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Two Atypical Kinases of Plastoglobules, ABC1K1/PGR6 and ABC1K3, Maintain Photosynthetic Efficiency in Arabidopsis by Acting on Plastoquinone Homeostasis

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Two Atypical Kinases of Plastoglobules, ABC1K1/PGR6 and ABC1K3, Maintain Photosynthetic Efficiency in Arabidopsis by Acting on Plastoquinone Homeostasis 10.35662/unine-thesis-2804 Faculty of Science, Institute of Biology Plant Physiology Laboratory Two atypical kinases of plastoglobules, ABC1K1/PGR6 and ABC1K3, maintain photosynthetic efficiency in Arabidopsis by acting on plastoquinone homeostasis. A dissertation submitted to the University of Neuchâtel For the degree of Doctor of Philosophy in Biological Sciences Presented by Thibaut Pralon Thesis committee Prof. Felix Kessler (Thesis Director) – University of Neuchâtel Dr. Laurent Mène-Saffrané – University of Fribourg Dr. Gaetan Glauser – University of Neuchâtel Dr. Paolo Longoni – University of Neuchâtel Supervisors Dr. Shanmungabalaji Ventakasalam – University of Neuchâtel January 2020 Faculté des Sciences Secrétariat-décanat de Faculté Rue Emile-Argand 11 2000 Neuchâtel – Suisse Tél : + 41 (0)32 718 21 00 E-mail : [email protected] IMPRIMATUR POUR THESE DE DOCTORAT 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: • Prof. Felix Kessler, directeur de thèse, Université de Neuchâtel, Suisse • Dr Paolo Longoni, Université de Neuchâtel, Suisse • Dr Gaëtan Glauser, Université de Neuchâtel, Suisse • Dr Laurent Mène-Saffrané, Université de Fribourg Neuchâtel, le 5 novembre 2019 Le Doyen, Prof. P. Felber Imprimatur pour thèse de doctorat www.unine.ch/sciences Abstract Life on Earth is mainly dependant on a single series of photochemical reactions: collectively known as photosynthesis. Indeed, these reactions provide chemical energy in the form of sugars for human nutrition and molecular oxygen that is necessary for human respiration. Photosynthesis is performed in photosynthetic organisms such as plants and algae inside green cellular organelles called chloroplasts. The light-dependent reactions of photosynthesis require a machinery consisting of multiple protein-pigment complexes embedded in the thylakoid membrane. While photosynthesis is a very robust process, its machinery is still fragile and may be damaged under environmental variations such as sudden changes in light intensity (e.g. during a sunny day with cloudy spells). Therefore, fine regulation and great photoprotection are necessary to maintain efficient photosynthesis. Small lipid droplets attached to thylakoid membrane, called plastoglobules (PG), contribute to photoprotection as they are filled with neutral lipid such as plastoquinone, phylloquinone (vitamin K1), tocopherols (vitamin E) and carotenoids that are either essential molecules for photosynthetic electron transport and/or powerful membrane anti-oxidants. Proteins at the surface of PG, including atypical ABC1K kinases, contribute to the neutral lipid metabolic pathways. This suggests that PG play an important role in the photosynthesis regulation and protection. My PhD thesis focuses on two of the atypical kinases, ABC1K1/PGR6 and ABC1K3, and their roles in photosynthesis regulation. We have discovered a previously uncharacterized mechanism of photosynthesis regulation implicating the two atypical kinases ABC1K1/PGR6 and ABC1K3 in the regulation of the photoactive plastoquinone pool size. In a nutshell, the role of ABC1K1/PGR6 is to maintain a sufficient photoactive plastoquinone pool under high light conditions whereas ABC1K3 functions as a limiter to plastoquinone availability. Thus, this PhD thesis provides new insight on the function of two atypical kinases in plastoglobules, ABC1K1/PGR6 and ABC1K3, in rapid adaptation of photosynthesis under high light. The chapter 2, entitled “Plastoglobules: Lipid droplets at the thylakoid membrane” was published in the book “Chloroplasts: Current Research and Future Trends” (Kirchhoff H. Eds.) in 2016. The third chapter “Plastoquinone homoeostasis by Arabidopsis proton gradient regulation 6 is essential for photosynthetic efficiency” was published in the scientific journal “Communication Biology” in 2019. Abstract 5 Résumé La vie sur Terre dépend principalement d’une suite de réactions photochimiques, appelée la photosynthèse. Ces réactions fournissent de l’énergie chimique sous forme de sucre pour notre alimentation et d’oxygène nécessaire à notre respiration. La photosynthèse s’effectue dans les organismes photosynthétiques tels que les plantes et les algues dans de petits organites nommés chloroplastes. Les réactions de la photosynthèse dépendantes de l’énergie lumineuse requièrent une machinerie composée de multiples complexes de pigments-protéines intégrés dans la membrane du thylakoïde. Alors que la photosynthèse est un mécanisme très robuste, sa machinerie reste fragile et peut être endommagée lors de conditions environnementales changeantes telle qu’une variation brusque d’intensité lumineuse (par ex. lors de passages nuageux par temps ensoleillé). Par conséquent, une régulation adaptée et une protection efficace sont nécessaires pour maintenir une photosynthèse optimale. Attachées aux thylakoïdes de petites gouttes lipidiques, nommées plastoglobules (PG), contribuent à la photoprotection par le fait qu’elles sont remplies de lipides neutres tels que la plastoquinone, la phylloquinone (vitamine K1), les tocophérols (vitamine E) et les caroténoïdes, des molécules essentielles pour le transport des électrons et/ou agissantes comme de puissants antioxydants. Les protéines des PG, incluant des kinases atypiques ABC1K, participent aux voies métaboliques des lipides neutres. Cela suggère un rôle important des PG dans la régulation et la protection de la photosynthèse. Ma thèse de doctorat porte sur deux kinases atypiques, ABC1K1/PGR6 et ABC1K3, et leurs implications dans la régulation de la photosynthèse. Nous avons découvert un mécanisme de contrôle de la photosynthèse jusque-là non identifié, impliquant les deux kinases atypiques ABC1K1/PGR6 et ABC1K3 dans la régulation de la plastoquinone photoactive. En quelques mots, le rôle de ABC1K1/PGR6, sous une intensité lumineuse élevée, est de maintenir un pool de plastoquinone photoactive suffisant, alors que ABC1K3 fonctionnerai comme un limiteur de la mobilité de la plastoquinone. Cette thèse de doctorat offre donc un nouveau regard sur la fonction de deux kinases atypiques des plastoglobules, ABC1K1/PGR6 et ABC1K3, dans l’adaptation rapide de la photosynthèse en condition de haute intensité lumineuse. Le chapitre 2, intitulé “Plastoglobules: Lipid droplets at the thylakoid membrane” a été publié dans le livre “Chloroplasts: Current Research and Future Trends” (Kirchhoff H. Eds.) en 2016. Le troisième chapitre “Plastoquinone homoeostasis by Arabidopsis proton gradient regulation 6 is essential for photosynthetic efficiency” a été publié dans la revue scientifique "Communication Biology" en 2019. Résumé 7 Keywords: Chloroplasts, plastoglobules, photosynthesis, plastoquinone, PQ, plastoquinol, PQH2, Activity of BC1 complex, Proton Gradient Regulation, ABC1K1, ABC1K3, PGR6, kinases, photoactive, phosphorylation, redox state, cytochrome b6f, electron transport, non-photochemical quenching, NPQ, light-harvesting complexes, LHC, state transitions. Mots clés: Chloroplastes, plastoglobules, photosynthèse, plastoquinone, PQ, plastoquinol, PQH2, Activity of BC1 complex, Proton Gradient Regulation, ABC1K1, ABC1K3, PGR6, kinases, photoactive, phosphorylation, état redox, cytochrome b6f, transport d’électrons, quenching non-photochimique, NPQ, antennes collectrices de lumière, LHC, transition d’état. Keywords – Mots clés 9 Contents Abbreviations ........................................................................................................................................ 15 Chapter I General introduction ............................................................................................................ 17 Abstract ............................................................................................................................................. 17 1.1 Chloroplast, a plastid designed for photosynthesis .................................................................... 17 1.2 Photosynthetic electron transport .............................................................................................. 22 1.3 Photoprotection .......................................................................................................................... 25 1.3.1 State transitions ................................................................................................................... 25 1.3.2 Non-photochemical quenching (NPQ) ................................................................................. 27 1.3.3 PSII repair cycle .................................................................................................................... 29 1.3.4 Antioxidants.......................................................................................................................... 30 References ......................................................................................................................................... 33 Chapter II Plastoglobules: lipid droplets at the thylakoid membrane ................................................. 47 Abstract ............................................................................................................................................. 47 2.1 Discovery of PG ..........................................................................................................................
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