Direct energy transfer from photosystem II to photosystem I is the major regulator of winter sustainability of Scots pine

Evergreen conifers in boreal forests can survive extremely cold (freezing) temperatures during the long dark winter and fully recover during the summer. A phenomenon called sustained quenching putatively provides photoprotection and enables their survival, but its precise molecular and physiological mechanisms are not understood. To unveil them, we have analyzed the seasonal adaptation of the photosynthetic machinery of Scots pine (Pinus sylvestris) trees by monitoring multi-year changes in weather, chlorophyll fluorescence, chloroplast ultrastructure, and changes in pigment-protein composition. Recorded Photosystem II and Photosystem I performance parameters indicate that highly dynamic structural and functional seasonal rearrangements of the photosynthetic apparatus occur. Although several mechanisms might contribute to sustained quenching of winter/early spring pine needles, time-resolved fluorescence analysis shows that extreme down-regulation of photosystem II activity along with direct energy transfer from photosystem II to photosystem I plays a major role. This mechanism is enabled by extensive thylakoid destacking allowing for mixing of PSII with PSI complexes. These two linked phenomena play crucial roles in winter acclimation and protection.