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.

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Multiple chloroplast-to-nucleus signaling pathways contribute to the regulation of chloroplast biogenesis during plant greening. Here, we provide evidence for the direct implication of the atypical kinase ABC1K1. ABC1K1 is required for sufficient plastoquinone (PQ) allocation to the photosynthetic electron transport chain. Unexpectedly, mutation of abc1k1 suppresses greening and results in pale cotyledons under red light. This phenotype was not observed in other photosynthetic mutants and points to a specific signaling defect. Under red light, abc1k1 accumulated EXECUTER1 (EX1), a trigger of singlet oxygen (1O2) signaling. Consistent with the role of the FTSH metalloprotease in chloroplast biogenesis and EX1 degradation, the ftsh2 mutant var2, mimicked the greening defect of abc1k1 and accumulated EX1 under red light. We propose that this novel ABC1K1-dependent signal is required for chloroplast biogenesis to progress in challenging light conditions.