Rising Atmospheric Carbon Dioxide and Plant Responses: Current and Future Consequences

CHAPTER 11

Rising Atmospheric Carbon Dioxide and Plant Responses: Current and Future Consequences Amit Kumar Mishra1, Shashi Bhushan Agrawal2 and Madhoolika Agrawal2 1

Texas A&M AgriLife Research and Extension Center, Texas A&M University, Uvalde, TX, United States Laboratory of Air Pollution and Global Climate Change, Department of Botany, Institute of Science, Banaras Hindu University, Varanasi, India

2

Contents 11.1 Introduction 11.2 Current Status and Trends of Atmospheric CO2 Levels 11.3 Plant Responses to Atmospheric CO2 11.3.1 CO2 Fertilization Effect 11.3.2 Growth Responses 11.3.3 Physiological Responses 11.3.4 Biochemical Responses 11.3.5 Molecular Changes in Plants Under CO2 Enrichment 11.3.6 Yield 11.4 Interaction With Air Pollutants 11.5 Summary Acknowledgments References Web references

265 267 268 268 269 271 281 283 284 286 294 295 295 306

11.1 INTRODUCTION The world’s population is predicted to increase by 2.3 billion people between 2009 and 2050, thus creating the need for a substantial rise in global food production with the aim of meeting the imminent food demand (Alexandratos and Bruinsma, 2012). The present and expected future changes in the climate will inhibit the attainment of food production goals Climate Change and Agricultural Ecosystems DOI: https://doi.org/10.1016/B978-0-12-816483-9.00011-6

Copyright © 2019 Elsevier Inc. All rights reserved.

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even further. Environmental variations are associated with increasing abiotic and biotic stresses, such as drought and heat stress, insect attack, new disease outbreaks, and rising greenhouse gas emissions. Amongst these, the levels of atmospheric CO2 are increasing continuously over time; the present atmospheric CO2 concentration has increased from 280 to more than 400 µmol mol21 (https://www.esrl.noaa.gov/gmd/ccgg/trends/global. html; Tans and Keeling, 2018) since the 1800s and is predicted to double by the end of the 21st century (IPCC Climate Change, 2013). Long-term exposure of plants to high CO2 levels, elevated temperature, and drought will considerably affect the equilibrium of ecosystem processes equally at local and global levels. Global food security will be contingent on key physiological processes of agricultural crop species and will be affected by the combined effects of the factors of climate change together with increasing levels of atmospheric CO2 (Tausz et al., 2013). Carbon dioxide is the key substrate for photosynthesis, and therefore, can be anticipated as the main contributor toward global food production. Approximately 90% of the existing plant species of the world possess C3 type processes to fix carbon during photosynthesis though saturation is not observed at current ambient CO2 levels, and thus, photosynthesis and growth are predicted to increase under high CO2 environments (Makino and Mae, 1999; Kimball, 2016). In contrast, plants having C4 type pathways develop a special mechanism of carbon fixation that principally prevents photorespiration (a respiratory process in which plants utilize oxygen in the presence of light and release some CO2 thereby significantly wasting energy generated by photosynthesis). In C3 plants, Ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO) catalyze the process of photosynthesis by reacting with both CO2 and oxygen (O2), instigating a photosynthetic carbon reduction (PCR) and photorespiratory carbon oxidation (PCO) cycles, respectively (Drake et al., 1997; Makino and Mae, 1999). Photosynthesis, respiration, and water relations are the three main physiological processes of plants swayed by high CO2 levels (Gamage et al., 2018). Thus, understanding the mechanisms of photosynthesis, respiration, and water use, and their impact on plant growth under high CO2 levels offers an exclusive opportunity to improve crop productivity under future climate change. The increase in global atmospheric CO2 levels will have a major influence on agricultural crop production. Plants could acclimatize to these changes by utilizing excess CO2 during the process of photosynthesis to produce photoassimilates leading to increased growth and productivity. Still, mechanisms to assimilate higher CO2 concentrations and their consequences are not yet completely

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clear. In this chapter, the effects of increasing CO2 levels on overall plant growth and development are highlighted and potential knowledge gaps in the understanding of plant responses to CO2 enrichment are outlined.

11.2 CURRENT STATUS AND TRENDS OF ATMOSPHERIC CO2 LEVELS The burning of fossil fuels, the continued growth of the population, and other anthropogenic activities have resulted in an increase in carbon dioxide (CO2) input into the atmosphere, from less than 300 ppm before the industrial revolution to the current concentration of above 400 ppm (https://www.esrl.noaa.gov/gmd/ccgg/trends/global.html) (Fig. 11.1), which is a major contributor to global greenhouse gas emissions. The increase in atmospheric greenhouse gases, such as CO2, methane, nitrous oxide, and halocarbons, is likely to result in an increased radiative forcing of 9% between 1998 and 2007, leading to a warming of the atmosphere (Forster et al., 2007). The concentrations of CO2 in the atmosphere are increasing linearly decade to decade. Data from the past 10 years suggests that the average yearly rate of increase is 2.24 ppm (https://www.esrl. noaa.gov/gmd/ccgg/trends/gl_gr.html). This rate of increase is more than

Figure 11.1 Annual mean data of global atmospheric CO2 from 1980 to 2017. Data adopted from https://www.esrl.noaa.gov/gmd/ccgg/trends/global.html.

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double that observed during the 1960s. Nevertheless, CO2 is an important substrate for the growth of plants other than being a potent greenhouse gas and a major contributor to global warming. The A1B emissions scenario indicates that the CO2 concentration will reach 700 1000 ppm by the end of 21st century (IPCC Climate Change, 2013), but this will sturdily depend on the future consequences of anthropogenic emissions (Woodward, 2002). This rapid surge in atmospheric CO2 concentrations encouraged researchers to study plant responses in order to better understand crop management in a future world under high CO2 levels.

11.3 PLANT RESPONSES TO ATMOSPHERIC CO2 11.3.1 CO2 Fertilization Effect The principal response of plants to elevated CO2 (EC) is an upsurge in net photosynthetic rate (Ps) and a diminution in stomatal conductance (gs) (Long et al., 2004; Gifford, 2004; Ainsworth and Rogers, 2007) (Fig. 11.2). According to Drake et al. (1997), in C3 plants, an increase in Ps arises because RuBisCO is not inundated at ambient levels of CO2. Ainsworth and Long (2005) noticed that treatment with EC resulted in a 31% rise in light-saturated leaf Ps and an upsurge of 28% in 24-hour (diurnal) photosynthetic carbon (C) assimilation during the analysis of 12 large scale free air CO2 enrichment (FACE) experiments. Under EC, contingent upon the type of plant species and C assimilation pathway, enhanced photosynthetic efficiency resulted in the modification of growth and yield responses, known as “CO2-fertilization” effect. According to Drennan and Nobel (2000), most vascular plants utilize the C3-C assimilation pathway, while approximately 3% use C4 carbon fixation, such as sorghum (Sorghum bicolor), sugarcane (Saccharum sp.), and maize (Zea mays), however, 6% 7% of species are reported to use Crassulacean acid metabolism (CAM) and these three mechanisms for C-assimilation show differential response to enhanced CO2. The current levels of atmospheric CO2 set a higher edge of Ps in C3 plants and apparently, in the past, the lower concentration of CO2 was even more curbing (Drake et al., 1997; Ainsworth and Rogers, 2007). According to Ainsworth et al. (2008), the kinetic properties of RuBisCO suggest that it functions optimally at a CO2 concentration of 200 ppm. An increase in atmospheric CO2 will certainly enhance the Ps in C3 plants (Drake et al., 1997; Makino and Mae, 1999). In comparison to C3 plants, C4 plants are not very responsive to EC as they possess a CO2 concentration mechanism

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Figure 11.2 Schematic representation of the effects of CO2 enrichment on the regulation of plant growth and metabolism.

in the mesophyll cells of their leaves (Ziska and Bunce, 1997; Ghannoum, 2009). However, the preliminary stimulation of C3 photosynthesis is not constantly sustained when plants are treated with EC for a long time and this modification is termed “photosynthetic acclimation” (Bowes, 1991; Moore et al., 1998; Seneweera et al., 2002), which conveys morphological and biochemical changes from cellular to whole plant level (Drake et al., 1997; Makino and Mae, 1999; Stitt and Krapp, 1999; Seneweera et al., 2002; Seneweera and Norton, 2011) (Fig. 11.2).

11.3.2 Growth Responses Morphological changes, growth, and development of plants in response to EC are well reviewed in both C3 and C4 species (Ghannoum et al., 2000; Ainsworth and Long, 2005), while there is a pronounced amount of interspecific variation. Commonly, EC increases the efficiency of leaf photosynthesis, causing tall plants with thick stems possessing additional

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branches and leaves (increased number of sinks) (Ainsworth and Long, 2005). Pritchard et al. (1999) observed increments in root length/diameter and branching patterns under EC, however, variations in nature and distribution could be an adaptation to root/shoot limitations, functioning rather than an inherent allometric association between shoot and root growth (Hunt and Nicholls, 1986). An increase in root growth could be an adaptation to the need to attain more nutrients to meet the increased C supplied to the roots (Rogers et al., 1997). An increase in root/shoot ratio (RSR) under EC may be attributed to higher photoassimilate partitioning to the roots due to greater Ps. This might be an adaptation to sequester more carbon for the initiation of the growth of more roots (Uprety et al., 1996). Under EC, taller and more branched plants are observed when changes arises in the shoot apices and vascular cambium. Such variations, particularly in the number of apical meristems, have a great effect on the establishment of prospective sink strength. The response of different plant species may be diverse but intraspecific variations also exist, with more determinate types showing less response than less determinate types, such as in wheat (Ziska, 2008) and soybean (Ziska and Bunce, 2000; Ainsworth et al., 2002). An explanation for higher shoot or pod numbers under EC could be the greater supply of photoassimilates (Nakano et al., 1997), while Seneweera et al. (2003) suggested that CO2 may modulate morphology and overall plant development via its impact on the variations in hormonal balance in plants (ethylene biosynthesis), such as in Oryza sativa L. (rice). Regardless of any mechanism, a yield response against EC needs an associated increase in sink capacity to compete for action of the source. Previous literature suggest substantial plasticity and several structural modifications/adaptations in leaves in response to varying environment conditions (Pritchard et al., 1999), including light and nitrogen (N) supply (Gutiérrez et al., 2009). Under elevated CO2, Ainsworth and Long (2005) established that the number of leaves increases, but leaf area index did not show a significant change in C3 grasses, while leaf expansion rate in the early growth stage may be higher (Pritchard et al., 1999; Seneweera and Conroy, 2005). Under high CO2, leaf thickness (i.e., leaf mass per unit area) frequently increases due to variations in the number and size of mesophyll cells per unit leaf area (Gutiérrez et al., 2009). Previous evidence on crop responses to EC, suggest that stomatal density reduces as the concentration of CO2 increases (Tricker et al., 2005),

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while there are some studies where density is higher, lower, or has not changed (Ainsworth and Rogers, 2007). Ainsworth and Rogers (2007) observed an average reduction in stomatal density of 5% in FACE experiments, but the findings were not statistically significant. They also suggested that variations in stomatal density are normally small ( 6 10%) and there are few evidences for a significant decline in stomatal density, so any variation in leaf conductance may be the outcome of changes in aperture and not density. The consequences of high CO2 levels on plant development and structure are many and diverse, working together with both C assimilation in plants and water relations (Seneweera and Norton, 2011). Pritchard et al. (1999) established that the most important effects of elevated CO2 are an upregulation of carbohydrate availability and a diminution in water use efficiency (WUE) and these cumulative events would lead to a rise in cell proliferation, phenological development, and availability of nutrients. In the past few years, the growth and productivity of agricultural crop species have been shown an upsurge under EC and this has enticed a substantial interest due to the variations in their response. In general, high CO2 levels pose potential positive effects on agricultural crop plants. The effects of CO2 enrichment on various plants studied so far are listed in Table 11.1.

11.3.3 Physiological Responses Elevated CO2 enhances the rate of photosynthesis and thereby the growth and productivity of plants. The key reason for this enriched photosynthesis is the increased carboxylation efficiency of RuBisCO, which is comparatively low at ambient atmospheric CO2. However, at EC, the rise in CO2 concentration at the place of CO2 fixation will unbalance the CO2/ O2 ratio; thus, the carboxylation efficiency of RuBisCO will be supported by a decreasing rate of photorespiration. C3, C4 and, CAM plants respond differently to increased CO2, which is further discussed. 11.3.3.1 Responses of C3 Plants In C3 plants, elevated CO2 stimulates photosynthesis due to the increased gradient of CO2 from ambient air to the place of CO2 fixation. According to Bowes (1991), RuBisCO is the main enzyme of the PCR cycle and also participates in the PCO cycle or photorespiration. When Ribulose-1,5-bisphosphate (RuBP) is carboxylated by RuBisCO, it generates two molecules of 3-phosphoglyceric acid (PGA) (Seneweera and Norton, 2011). Alternatively, when RuBP is oxygenated by RuBisCO, it

Table 11.1 Effects of elevated CO2 on various plants Plant CO2 dose Experimental setup

Parameter(s)

Reference

Triticum aestivum L.

Rao et al. (1995) Mulholland et al. (1997)

T. aestivum L., Triticum durum L., Triticum monococcum L.

800 ppm

CSTR

Total chl k (14.8%), carotenoids k, rbcL k, rbcS k

550 and 660 ppm

OTC

Double that of ambient 600 ppm

OTC OTC

680 ppm

OTC

680 ppm

OTC

600 ppm

OTC

702 ppm

Controlled chambers

Dry matter accumulation m (7% 23%), stem dry weight m (174%), ear dry weight m (5%), total grain dry weight m (10% 33%) Yield m (13.4% 33.8%), above ground biomass m (12.2% 32.2%) Shoot length m (14.7% 19.7%), total plant length m (13% 18%), number of tillers m (61.9% 65.8%), number of leaves m (32.8% 36.5%), leaf area m (33.6% 38.15%), leaf biomass m (46% 52.9%), total biomass m (21.6% 28.3%), grain yield m (30.4%) Grain yield m (21%), grain protein m (B12%), straw yield m (29%) Flag leaf photosynthesis m (B50%), gs k (B60%), WUE m (B40%) WUE m (81.3 91.2), foliar protein k (10.7% 11.1%), foliar nitrogen k (11.6% 14%), phenol m (17.3%), TSS m (7.5%), starch m (16% 16.4%) Total dry weight m (65.8%), RGR m (6.6%)

550 ppm

FACE

gs k (9.1% 33%), leaf area m (7.5% 21.8%), dry weight of whole plant m (21% 46%), grain yield m (13% 22%), harvest index m (7.6% 31%)

Bender et al. (1999) Deepak and Agrawal (1999)

Pleijel et al. (2000) Donnelly et al. (2000) Agrawal and Deepak (2003) CardosoVilhena et al. (2004) Uprety et al. (2009)

T. monococcum L., Triticum dicoccoides L., T. aestivum L. T. aestivum L.

550 ppm

FACE

700 ppm

OTC

OTC

Solanum tuberosum L.

280 ppm

OTC

570 ppm

OTC

Average size of starch grain m (54% 93%), starch content m (1.6 5 times), grain protein (11% 47%) Plant height m (27.5% 30.3%), number of leaves m (16.2% 32%), total biomass m (16.6 19.8), NAR m (24% 30%), LAR k (16.8% 18.6%), RSR m (26.3% 57%), grain yield m (46% 54.6%), grain protein k (5.4% 8.9%), TFAA k (6.9% 10.4%), TSS m (18.6% 28.9%), SC m (8.3% 19.7%) Total chl m (7.6% 11.2%), carotenoids k (9.6% 12.7%), Ps m (29.7% 30.8%), gs k (18.9% 35.4%), Fv/Fm m (1.7% 3.4%), H2O2 k (16% 41.6%), 2O2 k (23% 33%), LPO k (13% 32.6%), SL k (6.6% 22.5%), AA k (9.2% 15%), SOD k (12% 14%), APX k (44% 54%), GR k (33.3 38.8), foliar protein k (5.7% 7.3%), PAL m (23.9% 26.7%), total phenolics m (17.6% 24.6%) Haulm dry weight m (15%), haulm/tuber ratio m (13%), average size of tubers m (18%) Plant height m (29.3%), number of leaves m (21.4%), number of tubers m (82.5%), fresh tuber weight m (92.4%), tuber dry weight m (135%), total biomass m (17.4 107.4%), RGR m (9.3%), NAR m (12.5%), SLA k (28.7%), starch content m (130.6%), reducing sugars k (32%), soluble sugars m (63.8%), total nitrogen k (15.2%), organic carbon m (20%), C/N ratio m (41.6%)

Sinha et al. (2009) Mishra et al. (2013a)

Mishra et al. (2013b)

Persson et al. (2003) Kumari and Agrawal (2014)

(Continued)

Table 11.1 (Continued) Plant

Glycine max L.

Zea mays L.

Vigna radiata L.

CO2 dose

Experimental setup

Parameter(s)

Reference

OTC

Ps m (57.9% 65.3%), gs k (27.9%), Fv/Fm m (8.6%), total chl m (37.3%), carotenoids m (28.1% 31.6%), protein content k (13.9%), ascorbic acid k (8.1%), APX k (17.5%), CAT k (16.2%), SOD k (15.4%), GR k (24.7%) A m (56%), photorespiration k (36%), glycolate oxidase k, CAT k, hydroxy pyruvate reductase k A m (60%), relative RuBP regeneration limitation m (44%), relative stomatal limitation m (5%)

Kumari et al. (2015)

726 ppm

OTC

727 ppm

OTC

600 ppm

OTC

575 630 ppm

OTC

700 ppm

OTC

1180 ppm 575 630 ppm

OTC OTC

Plant height m (8% 14%), number of branches m (29% 48%), leaf area m (26% 47%), total biomass m (26% 35%), Ps m (30% 33%), foliar protein k, yield m (31% 38%) Ps m (ns-10%), dark respiration k (ns), R/P ratio k (ns-29%) gs k (35.6%), E k (32%), leaf area m (7%), leaf dry weight m (29%), SLW m (9%), shoot length m (11%), root dry weight m (19%), dry stem weight m (44%) gs k (38%), Am (ns) Ps m (23% 55%), dark respiration k (15% 37%), R/P ratio k (50% 59%), dry leaf weight m, weight of roots m (30% 57%), root/shoot weight m (28% 42%), seed yield m (19% 23%)

Booker et al. (1997) Reid and Fiscus (1998) Deepak and Agrawal (2001) Uprety et al. (1996) Vanaja et al. (2011)

Bunce (2014) Uprety et al. (1996)

Vigna mungo L.

600 ppm

OTC

600 ppm

OTC

600 ppm

OTC

700 ppm

OTC

600 ppm

OTC

Ps m (73.9% 124.9%), leaf dry weight m (12% 133%), leaf area m (30% 71%), root length m (12% 28%), root weight m (106% 236%), pod number m (32%), seed number m (39.6%) Dry weight m (36% 47%), leaf area m (3% 9%), leaf number (16% 29%), plant height m (3% 35%), chl a k (10% 18%), Ps m (13% 96%), rate of respiration k (54% 62%) Total soluble protein k (27.4%), total nitrogenase activity m 2 O2 k (11.8% 24.8%), H2O2 k (23.5% 27.8%), LPO k (17.6% 22.9%), SOD k (11.8% 14.7%), CAT k (64.3%), total chl m (30.6% 38.9%), carotenoids k (8.1% 14.7%), Ps m (25.4% 29.2%), gs k (18.6% 33.9%), Ci m (9% 14%), WUE m (47.5% 61.5%), plant height m (19% 26%), number of leaves m (21.3% 24.6%), leaf area m (20.5% 22.3%), number of nodules m (43% 50%), total biomass m (19.8% 33.6%), seed yield m (25.3% 40%), seed protein k (9.9%), TSS m (9.3% 15.1%), SC m (15.5%) % germination m (5.2% 22%), vigor index m (20% 31%), shoot length m (9.8% 12%), leaf area m (17% 27%), dry leaf weight m (28.43%), dry stem weight m (36% 44%), dry root weight m (20% 40%), total dry weight m (31% 41%)

Srivastava et al. (2001)

Das et al. (2002)

Srivastava et al. (2002) Mishra and Agrawal (2014)

Vanaja et al. (2006)

(Continued)

Table 11.1 (Continued) Plant

CO2 dose

Experimental setup

Parameter(s)

Reference

550 and 700 ppm

OTC

Vanaja et al. (2007)

Brassica juncea L.

600 ppm

OTC

Helianthus annus L.

700 ppm

OTC

550 ppm

OTC

550 ppm

OTC

550 ppm

OTC

Shoot length m (2% 34%), stem dry weight m (4% 80%), root length m (2% 38%), leaf area m (18% 90%), total biomass m (2% 70%), pod weight m (18.4% 51.3%), seed yield m (2.3% 47.6%), harvest index m (38.7% 39.5%) Carbon content in plant parts m (29% 40%), nitrogen content in plant parts k (29% 30%), C/N ratiom (50% 95%), nonreducing sugars m (44%), reducing sugars m (39%), starch content m (64%) gs k (46.8%), E k (18%), leaf area m (8%), leaf dry weight m (7%), SLW m (17%), shoot length m (11%), root dry weight m (45%), dry stem weight m (24%) Ps m (25.5% 52.1%), plant height m (14.6% 68%), 100-seed weight m (50% 64.3%), seed yield m (35% 46%), percentage of seed oil m (5.3% 15.4%), total seed protein k (10.9% 12.7%), Ca k (8.2%), Na k (43.6%), K k (35%), Fe k (34.6%), Mn k (26.2), Cu k (23.3%), Zn k (22.6%), percentage of oleic acid m (9%) Percentage of N (ns), leaf area (ns), shoot dry mass m, seed yield m TDM m (22.2% 54%), root dry weight m (65.3%), flower number m, pod yield m (76.7% 119.7%)

Phaseolus vulgaris L.

Uprety and Rabha (1999)

Vanaja et al. (2011)

Pal et al. (2014)

Bunce (2008) Rao et al. (2015)

Oryza sativa L.

760, 1140 and 1520 ppm 1200 ppm

Growth chamber FACE

Ps, gs, and E m up to 1140 ppm but k at 1520 ppm

1200 ppm

FACE

N content k, Ci/Ca ratio (ns), RuBisCO content k

gs k (0% 64%), decrease in leaf water potential k

Bokhari et al. (2007) Shimono et al. (2010) Zhu et al. (2012)

CSTR, Continuous stirred tank reactor; FACE, free air CO2 enrichment; OTC, open top chamber; m, increase; k, decrease; A, net assimilation rate; R/P ratio, respiration/photosynthesis ratio; TDM, above ground total dry matter; FBPase, fructose-1, 6-bisphosphate phosphatase; Vc,max, in vivo apparent RuBisCO activity; Amax: assimilation rate per unit leaf area under light and CO2 saturation; Ps, net photosynthetic rate; gs, stomatal conductance; E, transpiration rate; WUE, water use efficiency; Ci, internal CO2 concentration; Ca, atmospheric CO2 concentration; Fv/Fm, chlorophyll fluorescence; ANPP, cumulative above-ground net primary production; chl, chlorophyll; 2O2: superoxide radical; H2O2, hydrogen peroxide content; LPO, lipid peroxidation; SOD, superoxide dismutase activity; POD, peroxidase activity; CAT, catalase activity; APX, ascorbate peroxidase activity; GR, glutathione reductase activity; PAL, phenylalanine ammonia lyase activity; rbcL, RuBisCO large subunit; rbcS, RuBisCO small subunit; N, nitrogen; ns, not significant.

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forms one molecule each of PGA and 2-phosphoglycolate (PG). PGA is further reduced into carbohydrates and is also utilized in regenerating RuBP. Oxygenation of RuBP generates PG, which is considered a waste product that utilizes a considerable amount of light energy originating from the light reaction of photosynthesis. Sharkey (1985) suggested that at the present atmospheric concentration of O2 of 21 kPa and 380 µmol CO2 mol21, the generation of PG will lead to a decrease in potential photosynthetic capacity by 20% 50% depending on temperature. Bokhari et al. (2007) subjected 10 day-old rice seedlings to 760, 1140, and 1520 ppm CO2 concentrations, respectively for 24 hours each and noticed that Ps, gs, and transpiration rate (E) increased maximally at 1140 ppm CO2, but further treatment to 1520 ppm for 24 hours caused the downregulation of these. Doubling the present atmospheric CO2 will totally prevent C3 photorespiration, which will lead to a rise in the photosynthetic efficiency of these plants (Bowes, 1991; Sage and Kubien, 2007). Seneweera and Norton (2011) suggested three major limitations in C3 photosynthesis, namely: 1. Limitation of photosynthesis urged by RuBisCO due to the supply and utilization of CO2. 2. Supply and utilization of light, which confines the electron transport rate for the regeneration of RuBP. 3. Utilization of triose phosphate, which limits the ease of use of inorganic phosphorus (Pi) in the chloroplast for synthesis of ATP to regenerate RuBP (Farquhar and Sharkey, 1982; Sharkey, 1985). Under elevated CO2 conditions, the second and third limitations are generally observed (Sharkey, 1985; Makino and Mae, 1999). The second limitation may result due to low photosynthetic photon flux densities or the inability to transform light energy into chemical energy. The third constraint, triose phosphate limitation, arises when there is a disproportion in carbohydrate synthesis and its utilization (Sharkey, 1985; Paul and Foyer, 2001). 11.3.3.2 Responses of C4 Plants Plants possessing a C4 photosynthesis mechanism for C-assimilation are able to concentrate CO2 in the mesophyll tissue up to 2000 µmol mol21, which totally suppresses the oxygenation reaction leading to the saturation of carboxylation process (Hatch and Slack, 1968; Poorter and Navas, 2003). Because of this reason, photosynthesis in C4 plants is not supposed

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to rise under EC. However, previous reports suggest that C4 growth is stimulated under EC (Samarakoon and Gifford, 1996; Seneweera et al., 1998; Ziska et al., 1999; Leakey et al., 2006b; Ghannoum, 2009). Increased C4 growth under EC is partially interceded by changes in plant water relations (Seneweera et al., 1998, 2001; Ziska et al., 1999; Ghannoum et al., 2001; Leakey et al., 2004). The progressive responses of C4 plants to high CO2 may be the outcome of several other factors, such as leakage of CO2 into the bundle sheath cells, direct fixation of CO2 in the bundle sheath, and the occurrence of C3-plant-like photosynthesis during the expansion of leaves (Wand et al., 1999). From a meta-analysis, a decrease of 30% in gs of C4 plants under EC was reported, which is comparable to the response of C3 plants (Ghannoum et al., 2000; Ainsworth and Rogers, 2007). In general, EC decreases gs, which in turn lessens the transpiration rate of plants leading to better soil water availability at later growth stages (Seneweera et al., 1998; Leakey et al., 2004, 2006a); however, the mechanisms controlling stomatal movement under EC have not been clearly described. In a report, photosynthesis in maize plant did not increased under EC where there was no soil water scarcity during its growing season, but photosynthesis was enhanced in that year when episodic water stress took place (Leakey et al., 2006b). They concluded that EC indirectly enriches C gain during drought conditions. Therefore, enhanced growth in C4 plants under EC is not a straight photosynthetic response, but might have resulted due to decreased drought stress as water use is lesser, which reserves water in order to increase the duration of photosynthesis (Seneweera et al., 2002; Leakey et al., 2009). 11.3.3.3 Responses of CAM Plants CAM is an adaptation observed in some vascular plants, such as prickly pear (Opuntia stricta), agave (Agave salmania), and pineapple (Ananas comosus). Fixation of CO2 and CO2 metabolism are progressively divided in CAM plants. Fixation of CO2 occurs at night, the early morning, and/or the late afternoon catalyzed by the cytosolic enzyme phosphoenolpyruvate carboxylase (PEPC) to produce malate or aspartate, which is finally stored in the vacuoles (Seneweera and Norton, 2011). Decarboxylation takes place during the daytime and results in the release of CO2 from the malic or aspartic acid, which is finally converted into carbohydrates (Winter and Smith, 1996). Usually, CAM plants possess three to five-fold greater transpiration efficiencies than C3 or C4 plants

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(Nobel, 1996) and frequently these species exist in environments where water shortages prevail (Drennan and Nobel, 2000). Drennan and Nobel (2000) noticed an increase in both day and nighttime CO2 uptake in 10 species with an average biomass rise of about 35% when CO2 was doubled. They suggested that CO2 fixation by RuBisCO is enhanced in the late afternoon along with nocturnal CO2 fixation, however carboxylation activities of both RuBisCO and PEPC are reduced in response to EC. Under EC, nocturnal malate levels increase with increments in carbohydrate contents (Drennan and Nobel, 2000). Reductions in RuBisCO content in CAM species under EC are compensated by the upregulation of enzyme activities in order to maintain photosynthesis. With diminutive evidence of photosynthetic acclimation against EC, some CAM plants display greater CO2 assimilation (source capacity), higher transport of sucrose in the phloem, and sturdy sink strength (Drennan and Nobel, 2000; Osmond et al., 2008). Due to these adaptations, a better understanding of the mechanisms directing C gain in CAM plants may pave the way for new insights into physiological mechanisms that could help in the genetic manipulation of C3 species for C rich environments. 11.3.3.4 Effect of CO2 on RuBisCO In C3 plants, RuBisCO is a rate-limiting enzyme used in the process of photosynthesis and is comprised of about 56% of all soluble protein and 26% of total leaf nitrogen (N) (Makino and Osmond, 1991). According to Mae et al. (1983), the amount of RuBisCO in the leaves is the outcome of the equilibrium between its production and degradation. In plant cells, RuBisCO synthesis is regulated by transcriptional, posttranscriptional, and translational processes (Moore et al., 1999; Stitt and Krapp, 1999). RuBisCO is promptly generated during the development of leaves followed by a progressive degradation (Suzuki et al., 2001). The synthesis of RuBisCO and its degradation are influenced by environmental factors, such as light intensity, soil nitrogen, CO2, and O3. Under EC, changes in leaf N status are strongly associated to a diminution in RuBisCO content and photosynthetic acclimation. Under elevated CO2, Makino et al. (2000) reported a loss of 30% in RuBisCO before it begins to confine photosynthesis. The suppression of RuBisCO synthesis takes place when an imbalance occurs between supply and utilization of carbohydrates under EC (Moore et al., 1998, 1999). Approximately 80% 90% of RuBisCO is formed just before the full expansion of leaf blades in

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cereal crops (Suzuki et al., 2001; Feller et al., 2008; Seneweera and Norton, 2011). Similarly, upregulation in rbcS and rbcL mRNA occurs during leaf expansion and reaches a maximum a few days before full expansion, while little RuBisCO is synthesized after full expansion. According to Ludewig and Sonnewald (2000), the downregulation of photosynthetic genes under EC is evident only in senescing leaves and no association was noticed between gene transcripts and soluble sugars. In monocots, the degradation of RuBisCO is constantly preponderant after complete expansion of the leaf blade leading to a prompt decrease in RuBisCO content. This might be a modifying recovery mechanism in relation to nutrient remobilization for the development of sinks as RuBisCO characterizes a significant store of N as well as a role in its metabolism. However, the mechanism by which EC speeds up degradation of RuBisCO is not well understood. Under elevated CO2, the activities of antioxidative enzymes like superoxide dismutase (SOD), peroxidase (POX), catalase (CAT), ascorbate peroxidase (APX), and glutathione peroxidase (GPX) are lower (Pritchard et al., 2000; Vurro et al., 2009). These enzymes are well-known to combat highly reactive oxygen species (ROS). Under elevated CO2, a decrease in the activities of antioxidative enzymes may lead to an upregulation in ROS levels in the chloroplast, which could possibly contribute to the degradation of RuBisCO.

11.3.4 Biochemical Responses The primary effects of elevated CO2 include the stimulation of photosynthesis and growth in C3 species, declined RuBisCO content, and decreased stomatal conductance (Bowes, 1991; Drake et al., 1997; Ainsworth and Long, 2005; Ainsworth and Rogers, 2007). These physiological effects altogether have led to the general hypothesis that the antioxidant metabolism will be downregulated in plants grown under EC. This hypothesis has led to many assumptions, including: (1) that ROS formation will be conquered by lower rates of RuBisCO oxygenase reaction and subsequent photorespiration at EC (Polle et al., 1993; Mishra and Agrawal, 2014); (2) EC will reduce the electron leakage from photosystem I to oxygen and decrease the chloroplastic oxidative stress (Polle, 1996); and (3) less susceptibility to drought as a result of decreased stomatal conductance will reduce ABA-mediated upregulation of the antioxidant metabolism (Jiang and Zhang, 2002). However, direct evidence to

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support any of these predictions is not regular in the literature and the available studies show mixed up/down-regulation of specific biochemical constituents of the antioxidant metabolism in plants treated with EC (Rao et al., 1995; Polle et al., 1997; Pritchard et al., 2000; di Toppi et al., 2002; Mishra and Agrawal, 2014). Increments in the ascorbic acid and total phenolic contents were recorded in Beta vulgaris (Kumari et al., 2013) and stimulations in the ascorbate (ASC), glutathione (GSH), and ASC/GSH levels, along with their redox status were noticed in Lolium perenne and Medicago lupulina (Farfan-Vignolo and Asard, 2012), when the plants were subjected to elevated CO2. AbdElgawad et al. (2015) noticed that elevated CO2 can decrease the hydrogen peroxide (H2O2) level, lipid peroxidation (LPO), and lipoxygenase (LOX) activity, while the activities of SOD, CAT, GPX, and glutathione reductase (GR) levels were reduced and the ascorbate-glutathione cycle was unaffected in C3 grasses (L. perenne, Poa pratensis) and legumes (M. lupulina, Lotus corniculatus). Therefore, the principal form of the enzymatic antioxidant defense mechanism may sturdily depend on species and applied abiotic stress (Duarte et al., 2013; Singh and Agrawal, 2015). Havir and McHale (1987) found decreased CAT activity but no effect on the activity of SOD in tobacco treated with elevated CO2. Antioxidative enzyme activities were reduced in plants grown under EC compared to plants grown at ambient CO2 levels (Wustman et al., 2001). Based on a study performed by Badiani et al. (1998) with plants grown in naturally occurring EC springs, a mix of up/downregulation of antioxidant enzyme activities was revealed, with SOD and GR upregulated; and CAT, APX, dehydroascorbate reductase (DHAR), and monodehydroascorbate reductase (MDHAR) downregulated. Pritchard et al. (2000) noticed that antioxidant enzymes are commonly downregulated in soybean at elevated CO2. Mishra and Agrawal (2014) reported a marked downregulation of ROS levels, membrane disruption, and the activities of SOD and CAT in mung bean cultivars under elevated CO2. In contrast, a different hypothesis has been formulated which suggests that endogenous ROS production will increase in plants grown under EC leading to greater oxidative stress. Plants grown under EC possess increased rates of respiration (Leakey et al., 2009), a greater number of mitochondria (Griffin et al., 2001), and greater protein carboxylation (Qiu et al., 2008). Therefore, the question of, how the plant antioxidant system will be affected by elevated CO2 levels, is yet to be clearly investigated.

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11.3.5 Molecular Changes in Plants Under CO2 Enrichment Carbon dioxide enrichment can induce a noticeable decrease in photorespiration, advising that there may be an involvement of the expression of the genes in the photorespiration pathway (Sharkey, 1988; Novitskaya et al., 2002; Foyer et al., 2009; Florian et al., 2014; Wang et al., 2014). Differential expression in a number of genes and proteins associated with the process of photosynthesis take place when plants are subjected to elevated CO2 (Gamage et al., 2018). A study by Eisenhut et al. (2013) in Arabidopsis suggested that A BOUT DE SOUFFLE (BOU), a gene encoding a mitochondrial carrier, possibly participates in photorespiration since the knockout mutant bou-2 can check growth at ambient atmospheric CO2, but not at elevated CO2. In another study by Timm and Bauwe (2013), defective plants (glyk1 mutants) containing a gene which encodes glycerate kinase (GLYK), cannot develop at ambient CO2 levels but completely recuperate at elevated CO2, however, the exact mechanism that facilitates the requirement of high CO2 by the mutants is unknown. Florian et al. (2014) noticed that the transcript levels of photorespiratory genes were almost unaffected at elevated CO2 except for reductions in the transcript levels of GDCH1 (glycine decarboxylase H-protein) which is known to be involved in photorespiratory carbon recovery in Arabidopsis. Therefore, the role of photorespiratory gene expression in response to variations in atmospheric CO2 are typically unknown and need further examination (Foyer et al., 2009; Timm and Bauwe, 2013; Florian et al., 2014). Markelz et al. (2014) described the expression of the respiratory genes in Arabidopsis thaliana plants treated with elevated CO2 as having sufficient and limited N availability. The analysis showed that 4439 transcripts were significantly different under ambient and elevated levels of CO2, in particular, the genes related to protein synthesis (constituents of glycolysis, the TCA cycle, and the mitochondrial electron transport chain (ETC, and mitochondrial protein import complexes)) were higher during the day due to CO2 enrichment. Fukayama et al. (2011) noticed the upregulation of the transcription of genes related to respiration in rice under elevated CO2. The grain proteome is altered under CO2 enrichment in wheat, mainly the gluten proteins leading to a poor quality of bread (Wieser et al., 2008; Hogy et al., 2009a; Fernando et al., 2015). Hogy et al. (2009b) observed variations in metabolic proteins which are involved in different physiological processes under elevated CO2. Wieser et al. (2008)

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found that treatment with elevated CO2 decreased the gliadin to glutenin ratio, which led to a damaging effect on dough rheology physiognomies. A study by Panozzo et al. (2014) on wheat reported increments in metabolic proteins under CO2 enrichment. Arachchige et al. (2017) found altered protein composition during proteome-wide analysis in wheat under CO2 enrichment. Additionally, large genetic variations in grain protein concentrations (GPC) have been noticed (Fernando et al., 2014), but grain proteome response mechanisms in different genetic contexts are still unknown under elevated CO2. Hogy et al. (2009b) suggested that responsive proteins under EC may serve as genetic/molecular markers for the selection of associated traits for quality and could, thus, play an important role in prospective breeding programs for adaptation to global climate change. However, analysis of the grain proteome has been always a challenging task due to its broad range of proteins, but the main benefit of this approach is the estimation of post-transcriptional modifications in gene products that are not identified via analysis of transcriptomes. Thus, understanding the response of the grain protein and/or proteome under elevated CO2 conditions will become progressively significant as atmospheric CO2 levels have been predicted to rise in the near future.

11.3.6 Yield The forthright effects of elevated CO2 on photosynthesis and gs lead to variations in crop growth, the allocation of carbon, biomass accumulation, and finally seed yield. In general, crop responses under CO2 enrichment show higher growth and yield, although there are important interactions with N, water, and temperature. It is well-known that increases in seed yield due to EC are lesser in magnitude than the stimulation of photosynthesis and aboveground biomass, signifying that feedbacks constrain the prospective benefits of EC (Long et al., 2004). Foliar respiration during the nighttime in soybean is stimulated under EC (Leakey et al., 2006a, 2009), which decreases plant carbon balance but might be essential for the generation of energy for distribution of extra carbohydrates from the leaves to reproductive sinks. Meta-analysis data from 40 species across 12 FACE sites revealed that growth and aboveground biomass generally increase under EC, with an average crop yield increment of 17% (Ainsworth and Long, 2005). Among different plant groups, C3 species are the most responsive, although there are reports that N-fixing dicots respond well under low nutrient levels (Poorter and Navas, 2003).

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Increased economic yield under EC may involve larger seed or grain size, greater number of seeds/grains per pod/plant or ear/panicle, and/or additional reproductive structures per plant. Under CO2 enrichment, the yield benefit for most C3 crops, like wheat, rice, soybean, and mung bean, is due to increased aboveground dry matter production contributing toward a greater amount of reproductive structures (Pinter et al., 1996; Deepak and Agrawal, 1999; Kim et al., 2001, 2003; Morgan et al., 2005; Mishra and Agrawal, 2014). Under EC, the response of a number of C3 crops other than principal cereals have been studied in FACE experiments, including sugar beet (B. vulgaris), potato (Solanum tuberosum), barley (Hordeum vulgare), and oilseed rape (Brassica napus), which were reported to show greater yields. Tuber production was significantly higher under CO2 enrichment, whereas the production of aboveground dry matter was not changed in potato (S. tuberosum) (Bindi et al., 2006). Miglietta et al. (1998) suggested that the number of tubers, rather than the size of the tubers contributed to an increase in yield. Also, the proportion of deformed tubers was not affected by EC (Bindi et al., 2006). The response of two C4 crops, viz., sorghum (S. bicolor) and maize (Z. mays), under elevated CO2 has been evaluated in FACE experiments (Ottman et al., 2001; Leakey et al., 2004, 2006b). The results suggested that EC had no effect on seed yield when averaged across varying growth conditions and two growing seasons (Ottman et al., 2001; Leakey et al., 2004, 2006b). Under elevated CO2 treatment, the final yield, grain weight, and harvest index of C4 crops were not affected. Ottman et al. (2001) observed an inclination toward higher yield and aboveground biomass when sorghum was grown under high CO2 concentrations and water stress. According to Leakey et al. (2009), this observation supports the fact that in future, C4 plants will benefit from elevated CO2 in times and areas affected by drought, but more studies are needed to reduce the uncertainty of this prediction. A study conducted on sugarcane in opentop chambers (OTCs) showed that elevated CO2 (720 ppm) enhanced photosynthesis, plant height, biomass, and sucrose content by 30%, 17%, 40%, and 29%, respectively (de Souza et al., 2008). The data collected in the study also suggested that sugarcane productivity might increase in the near future; however, the OTCs may have overestimated the effects of elevated CO2 and caused transitory water stress (de Souza et al., 2008). Under CO2 enrichment, the two most studied characteristics of yield quality; protein and nitrogen, are important issues (Uddling et al., 2018). Taub et al. (2008) found a reduction in the protein content of grains

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during a meta-analysis of crops grown under EC. Significant reductions ranging between 10% and 14% were observed in nonleguminous crops, like barley, wheat, rice, and potato, however, for soybean, an important leguminous crop worldwide, the reduction was much smaller, only 1.5% (Taub et al., 2008). The reason may be accredited to the fact that legumes possess the ability to fix N, which would prevent N dilution. A decrease in N concentration has been observed in the grains of wheat (Manderscheid et al., 1995; Pleijel and Uddling, 2012), barley (Manderscheid et al., 1995), and rice (Kobayashi et al., 2006) under CO2 enrichment. Under elevated CO2, GPC was reduced by between 3.9% and 14.1% depending on the treatment system and volume of rooting (Kimball et al., 2002). The largest decrease in GPC was noticed in OTC experiments with restricted rooting volumes, which can be ascribed to a feedback inhibition of the photosynthetic CO2 response and the accrual of nonstructural carbohydrates (Weigel and Manderscheid, 2005). In a meta-analytic study by Taub et al. (2008), a 10% mean reduction in total GPC under elevated CO2 across a range of different environmental conditions was reported. Arachchige et al. (2017) reported a significant decrease in GPC in wheat and the responses varied between different genotypes at an elevated CO2 concentration of 550 6 20 µmol mol21. The findings of Arachchige et al. (2017) also suggested that it was mainly the storage proteins that was reduced at elevated CO2. A significant decline in the protein content of rice grains have also been noticed under CO2 enrichment (Conroy et al., 1994; Seneweera and Conroy, 1997; Uprety and Reddy, 2008). Mishra and Agrawal (2014) found a significant decrease in the soluble protein contents in the leaves and seeds of mung bean cultivars.

11.4 INTERACTION WITH AIR POLLUTANTS Key air pollutants that cause damage to flora include sulfur dioxide (SO2), fluorides, nitrogen oxides (NOx, principally NO and NO2), peroxy-acyl nitrates (PAN), and tropospheric ozone (O3). The different processes of fossil fuel combustion that release CO2 into the atmosphere also will introduce several other air pollutants or their precursors. NOx is produced by high-temperature incineration and participates in photochemical reactions with hydrocarbons, which generate phytotoxic oxidants, O3, and PANs. Other phytotoxic pollutants comprise of carbon monoxide, ambient oxidant complexes (other than O3, PAN, or NOx), chlorine,

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ammonia, hydrogen chloride, mercury vapors, fly ashes, dust, sulfuric acid mist, hydrogen sulfide, and ethylene. Presently, three major phytotoxic pollutants that cause damage to vegetation are O3, SO2, and NO2 due to their prevalent distribution across the commercial world. According to Rozema (1993), high atmospheric CO2 levels are accompanied by gaseous air pollutants, like SO2, NOx, and O3, in industrialized and populated areas. This has provoked widespread concern to estimate the effects of high CO2 and air pollutants (Barnes and Pfirrmann, 1992; Mulchi et al., 1992). The effects of elevated levels of CO2 and SO2 on plant development and productivity have been comprehensively studied individually for a large number of plant species, but in spite of widespread recognition that the levels of several trace gases will rise concurrently with atmospheric CO2 in ambient air, relatively few studies are available on plant responses to increasing concentrations of combined CO2 and SO2 (Carlson and Bazzaz, 1982, 1985; Carlson, 1983; Miszalski and Mydlarz, 1990; Rao and DeKok, 1994; Deepak and Agrawal, 1999, 2001; Agrawal and Deepak, 2003). Reductions in the growth and yield of wheat (Triticum aestivum L. cv. Malviya 234) have been observed, when plants were treated with SO2 alone at a concentration of 0.06 ppm, however, elevated CO2 (600 6 25 ppm) alone and in combination with SO2 stimulated growth and yield (Deepak and Agrawal, 1999). Another study by Agrawal and Deepak (2003) on wheat cultivars (T. aestivum L. cv. Malviya 234 and HP1209) suggested that elevated CO2 changed the plants’ response to elevated SO2. Similar observations were recorded by Deepak and Agrawal (2001) in a study conducted on two cultivars of soybean (Glycine max cv. Bragg and PK 472), where the adverse effects of SO2 was mitigated by elevated CO2 treatment. Saxe (1986) found an increase in photosynthesis of an average of 41% across a range of species under CO2 enrichment of 1000 µmol mol21 as compared to ambient air. Increased photosynthesis was also observed in a combined treatment of CO2 and nitrogen monoxide (NO), but the response was less than that found under CO2 enrichment alone (Saxe, 1986). The responses of the plants to elevated CO2 alone and in combination with NO were closely related day-by-day. Transpiration rate was also decreased under elevated CO2, which was further reduced after the addition of NO. According to Hand (1986), such gaseous conditions occur in commercial greenhouses when hydrocarbon fuels are burned for direct CO2 enrichment, so the effects of the mixture of these gases may be interesting.

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Ozone (O3) present in the troposphere is toxic, and adversely affects crop productivity, thus, posing a threat to global food security (Ainsworth et al., 2012; Mishra and Agrawal, 2015). Both CO2 and O3 have substantial effects on plant physiology and crop production, thus, understanding crop responses to a combination of elevated concentrations of both gases is one of the most important issues in view of future global climate change. Elevated CO2 generally has a growth stimulating effect as it causes a rise in photosynthesis; however, O3 tends to have the opposite effect (Fig. 11.3). According to Barnes and Davison (1988), both factors can directly affect physiological and biochemical processes, such as plant senescence, that might affect plant responses to other biotic/abiotic stresses. The nature of the interaction may be influenced by the features of the O3 exposure pattern (timing in relation to phenological development, chronic/acute exposure), plant species, water availability, and other climatic parameters, but it will also depend upon the kind of effect that is considered, that is, visible injury, photosynthesis, total biomass, or economic yield, etc. In general, elevated CO2 reduces O3-induced leaf

Figure 11.3 A diagrammatic representation of the effects of elevated CO2 and O3, singly and in combination.

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damage and yield losses, primarily through O3 exclusion via a decrease in gs, but also to a certain extent due to an increased detoxification capacity. To date, studies that have observed the effects of CO2 and O3, singly and in combination have shown a variety of plant responses (Table 11.2). Foliar O3 injury (interveinal chlorosis/chlorotic spots) was decreased substantially by CO2 enrichment in a number of agricultural crop plants, for example, tobacco (Heck and Dunning, 1967), wheat (Mortensen, 1990; McKee et al., 1995; Rao et al., 1995; Fangmeier et al., 1996; Mulholland et al., 1997; Cardoso-Vilhena et al., 1998; Mishra et al., 2013a), radish (Barnes and Pfirrmann, 1992), barley (Fangmeier et al., 1996), snap bean (Cardoso-Vilhena et al., 1998), and potato (De Temmerman et al., 2002). For wheat, CO2 treatment swayed the severity of visible foliar damage and provided protection against O3-induced early senescence during vegetative plant growth (Mulholland et al., 1997; Mishra et al., 2013a). However, CO2 enrichment had only a partial protective effect (decreased foliar injury) for a sensitive clone of white clover (Heagle et al., 1993) and had no effect on O3 injury in the leaves of Phaseolus vulgaris (Heck and Dunning, 1967). According to Volin et al. (1998), the exposure of C3 and C4 grass species to O3 increased leaf dark respiration and reduced photosynthesis, which was not observed in an elevated CO2 environment. As repair processes on a cellular level depend primarily on dark respiration, the cost of repair is lower in elevated CO2 conditions. The duration of the dark period is also an important factor for a plant to recover from O3 exposure during the day. De Temmerman et al. (2002) suggested that crops, such as potato, show visible injury symptoms at much lower O3 concentrations during the long days in summer when the dark period becomes too short for repair processes. Previous studies on the impact of high CO2 and air pollutant concentrations revealed that the elimination of toxicity caused by air pollutants at elevated CO2 was largely due to the stimulation of internal detoxification mechanisms rather than reduced pollutant uptake (Barnes and Pfirrmann, 1992; Mulchi et al., 1992). The relative stimulation by elevated CO2 tends to be larger in an atmosphere with increased levels of O3, or vice versa; in a CO2-enriched atmosphere, the negative effects of O3 are less than at ambient CO2. In determinate crops (such as cereals), yield not only depends on photosynthesis but also on the extent of the active period of leaf photosynthesis and the sink capacity of the grains. Booker et al. (2007) demonstrated that elevated CO2 alleviated the inhibitory effects of O3 on the photosynthesis and biomass of peanuts.

Table 11.2 Response of crop plants against combined exposure of CO2 and O3 Plant

CO2 dose

O3 dose

Experimental setup

Plant characteristics

Reference

G. max L.

700 ppm

80 ppb

OTC

Reid et al. (1998)

718 ppm

72 ppb

OTC

700 ppm

1.5 3 Ambient

OTC

550 ppm

1.23 3 ambient

SoyFACE

RuBisCO activity k (ns), RuBisCO content k (ns) Whole plant water loss k (22%), leaf area m (9%), WUE (ns), seed yield (ns) A m (20% 26%), Ci m (2.1 times), total soluble protein k (22% 29%) A m (19%), JPSII m (3%), gs k (16%)

550 ppm

Twice the ambient

SoyFACE

gs k (26%)

Raphanus sativus L.

765 ppm

73 ppb

Controlled chambers

Asat (ns), gs k (62%), WUE m, SLA k, plant growth (ns)

T. aestivum L.

800 ppm

120 ppb

CSTR

1150 ppm

40 ppb

OTC

550 and 660 ppm

140 ppb

OTC

Double than ambient 680 ppm

Low and high

OTC

150 ppb

OTC

680 ppm

1.5 3 ambient and 2 3 ambient

OTC

Shoot biomass m, total chl (ns), carotenoids (ns), rbcL (ns), rbcS (ns) Dry biomass (ns), straw (ns), grain yield (ns), number of seeds (ns), harvest index (ns), 1000 seed weight (ns) Dry matter accumulation (ns), stem dry weight (ns), ear dry weight (ns), total grain dry weight (ns) Grain yield m (18.7% 30%), above ground biomass m (16.9% 30.6%) Flag leaf photosynthesis m (B10% 20%), gs k (B20% 75%), WUE m (B10% 80%) Grain yield (ns), grain protein (ns), straw yield (ns), harvest index (ns)

Booker et al. (2004) Booker and Fiscus (2005) Bernacchi et al. (2006) Gillespie et al. (2012) Barnes and Pfirrmann (1992) Rao et al. (1995) Rudorff et al. (1996) Mulholland et al. (1997) Bender et al. (1999) Donnelly et al. (2000) Pleijel et al. (2000)

S. tuberosum L.

700 ppm

75 ppb

700 ppm

Ambient 1 10 ppb

Controlled chamber OTC

700 ppm

Ambient 1 10 ppb

OTC

714 ppm

72 ppb

Greenhouse

550 and 680 ppm 550 and 680 ppm 680 ppm

60 ppb

OTC

60 ppb

OTC and FACE OTC

50 and 70 ppb

Total dry weight m (95.5%), RGR m (9.06%), K m (3.5%), Fv/Fm k (3.47%) Plant height m (8.7% 9.3%), number of leaves m (11.6% 13.6%), total biomass m (7% 11%), LAR (ns), LWR m (27.6%), RSR m (18.3% 21.2%), number of grains m (12.8% 19%), weight of grains m (34.8% 37.5%), grain protein (ns), TSS m (9.7% 13.9%), starch m (8.3% 10.2%) Total chl m (4% 5.6%), carotenoids k (5.7% 21.6%), Ps m (8.4% 16.4%), gs k (49.5% 50.6%), Fv/Fm m, H2O2 m (8.1% 8.8%), 2O2 m (6% 14.4%), LPO m (8.6% 27%), solute leakage m (12.4% 13%), ascorbic acid m (2% 13.2%), SOD m (5%), APX m (16% 23%), GR m (44.6% 54%), PAL m (34.3% 39.2%), total phenolics m (11.7% 49.3%), protein (ns) Fv/Fm k (2.4%), Ci k (5.1% 8.3%), Vcmax m, Jmax m, Jmax/Vcmax m, K k (6%), RGRs m Tuber yield m (19% 29.7%), fructose content k, glycoalkaloids (ns) Tuber number k, above ground biomass k, green leaf k, senesced leaf dry weights k Dry weight of above ground biomass (ns), tuber number k, fresh weight of tubers m

Cardoso-Vilhena et al. (2004) Mishra et al. (2013a)

Mishra et al. (2013b)

Biswas et al. (2013) Donnelly et al. (2001) Craigon et al. (2002) Finnan et al. (2002) (Continued)

Table 11.2 (Continued) Plant

Beta vulgaris L.

CO2 dose

O3 dose

Experimental setup

Plant characteristics

Reference

Ambient 1 280 ppm 550 ppm

Ambient 1 20 ppb

OTC

Ambient 1 20 ppb

OTC

Persson et al. (2003) Kumari and Agrawal (2014)

550 ppm

Ambient 1 20 ppb

OTC

550 ppm

Ambient 1 20 ppb

OTC

Haulm dry weight k, haulm/tuber ratio k, average size of tubers k, number of tubers m Plant height m (15.5%), number of leaves m (13.3%), leaf area m (58.3%), total biomass m (10.9% 56.2%), starch content m (60.9%), soluble sugar m (26.6%), total nitrogen k (2.4%), organic carbon m (14.4%), C/N ratio m (17.2%), protein k, amino acid k Ps m (21.1% 47.1%), gs k (37.7%), Fv/Fm m (6.4%), total chl m (19.2%), carotenoids m (31.6%), solute leakage k, protein content k (9.6%), ascorbic acid m (5%), POD k (10.3%), SOD k (10.4%), CAT k (28.7%), GR k (76.7%), APX m (13.7%) Root length k (%), shoot length k (11.4%), total plant biomass m (12.8%), total chl k (18%), MDA m (52.2%), CAT m (53.3%), GR m (44%), POD k (18.7%), ascorbic acid m (56.9%), foliar protein k (25.4%), starch m (17.8%), soluble sugar k (29.4%)

Kumari et al. (2015)

Kumari et al. (2013)

OTC, Open top chamber; FACE, free air CO2 enrichment; m, increase; k, decrease; A, net assimilation rate; Asat, light saturated rate of CO2 assimilation; JPSII, whole chain electron transport through photosystem II; K, allometric root: shoot growth; LAR, leaf area ratio; LWR, leaf weight ratio; RSR, root shoot ratio; TSS, total soluble sugars; Vc,max, maximum in vivo rate of Rubisco carboxylation; Jmax, maximum electron transport rate for RUBP regeneration; RGRs, relative growth rate of shoot; MDA, malondialdehyde; Ps, net photosynthetic rate; gs, stomatal conductance; E, transpiration rate; WUE, water use efficiency; Ci, internal CO2 concentration; F0, initial fluorescence; Fm, maximum fluorescence; Fv, variable fluorescence; Fv/Fm, chlorophyll fluorescence; ANPP, Cumulative above-ground net primary production; chl, chlorophyll; 2O2, superoxide radical; H2O2, hydrogen peroxide content; LPO, lipid peroxidation, MDA, malondialdehyde; SOD, superoxide dismutase activity, POD, peroxidase activity, CAT, catalase activity; APX, ascorbate peroxidase activity; GR, glutathione reductase activity.

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The ameliorative effects provided by CO2 enrichment are mainly due to the exclusion of O3 from the interior of the leaves, which is caused by a decline in the gs of the plants upon CO2 enrichment (Cardoso-Vilhena et al., 2004) (Fig. 11.3). Elevated CO2 has been found to escalate the ability of plants to tolerate O3 toxicity (Rao et al., 1995; Gillespie et al., 2012). The amelioration of O3 induced damage has also been reported by Barnes and Pfirrmann (1992) and Mulchi et al. (1992) under CO2 enrichment. In wheat, elevated CO2 fully protects the detrimental effects of O3 on biomass, but not yield (McKee et al., 1997). Similar results have been observed with soybean (Fiscus et al., 1997), cotton (Heagle, 1989), and tomato (Reinert et al., 1997). On the other hand, Pleijel et al. (2000) noticed that wheat grain yield was negatively affected by O3 at ambient CO2 levels but unaffected by O3 at elevated CO2 levels. According to Bender et al. (1999), the response of wheat to elevated O3 and CO2 appears to be cultivar-dependent, as some cultivars do not respond significantly to elevated O3 levels and for those cultivars, no significant interactions between O3 and CO2 were observed. In potato, although CO2 enrichment did not prevent O3 induced yield losses, the increase in yield in response to high CO2 far exceeded the O3-induced losses (Craigon et al., 2002). Vorne et al. (2002) noticed significant interactions between CO2 and O3 regarding the glucose and reducing sugar content in potato tubers. Although a favorable impact of CO2 enrichment on the growth and yield of C3 cereal crops is observed, reductions in flour quality due to declined N content are likely in a CO2-enriched environment (Fangmeier et al., 1999), thereby counteracting the effect of O3 on flour quality (Vandermeiren et al., 1992; Pleijel et al., 1999). Rudorff et al. (1996) indicated that the maximum benefits for wheat production in response to elevated CO2 will not be accomplished under a simultaneous increase in O3 concentration. This observation suggests that predictive models based simply on the impacts of elevated CO2 will result in an overestimation of the possible effects of atmospheric changes on plant productivity (Barnes and Wellburn, 1998). A study conducted by Long et al. (2005) suggests that chamber studies, which have been the main mechanistic base for crop yield models, overestimate the increase in yield by elevated CO2 compared to what was observed under FACE systems (fully open-air conditions) in the field. Based on chamber experiments, the average yield stimulation for C3 crops with CO2 doubling was estimated at 30%, whilst estimates based on results from field-scale

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experiments under realistic conditions (including varying water availability) were lower. According to a review based on the responses of crop plants in FACE systems (Kimball et al., 2002), CO2 enrichment increases biomass in C3 grasses by an average of 12%, grain yield in wheat and rice (O. sativa L.) by 10% 15%, and tuber yield in potato by 28%. As compared to C3 crops, yield stimulation in C4 crops is much lesser. Morgan et al. (2003) suggested that some environmental differences between chamber and open-air microclimates also have an impact on plant interactions with O3 uptake and detoxification. Morgan et al. (2006) found that in an open-air study, the effects of season-long elevation in O3 induced significantly greater grain losses in soybean as compared to chamber experiments. According to Long et al. (2005), if season-long O3 elevation is representative of other major crops growing areas, then yield losses due to rising O3 will even compensate any gains due to rising CO2. Although leaf-level responses to elevated CO2 and O3 are well reviewed, a few studies have focused on canopy level responses to rising levels of these pollutants. In SoyFACE (Soybean-FACE), the results showed reductions in the evapotranspiration rate of soybean for all three treatments (elevated CO2, elevated O3, and elevated CO2 and O3), with the largest decrease observed for growth in elevated O3 (Bernacchi et al., 2006). When combined over a season, plants grown in elevated CO2 and O3 utilized 10% and 18% less water, respectively. While the direct response of soybean exposed to increases in CO2 and in O3 were similar, the mechanisms for these responses differ. Growth under elevated O3 resulted in reduced leaf area as compared with the control. It was expected that the O3-induced damage to the plant canopy, responsible for the lower biomass and leaf area, resulted in lower evapotranspiration in soybean. On the other hand, soybean grown under elevated CO2 revealed higher leaf area while showing a reduction in evapotranspiration, suggesting that a decrease in gs was sufficient enough to offset an increase in leaf area (Bernacchi et al., 2007). These results show that future changes in the atmosphere may influence soybean response to drought conditions and may have feedback effects on atmospheric moisture, potentially altering regional patterns of precipitation.

11.5 SUMMARY The effects of CO2 enrichment have been described with focus on phenotypical, physiological, biochemical, and molecular responses in relation

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to whole plant growth and development. In general, CO2 enrichment imposes its positive effects on plant growth and productivity. The responses of plant species to CO2 are variable and include photosynthetic acclimation at high levels of CO2. Generally, prolonged treatment with elevated CO2 decreases the primary stimulation of photosynthesis in many plant species and often suppresses photosynthesis. Excess accumulation of carbohydrates in leaf tissues may lead to the downregulation of photosynthetic gene expression and increased starch in order to impede the diffusion of CO2. Thus, plants possessing high sink strength for carbohydrate accumulation do not show a suppression of photosynthesis. Suppression of photosynthesis is always associated with reductions in leaf N and RuBisCO contents under high CO2 conditions. Rising global atmospheric CO2 contents counteract the negative effects of atmospheric pollutants (especially SO2, NOx, and O3) on vegetation. Prospective future research on the direct effects of CO2 and air pollutants on agricultural crop species should include interactions with environmental variables (e.g., rainfall, temperature, soil moisture, availability of nutrients, and vapor pressure deficit) that may be involved with predicted future global climate change. Global climate change poses a threat to agricultural productivity, and therefore, to global food and nutrient security. As CO2 is the key substrate for photosynthesis and plant development, exploring mechanisms of atmospheric CO2 utilization strategies in plants will pave the way to enhancing the productivity of agricultural crops to feed the growing population.

ACKNOWLEDGMENTS Authors are thankful to the Head, Department of Botany, Coordinator CAS, Botany, Institute of Science for necessary research facilities and to DST-Purse, ISLS (DBT), Banaras Hindu University and DST-FIST for providing financial support for the work.

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