Direct energy transfer from photosystem II to photosystem I confers winter sustainability in Scots Pine

Pushan Bag,Alexander G Ivanov,Stefan Jansson,Roberta Croce,Volha Chukhutsina,Alfred R Holzwarth,Suman Paul,Tatyana Shutova,Zishan Zhang

doi:10.1038/s41467-020-20137-9

Abstract

Evergreen conifers in boreal forests can survive extremely cold (freezing) temperatures during long dark winter and fully recover during 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, here we have analyzed seasonal adjustment 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. Analysis of 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 play a major role. This mechanism is enabled by extensive thylakoid destacking allowing for the mixing of PSII with PSI complexes. These two linked phenomena play crucial roles in winter acclimation and protection.

Highlights

Evergreen conifers in boreal forests can survive extremely cold temperatures during long dark winter and fully recover during summer
In the main figures we only present data from 2017 to 2018, which we divided into five distinct seasons, based on weather parameters: Summer (S, June–Aug), autumn (A, Sept–mid Nov), winter (W, mid Nov–mid Feb), early spring (ES, mid Feb–mid Apr), and late spring (LS, mid Apr–June)
Fv/ Fm was highest in S, fell with reductions in ambient temperatures during A and W (Fig. 1d, e), and was lowest in ES (63% lower than in S), when low temperatures coincided with rises in solar irradiance (Fig. 1a–c; see Supplementary Fig. 2a)

Summary

Introduction

Evergreen conifers in boreal forests can survive extremely cold (freezing) temperatures during long dark winter and fully recover during summer. Several mechanisms might contribute to ‘sustained quenching’ of winter/early spring pine needles, timeresolved fluorescence analysis shows that extreme down-regulation of photosystem II activity along with direct energy transfer from photosystem II to photosystem I play a major role. This mechanism is enabled by extensive thylakoid destacking allowing for the mixing of PSII with PSI complexes. Our data strongly indicate that chlorophyll fluorescence quenching and thylakoid destacking are strongly linked, mutually dependent and crucial for the survival of evergreen conifers in the extreme northern boreal winter and early spring, when temperatures are low but solar radiation levels may be high

Methods

Results

Conclusion