Elevated-CO2 Response of Stomata and Its Dependence on Environmental Factors

Abstract

Stomata control the flow of gases between plants and the atmosphere. This review is centered on stomatal responses to elevated CO2 concentration and considers other key environmental factors and underlying mechanisms at multiple levels. First, an outline of general responses in stomatal conductance under elevated CO2 is presented. Second, stomatal density response, its development, and the trade-off with leaf growth under elevated CO2 conditions are depicted. Third, the molecular mechanism regulating guard cell movement at elevated CO2 is suggested. Finally, the interactive effects of elevated CO2 with other factors critical to stomatal behavior are reviewed. It may be useful to better understand how stomata respond to elevated CO2 levels while considering other key environmental factors and mechanisms, including molecular mechanism, biochemical processes, and ecophysiological regulation. This understanding may provide profound new insights into how plants cope with climate change.

Keywords: drought; elevated CO2; global warming; guard cell; mesophyll-driven signals; photosynthesis; regulation mechanism; stomatal behavior.

FIGURE 1

A representation of the response to elevated CO₂ (eCO₂) with abiotic factor stress on stomatal density (SD) under regulation by leaf growth. Elevated CO₂ may lead to an acclimated reduction in SD by inhibition of guard cells, which involves the regulation of gene expression and adaptive evolution (1); meanwhile, eCO₂ could promote leaf enlargement (2) consequently decreasing SD (3). A severe abiotic stress factor such as drought may diminish leaf enlargement (4), ultimately increasing SD (5); it may directly decrease SD due to inhibition of guard cell development (6). However, under moderate stress, SD may be increased possibly due to an acclimated response (7). In summary, this synergic increase (8) or trade-off interaction (9) may occur between the effects of both leaf growth and changes in SD toward the variations in eCO₂ under abiotic stress, ultimately determining SD.

FIGURE 2

Possible stomatal response mechanisms controlling guard cells (GC) under elevated CO₂. With rising CO₂, a depolarization in GCs appears: the levels of K⁺, Ca²⁺, Cl^-, and zeaxanthin (Zea) may decrease (1), whereas the H⁺ concentration may remain at a high level (2) leading to a lower pH value. The pH gradient (3), protein phosphorylation (4), and photosynthesis-derived ATP (5, 6) are involved in the regulation process by modifying channel activities; together, they promote osmotic regulation (7) and decrease GC turgor (8) consequently causing the GCs to drain water (9) leading to stomatal closure to some extent (10). Meanwhile, Calvin–Benson–Basshan (CBB) cycle and sugar metabolism in GC may produce less malate (Mal^2-), (11) and sucrose (Suc) (12) with triose phosphate (triose-P) at eCO₂, which also affects osmotic regulation. Furthermore, elevated CO₂ may reduce Suc accumulation in the vicinity of the GC wall from the mesophyll due to the limitation of some apoplastic Suc in the transpiration stream toward GC (13) and enhance Mal^2- transport from GCs into mesophyll cells by stimulating anion efflux through channels such as GCAG1 and the potential involvement of the AtABCB14 gene (14), also resulting in stomatal closure. Finally, hexokinase (HXK) involvement may limit sugar synthesis and its entrance into GCs from mesophyll cells (15) and then inducing stomatal closure (e.g., Webb et al., 1996; Assmann, 1999; Schroeder et al., 2001; Kang et al., 2007; Lee et al., 2008; Kim et al., 2010; Fujita et al., 2013; Kelly et al., 2013; Lawson et al., 2014; Negi et al., 2014).

FIGURE 3

A representation of the response to elevated CO₂ (eCO₂) with drought on water use efficiency (WUE) under regulations by balancing stomatal conductance (g_s) and leaf growth. Elevated CO₂ may lead to an acclimated reduction in g_s, 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); g_s 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 g_s changes at eCO₂ under drought, ultimately affecting WUE.