Computational Analysis of Alternative Photosynthetic Electron Flows Linked With Oxidative Stress

Abstract

During photosynthesis, organisms respond to their energy demand and ensure the supply of energy and redox equivalents that sustain metabolism. Hence, the photosynthetic apparatus can, and in fact should, be treated as an integrated supply-demand system. Any imbalance in the energy produced and consumed can lead to adverse reactions, such as the production of reactive oxygen species (ROS). Reaction centres of both photosystems are known sites of ROS production. Here, we investigate in particular the central role of Photosystem I (PSI) in this tightly regulated system. Using a computational approach we have expanded a previously published mechanistic model of C3 photosynthesis by including ROS producing and scavenging reactions around PSI. These include two water to water reactions mediated by Plastid terminal oxidase (PTOX) and Mehler and the ascorbate-glutathione (ASC-GSH) cycle, as a main non-enzymatic antioxidant. We have used this model to predict flux distributions through alternative electron pathways under various environmental stress conditions by systematically varying light intensity and enzymatic activity of key reactions. In particular, we studied the link between ROS formation and activation of pathways around PSI as potential scavenging mechanisms. This work shines light on the role of alternative electron pathways in photosynthetic acclimation and investigates the effect of environmental perturbations on PSI activity in the context of metabolic productivity.

Approximating carbon fixation - how important is the Calvin-Benson cycle steady-state assumption?

“…To determine the required fidelity to represent the CBB cycle, pETC and photo-protective mechanisms, we first compared simulations of a detailed ordinary differential equation (ODE) model with and without a simplifying metabolic steady-state assumption [21, 13]. For this first simplification we removed the dynamic change of metabolite concentrations by pre-calculating steady-state fluxes of an ODE model in response to realistic field conditions using incoming photosynthetically active photon flux density (PPFD) measured in one minute intervals at a National Ecological Observatory Network site in Washington state, USA [17].…”

“…This finding indicates that care is needed when validating a model using only carbon fixation rates, since any model that keeps RuBP concentration stable can lead to realistic carbon fixation rates. Possible improvements include using predictions of other metabolite pools ( [2]) or fluorescence data if the model also contains the pETC ( [20]). Further work can test the ability to make steady-state assumptions with more complex models of carbon assimilation that include for example photorespiration, CO2 as a dynamic variable or dynamic temperature.…”

“…All code used to generate the publication results and figures is publicly available on our GitLab repository https://gitlab.com/qtb-hhu/photosynthesis-task-force/2022-how-realistic-is-the-cbb-ssa. We obtained field observation PPFD data measured in one minute intervals in Washington state (latitude 45.790835, longitude −121.933788) by the National Ecological Observatory Network (NEON) for which we identified which day had the highest data coverage for each month, which was the 25th, and the ODE model from Saadat 2021 [17, 21]. Due to model instabilities for PPFD values below 30, we clamped the minimum of the data to 30.…”

“…Notably, Hahn considered models with 17-31 non-linear differential equations to be large while nowadays genome-scale modeling techniques are frequently employed, which can contain thousands of reactions [14, 5, 6, 10]. To revisit the spirit of trying to understand the key features of a system we employ model reduction of a previously published model of the pETC and the CBB cycle to elucidate the main processes controlling carbon fixation in C3 plants under dynamic conditions [20]. The resulting simplified models can serve as robust alternatives in situations where few parameters are known and the research question is only concerned with carbon fixation rate, as their predictions are in very good agreement with the predictions of the original complex model.…”

What controls carbon sequestration in plants under which conditions?

“…Because control coefficients depend on the dynamics of the interactions of all components, they are systemic properties. MCA has been repeatedly applied to study the control of reaction steps in plant metabolic path-ways [25] with examples including applications to the benzoid pathway, sucrose accumulation, the CBB cycle, the electron transport chain, and combinations of these [30,3,5,17,26].…”