1. Introduction
Plant growth and grain yield account for 90% of the carbon accumulated as biomass via photosynthetic carbon dioxide (CO
2) reduction. Studies on the impacts of elevated CO
2 on crops are therefore crucial for understanding global food security and its link to malnutrition. Global climate change from anthropogenic activities is the major cause of the increasingly frequent occurrence of high temperatures, drought, flooding, wildfires, and cyclones, which threaten food security and increase outbreaks of emerging diseases. Although elevated CO
2 in the atmosphere has singularly contributed hugely to climate change, the growth and photosynthetic activity of land plants—especially C3 species like rice and wheat—are reported to increase under elevated CO
2 levels in both natural and agricultural ecosystems
[1],
[2],
[3]. This unexpected benefit of rising atmospheric CO
2 makes C3 plant species a major carbon (C) sink for CO
2 in the atmosphere. In practical terms, tree planting in both natural and agricultural ecosystems could be a green, nature-based solution to sequester the rising CO
2 concentration in the atmosphere and thereby reduce global warming.
The drought and low and irregular rainfall caused by climate change affect food security annually in Africa. In the Horn of Africa, where drought can persist consecutively for 3–4 years, loss of livestock is common and crop plant cultivation non-existent, often leading to famine and protein-calorie malnutrition. However, little data currently exist on the economic loss of crop and animal species to allow for the development of drought-tolerant crop plants and/or climate-resilient plant and animal species, especially under the continuously rising CO2 concentration in the atmosphere.
The net CO
2 emissions from 1850 to 2019 were (2400 ± 240) GtCO
2, with 58% of this occurring between 1850 and 1989 and 42% between 1990 and 2019
[4]. Similarly, the net global greenhouse gas emissions—largely from fossil fuel combustion and industrial processes—reached (59.0 ± 6.6) GtCO
2-equivalent (eq) in 2019, which was 12% (6.5 GtCO
2-eq) higher than the emissions in 2010 and 54% (21 GtCO
2-eq) higher than those in 1990, bringing global atmospheric CO
2 concentration to 410 ppm—the highest level in 2 million years
[4]. Clearly, the planet is overwhelmed by the rising CO
2 concentration in the atmosphere, which has huge consequences for global food security.
In comparison with the period from 1850 to 1900, the world’s land surface temperature was 0.99 °C higher during 2001–2020 and 1.09 °C higher during 2011–2020; in fact, the global atmospheric temperature has risen faster since 1970 than during the last 2000 years
[4]. The resulting frequent high temperatures and wildfires across various regions of the globe are likely to have a detrimental effect on biodiversity and ecosystem functioning. Unless current CO
2 emissions are curbed at the global scale, these events will have a negative impact on food security. At the practical level, considerable information has been gathered on the effects of elevated CO
2 on cereal and legume species, which include increased growth and yield
[5],
[6], as well as on attempts to narrow the uncertainties regarding the impacts of elevated CO
2 on food crops
[7]. However, there are several gaps in the literature and inconclusive studies on the biology of crop species exposed to elevated CO
2, especially with regard to mineral nutrition, plant function and ionomics, and the dietary quality of food crops produced under elevated CO
2. Although a reduction in tissue nitrogen (N) has been well documented in C3 plants under elevated CO
2 (
Table 1 [8],
[9],
[10],
[11],
[12],
[13],
[14],
[15],
[16],
[17],
[18],
[19],
[20],
[21],
[22],
[23],
[24],
[25]), the mechanisms remain unclear at both the gene-expression and metabolic levels. Moreover, the enzymes involved in the glutamate synthetase–glutamine synthase (GS-GOGAT) pathway and the different aminotransferases that catalyze amino acid biosynthesis require elucidation in C3 plants exposed to elevated CO
2. Similarly, the observed decreases in mineral nutrients in C3 species under elevated CO
2 require a reassessment to include gene expression involving ion transporters and mineral-transporting proteins. This review explores the impacts of elevated CO
2 on food security in relation to nutrient assimilation and plant growth, with an emphasis on the diazotrophic activity of soil microbes, mineral nutrient uptake, and the dietary quality of crops grown under elevated CO
2.
2. Effects of elevated CO2 on the growth of C3 plant species
Several studies have found an increase in the dry matter yield of C3 plants grown under elevated CO
2 versus ambient CO
2 [8],
[9],
[10],
[11],
[12],
[13],
[14],
[15],
[16],
[17],
[18],
[19],
[20],
[21],
[22]. In many of these field studies, shoot dry matter and grain yield were both significantly increased by high CO
2. For example, the shoot biomass of spring wheat increased by 11% and grain yield increased by 10.4% when plants were cultivated in elevated CO
2 under field conditions
[20]; rice yields also rose with exposure to elevated CO
2 [5],
[26],
[27],
[28]. In fact, yields of C3 crops were reported to increase by 18% on average under elevated CO
2 [5]. However, yields of wheat and rice were found to decrease by 10%–12% and 17%–35%, respectively, under the combined effects of elevated CO
2 and high temperature
[29].
In general, plant growth is stimulated more in shoots than in roots, although elevated CO
2 can increase both shoot growth and grain yield in crop species in comparison with ambient CO
2 [30]. From the seedling stage to physiological maturity, the growth of crop plants is determined and controlled by various processes involving morphogenic metabolites that alter cell division and cell expansion in plant parts. Thus far, however, little research has been done on the metabolomics of C3 species growing under elevated CO
2 conditions, although many biological changes have been documented for plants developing under high CO
2; these include increased leaf size, larger leaf anatomy, a greater number of leaves per plant, and an increase in root length, root diameter, and root branching
[31]. Leaf cell expansion plays a major role in these changes, as the greater leaf size resulting from the increased leaf area expansion per plant has been reported as a factor in plant growth in 66% of elevated CO
2 studies.
Plant growth is also stimulated by microbial activity in rhizosphere soils, especially by the metabolites released from plant-microbes interactions. For example, lumichrome, a signal molecule produced by rhizobia during nodule formation in legumes, can cause dramatic changes in stem elongation and trifoliate leaf development at a concentration of 5 nmol∙L
−1, compared with 0 and 50 nmol∙L
−1 levels, in both monocots and dicots
[32]. Elsewhere, we reported that providing 5 nmol∙L
−1 lumichrome to soybean increased its unifoliate leaf area by 20%, trifoliate leaf area by 75%, and stem elongation by 13%, resulting in 30% more biomass
[32]. Similar increases in root length, root diameter, and root branching are typically elicited by microbial molecules involved in plant development. Rhizobial bacteria, associative diazotrophs, and bacterial endophytes can synthesize and release plant hormones—including indole acetic acid (IAA), abscisic acid (ABA), lumichrome, riboflavin, cytokinins, and gibberellins—that promote plant growth via enhanced root branching and elongation and/or increased root hair density for greater water and nutrient absorption. However, few (if any) studies have assessed the role of these metabolites on plant growth under elevated CO
2, especially their effect on internode elongation, which has been reported to increase with elevated CO
2. For example, soybean plant height was reported to increase by 15%, and spring wheat height by 17% from an increase in internode length with plant growth in elevated CO
2 [31].
3. Elevated CO2 and microbial diazotrophic activity in soils
Earlier studies on grasses found significant nitrogenase activity associated with these species
[33],
[34],
[35],
[36], indicating that they can meet a part of their N requirements from biological nitrogen gas (N
2) fixation. Associative N
2 fixation by bacterial diazotrophs located on or inside the roots and stems of grasses, cereals, and other non-legume species has been reported to contribute significantly to the N economy of natural ecosystems. In fact, cereals and vegetables can obtain a substantial proportion of their N nutrition from associative and endophytic N
2-fixing bacteria—about 12%–33% in maize from
Pseudomonas,
Herbaspirillum,
Azospirillum, and
Brevundioronas [37], and 12.9%–20.9% in cucumber from
Paenibacillus beijingensis BJ-18
[38]. Using acetylene reduction assays and
15N
2 (gas) feeding, Dakora and Drake
[39] showed that exposing C3 and C4 grasses to elevated CO
2 increased nitrogenase activity by 35% (
Fig. 1) and
15N incorporation by 73% in the C3 plant
Scirpus olneyi (
S. olneyi), and the same by 13% and 23%, respectively, in the C4 plant
Spartina patens (
S. patens)
. While the rate of N
2 fixation in C3
S. olneyi was (611 ± 75) ng
15N fixed∙plant
–1∙h
–1 under elevated CO
2 and (367 ± 46) ng
15N fixed∙plant
–1∙h
–1 under ambient CO
2, the values for C4
S. patens were (12.5 ± 1.1) and (9.8 ± 1.3) ng
15N fixed∙plant
–1∙h
–1, respectively
[39], indicating that C4 plants are not photosynthetically stimulated by elevated CO
2 and would benefit less than C3 species from N
2 fixation in a high-CO
2 world.
A strong correlation was observed between the enhanced
15N
2 fixation and the increased photosynthetic rates by elevated CO
2 in both
S. olneyi (a C3 plant) and
S. patens (a C4 species), in that the N
2 fixation and photosynthesis were concurrently high in
S. olneyi but lower in
S. patens plants
[39]. However, in the case of
S. olneyi, the extra carbon supplied by photosynthesis from stimulation by the elevated CO
2 enhanced N
2 fixation, as found in nodulated legumes
[14],
[40],
[41],
[42]. Whether in the legume/rhizobia or cereal/microbe interaction, N
2 fixation remains the most energetically expensive biological process and is a major sink for
de novo photosynthate
[43], as the assimilation of about 10% of recently fixed carbon is required for nitrogenase activity to occur in symbiotic legumes
[44]. Thus, N
2-fixing plants that accumulate carbon under increasing CO
2 concentration would be expected to increase their photosynthetic rates as the atmospheric CO
2 concentration rises
[3], thereby providing an increased photosynthate supply to nitrogenase for higher N
2-fixing activity.
Elevated CO
2 also affects the activity of free-living microbes in the soil (
Fig. 2). For example, heterotrophic non-symbiotic N
2 fixation was found to be markedly increased by elevated CO
2 in a plant-free rooting medium compared with ambient CO
2 [39], possibly using sediment C as a source of energy. Taken together, these findings suggest that the rising atmospheric CO
2 concentration is slowly altering the terrestrial N cycle in natural ecosystems. However, the extent to which the N cycle has already been altered by elevated atmospheric CO
2 remains unknown. Further field studies are required, using many grass species and locations, to establish their contribution to the N economy of natural ecosystems under elevated CO
2—information that is currently lacking but vital for modeling the global effects of elevated CO
2 on the N cycle. However, a study on the response of the cropland N cycle to elevated CO
2 predicted an increase in N-use efficiency of 19% and in biological N
2 fixation of 55%
[45]—a finding with importance for global food security. This finding also implies that elevated CO
2 will have a positive impact on soil microbial communities through substrates released by plant root exudates.
4. Elevated CO2 and N2 fixation in legumes
Over the years, the Haber–Bosch process has been used to provide chemical N fertilizers for agriculture, which led to the first Green Revolution. However, this process is dependent on fossil fuels and is energy intensive, with a huge C footprint that contributed significantly to the net CO
2 emissions of (2400 ± 240) GtCO
2 reached in 2019 from fossil fuel combustion and industrial processes
[4]. While recognizing that the use of chemical fertilizers has more than doubled crop yields globally since the first Green Revolution, the contribution of CO
2 emissions to climate change and the causative effect of chemical N fertilizers on environmental degradation and global warming cannot be ignored. Biological N
2 fixation in legumes is a sustainable and environmentally friendly option for reducing the use of chemical fertilizers in agriculture and thus decreasing global warming.
A historic report by Wilson et al.
[40] in 1933 showed that CO
2 enrichment increases N
2 fixation in nodulated legumes and stimulates photosynthetic efficiency via providing N for ribulose-1,5-biphosphate carboxylase/oxygenase (rubisco), the enzyme reducing CO
2 in leaves, and for the biosynthesis of chlorophyll, the molecule capturing light energy for photosynthesis
[46]. This source-sink relationship between photosynthesis and N
2 fixation in legumes is well documented
[47],
[48], and N
2 fixation is a major sink for
de novo photosynthate
[49], with about 10% of recently fixed C being invested in the nitrogenase activity of nodulated legumes
[44]. N
2-fixing legumes are therefore expected to increase their photosynthetic rates with rising atmospheric CO
2 concentration
[42], thereby providing an increased C supply to nitrogenase for N
2-fixing activity. The extra carbon supplied by the stimulation of photosynthesis by elevated CO
2 has, in turn, been reported to enhance N
2 fixation in symbiotic legumes
[14],
[40],
[41],
[42] (
Fig. 3 [50]). With the changing climate due to the rising atmospheric CO
2 concentration, incorporating legumes that elicit greater N and C accumulation in cropping systems would promote carbon sequestration and reduce greenhouse gas emissions.
A recent study has suggested that, with climate change, legumes may have an additional advantage due to their ability to mitigate photosynthetic acclimation—a process in which plants adjust their photosynthetic activity in response to environmental changes, sometimes resulting in reduced efficiency
[51]. As global temperatures rise and fall, their pattern becomes less predictable, but the demand for crops that can maintain high photosynthetic rates under stress will continue to increase. Based on the functional relationship between N
2 fixation and photosynthesis
[52], legumes have a high chance of sustaining their photosynthetic activity under adverse conditions, thus offering a potential buffer against the negative impacts of climate change on crop yields
[53]. Leveraging the inherent beneficial traits of legumes could prove important for developing more resilient agricultural systems that can withstand climate change and produce sufficient food to support the growing global population while preserving existing natural resources.
5. Effects of elevated CO2 on NO3 uptake and assimilation
Several studies have assessed the effects of elevated CO
2 on NO
3 uptake and assimilation in different C3 plant species (
Table 1)
[10],
[11],
[16],
[17],
[18],
[19],
[21],
[22],
[54],
[55],
[56],
[57],
[58],
[59], all of which consistently found a decrease in tissue N concentration. In fact, an analysis of data from 75 publications revealed a global average reduction of 14% in the N concentration in tissues from C3 plants exposed to elevated CO
2 [60] (
Fig. 4). McGuire et al.
[23] also recorded an average N reduction of 21% in the leaves of woody forest vegetation, with 65 reports showing decreased leaf N and 26 showing decreased whole-plant N (i.e., in leaves, stems, and roots). Moreover, even when provided with N fertilization, 26 of these woody species still revealed decreased N in leaves and 12 showed a decrease in whole-plant N. Whether with or without added N, woody N
2-fixing species such as
Alnus rubra,
Gliricidia sepium, and
Robinia pseudoacacia also exhibited N reductions under elevated CO
2 [23], indicating a lower symbiotic N supply to support the increased photosynthetic rates stimulated by elevated CO
2. The N reductions in plant leaves must be linked to rubisco, the enzyme that reduces CO
2 during photosynthesis. Rubisco is highly abundant in plant leaves and constitutes 25% of leaf N; however, because lesser amounts of rubisco are required for photosynthetic functioning under elevated CO
2 conditions, the protein is reduced by 15% on average under such circumstances, which can lead to a 24% reduction in rubisco activity
[3].
Of the three functional types studied under elevated CO
2 (i.e., C3, C4, and N
2 fixers), only the C3 species recorded a marked N response
[52]. As a major C sink for high atmospheric CO
2 concentration, N
2-fixing plants in particular are expected to increase their photosynthetic rates and accumulate biomass
[3]. However, the observed decrease in tissue N under high CO
2 could limit the C sink size, since N is needed for photo-assimilate production but is decreased by elevated CO
2. Nevertheless, C3 plant species have been reported to adapt well to low-N conditions under elevated CO
2 by increasing their photosynthetic N-use efficiency, which was found to increase by 33% in
S. olneyi exposed to elevated CO
2 [24],
[39].
Native plants such as
Aspalathus species growing in the nutrient-poor soils of the Cape fynbos in South Africa are known to conserve N by increasing their photosynthetic N-use efficiency through metabolic switching from N-containing storage compounds to N-free storage molecules (e.g., aspalathin and other flavonoids) without decreasing their growth rate
[61]. However, this is unlikely to be the case for
S. olneyi in the study by Dakora et al.
[24], as the rooting medium supporting the growth of
S. olneyi under elevated CO
2 contained 2.27% N. The increase in photosynthetic N-use efficiency enables C3 species to raise their dry matter yield per unit N under elevated CO
2 when compared with ambient CO
2 conditions
[3],
[12],
[62]. Thus, the observed decrease in the tissue N concentration of
S. olneyi and other C3 species under elevated CO
2 represents a strategic shift in their N use; in the case of
S. olneyi, the N required for growth and reproduction is reduced, while the photosynthetic N-use efficiency is increased by 33% and the fixed-N contribution by 73% from associative symbiosis under elevated CO
2 [39].
Besides the increase in photosynthetic N-use efficiency of C3 plants exposed to elevated CO
2 [24],
[39], little is known about the mechanisms underlying N decreases in the photosynthetic organs of plants grown under elevated CO
2. Although N dilution through accumulated photosynthate and decreased N demand by shoots have been cited as factors causing decreased N concentration in C3 plants grown under elevated CO
2 [63], the N reductions in several studied C3 crop species were attributed to the elevated-CO
2-induced inhibition of nitrate assimilation
[50], suppression of tissue nitrate and nitrite reductase activities
[16],
[55], inhibition of leaf protein formation (e.g., in wheat and tobacco
[16],
[17]), and decline in NO
3–, NH
4+, and amino acids—especially glutamine, such as in tobacco
[16]. Other studies have also suggested that the expression of genes for N metabolic enzymes is suppressed in C3 plants by exposure to elevated CO
2, such as the nitrate reductase (NR) gene in
Medicago truncatula [59], NiR in tomato roots
[64], and glutamine synthetase (GS) in
Brassica chinensis [21].
At the uptake level, some studies have suggested a link between mineral nutrient absorption from soil solution and leaf transpiration
[63],
[65],
[66],
[67], with one report showing decreased N translocation to soybean leaves as a result of low transpiration rates
[68]. More specifically, reduced uptake of NO
3– and NH
4+ under elevated CO
2 has been attributed to low transpiration rates caused by decreased stomatal conductance, affecting the mass flow of solutes from soil to roots
[10],
[22],
[63]. Whatever the case, there is a definite effect of elevated CO
2 on N metabolism in C3 species. For example, the synthesis, concentration, and activity of rubisco were all found to decrease in plants with a low N supply
[69],
[70]. However, although reduced N concentration in tissues due to elevated CO
2 still occurred with adequate N provision, the increased photosynthetic rates, greater plant growth, and larger biomass associated with C3 plants grown under elevated CO
2 were not affected
[3],
[20]. Furthermore, wheat plants grown under elevated CO
2 while receiving a high dose of 200 kg of N per hectare still showed a decrease of more than 10% in leaf N concentration
[30], indicating that the N reduction in tissues was not due to N starvation caused by an inadequate exogenous N supply.
6. Effect of elevated CO2 on NH4+ uptake and metabolism
Several studies have found decreased N concentrations in the tissues of NO
3–-fed C3 species grown under elevated CO
2 and have attributed it to the elevated-CO
2-induced inhibition of NO
3– assimilation
[11],
[15],
[17],
[19],
[21],
[22]. Similar decreases in tissue N concentrations were also observed when NO
3– and NH
4+ (as ammonium nitrate) were fed to plants exposed to elevated CO
2 [11],
[16],
[17]. Despite these results from ammonium nitrate feeding, it has been reported that plants fed NH
4+ respond more positively to elevated CO
2 than their NO
3– counterparts due to the inhibition of NO
3– assimilation
[22]. Another study indicated that the negative effect of elevated CO
2 on NO
3– uptake is more evident and much greater than that on NH
4– uptake and assimilation
[50]. However, what remains unclear about the elevated-CO
2-induced inhibition of NO
3– assimilation is the point of blockage in the N metabolic pathway. Nitrate feeders must reduce NO
3– to NH
4+ (which involves two enzymatic steps) before it is incorporated into organic N via the GS-GOGAT pathway. Thus, it remains unknown whether the inhibition occurs at the point of nitrate reduction to nitrite, nitrite reduction to NH
4+, or NH
4+ assimilation into amino acids. However, it has been reported that elevated CO
2 can cause a decrease in NR activity in tobacco plants
[16], thereby affecting the NO
3– to NO
2– reduction step. C3 species can differ in their preference for NO
3– or NH
4+ as an N source. Nevertheless, even with NO
3– nutrition, the solute must still be reduced to NH
4+ before assimilation into organic N (i.e., NO
3−→NO
2−→NH
4+→GS-GOGAT). Therefore, tracer experiments are needed to track the destination and accumulation of
15N in different plant parts over time.
The results of a recent study using
15N-labeled ammonium sulfate as an N source showed that the inhibition of
15N assimilation by
S. olneyi plants (a C3 species) grown under elevated CO
2 occurred at the point of incorporation of NH
4+ into organic N
[24]—the first step in the conversion of mineral N into amino acids via the GS-GOGAT pathway. The report by Dakora et al.
[24] showed that
S. olneyi plants receiving 5 mmol∙L
−1 (
15NH
4)
2SO
4 solution and being exposed to elevated CO
2 for 19 h had lower
15N in stems, roots plus rhizomes, and whole plants in comparison with plants grown in ambient CO
2. In fact, the
15N concentration was 51% lower in stems, 63% in roots plus rhizomes, and 74% in whole plants of
S. olneyi grown under elevated CO
2, resulting in an overall 78% decrease in
15N uptake by
S. olneyi plants grown under elevated CO
2 compared with their ambient-CO
2-grown counterparts
[24]. Because the rooting medium supporting the growth of
S. olneyi contained 2.27% N, the plants were not N-starved, so the decrease in N uptake could not have been due to N limitation. This finding is supported by a report that wheat grown under elevated CO
2 while receiving a high dose of 200 kg of N per hectare still showed a decrease of more than 10% in leaf N concentration
[30]. In general, these findings suggest that exposing C3 plants to elevated CO
2 can decrease their leaf stomatal conductance and transpiration rates, resulting in reduced N uptake.
The reduction in tissue
15N concentration reported by Dakora et al.
[24] resulted in markedly decreased levels of amino acids in the organs of
S. olneyi plants exposed to elevated CO
2. For example, the concentrations of serine, glycine, alanine, gamma-aminobutyric acid (GABA), and lysine were reduced in
S. olneyi stems by 25.6% for glycine up to 65.0% for serine, while the concentrations of aspartate, serine, glutamate, glycine, alanine, cysteine, isoleucine, and GABA decreased in
S. olneyi roots under elevated CO
2 by 2% for GABA up to 80% for glutamate, resulting in a total amino acid pool decrease of 50% in stems and 23% in roots plus rhizomes in elevated CO
2 compared with ambient CO
2 [24].
More studies are needed to identify the steps in the GS/GOGAT pathway that are sensitive to elevated CO
2 and lead to decreased concentrations of individual amino acids and/or their pools
[16],
[24],
[57]. For example, a decrease of up to 80% was observed in glutamate concentration in C3 plants under elevated CO
2 [16],
[24]. Although the absence of glutamine in the study by Dakora et al.
[24] is the likely reason for the very low levels of glutamate found in the organs of
S. olneyi under elevated CO
2, it is also possible that 2-oxoglutarate (the precursor for glutamate biosynthesis via the GS-GOGAT pathway) was limited. Furthermore, the markedly reduced activity of GS (a key enzyme in the GS-GOGAT pathway) in the shoots and roots of
Brassica chinensis grown under elevated CO
2 [18] suggests that the decreased amino acid concentrations and pools in the tissues of plants exposed to elevated CO
2 could be due to repression or limited expression of GS, affecting the formation of glutamine from NH
4+ and glutamate. Clearly, the metabolic pathways and enzymes involved in the GS-GOGAT pathway, as well as the different aminotransferases, require elucidation in the organs of C3 plants exposed to elevated CO
2.
7. Ionomics: Changes in mineral nutrient concentrations under elevated CO2
Soil is the source of nutrients and water for the growth and reproduction of plant species. In areas with low soil nutrient concentrations, nutrient uptake by the roots of crop plants is also low, leading to the production of grain with poor nutritional quality. In Africa, where agricultural soils are inherently low in mineral nutrients, cultivated crops are also naturally low in these nutrients, which are needed for human nutrition and health. As a result, about 239 million people are suffering from protein-calorie malnutrition
[71],
[72] and another 232 million from trace element deficiency in Africa
[71],
[73] due to low N and micronutrient concentrations in soils. Thus, the observed 14% global average decrease in the N concentration of C3 plants under elevated atmospheric CO
2 levels
[60] implies a future much lower nutritional quality for the food crops produced in Africa under further increases in atmospheric CO
2, due to the inherently low-nutrient soils in that continent. Although Li et al.
[74] found significant decreases in iron (Fe), manganese (Mn), and zinc (Zn) in the soil solution of rice paddy fields exposed to long-term elevated CO
2, and Wang et al.
[75] reported 21.0% and 26.9% decreases in the plant-available phosphorus (P) of soil exposed to elevated CO
2 for 9 and 15 years, respectively, these changes in soil nutrient dynamics are more likely driven by plant uptake than by soil processes.
Whatever the case, the net CO
2 emissions between 1850 and 2019 were (2400 ± 240) GtCO
2, of which 42% occurred between 1990 and 2019
[4]—a very short period of only 29 years. Therefore, the impact of elevated CO
2 on food and nutritional security should be a top priority in climate change studies, especially given the observation that the decreased tissue N observed in crops grown under elevated CO
2 resulted in significant reductions in amino acid concentrations in plant organs (e.g., reductions in serine, glycine, alanine, GABA, and lysine in the C3 crop
S. olneyi when grown under elevated CO
2).
Furthermore, the decrease in the levels of certain sulfur (S)-containing essential amino acids—such as cysteine, methionine, leucine, iso-leucine, and threonine—in C3 species exposed to high CO
2 is likely to have implications for human nutrition and health, especially that as these essential amino acids cannot be synthesized
de novo by the human body
[76],
[77] but can only be obtained from consumed foods. The essential amino acids threonine, valine, iso-leucine, leucine, and phenylalanine were also significantly decreased in wheat grain grown under high CO
2 [57]. A 7.4% reduction in wheat grain protein under elevated CO
2 resulted in markedly reduced amino acids on a per unit flour weight basis, at 7.1% for serine, 10.7% for glycine, 7.4% for cysteine, 8.9% for tyrosine, 5.1% for histidine, 5.6% for arginine, 5.3% for tryptophan, and 8.7% for isoleucine
[20]. With the world’s rising atmospheric CO
2, an understanding of its effect on the functioning of crop species in relation to N nutrition and N metabolism is clearly critical for addressing food safety, nutritional security, and protein-calorie malnutrition.
Insights into the negative effects of elevated CO
2 on plant ionomics are important for ensuring not only the nutritional quality of crops but also the stability of soil organic matter, as well as for mitigating climate change through increased photosynthesis. Grain accumulation of the macronutrients sodium (Na), calcium (Ca), magnesium (Mg), P, and S, as well as the micronutrients Fe, Zn, and Mn, was found to decrease significantly in wheat grown under elevated CO
2 [57]. Reduced levels of Fe and Zn have also been recorded in the grain of legumes and C3 cereals exposed to elevated CO
2 [50],
[78], with implications for grain quality and hence for human nutrition and health. However, as found with N, the mechanisms of mineral reduction in C3 plants exposed to elevated CO
2 remain elusive. Because transpiration can be reduced by 30% under elevated CO
2 [50], the decreased uptake and assimilation of mineral nutrients such as N, P, Ca, Mg, Na, S, Fe, Zn, and Mn by C3 plants under elevated CO
2 have been linked to reduced leaf transpiration rates caused by decreased stomatal conductance
[63],
[66],
[67],
[79].
A comparison of the mineral uptake by rice (C3), maize (C4), soybean, and pea (both C3 legumes) grown under elevated CO
2 compared to crops grown under ambient conditions showed that P was respectively reduced by 1.0%, 7.1%, 0.7%, and 3.7%; S by 7.8%, 2.1%, 2.9%, and 2.2%; Fe by 5.2%, 5.8%, 4.1%, and 4.1%; Zn by 3.3%, 5.2%, 5.1%, and 6.8%; copper (Cu) by 10.6%, 9.9%, 5.7%, and 2.7%; and Mn by 7.5%, 4.2%, 1.4%, and 2.5%
[78]. The results shown here for maize—a major global food crop—contradict other reports suggesting that nutrient concentrations are reduced only in C3, not C4, species when grown under elevated CO
2 [50],
[80]. Elevated CO
2 has also been shown to reduce N, S, Mg, Fe, Cu, and Zn in rice, another major global food crop
[28],
[81]. The decreased nutrient levels documented for both C3 and C4 species suggest that nutritional security is likely to diminish on a global scale in the absence of resilient, climate-smart crops. In fact, overall tissue mineral concentrations are predicted to decrease by 8% and total non-structural carbohydrates (mainly starch and sugars) are predicted to increase in C3 plants under elevated CO
2 [80]. This report has implications for human nutrition and health in a high-CO
2 world, with a predicted increase in protein-calorie malnutrition, micronutrient deficiency, and diabetes, especially where dietary N and trace elements are respectively deficient in foods, while carbohydrates and sugars are relatively high. In fact, in their assessment of the integrated nutritional effect of the observed decreases in protein levels, micronutrients (e.g., Fe and Zn), and vitamins (e.g., B1, B2, B5, and B9) in rice, Zhu et al.
[82] found a strong correlation between the elevated CO
2 effect on vitamins and the molecular fraction of N in those vitamins, indicating that N reductions under elevated CO
2 led to decreased vitamin concentrations in rice grain. Furthermore, the potential health risks associated with these decreases in rice protein, minerals, and vitamins was found to correlate with the lowest gross domestic product (GDP) per capita for high-rice-consuming countries of about 600 million people
[82].
Various techniques have been employed in attempts to understand the mechanisms underlying nutrient reductions under elevated CO
2, including physiological, molecular, and structural approaches. For example, an analysis of xylem sap collected from wheat revealed a decrease in the concentrations of K
+, Ca
2+, and Mg
2+ in plants grown under elevated CO
2 in comparison with those grown under the ambient control
[83],
[84]—a finding consistent with the reported repression of xylem development
[85] and the marked reduction in root metaxylem
[86] of tomato roots grown under high CO
2. Because elevated CO
2 has the positive effect of promoting plant root growth and development
[30], the reduced uptake and assimilation of mineral nutrients is more likely to be influenced by root-controlled physiological processes such as the downregulation of ion transporters in the membranes of plant roots developed under elevated CO
2 [50].
8. Exploiting the benefits of high CO2 concentration in the atmosphere to reduce global warming and restore planetary health
Climate change has undoubtedly had many catastrophic effects on life on earth, including the loss of human and animal lives, beneficial microbes, and biodiversity through high temperatures, drought, flooding, cyclones, hurricanes, wildfires, and emerging diseases. It has thus already caused unquantified damage and economic losses involving crops, housing, infrastructure, road networks, and more. However, although the high CO
2 concentration in the atmosphere is a major contributor to climate change, it has benefits that can be tapped for planetary health. For example, plants often respond to elevated CO
2 in the atmosphere by increasing their resource-use efficiency, which includes reducing their stomatal conductance and transpiration, thereby increasing their water-use efficiency and stimulating higher rates of photosynthesis
[3]. If properly managed, the responses by C3 species exposed to elevated CO
2 can be exploited and used to minimize further increases in atmospheric CO
2 concentration, thus restoring planetary health.
To adapt to climate change, crop genotypes should be selected that are naturally superior in biofortification and should be recommended for use in breeding programs to produce new varieties with naturally biofortified grain in order to alleviate nutrient deficiency—a condition likely to double in a changing climate. For example, Jan et al.
[87] found that 60 common bean germplasms from the Himalayas differed markedly in nutrient accumulation, with one being 2.4-fold higher in Mg and another 17.8-fold greater in Ca than those that were naturally low in biofortification. Including such super-accumulating germplasms in breeding programs can reduce the vulnerability of key food crops to climate change (e.g., by lowering reductions in N, amino acids, and mineral nutrients of grain; see
Table 1).
Trees hold about 75% of the carbon found in agricultural land. Therefore, compulsory tree planting in rural areas could reduce CO
2 concentration in the atmosphere, especially if economic N
2-fixing C3 trees, shrubs, and grasses are planted for food, timber, and medicine, as well as for use as pasture or fodder for livestock. Mixed cultures, rather than monocultures, of these different species should be recommended, since tissue N reduction under elevated CO
2 is lower in mixed cultures
[14]. Africa, Asia, and South America collectively represent the centers of diversity for over 90% of the plant species in the world, making them a botanical asset awaiting exploitation for societal development. Dakora
[88] has documented some 24 legumes and 41 non-legume species used for traditional medicine in Africa. Such species are recommended for establishing plantations to reduce high CO
2 concentration in the atmosphere while providing medicines for local use. Furthermore, fast-growing, N
2-fixing shrub and tree species (e.g.,
Leucaena leucocephala L. and
Leucaena grandifolia L.) should be established as plantations to sequester the high CO
2 in the atmosphere and thus produce timber for household use, forage for livestock, and firewood for domestic energy use.
The elevated CO
2 stimulation of N
2 fixation in plants can also be tapped by growing more C3 food crops—especially legumes, which synthesize protein and accumulate substantial amounts of dietarily important mineral nutrients at high levels of N
2 fixation
[89],
[90]. Thus, a major shift from a heavily meat-based diet among humans to pulse-based foods would help to reduce methane production by livestock, which is one of the major causes of climate change. According to Kimball et al.
[30], applying high levels of N fertilizers to C3 crops could reduce decreases in the N and protein concentrations of C3 species grown under elevated CO
2. This finding implies that the increased cultivation of high N
2-fixing grain legumes for food and feed could minimize the reduction of grain N and protein concentrations observed under elevated CO
2—an argument that supports the increased production of grain legumes and the establishment of large-scale plantations of N
2-fixing economic C3 species.
The Great Green Wall of Africa is an African Union-led project that aims to create an 8000 km × 14.5 km (4400 miles × 9 miles) natural belt of vegetation across the entire width of Africa, from northern Senegal to Djibouti in the Horn of Africa along the Sahara Desert. This is being done with the view that high atmospheric CO
2 concentrations can promote plant growth, leading to increased vegetation that would take up more CO
2, thereby slowing down the rate of increase of CO
2 in the atmosphere
[91],
[92] while reducing global warming, which together would initiate a repair of planetary health
[25]. In fact, it has been shown experimentally that CO
2 enrichment induces a 12% increase in carbon uptake
[91], scientifically validating the aims for establishing the Great Green Wall of Africa.
So far, 15% of the Wall has been revegetated within just a decade and is providing food security for the millions living along its path. The Wall is a major nature-based solution for climate change mitigation and adaptation and is enhancing soil carbon sequestration through the uptake of CO
2 in the atmosphere. The Great Green Wall of Africa is a major project with huge potential to sequester large quantities of carbon and help restore planetary health, and it should be adequately funded both locally and internationally. In this way, more tree and shrub legumes, as well as C3 grasses, can be planted to “mop up” the high CO
2 levels in the atmosphere, despite reports that the global CO
2 fertilization effect has declined due to altered nutrient concentrations and limited soil water
[75]. That argument is consistent with the findings of earlier studies, which showed that, with high rainfall, high N availability, or both, elevated CO
2 increased plant biomass by 33% through the stimulation of photosynthesis. However, that gain was lost under low rainfall and low N regimes
[25].
9. Future research
9.1. Physiological responses to elevated CO2 in C3 species
N2-fixing legumes are viewed as model plants for future studies aimed at understanding N reductions and nutrient decreases in C3 species grown under elevated CO2, for two reasons: Firstly, when in symbiosis with soil rhizobia, legume species, varieties, or cultivars can differ in their levels of N2 fixation, with some fixing increased amounts of N (high fixers) and others fixing small amounts (low fixers). High N2-fixing legumes usually require a substantial amount of energy in the form of adenosine triphosphate (ATP), which is supplied by photosynthesis for N2 reduction to NH3 by nitrogenase, and vice versa. However, high CO2 also stimulates greater photosynthetic rates, thus producing increased de novo photosynthate for feeding N2 fixation, which in turn produces more symbiotic N for the synthesis of higher levels of Rubisco for CO2 reduction during photosynthesis. Therefore, reports of N2-fixing legumes exhibiting decreased N concentrations under elevated CO2 require reassessment. Future experiments using high N2-fixing and low N2-fixing legume varieties are needed to shed light on N reductions in nodulated legumes under elevated CO2.
Secondly, under field conditions, high N
2-fixing legume varieties accumulate more mineral nutrients than low fixers
[50],
[77],
[83]. High N
2-fixing rhizobia were also found to induce a greater accumulation of nutrient elements than low-fixing strains under controlled conditions in a glasshouse
[93]. Therefore, high N
2-fixing symbioses and legumes nodulated by high-fixing rhizobia are not expected to exhibit reductions in mineral nutrients under elevated CO
2. New studies are needed to reassess nutrient uptake and accumulation by high N
2-fixing and low N
2-fixing legume varieties in the field, which should be followed by the appropriate recording of decreases (if any) in nutrient elements under elevated CO
2. Similarly, legumes nodulated by rhizobia that have been identified as low and high N
2 fixers should be assessed for nutrient uptake and accumulation under elevated CO
2.
9.2. Molecular responses to elevated CO2 in C3 plants
The metabolic pathways and enzymes involved in the GS-GOGAT pathway, as well as the different aminotransferases that catalyze amino acid biosynthesis, require elucidation in the organs of C3 plants exposed to elevated CO2 in order to better understand the decreases in amino acids associated with high CO2. More work also needs to be done on ion transporters in the membranes of plant roots developed under elevated CO2, as genes for mineral-transporting proteins such as sulfate transporters, phosphate transporters, and zinc and iron transporters could be downregulated under elevated CO2, thus inhibiting root nutrient uptake.
9.3. Analysis of metabolites in C3 plants under elevated CO2
Levels of metabolites such as IAA, ABA, lumichrome, riboflavin, cytokinins, and gibberellins, which stimulate plant growth, cause stem elongation, enhance root branching, and increase root hair density for greater water and nutrient absorption, should be assessed in plants grown under elevated CO2 to obtain a better understanding of plant growth promotion by high CO2.
9.4. Ecological response to elevated CO2 in C3 plants
The Great Green Wall of Africa provides a living laboratory available to the world for studies of atmospheric physics and chemistry, plant and soil ecology, C sequestration, meteorology, and climatology, as well as being a botanical and zoological asset for field experimentation. However, it needs adequate funding to function as a global research platform.
9.5. Genomics and AI response to elevated CO2 in C3 species
The rapid application of artificial intelligence (AI) in plant breeding and plant science
[94] presents a valuable opportunity to accelerate the achievement of the goals outlined in this study. AI—particularly machine learning and deep learning algorithms—can process large-scale multi-omics data (including genomics, transcriptomics, metabolomics, and ionomics), providing insights into the key genes and metabolic pathways involved in nitrogen metabolism, nutrient assimilation, and amino acid biosynthesis under elevated CO
2 conditions. This will help identify genotypes that are more responsive to CO
2 concentration changes and predict their performance under different environmental scenarios.
In future breeding programs, AI-driven genomic selection models should integrate phenotypic, genotypic, and environmental data to facilitate the development of plant varieties with enhanced N2-fixation and nutrient-uptake efficiency. Moreover, AI can simulate and predict plant growth responses to future high-CO2 environments, guiding breeding strategies aimed at improving both nutritional security and climate resilience. By leveraging AI, researchers can overcome the complexities of plant–environment interactions, expediting the development of crops better suited to a high-CO2 world while maintaining or even enhancing their nutritional quality.
Finally, to cope with the environmental factors caused by climate change, such as drought, flooding, typhoons, wildfires, and temperature extremes, climate-adapted crop varieties with enhanced tolerance to multiple stresses should be developed using molecular techniques such as marker-assisted selection, transgenics, gene editing, and genomic selection. In this way, crop responses to field stresses and the underlying gene expression networks can be thoroughly and accurately phenotyped and genotyped using AI and high-throughput omics tools. The resulting traits, genes, elite alleles, and regulatory cis-elements identified through these analyses would be essential components for breeding new crop varieties to ensure food safety, nutritional security, and protein-calorie balance in a high-CO2 world.
10. Conclusions
Paradoxically, elevated CO
2 can stimulate an increase in N supply to C3 plants via greater N
2 fixation from higher photosynthetic rates, while conversely causing a decrease in mineral N uptake and assimilation in C3 plants. The GS-GOGAT pathway is the first step in incorporating NH
4+ into organic N, irrespective of whether the N originates from soil or symbiosis. As the GS-GOGAT pathway is the only route for incorporating NH
4+ into organic N, the source of NH
4+ should not matter with regard to its rate of assimilation into organic N. However, it has been shown through the use of
15N
2 (gas) feeding that the N
2 fixation by free-living, heterotrophic, non-symbiotic diazotrophs, as well as by associative microsymbionts, in the roots of
S. olneyi plants increased with exposure to elevated CO
2 [39], while the NH
4+ assimilation from
15N-labeled ammonium sulfate decreased
[39]. This finding is intriguing, as the GS-GOGAT enzyme complex is presumably the same in all plant species, and therefore should catalyze NH
4+ assimilation at the same rate, regardless of the source of the NH
4+ substrate. A possible explanation for the conflicting results with NH
4+ assimilation under elevated CO
2 could be that there are differences in the transporters, receptors, and binding sites for the NH
4+ from mineral N sources versus the NH
4+ from symbiotic N
2 fixation that could be affected differently by elevated CO
2. Future studies are needed to resolve this paradox.
In conclusion, rice, maize, and wheat are the three most important cereal crops in the world, providing food security to billions of people across the globe. However, global food security could be at risk from the negative effects of high atmospheric CO
2 concentration on crop plant functioning, grain yield, and quality. Under high CO
2 levels, the grain protein of wheat has been reported to decrease by 7.4% due to significant reductions in tissue N and essential amino acids such as threonine, valine,
iso-leucine, leucine, and phenylalanine. In fact, most amino acids were found to be markedly reduced in the flour of grain grown under elevated CO
2 on a per unit flour weight basis, by 7.1% for serine, 10.7% for glycine, 7.4% for cysteine, 8.9% for tyrosine, 5.1% for histidine, 5.6% for arginine, 5.3% for tryptophan, and 8.7% for isoleucine
[20]. Under elevated CO
2, mineral uptakes by rice and maize were also respectively reduced by 1.0 and 7.1% for P, 7.8 and 2.1% for S, 5.2 and 5.8% for Fe, 3.3 and 5.2% for Zn, 10.6 and 9.9% for Cu, and 7.5 and 4.2% for Mn
[78]. In fact, for C3 plants under elevated CO
2, tissue mineral concentrations are predicted to decrease by an average of 8%, while total non-structural carbohydrates (mainly starch and sugars) are predicted to increase
[80]. Although elevated CO
2 promotes plant growth and yield in general, the changes in grain protein and essential mineral nutrients could increase protein-calorie malnutrition, micronutrient deficiency, and diabetes from increased dependence on starchy diets, especially in Africa where the soils are inherently low in N and other mineral nutrients.
Acknowledgments
Felix D. Dakora is grateful to the National Research Foundation (NRF), Tshwane University of Technology (TUT), and the South African Research Chair in Agrochemurgy and Plant Symbioses for their continued support of his research. This work was supported by the Nanfan special project, CAAS (YBXM2408), and the Innovation Program of Chinese Academy of Agricultural Sciences (CAAS-CSIAF-202303) to Huihui Li. We are grateful for a grant from Sanya Municipal Program for Science and Technology Innovation (2022KJCX87), and the Nanfan special project, CAAS (YBXM2319), to Jun Zhao.
Compliance with ethics guidelines
Felix D. Dakora, Huihui Li, and Jun Zhao declare that they have no conflict of interest or financial conflicts to disclose.
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