosynthetic and biochemical processes. At the highest temperature (42 °C), the most responsive genes were down-regulated, especially in C. arabica rather than C. canephora. These DEGs were related to specialized metabolism, the lignin catabolic process in C. arabica (suggesting a decrease in lignin synthesis) and to molecular functions linked to calcium ion binding, oxidoreductase, sulfotransferase and xyloglucan:xyloglucosyl transferase activity in C. canephora (suggesting a decrease in cellulose synthesis). Moreover, the DEGs involved with photosynthetic and chlorophyll metabolic processes were up-regulated at 37 °C and down-regulated at 42 °C in C. arabica and down-regulated in both elevated temperatures in C. canephora compared to 25 °C [99] The down-regulated genes at 42 °C were related to photosynthesis, including Rubisco and Rubisco activase, and proteins involved with PSII assembly, stability and repair (PsbQ and PsbP). The authors reinforced the mitigating role of e[CO2] to extreme heat by keeping higher photosynthetic performance than plants under ambient CO2, especially in C. canephora plants [99]. Altogether, these results reveal that e[CO2] mitigates the effects of supra-optimal temperatures by keeping an integrated metabolism between photochemical efficiency, CO2 assimilation and specialized metabolism. These sink energy processes coupled with the stimulation of antioxidant pathways might be related to the maintenance of thylakoid membrane proteins and the maximum PSII quantum efficiency (Fv/Fm) under heat stress.
The effect of heat and e[CO2] on C. arabica bean quality was also investigated by Ramalho et al. (2018) [100]. It was observed that elevated temperature depreciates bean quality, but this effect was attenuated by the interaction with e[CO2], which kept bean properties closer to or even better than (higher acidity and more stable levels of O-caffeoylquinic acids) that obtained under control conditions. Therefore, woody plants might take advantage of e[CO2] to deal with mild high temperatures by enhancing photosynthetic machinery, cell wall composition and specialized metabolites that could be involved in stress signaling and defense.

3.2. Effects of Elevated CO2 and Drought

Climate change is completely altering the way we cultivate crops, as precipitation patterns are becoming scarce and drought events more frequent [6]. Furthermore, the expected higher temperatures, as mentioned above, will increase the leaf-to-air vapor pressure deficit (VPD), intensifying the dry effects on plants [101]. The increase in frequency and duration of drought has been associated with tree growth declines, mortality and regeneration reduction worldwide [102,103,104]. Stomatal closure, in response to abscisic acid (ABA) accumulation on leaves, is the initial response triggered by drought aiming to minimize water loss [105]. However, this response also contributes to decreasing CO2 assimilation, which may lead to insufficient carbohydrate supply for metabolism and cause plant death [106]. Therefore, it can also be hypothesized that the enrichment of CO2 ameliorates the negative effects of drought, taking into account the benefits of e[CO2] already mentioned. To test this hypothesis, some studies were performed employing physiological and biochemical approaches in field or greenhouse conditions.
However, it seems that some species will not benefit from the future predicted conditions, as demonstrated by Populus deltoides and Liquidambar styraciflua (sweetgum) [107,108]. In fact, the benefits caused by e[CO2] to decrease water loss by reducing stomatal conductance can be offset by the leaf area increase, which can be noticed in some woody plants [107]. Hence, Bobich et al. (2010) noticed that P. deltoides under e[CO2] in the field would be more susceptible to drought, as in that condition, these trees showed greater stomatal density and lower wood density than trees under ambient CO2 [107]. Both traits may facilitate xylem cavitation under severe drought. Later, it was demonstrated that e[CO2] promoted higher leaf senescence and abscission in temperate trees of sweetgum under severe summer drought when compared with ambient CO2 conditions [108]. In this study, the authors also showed that the canopy conductance and modelled photosynthesis were lower in stands exposed to e[CO2] than in ambient CO2. These responses could reduce latent heat loss and thereby elevate leaf temperature, which may decrease photosynthesis and increase respiration and further exacerbate the negative effects of drought [108].
It is worth considering that these first investigations were performed under natural field conditions in southern Arizona and eastern Tennessee (USA), in which the effect of e[CO2] was combined with multiple stresses (drought, high temperature and high deficit pressure vapor) characterizing severe drought. Moreover, these responses involve only two species with no well-watered stand to compare with, and some of the parameters were estimated and not properly measured. Therefore, more studies are needed to better understand how woody plants will cope with e[CO2] and drought in the near future.
Later, Bachofen et al. (2018) reported that pine seedlings (Pinus sylvestris and Pinus nigra) acclimated to high CO2 were not more susceptible to drought than plants grown under ambient CO2 [109]. These plant groups showed similar starch concentration, biomass production and mortality when subjected to water deficit in a semi-controlled condition. Another recent research work verified that drought-stressed Pinus halepensis (Aleppo pine) fertilized with e[CO2] had higher total biomass, net photosynthesis, water use efficiency and water potential, without changes in respiration rate, compared to ambient CO2-acclimated plants [110]. These results also concur with what has been reported on Coffea arabica plants under controlled or natural conditions [49,68,111,112,113,114]. In these studies, e[CO2] mitigated the negative effects of water deficit by increasing CO2 assimilation, photochemical efficiency, water use efficiency and soluble solutes content, decreasing photorespiration rate and oxidative pressure and keeping hydraulic conductance. The increase of water use efficiency is a common response triggered by e[CO2], as plants can keep lower stomatal conductance to uptake atmospheric CO2 without increasing leaf transpiration. Therefore, woody plant growth under drought is benefited by e[CO2], as already reported [68,110,111,113,114]. Moreover, the buffer effect of e[CO2] under drought conditions could be related to changes in specialized metabolites such as 5-O-caffeoylquinic acid (5-CQA) and caffeine [113].
Recently, studies have demonstrated that the buffering effect of e[CO2] in Coffea plants exposed to different levels of water deficit is genotype-dependent [114,115]. Elevated CO2 attenuated the negative drought impacts in C. canephora cv. Conilon and maintained the high tolerance to drought in C. arabica cv. Icatu plants [114]. While in Conilon plants, e[CO2] improved the photochemical efficiency by increasing the PSII efficiency and decreasing the thermal energy dissipation, this beneficial effect in Icatu plants was slight and more related to keeping the abundance of photosynthetic proteins and the cyclic electron flow at PSI under moderate or severe drought conditions [114]. The contrasting effect of e[CO2] in these Coffea genotypes exposed to different water deficit conditions was also noticed at the metabolic level [115]. While the abundance of the most primary metabolites (mainly amino acids) decreased in Conilon, they increased in Icatu exposed to the combination of e[CO2] and drought [115]. The metabolite profile was more affected by severe water deficit regardless of CO2 in both genotypes, except for Icatu plants under moderate water deficit and e[CO2], which were close to well-watered plants, suggesting a beneficial effect of CO2 enrichment in moderate drought conditions.

3.3. Effects of Elevated CO2 and Salinity

Land salinization is one of the major abiotic stresses that negatively impact plant growth and survival, especially in semiarid and arid regions [116]. This problem is increasing worldwide as a consequence of climate change, deforestation and irrigation practices [117,118,119]. Soil salinity is a serious threat to agriculture that already affects more than 6% of the total land area and 30% of the irrigated farmland around the globe [120,121]. Despite also being a problem for native plants and non-agriculture lands, the effects of salt stress are much less recognized and investigated in natural systems [122]. Plant physiology and development are adversely impacted by salinity through both osmotic and ionic stresses. In general, the accumulation of solutes in the soil limits root water uptake, decreasing photosynthesis, transpiration and plant growth [123]. Further, the high concentration of ions (i.e., Na+ and Cl) in leaves can lead to an alteration of K+ homeostasis and disrupt plant biochemical processes [124]. This condition can alter cellular protein structure, reduce photosynthesis and increase reactive oxygen species (ROS) [124].
The effect of salinity in woody plants is poorly studied, and much less is known about the interaction between this abiotic stress and e[CO2] and how this species will cope with this condition in the future. Investigating the simultaneous supply of e[CO2] and salinity on two cultivars of Olea europaea L. (cv. Picual–salt tolerant and cv. Koroneiki–salt sensitive), it was observed that salt stress decreased the positive effects of e[CO2], especially in the sensitive cultivar [125]. Additionally, e[CO2] enhanced WUE under salt stress on both cultivars and decreased salt ion uptake in the sensitive cultivar. A short treatment with high CO2 also alleviated the toxic effects of salt stress, favoring a higher K+/Na+ ratio than ambient CO2 cashew (Anacardium occidentale) plants [126]. In that study, e[CO2] decreased the activity of glycolate oxidase and the concentration of hydrogen peroxide (H2O2), NH4+ and glyoxylate in salt-stressed plants, suggesting a higher photoprotection and lower photorespiration rate than plants acclimated to ambient CO2. These responses related to the buffer effects of e[CO2] under salt stress corroborate with what has been found in non-woody plants, which showed better control of water status, osmotic adjustment and antioxidant activity [127,128,129].

3.4. Effects of Elevated CO2 and Ozone

Besides the accumulation of atmospheric CO2 amount, the increase of tropospheric ozone concentration (O3) has also been noticed, contributing to the greenhouse effect and negatively impacting plant growth [18]. This gas is a secondary pollutant synthesized from the photochemical oxidation of NOx in the presence of carbon monoxide (CO), methane (CH4) and non-methane hydrocarbons [130]. Tropospheric O3 can increase in the future, as the expected climate change scenarios (summer droughts and heatwaves conditions) favor its accumulation [86]. In general, high O3 induces oxidative stress in plants, which has contributed to large decreases in gross primary productivity in Europe (3–9%), China (10–18%) and the U.S. (5–10% for soybean and maize) in the last decades [131,132,133]. Therefore, considering the positive effects of e[CO2], some studies were developed aiming to investigate whether CO2 could ameliorate the stress induced by high O3 in the woody species aspen and birch.
In fact, high O3 caused foliar damage in Populus tremuloides due to reductions in chlorophyll, carotenoid, starch and Rubisco concentration and the transcription level of Rubisco small subunit [21]. The plants also showed higher activity of antioxidant enzymes (ascorbate peroxidase, catalase and glutathione reductase), phenylalanine ammonia-lyase (PAL) and 1-aminocyclopropane-1-carboxylic acid (ACC)-oxidase transcript levels. The combination with e[CO2] decreased the visible leaf injury and leaf growth but did not offset the main harmful effects of O3 as the activity of antioxidant enzymes and PAL decreased, which could exacerbate the stress by high O3 exposure in aspen [21]. The long acclimation of P. tremuloides to e[CO2] and high O3 revealed a different pattern of transcripts expression when analyzed either isolated or combined [72]. While e[CO2] up-regulated only small numbers of genes, high O3 increased the expression of many signaling and defense-related genes and decreased the expression of several photosynthetic and energy-related genes. Surprisingly, the combination of treatments (CO2 + O3) resulted in the differential expression of genes that were not up-regulated under the isolated conditions.
The studies involving birch (Betula pendula and Betula papyrifera) demonstrated that the effect of elevated O3 was variable and clone-dependent [59,60,80,134,135]. In those works, some sensitivity clones showed reductions in photosynthetic rate and advanced leaf senescence when exposed to high O3. The combination with e[CO2] had a synergistic effect and partially buffered the stress caused by O3 in the plants. This response was related to the higher carbon/nitrogen ratio, in which the greater quantity of carbohydrates may be used to detoxify and repair cell damage under elevated O3 and CO2 [80,134]. The buffer effect of e[CO2] in plants exposed to high O3 can also be involved with the decreased stomatal conductance triggered by the first gas, allowing a smaller amount of O3 flux into leaves and therefore less damage [21,136]. In addition to that, the lower O3 inside the leaves may less effectively induce the antioxidant system when combined with e[CO2] than under isolated high O3 [80].
The combination of elevated CO2 and O3 also increased the gene expression of proteins related to glycolysis, suggesting the requirement of energy and carbon skeletons for biosynthetic pathways and differential expression of genes related to steroid biosynthesis (increase of farnesyl-PP and phytyl-PP and decrease of pre-squalene and squalene) [80]. Indeed, the negative effects of O3 were smaller when combined with e[CO2], indicating that both gases induce a synergistic response in woody plants when applied simultaneously. Moreover, the studies with long-term exposure demonstrated that O3 sensitivity changes according to the growth stage and environmental conditions (season), where stressful conditions increase the O3 sensitivity [59,134]. The alleviation of O3 stress by e[CO2] can also be temporary, as demonstrated on Betula pendula, which showed a gene expression, phenology and physiology in August similar to plants exposed to e[CO2] alone, while in September, these traits were similar to plants exposed to high O3 alone [135].

3.5. Effects of Elevated CO2 and Multiple Stresses

Most of the studies mentioned above in this review considered the effect of e[CO2] combined with one abiotic stressor. The main responses associated or in common with specific conditions are highlighted in Figure 1. In general, the physiological responses are supported by biochemical and molecular data. Elevated CO2 decreases the negative effects of stress, such as photorespiration, oxidative stress, salt uptake and leaf senescence, and increases photosynthetic and water use efficiencies, plant biomass, the antioxidant system and the synthesis of carbohydrates, amino acids and specialized metabolites.
However, trees are constantly exposed to multiple stresses in the natural environment, and the effects on plant metabolism between e[CO2] and multiple stresses might be different. This condition was investigated in Alnus hirsuta and Alnus maximowiczii under e[CO2], phosphorus (P) availability and drought, which demonstrated the benefit of e[CO2] on N2 fixation by increasing nodule biomass under a high P supply [137]. This positive effect was absent under low P concentration, indicating that the e[CO2]-buffer effect is dependent on nutrient supplementation. This corroborates what has been found in Eucalyptus tereticornis, the growth of which was improved by e[CO2] under heat and sufficient soil P concentration [138]. The mitigating effect of e[CO2] in Quercus rubra and Eucalyptus seedlings exposed to high temperature and low water supply was reported by Bauweraerts et al. (2013) and Lewis et al. (2013), respectively [19,139]. It was observed that the extreme heat events differently affect growth and gas exchange when compared to constant high temperature, reinforcing the idea that the environmental fluctuations are important to consider to better understand plant performance in their natural condition [139]. Additionally, it was noticed that e[CO2] buffered the effect of heat treatments regardless of water availability, but this response is plant species and stress level-dependent [19,139].
Therefore, elevated e[CO2] buffers the negative effects of mild/moderate abiotic stress by improving the photosynthetic rate through Rubisco activity and increasing the concentration of primary metabolites. Possible negative feedback regulates stomatal aperture and increases water use efficiency. Moreover, there is evidence for alterations in other metabolic pathways, such as the enhancement of aquaporin genes, protective proteins (chaperones and antioxidative system), specialized metabolites, nutrient requirement, changes in the respiratory rate and a decrease of genes and proteins involved with leaf senescence. However, the mechanisms involved in these processes are poorly understood, especially the molecular bases. As the stress becomes severe, the beneficial role of e[CO2] is offset, probably as a consequence of stomatal closure and the severe cell damage caused by the stress (Figure 2).

4. Concluding Remarks

This review highlighted the main effects of elevated CO2 alone and combined with abiotic stresses in woody plants, focusing on the understanding of the extent to which e[CO2] should mitigate the predicted climate change scenarios and how molecular mechanisms should respond to these environments. In general, e[CO2] increases photosynthetic efficiency, with little or no photosynthetic acclimation, and biomass and buffers the negative effects of most abiotic stresses when they are not severe and no growth limitations are imposed, such as root growth and nutrient availability (Figure 1 and Figure 2).
The integration of modern omics (genomics, transcriptomics, proteomics, metabolomics and ionomics) along with gene editing offered a better understanding of the genetic and molecular basis of staple crops, allowing the production/selection of more resilient and productive cultivars [140]. However, these molecular approaches have been poorly applied to woody plants, especially involving the interaction with multiple abiotic stresses, making it unclear how the increase of atmospheric CO2 will affect tree species and forest ecosystems. Therefore, more studies that supply an integrative view of powerful tools (physiological, biochemical and molecular) and the combination of e[CO2] and abiotic stresses are needed to better understand the effects of these conditions on woody plant metabolism. Finally, this deep level of knowledge could be applied to select/produce more resilient and productive plants and also to create strategies to maintain agricultural and forest productivity and environmental sustainability.

Supplementary Materials

The following supporting information can be downloaded at: ****. Table S1. Overview of studies with woody species exposed to elevated CO2 alone or combined with abiotic stresses. * Studies involving molecular approaches.

Author Contributions

Conceptualization, A.K.M.L., E.A.S., D.C.C. and D.S.D.; formal analysis, A.K.M.L.; investigation, A.K.M.L. and I.C.A.C.; resources, E.A.S. and D.S.D.; data curation, I.C.A.C., E.A.S., D.C.C. and D.S.D.; writing—original draft preparation, A.K.M.L.; writing—review and editing, A.K.M.L., I.C.A.C., E.A.S., D.C.C. and D.S.D.; supervision, E.A.S. and D.S.D.; project administration, A.K.M.L., E.A.S. and D.S.D.; funding acquisition, E.A.S., D.C.C. and D.S.D. All authors have read and agreed to the published version of the manuscript.


This research was supported by São Paulo State Research Support Foundation (Fundação de Amparo à Pesquisa do Estado de São Paulo—FAPESP), National Council for Scientific and Technological Development (Conselho Nacional de Desenvolvimento Científico e Tecnológico—CNPq), and Coordination for the Improvement of Higher Education Personnel (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior–CAPES). FAPESP grant numbers #2018/08042-8 and #2021/06364-0, and fellowship number #2019/26850-7 to AKML. CAPES academic scholarship (Code 001) to ICAC.

Informed Consent Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.


  1. Vergara, W.; Rios, A.R.; Trapido, P.; Malarín, H. Agriculture and Future Climate in Latin America and the Caribbean: Systemic Impacts and Potential Responses. Inter-Am. Dev. Bank 2014, No. IDB-DP, 1–20. [Google Scholar]
  2. Dlugokencky, E.J.; Hall, B.D.; Montzka, S.A.; Dutton, G.; Mühle, J.E.J.W. Long-lived greenhouse gases. In State of the Climate in 2017; American Meteorological Society: Boston, MA, USA, 2018; Volume 99, pp. S46–S49. [Google Scholar]
  3. Burton, D.A. Sea-Level Information. Available online: (accessed on 1 July 2022).
  4. NOAA. National Oceanic and Atmospheric Administration. 2020. Available online: (accessed on 1 July 2022).
  5. Hartmann, D.L.; Tank, A.M.G.K.; Rusticucci, M.; Alexander, L.V.; Brönnimann, S.; Charabi, Y.; Dentener, F.J.; Dlugokencky, E.J.; Kaplan, A.; Soden, B.J.; et al. Observations: Atmosphere and surface. In Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change; Stocker, T.F., Qin, D., Plattner, G.-K., Eds.; Cambridge University Press: Cambridge, UK; New York, NY, USA, 2013; pp. 159–254. [Google Scholar]
  6. IPCC. Contribuição do Grupo de Trabalho II para o Quinto Relatório de Avaliação do Painel Intergovernamental Sobre Alterações Climáticas (IPCC); IPCC: Geneva, Switzerland, 2014; ISBN 978-972-9083-18-1. [Google Scholar]
  7. Dusenge, M.E.; Duarte, A.G.; Way, D.A. Plant carbon metabolism and climate change: Elevated CO2 and temperature impacts on photosynthesis, photorespiration and respiration. New Phytol. 2019, 221, 32–49. [Google Scholar] [CrossRef][Green Version]
  8. DaMatta, F.M.; Avila, R.; Cardoso, A.A.; Martins, S.C.V.; Ramalho, J.C. Physiological and Agronomic Performance of the Coffee Crop in the Context of Climate Change and Global Warming: A Review. J. Agric. Food Chem. 2018, 66, 5264–5274. [Google Scholar] [CrossRef]
  9. Hartmann, H.; Bastos, A.; Das, A.J.; Esquivel-Muelbert, A.; Hammond, W.M.; Martínez-Vilalta, J.; McDowell, N.G.; Powers, J.S.; Pugh, T.A.; Ruthrof, K.X.; et al. Climate Change Risks to Global Forest Health: Emergence of Unexpected Events of Elevated Tree Mortality Worldwide. Annu. Rev. Plant Biol. 2022, 73, 673–702. [Google Scholar] [CrossRef]
  10. Anderson, R.; Bayer, P.E.; Edwards, D. Climate change and the need for agricultural adaptation. Curr. Opin. Plant Biol. 2020, 56, 197–202. [Google Scholar] [CrossRef]
  11. Cataldo, E.C.; Salvi, L.S.; Paoli, F.P.; Fucile, M.F.; Masciandaro, G.M.; Manzi, D.M.; Mansini, C.M.; Mattii, G.B.M. Effects of natural clinoptilolite on physiology, water stress, sugar, and anthocyanin content in Sanforte (Vitis vinifera L.) young vineyard. J. Agric. Sci. 2021, 7–8, 488–499. [Google Scholar] [CrossRef]
  12. Cataldo, E.; Fucile, M.; Mattii, G.B. Effects of Kaolin and Shading Net on the Ecophysiology and Berry Composition of Sauvignon Blanc Grapevines. Agriculture 2022, 4, 491. [Google Scholar] [CrossRef]
  13. Wong, S.C. Elevated atmospheric partial pressure of CO2 and plant growth-I. Interactions of nitrogen nutrition and photosynthetic capacity in C3 and C4 plants. Oecologia 1979, 44, 68–74. [Google Scholar] [CrossRef]
  14. Moore, B.D.; Palmquist, D.E.; Seemann, J.R. Influence of plant growth at high CO2 concentrations on leaf content of ribulose-1,5-bisphosphate carboxylase/oxygenase and intracellular distribution of soluble carbohydrates in tobacco, snapdragon, and parsley. Plant Physiol. 1997, 115, 241–248. [Google Scholar] [CrossRef][Green Version]
  15. Taub, D.R.; Seemann, J.R.; Coleman, J.S. Growth in elevated CO2 protects photosynthesis against high-temperature damage. Plant Cell Environ. 2000, 23, 649–656. [Google Scholar] [CrossRef][Green Version]
  16. Xu, Z.; Jiang, Y.; Zhou, G. Response and adaptation of photosynthesis, respiration, and antioxidant systems to elevated CO2 with environmental stress in plants. Front. Plant Sci. 2015, 6, 1–17. [Google Scholar] [CrossRef][Green Version]
  17. Gamage, D.; Thompson, M.; Sutherland, M.; Hirotsu, N.; Makino, A.; Seneweera, S. New insights into the cellular mechanisms of plant growth at elevated atmospheric carbon dioxide concentrations. Plant Cell Environ. 2018, 41, 1233–1246. [Google Scholar] [CrossRef]
  18. Ainsworth, E.A.; Lemonnier, P.; Wedow, J.M. The influence of rising tropospheric carbon dioxide and ozone on plant productivity. Plant Biol. 2020, 22, 5–11. [Google Scholar] [CrossRef][Green Version]
  19. Lewis, J.D.; Smith, R.A.; Ghannoum, O.; Logan, B.A.; Phillips, N.G.; Tissue, D.T. Industrial-age changes in atmospheric [CO2] and temperature differentially alter responses of faster- and slower-growing Eucalyptus seedlings to short-term drought. Tree Physiol. 2013, 33, 475–488. [Google Scholar] [CrossRef][Green Version]
  20. Klein, T.; Ramon, U. Stomatal sensitivity to CO2 diverges between angiosperm and gymnosperm tree species. Funct. Ecol. 2019, 33, 1411–1424. [Google Scholar] [CrossRef]
  21. Wustman, B.A.; Oksanen, E.; Karnosky, D.F.; Noormets, A.; Isebrands, J.G.; Pregitzer, K.S.; Hendrey, G.R.; Sober, J.; Podila, G.K. Effects of elevated CO2 and O3 on aspen clones of varying O3 sensitivity. Dev. Environ. Sci. 2003, 3, 391–409. [Google Scholar] [CrossRef]
  22. Kgope, B.S.; Bond, W.J.; Midgley, G.F. Growth responses of African savanna trees implicate atmospheric [CO2] as a driver of past and current changes in savanna tree cover. Austral Ecol. 2010, 35, 451–463. [Google Scholar] [CrossRef]
  23. AbdElgawad, H.; Zinta, G.; Beemster, G.T.S.; Janssens, I.A.; Asard, H. Future climate CO2 levels mitigate stress impact on plants: Increased defense or decreased challenge? Front. Plant Sci. 2016, 7, 556. [Google Scholar] [CrossRef][Green Version]
  24. Damatta, F.M.; Godoy, A.G.; Menezes-Silva, P.E.; Martins, S.C.V.; Sanglard, L.M.V.P.; Morais, L.E.; Torre-Neto, A.; Ghini, R. Sustained enhancement of photosynthesis in coffee trees grown under free-air CO2 enrichment conditions: Disentangling the contributions of stomatal, mesophyll, and biochemical limitations. J. Exp. Bot. 2016, 67, 341–352. [Google Scholar] [CrossRef][Green Version]
  25. Rakocevic, M.; Ribeiro, R.V.; Ribeiro Marchiori, P.E.; Filizola, H.F.; Batista, E.R. Structural and functional changes in coffee trees after 4 years under free air CO2 enrichment. Ann. Bot. 2018, 121, 1065–1078. [Google Scholar] [CrossRef]
  26. Rahman, M.; Islam, M.; Gebrekirstos, A.; Braüning, A. Disentangling the effects of atmospheric CO2 and climate on intrinsic water-use efficiency in South Asian tropical moist forest trees. Tree Physiol. 2020, 40, 904–916. [Google Scholar] [CrossRef]
  27. Ainsworth, E.A.; Rogers, A. The response of photosynthesis and stomatal conductance to rising [CO2]: Mechanisms and environmental interactions. Plant Cell Environ. 2007, 30, 258–270. [Google Scholar] [CrossRef]
  28. Lobo, A.K.M.; de Oliveira Martins, M.; Lima Neto, M.C.; Machado, E.C.; Ribeiro, R.V.; Silveira, J.A.G. Exogenous sucrose supply changes sugar metabolism and reduces photosynthesis of sugarcane through the down-regulation of Rubisco abundance and activity. J. Plant Physiol. 2015, 179, 113–121. [Google Scholar] [CrossRef]
  29. Farquhar, G.D.; Caemmerer, S.; Berry, J.A. A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 1980, 149, 78–90. [Google Scholar] [CrossRef][Green Version]
  30. Von Caemmerer, S.; Farquhar, G.D. Some relationships between the biochemistry of photosynthesis and the gas exchange of leaaves. Planta 1981, 153, 376–387. [Google Scholar] [CrossRef]
  31. von Caemmerer, S. Biochemical models of leaf photosynthesis. In Techniques in Plant Science, No. 2; CSIRO Publishing: Clayton, Australia; Collingwood: Melbourne, Australia, 2000. [Google Scholar]
  32. Sharkey, T.D.; Stitt, M.; Heineke, D.; Gerhardt, R.; Raschke, K.; Heldt, H.W. Limitation of Photosynthesis by Carbon Metabolism: II. O₂- Insensitive CO₂ Uptake Results from Limitation of Triose Phosphate Utilization. Plant Physiol. 1986, 81, 1123–1129. [Google Scholar] [CrossRef]
  33. Gago, J.; De Menezes Daloso, D.; Figueroa, C.M.; Flexas, J.; Fernie, A.R.; Nikoloski, Z. Relationships of leaf net photosynthesis, stomatal conductance, and mesophyll conductance to primary metabolism: A multispecies meta-analysis approach. Plant Physiol. 2016, 171, 265–279. [Google Scholar] [CrossRef]
  34. Hsu, P.K.; Takahashi, Y.; Munemasa, S.; Merilo, E.; Laanemets, K.; Waadt, R.; Pater, D.; Kollist, H.; Schroeder, J.I. Abscisic acid-independent stomatal CO2 signal transduction pathway and convergence of CO2 and ABA signaling downstream of OST1 kinase. Proc. Natl. Acad. Sci. USA 2018, 115, E9971–E9980. [Google Scholar] [CrossRef][Green Version]
  35. Medlyn, B.E.; Barton, C.V.M.; Broadmeadow, M.S.J.; Ceulemans, R.; De Angelis, P.; Forstreuter, M.; Freeman, M.; Jackson, S.B.; Kellomäki, S.; Laitat, E.; et al. Stomatal conductance of forest species after long-term exposure to elevated CO2 concentration: A synthesis. New Phytol. 2001, 149, 247–264. [Google Scholar] [CrossRef]
  36. Ellsworth, D.S. CO2 enrichment in a maturing pine forest: Are CO2 exchange and water status in the canopy affected? Plant Cell Environ. 1999, 22, 461–472. [Google Scholar] [CrossRef]
  37. Kogawara, S.; Norisada, M.; Tange, T.; Yagi, H.; Kojima, K. Elevated atmospheric CO2 concentration alters the effect of phosphate supply on growth of Japanese red pine (Pinus densiflora) seedlings. Tree Physiol. 2006, 26, 25–33. [Google Scholar] [CrossRef][Green Version]
  38. Purcell, C.; Batke, S.P.; Yiotis, C.; Caballero, R.; Soh, W.K.; Murray, M.; McElwain, J.C. Increasing stomatal conductance in response to rising atmospheric CO2. Ann. Bot. 2018, 121, 1137–1149. [Google Scholar] [CrossRef][Green Version]
  39. Konrad, W.; Roth-Nebelsick, A.; Grein, M. Modelling of stomatal density response to atmospheric CO2. J. Theor. Biol. 2008, 253, 638–658. [Google Scholar] [CrossRef]
  40. Ramalho, J.C.; Rodrigues, A.P.; Semedo, J.N.; Pais, I.P.; Martins, L.D.; Simões-Costa, M.C.; Leitão, A.E.; Fortunato, A.S.; Batista-Santos, P.; Palos, I.M.; et al. Sustained photosynthetic performance of Coffea spp. under long-term enhanced [CO2]. PLoS ONE 2013, 8, e82712. [Google Scholar] [CrossRef][Green Version]
  41. Koike, T.; Watanabe, M.; Watanabe, Y.; Agathokleous, E.; Eguchi, N.; Takagi, K.; Satoh, F.; Kitaoka, S.; Funada, R. Ecophysiology of deciduous trees native to Northeast Asia grown under FACE Free Air CO2 Enrichment. J. Agric. Meteorol. 2015, 71, 174–184. [Google Scholar] [CrossRef]
  42. Lawson, T.; Vialet-Chabrand, S. Speedy stomata, photosynthesis and plant water use efficiency. New Phytol. 2019, 221, 93–98. [Google Scholar] [CrossRef][Green Version]
  43. Sage, R.F.; Sharkey, T.D.; Seemann, J.R. Acclimation of Photosynthesis to Elevated CO2 in Five C3 Species. Plant Physiol. 1989, 89, 590–596. [Google Scholar] [CrossRef][Green Version]
  44. Tausz-Posch, S.; Tausz, M.; Bourgault, M. Elevated [CO2] effects on crops: Advances in understanding acclimation, nitrogen dynamics and interactions with drought and other organisms. Plant Biol. 2020, 22, 38–51. [Google Scholar] [CrossRef]
  45. Moore, B.D.; Cheng, S.H.; Sims, D.; Seemann, J.R. The biochemical and molecular basis for photosynthetic acclimation to elevated atmospheric CO2. Plant Cell Environ. 1999, 22, 567–582. [Google Scholar] [CrossRef]
  46. Macabuhay, A.; Houshmandfar, A.; Nuttall, J.; Fitzgerald, G.J.; Tausz, M.; Tausz-Posch, S. Can elevated CO2 buffer the effects of heat waves on wheat in a dryland cropping system? Environ. Exp. Bot. 2018, 155, 578–588. [Google Scholar] [CrossRef]
  47. Ruiz-Vera, U.M.; De Souza, A.P.; Ament, M.R.; Gleadow, R.M.; Ort, D.R. High sink strength prevents photosynthetic down-regulation in cassava grown at elevated CO2 concentration. J. Exp. Bot. 2021, 72, 542–560. [Google Scholar] [CrossRef]
  48. Ulfat, A.; Shokat, S.; Li, X.; Fang, L.; Großkinsky, D.K.; Majid, S.A.; Roitsch, T.; Liu, F. Elevated carbon dioxide alleviates the negative impact of drought on wheat by modulating plant metabolism and physiology. Agric. Water Manag. 2021, 250, 1–10. [Google Scholar] [CrossRef]
  49. Avila, R.T.; de Almeida, W.L.; Costa, L.C.; Machado, K.L.G.; Barbosa, M.L.; de Souza, R.P.B.; Martino, P.B.; Juárez, M.A.T.; Marçal, D.M.S.; Martins, S.C.V.; et al. Elevated air [CO2] improves photosynthetic performance and alters biomass accumulation and partitioning in drought-stressed coffee plants. Environ. Exp. Bot. 2020, 177, 104137. [Google Scholar] [CrossRef]
  50. Dier, M.; Sickora, J.; Erbs, M.; Weigel, H.J.; Zörb, C.; Manderscheid, R. Decreased wheat grain yield stimulation by free air CO2 enrichment under N deficiency is strongly related to decreased radiation use efficiency enhancement. Eur. J. Agron. 2018, 101, 38–48. [Google Scholar] [CrossRef]
  51. Crous, K.Y.; Wujeska-Klause, A.; Jiang, M.; Medlyn, B.E.; Ellsworth, D.S. Nitrogen and phosphorus retranslocation of leaves and stemwood in a mature Eucalyptus forest exposed to 5 years of elevated CO2. Front. Plant Sci. 2019, 10, 1–13. [Google Scholar] [CrossRef][Green Version]
  52. Shi, S.; Xu, X.; Dong, X.; Xu, C.; Qiu, Y.; He, X. Photosynthetic Acclimation and Growth Responses to Elevated CO2 Associate with Leaf Nitrogen and Phosphorus Concentrations in Mulberry (Morus multicaulis Perr.). Forests 2021, 12, 660. [Google Scholar] [CrossRef]
  53. Feng, Z.; Rütting, T.; Pleijel, H.; Wallin, G.; Reich, P.B.; Kammann, C.I.; Newton, P.C.D.; Kobayashi, K.; Luo, Y.; Uddling, J. Constraints to nitrogen acquisition of terrestrial plants under elevated CO2. Glob. Chang. Biol. 2015, 21, 3152–3168. [Google Scholar] [CrossRef]
  54. Krämer, K.; Kepp, G.; Brock, J.; Stutz, S.; Heyer, A.G. Acclimation to elevated CO2 affects the C/N balance by reducing de novo N-assimilation. Physiol. Plant. 2022, 174, 1–13. [Google Scholar] [CrossRef]
  55. Ainsworth, E.A.; Rogers, A.; Nelson, R.; Long, S.P. Testing the “source-sink” hypothesis of down-regulation of photosynthesis in elevated [CO2] in the field with single gene substitutions in Glycine max. Agric. For. Meteorol. 2004, 122, 85–94. [Google Scholar] [CrossRef]
  56. Eguchi, N.; Karatsu, K.; Ueda, T.; Funada, R.; Takagi, K.; Hiura, T.; Sasa, K.; Koike, T. Photosynthetic responses of birch and alder saplings grown in a free air CO2 enrichment system in northern Japan. Trees Struct. Funct. 2008, 22, 437–447. [Google Scholar] [CrossRef]
  57. Watanabe, Y.; Satomura, T.; Sasa, K.; Funada, R.; Koike, T. Differential anatomical responses to elevated CO2 in saplings of four hardwood species. Plant Cell Environ. 2010, 33, 1101–1111. [Google Scholar] [CrossRef]
  58. Grombone-Guaratini, M.T.; Gaspar, M.; Oliveira, V.F.; Torres, M.A.M.G.; Do Nascimento, A.; Aidar, M.P.M. Atmospheric CO2 enrichment markedly increases photosynthesis and growth in a woody tropical bamboo from the Brazilian atlantic forest. New Zealand J. Bot. 2013, 51, 275–285. [Google Scholar] [CrossRef]
  59. Eichelmann, H.; Oja, V.; Rasulov, B.; Padu, E.; Bichele, I.; Pettai, H.; Möls, T.; Kasparova, I.; Vapaavuori, E.; Laisk, A. Photosynthetic parameters of birch (Betula pendula Roth) leaves growing in normal and in CO2- and O3-enriched atmospheres. Plant Cell Environ. 2004, 27, 479–495. [Google Scholar] [CrossRef]
  60. Riikonen, J.; Holopainen, T.; Oksanen, E.; Vapaavuori, E. Leaf photosynthetic characteristics of silver birch during three years of exposure to elevated concentrations of CO2 and O3 in the field. Tree Physiol. 2005, 25, 621–632. [Google Scholar] [CrossRef][Green Version]
  61. Taylor, G.; Street, N.R.; Tricker, P.J.; Sjödin, A.; Graham, L.; Skogström, O.; Calfapietra, C.; Scarascia-Mugnozza, G.; Jansson, S. The transcriptome of Populus in elevated CO2. New Phytol. 2005, 167, 143–154. [Google Scholar] [CrossRef][Green Version]
  62. Cseke, L.J.; Tsai, C.J.; Rogers, A.; Nelsen, M.P.; White, H.L.; Karnosky, D.F.; Podila, G.K. Transcriptomic comparison in the leaves of two aspen genotypes having similar carbon assimilation rates but different partitioning patterns under elevated [CO2]. New Phytol. 2009, 182, 891–911. [Google Scholar] [CrossRef]
  63. Amthor, J.S. The McCree-de Wit-Penning de Vries-Thornley respiration paradigms: 30 years later. Ann. Bot. 2000, 86, 1–20. [Google Scholar] [CrossRef][Green Version]
  64. Way, D.A.; Oren, R.; Kroner, Y. The space-time continuum: The effects of elevated CO2 and temperature on trees and the importance of scaling. Plant Cell Environ. 2015, 38, 991–1007. [Google Scholar] [CrossRef]
  65. Crous, K.Y.; Zaragoza-Castells, J.; Löw, M.; Ellsworth, D.S.; Tissue, D.T.; Tjoelker, M.G.; Barton, C.V.M.; Gimeno, T.E.; Atkin, O.K. Seasonal acclimation of leaf respiration in Eucalyptus saligna trees: Impacts of elevated atmospheric CO2 and summer drought. Glob. Chang. Biol. 2011, 17, 1560–1576. [Google Scholar] [CrossRef]
  66. Tissue, D.T.; Lewis, J.D.; Wullschleger, S.D.; Amthor, J.S.; Griffin, K.L.; Anderson, O.R. Leaf respiration at different canopy positions in sweetgum (Liquidambar styraciflua) grown in ambient and elevated concentrations of carbon dioxide in the field. Tree Physiol. 2002, 22, 1157–1166. [Google Scholar] [CrossRef][Green Version]
  67. Wu, F.; Sun, X.; Zou, B.; Zhu, P.; Lin, N.; Lin, J.; Ji, K. Transcriptional analysis of masson pine (Pinus massoniana) under high CO2 stress. Genes 2019, 10, 804. [Google Scholar] [CrossRef][Green Version]
  68. Sanches, R.F.E.; da Cruz Centeno, D.; Braga, M.R.; da Silva, E.A. Impact of high atmospheric CO2 concentrations on the seasonality of water-related processes, gas exchange, and carbohydrate metabolism in coffee trees under field conditions. Clim. Chang. 2020, 162, 1231–1248. [Google Scholar] [CrossRef]
  69. Markelz, R.J.C.; Vosseller, L.N.; Leakey, A.D.B. Developmental stage specificity of transcriptional, biochemical and CO2 efflux responses of leaf dark respiration to growth of Arabidopsis thaliana at elevated [CO2]. Plant Cell Environ. 2014, 37, 2542–2552. [Google Scholar] [CrossRef]
  70. Jiang, M.; Medlyn, B.E.; Drake, J.E.; Duursma, R.A.; Anderson, I.C.; Barton, C.V.M.; Boer, M.M.; Carrillo, Y.; Castañeda-Gómez, L.; Collins, L.; et al. The fate of carbon in a mature forest under carbon dioxide enrichment. Nature 2020, 580, 227–231. [Google Scholar] [CrossRef]
  71. Li, X.; Zhang, G.; Sun, B.; Zhang, S.; Zhang, Y.; Liao, Y.; Zhou, Y.; Xia, X.; Shi, K.; Yu, J. Stimulated leaf dark respiration in tomato in an elevated carbon dioxide atmosphere. Sci. Rep. 2013, 3, 2–9. [Google Scholar] [CrossRef][Green Version]
  72. Gupta, P.; Duplessis, S.; White, H.; Karnosky, D.F.; Martin, F.; Podila, G.K. Gene expression patterns of trembling aspen trees following long-term exposure to interacting elevated CO2 and tropospheric O3. New Phytol. 2005, 167, 129–142. [Google Scholar] [CrossRef]
  73. Taylor, G.; Tallis, M.J.; Giardina, C.P.; Percy, K.E.; Miglietta, F.; Gupta, P.S.; Gioli, B.; Calfapietra, C.; Gielen, B.; Kubiske, M.E.; et al. Future atmospheric CO2 leads to delayed autumnal senescence. Glob. Chang. Biol. 2008, 14, 264–275. [Google Scholar] [CrossRef]
  74. Druart, N.; Rodríguez-Buey, M.; Barron-Gafford, G.; Sjödin, A.; Bhalerao, R.; Hurry, V. Molecular targets of elevated [CO2] in leaves and stems of Populus deltoides: Implications for future tree growth and carbon sequestration. Funct. Plant Biol. 2006, 33, 121. [Google Scholar] [CrossRef][Green Version]
  75. Tallis, M.J.; Lin, Y.; Rogers, A.; Zhang, J.; Street, N.R.; Miglietta, F.; Karnosky, D.F.; De Angelis, P.; Calfapietra, C.; Taylor, G. The transcriptome of Populus in elevated CO2 reveals increased anthocyanin biosynthesis during delayed autumnal senescence. New Phytol. 2010, 186, 415–428. [Google Scholar] [CrossRef][Green Version]
  76. Liu, J.; Zhang, J.; He, C.; Duan, A. Genes responsive to elevated CO2 concentrations in triploid white poplar and integrated gene network analysis. PLoS ONE 2014, 9, e98300. [Google Scholar] [CrossRef]
  77. Atwell, B.J.; Henery, M.L.; Whitehead, D. Sapwood development in Pinus radiata trees grown for three years at ambient and elevated carbon dioxide partial pressures. Tree Physiol. 2003, 23, 13–21. [Google Scholar] [CrossRef][Green Version]
  78. Kilpeläinen, A.; Peltola, H.; Ryyppö, A.; Sauvala, K.; Laitinen, K.; Kellomäki, S. Wood properties of Scots pines (Pinus sylvestris) grown at elevated temperature and carbon dioxide concentration. Tree Physiol. 2003, 23, 889–897. [Google Scholar] [CrossRef][Green Version]
  79. Kaplan, F.; Zhao, W.; Richards, J.T.; Wheeler, R.M.; Guy, C.L.; Levine, L.H. Transcriptional and metabolic insights into the differential physiological responses of arabidopsis to optimal and supraoptimal atmospheric CO2. PLoS ONE 2012, 7, e43583. [Google Scholar] [CrossRef]
  80. Kontunen-Soppela, S.; Parviainen, J.; Ruhanen, H.; Brosché, M.; Keinänen, M.; Thakur, R.C.; Kolehmainen, M.; Kangasjärvi, J.; Oksanen, E.; Karnosky, D.F.; et al. Gene expression responses of paper birch (Betula papyrifera) to elevated CO2 and O3 during leaf maturation and senescence. Environ. Pollut. 2010, 158, 959–968. [Google Scholar] [CrossRef]
  81. Taylor, G.; Tricker, P.J.; Zhang, F.Z.; Alston, V.J.; Miglietta, F.; Kuzminsky, E. Spatial and temporal effects of free-air CO2 enrichment (POPFACE) on leaf growth, cell expansion, and cell production in a closed canopy of poplar. Plant Physiol. 2003, 131, 177–185. [Google Scholar] [CrossRef][Green Version]
  82. Taylor, G.; Ranasinghe, S.; Bosac, C.; Gardner, S.D.L.; Ferris, R. Elevated CO2 and plant growth: Cellular mechanisms and responses of whole plants. J. Exp. Bot. 1994, 45, 1761–1774. [Google Scholar] [CrossRef]
  83. Cheng, S.H.; Willmann, M.R.; Chen, H.C.; Sheen, J. Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol. 2002, 129, 469–485. [Google Scholar] [CrossRef][Green Version]
  84. Dhankher, O.P.; Foyer, C.H. Climate resilient crops for improving global food security and safety. Plant Cell Environ. 2018, 41, 877–884. [Google Scholar] [CrossRef]
  85. Carmo-Silva, A.E.; Gore, M.A.; Andrade-Sanchez, P.; French, A.N.; Hunsaker, D.J.; Salvucci, M.E. Decreased CO2 availability and inactivation of Rubisco limit photosynthesis in cotton plants under heat and drought stress in the field. Environ. Exp. Bot. 2012, 83, 1–11. [Google Scholar] [CrossRef]
  86. Meehl, G.A.; Tebaldi, C.; Tilmes, S.; Lamarque, J.-F.; Bates, S.; Pendergrass, A.; Lombardozzi, D. Future heat waves and surface ozone. Environ. Res. Lett. 2018, 13, 064004. [Google Scholar] [CrossRef]
  87. IPCC. Summary for policymakers. In Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change; Stocker, T.F., Qin, D., Plattner, G.-K., Tignor, M., Allen, S.K., Boschung, J., Nauels, A., Xia, Y., Bex, V., Midgley, P.M., Eds.; IPCC: Geneva, Switzerland, 2013. [Google Scholar]
  88. Grace, J. Climatic Tolerance and the Distribution of Plants. New Phytol. 1987, 106, 113–130. [Google Scholar] [CrossRef]
  89. Wise, R.R.; Olson, A.J.; Schrader, S.M.; Sharkey, T.D. Electron transport is the functional limitation of photosynthesis in field-grown Pima cotton plants at high temperature. Plant Cell Environ. 2004, 27, 717–724. [Google Scholar] [CrossRef]
  90. Wahid, A.; Gelani, S.; Ashraf, M.; Foolad, M.R. Heat tolerance in plants: An overview. Environ. Exp. Bot. 2007, 61, 199–223. [Google Scholar] [CrossRef]
  91. DaMatta, F.M.; Grandis, A.; Arenque, B.C.; Buckeridge, M.S. Impacts of climate changes on crop physiology and food quality. Food Res. Int. 2010, 43, 1814–1823. [Google Scholar] [CrossRef]
  92. Vu, J.C.V.; Allen, L.H. Stem juice production of the C4 sugarcane (Saccharum officinarum) is enhanced by growth at double-ambient CO2 and high temperature. J. Plant Physiol. 2009, 166, 1141–1151. [Google Scholar] [CrossRef] [PubMed]
  93. Ghannoum, O.; Phillips, N.G.; Conroy, J.P.; Smith, R.A.; Attard, R.D.; Woodfield, R.; Logan, B.A.; Lewis, J.D.; Tissue, D.T. Exposure to preindustrial, current and future atmospheric CO2 and temperature differentially affects growth and photosynthesis in Eucalyptus. Glob. Chang. Biol. 2010, 16, 303–319. [Google Scholar] [CrossRef]
  94. Madan, P.; Jagadish, S.V.K.; Craufurd, P.Q.; Fitzgerald, M.; Lafarge, T.; Wheeler, T.R. Effect of elevated CO2 and high temperature on seed-set and grain quality of rice. J. Exp. Bot. 2012, 63, 3843–3852. [Google Scholar] [CrossRef][Green Version]
  95. Yu, J.; Du, H.; Xu, M.; Huang, B. Metabolic responses to heat stress under elevated atmospheric CO2 concentration in a cool-season grass species. J. Am. Soc. Hortic. Sci. 2012, 137, 221–228. [Google Scholar] [CrossRef][Green Version]
  96. Rodrigues, W.P.; Martins, M.Q.; Fortunato, A.S.; Rodrigues, A.P.; Semedo, J.N.; Simões-Costa, M.C.; Pais, I.P.; Leitão, A.E.; Colwell, F.; Goulao, L.; et al. Long-term elevated air [CO2] strengthens photosynthetic functioning and mitigates the impact of supra-optimal temperatures in tropical Coffea arabica and C. canephora species. Glob. Chang. Biol. 2016, 22, 415–431. [Google Scholar] [CrossRef]
  97. Ghannoum, O.; Phillips, N.G.; Sears, M.A.; Logan, B.A.; Lewis, J.D.; Conroy, J.P.; Tissue, D.T. Photosynthetic responses of two eucalypts to industrial-age changes in atmospheric [CO2] and temperature. Plant Cell Environ. 2010, 33, 1671–1681. [Google Scholar] [CrossRef]
  98. Martins, M.Q.; Rodrigues, W.P.; Fortunato, A.S.; Leitão, A.E.; Rodrigues, A.P.; Pais, I.P.; Martins, L.D.; Silva, M.J.; Reboredo, F.H.; Partelli, F.L.; et al. Protective response mechanisms to heat stress in interaction with high [CO2] conditions in Coffea spp. Front. Plant Sci. 2016, 7, 947. [Google Scholar] [CrossRef][Green Version]
  99. Marques, I.; Fernandes, I.; Paulo, O.S.; Lidon, F.C.; Damatta, F.M.; Ramalho, J.C.; Ribeiro-barros, A.I. A transcriptomic approach to understanding the combined impacts of supra-optimal temperatures and CO2 revealed different responses in the polyploid coffea arabica and its diploid progenitor c. Canephora. Int. J. Mol. Sci. 2021, 22, 3125. [Google Scholar] [CrossRef] [PubMed]
  100. Ramalho, J.C.; Pais, I.P.; Leitão, A.E.; Guerra, M.; Reboredo, F.H.; Máguas, C.M.; Carvalho, M.L.; Scotti-Campos, P.; Ribeiro-Barros, A.I.; Lidon, F.J.C.; et al. Can elevated air [CO2] conditions mitigate the predicted warming impact on the quality of coffee bean? Front. Plant Sci. 2018, 9, 1–14. [Google Scholar] [CrossRef] [PubMed][Green Version]
  101. Grossiord, C.; Buckley, T.N.; Cernusak, L.A.; Novick, K.A.; Poulter, B.; Siegwolf, R.T.W.; Sperry, J.S.; McDowell, N.G. Plant responses to rising vapor pressure deficit. New Phytol. 2020, 226, 1550–1566. [Google Scholar] [CrossRef][Green Version]
  102. Lindner, M.; Fitzgerald, J.B.; Zimmermann, N.E.; Reyer, C.; Delzon, S.; van der Maaten, E.; Schelhaas, M.J.; Lasch, P.; Eggers, J.; van der Maaten-Theunissen, M.; et al. Climate change and European forests: What do we know, what are the uncertainties, and what are the implications for forest management? J. Environ. Manag. 2014, 146, 69–83. [Google Scholar] [CrossRef][Green Version]
  103. Rigling, A.; Bigler, C.; Eilmann, B.; Feldmeyer-Christe, E.; Gimmi, U.; Ginzler, C.; Graf, U.; Mayer, P.; Vacchiano, G.; Weber, P.; et al. Driving factors of a vegetation shift from Scots pine to pubescent oak in dry Alpine forests. Glob. Chang. Biol. 2013, 19, 229–240. [Google Scholar] [CrossRef]
  104. Cochrane, J.A.; Hoyle, G.L.; Yates, C.J.; Wood, J.; Nicotra, A.B. Climate warming delays and decreases seedling emergence in a Mediterranean ecosystem. Oikos 2015, 124, 150–160. [Google Scholar] [CrossRef]
  105. Creek, D.; Blackman, C.J.; Brodribb, T.J.; Choat, B.; Tissue, D.T. Coordination between leaf, stem, and root hydraulics and gas exchange in three arid-zone angiosperms during severe drought and recovery. Plant Cell Environ. 2018, 41, 2869–2881. [Google Scholar] [CrossRef]
  106. McDowell, N.; Pockman, W.T.; Allen, C.D.; Breshears, D.D.; Cobb, N.; Kolb, T.; Plaut, J.; Sperry, J.; West, A.; Williams, D.G.; et al. Mechanisms of plant survival and mortality during drought: Why do some plants survive while others succumb to drought? New Phytol. 2008, 178, 719–739. [Google Scholar] [CrossRef]
  107. Bobich, E.G.; Barron-Gafford, G.A.; Rascher, K.G.; Murthy, R. Effects of drought and changes in vapour pressure deficit on water relations of Populus deltoides growing in ambient and elevated CO2. Tree Physiol. 2010, 30, 866–875. [Google Scholar] [CrossRef][Green Version]
  108. Warren, J.M.; Norby, R.J.; Wullschleger, S.D.; Oren, R. Elevated CO2 enhances leaf senescence during extreme drought in a temperate forest. Tree Physiol. 2011, 31, 117–130. [Google Scholar] [CrossRef]
  109. Bachofen, C.; Moser, B.; Hoch, G.; Ghazoul, J.; Wohlgemuth, T. No carbon “bet hedging” in pine seedlings under prolonged summer drought and elevated CO2. J. Ecol. 2018, 106, 31–46. [Google Scholar] [CrossRef][Green Version]
  110. Birami, B.; Nägele, T.; Gattmann, M.; Preisler, Y.; Gast, A.; Arneth, A.; Ruehr, N.K. Hot drought reduces the effects of elevated CO2 on tree water-use efficiency and carbon metabolism. New Phytol. 2020, 226, 1607–1621. [Google Scholar] [CrossRef] [PubMed][Green Version]
  111. Sanches, R.F.E.; Catarino, I.C.A.; Braga, M.R.; Silva, E.A. da Influência da alta concentração atmosférica de CO2(↑[CO2]atm) × disponibilidade hídrica nas relações hídricas, trocas gasosas e acúmulo de carboidratos em Coffea arabica L. Hoehnea 2017, 44, 635–643. [Google Scholar] [CrossRef][Green Version]
  112. Avila, R.T.; Cardoso, A.A.; de Almeida, W.L.; Costa, L.C.; Machado, K.L.G.; Barbosa, M.L.; de Souza, R.P.B.; Oliveira, L.A.; Batista, D.S.; Martins, S.C.V.; et al. Coffee plants respond to drought and elevated [CO2] through changes in stomatal function, plant hydraulic conductance, and aquaporin expression. Environ. Exp. Bot. 2020, 177, 104148. [Google Scholar] [CrossRef]
  113. Catarino, I.C.A.; Monteiro, G.B.; Ferreira, M.J.P.; Torres, L.M.B.; Domingues, D.S.; Centeno, D.C.; Lobo, A.K.M.; Silva, E.A. Elevated [CO2] Mitigates Drought Effects and Increases Leaf 5-O-Caffeoylquinic Acid and Caffeine Concentrations During the Early Growth of Coffea Arabica Plants. Front. Sustain. Food Syst. 2021, 5, 1–12. [Google Scholar] [CrossRef]
  114. Semedo, J.N.; Rodrigues, A.P.; Lidon, F.C.; Pais, I.P.; Marques, I.; Gouveia, D.; Armengaud, J.; Silva, M.J.; Martins, S.; Semedo, M.C.; et al. Intrinsic non-stomatal resilience to drought of the photosynthetic apparatus in Coffea spp. is strengthened by elevated air [CO2]. Tree Physiol. 2021, 41, 708–727. [Google Scholar] [CrossRef]
  115. Rodrigues, A.M.; Jorge, T.; Osorio, S.; Pott, D.M.; Lidon, F.C.; Damatta, F.M.; Marques, I.; Ribeiro-Barros, A.I.; Ramalho, J.C.; António, C. Primary metabolite profile changes in Coffea spp. Promoted by single and combined exposure to drought and elevated CO2 concentration. Metabolites 2021, 11, 427. [Google Scholar] [CrossRef]
  116. Munns, R.; Gilliham, M. Salinity tolerance of crops—What is the cost? Tansley insight Salinity tolerance of crops—What is the cost ? New Phytol. 2015, 208, 668–673. [Google Scholar] [CrossRef][Green Version]
  117. Koyro, H.W.; Geissler, N.; Hussin, S.; Debez, A.; Huchzermeyer, B.S. Survival at extreme locations: Life strategies of halophytes—The long way from system ecology, whole plant physiology, cell biochemistry and molecular aspects back to sustainable utilization at field sites. In Biosaline Agriculture and High Salinity Tolerance; Springer London: London, UK, 2008; pp. 1–20. [Google Scholar]
  118. Athar, H.R.; Ashraf, M. The Church in the World: A Half Century of Ecumenism in Hungary. Theol. Today 1994, 51, 289–290. [Google Scholar] [CrossRef]
  119. Young, I.; Renault, S.; Markham, J. Low levels organic amendments improve fertility and plant cover on non-acid generating gold mine tailings. Ecol. Eng. 2015, 74, 250–257. [Google Scholar] [CrossRef]
  120. Rengasamy, P. World salinization with emphasis on Australia. J. Exp. Bot. 2006, 57, 1017–1023. [Google Scholar] [CrossRef] [PubMed][Green Version]
  121. FAO. Land and Plant Nutrition Management Service. Available online: (accessed on 1 July 2022).
  122. Shao, J.; Markham, J.; Renault, S. Nitrogen fixation symbiosis and salt tolerance of the boreal woody species Elaeagnus commutata. Acta Physiol. Plant. 2020, 42, 1–9. [Google Scholar] [CrossRef]
  123. Vicente, O.; Boscaiu, M.; Naranjo, M.Á.; Estrelles, E.; Bellés, J.M.; Soriano, P. Responses to salt stress in the halophyte Plantago crassifolia (Plantaginaceae). J. Arid Environ. 2004, 58, 463–481. [Google Scholar] [CrossRef]
  124. Bhaskar, G.; Bingru, H. Mechanism of Salinity Tolerance in Plants: Physiological, Biochemical, and Molecular Characterization. Int. J. Genom. 2014, 2014, 19. [Google Scholar]
  125. Melgar, J.C.; Syvertsen, J.P.; García-Sánchez, F. Can elevated CO2 improve salt tolerance in olive trees? J. Plant Physiol. 2008, 165, 631–640. [Google Scholar] [CrossRef]
  126. Souza, N.C.S.; Silveira, J.A.G.; Silva, E.N.; Lima Neto, M.C.; Lima, C.S.; Aragão, R.M.; Ferreira-Silva, S.L. High CO2 favors ionic homeostasis, photoprotection, and lower photorespiration in salt-stressed cashew plants. Acta Physiol. Plant. 2019, 41, 1–14. [Google Scholar] [CrossRef]
  127. Pérez-López, U.; Robredo, A.; Lacuesta, M.; Mena-Petite, A.; Muñoz-Rueda, A. The impact of salt stress on the water status of barley plants is partially mitigated by elevated CO2. Environ. Exp. Bot. 2009, 66, 463–470. [Google Scholar] [CrossRef]
  128. Pérez-López, U.; Miranda-Apodaca, J.; Muñoz-Rueda, A.; Mena-Petite, A. Lettuce production and antioxidant capacity are differentially modified by salt stress and light intensity under ambient and elevated CO2. J. Plant Physiol. 2013, 170, 1517–1525. [Google Scholar] [CrossRef]
  129. Geissler, N.; Hussin, S.; El-Far, M.M.M.; Koyro, H.W. Elevated atmospheric CO2 concentration leads to different salt resistance mechanisms in a C3 (Chenopodium quinoa) and a C4 (Atriplex nummularia) halophyte. Environ. Exp. Bot. 2015, 118, 67–77. [Google Scholar] [CrossRef]
  130. Myhre, G.; Shindell, D.; Bréon, F.-M.; Collins, W.; Fugle-Stvedt, J.; Huang, J.; Koch, D.; Lamarque, J.-F.; Lee, D.; Mendoza, B.; et al. Anthropogenic and natural radiative forcing. In Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change; IPCC: Geneva, Switzerland, 2013. [Google Scholar]
  131. Oliver, R.J.; Mercado, L.M.; Sitch, S.; Simpson, D.; Medlyn, B.E.; Lin, Y.S.; Folberth, G.A. Large but decreasing effect of ozone on the European carbon sink. Biogeosciences 2018, 15, 4245–4269. [Google Scholar] [CrossRef][Green Version]
  132. Yue, X.; Unger, N.; Harper, K.; Xia, X.; Liao, H.; Zhu, T.; Xiao, J.; Feng, Z.; Li, J. Ozone and haze pollution weakens net primary productivity in China. Atmos. Chem. Phys. 2017, 17, 6073–6089. [Google Scholar] [CrossRef][Green Version]
  133. McGrath, J.M.; Betzelberger, A.M.; Wang, S.; Shook, E.; Zhu, X.G.; Long, S.P.; Ainsworth, E.A. An analysis of ozone damage to historical maize and soybean yields in the United States. Proc. Natl. Acad. Sci. USA 2015, 112, 14390–14395. [Google Scholar] [CrossRef] [PubMed][Green Version]
  134. Riikonen, J.; Lindsberg, M.M.; Holopainen, T.; Oksanen, E.; Lappi, J.; Peltonen, P.; Vapaavuori, E. Silver birch and climate change: Variable growth and carbon allocation responses to elevated concentrations of carbon dioxide and ozone. Tree Physiol. 2004, 24, 1227–1237. [Google Scholar] [CrossRef][Green Version]
  135. Kontunen-Soppela, S.; Riikonen, J.; Ruhanen, H.; Brosché, M.; Somervuo, P.; Peltonen, P.; Kangasjärvi, J.; Auvinen, P.; Paulin, L.; Keinänen, M.; et al. Differential gene expression in senescing leaves of two silver birch genotypes in response to elevated CO2 and tropospheric ozone. Plant Cell Environ. 2010, 33, 1016–1028. [Google Scholar] [CrossRef]
  136. Riikonen, J.; Syrjälä, L.; Tulva, I.; Mänd, P.; Oksanen, E.; Poteri, M.; Vapaavuori, E. Stomatal characteristics and infection biology of Pyrenopeziza betulicola in Betula pendula trees grown under elevated CO2 and O3. Environ. Pollut. 2008, 156, 536–543. [Google Scholar] [CrossRef]
  137. Tobita, H.; Uemura, A.; Kitao, M.; Kitaoka, S.; Utsugi, H. Interactive effects of elevated CO2, phosphorus deficiency, and soil drought on nodulation and nitrogenase activity in alnus hirsuta and alnus maximowiczii. Symbiosis 2010, 50, 59–69. [Google Scholar] [CrossRef]
  138. Duan, H.; Ontedhu, J.; Milham, P.; Lewis, J.D.; Tissue, D.T. Effects of elevated carbon dioxide and elevated temperature on morphological, physiological and anatomical responses of Eucalyptus tereticornis along a soil phosphorus gradient. Tree Physiol. 2019, 39, 1821–1837. [Google Scholar] [CrossRef]
  139. Bauweraerts, I.; Wertin, T.M.; Ameye, M.; Mcguire, M.A.; Teskey, R.O.; Steppe, K. The effect of heat waves, elevated [CO2] and low soil water availability on northern red oak (Quercus rubra L.) seedlings. Glob. Chang. Biol. 2013, 19, 517–528. [Google Scholar] [CrossRef]
  140. Kumar, A.; Anju, T.; Kumar, S.; Chhapekar, S.S.; Sreedharan, S.; Singh, S.; Choi, S.R.; Ramchiary, N.; Lim, Y.P. Integrating omics and gene editing tools for rapid improvement of traditional food plants for diversified and sustainable food security. Int. J. Mol. Sci. 2021, 22, 8093. [Google Scholar] [CrossRef]
Figure 1. Venn diagram of the main effects caused by elevated CO2 in combination with abiotic stresses (heat, drought, salinity and ozone) in woody plants. Green effects are increased or stimulated, and red effects are decreased or inhibited.
Figure 1. Venn diagram of the main effects caused by elevated CO2 in combination with abiotic stresses (heat, drought, salinity and ozone) in woody plants. Green effects are increased or stimulated, and red effects are decreased or inhibited.
Plants 11 01880 g001
Figure 2. The main effects triggered by elevated CO2 according to abiotic stress severity. Elevated CO2 buffers the negative effects of mild/moderate abiotic stresses by inducing a range of molecular and metabolic changes. The positive response is eliminated under severe stress where the stomata is closed and photosynthesis and other processes are impaired. CHO: carbohydrate; AA: amino acids.
Figure 2. The main effects triggered by elevated CO2 according to abiotic stress severity. Elevated CO2 buffers the negative effects of mild/moderate abiotic stresses by inducing a range of molecular and metabolic changes. The positive response is eliminated under severe stress where the stomata is closed and photosynthesis and other processes are impaired. CHO: carbohydrate; AA: amino acids.
Plants 11 01880 g002
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Lobo, A.K.M.; Catarino, I.C.A.; Silva, E.A.; Centeno, D.C.; Domingues, D.S. Physiological and Molecular Responses of Woody Plants Exposed to Future Atmospheric CO2 Levels under Abiotic Stresses. Plants 2022, 11, 1880.

AMA Style

Lobo AKM, Catarino ICA, Silva EA, Centeno DC, Domingues DS. Physiological and Molecular Responses of Woody Plants Exposed to Future Atmospheric CO2 Levels under Abiotic Stresses. Plants. 2022; 11(14):1880.

Chicago/Turabian Style

Lobo, Ana Karla M., Ingrid C. A. Catarino, Emerson A. Silva, Danilo C. Centeno, and Douglas S. Domingues. 2022. "Physiological and Molecular Responses of Woody Plants Exposed to Future Atmospheric CO2 Levels under Abiotic Stresses" Plants 11, no. 14: 1880.

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop