Elevated atmospheric carbon dioxide concentration (elevated CO2) is a major component of climate change. It has increased from the pre-industrial level of 280 μmol mol-1 in 1750 to c. 400 μmol mol-1 at present and is expected to increase to c. 900 μmol mol-1 by the end of the 21st century. The global surface temperature is projected to rise 2.6–4.8°C by the end of this century, according to RCP8.5 (IPCC, 2013), a more undisciplined management scenario. Climate change, including elevated CO2, rising temperatures, and altered precipitation patterns, have markedly affected terrestrial ecosystem structure and function, carbon and water balance, and crop productivity (Lobell et al., 2011; Peñuelas et al., 2013; Ruiz-Vera et al., 2013; Bagley et al., 2015; Lavania et al., 2015). Moreover, a profound interaction between climate change and other critical environmental factors, including limited nutrition and air pollution, as well as some biotic factors, such as herbivorous insects, may intensify the adverse impacts (Gillespie et al., 2012; Peñuelas et al., 2013; Xu et al., 2013; Zavala et al., 2013; Sun et al., 2015; Xu et al., 2016). Many studies have reported the biological responses to CO2 enrichment and their interaction with environmental change at various levels (Ainsworth and Rogers, 2007; Medeiros et al., 2015; Xu et al., 2015; Rodrigues et al., 2016). Elevated CO2 generally can enhance CO2 fixation and consequently plant growth and production (Ainsworth and Rogers, 2007; Xu et al., 2013). On the other hand, the decrease in stomatal conductance (gs) under elevated CO2 conditions may limit the CO2 fixation rate but promote water use efficiency (WUE) to benefit plant growth, especially within a climate change context where water shortage periods are expected to increase (Leakey et al., 2009; Sreeharsha et al., 2015). Of these responses, the stomata are pivotal doors that control the gas exchange between vegetation and the atmosphere, i.e., CO2 entering from the atmosphere and water vapor releasing from plants into the atmosphere (Woodward, 1987). Carbon dioxide can reach the fixed Rubisco site through CO2 gas diffusions from the boundary layer, stomata, and intercellular airspaces near the chloroplast (Ball et al., 1987; Woodward, 1987; Warren, 2008). The main factors controlling stomatal opening processes include Ca2+ level, guard cell turgor, and hormones (Assmann, 1999; Lawson et al., 2014). Stomatal behavior may be affected by environmental factors, such as water status (e.g., soil water deficit, vapor pressure deficit [VPD]), temperature, CO2 concentrations, and light either alone and/or in combination (e.g., Lee et al., 2008; Perez-Martin et al., 2009; Hubbart et al., 2013; Laanemets et al., 2013; Šigut et al., 2015). Furthermore, stomatal short-term behavior (e.g., stomatal closure) and a long-term developmental (e.g., stomatal size and its density) responses to environmental changes might occur together, depending on species and genotypes (Gray et al., 2000; Ainsworth and Rogers, 2007; Haworth et al., 2013; DaMatta et al., 2016). Our review focuses on the stomatal responses to elevated CO2 conditions with climatic change as well as the relevant metabolic processes and underlying mechanisms. The future perspectives for this study and possible implications are briefly presented and discussed. The present report may advance our current knowledge of the stomatal response to climatic change. It may also provide a new vision of its interdisciplinary and systematic synthesis to promote further relevant research. Soil water deficit and high VPD often reduce the stomatal opening, depending on the species (Warren, 2008; Perez-Martin et al., 2009; Peak and Mott, 2011). Generally, water status has a stronger impact on gs than changes in CO2 concentration. A relatively small effect of elevated CO2 on gs generally appears as water deficit stress occurs, possibly because the drought-induced reduction dramatically outweighs the reduction caused by elevated CO2 (Morgan et al., 2004; Leakey et al., 2006b). Flexas et al. (2004) indicated that decreases in gs and gm, but not biochemical activities, may limit the photosynthetic capacity in drought-stressed leaves, depending on the species (Bota et al., 2004; Flexas et al., 2014). Even for drought-severely stressed plants, the biochemical limitation can be negligible (Galmés et al., 2007). A non-stomatal limitation appears only when gs is below 250 mmol m-2s-1 in grass plants grown in drought conditions (Xu et al., 2009a). In tall fescue (Festuca arundinacea) plants exposed to elevated CO2, an increased A with a low gs but high Rubisco activity during both drought and rewatering may also indicate the alleviation of metabolic limitations caused by drought damages rather than stomatal limitations imposed by elevated CO2 (Chen et al., 2015). CO2 enrichment may relieve non-stomatal limitations by protecting the photosynthetic apparatus during severe drought (Xu et al., 2014). However, a recent report showed that Ramonda nathaliae plants with smaller stomata have higher resistance to drought than R. serbica, which have larger stomata (Rakić et al., 2015). This highlights the role of the stomatal size. Elevated CO2 may improve plant water status by reducing gs and thereby raising WUE, ameliorating the adverse effects of stressful factors on plant growth and physiological processes (Ainsworth and Rogers, 2007; Xu et al., 2013, 2014). A decrease in soil water availability under elevated CO2 may be closely linked to an increase in leaf area, which offsets a decline in gs and promotes plant growth (Manea and Leishman, 2015). Studies have clearly shown that water status mediates rising CO2 effectiveness through the coupling of processes between gas exchange and leaf enlargement. Nevertheless, the pros and cons of acclimation to changes in water conditions may coexist in response to elevated CO2. Leaf area enlargement, i.e., canopy enhancement induced by CO2, may exaggerate water use, whereas decreased gs would promote WUE (e.g., Woodward, 1990; Ward et al., 2013; Manea and Leishman, 2015), depending on canopy density and its homogeneity (Bernacchi and VanLoocke, 2015). However, an intrinsic WUE decline might appear during severe drought in some relict species plants exposed to elevated CO2 (Linares et al., 2009). Thus, future research is necessary to focus on the linkage among leaf area, gs, and both WUEi and total plant biomass water use efficiency (WUEt) under climatic change. Furthermore, some results indicated that although WUEt and WUEi showed a similar response to elevated CO2, the former seemed to have a higher level of sensitivity, implying that WUEt may be a better indicator than WUEi of the response to climate change (Duan et al., 2014). WUE and the root: shoot biomass ratio increased significantly with decreased precipitation but decreased with elevated CO2 levels (Li et al., 2014). Thus, besides the regulation of leaf growth, root development may also involve stomatal movement behavior and WUE changes under climatic change. The possible primary stomatal closure induced by elevated CO2 may be offset by positive indirect effects on gs, possibly caused by root system promotion and hydraulic capacity under rising CO2 conditions (Uddling et al., 2009). Forest canopy evapotranspiration can be reduced under high CO2 concentration levels (Medlyn et al., 2001), possibly due to leaf gs slowdown. Thus, water loss is diminished. However, a lower response to elevated CO2 in the canopy evapotranspiration rate relative to leaf gs was found in a rice field (Shimono et al., 2013). Nevertheless, the canopy carbon fixation and its association with gs at the leaf and canopy scales during climatic change remains to be tested. A succinct description on the trade-off between gs, leaf enlargement, and WUE under elevated CO2 and drought conditions is summarized in Figure 3.  A representation of the response to elevated CO2 (eCO2) with drought on water use efficiency (WUE) under regulations by balancing stomatal conductance (gs) and leaf growth. Elevated CO2 may lead to an acclimated reduction in gs, which involves signaling sensing and transduction, biophysical and biochemical processes, and gene expression (1); meanwhile, eCO2 could promote leaf enlargement (2), possibly increasing transpiration (E) of the total leaf subsequently reducing WUE (3). A severe drought stress may shrink leaf growth (4), consequently decreasing E and finally increasing WUE (5); gs can directly be reduced by drought (6). However, a moderate drought may directly enhance WUE by some adaptive responses such as a relative increase in the root systems (7), which can be further improved by elevated CO2 (8). Root systems may be enhanced by eCO2, particularly under drought through alterations in carbon allocation between above- and belowground parts (9), which may lead to either decreased WUE at eCO2 (10), or increased WUE under drought conditions (11). Consequently, this trade-off interaction (12) or synergic increase (13) may occur with leaf growth and gs changes at eCO2 under drought, ultimately affecting WUE. Moreover, most studies have confirmed that elevated CO2 may improve the water status of drought-stressed plants by reducing gs (e.g., Brodribb et al., 2009; Katul et al., 2010; Chen et al., 2015; Easlon et al., 2015), but these findings were species-dependent (Beerling et al., 1996; Bernacchi et al., 2007; Liu et al., 2016). However, this case may not occur under severe or extreme drought conditions, possibly due to the depression of stomatal regulatory ability (Xu and Zhou, 2008). Furthermore, plant size and root distribution may override the expected direct physiological effects of elevated CO2 (Duursma et al., 2011; Liu et al., 2016). Generally, stomata may exert a similar response to salt stress relative to drought (Clough and Sim, 1989; Wang et al., 2003; Flexas et al., 2004; Chaves et al., 2009). Stomatal conductance often decreases remarkably with increased salinity and/or aridity, such as leaf to air VPD, depending on the species and its habits (e.g., Clough and Sim, 1989; Chaves et al., 2009; Ashraf and Harris, 2013; Nguyen et al., 2015; Sanoubar et al., 2016). Enhanced salt stress and elevated CO2 concentrations are projected to co-occur in the future (Chaves et al., 2009; Pérez-López et al., 2009; Hoque et al., 2016). Generally, stomatal conductance was decreased by severe salt stress and elevated CO2 alone or in combination (Pérez-López et al., 2012; Nguyen et al., 2015; Stavridou et al., 2016). For example, as barley (Hordeum vulgare) plants are grown in high salinity soil, the rate of CO2 diffusion to the carboxylating site and photochemical electron sink capacity increased under elevated CO2 conditions, despite stomatal and internal conductance being decreased (Pérez-López et al., 2012). Similar to the severe desiccation effect, high salinity stress may lead to oxidative damage in plant tissue (Shalata et al., 2001; Sanoubar et al., 2016). However, elevated CO2 may alleviate the oxidative stress-induced by salinity with lower ROS level and a higher A, thus improving plant growth under high salinity conditions (Nicolas et al., 1993; Pérez-López et al., 2009). Studies have indicated that the rising-CO2 protection from salt-inhibited plants alleviates the metabolic limitations rather than the stomatal limitations. Moreover, although there was a gs decrease of 1–2 factors by high soil salinity in wetland grass Phragmites australis plants, the salinity effect hardly occurred with the combination of elevated CO2 and temperature (plus 310 μmolmol-1 CO2, and plus 5°C relative to ambient variables; Eller et al., 2014). The non-species expansion into saline areas may be promoted because the salinity-caused non-stomatal limitations (i.e., carboxylation rates of Rubisco or electron transport rates) may be mitigated under the elevated climatic conditions (Eller et al., 2014). However, the alleviated effect of elevated CO2 on severe salt stress strongly depends on species and cultivars/ecotypes (Eller et al., 2014; Geissler et al., 2015). Nevertheless, the responses of stomatal characteristics to the combination of elevated CO2 on salt stress are scarcely reported and need to be explored further. The combined effects of elevated CO2 and high temperatures have also been reported in some studies. While there are exceptional cases (e.g., Bernacchi et al., 2007), elevated CO2 decreases gs, thus increasing leaf temperature because lower transpiration releases less heat (Kim et al., 2006; Negi et al., 2014; Šigut et al., 2015). As a consequence, elevated CO2 with high temperatures may play an antagonistic role by exaggerating heat damage partly due to decreased gs (Warren et al., 2011). However, an elevated CO2-induced 13–30% decline in gs induced a 2°C increase in leaf temperature, leading to a 2.9–6.0°C increase in the temperature optima for the light-saturated rate of CO2 assimilation (Amax). Thus, this would enhance heat stress tolerance in beech and spruce saplings (Šigut et al., 2015). The increased adaptation to heat stress may be due to reduced photorespiration and the limitation of photosynthesis by RuBP regeneration under elevated CO2 (Šigut et al., 2015). A recent report also confirmed the heat-tolerance enhancement due to elevated CO2 for coffee crops (Rodrigues et al., 2016). Thus, the negative effect of elevated CO2 on heat stress due to reduced gs was not confirmed. In contrast, a beneficial adaptation may occur. Yet, this may depend on the species and the range of temperature variation. Based on a recent report (Easlon et al., 2015), better plant growth and photosynthesis in the low gs in A. thaliana lines under N-limitation, rather than sufficient N supply under elevated CO2, may imply an adaptive coupling between lowered gs and improved N utilization. Increased conservative N investment in photosynthetic biochemistry in order to acclimate to CO2 fertilization highlights a positively synergistic relationship between stomatal regulation and nutrition status. However, a lower gs in elevated CO2 concentrations but a higher gs with an abundant N supply have been found in Liquidambar styraciflua plants (Ward et al., 2013), suggesting that these factors may play opposite roles in the gs response. A recent study has indicated that improved phosphorus (P) nutrition can enhance drought tolerance in the field pea due to the CO2-induced decrease in gs and the promotion of root systems (Jin et al., 2015). A general decline in gs by elevated CO2 and ozone (O3) alone or their combination has been extensively reported, suggesting that rising CO2 may alleviate the injury caused by high O3 pollution decreasing gs (Kellomäki and Wang, 1997; Mansfield, 1998; Warren et al., 2006; Hoshika et al., 2015). However, some species, such as aspen (Populus tremuloides Michx.) and birch (Betula papyrifera Marsh.), have a high gs under both high CO2 and high O3 concentrations (Uddling et al., 2009). This indicates that the interactive effects between elevated CO2 and O3 on stomatal behavior may depend on species, plant/leaf ages, and treatment regimens, such as time and sites (Uddling et al., 2009; Hoshika et al., 2015; Matyssek et al., 2015). Thus, it again highlights the complex/specific response. The stomatal response to elevated CO2 with biotic factors has received much attention (e.g., Casteel et al., 2012; Zavala et al., 2013). For instance, a greater gs reduction in cabbage with decreased aphid (one of the most destructive insect pests in crops) colonization rates and total plant volatile emissions, such as terpene emissions, occurred when plants were exposed to elevated CO2 over the long-term (6–10 weeks) rather than the short-term (2 weeks; Klaiber et al., 2013). This indicates that, as hosts, plants may acclimatize to future increases in elevated CO2 by modifying stomatal behavior. Under elevated CO2, a decrease in micronutrients, such as calcium, magnesium, or phosphorus, due to the gs reduction may lead to poor aphid performance (Myzus persicae; Dáder et al., 2016). Furthermore, a recent report (Sun et al., 2015) showed that aphid infestation may synergistically promote the effects of elevated CO2 on stomatal closure, possibly by triggering the ABA signaling pathway. Therefore, the water status of the host plants of Medicago truncatula was improved, ultimately enhancing feeding efficiency and abundance of aphid (Zavala et al., 2013; Sun et al., 2015). Taken together, plant–insect interactions might be modified by stomatal closure under high levels of CO2. The metabolism and emission of plant biogenic volatile organic compounds may also be involved (Klaiber et al., 2013; Zavala et al., 2013). It is suggested that an enhanced accumulation of JA and SA may also be involved in signal transduction in relation to stomatal movement as plants are subjected to CO2 enrichment and herbivore attack. This highlights an important role in stomatal regulation to cope with a combination of climate change and biotic factors (Poór et al., 2011; Casteel et al., 2012; Zavala et al., 2013; Sun et al., 2015). Thus, the herbivore’s adaptive capacity to its host might be promoted when exposed to elevated CO2, at least partly through stomatal regulation. Under high CO2 conditions, both stomatal conductance and its density generally decreased with a few exceptions. The decline in SD may be the result of a long-term genetic variation or short-term structural plasticity under elevated CO2. Elevated CO2 may induce the excessive depolarization of guard cells to cause stomatal closure when mesophyll-driven signals, such as malate, ATP, zeaxanthin, and NADPH, may be involved in stomatal movement. Their photosynthesis in both guard cells and mesophyll cells and their link to the stomatal response in elevated CO2 conditions may play an important role. However, challenges remain in elucidating the underlying mechanism. The differences and linkage in stomatal responses to elevated CO2 levels across the molecular, cellular, biochemical, eco-physiological, canopy, and vegetation levels (Zhu et al., 2012; Peñuelas et al., 2013; Shimono et al., 2013; Armstrong et al., 2016) should raise concerns about ecological and climatic management. Several crucial aspects of research into the stomatal response may need to be strengthened in the future. (1) The underlying mechanism of responses to CO2 enrichment for key biological processes, including stomatal behavior; the critical metabolic bioprocesses, such as hormone-involved regulation; and relevant biochemical signal cascades must be further elucidated. (2) The diverse responses from different species and PFTs to elevated CO2 or its combination with other abiotic and biotic factors must be compared and clarified. (3) Various spatial–temporal scales from the molecular, biochemical, physiological, individual, and canopy to vegetation levels must be integrated. Instantaneous to annual or longer time-scales (e.g., Zhu et al., 2012; Shimono et al., 2013; Armstrong et al., 2016) must also be integrated. We should elucidate the underlying mechanism of the stomatal responses associated with key biological processes across the multiple scales under different climatic factors, including elevated CO2, warming, drought, and air pollution. (4) We need to investigate whether improving stomatal response to elevated CO2 by manipulating guard cell performance may yield a better balance between CO2 uptake and water loss through transpiration to enhance photosynthetic capacity with high WUE (e.g., Engineer et al., 2014; Lawson and Blatt, 2014; Grienenberger and Fletcher, 2015). Enhanced expression of some related genes, such as patrol1, may drastically increase both gs and plant growth under higher CO2 levels (Hashimoto-Sugimoto et al., 2013). This task needs to be implemented urgently. Finally, understanding how to improve or combine earth system models (ESMs), general circulation models (GCMs), and land surface models (LSMs) may help to correctly interpret the gs response to climate change (Sato et al., 2015). The integration issue should be solved urgently to precisely assess the response and feedback of terrestrial ecosystem to global change.
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Which of the following best explains how the leaves from the same plant can have different stomatal densities when exposed to an elevated carbon dioxide level?
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