Modelling the role of LHCII-LHCII, PSII-LHCII and PSI-LHCII interactions in state transitions

The light-dependent reactions of photosynthesis take place in the plant chloroplast thylakoid membrane, a complex three-dimensional structure divided into the stacked grana and unstacked stromal lamellae domains. Plants regulate the macro-organization of photosynthetic complexes within the thylakoid membrane to adapt to changing environmental conditions and avoid oxidative stress. One such mechanism is the state transition which regulates photosynthetic light harvesting and electron transfer. State transitions are driven by changes in the phosphorylation of light harvesting antenna complex II (LHCII), which cause a decrease in grana diameter and stacking, a decreased energetic connectivity between photosystem II (PSII) reaction centres and an increase in the relative LHCII antenna size of photosystem I (PSI) compared to PSII. Phosphorylation is believed to drive these changes by weakening the intra-membrane lateral PSII-LHCII and LHCII-LHCII interactions and the inter-membrane stacking interactions between these complexes, while simultaneously increasing the affinity of LHCII for PSI. We investigated the relative roles and contributions of these three types of interaction to state transitions using a lattice-based model of the thylakoid membrane based on existing structural data, developing a novel algorithm to simulate protein complex dynamics. Monte Carlo simulations revealed that state transitions are unlikely to lead to a large-scale migration of LHCII from the grana to the stromal lamellae. Instead, the increased light harvesting capacity of PSI is largely due to the more efficient recruitment of LHCII already residing in the stromal lamellae into PSI-LHCII supercomplexes upon its phosphorylation. Likewise, the increased light harvesting capacity of PSII upon dephosphorylation was found to be driven by a more efficient recruitment of LHCII already residing in the grana into functional PSII-LHCII clusters, primarily driven by lateral interactions.Statement of significanceFor photosynthesis to operate at maximum efficiency the activity of the light-driven chlorophyll-protein complexes, photosystems I and II (PSI and PSII) must be fine-tuned to environmental conditions. Plants achieve this balance through a regulatory mechanism known as the state transition, which modulates the relative light-harvesting antenna size and therefore excitation rate of each photosystem. State transitions are driven by changes in the extent of the phosphorylation of light harvesting complex II (LHCII), which modulate the interactions between PSI, PSII and LHCII. Here we developed a novel algorithm to simulate protein complex dynamics and then ran Monte Carlo simulations to understand how these interactions cooperate to affect the organization of the photosynthetic membrane and bring about state transitions.