Essential mitochondrial activity in Physcomitrium patens relies on complementary cytochrome and alternative oxidase pathways.

Mitochondrial respiration catalyses the transfer of electrons from NADH to oxygen through the activity of five multiprotein complexes. In plants, mitochondria also possess additional alternative electron transport pathways, including the alternative oxidase (AOX) pathway, which transfers electrons from ubiquinol to O2, bypassing the cytochrome-dependent electron transport chain. This study investigates the functional role of AOX during plant evolution by analysing Physcomitrium patens plants that lack or overexpress AOX. In the moss P. patens, AOX exhibits a remarkably high electron transport capacity, sufficient to fully compensate for the inactivation of the cytochrome pathway. Despite the high potential activity of AOX, aox knockout lines did not show significant defects in growth under various abiotic stresses. This suggests that the cytochrome pathway can compensate for AOX loss and effectively support the consumption of reducing power produced by photosynthesis even under stressful conditions. Although photosynthetically active cells can produce ATP in chloroplasts under illumination independently of mitochondrial electron transport, respiration is shown to be essential for the conversion of reducing power into ATP for distribution throughout the cell. Simultaneous inactivation of AOX and CIII was lethal, indicating that AOX and the complementary cytochrome pathway contribute to the essential role of mitochondrial respiration in the redox and energy balance in P. patens cells.