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Study of the physiological and molecular functions of ABC1K1 protein during early development of "Arabidopsis thaliana"

2022, Collombat, Joy, Kessler, Félix, Longoni, Fiamma

Photosynthesis is a key bioenergetic mechanism allowing photosynthetic organisms such as plants or algae to convert sunlight energy into chemical energy to produce sugar, while releasing molecular oxygen. This process takes place in a specific cellular organelle called chloroplast. Inside the chloroplast, the components of the photosynthetic machinery required to perform the photochemical part of photosynthesis, are inserted in a highly dynamic structure, the thylakoid membrane. Plastoglobules, small lipoprotein particles (lipid droplets) associated with the thylakoid membrane, are essential for chloroplast lipid metabolism, thylakoid formation and photoprotection. These structures contain a large diversity of neutral lipids some of which have strong antioxidant properties, such as tocopherols, carotenoids or plastoquinone. Most of the plastoglobule proteins are involved in lipids metabolisms. Among them, the ABC1K proteins are involved in the regulation of neutral lipid metabolism and contribute to the maintenance of photosynthetic activity by plastoquinone homestasis. My PhD consists in the study of the physiological and molecular functions of ABC1K1 protein in the early development of Arabidopsis thaliana. In particular, we studied its role in early chloroplast biogenesis under stress-enhancing red and high light conditions. We have discovered a new signaling mechanism in which ABC1K1 promotes the degradation of EX1, a singlet oxygen trigger (1O2), though the FTSH2 protease, particularly active under red light conditions. The accumulation of EX1 in abc1k1 and ftsh2 mutant led to the arrest of chloroplast biogenesis and a greening defect. Mutation of EX1 by CRISPR/Cas9 in the abc1k1 background partially alleviated the greening defect observed in the abc1k1 mutant (Chapter 2.1). During my PhD, we also observed that abc1k1 displayed a variegated phenotype under high light conditions, similarly to the ftsh2 mutant. This result was integrated in the publication called “Plastoquinone homoeostasis by Arabidopsis proton gradient regulation 6 is essential for photosynthetic efficiency” published in the scientific journal “Communication Biology” in 2019 (Chapter 2.2). Finally, we have shown that the dark re-oxidation of the photoactive plastoquinone pool is impaired in the abc1k1 mutant suggesting a defect in the plastoquinone mobility. This defect is restored in the abc1k1/abc1k3 double mutant. This result was integrated in the publication “Mutation of the Atypical Kinase ABC1K3 Partially Rescues the PROTON GRADIENT REGULATION 6 Phenotype in Arabidopsis thaliana” published in the scientific journal “Frontiers in Plant Science” in 2020 (Chapter 2.3). This thesis provides new insight into the role of ABC1K1 and ABC1K3 proteins in theregulation of early chloroplast biogenesis and photosynthesis under stressful light conditions.

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Publication
Accès libre

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

2019-6-20, Pralon, Thibaut, Venkatasalam, Shanmugabalaji, Longoni, Fiamma, Ksas, Brigitte, Collombat, Joy, Desmeules, Saskia, Glauser, Gaëtan, Havaux, Michel, Finazzi, Giovanni, Kessler, Félix

Photosynthesis produces organic carbon via a light-driven electron flow from H2O to CO2 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.