Dessication of the leaf mesophyll and its implications for C02 diffusion and light processing

Authors: MOMAYYEZI, MINA - University Of California, Davis; BORSUK, ALECA - Yale University; BRODERSEN, CRAIG - Yale University; GILBERT, MATTHEW - University Of California, Davis; THEROUX-RANCOURT, GUILLAUME - University Of Natural Resources & Applied Life Sciences - Austria; Kluepfel, Daniel; McElrone, Andrew

Submitted to: Plant, Cell & Environment
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/24/2022
Publication Date: 2/10/2022
Citation: Momayyezi, M., Borsuk, A., Brodersen, C., Gilbert, M., Theroux-Rancourt, G., Kluepfel, D.A., McElrone, A.J. 2022. Dessication of the leaf mesophyll and its implications for C02 diffusion and light processing. Plant, Cell & Environment. 45(5):1362-1381. https://doi.org/10.1111/pce.14287.
DOI: https://doi.org/10.1111/pce.14287

Interpretive Summary:

Technical Abstract: Leaves must effectively absorb both CO2 and light to maximize photosynthetic efficiency. Fixation of the CO2 molecules that diffuse to carboxylation sites is highly dependent on the efficiency of the light absorption in mesophyll cells through the leaf profile. In this study, we evaluated how dehydration impacts these processes through changes in leaf structure and function in two walnut species, Juglans regia and J. microcarpa, with varying leaf anatomy. We investigated optical properties through leaf profiles and anatomical and biophysical traits associated with changes in gas exchange and mesophyll conductance (gm). Chlorophyll distribution determined from fluorescence under epi-illumination of leaf cross sections was different between the species with J. microcarpa exhibiting higher relative fluorescence in lower mesophyll. X-ray microcomputed tomography (micro CT) imaging showed that mesophyll surface area per mesophyll volume (Ames/Vmes) was higher in J. microcarpa. Porosity, tortuosity and intercellular air space conductance (gIAS) were the same between species under well-watered conditions despite net photosynthesis (An), stomatal conductance (gs) and gm being lower in J. microcarpa. Water stress-induced, species-specific changes in the location and magnitude of absorption peaks across the leaf profile were associated with changes in cell geometry; J. microcarpa exhibited decreased tortuosity, increased porosity and gIAS coincident with changes in light absorption patterns under epi-illumination and a generally lower relative fluorescence response from adaxial surface in all wavelengths. Interestingly, the reduction in An at ambient CO2 under dehydration was reversible at saturating CO2 in J. microcarpa suggesting that water-stress induced limitations are due to CO2 diffusivity. Parameters derived from plastic structural traits showed a significant negative relationship with changes in An, gm and Kleaf under dehydration demonstrating the interdependence of the carbon capture and water transport systems, but responses were stronger in one species. J. regia with an aggregated IAS, packed cells near adaxial epidermis in upper mesophyll and higher lateral path lengthening has a higher photosynthetic rate at ambient CO2 under well-watered and dehydrated conditions. Less flexibility and changes in structural traits under dehydration in J. regia matches with no consistent changes in light absorption profiles under epi- and single wavelengths illumination. In contrast, J. microcarpa with a compartmented mesophyll, more distributed IAS between cells over mesophyll volume and lower lateral path lengthening shows a more plastic anatomy that overcomes limitation of CO2 diffusivity at saturating CO2.