Low-temperature modulation of the redox properties of the acceptor side of photosystem II: photoprotection through reaction centre quenching of excess energy

Although it has been well established that acclimation to low growth temperatures is strongly correlated with an increased proportion of reduced Q_A in all photosynthetic groups, the precise mechanism controlling the redox state of Q_A and its physiological significance in developing cold tolerance in photoautotrophs has not been fully elucidated. Our recent thermoluminescence (TL) measurements of the acceptor site of PSII have revealed that short‐term exposure of the cyanobacterium Synechococcus sp. PCC 7942 to cold stress, overwintering of Scots pine (Pinus sylvestris L.), and acclimation of Arabidopsis plants to low growth temperatures, all caused a substantial shift in the characteristic T_M of S₂Q_B^– recombination to lower temperatures. These changes were accompanied by much lower overall TL emission, restricted electron transfer between Q_A and Q_B, and in Arabidopsis by a shift of the S₂Q_A^–‐related peak to higher temperatures. The shifts in recombination temperatures are indicative of a lower activation energy for the S₂Q_B^– redox pair and a higher activation energy for the S₂Q_A^– redox pair. This results in an increase in the free‐energy gap between P680⁺Q_A^– and P680⁺Pheo^– and a narrowing of the free energy gap between Q_A and Q_B electron acceptors. We propose that these effects result in an increased population of reduced Q_A (Q_A^–), facilitating non‐radiative P680⁺Q_A^– radical pair recombination within the PSII reaction centre. The proposed reaction centre quenching could be an important protective mechanism in cyanobacteria in which antenna and zeaxanthin cycle‐dependent quenching are not present. In herbaceous plants, the enhanced capacity for dissipation of excess light energy via PSII reaction centre quenching following cold acclimation may complement their capacity for increased utilization of absorbed light through CO₂ assimilation and carbon metabolism. During overwintering of evergreens, when photosynthesis is inhibited, PSII reaction centre quenching may complement non‐photochemical quenching within the light‐harvesting antenna when zeaxanthin cycle‐dependent energy quenching is thermodynamically restricted by low temperatures. We suggest that PSII reaction centre quenching is a significant mechanism enabling cold‐acclimated organisms to acquire increased resistance to high light.