Plastoquinone homoeostasis by Arabidopsis proton gradient regulation 6 is essential for photosynthetic efficiency

Abstract

Photosynthesis produces organic carbon via a light-driven electron flow from H 2 O to CO 2 that passes through a pool of plastoquinone molecules. These molecules are either present in the photosynthetic thylakoid membranes, participating in photochemistry (photoactive pool), or stored (non-photoactive pool) in thylakoid-attached lipid droplets, the plastoglobules. The photoactive pool acts also as a signal of photosynthetic activity allowing the adaptation to changes in light condition. Here we show that, in Arabidopsis thaliana , proton gradient regulation 6 (PGR6), a predicted atypical kinase located at plastoglobules, is required for plastoquinone homoeostasis, i.e. to maintain the photoactive plastoquinone pool. In a pgr6 mutant, the photoactive pool is depleted and becomes limiting under high light, affecting short-term acclimation and photosynthetic efficiency. In the long term, pgr6 seedlings fail to adapt to high light and develop a conditional variegated leaf phenotype. Therefore, PGR6 activity, by regulating plastoquinone homoeostasis, is required to cope with high light.

Mutation of the Atypical Kinase ABC1K3 Partially Rescues the PROTON GRADIENT REGULATION 6 Phenotype in Arabidopsis thaliana

“…We found that the abc1k3 mutant has no photosynthetic defect compared to the wild type under the tested conditions. However, by stacking this mutation with abc1k1 we observe a partial alleviation of all the photosynthetic defects previously reported in abc1k1 (Shikanai et al, 1999;Martinis et al, 2014;Pralon et al, 2019). Surprisingly, the phenotype complementation does not originate from an effect on the size of the photoactive PQ pool but rather from an effect on PQ mobility in the thylakoid membrane.…”

“…The kinetic of the subsequent reoxidation induced by FAR were followed with a saturating flash of actinic light (1000 µmol m −2 s −1 for 100 µs) to fully reduce the ETC or without so that the ETC was fully oxidized. The ratio between the lag times between the FAR onset and the beginning of the P 700 oxidation in these two conditions is used as a proxy for the number of available electrons per PSI (Pralon et al, 2019).…”

“…The analysis of the photoactive PQ pool, and of the total pool were performed as previously described (Pralon et al, 2019). Briefly, leaf disks of 0.8 cm of diameter were collected from 5 weeks old plants.…”

“…Independent studies indicate that abc1k1 is impaired in NPQ as well as electron transport (Shikanai et al, 1999;Martinis et al, 2014;Pralon et al, 2019), while the abc1k3 mutant did not show defects in those parameters even after prolonged high light exposure (Martinis et al, 2013). To further characterize the abc1k1/abc1k3 double mutant, we measured photosynthetic parameters such as PSII maximum efficiency [ϕ MAX (= F V /F M )], NPQ as well as electron capacity of the ETC in 4-5 weeks old plants grown under moderate light (120 µmol m −2 s −1 ) (ML) and after 3 h of high light (500 µmol m −2 s −1 ).…”

“…Recently, a molecular mechanism explaining the pgr6(abc1k1) defect was proposed: ABC1K1 would be required for the homeostasis of photoactive PQ. Indeed, upon high light, the photoactive PQ pool in abc1k1 mutant becomes limiting and this can explain the diminished linear electron transport and NPQ, the dephosphorylation of the LHCII antenna and perturbation of the state transitions; all these leading to an overall decrease in the photosynthetic efficiency (Pralon et al, 2019).…”