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Abstract Green organisms evolve oxygen (O2) via photosynthesis and consume it by respiration. Generally, net O2 consumption only becomes dominant when photosynthesis is suppressed at night. Here, we show that green thylakoid membranes of Scots pine (Pinus sylvestris L) and Norway spruce (Picea abies) needles display strong O2 consumption even in the presence of light when extremely low temperatures coincide with high solar irradiation during early spring (ES). By employing different electron transport chain inhibitors, we show that this unusual light-induced O2 consumption occurs around photosystem (PS) I and correlates with higher abundance of flavodiiron (Flv) A protein in ES thylakoids. With P700 absorption changes, we demonstrate that electron scavenging from the acceptor-side of PSI via O2 photoreduction is a major alternative pathway in ES. This photoprotection mechanism in vascular plants indicates that conifers have developed an adaptative evolution trajectory for growing in harsh environments.

Evergreen conifers rely on ‘sustained quenching’ to protect their photosynthetic machinery during long, cold winters. Here, Bag et al. show that direct energy transfer (spillover) from photosystem II to photosystem I triggered by loss of grana stacking in chloroplast is the major component of sustained quenching in Scots pine.

A Correction to this paper has been published: https://doi.org/10.1038/s41467-021-22013-6