Balancing energy supply during photosynthesis - a theoretical perspective

Abstract

The photosynthetic electron transport chain (PETC) provides energy and redox equivalents for carbon fixation by the Calvin-Benson-Bassham (CBB) cycle. Both of these processes have been thoroughly investigated and the underlying molecular mechanisms are well known. However, it is far from understood by which mechanisms it is ensured that energy and redox supply by photosynthesis matches the demand of the downstream processes. Here, we deliver a theoretical analysis to quantitatively study the supply-demand regulation in photosynthesis. For this, we connect two previously developed models, one describing the PETC, originally developed to study non-photochemical quenching, and one providing a dynamic description of the photosynthetic carbon fixation in C3 plants, the CBB Cycle. The merged model explains how a tight regulation of supply and demand reactions leads to efficient carbon fixation. The model further illustrates that a stand-by mode is necessary in the dark to ensure that the carbon fixation cycle can be restarted after dark-light transitions, and it supports hypotheses, which Abbreviations: CBB, Calvin-Benson-Bassham; Fd, ferrodoxin; MCA, Metabolic Control Analysis; NPQ, non-photochemical quenching; ODE, ordinary differential equations; PC, plastocyanin; PETC, photosynthetic electron transport chain; PFD, photon flux density; PPP, Pentose phosphate pathway; PQ, plastoquinone; PS, photosystem; RuBP, Ribulose 1,5-bisphosphate; Ru5P, Ribose-5-phosphate; TPT, triose phosphate transporters * Equally contributing authors. AM merged the models and provided all mathematical descriptions. NPS performed the computational analyses and prepared the first draft of the Results. All authors were involved in the interpretation of the results and preparation of the manuscript. 1 2 MATUSZYŃSKA ET AL.reactions are responsible to generate such mode in vivo. K E Y W O R D Scarbon assimilation, electron transport, mathematical model | INTRODUCTIONDecades of multidisciplinary research of photosynthesis resulted in our today's detailed understanding of the molecular, regulatory and functional mechanisms of light driven carbon fixation. Yet, still much is to uncover, especially in terms of identifying processes limiting photosynthetic productivity, calling for further basic research that may help redesigning photosynthesis [1, 2]. Historically, the process of photosynthesis has been divided into two parts. The so-called light reactions carried by the photosynthetic electron transport chain (PETC) convert light into chemical energy, supplying ATP and NADPH. This energy is next used to drive the carbon dioxide reduction and fixation in the processes known as the dark reactions. Thus, the metabolic light and dark reactions can be viewed as a molecular economy supply-demand system [3, 4, 5].Despite this clear interdependence, these processes are often studied in isolation, permitting detailed and in-depth analysis of particular components at the cost of simplification of the preceding / following processes. Such separation is also ref...