Mesophyll porosity is modulated by the presence of functional stomata

Abstract

The formation of stomata and leaf mesophyll airspace must be coordinated to establish an efficient and robust network that facilitates gas exchange for photosynthesis, however the mechanism by which this coordinated development occurs remains unclear. Here, we combine microCT and gas exchange analyses with measures of stomatal size and patterning in a range of wild, domesticated and transgenic lines of wheat and Arabidopsis to show that mesophyll airspace formation is linked to stomatal function in both monocots and eudicots. Our results support the hypothesis that gas flux via stomatal pores influences the degree and spatial patterning of mesophyll airspace formation, and indicate that this relationship has been selected for during the evolution of modern wheat. We propose that the coordination of stomata and mesophyll airspace pattern underpins water use efficiency in crops, providing a target for future improvement.

The influence of stomatal morphology and distribution on photosynthetic gas exchange

“…This may be explained by a misalignment between the stomata, intercellular airspaces and underlying photosynthetic tissue in the transgenic plants (see asterisk in Figure e), as suggested by Dow et al (). The coordination that exists between the formation of stomata and their substomatal cavities (Lundgren et al , ) may have been disrupted when altering the developmental signalling responsible for enforcing cell spacing. This may impede CO 2 diffusion through the mesophyll, leading to an uneven C i and reduced photosynthetic potential of the leaf.…”

“…Secondly, plants may compensate for reductions in D by altering leaf architecture in a manner that enhances CO 2 diffusion to the chloroplast. Indeed, a level of coordination exists between the stomata and the underlying tissues, which affects both mesophyll cell and intercellular air characteristics (Dow et al, 2017;Lundgren et al, 2019). Finally, if a source of resistance within the CO 2 diffusion pathway is greater than the increased stomatal resistance generated by the reduction in D, then this may place a bottleneck on CO 2 movement to the site of carboxylation, and produce a greater limitation than that imposed by moderate reductions in D. This resistance is perhaps most likely to occur between the intercellular airspace and the chloroplast stroma (i.e.…”

Maximum CO2diffusion inside leaves is limited by the scaling of cell size and genome size

“…As was expected, genome size did not correlate with porosity ( Figure S3) because porosity is quantified as a volumetric fraction, and cell size can vary independently of porosity. Despite the role of porosity in facilitating diffusion in the intercellular airspace 30 , traits other than porosity related to cellular organization within the mesophyll are likely to have a greater influence on the diffusive conductance of CO2 through the intercellular airspace and into the photosynthetic mesophyll cells 27 .…”

“…Within a leaf, the spongy and palisade layers have divergent cell shapes and organizations that are thought to accommodate these opposing gradients by facilitating CO2 diffusion in the gaseous and liquid phases. Both cell size and porosity can affect SAmes/Vmes and the diffusive conductances (gias and gliq) considered targets of selection to increase photosynthesis 20,25,[30][31][32] . To determine whether cell size or porosity has a greater effect on SAmes/Vmes, gias, and gliq, we first quantified cell size, porosity, and SAmes/Vmes for the spongy and palisade layers separately for 47 species in our dataset, encompassing all major lineages of vascular plants.…”

Digitally Deconstructing Leaves in 3D Using X-ray Microcomputed Tomography and Machine Learning

“…Yet only recently has imaging technology enabled a clear view and, more importantly, the capacity to digitally represent leaf 3D anatomy (Théroux-Rancourt et al, 2017). Today, 3D imaging permits precise spatial measurement and biophysical modeling of leaf internal geometry that can deliver novel insights about basic leaf function, such as CO2 transport (Ho et al, 2016;Lehmeier et al, 2017;Earles et al, 2018Earles et al, , 2019Lundgren et al, 2019), H2O transport (Scoffoni et al, 2017), and mechanical structure (Pierantoni et al, 2019). Embracing the 3D complexity of leaf geometry permits us to understand when dimensionality reduction is tolerable and will ultimately guide more precise mechanistic scaling from tissue to crop/ecosystem.…”