Mitochondria affect photosynthesis through altered tissue levels of oxygen

Interactions between plant energy organelles, the chloroplasts and the mitochondria, are crucial for plant development and acclimation. These interactions occur at different levels including exchange of metabolites and reducing power, organelle signaling pathways and intracellular gas exchange. Mitochondrial retrograde stress signaling activates expression of nuclear genes encoding mitochondrial components, including alternative oxidases. High abundances of these respiratory enzymes coincide not only with the changes in plant respiration but also with alterations in the chloroplast. For example, plants that overexpress alternative oxidases are tolerant to methyl viologen, a redox-active compound that catalyzes transfer of electrons from Photosystem I to molecular oxygen. The mechanism of this inter-organelle interaction is unclear but could be related to diminished availability of tissue oxygen. Here we assessed respiration, photosynthesis and in vivo levels of oxygen in a set of Arabidopsis lines with perturbations in diverse mitochondrial functions, including defects in respiratory complex I, mitochondrial protein processing, transcription, nucleoid organization, altered fission and architecture or suppressed ATP synthase activity. In these lines, the increased abundance and activity of alternative oxidases strongly correlated with higher oxygen consumption in darkness, lower oxygen re-accumulation in light, and diminished effects of methyl viologen in chloroplasts. These results support the hypothesis that increased mitochondrial oxygen sink capacity affects photosynthesis by decreasing oxygen levels in tissues. This phenomenon can be one of the reasons for the impact that stressed mitochondria have on chloroplasts and photosynthesis. It contributes to our understanding of the mechanisms of hypoxia establishment and acclimation in plants.