Dynamic thylakoid stacking and state transitions work synergistically to avoid acceptor-side limitation of photosystem I

TAP38/STN7-dependent (de)phosphorylation of light-harvesting complex II (LHCII) regulates the relative excitation rates of photosystems I and II (PSI, PSII) (state transitions) and the size of the thylakoid grana stacks (dynamic thylakoid stacking). Yet, it remains unclear how changing grana size benefits photosynthesis and whether these two regulatory mechanisms function independently. Here, by comparing Arabidopsis wild-type, stn7 and tap38 plants with the psal mutant, which undergoes dynamic thylakoid stacking but lacks state transitions, we explain their distinct roles. Under low light, smaller grana increase the rate of PSI reduction and photosynthesis by reducing the diffusion distance for plastoquinol; however, this beneficial effect is only apparent when PSI/PSII excitation balance is maintained by state transitions or far-red light. Under high light, the larger grana slow plastoquinol diffusion and lower the equilibrium constant between plastocyanin and PSI, maximizing photosynthesis by avoiding PSI photoinhibition. Loss of state transitions in low light or maintenance of smaller grana in high light also both bring about a decrease in cyclic electron transfer and over-reduction of the PSI acceptor side. These results demonstrate that state transitions and dynamic thylakoid stacking work synergistically to regulate photosynthesis in variable light.

Automated summary

The phosphorylation of LHCII by TAP38/STN7 regulates the excitation rates of PSI and PSII, as well as the size of thylakoid grana stacks. By comparing different plant mutants, it was found that smaller grana enhance PSI reduction and photosynthesis under low light, while larger grana optimize photosynthesis by preventing PSI photoinhibition under high light. State transitions and dynamic thylakoid stacking work synergistically to regulate photosynthesis in variable light conditions.