Abstract
Key aspects of leaf mitochondrial metabolism in the light remain unresolved. For example, there is debate about the relative importance of exporting reducing equivalents from mitochondria for the peroxisomal steps of photorespiration versus oxidation of NADH to generate ATP by oxidative phosphorylation. Here, we address this and explore energetic coupling between organelles in the light using a diel flux balance analysis model. The model included more than 600 reactions of central metabolism with full stoichiometric accounting of energy production and consumption. Different scenarios of energy availability (light intensity) and demand (source leaf versus a growing leaf) were considered, and the model was constrained by the nonlinear relationship between light and CO2 assimilation rate. The analysis demonstrated that the chloroplast can theoretically generate sufficient ATP to satisfy the energy requirements of the rest of the cell in addition to its own. However, this requires unrealistic high light use efficiency and, in practice, the availability of chloroplast-derived ATP is limited by chloroplast energy dissipation systems, such as nonphotochemical quenching, and the capacity of the chloroplast ATP export shuttles. Given these limitations, substantial mitochondrial ATP synthesis is required to fulfill cytosolic ATP requirements, with only minimal, or zero, export of mitochondrial reducing equivalents. The analysis also revealed the importance of exporting reducing equivalents from chloroplasts to sustain photorespiration. Hence, the chloroplast malate valve and triose phosphate-3-phosphoglycerate shuttle are predicted to have important metabolic roles, in addition to their more commonly discussed contribution to the avoidance of photooxidative stress.
Highlights
The role of mitochondria in leaves in the light has long been a matter of debate (Nunes-Nesi et al., 2008; Dahal et al, 2017; Tcherkez et al, 2017; O’Leary et al, 2018)
This is in part because photosynthesis dominates the energetics of a leaf during the day, and because the biochemistry of leaf mitochondria during the day departs substantially from the conventional tricarboxylic acid (TCA)-cycle-coupled-to-oxidative-phosphorylation mode that is the norm for non-photosynthetic cells (Sweetlove et al, 2010; Millar et al, 2011; Tcherkez et al, 2012; O’Leary et al, 2018)
The engagement of mitochondrial ATP synthesis in a leaf in the light is likely to depend upon the balance between the available light energy (PPFD) and energy demand
Summary
The role of mitochondria in leaves in the light has long been a matter of debate (Nunes-Nesi et al., 2008; Dahal et al, 2017; Tcherkez et al, 2017; O’Leary et al, 2018) This is in part because photosynthesis dominates the energetics of a leaf during the day, and because the biochemistry of leaf mitochondria during the day departs substantially from the conventional tricarboxylic acid (TCA)-cycle-coupled-to-oxidative-phosphorylation mode that is the norm for non-photosynthetic cells (Sweetlove et al, 2010; Millar et al, 2011; Tcherkez et al, 2012; O’Leary et al, 2018). Stoichiometrically equal amounts of NADH are generated by mitochondrial glycine decarboxylase and consumed by peroxisomal hydroxypyruvate reductase (Bauwe et al, 2010). This had led to the suggestion that all of the mitochondrial NADH generated by glycine decarboxylase would be transferred to the peroxisome using a malate-oxaloacetate (OAA) metabolite shuttle system (Fig. 1)
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