Shrink or expand? Just relax! Bidirectional grana structural dynamics as early light-induced regulator of photosynthesis

Abstract

Light-induced structural changes in thylakoid membranes have been reported for decades, with conflicting data regarding their shrinkage or expansion during dark–light transitions. Understanding these dynamics is important for both fundamental photosynthesis research and agricultural applications. This research investigated the temporal sequence of thylakoid structural changes during light exposure and their functional significance. We combined high-resolution structural approaches (transmission electron microscopy, confocal microscopy with 3D modeling, and small-angle neutron scattering) with spectroscopic and electrophoretic analyses of the photosynthetic apparatus of Arabidopsis thaliana and Ficus elastica plants. A meta-analysis of published ultrastructural data complemented our experimental approach to resolve existing contradictions. We discovered a three-phase response pattern: initial shrinkage, expansion, and relaxation to dark-state equilibrium. The initial shrinkage specifically regulated the cyclic/linear electron transport ratio, providing rapid photoprotection. We also showed that plants' acclimation to different light regimes modulates the kinetics of this response, with constant-light-grown plants exhibiting faster structural adaptations than those acclimated to glasshouse conditions. This work challenges the traditional binary model of light-induced thylakoid structural dynamics, revealing a sophisticated temporal regulatory mechanism, with the dark-adapted state serving as a relaxed equilibrium. The discovered three-phase response reconciles decades of conflicting observations and reveals how plants achieve rapid photoprotection before engaging longer term adaptive responses.