Leaf anatomy and photosynthesis : unravelling the CO2 diffusion pathway in C3 leaves

Abstract

Keywords: CO2 diffusion, C3 photosynthesis, mesophyll conductance, mesophyll resistance, re-assimilation, photorespiration, respiration, tomato Herman Nicolaas Cornelis Berghuijs (2016). Leaf anatomy and photosynthesis; unravelling the CO2 diffusion pathway in C3 leaves. PhD thesis. Wageningen University, Wageningen, The Netherlands, with summaries in English and Dutch. 286 pages Optimizing photosynthesis can contribute to improving crop yield, which is necessary to meet the increasing global demand for food, fibre, and bioenergy. One way to optimize photosynthesis in C3 plants is to enhance the efficiency of CO2 transport from the intercellular air space to Rubisco. The drawdown of CO2 between these locations is commonly modelled by Fick's first law of diffusion. This law states that the flux from the air spaces to Rubisco is proportional to the difference in partial pressure between these locations. The proportionality constant is the mesophyll conductance. Its inverse is mesophyll resistance. Mesophyll resistance is a complex trait, which lumps various structural barriers for CO2 transport and processes that add or remove CO2 along the diffusion pathway. In order to better understand how and to what extent these factors affect photosynthesis, it is necessary to find a more mechanistic description of CO2 transport in the mesophyll. The aim of this dissertation is to investigate how leaf anatomical properties and CO2 sources and sinks along the CO2­ diffusion pathway in C3 leaves affect the photosynthetic capacity of these leaves. In this study, Solanum lycopersicum was used as a model organism. In a first approach, we developed a model in which we partitioned mesophyll resistance into two sub-resistances. The model assumed that CO2 produced by respiration and photorespiration was released between the two sub-resistance components. By quantifying these resistances using measured thicknesses, exposed mesophyll and chloroplast surfaces, and assumed diffusive properties, we were able to simulate the effect of various anatomical properties on photosynthesis. A disadvantage of this two-resistance approach is that it assumes either that (photo)respiratory CO2 release takes place in the outer cytosol or that there is no CO2 gradient in the cytosol. Therefore, in a second approach we modelled CO2 transport, production and consumption by use of a reaction-diffusion model. This model is more flexible in terms of determining the location of CO2 sources and sinks. We developed methods to estimate physiological parameters of this model using combined gas exchange and chlorophyll fluorescence measurements on leaves. The results suggest that the rate of respiration depends on the oxygen partial pressure, which is often not considered in previous photosynthesis models. We also presented a method to calculate the fraction of (photo)respiratory CO2 that is re-assimilated. We found that this fraction strongly depends on both environmental factors (CO2, irradiance), the location of mitochondria relative to the chloroplast, stomatal conductance and various physiological parameters. The reaction-diffusion model and associated methods presented in this study provide a more mechanistic framework to describe the CO2 diffusion pathway in C3 leaves. This model could, therefore, contribute to identifying targets to increase mesophyll conductance in future research.