Analyzing anatomy over three dimensions unpacks the differences in mesophyll diffusive area between sun and shadeVitis viniferaleaves

Abstract

Leaves grown at different light intensities exhibit considerable differences in physiology, morphology, and anatomy. Because plant leaves develop over three dimensions, analyses of the leaf structure should account for differences in lengths, surfaces, as well as volumes. In this manuscript, we set out to disentangle the mesophyll surface area available for diffusion per leaf area (Sm,LA) into underlying one-, two-, and three-dimensional components. This allowed us to estimate the contribution of each component to Sm,LA, a whole-leaf trait known to link structure and function. We introduce the novel concept of a “stomatal vaporshed,” i.e. the intercellular airspace unit most closely connected to a single stoma, and use it to describe the stomata-to-diffusive-surface pathway. To illustrate our new theoretical framework, we grew two cultivars of Vitis vinifera L. under high and low light, imaged 3D leaf anatomy using microcomputed tomography (microCT), and measured leaf gas exchange. Leaves grown under high light were less porous and thicker. Our analysis showed that these two traits and the lower Sm per mesophyll cell volume (Sm,Vcl) in sun leaves could almost completely explain the difference in Sm,LA. Further, the studied cultivars exhibited different responses in carbon assimilation per photosynthesizing cell volume (AVcl). While Cabernet Sauvignon maintained AVcl constant between sun and shade leaves, it was lower in Blaufränkisch sun leaves. This difference may be related to genotype-specific strategies in building the stomata-to-diffusive-surface pathway.

The effects of genome size on cell size and the functional composition and morphology of leaves: a case study inRhododendron(Ericaceae)

“…Leaf thickness (and, thus, SA leaf /V leaf ), LMA , and W area can be modified independently of cell size to influence photosynthetic capacity, leaf optics, and biomechanics. For example, sun leaves and shade leaves on the same plant that have the same genome size can vary dramatically in leaf thickness, LMA , and W area , resulting in different mesophyll structures for CO 2 diffusion and different photosynthetic rates (Théroux-Rancourt et al . 2023).…”

“…Though normalizing leaf surface conductance by leaf surface area is useful in characterizing the constraints on epidermal construction, area-normalized stomatal conductance does not account for the fact that each stoma must provide CO 2 for an entire leaf volume, i.e. a stomatal vaporshed (Théroux-Rancourt et al 2023). To account for the role of stomata in providing leaf volumes with CO 2 , we scaled maximum surface conductance by leaf volume (g max,vol ).…”

“…In order for CO 2 to enter the mesophyll cells it must cross the leaf surface and diffuse through the intercellular airspace volume inside the mesophyll tissue, both of which are constructed to optimize the supply of CO 2 to sites of photosynthetic metabolism (Théroux-Rancourt et al 2021). Stomata in the leaf epidermis control the surface conductance for net CO 2 transport into the intercellular airspaces of the leaf, and the size and spatial arrangement of cell surfaces that define the intercellular airspace volume supplied by stomata determine the total surface area available for CO 2 uptake (Trueba et al 2022;Théroux-Rancourt et al 2023). This suggests that scaling from cell-and tissue-level traits to whole-leaf traits should account for variation in the total surface area available for CO 2 uptake per unit leaf volume (Earles et al 2018;Théroux-Rancourt et al 2021;Borsuk et al 2022).…”

“…Stomata in the leaf epidermis control the surface conductance for net CO 2 transport into the intercellular airspaces of the leaf, and the size and spatial arrangement of cell surfaces that define the intercellular airspace volume supplied by stomata determine the total surface area available for CO 2 uptake (Trueba et al . 2022; Théroux-Rancourt et al . 2023).…”

Systemic stomatal responses in plants: Coordinating development, stress, and pathogen defense under a changing climate

“…As stomata are nested within a 'monolayer' of epidermal cells, they share their apoplastic space with all other cells in this layer, as well as have cell wall-to-cell wall contacts with their neighbouring epidermal cells (but have no PD connections to them, Cui et al, 2023;Harwood, 2023;Théroux-Rancourt et al, 2023). They can therefore initiate different systemic signals that propagate within the epidermal layer and from that layer to other cell types, layers and tissues, including the vascular bundles (Figure 5).…”