Beyond porosity: 3D leaf intercellular airspace traits that impact mesophyll conductance

Authors: EARLES, J - Yale University; THEROUX-RANCOURT, GUILLAUME - University Of California; RODDY, ADAM - Yale University; GILBERT, MATTHEW - University Of California; McElrone, Andrew; BRODERSEN, CRAIG - Yale University

Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/10/2018
Publication Date: 9/7/2018
Citation: Earles, J.M., Theroux-Rancourt, G., Gilbert, M.E., McElrone, A.J., Brodersen, C. 2018. Beyond porosity: 3D leaf intercellular airspace traits that impact mesophyll conductance. Plant Physiology. 178(1):148-162. https://doi.org/10.1104/pp.18.00550.
DOI: https://doi.org/10.1104/pp.18.00550

Interpretive Summary: The leaf intercellular airspace (IAS) is generally considered to have a relatively high conductance to CO2 diffusion. Yet, previous studies only accounted for leaf-level variation in porosity and mesophyll thickness, omitting inherently 3D IAS traits that potentially influence IAS conductance (gIAS): tortuosity, lateral diffusivity, and IAS connectivity. We theoretically re-evaluate the standard equation for gIAS with respect to tortuosity, lateral diffusivity, and IAS connectivity. Then, measure and spatially map these geometric IAS traits for nineteen CAM versus C3 species using X-ray microCT imaging and a novel computational approach. We find substantial variation in mesophyll thickness, porosity, tortuosity, lateral diffusivity, and IAS connectivity, predicting significantly lower gIAS in CAM versus C3 plants due to a coordinated decline in these traits. Moreover, we observed a high degree of spatial heterogeneity in these IAS geometric traits throughout the mesophyll, especially within CAM leaves. In conclusion, we argue that IAS traits beyond porosity influence gIAS and that the impact of the IAS on mesophyll conductance should be carefully considered with respect to leaf anatomy, including stomatal distribution. Imaging tools such as X-ray microCT and the 3D image processing techniques employed in this study provide a platform for future investigation.

Technical Abstract: The leaf intercellular airspace (IAS) is generally considered to have a relatively high conductance to CO2 diffusion. Yet, previous studies only accounted for leaf-level variation in porosity and mesophyll thickness, omitting inherently 3D IAS traits that potentially influence IAS conductance (gIAS): tortuosity, lateral diffusivity, and IAS connectivity. We theoretically re-evaluate the standard equation for gIAS with respect to tortuosity, lateral diffusivity, and IAS connectivity. Then, measure and spatially map these geometric IAS traits for nineteen CAM versus C3 species using X-ray microCT imaging and a novel computational approach. We find substantial variation in mesophyll thickness, porosity, tortuosity, lateral diffusivity, and IAS connectivity, predicting significantly lower gIAS in CAM versus C3 plants due to a coordinated decline in these traits. Moreover, we observed a high degree of spatial heterogeneity in these IAS geometric traits throughout the mesophyll, especially within CAM leaves. In conclusion, we argue that IAS traits beyond porosity influence gIAS and that the impact of the IAS on mesophyll conductance should be carefully considered with respect to leaf anatomy, including stomatal distribution. Imaging tools such as X-ray microCT and the 3D image processing techniques employed in this study provide a platform for future investigation.