Impaired Cyclic Electron Flow around Photosystem I Disturbs High-Light Respiratory Metabolism

The cyclic electron flow around photosystem I (CEF-PSI) increases ATP/NADPH production in the chloroplast, acting as an energy balance mechanism. Higher export of reducing power from the chloroplast in CEF-PSI mutants has been correlated with higher mitochondrial alternative oxidase (AOX) capacity and protein amount under high-light (HL) conditions. However, in vivo measurements of AOX activity are still required to confirm the exact role of AOX in dissipating the excess of reductant power from the chloroplast. Here, CEF-PSI single and double mutants were exposed to short-term HL conditions in Arabidopsis (Arabidopsis thaliana). Chlorophyll fluorescence, in vivo activities of the cytochrome oxidase (ν_cyt) and AOX (ν_alt) pathways, levels of mitochondrial proteins, metabolite profiles, and pyridine nucleotide levels were determined under normal growth and HL conditions. ν_alt was not increased in CEF-PSI mutants, while AOX capacity was positively correlated with photoinhibition, probably due to a reactive oxygen species-induced increase of AOX protein. The severe metabolic impairment observed in CEF-PSI mutants, as indicated by the increase in photoinhibition and changes in the levels of stress-related metabolites, can explain their lack of ν_alt induction. By contrast, ν_cyt was positively correlated with photosynthetic performance. Correlations with metabolite changes suggest that ν_cyt is coordinated with sugar metabolism and stress-related amino acid synthesis. Furthermore, changes in glycine-serine and NADH-NAD⁺ ratios were highly correlated to ν_cyt Taken together, our results suggest that ν_cyt can act as a sink for the excess of electrons from the chloroplast, probably via photorespiratory glycine oxidation, thus improving photosynthetic performance when ν_alt is not induced under severe HL stress.