Light triggers chloroplast differentiation whereby the etioplast transforms into a photosynthesizing chloroplast and the thylakoid rapidly emerges. However, the sequence of events during chloroplast differentiation remains poorly understood. Using Serial Block Face Scanning Electron Microscopy (SBF-SEM), we generated a series of chloroplast 3D reconstructions during differentiation, revealing chloroplast number and volume and the extent of envelope and thylakoid membrane surfaces. Furthermore, we used quantitative lipid and whole proteome data to complement the (ultra)structural data, providing a time-resolved, multi-dimensional description of chloroplast differentiation. This showed two distinct phases of chloroplast biogenesis: an initial photosynthesis-enabling ‘Structure Establishment Phase’ followed by a ‘Chloroplast Proliferation Phase’ during cell expansion. Moreover, these data detail thylakoid membrane expansion during de-etiolation at the seedling level and the relative contribution and differential regulation of proteins and lipids at each developmental stage. Altogether, we establish a roadmap for chloroplast differentiation, a critical process for plant photoautotrophic growth and survival.

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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Light triggers chloroplast differentiation whereby the etioplast transforms into a photosynthesizing chloroplast and the thylakoid rapidly emerges. However, the sequence of events during chloroplast differentiation remains poorly understood. Using Serial Block Face Scanning Electron Microscopy (SBF-SEM), we generated a series of chloroplast 3D reconstructions during differentiation, revealing chloroplast number and volume and the extent of envelope and thylakoid membrane surfaces. Furthermore, we used quantitative lipid and whole proteome data to complement the (ultra)structural data, providing a time-resolved, multi-dimensional description of chloroplast differentiation. This showed two distinct phases of chloroplast biogenesis: an initial photosynthesis-enabling ‘Structure Establishment Phase’ followed by a ‘Chloroplast Proliferation Phase’ during cell expansion. Moreover, these data detail thylakoid membrane expansion during de-etiolation at the seedling level and the relative contribution and differential regulation of proteins and lipids at each developmental stage. Altogether, we establish a roadmap for chloroplast differentiation, a critical process for plant photoautotrophic growth and survival.

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La Faculté des sciences de l'Université de Neuchâtel autorise l'impression de la présente thèse soutenue par Monsieur Thibaut PRALON Titre: "Two atypical kinases of plastoglobules, ABC1K1/PGR6 and ABC1K3, maintain photosynthetic efficiency in Arabidopsis by acting on plastoquinone homeostasis" sur le rapport des membres du jury composé comme suit:

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.