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

Abstract

Maintaining high rates of photosynthesis in leaves requires efficient movement of CO 2 from the atmosphere to the mesophyll cells inside the leaf where CO 2 is converted into sugar. CO 2 diffusion inside the leaf depends directly on the structure of the mesophyll cells and their surrounding airspace, which have been difficult to characterize because of their inherently three-dimensional organization. Yet faster CO 2 diffusion inside the leaf was probably critical in elevating rates of photosynthesis that occurred among angiosperm lineages. Here we characterize the three-dimensional surface area of the leaf mesophyll across vascular plants. We show that genome size determines the sizes and packing densities of cells in all leaf tissues and that smaller cells enable more mesophyll surface area to be packed into the leaf volume, facilitating higher CO 2 diffusion. Measurements and modelling revealed that the spongy mesophyll layer better facilitates gaseous phase diffusion while the palisade mesophyll layer better facilitates liquid-phase diffusion. Our results demonstrate that genome downsizing among the angiosperms was critical to restructuring the entire pathway of CO 2 diffusion into and through the leaf, maintaining high rates of CO 2 supply to the leaf mesophyll despite declining atmospheric CO 2 levels during the Cretaceous.

Understanding airspace in leaves: 3D anatomy and directional tortuosity

“…We present this example because Buckley (2015) developed a model to estimate horizontal and vertical water transport in both the spongy and palisade regions, and the model would benefit from having the random walk observations incorporated. Our data show that vertical movement is less tortuous than horizontal movement in both the palisade and spongy mesophyll and overall the palisade mesophyll is more tortuous than the spongy mesophyll, result that parallel modelled g ias and g liq for both spongy and palisade mesophyll across the plant phylogeny (Théroux-Rancourt et al, 2021). Our understanding of water transport could also be enhanced by combining S mc , S m and directional tortuosity.…”

“…At the time Roderick et al (1999) lamented that there was 'currently no simple means to measure the volume of solution or structure within a leaf', a situation that has been remedied in the intervening time including by this paper. Considering leaf construction economics begins to explain why leaves appear not to have 'perfect' anatomical arrangements that optimize CO 2 and H 2 O exchange and will be an important factor when interpreting 3D leaf anatomy data (Deans, Brodribb, Busch, & Farquhar, 2020;Lundgren & Fleming, 2020;Théroux-Rancourt et al, 2021).…”

The Optical Properties of Leaf Structural Elements and Their Contribution to Photosynthetic Performance and Photoprotection

“…CaOx crystals contained in vascular bundle sheaths and other tissues such as sclerenchyma, collenchyma, or parenchyma, could also scatter light comprising a key component in the homogenization of the light gradient profile along the depth within the mesophyll [ 103 ] (see also Section 3.3 and Section 3.4 , below). Microscopic observations confirmed that the spatial distribution of the CaCIs is compatible with their proposed optical function [ 94 ]. Moreover, CaOx crystals within the epidermis of Lithops aucampiae leaves may scatter light within the below-ground region of the leaves, thus enriching the lower tissues with photons [ 59 ].…”

“…The spongy cells are irregularly shaped, forming large intercellular air spaces that result in a greater effective light path lengthening and, subsequently, increased light absorption through multiple light scattering as the photons encounter numerous air–cell wall interfaces [ 90 , 91 , 92 , 93 ]. This anatomy also allows for the effective diffusion of CO 2 from the stomata, usually located at the abaxial epidermis in bifacial leaves, to the upper palisade layer where the larger proportion of photosynthesis takes place [ 94 ].…”

The three‐dimensional construction of leaves is coordinated with water use efficiency in conifers

“…Previous work has shown that mesophyll surface area per leaf area (S m ; µm 2 µm À2 ) has a strong influence on maximum photosynthesis (Nobel et al, 1975;Smith & Nobel, 1977). More recently, it has been suggested that the surface area of the mesophyll exposed to the IAS per unit of mesophyll volume (SA mes /V mes ; µm 2 µm À3 ) can influence plant photosynthetic performance given that the mesophyll-IAS boundary is the primary interface between the atmosphere and the photosynthetic cells (Earles et al, 2018;Th eroux-Rancourt et al, 2021). Other volumetric anatomical traits such as mesophyll porosity (i.e.…”