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Role of Plastoglobule Proteins in Photosynthesis and Plastoquinone Pool Regulation

English title Role of Plastoglobule Proteins in Photosynthesis and Plastoquinone Pool Regulation
Applicant Kessler Felix
Number 176191
Funding scheme Project funding
Research institution Laboratoire de Physiologie Végétale Institut de biologie Université de Neuchâtel
Institution of higher education University of Neuchatel - NE
Main discipline Cellular Biology, Cytology
Start/End 01.03.2018 - 31.03.2022
Approved amount 659'469.00
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All Disciplines (2)

Discipline
Cellular Biology, Cytology
Biochemistry

Keywords (12)

Lipid droplets; Fibrillin; Photosynthesis; Plastoglobules; Chloroplast; Phosphoprotein network; Lipid metabolism; Phosphoproteomics; Phosphorylation; Photosynthetic electron transport; Plastoquinone; Kinase

Lay Summary (French)

Lead
Titre du projet de rechercheRole of Plastoglobule Proteins in Photosynthesis and Plastoquinone Pool RegulationRôle des protéines des plastoglobules dans la photosynthèse et la régulation de la répartition des plastoquinonesRolle der Plastoglobuliproteine in der Photosynthese und Regulation der Plastoquinonverfügbarkeit.La photosynthèse utilise l’énergie lumineuse du soleil et fournit toute la biomasse sur Terre. Pour cela, une molécule, la plastoquinone, est essentielle. Elle transporte des électrons dans la chaîne photosynthétique et sa disponibilité doit être finement régulée. Nous examinons le rôle des kinases ABC1K1 et -K3 dans sa régulation.
Lay summary

Contenu et objectifs du travail de recherche

Les kinases sont des protéines régulatrices importantes dans le royaume du vivant. Chez les plantes, des kinases de la famille ABC1 (ABC1K1 et ABC1K3) ont un rôle critique dans la régulation de la photosynthèse. Sans ABC1K1, elle est limitée en condition de forte lumière causant un blanchissement des plantes. Nos récents travaux ont démontré qu’ABC1K1 est nécessaire pour l’exploitation optimale de la lumière et la dissipation de l’énergie excessive. Les plastoquinones jouent un rôle central dans ces processus. Ces molécules sont contenues dans des réservoirs (les plastoglobules) qui approvisionnent la chaîne photosynthétique. Il semble qu’ABC1K1 régule la mise à disposition des plastoquinones pour la photosynthèse. Un premier objectif de ce projet est de mieux comprendre les mécanismes de ce phénomène fascinant.

De plus, les plastoglobules servent également de lieu de stockage des pigments rouges (des caroténoides, précieux antioxidants de notre alimentation) notamment dans le fruit de tomate. Un deuxième objectif de ce projet est d’étudier le rôle des kinases ABC1 dans la production des caroténoides et dans leurs stockages.

Contexte scientifique et social du projet de recherche

Ce projet de recherche fondamentale vise à mieux comprendre les mécanismes de régulation de la photosynthèse. L’optimisation de ces processus est stratégique pour la sélection de plantes cultivées de plus haut rendement. Dans le cadre de ce projet, nous exploitons cette stratégie dans la tomate (Solanum lycopersicon).

Direct link to Lay Summary Last update: 26.01.2018

Responsible applicant and co-applicants

Employees

Project partner

Publications

Publication
Plastoglobules: A hub of lipid metabolism in the chloroplast
Shanmugabalaji Venkatasalam, Zita Wayne, Collombat Joy, Kessler Felix (2022), Plastoglobules: A hub of lipid metabolism in the chloroplast, in Eric Maréchal, Rébeillé Fabrice (ed.), Elsevier, London, U.K, 91-119.
A multifaceted analysis reveals two distinct phases of chloroplast biogenesis during de-etiolation in Arabidopsis
Pipitone Rosa, Eicke Simona, Pfister Barbara, Glauser Gaetan, Falconet Denis, Uwizeye Clarisse, Pralon Thibaut, Zeeman Samuel C, Kessler Felix, Demarsy Emilie (2021), A multifaceted analysis reveals two distinct phases of chloroplast biogenesis during de-etiolation in Arabidopsis, in eLife, 10(e62709), 1-32.
SUMOylation contributes to proteostasis of the chloroplast protein import receptor TOC159 during early development
Accossato Sonia, Kessler Felix, Shanmugabalaji Venkatasalam (2020), SUMOylation contributes to proteostasis of the chloroplast protein import receptor TOC159 during early development, in eLife, 9(e60968), 1-16.
Mutation of the Atypical Kinase ABC1K3 Partially Rescues the PROTON GRADIENT REGULATION 6 Phenotype in Arabidopsis thaliana
Pralon Thibaut, Collombat Joy, Pipitone Rosa, Ksas Brigitte, Shanmugabalaji Venkatasalam, Havaux Michel, Finazzi Giovanni, Longoni Paolo, Kessler Felix (2020), Mutation of the Atypical Kinase ABC1K3 Partially Rescues the PROTON GRADIENT REGULATION 6 Phenotype in Arabidopsis thaliana, in Frontiers in Plant Science, 11(337), 1-18.
Characterization of a Plastoglobule-Localized SOUL4 Heme-Binding Protein in Arabidopsis thaliana
Shanmugabalaji Venkatasalam, Grimm Bernhard, Kessler Felix (2020), Characterization of a Plastoglobule-Localized SOUL4 Heme-Binding Protein in Arabidopsis thaliana, in Frontiers in Plant Science, 11(2), 1-9.
Plastoquinone homoeostasis by Arabidopsis proton gradient regulation 6 is essential for photosynthetic efficiency
Pralon Thibaut, Shanmugabalaji Venkatasalam, Longoni Paolo, Glauser Gaetan, Ksas Brigitte, Collombat Joy, Desmeules Saskia, Havaux Michel, Finazzi Giovanni, Kessler Felix (2019), Plastoquinone homoeostasis by Arabidopsis proton gradient regulation 6 is essential for photosynthetic efficiency, in Communications Biology, 2(1), 220-220.
How chloroplasts protect themselves from unfolded proteins
Kessler Felix, Longoni Paolo (2019), How chloroplasts protect themselves from unfolded proteins, in eLife, 8(e51430), 1-3.
CHLORAD: Eradicating Translocon Components from the Outer Membrane of the Chloroplast
Shanmugabalaji Venkatasalam, Kessler Felix (2019), CHLORAD: Eradicating Translocon Components from the Outer Membrane of the Chloroplast, in Molecular Plant, 12(4), 467-469.
Affinity Purification of Chloroplast Translocon Protein Complexes Using the TAP Tag
Shanmugabalaji Venkatasalam, Douet Véronique, Agne Birgit, Kessler Felix (2018), Affinity Purification of Chloroplast Translocon Protein Complexes Using the TAP Tag, in Journal of Visualized Experiments, 141(e58532), 1-6.
Plastidial NAD-Dependent Malate Dehydrogenase: A Moonlighting Protein Involved in Early Chloroplast Development through Its Interaction with an FtsH12-FtsHi Protease Complex
Schreier Tina B., Cléry Antoine, Schläfli Michael, Galbier Florian, Stadler Martha, Demarsy Emilie, Albertini Daniele, Maier Benjamin A., Kessler Felix, Hörtensteiner Stefan, Zeeman Samuel C., Kötting Oliver (2018), Plastidial NAD-Dependent Malate Dehydrogenase: A Moonlighting Protein Involved in Early Chloroplast Development through Its Interaction with an FtsH12-FtsHi Protease Complex, in The Plant Cell, 30(8), 1745-1769.
The plant pathogen Pseudomonas aeruginosa triggers a DELLA-dependent seed germination arrest in Arabidopsis
Chahtane Hicham, Nogueira Füller Thanise, Allard Pierre-Marie, Marcourt Laurence, Ferreira Queiroz Emerson, Shanmugabalaji Venkatasalam, Falquet Jacques, Wolfender Jean-Luc, Lopez-Molina Luis (2018), The plant pathogen Pseudomonas aeruginosa triggers a DELLA-dependent seed germination arrest in Arabidopsis, in eLife, 7(e37082), 1-34.
Chloroplast Biogenesis Controlled by DELLA-TOC159 Interaction in Early Plant Development
Shanmugabalaji Venkatasalam, Chahtane Hicham, Accossato Sonia, Rahire Michèle, Gouzerh Guillaume, Lopez-Molina Luis, Kessler Felix (2018), Chloroplast Biogenesis Controlled by DELLA-TOC159 Interaction in Early Plant Development, in Current Biology, 28(16), 2616-2623.e5.

Collaboration

Group / person Country
Types of collaboration
SAVE, BIAM, CEA France (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
Luis Lopez Molina lab, University of Geneva Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Plant biochemistry, ETH Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
Light-Photosynthesis & Metabolism (LP&M), CEA-Grenoble France (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure

Scientific events

Active participation

Title Type of contribution Title of article or contribution Date Place Persons involved
Symposium of the plant science research community in Switzerland Talk given at a conference Proton Gradient Regulation 6 (PGR6)/ABC1K1 maintains plastoquinone levels in the photosynthetic electron transport chain 29.01.2020 Ovronnaz, Switzerland Kessler Felix;
Three seminar series, Higher-Level Foreign Expert Invitation Program of Ministry of Science and Technology of China Individual talk Plastoglobules and the regulation of photosynthetic electron transport 25.11.2019 Wuhan, China Kessler Felix;
Three seminar series, Higher-Level Foreign Expert Invitation Program of Ministry of Science and Technology of China Individual talk Diversity of metabolic functions in plastoglobules 24.11.2019 Wuhan, China Kessler Felix;
Three seminar series, Higher-Level Foreign Expert Invitation Program of Ministry of Science and Technology of China Individual talk Origin, physiology, and ultrastructure of the chloroplast lipid droplets 23.11.2019 Wuhan, China Kessler Felix;
SwissPlant Symposium 2019 Talk given at a conference Role for DELLA in early chloroplast biogenesis 30.01.2019 Meiringen, Switzerland Kessler Felix;
Cytoplasmic events in early chloroplast biogenesis Individual talk Cytoplasmic events in early chloroplast biogenesis 22.11.2018 Oxford, Stateless Kessler Felix;
GRC-Mitochondria and Chloroplasts Poster The plant hormone gibberellin controls early chloroplast biogenesis via DELLA mediated degradation of TOC159 by the ubiquitin-proteasome system 08.07.2018 Lucca (Barga), Italy Venkatasalam Shanmugabalaji;
Plastoglobuli: Plastid microcompartments with integrated functions in plastoquinone metabolism and photosynthesis Individual talk Plastoglobuli: Plastid microcompartments with integrated functions in plastoquinone metabolism and photosynthesis 28.06.2018 Munich, Germany Kessler Felix;


Communication with the public

Communication Title Media Place Year
Media relations: radio, television La photosynthèse mieux comprise grâce à l’Université de Neuchâtel arcinfo Western Switzerland 2021
Media relations: radio, television Le mécanisme de la photosynthèse découvert par des chercheurs de l’UniNE RTJ Western Switzerland 2021
Media relations: radio, television Le verdissement des plantes n'a plus de secrets Canalalpha Western Switzerland 2021
Media relations: print media, online media When the seed becomes a plant, it has 48 hours to survive sciencedaily International 2018

Associated projects

Number Title Start Funding scheme
160786 Sugar wars: Glucose-mediated activation, neutralization and re-activation of defensive metabolites in a soil tritrophic system 01.10.2015 Sinergia
183365 Ultra High Performance Liquid Chromatography-High Resolution Tandem Mass Spectrometry (UHPLC-HRMS/MS) for metabolomics and identification of bioactive molecules 01.10.2019 R'EQUIP
156998 Exploring the chloroplast ABC1-like kinase phosphoprotein network: roles in remodeling thylakoid lipid composition, photosynthesis and beyond. 01.01.2015 Project funding
156998 Exploring the chloroplast ABC1-like kinase phosphoprotein network: roles in remodeling thylakoid lipid composition, photosynthesis and beyond. 01.01.2015 Project funding
144156 Role of phosphorylation at Toc159 in chloroplast protein import and identification of a new outer chloroplast membrane kinase 01.10.2012 Project funding
208000 Role of plastoglobule atypical ABC1-like kinases in lipid homeostasis and retrograde signaling 01.04.2022 Project funding

Abstract

Members of the atypical ABC1-like kinase family constitute the largest group of kinases in the chloroplast. The family members ABC1K1 and -K3 play essential roles in proton gradient regulation (PGR) in photosynthesis and tocopherol biosynthesis presumably by phosphorylating tocopherol cyclase (VTE1). Moreover, ABC1K1 and -K3 physically interact but have genetically opposed functions. However, their functional mechanisms in photosynthesis are largely mysterious. Surprisingly, they near-exclusively associate with plastoglobules (PGs), a lipid subcompartment that is physically attached to the photosynthetic thylakoids by a neck-like membrane structure. Key metabolites, such as the electron carrier plastoquinone and the antioxidant tocopherol, partition between PG and thylakoids and ample evidence suggests their trafficking between the two compartments. Yet, it is not known how trafficking works. In addition to the ABC1-like kinases, PGs are decorated with metabolic enzymes (e.g. VTE1) and members of the fibrillin (FBN) family. In an apple fbn4 mutant, PGs are devoid of plastoquinone while total plastoquinone concentration is not affected. It has been suggested that FBNs play a role in trafficking and distribution between the two compartments. Several lines of evidence suggest that also in the abc1k1 mutant plastoquinone distribution and/or availability in the thylakoids may be perturbed while total plastoquinone concentration again is unchanged. In fact, abc1k1 exhibits faster saturation of photosynthetic electron transport (PET), reduced non-photochemical quenching and stronger photoinhibition under high light. These observations are consistent with plastoquinone limitation in the PET chain. However, other explanations cannot be excluded. We entertain several, mutually non-exclusive scenarios implicating the ABC1K1/-K3 kinase pair as well as FBNs that may explain these observations.1. ABC1K1/-K3, possibly together with FBNs, act indirectly on photosynthesis by regulating plastoquinone distribution or allocation to the PET chain. 2. ABC1K1/-K3 act directly by phosphorylating targets in the photosynthetic machinery or elsewhere e.g. VTE1 in PG.3. ABC1K1 and -K3 act directly by binding to components of the photosynthetic machinery or interaction partners elsewhere e.g. to each other in PG.
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