The influence of stomatal morphology and distribution on photosynthetic gas exchange

Abstract

The intricate and interconnecting reactions of C₃ photosynthesis are often limited by one of two fundamental processes: the conversion of solar energy into chemical energy, or the diffusion of CO₂ from the atmosphere through the stomata, and ultimately into the chloroplast. In this review, we explore how the contributions of stomatal morphology and distribution can affect photosynthesis, through changes in gaseous exchange. The factors driving this relationship are considered, and recent results from studies investigating the effects of stomatal shape, size, density and patterning on photosynthesis are discussed. We suggest that the interplay between stomatal gaseous exchange and photosynthesis is complex, and that a disconnect often exists between the rates of CO₂ diffusion and photosynthetic carbon fixation. The mechanisms that allow for substantial reductions in maximum stomatal conductance without affecting photosynthesis are highly dependent on environmental factors, such as light intensity, and could be exploited to improve crop performance.

Keywords: Arabidopsis thaliana; carbon dioxide; development; diffusion; distribution; gaseous exchange; morphology; photosynthesis; stomata.

Figure 1

The pathway of diffusive resistance for CO₂ entry and H₂O exit in a C₃ leaf. (a) Diagram of a leaf cross‐section illustrating the route of gaseous exchange. CO₂ diffuses into the leaf along a concentration gradient from the atmosphere (C _a) into the intercellular airspaces of the leaf (C _i), before finally reaching the chloroplast (C _c). In contrast, water vapour diffuses out of the leaf along a concentration gradient from the intercellular airspaces (W _i) to the atmosphere (W _a). (b) The CO₂ diffusion pathway comprises a series of resistances, indicated between (b) and (a) via dashed lines. To summarise, CO₂ diffuses from the atmosphere through a boundary layer of air surrounding the leaf and enters the substomatal cavity via the stomatal pore, encountering boundary layer and stomatal resistance, respectively. CO₂ must then diffuse through the intercellular airspaces and into the mesophyll cell, encountering gas‐phase resistance, followed by mesophyll cell wall, plasma membrane and cytosol resistances. Finally, CO₂ diffuses into the chloroplast, encountering chloroplast envelope and stroma resistances, before reaching RuBisCO, where it is used as a substrate in the Calvin–Benson cycle. The size of the boxes represent the assumed magnitude of resistance. (c) The inverse of these resistances are termed conductances, with the corresponding pair shown in the same colour. Boundary layer conductance (g _bl) is shown in orange, stomatal conductance (g _s) is shown in purple and mesophyll conductance (g _m) is shown in green (which corresponds to the collective resistances that exist between gas‐phase and chloroplast). (d) Similarly, the water vapour diffusion pathway encounters a series of resistances. Water vapour diffuses from the intercellular airspaces and out into the atmosphere, encountering stomatal and boundary layer resistances along the way. Again, the corresponding resistances are linked between (c) and (a) via dashed lines.

Figure 2

The generalised interactions between light intensity, theoretical stomatal conductance and gas exchange, in plants with altered stomatal density and patterning. Stylised cross sections of plants with (a) low stomatal density and (b) high stomatal density. Increasing stomatal density (D) leads to a corresponding increase in the theoretical maximum stomatal conductance (g _smax). Assuming no compensatory mechanisms, the interactions between theoretical g _smax, light intensity and gas exchange have been generalised as follows. (c) Increasing D and theoretical g _smax corresponds to an increase in stomatal conductance (g _s) and the rate of CO₂ diffusion to the chloroplast. The size and strength of this relationship is stronger under saturating light (blue line) compared with low light (red dashed line). (d) Under saturating light, increasing D and theoretical g _smax, and thus g _s and CO₂ diffusion, leads to an increase in carbon assimilation (A). However, under low light conditions, this benefit is only realised when carbon availability is limiting A. Once light becomes the limiting factor, as denoted by the greyed area, any increase to D and theoretical g _smax no longer increases A. The point at which A changes from being carbon limited to light limited is denoted by the arrow; however, this is dependent on species and environmental conditions. (e) An increase in D is often accompanied by an increase in stomatal clustering, as depicted in the stylised cross section. When stomata are present in clusters, the relationship between theoretical g _smax and gas exchange parameters, seen in (c) and (d), is weakened or broken. Whilst maintaining a high D, and thus high theoretical g _smax, increasing stomatal clustering results in a decrease in (f) g _s and CO₂ diffusion and (g) A, under saturating light. This may be explained by factors including altered diffusion kinetics and/or the incorrect alignment of stomata over mesophyll cells rather than substomatal cavities, as shown by the asterisk in (e).