Photorespiration does not act as a photoprotective electron sink under unstressed conditions

Photosynthesis is comprised of two sets of reactions that must coordinate activities to maintain optimal efficiency and avoid harmful side reactions. The first set of reactions is light driven electron transfer, in a second set the electrons are used for carbon fixation in the C3 cycle. In addition to the C3 cycle, electrons are used to drive photorespiration, the metabolic pathway that detoxifies the harmful product of the rubisco oxygenase reaction. It has been hypothesized that photorespiration is a photoprotective electron sink to avoid metabolic congestion that could lead to damage of the electron transport chain and reduced activity of photosystem II. To tease apart the impact of C3 and photorespiratory metabolic sink on both photosynthetic efficiency and photoprotection, we used chlorophyll a fluorescence coupled to gas exchange to probe the response of the electron transport chain to a wide range of metabolic poise, set by O₂ and CO₂ gas mixing. We found that, while metabolic flux correlated well with efficiency of photosystem II, fractional metabolic poise towards photorespiration was the largest metabolic determinant of long-lived downregulation of light harvesting at photosystem II. This long-lived downregulation does not correlate with observed D1 loss, suggesting accumulation of a quencher that is not damage to the photosystem. Together, these findings are contradictory to the proposed role of photorespiration as a photoprotective electron sink. Additionally, we have demonstrated that O₂ concentration interacts with downregulation of photosystem II separately from the effects of O₂ on metabolic poise which complicates the interpretation of photoprotection data generated when using O₂.