Short-term acclimation of the photosynthetic electron transfer chain to changing light: a mathematical model

Abstract

One contribution of 20 to a Theme Issue 'Changing the light environment: chloroplast signalling and response mechanisms'. Photosynthetic eukaryotes house two photosystems with distinct light absorption spectra. Natural fluctuations in light quality and quantity can lead to unbalanced or excess excitation, compromising photosynthetic efficiency and causing photodamage. Consequently, these organisms have acquired several distinct adaptive mechanisms, collectively referred to as non-photochemical quenching (NPQ) of chlorophyll fluorescence, which modulates the organization and function of the photosynthetic apparatus. The ability to monitor NPQ processes fluorometrically has led to substantial progress in elucidating the underlying molecular mechanisms. However, the relative contribution of distinct NPQ mechanisms to variable light conditions in different photosynthetic eukaryotes remains unclear. Here, we present a mathematical model of the dynamic regulation of eukaryotic photosynthesis using ordinary differential equations. We demonstrate that, for Chlamydomonas, our model recapitulates the basic fluorescence features of short-term light acclimation known as state transitions and discuss how the model can be iteratively refined by comparison with physiological experiments to further our understanding of light acclimation in different species.

Chloroplast remodeling during state transitions in Chlamydomonas reinhardtii as revealed by noninvasive techniques in vivo

“…We conclude that the consequences of ST on the antenna size of PSI are small (around 20%) in both light (8) and anaerobic (this study) conditions. In the light, the functional size of the PSII antenna is decreased by a similar extent in plants and green algae (8,38) and its changes are similar to the increase in the PSI antenna. Thus, STs serve the purpose of balancing light utilization by the two PSs for optimal photosynthesis under these conditions.…”

On the quantitative relation between dark kinetics of NPQ-induced changes in variable fluorescence and the activation state of the CF₀.CF₁.ATPase in leaves

“…The proper orientation and membrane organization of the photosynthetic machinery serves (1) the planar separation of two photochemical systems PSI and PSII, laterally connected by the cytochrome b 6 f complex that interacts with the plastoquinone (PQ) pool; it allows the uphill ---Received 30 April 2017; accepted 1 November 2017, published as online-first 10 January 2018. Phone: +31 317 482147/+31 318 430303, e-mail: wim@vredenberg.nl Abbreviations: CET -cyclic electron transport involving PSI; CF0·F1 -subunits of chloroplasts ATPase; ECS -absorbance changes associated with the electrochromic band shift; F0 -fluorescence level of dark-adapted system with 100% open RCs; Fm -fluorescence level of dark-adapted system with 100% closed RCs after fluorescence saturating pulse excitation; gH thyl -the conductivity of the thylakoid membrane to protons, predominantly determined by the activity of the ATP synthase; gH closed_CF0 -H + conductance of the closed CF0 channel of the CF0·F1·ATPase; gH open_CF0 -H + conductance of the open CF0 channel of the CF0·F1·ATPase; LET -linear electron transport involving PSI and PSII; M -time range (~30 s) at which the final F-decline in the Kautsky induction curve starts; NPQ -nonphotochemical quenching; OJIPSMT -Kautsky fluorescence induction curve; P -time range (~0.5-2 s) in Kautsky induction curve where stimulation of variable chlorophyll fluorescence F by pmf and release of photochemical and electrochemical quenching is maximal; pmf -proton motive force; RC -reaction center of photosystem; S -time range (~15 s) in Kautsky induction curve where the contribution of the slow component of F-decay has become minimal; SP -fluorescence saturating pulse with duration exceeding 3,000 ms; sSP -short fluorescence excitation light pulse with duration between 0.25 and 3,000 ms; 3k (0.05k) pulse -light pulse with intensity 3,000 (50) µmol(photon) m -2 s -1 electron transfer from water in contact with the oxygenevolving complex (OEC) on the donor side of PSII to a reductant NADP(H) at the acceptor side of PSI; (2) exciton trapping, and subsequent trans-membrane charge separation in the reaction centers (RCs) of both photosystems that results in an electrogenic event associated with the generation of a trans-membrane electric potential (ΔΨ) with associated electromotive force that acts as a driving force for the generation of electrochemical gradients of ions, in particular protons; (3) the anchoring and proper orientation of active proton pumps, such as the RCs, the cytochrome b 6 f complex, and the ATP(synth)ase (for recent surveys and schematic representations see Vredenberg 2011, Ebenhöh et al 2014, Tikkanen and Aro 2014, Tikhonov 2015, Shikanai 2016. Many experimental and theoretical approaches from the basic life sciences have enabled time, structure, and function analyses of (parts of) the photosynthetic light and dark reactions down to the nano scale, or even lower.…”

A reductionist approach to model photosynthetic self-regulation in eukaryotes in response to light

“…State transitions are triggered by the imbalance in the redox poise of the plastoquinone (PQ) pool, where an over-reduced pool indirectly activates a kinase [36] (serine/threonine-protein kinase STN7 in Arabidopsis thaliana, serine/threonineprotein kinase Stt7 in Chlamydomonas reinhardtii) that phosphorylates antenna associated with PSII, triggering reversible antenna movement, thus resulting in a decreased delivery of photons to the PSII RC, therefore reducing PSII activation [37]. To our knowledge, the only available dynamic model of qT has been published recently by one of the authors [38]. This model provides a reliable representation of qT and presents a good basis for analysing the entire photosynthetic electron transport chain and its interaction with environmental cues and downstream processes.…”