In Silico Analysis of the Regulation of the Photosynthetic Electron Transport Chain in C3 Plants

Abstract

ORCID IDs: 0000-0002-6129-4570 (A.M.); 0000-0001-8273-8022 (X.Y); 0000-0002-0607-4508 (J.H.); 0000-0003-4144-6028 (S.M.D.); 0000-0001-6011-7487 (J.M.); 0000-0003-2196-547X (P.C.S.).We present a new simulation model of the reactions in the photosynthetic electron transport chain of C3 species. We show that including recent insights about the regulation of the thylakoid proton motive force, ATP/NADPH balancing mechanisms (cyclic and noncyclic alternative electron transport), and regulation of Rubisco activity leads to emergent behaviors that may affect the operation and regulation of photosynthesis under different dynamic environmental conditions. The model was parameterized with experimental results in the literature, with a focus on Arabidopsis (Arabidopsis thaliana). A dataset was constructed from multiple sources, including measurements of steady-state and dynamic gas exchange, chlorophyll fluorescence, and absorbance spectroscopy under different light intensities and CO 2 , to test predictions of the model under different experimental conditions. Simulations suggested that there are strong interactions between cyclic and noncyclic alternative electron transport and that an excess capacity for alternative electron transport is required to ensure adequate redox state and lumen pH. Furthermore, the model predicted that, under specific conditions, reduction of ferredoxin by plastoquinol is possible after a rapid increase in light intensity. Further analysis also revealed that the relationship between ATP synthesis and proton motive force was highly regulated by the concentrations of ATP, ADP, and inorganic phosphate, and this facilitated an increase in nonphotochemical quenching and proton motive force under conditions where metabolism was limiting, such as low CO 2 , high light intensity, or combined high CO 2 and high light intensity. The model may be used as an in silico platform for future research on the regulation of photosynthetic electron transport.Plants face highly variable environmental conditions, with fluctuations of light intensity, temperature, humidity, and CO 2 that occur over a wide range of time scales, from seconds to seasons. Imbalances between the rate of light capture and CO 2 assimilation can lead to an excess of energy in the system. Under such conditions, photosynthesis faces three main challenges:1. To dissipate the excess of energy that could otherwise result in the production of reactive oxygen species (Foyer et al., 2011); 2. To couple the production and demand of ATP and NADPH in chloroplasts under a fluctuating environment (Noctor and Foyer, 2000); 3. To maintain an adequate redox state (Allen, 2004) of the photosynthetic electron transport chain (PETC).In this study, we use the term regulation to indicate those mechanisms that allow photosynthesis to achieve these goals. These goals must be met simultaneously, and several mechanisms have been identified as contributing (Kramer et al., 2004), including:1. Nonphotochemical quenching (NPQ) of excess energy absorbed by photosynthetic...

Growth at Elevated CO2 Requires Acclimation of the Respiratory Chain to Support Photosynthesis

“…A consequence of excessive sugar phosphate accumulation in the cytosol is that it sequesters P i that would otherwise be returned to the stroma in exchange for triose phosphates, following consumption of the cytosolic sugar phosphates by Suc synthesis or by respiration (Stitt et al, 2010). In turn, too low P i in the stroma could restrict ATP synthase activity (Sharkey and Vanderveer, 1989;Kanazawa and Kramer, 2002;Takizawa et al, 2008;Kiirats et al, 2009;Morales et al, 2018). Consistent with this possibility, the well-watered ECO 2 -grown knockdowns maintained higher pmf (ECS t ) and ∆pH (ECS inv ) across the thylakoid membrane than the other plant lines (Fig.…”

“…However, this exaggerated CET rate may be higher than necessary to meet the ATP demands of the chloroplast at ECO 2 . The resulting high chloroplast ATP/ADP ratio would then act to slow ATP synthase activity (Morales et al, 2018), resulting in the high ECS t and low g H + mentioned above. The higher CET rate in the knockdowns also may explain why v H + did not differ across plant lines at ECO 2 , even though the knockdowns tended to maintain a lower ETR (rate of linear electron transport) than the other plant lines.…”

Optimization of ATP Synthase c–Rings for Oxygenic Photosynthesis

“…The resulting energy imbalance requires that chloroplasts activate processes to make up the differences in response to photosynthetic output capacity (Kramer and Evans, 2011). These include cyclic electron flow (reviewed in Strand et al, 2016), the water-water-cycle (Asada, 1999), the malate valve (Scheibe, 2004), as well as balancing the adenylate and electron (either ferredoxin or NADPH) requirements of other metabolic processes (Noctor and Foyer, 2000;Walker et al, 2014;Morales et al, 2018) all of which consume (directly or indirectly) photosynthetic energy. Thus, the large c stoichiometries in chloroplasts decrease energy efficiency both at the ATP synthase itself and in imposing a need for additional ATP producing reactions that decrease overall quantum efficiency of photosynthesis.…”

The Dynamic Plant: Capture, Transformation, and Management of Energy

“…In a pioneering study, Lichtenberg et al (2017) performed laser light sheet microscopy with defined spectra on the thalli of the aquatic macrophyte Fucus to improve the estimation of PSII efficiency. To better understand photosynthetic electron transport, Morales et al (2018) leveraged an extensive published dataset for the C3 species Arabidopsis, including gas exchange, chlorophyll fluorescence, light intensity, and CO 2 availability, to model interactions between multiple mechanisms and reactions. These interactions include regulation of cyclic and noncyclic alternative electron transport and Rubisco activity.…”